cells is highly unlikely because it would then be a kind of parasitic cell, gaining water and...

1 23

The Botanical Review ISSN 0006-8101 Bot. Rev.DOI 10.1007/s12229-018-9198-5

Living Cells in Wood 3. Overview;Functional Anatomy of the ParenchymaNetwork

Sherwin Carlquist

1 23

Your article is protected by copyright and

all rights are held exclusively by The New

York Botanical Garden. This e-offprint is

for personal use only and shall not be self-

archived in electronic repositories. If you wish

to self-archive your article, please use the

accepted manuscript version for posting on

your own website. You may further deposit

the accepted manuscript version in any

repository, provided it is only made publicly

available 12 months after official publication

or later and provided acknowledgement is

given to the original source of publication

and a link is inserted to the published article

on Springer's website. The link must be

accompanied by the following text: "The final

publication is available at link.springer.com”.

Living Cells in Wood 3. Overview; Functional Anatomyof the Parenchyma Network

Sherwin Carlquist1,2

1 Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, CA 93105, USA2Author for Correspondence; e-mail: [email protected]

# The New York Botanical Garden 2018

Abstract The very different evolutionary pathways of conifers and angiosperms arevery informative precisely because their wood anatomy is so different. New informa-tion from anatomy, comparative wood physiology, and comparative ultrastructure canbe combined to provide evidence for the role of axial and ray parenchyma in the twogroups. Gnetales, which are essentially conifers with vessels, have evolved parallel toangiosperms and show us the value of multiseriate rays and axial parenchyma in avessel-bearing wood. Gnetales also force us to re-examine optimum anatomical solu-tions to conduction in vesselless gymnosperms. Axial parenchyma in vessel-bearingwoods has diversified to take prominent roles in storage of water and carbohydrates aswell as maintenance of conduction in vessels. Axial parenchyma, along with othermodifications, has superseded scalariform perforation plates as a safety mechanism andpermitted angiosperms to succeed in more seasonal habitats. This diversification hasrequired connection to rays, which have concomitantly become larger and morediverse, acting as pathways for photosynthate passage and storage. Modes of growthsuch as rapid flushing, vernal leafing-out, drought deciduousness and support of largeleaf surfaces become possible, advantaging angiosperms over conifers in various ways.Prominent tracheid-ray pitting (conifers) and axial parenchyma/ray pitting to vessels(angiosperms) are evidence of release of photosynthates into conductive cells; inangiosperms, this system has permitted vessels to survive hydrologic stresses andfunction in more seasonal habitats. Flow in ray and axial parenchyma cells, suggestedby greater length/width ratios of component cells, is confirmed by pitting on end wallsof elongate cells: pits are greater in area, more densely placed, and are often bordered.Bordered pit areas and densities on living cells, like those on tracheids and vessels,represent maximal contact areas between cells while minimizing loss of wall strength.Storage cells in rays can be distinguished from flow cells by size and shape, by fewerand smaller pits and by contents. By lacking secondary walls, the entire surfaces ofphloem ray and axial phloem parenchyma become conducting areas across whichsugars can be translocated. The intercontinuous network of axial parenchyma and rayparenchyma in woods is confirmed; there are no “isolated” living cells in wood whenthree-dimensional studies are made. Water storage in living cells is reported anatomi-cally and also in the form of percentile quantitative data which reveal degrees and kindsof succulence in angiosperm woods, and norms for “typically woody” species. Thediversity in angiosperm axial and ray parenchyma is presented as a series of probable

Bot. Rev.https://doi.org/10.1007/s12229-018-9198-5

Author's personal copy

http://crossmark.crossref.org/dialog/?doi=10.1007/s12229-018-9198-5&domain=pdf

optimal solutions to diverse types of ecology, growth form, and physiology. Thenumerous homoplasies in these anatomical modes are seen as the informative resultsof natural experiments and should be considered as evidence along with experimentalevidence. Elliptical shape of rays seems governed by mechanical considerations;unusually long (vertically) rays represent a tradeoff in favor of flexibility versusstrength. Protracted juvenilism (paedomorphosis) features redirection of flow fromhorizontal to vertical by means of rays composed predominantly or wholly of uprightcells, and the reasons for this anatomical strategy are sought. Protracted juvenilism, stilllittle appreciated, occurs in a sizeable proportion of the world’s plants and is a majorsource of angiosperm diversification.

Keywords Flow in rays . Gnetales . Growth flushes . Juvenilism . Succulence .

Xeromorphy

Introduction

As the physiology of water conduction in vessels and tracheids has become betterunderstood, attention has turned to the roles that ray and axial parenchyma in func-tioning of secondary xylem of conifers and angiosperms. This wave of interest, mostrecently represented by the thoroughly-referenced papers by Morris et al. (2015, 2017)and Morris and Jansen (2016), seeks to clarify what living cells, including living fibers,do with regard to wood function. The approaches to study of parenchyma functionmust of necessity be different from those applied to sap-conducting cells of the wood.Axial parenchyma, and, indirectly, ray parenchyma are concerned in suppression andreversal of embolisms (Braun, 1984; Holbrook and Zwieniecki 1999; Holbrook et al.2002; Johnson et al., 2012; Lens et al., 2013; Nardini et al., 2011; Salleo et al., 2004,Salleo et al., 2009; Secchi et al., 2016; Trifilo et al., 2014). These authors do notexamine the role of ray parenchyma, but there is no other source for the sugars and ionsthan via the rays. In examining the function of axial and ray parenchyma, assembling ofquantitative data has, to a large extent, been the method of choice (Morris et al. 2015,Morris et al., 2017 and literature cited therein).

The present paper attempts to use new data in comparative anatomy obtained withlight microscopy, ultrastructure as seen with scanning electron microscopy (SEM), andobservations on growth form and habit primarily. References to experimental work inphysiology are considered a vital parallel source of information, and are cited here, asthey were in Carlquist (2012a). The value of comparative anatomical data is consider-able in interpreting the functioning of wood, because wood anatomical diversityultimately must be explained in terms of selection for structural features. The manyparallel acquisitions of wood character states in clade after clade represent the results ofnatural experiments performed on immense numbers of individuals in thousands ofspecies over many million years. There has been some appreciation of the value ofanatomical data (e.g., Morris & Jansen, 2016). Such works, rich in illustration, as Molland Janssonius (1909-1936) and Metcalfe and Chalk (1950) are cited by Morris andJansen (2016). To those we must add such works as Greguss (1955, 1959), Meylan andButterfield (1978), and many other important sources. Many of these are expensive andfound in a relatively small number of libraries, and are not available on the internet,

S. Carlquist


which increasingly has become the source of references and the basis for documenta-tion in research. Simultaneously, there has been a disappearance from many collegesand universities of courses in plant anatomy, so that those able to do interpretive workin wood anatomy are fewer. Those with encyclopedic knowledge of comparative woodanatomy of large numbers of species, such as I. W. Bailey, C. R. Metcalfe, and S. J.Record, are almost non-existent today, although some a few specialists conversant withcomparative wood anatomy of some families and clades do, fortunately, exist. Exper-imental studies of wood function are, by contrast, relatively recent and easy to access.The complexity and diversity of wood anatomy and the difficulty of access to the fieldhave worked to the disadvantage of visual understanding of the function-structurecontinuum. The present paper is an attempt to work with microscopy and some allieddata by way of supplying the visual component. This is done by presenting illustrationsfor a number of modes of structure in wood anatomy and attempting to show how theymay be related to functional aspects.

Cross-comparisons of wood of unrelated or distantly-related groups can be highlyinformative. Metcalfe (1983, p. 4) says, “The development of the vessel has had aprofound effect on the xylem of angiosperms….it has made specialization possible inother directions: specialization of fibers [i.e, change from tracheids to libriformfibers]….and this in turn has been linked with changes in the distribution of parenchy-ma cells.” Now that we know that Gnetales are conifer derivatives (Bowe et al., 2000;Burleigh & Mathews, 2004), and that Gnetales have attained, parallel to angiosperms,essentially all of the important anatomical features of angiosperm wood (Carlquist,2012b), we have a source for demonstrating quite dramatically pathways of woodevolution in vessel-bearing angiosperms and their significance. The wood of Gnetales,uniquely valuable precisely because of its independent acquisition of vessels, isvirtually unmentioned in consideration of angiosperm wood evolution. Likewise,physiological studies of wood function have not included Gnetales. Key anatomicalfeatures are presented here as a way of showing probable associations of angiosperm-like parenchyma and other living cells in Gnetales with vessels.

The method of anatomical cross-comparisons can be used quite productively as away of generating hypotheses about the significance of divergent modes of structurewithin conifers and within angiosperms. Molecular phylogenies can show us thatparallel evolution of axial parenchyma amounts and distributions, as well as kinds ofray histology, can be used to demonstrate not merely continuations of basic types, butsensitive adaptations to ecology and growth form. We tend to forget the ease withwhich genetic changes and ontogenetic variations can occur. For example, we tend toaccept that the almost exclusive presence of uniseriate rays in conifers has a selectivevalue. Conifers can produce multiseriate rays if the rays contain resin canals, andGnetales are all characterized by multiseriate rays. The development of vessels has ledto repurposing and diversification of parenchyma in angiosperms. We need to movebeyond descriptive knowledge of living cell types in wood, although ironically, morecomparative microscopical data, especially those obtained at higher magnifications,will help advance our understanding of cell function in wood.

The three-dimensional nature of the network of living cells in wood has beenestablished and studied, most notably by Zimmermann (1971) and Kedrov (2012).Understanding that in plants as diverse as Fitzroya (Cupressaceae) and Alnus(Betulaceae), as shown by Kedrov (2012), the network system prevails and no isolated

Living Cells in Wood 3. Overview; Functional Anatomy of the...


living cells exist is important to our interpretation of wood structure. In analyzing axialparenchyma, we are told that diffuse parenchyma is present as “isolated” cells, but infact, all of these are part of an intercontinuous network. Transverse sections, often theprimary basis for determining the nature of axial parenchyma, are misleading in thisrespect. In fact, the idea of an axial parenchyma cell not in contact with other livingcells is highly unlikely because it would then be a kind of parasitic cell, gaining waterand nutrition from water-conducting cells. Kedrov’s (2012) work goes far to promote athree-dimensional understanding of the living cell network as well as the way othercells in wood contact each other. Braun’s (1970) “Stufen” (stages) in parenchymaevolution were proposed prior to our knowledge of molecular phylogeny, and thus canat best be interpreted as physiological conditions divorced from phylogeny.

Cell contents have been relatively neglected. The reasons for this lie largely in the use ofxylarium specimens. For example, starch in parenchyma cells agglutinates into amorphousmasses or, more commonly, is lost entirely by the rapid action of bacteria during the dryingof wood samples. The use of liquid-preserved wood samples as a basis for studies shouldhave become a standardmethodology by now, but it is not. To be sure, liquid preservation ofwood samples is logistically less easy than drying them, but has been routinely accom-plished by a few individuals. The presence of starch and other photosynthates in living cellsof woods is obviously important, as the work of Sauter (1966a, b) on starch storage andconversion into sugars in ray tissue of Acer tells us about the seasonal course of storage.Perhaps the most important (but least cited) paper with relation to the role of parenchyma inwoods by releasing sugar into vessels (and thereby maintaining conduction through embo-lism prevention or even reversal) is that of Sauter et al. (1973). The accumulation,mobilization, and differential storage of photosynthates in particular parenchyma cellsthroughout seasons, especially those that feature marked temperature fluctuations, is notthe same in all species, and is not difficult to study.

Parenchyma cell size and shape are prime indicators of function, along with otherindicators. The present paper takes, for the purposes of an initial assessment, theconcept that cells are elongate in the direction of conduction and flow. Elongate cellswith minimal contents are considered to be indicative of flow, and the non-committal“flow cell” is applied to them unless there are contrary indicators. For example,fibriform cells are not considered to be flow cells. A substantial end wall contact withanother cell is essential. The existence of elongate—and non-elongate cells in rays haslong been known. By applying the terms “upright,” “procumbent,” and “square,” to raycells as seen in radial section, most authors conclude their investigations. The func-tional distinctions of parenchyma cells of different shapes is only beginning to beappreciated at the present time. The same considerations apply to sizes and abundanceof parenchyma cells. The present essay makes use of information on size, shape,abundance, and degree of elongation as functional indicators. Anatomical literaturehas followed the dictum that “square cells [in rays, as seen in radial section] aremorphologically equivalent to upright cells.” This seems reductive and a way ofconcealing information for the sake of nomenclatural simplicity. Square cells areobviously not upright cells, and the quantity of them produced in any given place bythe plant can be significant. The point here is not to counter existing nomenclature butto re-explore ordinary light microscopy as a way of revealing functional significance.As Kedrov (2012) says, the entirety of a wood, not just individual parts of it, mustultimately be taken into account in explaining how it functions.

S. Carlquist


The relative proportions of upright and procumbent cell in woods are not conveyedby the terms “heterocellular,” “homocellular,” “heterogeneous” or “homogeneous.”While convenient to use for initial assessments or for diagnostic purposes such aswood identification, we must realize that we are dealing with physiological andecological wood anatomy. The fact that there are woods in which all ray cells areupright seems not to have been mentioned in wood literature prior to my paper onjuvenilism in woods (Carlquist, 1962), and I now propose that we confront thephysiological significance of prolonged juvenilism in woods.

Cell wall thickness and pitting have generally been considered subordinate to celltypes. Wood descriptions, if they mention these features at all, do not give dimensionsfor cell wall thickness, and pay little or no attention to pitting. The concept that all pitsin ray cells are simple pits has been propagated if only by lack of contrary information.In fact, bordered pits on the tangential walls of ray cells can be found in a largepercentage of angiosperm woods (Carlquist, 2007a). Such walls, easily visible insectional view in radial sections, are almost never figured or explained. Tangentialwalls of ray cells in conifers have been given a separate terminology: strips ofsecondary walls between pits are considered “nodular” or “nodulated.” The point thatlarge pits, either bordered or non-bordered, are present is thus lost in favor of a term thatmisses the fact that large pit membranes are present. The term “nodulated,” used bysuch authors as Panshin and De Zeeuw (1964), Hoadley (1990), and Roman-Jordanet al. (2016) should be abandoned in favor of descriptive language that shows that weare dealing with pitting, not some form of ornamentation superimposed on a cell wall.The same applies to the term “indentures” (Roman-Jordan et al., 2016). Tangentialwalls of ray cells and on the horizontal walls of strand cells in axial parenchyma canbear pits that differ with respect to size, density, border presence, and thickness of pitmembranes compared with pits on other walls of these cells. These are features thatgovern flow of liquids through these walls, and flow from one parenchyma cell to thenext is obviously the important concern here. Drawings of walls of parenchyma cells inwood often show perfunctory renderings in which pit borders are never indicated, anddifferences in pitting between end walls and lateral wall of elongate cells are notaccurately illustrated.

Such a basic structural component of woods as the shape and axial length of rays inwood seems not to have been subjected to interpretation. Why are rays elliptical inshape? Why do conifers lack multiseriate rays (with rare exceptions)? Axial parenchy-ma configurations are likewise dealt with almost exclusively at the descriptive level.The concept of “compartmentalization” by means of axial parenchyma bands (Shigo,1984) is an attempt at interpretation, although compartmentalization related to fungusspread in wood is sufficiently infrequent (Morris & Jansen, 2016) that one may doubtthat this is the sole reason for tangential banding of axial parenchyma. Shigo (1984)quite rightly feels that we should consider the role of wood structure in defense againstpredators. Rays and even axial parenchyma can exhibit cellular polymorphisms in cellshape, content, and abundance. We need to account for this diversification. Can weseparate axial parenchyma that is involved in osmotic maintenance of water columns inwoods from axial parenchyma that is involved in storage?What criteria can we use, andwhat methodologies are required?

Separating descriptive wood anatomy and wood physiology as two different fields isvery easy, but counterproductive in terms of the progress of biology. Progress in



biology and the other sciences has usually proceeded from fusion of fields andmethodologies, not from their separation. Wood structure represents selection foroptimal function, or at least selection for optimal compromises between conflictingstructural requirements (Carlquist, 2017). We should be aware that all wood featureshave adaptive aspects, even though the goal of a particular study may not be physio-logical or ecological in nature. Although stability in nomenclature is to be desired,nomenclature that is meaningful in conveying biological concepts is even moredesirable. This latter goal can be achieved with relatively little modification to existingnomenclature, and thereby relative stability can be achieved while synthesis of allfeatures of woods (including physiological ones) can be accomplished. Some nomen-clatural changes may be required, however.

Interpretive Data

Conifer Wood

Conifers (Fig. 1) have relatively small amounts of ray and axial parenchyma tissuecompared with Gnetales (Figs. 2 and 3) and angiosperms (Figs. 4, 5, 6, 7, 8, 9, 10, 11,12, 13, 14, 15, 16, and 17). Axial parenchyma is often sparse (Fig. 1a) and rays (Fig.1b–f) are sparse, uniseriate, and composed wholly of procumbent cells, suggesting thatthey are involved in radial flow of solutes. Present evidence indicates that tracheids,which average 3530 μm in length in conifers (Carlquist, 1975, Fig. 11), would be likelyto contact one or more rays. The length of axial parenchyma strands in angiospermswith simple transverse perforation plates (length of axial parenchyma strands approx-imately equal to that of vessel elements) is about 400 μm. If axial parenchyma strandsin those angiosperms are one-tenth the length of axial parenchyma strands in conifers,the number of axial parenchyma strands required to make contact to form a network inconifers is one order of magnitude smaller than that in angiosperms.

Do Any Conifers Lack Axial Parenchyma, and What Does This Indicate?

Axial parenchyma is absent in some species of Araucaria and Agathis (Greguss, 1955)andWollemia (Heady et al., 2002) of the Araucariaceae. In Pinaceae, axial parenchymais uncommon in Picea and Pinus (except around secretory canals) and in some speciesof Abies. It is present in Cephalotaxus and Torreya but absent in the other genus ofTaxaceae, Taxus. Axial parenchyma is present inGinkgo (Greguss, 1955) and in cycads(Greguss, 1968). In all genera not named above, axial parenchyma is figured indrawings by Greguss (1955). What accounts for this situation?

Axial wood parenchyma cells are not in contact with axial phloem parenchyma oncea layer of tracheids has formed to separate them from the cambium, whereas wood raysare intercontinuous with phloem rays via living cells of the cambium. Therefore, thetransfer of photosynthates into xylem rays is to be expected, and from rays, flow ofsolutes into axial parenchyma can occur (Höll, 1975). If there is less functional valuefor axial parenchyma than for rays in conifers, various degrees of diminution leading toabsence on axial parenchyma is to be expected. The genetic information to form axialparenchyma is present in such instances, but expressed only in limited situations. Thin-

S. Carlquist


walled parenchyma may be seen near axial secretory canals (Fig. 1e). In Pinus strobus(Fig. 1e), thin-walled ray cells are in contact with the thin-walled axial parenchyma

Fig. 1 Wood features of conifers. a Chamaecyparis lawsoniana (A. Murr.) Parl., Ripon W7w, transversesection. Axial parenchyma is sparse. b–d Sequoia sempervirens Endl., Ripon W57w. b Tangential section.Tangential section, axial parenchyma contains resins. c Transverse section with latewood below, earlywoodabove. d Pinus strobus L., Ripon W18w. Radial section near an axial resin canal, showing thin-walled rayparenchyma. f Pinus ponderosa Douglas ex Loudon, Ripon W48w, radial section. Ray tracheids occupynearly all of the ray shown; one file of ray parenchyma is included. Abbreviations: ap = axial parenchyma;rp = ray parenchyma file; rtp = ray-to-tracheid pitting (“cross-field pitting”); tw = thin-walled parenchyma



surrounding secretory canals. There may be a few axial parenchyma cells with lignifiedwalls (Fig. 1e).

Fig. 2 Wood features of Ephedra (Ephedraceae) and Gnetum (Gnetaceae). a–d Ephedra pedunculataEngelm. ex S. Watson, Carlquist 15,819 (RSA). a Transverse section; living fiber-tracheids (cells withcontents) adjacent to vessels. b Tangential section. Rays are multiseriate and uniseriate. c Radial section.All pits on ray cell walls are bordered. d Tangential section. Living fiber-tracheids contain nuclei andvestigially bordered pits. e-f Gnetum gnemon L., Carlquist 8088 (RSA). Tangential sections of root wood. eAxial parenchyma cells containing starch. f Portions of two rays; ray cells have prominent pits; starch isevident in some cells.

S. Carlquist


Fig. 3 Gnetum gnemon, Carlquist 8088 (RSA), Wood sections. a-b Sections of root wood. a Transversesection. Parenchyma cells are filled with starch and are about equal in number to the tracheids. b Tangentialsection. Wide and narrow rays about equally numerous. c-dWood from outer part of older stem. c Transversesection. Most axial parenchyma cells are located adjacent to vessels. d Tangential section. Wide and narrowrays are about equally numerous. e-fWood of young stem. e Transverse section. Axial parenchyma cells tendto form tangential bands between the vessels. f Tangential section; Wide multiseriate rays are very tall, andnarrow multiseriate rays and uniseriate rays are abundant



Fig. 4 Details of ray cell pitting in angiosperms (a, b, c, e) and Gnetales (d). a Zygogynum baillonii Tiegh.,Carlquist 15,609 (RSA). Radial section, showing thick tangential ray cell walls with pits mostly slightlybordered. b Laurelia sempervirens Tul., Carlquist 7223 (RSA). Radial section; pits few on horizontal andwalls, but abundant and bordered on tangential and radial vertical walls. c Forchhammeria pallida Liebm.,Olson 899 (UNAM). SEM of outer surface of tangential wall of a ray cell, showing numerous bordered pits. dGnetum gnemon, Carlquist 8088 (RSA). Tangential section; starch grains visible in some cells; in others, thetangential walls with numerous pits can be seen. e Chorisia speciosa, cultivated in Santa Barbara, CA.Tangential section: pitting denser in narrower ray cells, below; pits sparser and with smaller pits or pit fields inlarger cells which contain starch grains, above. Abbreviations: s = septum in septate fiber-tracheid

S. Carlquist


Fig. 5 Pitting in axial parenchyma of angiosperms (a–e) and Gnetales (f). a Akania bidwillii (Hogg) Mabb.,NSW Forestry Commission SFCw-D10096. Radial section, pits dense and mostly bordered on transverse wallof axial parenchyma strand. b Bretschneidera sinensis Hemsley, MADw-21,841. Radial section: five axialparenchyma strands and one septate fiber; pits on cross-walls of axial parenchyma are numerous and bordered.c-e Solmsia calophylla Baill., McPherson 5511 (MO). c, d SEM images of cross-walls of axial parenchymastrands in radial section, to show a single bordered pit in each. e Transverse section, outer face of cross-wall ofaxial parenchyma; all pits are bordered. f Gnetum gnemon, Carlquist 8088 (RSA). Tangential section,illustrating large pits on transverse wall of axial parenchyma strand. Abbreviations: ap = axial parenchyma;sf = septate fiber; tw = transverse wall



Fig. 6 Diffuse and diffuse-in-aggregates axial parenchyma from transverse sections of Winteraceae (a),Canellaceae (b-e) and Sapotaceae (f). a Zygogynum baillonii, Carlquist 15,609 (RSA). Diffuse and diffuse-in-aggregates axial parenchyma. b Warburgia ugandensis Sprague (Forestry Commission of New SouthWales), axial parenchyma diffuse and very scanty pararacheal (arrows point to axial parenchyma cells). c.Canella winterana (L.) Gaertn., USw-6082. Axial parenchyma abaxial. d Pleodendron macranthum Tiegh.,MADw-36,444, axial parenchyma abaxial with a few laeral extensions. e Cinnamosma fragrans Baill., USw-5502, axial parenchyma abaxial and in paratracheal bands. f Dipholis salicifolia A. DC., USw-5740. Axialparenchyma predominantly diffuse-in-aggregates

S. Carlquist


Fig. 7 Angiosperm woods with less water storage in secondary xylem. a-b Prunus lyonii, adventive,Claremont CA. a Transverse section. Axial parenchyma is predominantly pararacheal banded. b Tangentialsection; uniseriate rays as abundant as multiseriate rays. c-d Fouquieria splendens. Cultivated specimendonated by Rancho Santa Ana Botanic Garden. c Transverse section, axial parenchyma in uniseriate diagonalbands, abundant in earlywood. d Tangential section; rays mostly multiseriate, but with no obvious waterstorage cells. e-f Hedera helix, cultivated in non-watered area, Claremont, CA. e Tangential section: raysmostly wide multiseriate, but without obvious storage cells. f Radial section: the fibriform cells are all septatefibers



Fig. 8 Angiosperm woods with perceptible water storage in axial parenchyma. a-d Sections of Malvaassurgentiflora (plant donated by Rancho Santa Ana Botanic Garden) that show various degrees of waterstorage in parenchyma. a Transverse section; axial parenchyma bands mostly narrow, paratracheal, with noobvious water storage. b Tangential section; rays large, multiseriate only, with cells large enough to permitappreciable water storage. c Transverse section from outer wood; pockets of thin-walled axial parenchymawater storage tissue present; some crystals in the thin-walled ray cells. d Tangential section with some thinner-walled axial parenchyma (left), some thicker-walled. e-f Erythrina caffra, adventive in Claremont, CA. eTransverse section. Paratracheal axial parenchyma bands composed of wide cells that account for most waterstorage. f Tangential section: rays narrow, small in volume compared to axial parenchyma

S. Carlquist


Fig. 9 Angiosperm woods with minimal fiber presence. a Crepidiastrum lanceolatum (Asteraceae), Carlquist15,679 (RSA). Transverse section; libriform fibers are relatively scarce compared to axial parenchyma. b–dChorisia speciosa (bombacoid Malvales), cultivated, Claremont, CA. b Ray cells from tangential section;larger cells contain starch, narrower cells have dense pitting on end walls. c Transverse section. Libriformfibers are much less common than the relatively large axial parenchyma cells. d Tangential section. Margins ofrays merge imperceptibly into axial parenchyma; packets of narrow radially elongate cells occur in the rays. e-fPlumiera alba (Apocynaceae), cultivated in Claremont, CA. e Transverse section. Axial parenchyma cellslarge, fibers isolated or in tangential groups. f Tangential section; rays narrow, composed mostly of procum-bent cells distinguishable from the axial parenchyma



Fig. 10 Angiosperms with water-storage wood and raylessness. a–b Jacaratia hassleriana Chodat(Caricaceae), Arid Lands Greenhouses. a Transverse section; secondary xylem of stem, fibers lacking inxylem; fibers present in secondary phloem at top. b Tangential section of stem; secondary xylem consistswholly of water storage tissue except for the vessels. c-d Crassula argentea, cult. Claremont, CA. c Transversesection; axial parenchyma in fascicular secondary xylem, wide ray at right contains tannin idioblasts. dTangential section, ray portion at right; vessels have helical thickenings. e-f Kalanchoe beharensis Drake(Crassulaceae), cultivated in Santa Barbara, CA. e Transverse section of wood; vessels occur in small clustersthat contain axial parenchyma. f Tangential section; wood is rayless

S. Carlquist


Does Axial Parenchyma in Conifers Function in Supporting Conduction as it Doesin Angiosperm Woods?

The distribution of axial parenchyma in angiosperms supports the idea that conductionin vessels is supported or maintained by the action of adjacent axial parenchyma cells(see references cited in Introduction). This does not seem likely in conifers because ofsparseness or absence of axial parenchyma in an appreciable number of conifers. Infact, one can ask what, if the all-tracheid secondary xylem of conifers is so successfulthat hydraulic safety margins in conifers are so much greater in conifers as a whole thanin angiosperms (Hacke et al., 2015), is the function of axial parenchyma in conifers thathave it? The quantities seem insufficient for storage or photosynthates, so that one isinclined to look for subsidiary functions. Axial parenchyma cells in conifers often fillwith resins or other secondary compounds rapidly, suggesting a rot or predatordeterrence. The potential function of axial parenchyma in regeneration following steminjury is difficult to demonstrate. Axial parenchyma in conifers can be confined to theterminal portions of growth rings, but more commonly is scattered in a diffuse patternthroughout the ring (Fig. 1a).

Axial parenchyma in conifers can be rapidly converted to resin-containing cells (Fig.1c) in growth rings that are no longer actively conducting, another evidence of thelimited function of axial parenchyma in conifers. An axial parenchyma that issubdivided, but with bordered pits, shown in Fig. 1d, exemplifies the fact that axialparenchyma is more diversified in conifers than most studies would lead us to believe.

What Do Rays in Conifers Do?

Rays in conifers (other than Gnetales) are rarely more than one cell in thickness (Fig.1b; Greguss, 1955). This does not seem compatible with a storage function, andmentions of starch presence in rays are virtually non-existent. Resins or similarcompounds are often seen in conifer ray cells, however (Fig. 1b), just as they are,simultaneously, in axial parenchyma (Fig. 1a–d). Some ray cells can remain devoid ofcontents. The tangential walls of such cells are often thin, or bear large pits, simple orbordered, (“nodular,” or “nodulated”) with intervening secondary wall portions thatdefine the large size of the pits. There are accurate drawings of the circular and oval pitson the tangential walls of ray cells of Cupressaceae, etc. in Greguss (1955) and similarSEM images in Roman-Jordan et al. (Roman-Jordan et al., 2016, Figs. 6c and 9c).These cells could certainly serve for flow of solutes. The presence of such large pitsbetween ray cells and tracheids would be difficult to explain otherwise.

That rays in conifers have cell polymorphism and therefore more than one functionis clearly demonstrated by the occurrence of ray tracheids in Pinus and Abies (Holden,1913; Greguss, 1955) as well as a few Cupressaceae (Roman-Jordan et al., 2016). Raytracheids have been reported in one angiosperm, Tetracentron (Kedrov, 2012). Theconifers without ray tracheids seem more characteristic of tropical or moist habitats as awhole, but there are exceptions. Ray tracheids as a pathway for sap flow suggests a rolein transferring water from one tracheid to another. One might be able to answer thisquestion with the use of dyes.

Conifer rays can contain secretory canals (Picea, Pinus, Pseudotsuga). This seemsclearly a use of rays as a defense mechanism for the wood, similar to the axial secretory



canals in wood and the abundant amount of resin secretion to be seen in conifer bark.Defense mechanisms, such as crystals, tannins, etc., are often more abundant closer tothe surface of a stem (or other organ) than further inside. However, we should note thatthe expenditure of space and photosynthates on resin canals and on resin-containing raycells and axial parenchyma is larger than on cells that could be claimed to be involved

S. Carlquist


in flow or storage of some sort. Conifers are capable of producing wider rays and moreaxial parenchyma where resin canals occur. Parenchyma cells in conifer woods mayplay less of a role in the osmotic regulation of conduction than they do in angiosperms.However, various types of “cross-field pitting” (pits between tracheids and ray cells,Fig. 1e) lead us to believe that ray cells do have large pit areas in contact with tracheids,and these contacts are likely to be involved in some kind of sugar and/or ion interactionin growth rings that are actively conducting. Storage of starch in conifer rays is scarcelymentioned in literature on conifer woods. These facts tell us much about the efficiencyof the conifer tracheid, suggesting than it requires less of a conduction support systemthat do angiosperm vessels, which are relatively wide.

The diameter of conifer tracheids must be relatively small in order to achieveresistance to embolisms and recovery from freezing (Davis et al., 1999). More numer-ous tracheids of relatively small diameter (compared to vessels of angiosperms) form abasic principle of conifer woods.

There is a potential gain in various types of wood strength if rays are relativelysmall. Strength in mechanical cells of wood is conferred by helical cellulose microfi-brils in a lignified background in secondary walls, but also, quite significantly, bycementing substances between fibriform cells. The relatively great length of fibriformcells increases their adhesive surface (Wellwood, 1962). Thus, the interruption offibriform tissue by rays would decrease strength. Indeed, we can see this macroscop-ically in samples of dried angiosperm woods, where the surfaces of shrinkage cracksrun parallel to rays (“checking”). Thus, there is a negative selective value for large(especially tall) rays in woods. Such rays are most prominent in the stems of lianas,where flexibility is at a premium compared to trunks of larger trees. In this perspective,space in conifer woods is better devoted to more tracheary elements than to larger raysand more axial parenchyma, which thereby play a modally different role in conifersthan they do in angiosperms.

Gnetales

The inclusion of data from Gnetales is important to our understanding of hydraulics inconifers and angiosperms. Long ago, Thompson (1918) presented reasons whyGnetales should not be placed close to angiosperms, a conclusion accepted by Bailey(1944) and confirmed on the basis of molecular data by Bowe et al. (2000), Burleighand Mathews (2004), and subsequent authors. Thus, conifers plus Gnetales become agroup that has been called “gnetifers” or “gnepines.” Wood of Gnetales contains

Fig. 11 Woods of Cactaceae (a-e); wood with successive cambia (f-g). a-b Pereskia aculeata, cult. InClaremont, CA. a Transverse section, starch present in axial and ray parenchyma. b Tangential section;axial parenchyma cells (non-subdivided), caner’ libriform fibers, left. c-e Cereus repandus, cultivated inClaremont, CA. c Transverse section. Two files of secondary xylem fibers have changed to production of axialparenchyma. d Tangential section; portions of two large multiseriate rays. e Tangential section, higher power;limits between ray and axial parenchyma are uncertain. f-g Stegnosperma halimifolium Benth., Carlquist s. n.,1969. f Transverse section of outer portion of stem, to show two vascular increments and the bands ofparenchymatous conjunctive tissue that alternate with them. g Ontogenetic origin of successive cambia andconjunctive tissue from a master cambium. Abbreviations: ap = axial parenchyma; c = cortex; ct = conjunctivetissue; mc =master cambium; mc (d) = location of the dormant master cambium; r = ray; sc = secondarycortex; sp. = secondary phloem; sx = secondary xylem

R



virtually all of the characters found in angiosperm woods (Carlquist, 2012b), in contrastwith conifer wood. Thus, wood of Gnetales offers us an excellent answer to thequestion: what would happen to parenchyma if vessels were evolved in a vessellessgymnosperm?

S. Carlquist


Ray and Axial Parenchyma of Gnetales: Details Related to Function

The parenchyma features by which Gnetales differ from conifers include pres-ence of both multiseriate and uniseriate rays (Figs. 2b and 3b, d, f). Borders arepresent on pits of ray cell walls (Fig. 2c, f) of Ephedra and Gnetum. Borderedpits are also present on axial parenchyma of Gnetum (Fig. 5f), although simplepits with wide pit membrane areas predominate. Small borders occur on pits ofthe living fiber-tracheids of Ephedra, which are functionally equivalent to theaxial parenchyma of Gnetum (Fig. 2d). Similar pits occur on septate fibers ofGnetum (Fig. 2f and 4d). Some, or a large proportion of the axial parenchymacells of Gnetum (Fig. 3a, c, e) as well as the living fiber-tracheids of Ephedra(Fig. 2a) are associated with vessels. Septa sometimes occur within the axialparenchyma strand cells of Gnetum (new report). Welwitschia has thin-walledaxial parenchyma and thin-walled ray cells, both with simple pits (Carlquist andGowans 1995).

In Gnetum gnemon, rays in wood of roots (Fig. 3b) are similar to those in the adultstem (Fig. 3d), whereas those in wood of a young stem (Fig. 3f) are taller, withuniseriates more common. These features of the young stem wood rays accords withwell-known earlier stages in ray ontogeny (see Barghoorn, 1941; Carlquist, 1988) inangiosperms, as illustrated in those two sources for Bursera simaruba. We can evenrefer the rays ofGnetum gnemon to the Heterogeneous Type I of Kribs (1935), whereasthe rays of Welwitschia secondary xylem (Carlquist and Gowans 1995) correspond toPaedomorphic Type I of Carlquist (1988). The juvenilistic rays of Welwitschia arerelated to the fact they are produced within successive cambia, each of which haslimited duration, although the vascular cambium of each of the numerous vascularincrements does produce secondary phloem and secondary xylem.

Parenchyma in Wood of Gnetales: Indicators of Photosynthate Flow or Storage

Starch in rays (Figs. 2c, f and 4d), and in septate fiber-tracheids (Fig. 2e) is seen in theGnetales, as it is in angiosperms. In Gnetales, the nature of pitting, ray cell size, andstarch presence does not suggest a strong differentiation into flow cells versus storagecells. Perhaps the ray cells of Ephedra (and living fiber-tracheids in Ephedra) can serveboth purposes, changing on a seasonal basis. The storage of starch in roots of Gnetumgnemon is considerable (Figs. 2e and 3a): axial parenchyma cells are more commonthan tracheids. No conifer has been reported to have such a high proportion of rootwood cells devoted to storage.

Fig. 12 Angiosperm woods showing cell type dimorphism. a-e Ficus elastica (Moraceae), cultivated inClaremont, CA. a Transverse section; fiber bands alternate with wide axial parenchyma bands which areneither apotracheal nor paratracheal. b Tangential section; axial parenchyma at left, libriform fibers at right. cRadial section; axial parenchyma strands at right, vessel-adjacent parenchyma cells at right are small andcontain gummy (latex?) droplets. d Enlarged transverse section to show starch-rich cells of axial parenchymaband; recent divisions evident in vessel-adjacent parenchyma. e Radial section; point of intersection betweenaxial parenchyma and ray. f Eryngium bupleuroides Hook. & Arn. (Apiaceae), USw-33,857, Transversesection; earlywood fibers are living, latewood fibers are non-living. g Robinia pseudoacacia L., (Fabaceae)Ripon W380w, transverse section. Fibers that are sectioned at their widest point appear like axial parenchyma,but are not

R



The abundant starch storage in rays, axial parenchyma, and septate fiber-tracheids of Gnetales is clearly different from the minimal presence of starchstorage in conifers, but Gnetales are quite similar to angiosperms in the storageof starch in living cells. This suggests that Gnetales can store starch in relation to

S. Carlquist


flushes of growth and fruiting. More importantly, perhaps, living cells accompanyvessels and tracheids in Gnetales, so there is a potential source of carbohydratesthat could serve for transfer into the water columns of vessels. We can see thisassociation in Ephedra. In Fig. 2a, living fiber-tracheids (identifiable by cytoplas-mic contents) can be seen above the larger vessel. The fiber-tracheids are morecommon around vessels than in the tracheid background. In Gnetum gnemon, axialparenchyma is also mostly vasicentric in older stems (Fig. 3c), although somediffusely distributed axial parenchyma stands can easily be found. In the youngstems of Gnetum gnemon (Fig. 3e), axial parenchyma, identifiable by thinnerwalls, tends to form tangential bridges between vessels, not unlike paratrachealbanded axial parenchyma of angiosperms.

Studies on wood physiology of Gnetales are effectively non-existent. The reasonsfor this presumably lie in the lack of commercial value of Gnetales. Gnetales are notdifficult to grow, so such studies should be attempted, because the implications willprobably go well beyond the Gnetales, to conifers and to angiosperms. Likewise, weneed studies on the physiology of wood of cycads, which have multiseriate rays andaxial parenchyma (Greguss, 1968), and also on wood of Ginkgo, which has bothuniseriate rays and axial parenchyma (Greguss, 1955).

Angiosperms

Functions of the Parenchyma Network Listed

If conifer phylogeny has involved minimization of the parenchyma network in woods,whereas angiosperms feature increased quantities of parenchyma, there is the possibil-ity of multiplication of functions in angiosperm wood parenchyma. In order to look foranatomical signals of these functions, we first should have an idea of what functionsmight be served. The following list represents the underpinning of anatomical infor-mation reported in the balance of this paper.

(1) Conduction of photosynthates in solution.(2) Storage of photosynthates, chiefly as starch.(3) Control of conduction by transfer of sugars and ions into the apoplastic stream.(4) Water storage.(5) Structural support by means of turgor.(6) A subsidiary source of mechanical strength by means of secondary walls; thinner

ray cell walls aid in expansion and contraction of stems.(7) Closure of vessels (especially in earlywood) by means of tylosis formation.

Fig. 13 Transverse sections of stem wood of Brassicales to show unusual axial parenchyma distributions. a-bReseda alba L., Kennedy March 2, 1973 (POM). a Axial parenchyma associated with earlywood. b On thesame section, axial parenchyma associated with latewood. c Caylusea hexagynaM. L. Green, Podlech 42,683(RSA). Axial parenchyma is both apotracheal and paratracheal. d Stanleya pinnata Britton, cult. Rancho SantaAna Botanic Garden, axial parenchyma band in both latewood and earlywood. e Tersonia brevipes Moq.,Carlquist 5385 (RSA), axial parenchyma abundant in earlywood; elsewhere diffuse or diagonal diffuse-in-aggregates. f Salvadora persica L., cult. Univ. Calif. Santa Barbara greenhouses. Arrows indicate vascularcambium; Interxylary phloem strand located in axial parenchyma band. Abbreviations: ew = earlywood; ixp =interxylary phloem; lw = latewood; sp = secondary phloem

R



(8) Sites for adjustment to torsion (e.g., rays in liana stems).(9) Auxiliary cells in latewood aiding survival of cambium.(10) Sites for beginning of tissue regeneration following injury.

S. Carlquist


Ray Parenchyma Cell Walls Reveal Modes of Flow in Living Cells

Ray cells commonly are much more prominently pitted on tangentially-oriented walls thanonwalls that have radial (either vertical or horizontal) orientation. This is shown by all of thephotographs of Fig. 4. The pits, when secondary walls are thick enough to aid examinations,and when seen in sectional view, may be simple or bordered (a dumbbell shape of wallsegments between pits in sectional view is a key to presence of borders). Particular attentionshould be paid to Fig. 4b, in which one can compare the prominently pitted tangential walls(vertically oriented in the photograph, seen in sectional view) with the sparsely pittedhorizontal radial walls (oriented horizontally in the photograph) and the sparsely pittedvertical radial walls (in face view in the photograph). The pits in Fig. 4b are all bordered.

One may also see borders on ray cell walls by SEM imaging of the outer surfaces ofray cells (Fig. 4c). The presence of borders, as in borders on cells of the apoplasticwater-conduction system (vessels, tracheids), shows a combination of wide pit mem-branes with overarching pit borders. The wide pit membranes maximize conductionacross the pit membrane, the borders minimize loss of mechanical strength (Carlquist,1988, 2017), a compromise between two opposed requirements. Bordered pits on raycells have been held to indicate flow (Carlquist, 2007a). The appreciation of borderedpits on ray cells has lagged because wood students are accustomed to viewing borderedpits in face view, as in tracheids and vessels, rather than in sectional view. The thicktangential walls of ray cells make detection of borders in face views of pits difficult,although they are clearly revealed with SEM preparations that expose the outertangential surface of a ray cell (Fig. 4c).

Sizes of pits in ray cells can also be assumed to indicate adaptation to flow. Ray cellsof Gnetum (Fig. 4d) are used to illustrate this for convenience, but the same phenom-enon can readily be seen in rays of angiosperm woods. Pits on tangential walls of raycells, especially radially elongate ray cells, are frequently much larger than those on theradial walls, indicative of probable direction of flow.

Density of pitting on ray cell walls can also be assumed to be indicative ofadaptation to flow. Chorisia speciosa (Fig. 4e) has pits densest on the narrow tangentialwalls of radially elongate ray cells, grading to medium density in medium-diametercells (Fig. 4e, lower right), and to sparse in larger cells. The pitting in walls in the largerray cells in Fig. 4e are not shown, but the presence of starch grains is.

Axial Parenchyma Cell Walls Often Reflect a Conductive Function

Certainly pits are more prominent on ray cells than on axial parenchyma cells. If onelooks at the transverse walls between the stand cells of an axial parenchyma strand, one

Fig. 14 Septate and living fibers in angiosperm woods. a-b Trattinckia demerarae Sandwith (Burseraceae),MADw-19,938. a Transverse section; background cell type is septate fibers; axial parenchyma identifiable asslightly wider cells around the vessels. b Radial section. Axial parenchyma strands (lower left) can bedistinguished from ray cells (top) and septate fibers (lower right and center). c Nerium oleander(Apocynaceae), cult. Claremont, CA. Tangential section. All fibers are septate. d Foeniculum vulgare Mill.(Apiaceae), adventive in Santa Barbara, CA. Fibers are living (some septate), rays tall, juvenilistic. e-gPimpinella dendrotragium Webb & Berthel. (Apiaceae), Carlquist 2709 (RSA). e Transverse section. Raysabsent. f Transverse section, higher power: axial parenchyma cells surround vessels (some recently divided,walls thinner than those of fiber). g Tangential section; section entirely rayless except for the two smalluniseriate rays shown

R



can see that these walls bear pitting more pronounced than that of the axial (vertically-oriented) walls of axial parenchyma. This can be seen in radial sections of wood of twogenera of Akaniaceae, Akania (Fig. 5a) and Bretschneidera (Fig. 5b). In Akania, thepits on the end walls (sectional view, upper right) are much more numerous than thoseof the vertical walls (below the cross wall, in face view). All of these pits have borders,

S. Carlquist


albeit inconspicuous ones. In the Bretschneidera section (Fig. 5b), transverse walls offive parenchyma strands are shown. In each of these diagonal cross-walls, bordered pitsare densely placed. Pits are much sparser (but slightly bordered) on lateral walls ofthese strand calls.

Solmsia of the Thymeleaceae was selected for SEM study of axial parenchymapitting because it has thick axial parenchyma walls. Bordered pits in sectional viewoccur on the transverse walls of axial parenchyma strands (Fig. 5c, d). As seen in faceview of the outer wall surface (from a transverse section of the wood). The borderednature of the pits is clear (Fig. 5e).

The transverse wall of an axial parenchyma strand in wood of Gnetum gnemon isshown in Fig. 5f. Pit membrane areas are more extensive in the transverse wall than arethe secondary wall portions. This condition can often be seen in angiosperms. Some-times the transverse wall of an axial parenchyma strand bears a single large pit.

Axial Parenchyma: Changes in Patterns of Aggregation and Abundance

Although Amborella is considered the sister to the remainder of the angiosperms in allrecent molecular phylogenies, particular features of this monotypic genus may or maynot be plesiomorphic. However, Amborella has sparse diffuse axial parenchyma(Carlquist, 2012a), as do a number of other angiosperms with a large number offeatures now interpreted a plesiomorphic (Metcalfe & Chalk, 1950; Metcalfe &Chalk, 1983; Metcalfe, 1987). Although one can say that the axial parenchyma ofAmborella, or for that matter, Warburgia (Fig. 6b) is too scarce to function in theparenchyma network, one must remember that three-dimensional wood studies(Zimmermann, 1971; Kedrov, 2012) indicate that living cells in wood are not isolated.Also, the tracheids in these genera are long, so more numerous axial-parenchyma-to-tracheid contacts are likely to occur than study of transverse sections might suggest.

One notices in woods that have “diffuse” axial parenchyma that some axial paren-chyma cells do contact vessels (Fig. 6b) and some form tangential groupings (Fig. 6a,f). Truly random distributions of axial parenchyma are rare—and even if they occur,some of the axial parenchyma strands would contact vessels here and there. Thetangential groupings, commonly called diffuse-in-aggregates (Fig. 6a, f), rarely formlong continuous tangential bands, nor do bands two or three cells thick. Thereby,tangential lines or bands of axial parenchyma do not seem likely to compartmentalizepockets of fungus invasion, as envisioned by Shigo (1984), although that may beoperative in certain woods. One can ask why, when vessels are mostly radially groupedin angiosperm woods, banded axial parenchyma runs not parallel to those bands but atright angles to them. The most obvious explanation would be that upright cells

Fig. 15 Wood functions related to axial parenchyma in Apiales. a-f Foeniculum vulgare, adventive in SantaBarbara, CA 93110. a Primary xylem pole of a main vascular bundle in transverse section; protoxylemelements collapse, leaving uniseriate rings of axial parenchyma. b Area between main bundles in whichsecondary xylem forms from interfascicular cambium without primary xylem formation. c Transverse sectionof secondary xylem; a narrow band of latewood is present. d Radial section of terminal latewood. e Avasculartracheid from the terminal latewood, from a radial section. f Metaxylem vessel with an associated strand ofaxial parenchyma (left). g Oreopanax steinbachianus Harms, cult. Santa Barbara, CA. SEM image of radialsection of stem, primary xylem at left, secondary xylem at right. Abbreviations: ew = earlywood; lw =latewood; ptx = protoxylem; px = primary xylem; sf = starch in septate fiber; sx = secondary xylem

R



belonging to wings of multiseriate rays or in uniseriate rays do run parallel to radialchains of vessels. Radial chains of axial parenchyma would therefore be redundant.

Winteraceae (Fig. 6a) and Canellaceae (Fig. 6b–e) are sister families according torecent molecular phylogenies, so they give us a chance to compare woods with vessels(Canellaceae) with vesselless woods (Winteraceae). One unexpected result is that the

Fig. 16 SEM images of tangential (a-d) and radial (e-f) sections of young stem of Oreopanax steinbachianus(cult. Santa Barbara, CA). a Outer (left) and inner (right) surfaces of ray cells. Pits are bordered. Inner surfaceof ray cell; pits of various sizes, some subdivided. c Starch storage cell (left) and flow cell (right) fromtangential section of ray, showing contrasting sizes and densities of pits. d Tip (wing) cell of ray fromtangential section of ray; as seen from outer surface (below), pits are minute and bordered) inner surface of cellwith starch, above. e Radial section, procumbent (flow) cells above, wing cell file below; pits on outer surfacesof cells are minute, sparse. f Metaxylem—secondary xylem transition in radial section as indicated byprogressive dwindling of bar number in perforation plates. Axial parenchyma surrounds all vessels

S. Carlquist


vesselless wood (Fig. 6a) has tracheids much wider than the tracheids or fiber-tracheidsin the vessel-bearing woods (Fig. 6b–e). Thus, the conductivity of the tracheids in mostWinteraceae is much greater than one would have supposed (all of the photographs onFig. 6 are at the same scale of magnification). With the potential support of thetracheids by diffuse and diffuse-in-aggregates axial parenchyma, a vesselless wood isthereby not disadvantaged.

Although Metcalfe (1987) figures more abundant diffuse axial parenchyma (anddefinitely tracheids) for Warburgia stuhlmannii Engl., some axial parenchyma cellscontact vessels in his figures as well as mine (Fig. 6b). In Canella (Fig. 6c) andPleodendron (Fig. 6d), the axial parenchyma is clearly abaxial (a form of paratrachealparenchyma), with some lateral extensions in Pleodendron. In Cinnamosma (Fig. 6e),the axial parenchyma is transitional between paratracheal and paratracheal-banded.Thus, the wood anatomy of Canellaceae features repatterning of the axial parenchymaso that the arrangement of axial parenchyma strongly suggests a functional interactionwith vessels. The most probable one at this moment seems to be the transfer of sugarsinto vessels as a way of maintaining the safety of water columns.

Although Canellaceae have tracheids (possibly sometimes fiber-tracheids), as clearlyshown in the Metcalfe (1987) figure for Warburgia stuhlmannii, Dipholis of theSapotaceae (Fig. 6f) has fiber-tracheids. Thus, although there is an association betweentracheids and diffuse parenchyma in the majority of woods with tracheids, there areexceptions. One should note that the lines of diffuse-in-aggregates axial parenchymaand diffuse cells in Dipholis contact both vessels and rays in places. Thus, just anoccasional axial parenchyma cell or two in contact with a vessel may serve formaintenance of water columns. In fact, axial parenchyma in Asteraceae is mostlyscanty paratracheal (scanty vasicentric), also illustrating that whatever the function ofaxial parenchyma may be in relation to vessels, the quantity of axial parenchyma cellstouching a vessel or vessel group can be rather minimal.

Diffuse parenchyma should not be viewed as an inefficient way of contact betweenthe parenchyma network and vessels. Rather, a relatively high degree of associationbetween diffuse axial parenchyma and presence of tracheids (Kribs, 1937) suggests thatdiffuse axial parenchyma is supporting conduction processes in both tracheids andvessels of a given wood. Diffuse-in-aggregates very likely has the effect of increasingthe number of contacts between rays and axial parenchyma as well as among axialparenchyma cells.

The Anatomy of Water Content in Woods

Comparisons of water content in freshly harvested (“green”) conifer and angiospermwoods are few. One is the USDA (1974) compilation, based largely on results from theForest Products Laboratory (J. F. Siau, 1995, personal communication). According toTable 3–3 in that reference, sapwood water percentages are higher in conifers than inangiosperms, probably because at the time of harvesting, tracheids in conifer woodsretain water, whereas in angiosperm woods, vessels empty and fibrous tissue (libriformfibers mostly) is less likely to contain water. In the list of the woods in Table 3–3(USDA, 1974), none of the woods would be considered succulent. That would not beexpected in a publication concerned with commercially usable woods. Within theangiosperms listed in that table, higher percentages of water content were reported in



angiosperms of wetter habitats: Betula, Liquidambar, Magnolia, Nyssa, Platanus, andPopulus. Half of those six genera have tracheids as their imperforate tracheary ele-ments, so water may be retained in those tracheids upon harvesting.

S. Carlquist


Water content in typically woody angiosperms is relatively small compared to that inangiosperm wood and bark which could be considered to have degrees of succulence.In Table 1, the values reported for “WM/WD” for typically woody angiosperms arevery similar to those reported in Table 3–3 of USDA (1974). However, the species inTable 1 were selected as a ways of comparing angiosperm species with wood probablydevoted to sequestering relatively large quantities of water to the typically woodyspecies. To develop the data of Table 1, stems of the selected species were harvestedbetween 9 and 10 AM between January 10 and 13, 1986. The plants had received onlyrainwater since November 1 of 1985, but that season was above average in rainfall inClaremont, California. Bark was separated from secondary xylem and pith, and barkand wood were weighed separately fresh and after drying in a 60 °C oven. Values arepresented as percentages in Table 1 in order to reveal the relative roles of bark andwood in water storage in the various species.

Microtome sections were also prepared of the woods listed in Table 1 as a way ofdetermining the probable sites of water storage within the woods. From those, exampleswere selected for illustrations (Figs. 7, 8, 9, 10, 11, 12, 13, and 14). We find that sitesfor water storage are quite diverse in the more succulent (boldface) species studied. Notincluded in this study is the effect of seasonal stem expansion and contraction that iscovered by Scholz et al. (2008). That study included bark as well as wood.

Characters of Non-succulent Stems

In Table 1, non-succulent bark is indicated for Artemisia californica, Bougainvilleaglabra, Cercidium floridum, Erythrina caffra, Fouquieria splendens, Hedera helix,Malosma laurina, Malva assurgentiflora, Nerium laurina, Peritoma (Isomeris)arborea, and Prunus lyonii. Fouquieria splendens, a desert shrub, is often thought ofin conjunction with succulents, but its bark features thick sclerenchyma layers. In fact,most desert shrubs other than cacti do not have much water storage in bark. Instead,drought deciduousness is the most common way of dealing with the dry season.

Succulent Bark

Bark relatively high in water storage is shown in Aeonium arboreum, Cereus repandus,Chorisia speciosa, Crassula argentea, Euphorbia pentagona, Ficus elastica, Nicotianaglauca, Leptosyne (Coreopsis) gigantea, Pereskia aculeata, Portulacaria afra, andRicinus communis. About half would traditionally be classified as succulents (thespecies of Aeonium, Euphorbia, Leptosyne, Pereskia, and Portulacaria), but the

Fig. 17 Rays of Apiales (a-e), Chloranthaceae (f-g) and Campanulaceae (h). a-g. Radial sections to illustrateray cell shape. a. Myodocarpus fraxinifolius Brongn. & Gris (Myodocarpaceae), Carlquist 4268 (RSA). Raycells are radially elongate, typical of the basal woody Apiales (e.g., Araliaceae). b Heteromorpha trifoliataEckl. & Zeyh. Apiaceae), Carlquist 2670 (RSA). Ray cells are mostly square to upright. c. Eryngiuminaccessum Skottsb., (Apiaceae), Skottsberg 20 (Göteborg Botanic Garden). A few files of procumbent cellsin center of ray, ray otherwise of square and upright cells. d-e Arracacia atropurpurea Benth. & Hook. f.(Apiaceae), Iltis 277 (MAD). d Secondary xylem close to pith; ray cells are all upright. e Secondary xylemclose to cambium; several files of procumbent cells, other ray cells are square to upright. fHedyosmum scabrumSolms, SJRw-2864, radial section. All ray cells are upright. g Chloranthus officinalis Blume, Stone 12,116(KL), radial section. All ray cells are upright. h Cyanea leptostegia A. Gray, Carlquist 1961 (RSA), tangentialsection. Rays are very tall, composed wholly of upright cells



exceptions are of special interest. Ricinus communis would probably be considered asemi-succulent shrub or small tree, and Nicotiana glauca would probably also fall intothis category. The idea that Ficus elastica has water storage in its bark should not besurprising, because Ficus is prominent in dry tropical localities. Malva assurgentiflorafalls only slightly below the species in the “succulent bark” category; it grows onmaritime rocky shores and is thus a marginal halophyte. The succulence of a coastalhalophyte such as Cakile edentula (Bigel.) Hook. is somewhat more pronounced.

The third and fourth columns of Table 1 compare the water content of bark to that ofwood for the species studied. These figures highlight concordance or disparity betweenbark and wood for the species studied. Disparity is most evident for Aeonium

Table 1 Water content of bark and wood in angiosperm species

Species BF/BD BM/BD BM/WM BF/WF WF/WD WM/WD WM/WF

Aeonium arboreum Webb & Berth. 7.32 6.32 9.38 7.06 2.85 1.85 0.65

Aesculus californica Nutt. 3.27 2.27 0.34 0.26 2.21 1.21 0.55

Artemisia californica Less. 1.90 0.90 0.37 0.20 1.59 0.59 0.37

Bougainvillea glabra Choisy 2.78 0.64 0.38 0.22 1.60 0.59 0.37

Calliandra inaequilatera Rusby 2.41 1.41 0.68 0.68 1.63 0.62 0.38

Cercidium floridum Benth.ex A. Gray

1.83 0.84 0.19 0.16 1.60 0.60 0.37

Cereus repandus Mill. 9.14 8.14 5.62 5.09 5.14 4.14 0.85

Chorisia speciosa A. St. Hil. 4.16 3.16 1.43 1.17 2.63 1.63 0.62

Crassula argentea Thunb. 8.92 7.92 4.74 4.51 11.90 10.95 0.92

Erythrina caffra Thunb. 3.66 2.66 2.34 1.43 3.93 2.93 0.74

Euphorbia pentagona Haw, 6.25 5.25 1.33 1.05 2.99 2.93 0.67

Ficus elastica Roxb. ex Hornem. 4.10 3.11 1.40 1.00 2.19 1.19 0.54

Fouquieria splendensEngelm in Wisl.

2.40 1.40 1.13 1.39 1.59 0.59 0.37

Hedera helix L. 2.78 1.79 0.23 0.19 2.10 1.10 0.52

Leptosyne gigantea Kellogg 8.92 7.92 1.93 1.50 4.55 3.49 0.78

Malosma laurina Engl. 2.43 1.43 0.45 0.31 1.66 0.66 0.40

Malva assurgentiflora(Kellogg) M. Ray

3.86 2.86 0.80 0.73 3.14 2.14 0.68

Nerium oleander L. 2.18 1.17 0.56 0.43 1.72 0.74 0.72

Nicotiana glauca Graham 5.16 4.14 0.40 0.29 2.33 1.33 0.57

Pereskia aculeata Mill. 4.44 3.44 1.14 0.80 2.23 1.23 0.55

Peritoma arborea (Nutt.) Iltis 2.02 1.01 0.21 0.24 2.27 1.28 0.56

Plumeria alba L. 6.64 5.64 1.69 1.24 2.66 1.66 0.62

Portulacaria afra Jacq. 4.69 3.69 0.67 0.56 2.96 1.98 0.66

Prunus lyonii Sudw. 2.60 1.16 0.31 0.16 1.47 0.46 0.32

Ricinus communis L. 4.68 3.66 0.61 0.50 2.80 1.80 0.65

Higher values for each column are in boldface, and indicate greater water content; lower values in eachcolumn are in italics and indicate lower water content. Columns 3 and 4 indicate degree of allocation of waterbetween bark and wood. B = bark; D = dried; F = Fresh (weight); M =moisture (difference between freshweight and dry weight); W =wood. Further explanations in text

S. Carlquist


arboreum, which has a fiber-free succulent bark but a dense, fibrous rayless wood,much like that of Kalanchoe beharensis (Fig. 10e, f), also in Crassulaceae. The treespecies of Erythrina have prominent water storage in secondary xylem, but not in bark.

The species in Table 1 in which neither bark nor wood is adapted for water storageinclude Aesculus californica, Artemisia californica, Bougainvillea glabra, Cercidiumfloridum, Hedera helix, Malosma laurina, and Peritoma arborea. These species growin dryland situations, but can be regarded as truly woody species. Aesculus californica,Artemisia californica, and Cercidium floridum are all drought-deciduous.

Water Storage in Secondary Xylem

Figure 7 is devoted to species that show no evidence of enhanced water storage inwood. These are all species included in Table 1. Prunus lyonii (Fig. 7a, b) has bands ofaxial parenchyma, not exceptional in amount for a woody species; the bands intersectmost vessels or vessel groupings as seen in transverse section. Rays in this species donot occupy a large proportion of the wood as seen in tangential section (Fig. 7b). Thecells are of moderate size and thick-walled, and thus are not suited for water storage toany pronounced degree. Ray cells have rigid secondary walls (Fig. 7a, b) which wouldbe antithetical to the demands of water storage, in which a cell volume fluctuates. Axialparenchyma is similar in wall thickness, but the cells are even smaller.

The wood of Fouquieria splendens (Fig. 7c, d) is similar to that of Prunus lyonii.The rays (Fig. 7d) are larger than those of Prunus lyonii, but when compared to those ofMalva assurgentiflora (Fig. 8b, they are relatively small, and occupy a smaller propor-tion of the wood. The axial parenchyma of F. splendens is more abundant in earlywoodthan in latewood, and most of each growth rings is latewood (Fig. 7c). Axial paren-chyma in latewood occurs in groupings that look diagonal more often than tangential.In any case, the total volume of axial parenchyma and its cell size in F. splendensmitigate against this tissue serving as a locus for water storage. The short shoots ofF. splendens do leaf out very rapidly (in a few days or a week), a habit that correlateswith the greater volume of rays compared to those of P. lyoni.

Hedera helix (Fig. 7e, f) has large rays, composed of procumbent cells (Fig. 7e).Such rays can serve as massive conduits for photosynthates in solution that are requiredfor the flushing habit characteristic of Araliaceae (the upright adult shoots of Hederashow this much more clearly than the sprawling juvenile shoots). Axial parenchyma isnot prominent. Instead, the background of Hedera wood, as in other Araliaceae, iscomposed of septate fibers that can be shown to store starch prior to growth events (seeFig. 15g). Thus, the wood of Hedera is not a prominent source of water storage, but isinstead devoted to photosynthate storage and retrieval.

Diverse Designs for Water Storage in Wood

Malva (Lavatera) assurgentiflora wood (Fig. 8a-d) shows some wood succulence, adegree confirmed by the figures for it in Table 1. Axial parenchyma is banded, mostlyparatracheal but with some apotracheal patterning as well (Fig. 8a). The bands in Fig.8a are not unusually abundant, but some stems of this species, especially older ones,tend to show radially wider bands of axial parenchyma with thin walls (Fig. 8c, d).Thus, M. assurgentiflora has a flexible system for devoting more prominence to



mechanical tissue in younger upright stems while producing more abundant waterstorage tissue at the periphery of outer stems and at the bases of branches and in roots.Wall thickness varies in axial parenchyma, presumably in accordance with shifttowards storage and away from mechanical strength, of vice versa. The contactsbetween axial parenchyma bands and rays are massive (Fig. 8c). The amount of raytissue in M. assurgentiflora is much greater than in the non-succulent species or Fig. 7(compare with Fig. 8b, d). The rays are also taller than those of a typical woody plant.The rays are composed of three kinds of cells: (1) most common, isodiametric cellswith no visible contents; (2) similar cells with rhomboidal calcium oxalate crystals,presumably to deter wood predation; and (3) packets of cells of smaller diameter,scattered at various positions in the multiseriate rays. The smaller-diameter ray cells areelongate as seen in a radial section, and can therefore be suspected of having a designmore characteristic of flow than storage.

Erythrina is a genus of Fabaceae that is typically a tree of seasonally dry subtropicalhabitats; it may also be a shrub. Most of the species are drought-deciduous. Althoughthe bark of E. caffra is very thin with negligible water content, the wood is mostlydevoted to water storage. As can be seen in Fig. 8e, f), the tissue used for this storage ismostly axial parenchyma, not rays. Fibrous bands alternate with prominent bands ofaxial parenchyma (Fig. 8e). As seen in tangential section (Fig. 8f), the axial parenchy-ma strands are commonly two cells in length, but some are a single cell in length, andthe strands or single cells are storied. The rays of E. caffra (Fig. 8f). The rays are muchsmaller than those, for example, of M. assurgentiflora (Fig. 8b), and are mostlycomposed of cells of small diameter as seen in tangential sections. In radial ortransverse sections (Fig. 8f), the ray cells are mostly markedly elongate, and cantherefore be termed flow cells.

Increasing degrees of conversion of secondary xylem to water storage can be seen inthe species shown in Fig. 9. Crepidiastrum lanceolatum (Fig. 9a) has upright stems. Itis a scarce secondarily woody shrub of the Ogasawara Islands. The secondary xylemconsists of vessels, thin-walled ray cells and axial parenchyma, and occasional patchesof libriform fibers, which are narrower than the vessels. The libriform fibers are notuniformly distributed, but seem to occur in response to seasonal or other requirement ofmechanical strength for upright stems (Carlquist, 1983). Fiber-free zones presumablyfunction in water storage primarily.

In Chorisia speciosa (Fig. 9b–d), a tank tree, libriform fibers occur singly or in smallgroups, which form tangential bands (Fig. 9c). The remaining axial tissue consists ofvessels and axial parenchyma. Libriform fibers can be seen in a tangential section (Fig.9d); the axial parenchyma cells are not markedly elongate, whereas the libriform fibersare very long. The cells of the rays, as seen in tangential section (Fig. 9b) grade fromlarger cells containing starch to smaller cells relatively poor in starch. The smaller cellsare more elongate, as seen in radial section; the starch-storage cells are more nearlyisodiametric. In tangential section (Fig. 9d), the axial parenchyma cells grade into themargins of the rays, so that the rays appear poorly delimited. The narrower cells(probably flow cells) are located in the central portions of the rays.

Plumeria is a drought-deciduous shrub with thick stems. The secondary xylem (Fig.9e, f) is very similar to that of Chorisia, although the two are in unrelated families.Alternation of fibrous cells (fiber-tracheids in Plumeria) with axial parenchyma formsan optimal plan for simultaneous strength and water storage in Plumeria. Chorisia, in

S. Carlquist


contrast to Erythrina, has alternation of the two types of cells in bands—a modificationof a basic legume wood plan. In tangential section, there is a marked difference, in thatPlumeria has well-defined rays composed of radially elongate cells. The tip cells of therays are vertically elongate, like the axial parenchyma they accompany. The stems ofEuphorbia pentagona (Table 1; not illustrated) are quite different, because they haveuniseriate rays predominantly and store water in living fibers and axial parenchyma, notunlike other cactiform species of Euphorbia (Carlquist, 1970).

Conversion of Wood (Except for Vessels) Entirely to Storage Parenchyma

The family Caricaceae has woods the rays and background tissue of which are converted tostorage parenchyma (Fisher, 1980; Carlquist, 1998). This is illustrated by Jacaratia(Fig. 10a, b). Bands of laticifers (Fig. 10a) are the only exception to that. Rays are composedwholly of upright ray cells, a feature of permanent juvenilism,which is also suggested by thepitting in vessels (Fig. 10b). The remainder of the axial xylem is composed of axialparenchyma strands 1–2 cells in length. Compensating for this minimal-strength configura-tion is the secondary phloemwhich has prominent bands of phloem fibers (Fig. 10a, top). Infact, xylarium specimens of Caricaceae are sometimes composed wholly of secondaryphloem, which is sometimes mistaken for wood because of its fibrous nature.

A water storage modality similar to that of Caricaceae occurs in Crassula argentea(Fig. 10c, d). The secondary phloem of C. argentea, however, consists only of thin-walled cells. Rays are very wide (Fig. 10c, d, right halves of photographs). Tanninidioblasts may be found scattered throughout the axial parenchyma and the rays. Axialparenchyma cells are not subdivided into strands (Fig. 10d). Crassula argentea is asucculent in which turgor of water storage cells is responsible for achieving the upright,shrublike form of the plant, which can, in fact, bend over after several months withoutwatering or rainfall. This type of succulence can also be found in the globular cereoidcacti, in which shrinkage between the ribs is prominent, rather than longitudinalshrinkage (Gibson 1970).

Kalanchoe beharensis (Fig. 10e, f) and the woodier species of Aeonium, such asA. arboreum, have an entirely different mode of mechanical support. The wood in theseis rayless. A few axial parenchyma cells, insufficient to achieve much water storage, arein contact with the vessels in A. arboreum and K. beharensis. The thick cortex in bothof these is the source of water storage, and is without fibers. With respect to wood, mostspecies of Crassulaceae are between the extremes shown for these two species(Metcalfe & Chalk, 1950).

Wood of Pereskia aculeata (Cactaceae) is shown in Fig. 11a, b. One would notjudge from these photographs that this is the wood of a succulent, and the values inTable 1 show that in fact, it does not rank as a true succulent with respect to woodanatomy. The amount of axial parenchyma does not seem exceptional (Fig. 11a), but asseen in tangential section (Fig. 11b), some of the libriform fibers are wider and thinner-walled (and thereby probably qualify as water-storage cells, whereas others (darker) arenarrower and thicker-walled. The amount of ray tissue does seem more than average fora woody species, but not by much. Pereskia aculeata does qualify as a leaf succulent.

Cereus repandus (Fig. 11c–e) would qualify as a true succulent based on the muchgreater proportion of tissue devoted to living cells, especially the rays, and the figures inTable 1 verify this impression. The vessel groupings of this cactus are sheathed by one



to three layers of axial parenchyma (Fig. 11c). Interestingly, although axial parenchymais abundant (Fig. 11e, right), the septa in fibers indicate that the fibers are living also(Fig. 11e. left). In both cereoid and opuntioid cacti, giant primary rays continue withoutsubdivision during secondary growth, so that when thin-walled parenchyma is removedfrom a stem, a coarse reticulate woody “skeleton” is visible. The rays in Fig. 11d aresmall by comparison with the giant primary rays which are extended by cambialactivity into the secondary xylem.

The localities for water storage are quite varied, and may be correlated withgrowth form and with phylogeny. Some of these are explored by Gibson(1970). A paper by Chapotin et al. (2006) is particularly valuable for showingthat in Adansonia, a close relative of Chorisia, water storage works seasonally,rather than daily. We very much need further studies of this kind, but themorphology of succulence and the participation of wood in the water storageprogram of a plant suggest that succulence usually works on a seasonal basis,with the exception of, for example, halophytes, where salt accumulation viawater storage permits growth in saline environments. The plants we typicallythink of as succulents grow in environments that are highly seasonal. In theseenvironments, such as the summer-wet Colorado Desert of Arizona and adjacentSonora, or the summer-wet deserts of South Africa, not only is water accumu-lation accomplished in a few months of the year, flowering and fruiting are alsoseasonal. Some succulents are notable for their flushing habit, which requiresnot only water storage, but photosynthate storage as well. Adansonia andChorisia exhibit flushing growth of shoots, followed in the warmer monthsby massive flowering and then fruit production. External behavior is thuscorrelated with the physiological studies of Chapotin et al. (2006).

Photosynthate Storage: What Do We Know?

In the above account, the word “storage” might mean either starch or waterstorage. Water storage is more readily visible by means of larger cell size,thinner-walled cells, more nearly isodiametric shape (except for living fibers),and greater-than-normal quantity of cells conforming to this description. Photo-synthates, most easily observed in the form of starch, may not be accompanied byany of these special features. For example, in deciduous species of Quercus, raycells and axial parenchyma cells all contain numerous starch grains during winter.We know that these serve for leafing out, flowering, and fruiting as the yearprogresses, although we do not have quantitative measures. Starch accumulationand hydrolysis/utilization may occur on a daily basis in actively-growing herbs(Scialdone & Howard, 2015), but deciduous trees, drought-deciduous trees andshrubs, and tank plants must have cycling that features other time periods. Wevery much need to know the cycling of such events in woody plants in relation toseasonal temperature and water availability. In fact, SEM study of starch grainpresence is ideal because it is accomplished simply (liquid-preserved plant por-tions are required for study), and starch grains can be observed in material fixed atintervals throughout the year. Moreover, the size and surfaces of starch grains canreveal whether they are increasing in size or are eroding away.

S. Carlquist


Conjunctive Tissue: Origin and Function

The phenomenon of successive cambia was clearly enunciated and correctly applied toa roster of angiosperm species by Pfeiffer (1926). An example is shown here forStegnosperma (Fig. 11f). Successive vascular increments are produced. Each consistsof a vascular cambium that produces secondary phloem and secondary xylem. Thevascular increments are produced by a master cambium, a lateral meristem that beginsin the cortex and functions for long periods as a single functional meristematic celllayer, producing conjunctive tissue (a type of parenchyma, usually), then a vascularcambium, inwardly (Fig. 11g). The vascular cambium may be dormant after a cycle ofinitiating a master cambium and conjunctive tissue. This dormancy has led variousworkers to assume that a vascular cambium, rather than the master cambium in thecortex, is responsible for the process. In plants that grow actively, such as the beet,Beta, the master cambium does not become dormant (until the beet stops growing), butin woodier plants, there can be numerous alternating periods of dormancy and activityin the master cambium, resulting in the corresponding number of vascular increments(Carlquist, 2007b). There have been many erroneous interpretations of the ontogeny ofsuccessive cambia, based on illustrations that omit the master cambium or the vascularcambia and thereby do not show the entire process.

The interest of successive cambia in the present essay is not so much the ontogeny aswhat the parenchyma of the conjunctive tissue actually does. In Beta, it stores sugar, butat the same time, it stores ions. The family Chenopodiaceae, to which Beta belongs, isnoted for growing in salty soils. In Beta, the conjunctive tissue sequesters salts, therebybeing at a kind of osmotic par with salty soil (globular trichomes on the surfaces ofAtriplex and Chenopodium leaves are another way of sequestering excess salt). Thesugar in the conjunctive tissue forms the basis for the bolting of the single largeinflorescence of Beta (Biancardi et al., 2012). Conjunctive tissue in plants withsuccessive cambia is a way of forming parenchyma cylinders alternating with activexylem and phloem, thus providing an excellent way of innervating a storage tissue. Inmost plants with successive cambia, the vascular cambia remain active for indefiniteperiods, as evidenced by their continued production of secondary xylem and phloem(Carlquist, 2007b). Conjunctive tissue also serves for enhancing flexibility of lianoidstems, as in Bougainvillea, Boussingaultia, Chamissoa and others. In a sense, thebackground ground tissue of monocot stems serves for this purpose, as inDioscoreaceae.

Diversification in Axial Parenchyma Functions

We tend to think of axial parenchyma as anatomically homogeneous, and it oftenappears to be, but perhaps our observations have been incomplete. This could becaused by the observation of dried wood samples that do not, for example, reveal theoccurrence of starch in some axial parenchyma cells of a wood, but absence in others.Ficus elastica (Fig. 12a-e) is introduced as an example here, but there must be manymore that are currently unreported. A transverse section of wood of F. elastica(Fig. 12a) shows prominent tangential bands of axial parenchyma, alternating withapproximately equally thick bands of libriform fibers. The axial parenchyma (Fig. 12bleft) consists of strands mostly 4 cells long. These bands form large contact areas with



rays (Fig. 12e). The rays are narrow multiseriate, with mostly procumbent cells but alsoupright cells contact and simulate the axial parenchyma (Figs. 12b). The tangentialbands of axial parenchyma contrast with the sheaths, one to three cells in thickness, ofparatracheal axial parenchyma. The paratracheal parenchyma is histologically distinct,and has much smaller cells (compare Fig. 12c, right, with axial parenchyma cells, left).The paratracheal cells are smaller in diameter, Fig. 12d, compared to the cells of thebanded axial parenchyma, Fig. 12d, top. The bands of axial parenchyma contain starch(Fig. 12d, top), the paratracheal axial parenchyma cells were not observed to containstarch in the specimen examined.

Another type of axial parenchyma cell dimorphism can be found with respect tostrands of small crystal-bearing cells (“chambered crystals”). These are reported forcaesalpinoid, mimosoid, and papilionate Fabaceae (Metcalfe & Chalk, 1950). “Idio-blastic” axial parenchyma cells are reported in Dinizia (Fabaceae) by Evans et al.(2006), but no difference between these diffuse cells and the paratracheal cells ismentioned. The wood of Robinia (Fabaceae) appears to have diffuse axial parenchymacells as seen in transverse section (Fig. 12g), but these prove to be merely the widestpoints of libriform fibers which are identical to other libriform fibers, as can becofirmed in longitudinal sections.

Fiber Dimorphism as a Source of Living Cells

Fiber dimorphism, monographed recently (Carlquist, 2014) includes instances in whichwide living fibers occur in patches whereas other fibers in the same wood are narrowerand non-living. This phenomenon is widespread but not common in angiosperms. Apreviously unreported instance in Eryngium bupleuroides (Apiaceae) is reported here(Fig. 12f). More instances are likely to be reported, and these will demonstrate theflexibility that angiosperms possess for degrees of modification of cell types in order toperform more than a single function.

Functions of Axial Parenchyma in Brassicales: Shifts in Axial ParenchymaDuring a Year

Marginal axial parenchyma is an umbrella term that includes terminal parenchyma, atthe end of a growth ring, and initial axial parenchyma, at the beginning of a growthring. Transverse sections of wood from four families of Brassicales are included inFig. 13: Resedaceae (A-C), Brassicaceae (D), and Gyrostemonaceae (E). Reseda alba(Fig. 13a, b), Caylusea hexagyna (Fig. 13c), Stanleya pinnata (Fig. 13d), and Tersoniabrevipes (Fig. 13f) are all short-lived perennials or shrubby annuals that grow in dryopen areas subject to drying—or an occasional rain—during the growing season. Thesecircumstances may account for the irregular patterning of axial parenchyma. Resedaalba can have initial parenchyma (Fig. 13a) as well as terminal parenchyma (Fig. 13b)in the same stem. Likewise, Caylusea hexagyna (C) can have axial parenchyma bandsassociated with both wide and narrow vessels. In Stanleya pinnata (D), parenchymabands extend from latewood into earlywood—perhaps indicating secondary growthduring wet winter month, followed by more active growth during warm spring monthswhile the soil is still moist. Tersonia brevipes (E) has small latewood vessels as well asvery large earlywood vessels in a background of axial parenchyma, plus diffuse or

S. Carlquist


small groupings of axial parenchyma during the balance of a growth ring. What thesethree species of woody-herb Brassicales show is sensitive response in vessel diameterand parenchyma presence to availability of water, but also to temperature. The datafrom comparative anatomy can yield a pattern, but experimental work is much neededto find the physiological explanations for these woods. By determining that, we willlearn more about the role of axial parenchyma.

Interxylary Phloem as an Axial Parenchyma Adjunct

Wood of another species of Brassicales, Salvadora persica (Salvadoraceae) is shown(Fig. 13f). This species, like other Salvadoraceae, consists of shrubs or small trees ofhot, dry areas. As seen in a transverse section of the wood of Salvadora, vessels areembedded in fibers, and would thus be classified as apotracheal. The axial parenchymabands are tangential, and of various sizes. In Salvadora, the parenchyma bands increasein tangential length with the diameter of the stem. In these bands, strands of phloemform occasonally. Strands of Interxylary phloem often seem to function as suppliers ofcarbohydrates during flushes of growth or sudden flowering when water is available(Carlquist, 2013a, b), but the number of species with this peculiar formation is toosmall to furnish a clear correlation: Interxylary phloem and associated parenchyma canbe present in herbs such as Oenothera (Onagraceae) as well as tropical trees such asStrychnos or species of Convolvulaceae.

Living/Septate Fibers as a Dual-Purpose Living Cell Type

Some living fibers do not develop septa, although they remain nucleate for indefiniteperiods of time (Wolkinger, 1970a, b, 1971). Probably the majority of fibers withextended longevity develop septa; a living cell with such a great length to width ratiocan probably function more readily in such respects as starch storage if subdivided intoa series of cells. Input and retrieval of photosynthates can be achieved more readily bymeans of a series of shorter cells, each with its own nucleus and its own pitting, than bymeans of a single long cell. One can say that all fibers are living at first, but most dieupon completing secondary wall formation.

Our knowledge of the systematic distribution of living and septate fibers is still limited(Carlquist, 2015a). This can in part be attributed to the preservation of woods in xylaria.Septate fibers can usually be detected in wood samples have been dried, but there may bemany more instances of non-septate living fibers that have been missed because living butnon-septate fibers cannot be identified in dried wood samples. Presence of septate fibers isoften linked to absence or scarcity of axial parenchyma (Carlquist, 2015a). For example, inRosaceae, axial parenchyma is absent or very scarce in Prunoideae and Spiraeoideae, whichhave septate fibers. In the other subfamilies of Rosaceae, axial parenchyma is present andseptate fibers are not reported (Metcalfe & Chalk, 1950). This is demonstrated inBurseraceae. However, in some genera and species of that family (Trattinckia,Fig. 14a, b), both cell types can be present. The wood of Burseraceae can consist whollyof living cells except for the vessel elements. According to the criteria of Table 1,Burseraceae are subsucculent, which indicates that although the septate fibers serve forwater and starch storage, the investment in secondary wall material is sufficient to serve forsupport in an arborescent growth form.



The same indefinite longevity of fibriform cells can be cited for Nerium oleander ofthe Apocynaceae (Fig. 15c). This fact, along with other features (stomatal crypts inleaves, vestured pits in vessels) that may explain the remarkable drought tolerance ofNerium. The pervasiveness of living cells in the wood of Apocynaceae may explainhow some clades of the family, such as Adenium, have transitioned into succulence.Hedera (Fig. 7f) and other Araliaceae have septate fibers and are notably droughtresistant and fire resistant.

Mechanical Significance of Rays

Burgert & Eckstein (2001) and Ozden & Ennos (2014) show that rays are of consid-erable importance in the tensile and radial stiffness of wood. Ozden & Ennos (2014)indicate that among the woods they studied, Fraxinus has greater resistance to fracture,a fact they attribute to the “homogeneous” (predominance of procumbent ray cells)nature of the rays. The number of species studied in the papers mentioned above is notvery great, and we very much need to examine the ray mechanics of other species,which depart further from norms of density in the woods these authors have studied.

Some other questions are of major significance: why do rays have an ellipticalshape, and why is there a modal distribution of ray height (Metcalfe & Chalk, 1950,Introduction)? Do rays represent weak points in wood if they are vertically moreelongate, as in Foeniculum vulgare (Fig. 14d)? Vining and lianoid species of Piper,Aristolochia, Gnetum, and other genera have extremely tall rays, which can be mea-sured in centimeters rather than microns. Do such rays confer greater flexibility thatpermits vines and lianas to twist in relation to plants that support them? The signifi-cance of very wide rays may have more than one explanation. In Betulaceae andFagaceae, aggregate rays are formed as a result of coalescence of uniseriate rays. Thismay have both physiological and mechanical explanations.

Rayless Woods Can Have Living Cells

Raylessness can occur in the first growth ring of some genera, such as Artemisia. Thishas been called early onset raylessness (Carlquist, 2015b). Rays arrive at some pointlater. This also happens in the insular species of Plantago. Lack of living cells in theearly-formed secondary xylem of these genera is understandable because the value ofrays and axial parenchyma becomes greater with increase in stem diameter, judgingfrom anatomical data.

The presence of axial parenchyma in a rayless wood need not be accompanied withpresence of rays. In Pimpinella dendrotragium (Fig. 14e-f). Only two very small rayswere observed in the wood of my sample of P. dendrotragium (Fig. 14g). However, allvessels in this species are accompanied by axial parenchyma cells, which may even belongitudinally subdivided (Fig. 14f). In Kalanchoe beharensis (Fig. 10e, f) wood isentirely rayless but there are axial parenchyma cells surrounding the vessels. Septateand living fibers are present in the wood of P. dendrotragium and may account forradial transportation of solutes. In a rayless species, axial parenchyma may be moreimportant than rays if it has a physiological value in osmotic maintenance of watercolumns.

S. Carlquist


The significance of rayless woods appears to be a temporary increase in somekinds of mechanical strength at the expense of radial transport capabilities(Carlquist, 2015b), a balance that can be reversed if a stem increases in diameterand ultimately develops rays. Stems that increase in diameter but never form raysmay manage radial transport by means of living fibers. The wood of the species ofHebe (Veronica) that I have examined consists of vessels, living (but non-septate)fibers, and vasicentric tracheids.

Axial Parenchyma Can Have Multiple Functions in a Given Stem at Different Times

An obvious but infrequently mentioned function of axial parenchyma in stems androots is its relationship to protoxylem. Protoxylem vessel elements and tracheids areextensible, and thereby require contact with equally extensible parenchyma cells (Fig.15a, g).

The illustrations to demonstrate this are taken from Araliaceae and its sisterfamily, Apiaceae. In a transverse stem section of Foeniculum vulgare (Fig. 15a)and in a radial section of Oreopanax steinbachianus (Fig. 15g) clear sequencesfrom protoxylem to metaxylem can be seen. As seen in transverse section, theaxial parenchyma cells that surround protoxylem vessels expand to extinguishcanals left by collapse of annular and helical vessels (Fig. 15a). This collapse isnot so evident in Fig. 15g, left. One can question whether one should refer toparenchyma around protoxylem vessels as axial parenchyma, but it does formcylinders that surround the metaxylem vessels (Fig. 15a, top, Fig. 15f, left) andearly secondary xylem vessels (Fig. 15b, center, g, right). A minimum of starchcan be seen in the parenchyma of the protoxylem (Fig. 15g, left) and in themetaxylem (Fig. 15g, center). Just to the right of the metaxylem vessel inFig. 15g is a septate fiber that contains abundant starch. We very much needstudies that capture the deposition and removal of starch from these various sites,because differential activity is very likely to be found. SEM is a promising methodto explore this.

The axial parenchyma that surrounds metaxylem and early secondary xylem(Fig. 15g, center and right; Fig. 16f) is not involved in elongation, but rather probablyfunctions in osmotic maintenance of the conductive stream. The vessel elements shownin Fig. 16f are all pitted metaxylem vessels, but the near-simple perforation plate(Fig. 16f, right) indicates a transition to secondary xylem. This pattern of axialparenchyma sheathing of vessels continues until the end of the growing season, whichends in serious drought for Foeniculum vulgare. The stem studied lived for two years;the very narrow vessels (and very likely some vasicentric tracheids) can be seen inFig. 15c (arrows). A radial section of the end of the second year’s growth shows aneven more pronounced narrowing of the vessels, which are very numerous, accompa-nied by more parenchyma. Some of the vessels are so narrow that they are imperforate(Fig. 15e), and thus qualify as vascular tracheids. Narrower vessels and vasculartracheids resist embolization to a greater extent than wider vessels (Hargrave et al.1994). At the end of the growth of an annual or short-lived perennial that terminates assoil reaches drought conditions, axial parenchyma seems exceptional in quantity andalso perhaps in function. If so, it could be considered a kind of drought axial paren-chyma, supplying water to seeds as the plant ceases to grow.



Cell Type Diversification Within Rays

Multiseriate rays of Araliaceae contain procumbent cells predominantly (Fig. 16e). Thisis also true in a sister family of Araliaceae, Myodocarpaceae (Fig. 17a). The sections ofOreopanax wood (Fig. 16a–d, f) were made from a young stem with relatively littlesecondary xylem, because these relatively juvenile stems have radially shorter rayparenchyma cells, and thus one can encounter end (tangential) walls more readily thanin older stems (Fig. 16e).

Light microscope examination of tangential walls of ray cells shows that they arepitted, but SEM is desirable to show details of this pitting. In Fig. 16a (left) we see anend wall exposed, with bordered pits on the outer surface. Aview of the inner surface ofan end wall can also be seen (Fig. 16a, right). An end wall of a narrower ray cell(Fig. 16b) shows that large pits are present, with intervening strands of wall material.This is shown to a greater degree in Fig. 16c, right, where pits occupy most of the wall.Such cells can be considered flow cell. This is also suggested by the absence of starchgrains in the two cells designated as flow cells here. The cell to the left in Fig. 16c canbe considered a storage cell, because the pits are small and sparse, and starch is present.There is the possibility that starch grains can be displaced during the sectioning process,so several similar cells should be examined before this conclusion is reached. The tipcell of a ray is also presented (Fig. 16d). At the top, starch grains are seen, but below, aview of the outer surface of a tangential wall of this tip cell is evident. The pits aremoderately dense, but small and bordered. This tip cell is probably functionally astorage cell. All of these pits in Fig. 16a–d are probably bordered—no simple pits wereobserved on tangential walls of Oreopanax in this survey.

The pits on radial walls of the procumbent ray cells ofOreopanax are very small andvery sparse (Fig. 16e). These pits contact either other ray cells or septate fibers.Conduction across these interfaces must be minimal.

The occurrence of tile cells in rays of Malvales, monographed by Chattaway (1933)is an example of diversification of ray cells, because tile cells represent axial subdivi-sions of procumbent cells, and could thus be considered an additional type of ray cell.We do not know the function of tile cells, which are apparently restricted to only somegenera of Malvales. This is an example of how problematic it may be to study thefunction of particular parenchyma cell manifestations in wood.

Juvenilism in Wood: Redirection of Flow Patterns of Photosynthates

In my paper on the occurrence of protracted juvenilism (paedomorphosis; neoteny ofsome authors), I described the patterns seen in rosette trees, rosette shrubs, succulents,and various annuals and perennials (Carlquist, 1962). In these species, there is adescending curve for length of vessel elements, and a corresponding delay of circularpitting in vessels; scalariform and pseudoscalariform pitting, such as is seen in Fig. 16f(top center) continues indefinitely into the secondary xylem. In that paper, I alsomentioned the tendency for upright cells in rays, common at the beginning of second-ary growth in most plants, to be produced indefinitely in the secondary xylem. Suchrays (e.g., Fig. 17f) were integrated into the Kribs (1935) system of ray types (Carlquist,1988, 200–204) as “Paedomorphic Type I,” etc. Raylessness was considered a kind ofultimate expression of juvenilism: the delay of ray production, and the production of

S. Carlquist


upright cells that were so much like libriform fibers that they were indistinguishablefrom them. The anatomical data presented in those sources seem entirely accurate, butno physiological explanations for these conditions were attempted at that time. Giventhe concept that flow in elongate cells occurs in the direction of cell elongation and thedesignation of radially elongate ray cells as flow cells in the present paper, aninterpretation of juvenilism in rays that hypothesizes patterns of flow vertically ratherthan horizontally seems justifiable. One must be careful in reporting cell shape of raysbecause particular rays may not be sectioned through their central portions (sagittally),and thus fewer procumbent ray cells may appear to be present.

In the woody families of Apiales, Myodocarpaceae (Fig. 17a) and Araliaceae, raycells in multiseriate rays are predominantly procumbent. This may related to theproduction of rather large leaves in these families, as well as other factors, such asgrowth in flushes. These two families are somewhat unusual in this respect, because thebulk of the families of woody angiosperms have multiseriate rays that are typicallyheterogeneous or heterocellular: composed of cells upright, square, and procumbent inradial sections. With woody Apiales as a basal type in the order, juvenilism in rayswould be expected to be characterized by fewer procumbent cells as well as the squareand upright cells characteristic of paedomorphic rays in angiosperms generally.Apiaceae can be considered a predominantly herbaceous derivative of Araliaceae inwhich instances of secondary woodiness, which would involve paedomorphosis(Carlquist, 2009), occur. If we examine wood of Apiaceae (Fig. 17b–e) we find thatthis is true. Both Heteromorpha trifoliata (Fig. 17b) and Eryngium inaccessum(Fig. 17c) have wood in which a few procumbent cells are present, but most ray cellsare square or upright. Heteromorpha trifoliata is an African small tree from highlandelevations, where the climate is close to temperate throughout the year. Eryngiuminaccessum is a shrubby species, on the moist and temperate Juan Fernandez Islands,of a genus that is otherwise mostly rosette-forming. Arracacia atropurpurea (Fig. 17d–e) is a somewhat woody species in a genus that contains carrot-like herbaceous species.It grows on temperate Mexican uplands. In A. atropurpurea, wood begins with rayscomposed wholly of upright cells (Fig. 17d). Over time, as the plant becomes woodier,some procumbent cells are produced (Fig. 17e). All three of these species grow inconditions that do not change much throughout the year. In these climates, secondarywoodiness would be likely to occur. Secondary woodiness is an economical form ofincreasing plant mass if conduction can be sustained throughout the year. Axialparenchyma may provide vertical flow of photosynthates to sustain growth. In annualsand short-lived perennials, upright axial parenchyma cells may convey photosynthatesfor flowering and fruiting. Uniseriate rays and uniseriate wings of multiseriate rays mayoffer links for vertical conduction of photosynthates from rays into axial parenchyma.

Juvenilistic rays can be found in a series of angiosperms that are not rosette trees orshrubs, nor are they annuals or perennials or succulents, which typically havejuvenilistic wood. Chloranthaceae is a family with many “primitive” characters thathas protracted wood juvenilism. Rays in this family are mostly composed of uprightcells, as in Hedyosmum (Fig. 17f). Hedyosmum species can be trees, but not large ones,and the overall habit in the genus is shrubby. Chloranthus has even more pronouncedray cells (Fig. 17g), which are composed entirely of upright ray cells. Chloranthusconsists of subshrubs branched from the base. The habit of protracted production ofupright cells may be found in some Eupomatiaceae, Winteraceae, Aristolochiaceae,



Piperaceae and Austrobaileyaceae. Individuals of some species in these families devel-op from shrubs into trees, at which juncture procumbent cells become more abundant.

The occurrence of radially-elongate (procumbent) cells in rays is certainly related toarborescence. The bigger the diameter of a stem, the greater the value of radial flow ofphotosynthates into and out of the stem. We should not be surprised that as Barghoorn(1941) showed, rays become wider and contain more procumbent cells in wider stems.The fact that rays also subdivide suggests that mechanical optima are being served. Thepoles of herbaceousness and woodiness were not appreciated by earlier wood anato-mists, who wanted to study “mature” wood patterns of species that were oftencommercially valuable timbers. The idea that ontogenetic changes in ray, axial paren-chyma, and tracheary elements (fibriform cells, including tracheids; vessel elements)can be shifted toward herbaceous modes or woodier modes (Carlquist, 1962, 2009;Carlquist, 2013a, b) places us in a new perspective. Features of protracted juvenilismon the one hand, or accelerated adulthood on the other, can be selected to achievetranslocation of photosynthates and other substances vertically or horizontally. Like-wise, the mechanical properties of earlier-formed secondary xylem can be quitedifferent from wood of an older stem. Axial parenchyma and ray parenchyma areimportant elements in these ontogenetic changes. The success of angiosperms in nosmall measure derives from the fact that degrees and kinds of shifts from juvenile toadult patterns of wood structure can be increased or decreased, a flexibility not possiblein conifers, Gnetales, cycads, or Ginkgo.

Conclusions

The following conclusions can be derived from the studies reported above, combinedwith findings in literature cited in this paper. Some of the statements representhypotheses that seem supported by wood anatomy, but additional evidence is neededon a number of points.

1. Anatomical features of living wood cells should be regarded as indictors ofprobable function. We have so many ways of determining activities of these cellsthat retreat to a purely descriptive approach, guided by what is in glossaries,should be regarded as outmoded methodology. When we view the variability inanatomical expressions in these cells within a plant and among species, we shouldbe prepared to see that they represent optimal structural modes, not relictualdetails that have failed to change.

2. Gnetales are a vessel-bearing group that we now know are part of the conifer cladeand not a derivative or ancestor of angiosperms. Because Gnetales have acquiredvessels independently of angiosperms, they show us the anatomical and physio-logical consequences of vessel presence. These include the function of multiseriaterays and axial parenchyma (living fiber-tracheids in the case of Ephedra) toconduct photosynthates into the wood where they can participate in functions ofstorage and relate to the conductive process. Multiseriate rays can function inproviding flexibility of stems (hence the numerous lianoid species of Gnetum;some species of Ephedra are also lianoid). Gnetales have essentially all of thexylary features of woody angiosperms, and therefore represent a kind of

S. Carlquist


experimental verification of how equivalent angiosperm structures function. An-giosperms have exceeded Gnetales in evolutionary diversification mostly becausethe long gymnospermous life cycle of Gnetales makes for slow reproduction andslow territorial expansion of species. Gnetales have conducting systems that seemquite equivalent to those of angiosperms in functional characteristics.

3. Rays and axial parenchyma in angiosperms form a continuous network; axialparenchyma cells cannot exist isolated from other living cells. Rays are theprimary point of entry for carbohydrates into the secondary xylem, and throughcontacts with axial parenchyma provide entry of photosynthates and ions to axialparenchyma strands.

4. Although most conifers have axial parenchyma strands, some (certain species ofAgathis and Araucaria; some species of Picea and Tsuga) do not. This is anindication of a subsidiary role for axial parenchyma in conifers compared toangiosperms (and Gnetales). Axial parenchyma in conifers is part of a syndromeof differences in hydraulic systems between conifers and angiosperms. Tracheidsin conifers are sufficiently long that all tracheids contact one or more rays. Rays inconifers are almost never more than one cell layer wide, and diversification infunction is thereby limited (except for presence of ray tracheids, primarily inPinus). Presence of prominent tracheid-to-ray pitting is indicative of a role forrays in conduction in tracheids.

5. The tracheids of conifers are narrow enough so that water columns are easilyrestored when water frozen in them thaws. Wood of tropical conifers in localitieswhere water in tracheids is not likely to freeze can exceed that limitation indiameter. The diameter of circular bordered pits in conifer tracheids (which is lessthan tracheid diameter), restricts the amount of the water-conducting margoporosities. The conductive capability of the pit aperture, and the ability of pitsto aspirate form a syndrome of safety for conifers that represents a patterndifferent from that of ray plus axial parenchyma in angiosperms. With functionsof axial parenchyma and rays in conifers limited (or adequately served by fewercells), volume occupancy by greater volume of tracheids and smaller volume ofliving cells becomes a conifer wood strategy.

6. Axial parenchyma in angiosperm woods serves for maintenance (by osmoticfunctioning) to deter and repair embolisms. Ray parenchyma introduces photo-synthates to the parenchyma network and thereby makes this possible. Thefunction of parenchyma in maintaining flow in vessels and tracheids of angio-sperm woods provides a pre-existing system that can take on other functions:water storage, photosynthate storage, defense against predation, zones of flexi-bility, etc.

7. Axial parenchyma and (indirectly) rays, vessel grouping, narrowing of vessels,and presence of tracheids and other mechanisms provide conductive safety inangiosperms and supersede scalariform perforation plates. Scalariform perforationplates offer devices for potentially confining air bubbles, but have the disadvan-tage of providing a high degree of resistance to flow. This resistance is tolerable inplants with low and steady rates for flow. Such plants are either in mesic habitats,such as cloud forests, or have microphyllous foliage (Bruniaceae) to minimizetranspiration. Reduction in number and thickness of the bars in perforation platescan be seen in some families (Hamamelidaceae, Monimiaceae) as ways of



reducing flow resistance, but these midpoints on the way to simple perforationplates are relatively few.

8. Axial parenchyma is sparse and often diffuse in “primitive” angiosperm woods,as it is in many conifers. With the development of vessels, axial (and indirectly,ray) parenchyma become sources of osmotic support of the water columns ofvessels. Accordingly, volume devoted to axial and ray parenchyma increasesmarkedly in vessel-bearing angiosperms, and this increased volume parallelsdegrees and kinds of increase in vessel presence, vessel diameter, and vessel areaas seen in transverse sections. Similar trends may be cited for the increase in axialand ray parenchyma in Gnetales as compared to conifers.

9. In angiosperms, conversion of axial and ray parenchyma to sites for deposition ofsecondary compounds for deterrents of phytophagous insects and fungi is generallyslower and more partial than it is in conifers. Angiosperm rays (and to a lesser extentaxial parenchyma) show marked division of labor into flow cells, storage cells, and“defense” cells. Amorphous deposits of tannins, resin-like compounds, and latex, aswell as crystalline (usually calcium oxalate crystals of various sizes and forms) andnon-crystalline dissolved compounds serve for defense purposes. Over time, someof these substances may extend into storage and flow cells (as well as vessels andtracheids) in portions of secondary xylem that are no longer active.

10. Elongate shape of ray and axial parenchyma cells is indicative of direction of flowthrough those cells. End walls (tangential walls of ray cells, horizontal walls ofaxial parenchyma strands) show pits that are wider, more densely placed, morenumerous, and are frequently bordered. Presence of borders allows for more flowthrough wider pit membranes plus minimal interruption of the secondary wall.Denser, larger, and more numerous pits also increase flow possibilities. Pitting onlateral walls of elongate cells and on storage cells, which are more nearlyisodiametric, is sparser and consists of smaller pits. The secondary walls of rayand axial parenchyma cells are sometimes described as “nodular” or “nodulated,”but this is a misnomer for the borders of pits or the thickness of secondary wallsbetween pits on ray or axial parenchyma walls.

11. Walls of phloem ray parenchyma and axial phloem parenchyma cells are usuallythin, and often lack secondary walls. Such walls can be considered equivalent touse of the entire cell wall as a pit membrane, and thus valuable for flow ofphotosynthates. Although the pathways of sugars from phloem into secondaryxylem have not been studied sufficiently, the phloem and xylem rays represent, bydefault, the most obvious and potentially most efficient route for this flow.

12. Vessel-to-ray and vessel-to-axial parenchyma pit areas are often prominent in areaand density. This is also true of the contact points between rays and tracheids inconifers, producing the various patterns collectively known as “cross-field” pitting.The large areas of pit membranes in these contact points in gymnosperms andangiosperms, respectively, suggest a correlation with release of sugars and ions intothe conductive stream.Although the relative paucity or absence of axial parenchymain conifers may suggest a smaller role in conifers for such osmotic action, the greatlength of tracheids in most conifers has the effect of putting all tracheids in contactwith at least one ray. In angiosperms, a similar statement could be mode, not onlywith regard to vessel-ray contacts and vessel-axial parenchyma contacts, but alsoaxial parenchyma-ray parenchyma contacts (the “contact cells” of some authors).

S. Carlquist


13. Photosynthate storage (mostly as starch) and water storage in ray and axialparenchyma of angiosperms permit development of growth forms not possiblein conifers: succulents, lianas, rosette trees, trees that grow by means of flushing,drought-deciduous trees, tank trees, and many others. This diversity of growthforms in angiosperms can be considered as made possible by the devotion ofmore volume to water and starch storage cells. Thus, the introduction of paren-chyma volume (perhaps primarily as a means of osmotic regulation of flow invessels) in earlier angiosperms has formed the basis for this radiation.

14. The strategies of water storage within secondary xylem are not uniform. Storagein rays may be more prominent in some angiosperms, storage in axial parenchy-ma more prominent in others. In some plants, the entirely of the secondary xylemother than vessels is devoted to water storage and/or starch storage. Bark may bethe primary source of water and/or starch storage in some species. Turgor canhave mechanical aspects as well as being related to water storage.

15. Water storage cells in axial parenchyma and rays tend to be larger, more sparselypitted, capable of expansion and contraction, and without visible contents ascompared to parenchyma cells that serve for photosynthate storage or otherpurposes (accumulation of defensive substances). Liquid-preserved wood sam-ples are required to establish clearly the function of living cells. Function of woodcells can be inferred from study of dried wood samples, but not determined withcertainty. The volume of starch in axial parenchyma cells and ray cells isconsiderable, and should be figured, wherever possible, in wood studies (espe-cially those designed for students). Although we have no good comparative data,workers familiar with study of liquid-preserved wood samples occasionallyremark that the totality of starch storage is perhaps never mobilized, and thus a“standby” supply is present.

16. Living fibers (which may be septate or non-septate) are part of the system ofliving cells in certain woods, and can serve for storage (usually starch). Livingfibers, where abundant, may be accompanied by reduction in abundance orpresence of axial parenchyma, although exceptions exist. Living fibers representa compromise between mechanical strength (by virtue of greater wall thicknessand fiber length) and photosynthate storage capabilities (wider lumen diameter).

17. Rays have mechanical strength properties that can be analyzed in terms of variousforces (stiffness, torsion, etc.), and these factors are definitely part of ray design inany given species. Only a small number of woody species have been studied inthis regard, and many more studies are needed to develop a picture. As seen intangential section, rays have an ellipsoidal shape and are more commonly finite inheight (less than about 500 μm in vertical length). Rays vertically longer than thismay be associated with greater stem flexibility or other properties, and are thusvaluable for vines, lianas, and some kinds of herbs and subshrubs. Ellipsoidalshape of rays would tend to interrupt the strength pattern conferred by fibers lessthan rays of indefinite length; the diagonal structural members interconnectinglinear bridge parts is a parallel.

18. Ray cells in conifers, as a generalization, have thinner walls than those ofangiosperms. The uniseriate nature of rays in conifer woods suggests that asmaller volume devoted to parenchyma is correlated with a greater volumedevoted to tracheids, and that storage of either water or photosynthates in rays



of conifers is much less that in angiosperms. The radially elongate nature ofconifer ray cells also gives them the aspect of “flow” cells rather than “storage”cells. Rays in conifers also interrupt the mechanical strength pattern of coniferwoods minimally. In angiosperms, rays are wider, taller, and greater in totalvolume. The gain in volume for photosynthate and water storage has the potentialof lessening the tensile and torsion aspects of mechanical strength, but this can becountered by greater thickness of secondary walls in ray cells and greaterthickness of fibriform wood cells (libriform fibers, fiber-tracheids). The greaterwidth of rays in angiosperms as compared to those of conifers offers potentialadvantages for growth forms that experience more torsion, such as lianas.

19. Many angiosperm woods have limited numbers of axial parenchyma cells asso-ciated with vessels or vessel groupings (vasicentric or paratracheal scanty areterms applied). This suggests that the function of osmotic control of conduction inthe vessels is accomplished with a limited number of cells. Larger aggregations ofaxial parenchyma may therefore be involved in part in some other function aswell. Multiplicity of functions is sometimes indicated by differing cell morphol-ogy (e.g., the two types of axial parenchyma in Ficus; crystal strands in axialparenchyma of Fabaceae) but is usually not apparent.

20. Angiosperm axial parenchyma in transverse section is often labeled as eitherapotracheal (no consistent association pattern of vessels with axial parenchyma)or paratracheal (vessels always associated with parenchyma in variously shaped orpositioned aggregations). If we view these two types in three dimensions, we findboth that vessels shift in position along their vertical course, and all vessels contactaxial parenchyma (and rays) somewhere along their length. No clear correlationsof apotracheal and paratracheal arrangements have been demonstrated. The causesfor divergent modes of axial parenchyma distribution should be investigated.

21. Axial parenchyma and rays may shift in abundance and wall characteristics, asfunctions in a stem change. For example, axial parenchyma and rays are minimalin quantity and thick-walled early in secondary growth in Ipomoea (and othervines and lianas), but abundant and thin-walled in later-formed wood, as there is ashift from upward progress to flexibility in stems. Other examples include shiftsfrom fibrous (stiffness) to parenchymatous (water storage).

22. Some investigators have pointed to correlations between particular characterstates in wood. For example, diffuse axial parenchyma is often claimed to beassociated with heterocellular rays, presence of tracheids as the imperforatetracheary type, and vessels with scalariform perforations plates. The exceptionsto this correlation and other correlations are numerous. We may attribute that tohomoplasies, or to the idea that optimal wood patterning may be diverse becausecell types are not uniform (e.g., rays are polymorphic in cell types and in theproportion of the various types; in dimensions; and in numbers per horizontalmm). Attempts have been made by some workers to refer particular wood types to“stages” of organization. Rather than begin with an attempt to refer a given woodto particular types or correlations, analyzing woods on an individual basis withrelation to growth form, ecology, and other factors is likely to be more productiveto our understanding of how woods function and evolve.

23. Upright cells (as seen in radial sections) in rays are more likely to serve for verticaltransportation of solutes, whereas procumbent cells architecturally seem ideal for

S. Carlquist


horizontal photosynthate flow. Upright cells, especially where abundant, are likelyto intersect with axial parenchyma more often, and thereby form links betweenhorizontal flow and vertical flow. Square cells have been claimed to be “morpho-logically equivalent to upright cells,” but they are better regarded as cells that servefunctions related to isodiametric shape (e.g., storage or interconnection betweenaxial and radial cells) better. Density and number of pits are probably excellentclues to function in ray cells. These features can best be studied with SEM.

24. Protracted juvenilism (heterochrony, paedomorphosis, or neoteny of various au-thors) is a feature of angiosperm woods almost exclusively. Where ray parenchymais concerned, juvenilismmeans the production of upright cells exclusively or mostlyso, sometimes for the entire life of the plant. This has the effect of directingphotosynthate flow vertically. Vertical flow of water containing sugars in parenchy-ma of woods is easily understood in rosette trees and rosette shrubs, in whichdiameters of stems do not increase very much over time. Most trees have markedincrease in stem (and root) diameter, and therefore feature radial flow, to supplyphotosynthates to storage sites and to the axial parenchyma. Radial flow is achievedmostly in procumbent cells, which become more numerous as a tree increases indiameter. Vertical flow in upright ray cells would correlate with flow of photosyn-thates in the wood to flowers and fruits that terminate shoots in annuals andperennials (“woody herbs”). Vertically longer rays are often a manifestation ofjuvenilism, because in woody species they are not subdivided ontogenetically overtime. Protracted juvenilism has other manifestations in vessel-element length, vesselpitting, and mechanical cell length. By being an “ontogenetic intervention” (asopposed to accelerated adulthood, seen uniformly in conifer woods), the ability toprotract juvenilism is a rich source of architectural repatterning present in angio-sperm woods. Protracted juvenilism does not occur merely in the wood of a fewwoody herbs on islands; it occurs in annuals and perennials throughout the world.

25. Raylessness can be considered a penultimate form of juvenilism, in which uprightray cells are produced exclusively and simulate fibers so closely that they areindistinguishable. Some rayless woods develop rays eventually, demonstratingthat the adult condition of having rays has been delayed. Raylessness in this casemay be considered an initial emphasis on mechanical strength of fibriform cellsover parenchyma cells designed for radial flow, followed by a balance between thetwo. Rayless woods are not all alike; some may have living fibriform cells, somehave axial parenchyma but no rays. The ultimate form of juvenilism is representedby loss of the vascular cambium, which has occurred in monocots. Monocot stemscounteract the loss of a vascular cambium by producing vascular tissue in a widercylinder of scattered bundles embedded within a parenchymatous (or sclerenchy-matous) background. Some shrubby, rosette-forming (Agave), or arborescentmonocots (Dracaena) have restored the value of secondary growth via a monocotcambium which produces bundles and associated parenchyma inwardly.

26. Plants with successive cambia, such as Beta, the beet, produce rings of vasculartissue, each with secondary phloem, a cambium, and secondary xylem, separatedfrom each other by conjunctive tissue. In the majority of woods with successivecambia, conjunctive tissue is composed of parenchyma cells. Conjunctive tissueis quite different from axial parenchyma: most plants with successive cambiahave axial parenchyma in the secondary xylem, just as plants with a single



cambium do. The function of conjunctive tissue may be in storing sugars (Beta)or starch; in sequestering salts; in achieving flexibility (lianas); or in providingliving phloem and xylem alternating with tissue devoted to storage, therebyshortening input and retrieval pathways.

27. The size, location, density, location, number and morphology (e.g., presence ofborders) of pits on parenchyma cells in woods are strongly correlated withfunction. These features can be seen in sectional view. However, they areprobably best displayed when we look at the outer surfaces of parenchyma cells.Preparations made by hand sectioning with single-edge razor blades and exam-ined with SEM are particularly valuable, because cells are often separated ratherthan sliced open, so cell contexts, cell shapes and details of pitting are revealed.We lose information when we limit ourselves to a single method of preparation.Wood is a three-dimensional structure, and if sections are convenient ways ofobtaining information (because they present easily-grasped two-dimensional im-ages of wood), we must conceptually reconstitute the three-dimensionality ofwoods if we are to understand them thoroughly.

28. Ray parenchyma and axial parenchyma configurations, like other features inwood, should be regarded not as historical markers of levels of “specialization”achieved by lineages fortunate enough to escape “primitive” or “unstable” con-ditions. Rather, character states in woods living today are likely to be optimal inparticular localities in particular growth forms. Some of these optimal construc-tion plans in wood may contain more “primitive” features than others, but bybeing alive today, they are all still functional. The fact that early angiospermsprobably had wood with multiseriate rays and some degree of axial parenchymameans that diversification in these tissues could be utilized as a source fordevelopment of growth forms and adaptations that have not be achieved byconifers and other vascular plants. Individual species quite frequently divergefrom generalities derived from quantification of large numbers of species. Theseapparent deviations from mathematical norms, averages, or modes may tell usmore about adaptation than the data points that adhere more closely tomathematically-obtained curves for groups of species.

Literature Cited

Bailey, I. W. 1944. The development of vessels in angiosperms in morphological research. American Journalof Botany 32: 421–428.

Barghoorn E. S. 1941. The ontogenetic development and phylogenetic specialization of rays in the xylem ofdicotyledons. 2. Modification of the multiseriate and uniseriate rays. American Journal of Botany 28:273–282.

Biancardi, E., L. W. Panella, & R. T. Lewellen. 2012. Beta maritima. The origin of beets. Springer Verlag,Heidelberg.

Bowe, L. M., G. Coat & C.W. dePamphilis. 2000. Phylogeny of seed plants based on all three genomiccompartments: extant gymnosperms are monophyletic and Gnetales’ closest relatives are conifers.Proceedings of the National Academy of Sciences USA 97: 4092–4097.

Braun, H. J. 1970. Funktionelle Histologie der sekundären Sprossachse. I. Das Holz. Encyclopedia of PlantAnatomy IC, part 1. Borntraeger, Berlin.

S. Carlquist


Braun, H. J. 1984. The significance of the accessory tissues of the hydrosystem for osmotic water shifting asthe second principle of water ascent, with some thoughts concerning the evolution of trees. IAWA Bull.n.s. 5: 275–294.

Brodersen, C. R., Knipfer, T. & A. J. McElrone. 2017. In vivo visualization of the final stages of xylemrefilling in grapevine (Vitis vinifera) stems. New Phytologist 217: 117–126.

Burgert, I. & D. Eckstein. 2001. The tensile strength of isolated wood rays of beech (Fagus sylvatica L.) andits significance for the biomechanics of living trees. Trees 15: 168–170.

Burgert, I., A. Bernasconi & D. Eckstein. 1999. Evidence for the strength function of rays in living trees.Holz als Roh- und Werkstoff 57: 397–399.

Burleigh, J. G. & Mathews. 2004. Phylogenetic signal in nucleotide data from seed plants: implications forresolving the seed plant tree of life. American Journal of Botany 91: 1599–1613.

Carlquist, S. 1962. A theory of paedomorphosis in dicotyledonous woods. Phytomorphology 12: 30–45.Carlquist, S. 1970. Wood anatomy of Hawaiian, Macaronesian, and other species of Euphorbia. Botanical

Journal of the Linnean Society 63 (Supplement 1): 181–193.Carlquist, S. 1975. Ecological strategies of xylem evolution. University of California Press, Berkeley.Carlquist, S. 1983. Observations on the vegetative anatomy of Crepidiastrum and Dendrocacalia. Aliso 10:

383–395.Carlquist, S. 1988. Comparative wood anatomy. Springer Verlag, Heidelberg.Carlquist, S., & D. A. Gowans. 1995. Secondary growth and wood histology of Welwitschia. Botanical

Journal of the Linnean Society 118: 107–121.Carlquist, S. 1998. Wood and bark anatomy of Caricaceae: correlations with systematics and habit. IAWA

Journal 19: 191–206.Carlquist, S. 2007a. Bordered pits in ray cells and axial parenchyma: the histology of conduction, storage,

and strength in living wood cells. Botanical Journal of the Linnean Society 153: 157–168,Carlquist, S. 2007b. Successive cambia revisited: ontogeny, histology, diversity, and functional significance.

Journal of the Torrey Botanical Society 134: 301–332.Carlquist, S. 2009. Xylem heterochrony: an unappreciated key to angiosperm origins and diversification.

Botanical Journal of the Linnean Society 161: 26–65.Carlquist, S. 2012a. How wood evolves: a new synthesis. Botany 90: 901–940.Carlquist, S. 2012b. Wood adaptation of Gnetales in a functional, ecological, and evolutionary context. Aliso

30: 33–47.Carlquist, S. 2013a. Interxylary phloem: diversity and functions. Brittonia 65: 477–495.Carlquist, S. 2013b. More woodiness/less woodiness: evolutionary avenues, ontogenetic mechanisms.

International Journal of Plant Sciences 174: 964–991.Carlquist, S. 2014. Fibre dimorphism: cell type diversification as an evolutionary strategy in angiosperm

woods. Botanical Journal of the Linnean Society 174: 44–67.Carlquist, S. 2015a. Living cells in wood. 1. Absence, scarcity and histology of axial parenchyma as keys to

function. Botanical Journal of the Linnean Society 177: 291–321.Carlquist, S. 2015b. Living cells in wood. 2. Raylessness: histology and evolutionary significance. Botanical

Journal of the Linnean Society. 178: 529–555.Carlquist, S. 2017. Conifer tracheids resolve conflicting structural requirements: data, hypotheses, questions.

Journal of the Botanical Research Institute of Texas 11: 123–141.Chapotin, S. M, J. H. Razanameharizaka & N. M. Holbrook. 2006. Water relations of baobab trees

(Adansonia spp. L.) during the rainy season: does stem water buffer daily water deficits? Plant Cell andenvironment 29: 1021–1032.

Chattaway, M. M. 1933. Tile cells in the rays of Malvales. New Phytologist 32: 261–273.Davis, S. D., J. S. Sperry, and U. G. Hacke. 1999. The relationship between xylem conduit diameter and

cavitation caused by freezing. American Journal of Botany 86: 1367–1372.Evans, J. A., P. E. Gasson & Gwilym P. Lewis. 2006. Wood anatomy of the Mimosoideae (Leguminosae),

IAWA Journal, Supplement 5: 1–117.Fisher, J. B. 1980. The vegetative and reproductive structure of papaya (Carica papaya) Lyonia 1: 191–208.Gibson, A. C. 1970. Comparative anatomy of secondary xylem in Cactoideae (Cactaceae). Biotropica 5: 29–

65.Greguss, P. 1955. Identification of living gymnosperms on the basis of xylotomy. Akademiai Kiado,

Budapest.Greguss, P. 1959. Holzanatomie der Europaïschen Laubhölzer und Sträuchern. Akademiae Kiado, Budapest.Greguss, P. 1968. Xylotomy of the living cycads. Akademiai Kiado, Budapest.



Hacke, U., B. G. Lachenbruch, J. Pitterman, S. Mayr, J.-C. Domec & P. Schulte. 2015. The hydraulicarchitecture of conifers. In, U. G. Hacke, ed. Functional and ecological xylem anatomy, 39–75. SpringerVerlag, Heidelberg.

Hargrave, K. R., Kolb, K. J., Ewers, F. J. & S. D. Davis. 1994. Conduit diameter and drought-inducedembolism in Salvia mellifera Greene (Labiatae). New Phytologist 126: 695–705.

Heady, R. D., J. G. Banks & P. D. Evans. 2002. Wood anatomy of Wollemi pine (Wollemia nobilisAraucariaceae). IAWA Journal 23: 339–357.

Hoadley 1990. Identifying woods: accurate results with simple tools. Taunton Press, USA.Holbrook, N. M., & M. A. Zwieniecki. 1999. Embolism repair and xylen tension: do we need a miracle?

Plant Physiology 120: 7–10.Holbrook, N. M., Zwieniecki, M. A., & P. J. Melcher. 2002. The dynamics of dead wood: maintenance of

water transport through plant stems. Integrative and Comparative Biology 42: 492–496.Holden, R. 1913. Ray tracheids in the Coniferales. Botanical Gazette 55: 56–65.Höll, W. 1975. Radial transport in rays. In Zimmermann, M. H. & J. A. Milburn (eds.), Transport in plants. I.

Phloem transport, 432–450. Springer Verlag, Heidelberg.Johnson, D. M., K. A. McCulloh, D. R. Woodruff & F. C. Meinzer. 2012. Hydraulic safety margins and

embolism reversal in stems and leaves: why are conifers and angiosperms so different? Plant Science 195:48–53.

Kedrov, G. B. 2012. Functioning wood (compiled from various articles of G. B. Kedrov by A. C. Timonin).Wulfenia 19: 57–95.

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

Kribs. 1937. Salient lines of structural specialization in the wood parenchyma of dicotyledons. Bulletin of theTorrey Botanical Club 65: 177–186.

Lens, F., A. Texier, H. Cochard, J. S. Sperry, S. Jansen & S. Herbette. 2013. Embolism resistance as a keymechanism to understand adaptive plant strategies. Current Opinion in Plant Biology 16: 287–292.

Metcalfe, C. R. 1987. Anatomy of the dicotyledons, ed. 2, vol. 3. Magnoliales, Illiciales, and Laurales. TheClarendon Press, Oxford.

Metcalfe, C. R. & L. Chalk. 1950. Anatomy of the dicotyledons. The Clarendon Press, Oxford.Metcalfe, C. R. & L. Chalk. 1983. Anatomy of dicotyledons, ed. 2, vol. 2. Wood structure and conclusion of

the general introduction. Clarendon Press, Oxford.Meylan, B. A. & B. G. Butterfield. 1978. The structure of New Zealand woods. DSIR Bulletin 122. DSIR,

Wellington.Moll, J. W. & H. H. Janssonius. 1909-1936. Mikrographie des Holzes der auf Java vorkommenden

Baumarten. 6 vols. Brill, Leiden.Morris, H. & S. Jansen. 2016. Secondary xylem parenchyma—from classical terminology to functional

traits. IAWA Journal 37: 1–15.Morris, H., L. Plavcova, P. Cvecko, E. Fichtler, M. A. F. Gillingham, H. I. Martinez-Cabrera, D. J.

McGlinn, E. Wheeler, J. Zheng, K. Sieminska, & S. Jansen. 2015. A global analysis of parenchymatissue fractions in secondary xylem of seed plants. New Phytologist 209: 1553–1565.

Morris, H., M. A. F. Gillingham, L. Plavcova, S. M. Gleason, M. E. Olson, D. A. Coomes, E. Fichtler, M.M. Klepsch, H. I. Martinez-Cabrera, D. J. Glinn, E. A. Wheeler, J. Zheng, K. Zieminska & S.Jansen. 2017. Vessel diameter is related to amount and spatial arrangement of axial parenchyma inwoody angiosperms. Plant Cell and Environment 1–16.

Nardini, A, M. A. Lo Gullo & S. Salleo. 2011. Refilling embolized xylem conduits: is it a matter of phloemunloading? Plant Science 180: 804–811.

Ozden, S. & A. R. Ennos. 2014. Understanding the function of rays and wood density on transverse fracturebehavior of green wood of three species. Journal of Agricultural Science and Technology B4: 731–743.

Panshin, A. & C. De Zeeuw. 1964. Textbook of wood technology. Vol. I. Structure, identification, uses, andproperties of the commercial woods of the United States. McGraw Hill, New York.

Pfeiffer, H. 1926. Das abnorme Dickenwachstum. Handbuch der Pflanzenanatomie Vol. 9(2). GebrüderBorntraeger, Berlin.

Pittermann, J. and J. Sperry. 2003. Tracheid diameter is the key trait determining the extent of freezing-induced embolism in conifers. Tree Physiology 23: 907–914.

Roman-Jordan, E., L. G. Esteban, P. de Palacios & F. G. Fernandez. 2016. Wood anatomy of Cupressusand its relation to geographical distribution. IAWA Journal 37: 48–68.

Salleo, S., M. A. Lo Gullo, P. Trifilo & A. Nardini. 2004. New evidence for a role of wood-associated cellsand phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant, Cell andEnvironment 27: 341–376.

S. Carlquist


Salleo, S., P. Trifilo, S. Esposito, A Nardini & M. A. Lo Gullo. 2009. Starch to sugar conversion in woodparenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolismrepair? Functional Plant Biology 36: 815–825.

Sauter, J. J. 1966a. Untersuchungen zur Physiologie der Pappelholzstrahlen. I. Jahresperiodischer Verlauf derStärkespeicherung in Holzstrahlparenchym. Zeitschrift für Pflanzenphysiologie 55: 246–258.

Sauter, J. J. 1966b. Untersuchungen zur Physiologie der Pappelholzstrahlen. II. JahresperiodischeAnderungen der Phosphatase Aktivität im Holzparechym und ihre mögliche Bedeutung für denKohlhydratstoffwechsel und den aktiven Assimilattransport. Zeitschrift für Pflanzenphysiologie 55:349–382.

Sauter, J. J., W. I. Iten & M. H. Zimmermann. 1973. Studies on the release of sugar into the vessels of thesugar maple (Acer saccharum). Canadian Journal of Botany 51: 1–8.

Scholz, F. C., S. J. Bucci, G. Goldstein, F. C. Meinzer, A. C. Franco & F. R. Miralles-Wilhelm. 2008.Temporal dynamics of stem expansion and contraction o Scialdone, A. & M. Howard. 2015. How plantsmanage food reserves at night: quantitative models and open questions. Frontiers in Plant Science 6: 1–6.

Scialdone, A., &M. Howard. 2015. How plants manage food reserves at night: quantitative models and openquestions. Frontiers in Plant Science 6: 204–213.

Secchi, F., C. Pagliarani & M. A. Zwieniecki. 2016. The functional role of xylem parenchyma cells andaquaporins during recovery from severe water stress. Plant Cell and Environment 40: 858–871.

Shigo, A. L. 1984. Compartmentalisation: a conceptual framework for understanding how trees grow anddefend themselves. Annual Review of Phytopathology 22: 189–214.

Trifilo P., P. M. Barbera, F. Raimondo, A. Nardini & M. A. Lo Gullo. 2014. Coping with drought-inducedxylem cavitation: coordination of embolism repair and ionic effects in three Mediterranean evergreens.Tree Physiology 34: 109–122.

USDA. 1974. Wood Handbook. Government Printing Office, Washington, D. C.Wellwood, R. W. 1962. Tensile testing of small wood samples. Pulp and Paper Magazine of Canada 63(2):

T61-t67.Wolkinger, F. 1970a. Morphologie und systematische Verbreitung lebender Holzfasern bei Sträuchern und

Bäumen. II. Zur Histologie. Holzforschung 24: 141–151.Wolkinger, F. 1970b. Das Vorkommen lebender Holzfasern in Sträuchern und Bäumen Phyton (Austria) 14:

55–67.Wolkinger. 1971. Morphologie und systematische Verbreitung lebender Holzfasern bei Sträuchern und

Bäumen. III. Systematische Verbreitung. Holzforschung 25: 29–30.Zimmermann. M. H. 1971. Dicotyledonous wood structure made apparent by sequential sections: Film E

1975 (film data and summary available as a reprint). Institut Wissenschaftliche Film, Göttingen, Germany.



cells is highly unlikely because it would then be a kind of parasitic cell, gaining water and...

Documents