Journal of the Torrey Botanical Society 134(2). 2007. pp. 301-332

Successive cambia revisited: ontogeny, histology, diversity, and functional significance

Sherwin Carlquist1 Santa Barbara Botanic Garden. 1212 Mission Canyon Road, Santa Barbara. CA 93105

CARLQUIST. S. (Santa Barbara Botanic Garden. 1212 Mission Canyon Road. Santa Barbara, CA 93105). Successive cambia revisited: ontogeny, histology, diversity, and functional significance. J. Torrey Bot. Soc. 134: 301 332. 2007.— Plant anatomists are generally agreed on the histological products o\' successive cambia: bands of secondary phloem and associated secondary xylem ("vascular increments") embedded in a background of conjunctive tissue (parenchyma, sometimes fibers). Interpretations have varied widely on the ontogeny of this plan. Studies have usually involved one or a few species. The study of numerous taxa, especially in centrospermoid families, leads to the conclusion that there is a common plan, although variations on it are manifold. A master cambium produces secondary cortex externally and. internally, rays, conjunctive tissue, vascular cambia. secondary phloem, and secondary xylem. Secondary phloem and secondary xylem are formed from the vascular cambium in each vascular increment. Vascular cambia function indefinitely, so that a master cambium and a series of vascular cambia (each in a vascular increment) function indefinitely. The master cambium either remains active as long as an axis is actively growing (although it may become quiescent following the initiation of each vascular increment and associated conjunctive tissue), or. less commonly, may be reinvented in the secondary cortex. In order to establish a framework for interpretations, the varied appearances of each ol these tissues in genera thai have successive cambia is discussed. Themes that particular genera represent are then examined: diversification in ray types and raylessness (Nyctaginaceae): diversification in conjunctive tissue (Aizoacaeae); rays as key structural elements (Gnetaceae); successive cambia as an apomorphy (Clirysanthemoiclesy. protraction of cambial activity (Menispermaceae); and cambial fracture and parenchyma proliferation {Bauhinia, Mendoncia). In some taxa. such as Gncttnn africanuni and the large tropical lianas (Bauhinia, Menispermaceae) a master cambium is absent; new vascular cambia arise by one or a few cell divisions in cortical parenchyma, followed by rapid tangential widening of the vascular cambium. Pervasive ecophysiological themes in plants with successive cambia are examined: storage and retrieval: promotion of mechanical strength and longevity of vascular tissues: and modes of lianoid structure. Because the background tissue in plants with successive cambia is conjunctive tissue, not secondary xylem, the terms "included phloem: and "interxylary phloem" are inapplicable. The term "lateral meristem"' is abandoned in favor of "master cambium."

Key words: anomalous secondary growth, cambial variants, Caryophyllales. Centrospermae. interxylary phloem, lateral meristem. lianas, master cambium.

Successive cambia are familiar as the cause thickening" or "included phloem." The sec­ of concentric rings in a beet. They also occur ondary phloem of successive cambia is not in stems and roots of such familiar plants as included within wood at all. a point made by Amaranthus, A triplex. Bougainvillea, Chenopo- Stevenson and Popham (1973). Maintenance (/iitin. Cycas, Mirabilis, Phytolacca, and Wel- of such terms may have been furthered by wit.se/iia. They occur in the flattened or those who are involved with wood identifica­ variously shaped forms of the giant lianoid tion (IAWA Committee 1989) and who stems of Bauhinia. Gnctum, and numerous therefore want simple terms. The distinctive Menispermaceae. Successive cambia occur in appearance of successive cambia and their bands or strands of secondary phloem and products can easily be learned by wood secondary xylem (vascular increments), which anatomists, however. The desire to use such are embedded in a background of parenchyma a term as "included phloem" probably in­ or fibers (conjunctive tissue). Schenck (1893) dicates a desire to consider the background and Pfeiffer (1926) used the term: the latter tissue of plants with successive cambia as accurately applied it to many of the genera "wood," but although often woody in texture. in which the phenomenon is known today. this background tissue is not wood in the Others have referred to successive cambia ordinary sense. Wood anatomists who have under the vague terms "anomalous secondary dealt in detail with plants with successive cambia have used the term conjunctive tissue for the background of fibers and/or parenchy­ 1 E-mail: [email protected] Received for publication December 19, 2006, and ma in which vascular increments are embed­ in revised form February 24. 2007. ded.

301 302 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

Terminology is only one symptom of the the "eentrospermoid" families) form a promi­ problems involved in analysis of successive nent nexus on the list, successive cambia must cambia and their products. Although various have arisen in about 15 other clades. Wel- authors describe the histology of species witschia and all species of Gnetum (Carlquist involved with reasonable accuracy, under­ 1996a) contain successive cambia. and they standing of the ontogeny of successive cambia have been reported in several species in each of has been troublesome. One cause is that soft the cycad genera Cycas, Encephalartos, and and hard tissues are intermixed in stems and Macrozamia (Greguss 1968). The listing of roots with successive cambia. Soft tissues and successive cambia genera represents a small stages in their development are frequently proportion of vascular plants at large, but it damaged and uninterpretable when such axes poses an evolutionary question out of pro­ are sectioned untreated on a sliding micro­ portion to numbers: why should this mode of tome. One solution to this problem is the use structure have been evolved repeatedly, and of a softening agent followed by paraffin what are its adaptive values? The picture of embedding and sectioning on a sliding micro­ how successive cambia arise evolutionarily and tome (Carlquist 1982). This is best applied to how they are correlated with particular modes liquid-preserved material. With material from of habit, ecology, and physiology has been xylaria. the drying process has damaged soft blocked by failure to understand the ontogeny tissues prior to sectioning. Unfortunately, of these histological systems. Various ontoge­ xylaria have served as a primary basis for netic interpretations have led to thickets of materials studied by wood anatomists. How­ terminology and controversy, which in turn ever, once liquid-preserved materials have have led to marginalization and avoidance of been studied successfully, the appearances of successive cambia in plant anatomical studies those materials based on dried specimens can and teaching. be interpreted successfully. All of the illustra­ In order to counter widespread neglect. I am tions in the present study are based on liquid- attempting to present a template for how- preserved materials. successive cambia at large originate and A third cause of misinterpretation can be operate. A consistent terminology that can likened to the parable of the blind men and the be uniformly applied is offered. Interpreta­ elephant. Most wood anatomists who have tions together with the evidence for them are looked at successive cambia have studied only offered. Those who wish more extensive a single genus, sometimes only a single species. citations of literature on successive cambia Although I believe, as obviously did Pfeiffer can consult Stevenson and Popham (1973). (1926), that a common plan underlies the Costea and DeMason (2001), and Carlquist various cases, the differences in expression (2001). when one looks at such extremes as Siuyiwriu. The concept of successive cambia differs Gnetum africamtm, or Meiuloncia may offer from manifestations that are called 'interxy- problems in interpretation. Over the past 25 lary phloem formed from a single cambium" years, I have attempted to analyze instances of (Carlquist 2001). These instances occur in such successive cambia in most clades in which they groups as Combretaceae (van Vliet 1979), occur. The value of comparative studies is, I Onagraceae (Carlquist 1975a). and Strychos believe, considerable in providing necessary and allied genera of Loganiaceae (Cockrell insights. 1941. Mennega 1980). Interxylary phloem The complexity of wood produced by strands or bands formed from a single cambi­ a single ('"normal") cambium is daunting, so um do not form pairwise relationship to neglect of successive cambia, which represent strands or bands of vessels or vessel groups; an intricate series of histological phenomena, the vessels are distributed within secondary has become commonplace. This is unfortu­ xylem. In instances of successive cambia. the nate, because successive cambia occur in a wide strands or bands of secondary phloem occur diversity of plants, and represent a fascinating external to strands or bands of secondary alternative pathway of secondary growth. xylem, respectively. These strands or bands, Successive cambia are known in 34 families considered vascular increments here, are sep­ of dicotyledons (Carlquist 2001: number of arated from each other by conjunctive tissue. families varies with taxonomic practice). Al­ Because conjunctive tissue is not secondary though the caryophyllalean families (especially xylem. the term "'interxylary" is not permissi- 2007] CARLQUIST: SUCCESSIVE CAMBIA 303 ble in plants with successive cambia. This fact a generalized plan, many features of which was noted by Stevenson and Popham (1973) are observable in the species discussed. Be­ and others. cause it is a generalized plan, any given genus will depart in various ways, discussed below. Materials and Methods. Comments on For- As far as is known, the first vascular chhanvneria (Brassicales) are based on my cambium in species with successive cambia unpublished data: work on the stem anatomy produces secondary xylem and secondary of this genus is in progress. The slides of phloem in the same fashion as does the Bougainvillca spec nihil is were given to me by vascular cambium in vascular plant species Vernon I. Cheadle. They represent the slide set that have only a single vascular cambium on which the paper by Esau and Cheadle during the secondary growth of stems or roots. (1969) was based. With the exception of these The master cambium forms from a periclinal materials, specimens and nomenclature repre­ division in cortical cells of stems (pericycle in senting the taxa mentioned below are cited in roots). Although a single cortical cell is shown the following papers: Carlquist 1966, 1981, in Fig 1 A, divisions in a series of cortical cells 1995, 1996a, 1996b. 1996c. 1999a. 1999b. form a band of indefinite circumference, or 1999c, 2000. 2002. 2003, 2004. 2007: Carlquist a cylinder around the entire axis (Kirchoff and and Robinson 1995: Carlquist and Zona 1988. Fahn 1984). There has been general agreement The microtechnical methods used and docu­ about this since De Bary (1884). The paren­ mentation of the specimens studied can be chyma between the secondary phloem of the found in those papers. Most of the photo­ first vascular cylinder and the master cambium graphs in the present study represent new is parenchyma from the primary cortex (in photomicrographs based on the slides pre­ stems). Conjunctive tissue is produced from pared for those studies. Liquid-preserved the master cambium, as shown by the radial material was used for most of the species alignment of its cell files. Conjunctive tissue is illustrated: exceptions occur in Gtietum not formed adjacent to the first vascular schwaekeanum and Mendoncia gigas, which cylinder, but is formed interior to each sub­ were studied on the basis of xylarium speci­ sequent vascular increment. Conjunctive tissue mens. is easily distinguished from cortical parenchy­ ma not only because conjunctive tissue is in Terminology is similar to that in Carlquist radial rows but because cortical parenchyma (2004), except that "master cambium'* is cells are wider in diameter (Fig. 22). Note substituted for the relatively vague "lateral should be taken that after origin of the master meristem" used in that study. Because inter­ cambium, each vascular cambium continues to pretations and thus terminology have been so add secondary xylem and secondary phloem varied, terms and synonyms of them are to its own vascular increment. Secondary explained in the contexts below. On photo­ xylem and secondary phloem continue to be micrographs, the "pointers'* (<, >) indicate added to the original vascular cylinder (see master cambia, whereas arrows indicate vas­ lower row of drawings in Fig. 1). The master cular cambia. The term "vascular cambium"* is cambium and an indefinite number of the used in a restricted sense here: a meristematic vascular cambia coexist. The master cambium layer that produces phloem to the outside and may be active or quiescent at any given time. xylem to the inside; this usage excludes pro­ In some cases a master cambium may be duction of conjunctive tissue from a vascular reinvented further out in the cortex or (more cambium. A vascular cambium can include likely) secondary cortex, but this is considered ray initials and produce phloem rays and less common than maintenance of the master xylem rays. In some instances, as in Pisonia, cambium at its original site. Secondary cortex rays are produced by the master cambium. (identifiable by its radial lines of cells) is produced externally by the master cambium. Ontogeny and Products of Successive Cambia

The drawings in Fig. 1 represent a series of The Master Cambium. The term master stages beginning with the origin of what is cambium is offered here hesitantly. A plethora termed the master cambium here. This series of terms for this layer is encountered, in­ of drawings is designed to introduce concepts cluding anomalous cambium, lateral meri­ and developmental stages. These present stem, primary thickening meristem. second 304 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

origin of master cambium by divisions in cortex cells periclinal divisions begin conjunctive origin of tissue vascular secondary formation cambium phloem cells formed secondary from vascular cortex cambium cells forming conjunctive tissue completed

primary vascular tissues complete differentiation secondary phloem and secondary more secondary xylem phloem and derived from secondary xylem; vascular primary phloem cambium crushed

FIG. I. Origin of the master cambium as seen in a hypothetical stem transection, followed by stages in the production of cell types (including a vascular cambium produced from that master cambium). Stage H represents a stage just prior to origin of a second vascular cambium from the master cambium. The drawings in the lower row are schematic and indicate the location of the cellular progressions depicted in the upper row. This series of drawings, although based on centrospermoid genera with ra\s such as Cluirpentiera and Stegrtosperma, is intended for orientation purposes and may not correspond in detail to what is observed in any given species. Labels: c = cortex, ct = conjunctive tissue, mc = master cambium, pd = periderm, pp = primary phloem, pr = primary ray. r = ray. re = ray cambium, sc = secondary cortex, sp = secondary phloem, sx = secondary xylem, vc = vascular cambium. cambium, and supernumerary cambium. Per­ the master cambium and the vascular cambi­ haps even more dangerous is to refer to this um (which may correspond to their "old" and layer merely as "cambium,"* as Esau and "new" cambia respectively) have quite differ­ Cheadle (1969) do. Esau and Cheadle (1969) ent extents and actions. Esau and Cheadle use the terms "old cambium" and "new (1969) contrast their use of the term vascular cambium" in Bougainvillea, not realizing that cambium with the results of other workers. In 2(M)7] CARLQUIST: SUCCESSIVE CAMBIA 305

H

7 renewed -]0 r- 73— master cambium mc—-—p E^Efrgfaeta— crushed sp ray Jf (_p •~~rrjT~TLrTT)i 1> recent sp cells) y h3—&-n ^

secondary xylem

master cambium quiescent outside of vascular tissues

mc

new rays added, increased circumference of master cambium and secondary cortex

FIG. 1. Continued. fact. Esau and Cheadle (1969) are inconsistent, interpretation with that of workers (e.g.. because they claim that a vascular cambium Studholme and Philipson 1966) who find that (in plants with successive cambia) produces there is a "self-perpetuating meristematic phloem to the outside and xylem to the inside zone." This pervasive contrast is unjustified. (p. 807), but later state (p. 815) that each of The concept of a master cambium giving rise llie '"cambia"" produces "xylem and conjunc­ to conjunctive tissue and vascular cambia tive tissue to the inside and phloem and internally is the concept that consistently conjunctive tissue to the outside." Esau and explains what is observed in diverse centro- Cheadle (1969) attempt to contrast their spermoid Caryophyllales and most other cases. 306 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

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FIGS. 2-5. Transections of stems. Figs. 2-3, Stegnosperma halimifoltum (Stegnospermaceae). Fig. 2. A zone that includes cortical sclereids and the products of two vascular increments; note that the older increment has accumulated more secondary xylem than the upper. Fig. 3. Area showing secondary cortex, a master cambium, and tissues produced by the most recently formed vascular cambium. Figs. 4-5. Bouguinvillca spectabilis (Nvctaginaceac). Fig. 4. Area near the outside of the stem, showing the coexistence ofa master cambium (several recent divisions to the right of the pointer) and a vascular cambium. Fig. 5. An 2007] CARLQUIST: SUCCESSIVE CAMBIA 307

In the examples cited here, a master cambium DeMason (2001). There may be exceptions in is lacking only in Gnetum ajricanum and the some lianas, such as Gnetum africanum large tropical lianas, such as Bauhiniu. These (Figs. 28, 29) and Mendoncia (Figs. 32, 33), lianas show rapid lateral widening of vascular in which new master cambia do form de novo cambia; they also show proliferation of paren­ in cortical cells. chyma that form sites for initiation of new In some species, the constraints imposed by cambia. The important feature to be noted is the existence of a cylinder of cortical fibers that two types of cambial action in a single prevents origin of a master cambium further stem are envisioned in the present paper (as in outwards. This is shown clearly (Fig. 27, upper earlier work. Carlquist 2004). whereas those right). In this instance, one may regard the who have dealt with successive cambia mostly master cambium as the outermost layer of thin- have attempted to think in terms of a single walled cells shown. In that case, no secondary type of cambium. cortical cells are produced. Esau and Cheadle The master cambium is most easily visible (1969) and Costea and DeMason (2001) devote when actively dividing (Figs. 3, 24). The radial much space to a discussion of whether a "cam­ rows of conjunctive tissue between a master bium" is bidirectional or unidirectional. The cambium and the preceding vascular incre­ confusion on which such discussions are based ment (ct. Fig. 22) make the master cambium may relate to varied concepts of what cells readily distinguishable. If the master cambium a master cambium produces outwardly, but is actively dividing, it may appear to consist of more likely the cause is a conflation of a master several layers. The term "diffuse lateral cambium and a vascular cambium and their meristem,"' inadvisablv applied to this phe­ products before two types of cambia were nomenon, was used earlier (Carlquist 2001). recognized. Esau and Cheadle (1969) claimed The concept presented here is that the master that their study of Bougainvi/lea "revealed no cambium is functionally a single layer in uniform continuous perpetuation of a meriste- thickness. As in an "ordinary" vascular matic zone. Instead, a sequence of cambia were cambium in most woody plants, the sequence found arising outside each successive growth of products is not disorderly a fact, together increment." This statement is at odds with with radial alignment of wells and observa­ what is seen in Pisonia and allied genera, also tions on cambium in winter condition, that has of Nyctaginaceae (Carlquist 2004). Esau and led to the idea that a vascular cambium is Cheadle (1969) claim that conjunctive tissue is a single cell in thickness. In some species with an abaxial product of each "successive cambi­ successive cambia. a master cambium never um" (which they say also produces conjunctive ceases to function. Although the occurrence of tissue inwardly). The origin of each "successive marked discontinuity in radial cell alignment growth increment" in such alleged outer in some axes and stems may be evidence that conjunctive tissue is at odds with the histology. one master cambium has ceased to function Esau and Cheadle (1959, Plate 2A) show this and a new one has formed. In most species, tissue to consist of raphide idiobiasts and of however, the master cambium apparently parenchyma cells subdivided transversely into functions over a long period of time. It can strands of several cells. My study of the become quiescent, and after being quiescent, Cheadle slides confirms the histological nature may regain activity, a condition shown in of this tissue (which I would call secondary Fig. 1. In most species with successive cambia. cortex). Obviously, the fusiform cells from the master cambium does not relocate: this which both the master cambium and the concept is in contrast to the idea that the vascular cambium are composed in Bougain­ [master] cambium "moves outward" as ex­ villea could not have their origins in such pressed by several authors, such as Costea and a tissue.

area from an older part of the stem; the vascular cambium has produced more secondary phloem, crushing the earlier-formed secondary phloem. Labels: c = cortex, cs = cortical sclereids, csp = crushed secondary phloem, ct = conjunctive tissue, r = ray. sc = secondary cortex, sp = secondary phloem, sx = secondary xylem. v = vessel, arrow = vascular cambium, pointers (<.>) = master cambium. Fig. 2. bar = 100 urn; Figs. 3-6, bar (Fig. 3) = 100 urn. 308 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

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FIGS. 6-9. Tangential (Figs. 6-8) and radial (Fig. 9) sections of stems. Figs. 6 7 BougainvUlea spectabilis (Nyctaginaceae). Fig. 6. Section from a relatively small (ca. 1 cm diameter) stem, showing secondary phloem (at right) and secondary xylem (left) from a vascular increment. Fig. 7. Section from a relatively large (ca. 16 cm diameter) stem showing rays (center) and other tissues of a vascular increment. Fig. 8. Heimerliodauiron brunonianum (Nyctaginaceae), showing rayless condition, with a single vessel traversing the fibrous xylem. Fig. 9. Nototrichium sandwicen.se (Amaranthaceae). showing that vessel elements and 2007] CARLQUIST: SUCCESSIVE CAMBIA 309

In some species with successive cambia, the lar increment. Secondary phloem is added by long and clearly radially aligned files of cells each vascular cambium, as is seen by crushing demonstrate the existence of a master cambi­ of earlier-formed secondary phloem and a de­ um with prolonged activity. The long radial gree of compression of the arcs of parenchyma series of cells that are figured by Lev-Yadun cells exterior to the secondary phloem. and Aloni (1991) for Suaeda suggest this. Other examples are shown here in the cases of Pisonia Vascular Cambium. A vascular cambium (Fig. 10), Quapira (Figs. 12. 13), and Stayneria originates from a master cambium which can. (Fig. 25). There is probably little or no in the process, retain its own identity (Fig. ID quiescence in the activity of the master cambia as in Pisonia and allied genera). The criterion of these species, in keeping with the relatively for the origin of a vascular cambium here is no nonseasonal nature of their habitats. The different from that in most vascular plants: vascular cambia are active in these at the same cells are produced externally and internally, time that the master cambium is active, so that and these products mature into identifiable these above examples form strong evidence mature cell types. At the point indicated, for the co-existence of two types of cambia. division of an initial cell into a sieve tube Pisonia forms a critical example, because the element and a companion cell is evident illustration by Solereder (1899. 1908; repro­ (Fig. 15: the letters po are superimposed over duced in Metcalfe and Chalk 1950. p. 1064) for these cells). The cell below those is a vascular Pi\onia nigricans Swart/, which is much like cambium cell. In addition, the cell below the the material studied here for P. rotumlata. vascular cambium cell is probably an imma­ cannot be explained in terms of the action of ture conjunctive tissue cell. Divisions leading a single cambium. Solerederis illustration has to the formation of a sieve tube element and never received the comment and interpretation a companion cell are readily evident because it so obviously invites. There are a few flaws in of the narrowness of phloem cells: production the illustration: crushed secondary phloem is of conjunctive tissue is not so easily ascer­ not shown (and therefore the action of vascular tained. The master cambium has produced cambia in producing secondary xylem and conjunctive tissue initials before the origin of secondary phloem is not illustrated), and there sieve tube elements. An anticlinal division is should be radial alignment of the fibers with implicated in the origin of a vascular cambium the immature cells between fibers and the (Fig. ID). This is shown in photomicrographs master cambium (see Fig. 17). But the central in (Fig. 15, the three pairs of files above the issue at hand is clearly figured by Solereder: letter d; Fig. 29). Why should one expect an there is a master cambium that extends around anticlinal division? the stem: it produces rays, vascular cambia. and most of the fibers internally. The strands The master cambium cells, because they are of vessels and associated phloem (Fig. 17) initiated by periclinal divisions in cortical contain vascular cambia. a feature not consid­ parenchyma cells, tend to have tangential cell ered by Solereder: these produce phloem widths like those of such parent parenchyma externally and vessels and fibers associated cells. Phloem cells and xylem cells, in accor­ with the vessels internally. Although the master dance with their functional nature, tend to be cambium extends around the stem, the vascu­ cells much narrower than parenchyma cells. lar cambia are narrow strips, each perhaps 10- Thus, for a vascular cambium to produce 12 cells wide tangentially. Because the back­ xylem and phloem, periclinal divisions must ground of the stem is fibrous, few if any vessels occur (Fig. ID). We find, in fact, that the are added by any given vascular cambium once number of files of vascular cambium cells and the fibers have matured around a given vascu­ derivatives thereof is greater than the number of files of master cambium cells and deriva-

conjunctive tissue, and sieve elements have similar lengths, although some files of conjunctive tissue subdivide. Labels: ct = conjunctive tissue, fx = fibrous xylem. jr = juvenilistic (paedomorphic) ray. pb = band of axial parenchyma, sp = secondarv phloem, v = vessel. Figs. 6-8, scale in Fig. 2; Fig. 8, scale in Fig. 3. 310 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

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FIGS. 10-13. Sections of stems of Nyctaginaceae. Figs. 10 11. Pisonia rolundata. Fig. 10. Transection, showing three vascular increments in a fibrous background. Fig. 11. Tangential section, showing vessel (far left), uniseriate rays, and a biseriate ray (lower right) in a background of fibrous tissue. Figs. 12 13. Guapira discolor. Transections from a large stem (ca. 4 cm diameter). Fig. 12. Area showing three vascular increments; five fibers delimit primary cortex, outside of stem (top), from secondary cortex. Fig. 13. Area from cortex (top) to secondary xylem of outermost vascular increment. Labels: c = primary cortex, ctf = 2007] CARLQUIST: SUCCESSIVE CAMBIA 311 tives thereof—often two times as great. For Preparations that reveal divisions in cambia in example, in Stegnosperma (Fig. 3), the ratio of plants with single vascular cambia are by vascular cambium cells to master cambium comparison much easier to obtain. cells in the area shown is about 18:11; in As in vascular plants with a single cambium, Heinwrliodendron (Fig. 14) about 17:11. One there is no evidence in the plants considered must be careful not to count fiber tips (which here to counter the idea that a vascular are intrusive, of course) in estimating the cambium is functionally more than one cell number of cells in the vascular cambium and layer thick. The fact that secondary phloem is its derivatives. The process of conversion of always produced outward and secondary master cambium derivatives to vascular cam­ xylem is always produced inward in plants bium initials has not been mentioned in the with a single vascular cambium is cited as one literature, evidently because authors have line of evidence that these should be termed depended on the concept of a single kind of vascular cambia (instances of interxylary operative cambium. phloem, as in Combretaceae, Onagraceae, A fascinating exception to the above is in and Loganiaceae, are an obvious exception Pisoniii and allied genera (Guapira, Neea, in plants with a single cambium). In all of the Torruhia). In these genera, fibers form the genera considered here, each vascular cambi­ background tissue of the stem. This also um produces secondary xylem inwardly and occurs in Aizoaceae. in Stayneria (Fig. 25). secondary phloem outwardly, a fact that I Thus, the master cambium must consist of believe supports the recognition of the concept tangentially narrow cells from the outset in of a vascular cambium functioning separately these particular genera, and it does. Vascular from (but ontogentically derived from) a mas­ cambia do arise from master cambia in Pisonia ter cambium. and allied genera, but anticlinal divisions do Frequency of initiation of vascular cambia not occur in that process, because they have over time is omitted from most studies, occurred earlier. Note should be taken that in perhaps because most anatomists do not know the Pisonia group of genera and in Stayneria, the age of the stems or roots they study. The fibers are derived from both master cambium roots of Beta show that numerous vascular and vascular cambia. with no boundary in­ cambia can be formed per year, and more than dicating which fibers are derived from which one per year is probably the prevailing cambium. This is completely understandable, condition in successive cambial plants. The because tangential cell diameter is the same in longevity of each vascular cambium can both types of cambia. extend over a series of years. The sympodial The sequences of divisions and their prod­ nature of shoots in Phytolacca dioica can be ucts in the schematic drawing (Fig. 1) do not used as a marker for number of vascular apply to all species, but can serve as a way of increments produced per season; in Phytolacca demonstrating common conditions. Materials dioica. several vascular increments are pro­ that show these division stages are very duced per season (Bruce Kirchoff, personal difficult to obtain. Microtechnical prepara­ communication). tions that reveal divisions in tissues with The period of viability of vascular cambia is delicate thin walls but also reveal hard tissues a separate issue from number of vascular (such as cortical fibers or conjunctive tissue cambia formed per season. Length of viability fibers), necessary to identification of meriste- of the vascular cambia has not been specifi­ matic cells, are extraordinarily difficult to cally studied in any plant, as far as I know make. More importantly, active division in Studies that show whether vessels in earlier meristematic tissues of a species with succes­ vascular increments are still conducting are sive cambia may well not be occurring at needed. Vascular cambia are not alike in all a given time in a given piece of stem or root. species that have successive cambia. These

conjunctive I issue fibers, ctp = wide zone of conjunctive tissue parenchyma, ft = fibrous tissue, pet = narrow band of conjunctive tissue parenchyma, r = ray, sc = secondary cortex, sp = secondary phloem, sx = secondary \\lem. v vessel, arrow = vascular cambium, pointers = master cambium. Figs. 10. 11. 13. scales in Fig. 3; Fig. 12. scale in Fig. 2. 312 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

FIGS. 14-17. Transections of stems of Nyctaginaceae. Figs. 14-16. Heimerliodendron brummiaum. Fig. 14. Area showing, from top to bottom, secondary cortex, master cambium, a band of libers abaxial to which no phloem is evident: conjunctive tissue parenchyma; and a portion of an older vascular increment. Fig. 15. Master cambium and its products; origin of a phloem strand (po. superimposed on the phloem cells) and divisions indicative of vascular cambium origin (three pairs of cells above the letter d) are indicated, Fig. 16. Section showing origin of secondary phloem from vascular cambium; note the relative number of 2007] CARLQUIST: SUCCESSIVE CAMBIA 313 differences, most readily determined by exam­ successive cambia innovate master cambia ining the products of the vascular cambia, are infrequently, often only once in the life of an detailed in the taxonomic groups considered in axis. Reasons for this interpretation include the second major section of this paper. the following: Note should be taken that when vascular (1) Beta produces numerous vascular incre­ cambia form, the fusiform cambial initials are ments ("rings") in a single season, each longer and narrower than are cells of the vascular increment with its own vascular master cambium, conjunctive tissue cells, or cambium. The examination of Artsch- secondary cortex cells. This is one obvious wager's (1926) photographs and draw­ correlation with the fact that conjunctive ings is compatible with the idea of tissue and secondary cortex tissue are not a single master cambium, with very little produced by vascular cambia. Radial sections secondary cortex production. To imag­ show that the fusiform cambial initials remain ine otherwise, we would have to imagine fusiform cambial initials and do not subdivide the numerous vascular increments pro­ or change shape. duced from two or more origins of a master cambium, and more than one Secondary cortex. The master cambium master cambium would be an uneco­ produces radial files of parenchyma to the nomical way to achieve that. outside (Figs. 2. 3). Only a single layer of (2) Those who have successfully prepared secondary cortex is present in some prepara­ extensive transactions of Chenopodia- tions, although a second layer may be formed ceae (Lev-Yadun and Aloni 1991) show- (Fig. 1H). Esau and Cheadle (1969) apparent­ unbroken radial seriation of segments of ly regard the secondary cortex as "conjunctive vascular cambia, rays, etc. One would tissue," an interpretation that is not supported expect disjunctions (offsets, discontinu­ here. The term conjunctive tissue implies used ities) in radial seriation if master cambia by most authors denotes tissue that lies were innovated continually. between one vascular increment and the next. (3) The centrospermoid families mostly Secondary cortex may. in fact, not be have a distinctive cylinder of cortical present in some species with successive cam­ fibers (Figs. 2, 12. 13) that delimit inner bia. In an illustration of Pisonia (Fig. 17), the from outer cortex. If new master cambia layer just inside the fibers and sclerenchyma were continually produced outwardly, shows periclinal divisions that indicate the one would expect to see some of these existence of a master cambium. There are fibers incorporated into secondary tis­ about three or four layers of secondary cortex sues of the stem (or root), but in fact, in the stem of Guapira illustrated (Fig. 13). A that has never been reported. A master scattering of divisions in various planes may cambium may be present in the cell layer be seen in the secondary cortex of Stegno- just interior to such fibers (Fig. 17). sperma (Fig. 3). Such divisions are generally not common in the species with successive (4) While there may be shifts in successive cambia. because the radial rows of cells in the cambial schemes within centrosperms and secondary cortex are usually conspicuous between centrosperms and the other clades (Figs. 14. 16. 24). in which successive cambia occur, one The large tropical lianas (e.g., Bauhiniu) would not expect radical departure from form new vascular cambia frequently, and a basic plan unless there were some such events can be detected by the appearance histological evidence (as there is in Gnetum of vascular strands, isolated within a paren­ africanum and certain woody tropical chyma background. Most other species with lianas) that master cambia are absent.

files of master cambium cells compared to vascular cambium cells. Fig. 17. Pisonia rotundata. Section showing master cambium activity just inside the cortical fiber band. Labels: cf = cortical fibers, ctf = conjunctive tissue fibers, ctp = conjunctive tissue parenchyma, d = anticlinal division indicating vascular cambium origin, f = fiber band, po = origin of secondary phloem from vascular cambium, r = ray, sc = secondary cortex, sp = secondary phloem, sx = secondary xylem, v = vessel, arrow = vascular cambium, pointers = master cambium. Figs. 14-17. bar in Fig. 4. 314 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

FIGS. 18-21. Transections of stems of Aizoaceae. Figs. 18 20. Trichoiliadema bulhosum. Fig. 18. Area from secondary cortex (top) inward showing a series of vascular increments (looking like but not equivalent to vascular bundles) in a background of conjunctive tissue parenchyma. Fig. 19. A portion of a vascular increment, showing fibrous secondary xylem (bottom) adaxial to parenchymatous secondary xylem. Fig. 20. A strand of fibers formed by vascular cambial action that has produced no vessels and no secondary phloem. Fig. 21. Aptenia cordtfotia Area showing, from top to bottom: active divisions in master cambium cells. 2007] CARLQUIST: SUCCESSIVE CAMBIA 315

(5) Numerous innovations of master cambia of undifferentiated cambium and some phlo­ would present problems in forming em." There is phloem in all of the vascular interconnections between a series of increments, as his drawings show, but the vascular increments; such interconnec­ •'undifferentiated cambium"' proves to be tions do occur (Fahn and Schchori 1967, mostly parenchyma of secondary xylem. The Kirchoff and Fahn 1984). cell layer identified as by Artschwager (1926) as cambium elsewhere in his paper would Conjunctive Tissue. A master cambium is support the idea that the vascular cambium is most frequently separated from the secondary functionally only a single layer in thickness. phloem of the previous vascular increment by about four cells of conjunctive tissue (Fig. 22), Secondary Phloem. The phloem produced although there are more numerous layers in by vascular cambia is by definition secondary those species that have bands of sclerenchyma phloem, and this holds in plants with succes­ in conjunctive tissue. As a master cambium sive cambia. Radial files are readily evident in becomes active, at first few or no layers of secondary phloem of these species (Figs. 15, conjunctive tissue are evident between the 16). In successive cambial species studied to master cambium and the secondary phloem date, secondary phloem differentiates before of the preceding increment (Fig. 21). Quies­ secondary xylem in any particular vascular cence of the master cambium may obscure this increment (Artschwager 1926, Esau and Chea- at times (Fig. 4). When several layers (the dle 1969). Secondary phloem may contain approximate number is characteristic of par­ fibers (Fig. 27). It may consist mostly of ticular species) have been formed, no more parenchyma, as in the roots of Beta (Artsch­ layers are added to that band, as study of wager 1926) or Mirabilis (Mikesell and Pop- stems with numerous vascular increments ham 1976). (Fig. 22) shows. The fact that several layers A feature of successive cambia not often of conjunctive tissue may be seen internal to mentioned in the literature is the prolonged a master cambium before other tissues are production of secondary phloem by each appear (Fig. 15) is taken as evidence that vascular cambium. Earlier-formed secondary conjunctive tissue is the first product of phloem is crushed (Figs. 5. 10, 17. 19. 25). a master cambium (Figs. 1C, ID). Some conjunctive tissue consists wholly of Secondary Xylem. Amounts of secondary parenchyma, as in Beta. The familiarity of this xylem produced by a vascular cambium vary example may lead some to consider conjunc­ from a few cells (Fig. 22) to increments several tive tissue always to be parenchyma. However, cm wide, as in some Menispermaeeae (Carl- in addition to parenchyma, fibers, sclereids. quist 1996c). Distinctive parenchyma bands and occasionally idioblasts ma\ be present in (Fig. 19) or various distributions of parenchy­ conjunctive tissue. The distribution of these ma and fibers beside the vessels may occur cell types in amount and in spatial relationship (Figs. 4. 5). These represent characteristics of to each other within conjunctive tissue varies particular genera, as discussed later. markedly in species with successive cambia. If growth rings occur in plants with The distinctive expressions of conjunctive successive cambia. they will be evident in tissue are considered in the second major secondary xylem. An instance of these is section of this paper. Artschwager (1926) illustrated here (Fig. 31). and they have been claims that in a photomicrograph of numerous identified in Charpentiera densiflora of the vascular increments of Beta (that illustration Amaranthaceae (Carlquist 2003). The mention inverted with relation to drawings in the of "annual rings'* in Beta by Artschwager paper) that these rings are "composed mostly (1926: 168. 175) is presumably a wording error

secondary phloem, a vascular cambium, and secondary xylem. Note that about four files of master cambial cells are evident, whereas about nine or ten files of vascular cambium cells can be identified. Labels: csp = crushed secondary phloem, cl = conjunctive tissue, ctp = background of conjunctive tissue parenchyma, f = fibrous conjunctive tissue, psx = parenchymatous secondary xylem, sp = secondary phloem, sx = secondary xylem. vl = vessel, arrow = vascular cambium, pointers = master cambium. Fig. 18, scale in Fig. 2; Figs. 19-20, scale in Fig. 3: Fig. 21, scale = 30 um. 316 JOURNAL OF THE TORREY BOTANICAL SOC If n [VOL. 134

FIGS. 22-25. Stem transections of ALzoaceae. Figs. 22 23. Aptenia cordtfolla. Fig. 22. Area showing primary cortex (top) and portions of two vascular increments. Although secondary phloem is present in both increments, no vessels have formed at this stage. Fig. 23. Area showing portion of an older vascular increment, showing vessels. Fig. 24. Marloihisiella uniondulensis. Most of the secondary tissue consists of conjunctive tissue parenchyma. Fig. 25. Stayneria netiii. A pair of vascular increments in a rayless fibrous background tissue. Labels: c = cortex, csp = crushed secondary phloem, ct = conjunctive tissue, f = fibrous 2007] CARLQUIST: SUCCESSIVE CAMBIA 317

(annular would be correct). Although the idea unaware of the concept of paedomorphosis that one vascular increment per year would be (juvenilism) in rays, although that concept had produced by a successive cambial plant may be been enunciated earlier (Carlquist 1962). appealing, it does not seem to be true. More Paedomorphic rays consist wholly or pre­ than one vascular increment per year seems dominantly of upright cells, not just at the the common condition. beginning of secondary growth, but indefinite­ One feature that has not been expressly ly thereafter (Carlquist 2001). Bougainviilea addressed when analyzing secondary xylem in has rays, as defined the rays usually are. radial plants with successive cambia is how to sheets of parenchyma, which take the form of describe it separately from conjunctive tissue. elliptical zones one to several cells wide as seen If the scheme proposed in the present paper is in tangential section. These can be seen in the followed, secondary xylem is always defined as preparations of Cheadle (Fig. 6 here; Plates the internal product of a vascular cambium. 1 A, B and Plate 3C in Esau and Cheadle 1969) This becomes significant in families where and. more clearly, in some of my preparations some genera have successive cambia while (Fig. 7). In the latter, the rays are distinct from others do not. such as Phytolaccaceae (Carl- parenchyma bands (pb) of conjunctive tissue. quist 2000). Secondary xylem in genera with Metcalfe and Chalk (1950) term the rays of successive cambia can have distinctive axial Bougainviilea "raylike radial sheets of con­ parenchyma distributions (e.g.. scanty vasi- junctive parenchyma." centric in Caryophyllales: Fig. 11. cells to the The occurrence of paedomorphic rays in right of the vessel) that should not be confused species with successive cambia should not be with conjunctive tissue parenchyma. a surprise. The nature of a master cambium is distinctive in that it makes repeated copies (the Rays: paedomorphosis and raylessness. If one vascular cambia) of its cells. Because each of is familiar with ray types in typical dicotyle­ the vascular cambia is of relatively short donous woods produced by a single cambium duration compared to that of a normal woody (the "Kribs Ray Types": Carlquist 2001), one dicotyledon, the changes seen in fusiform finds that such rays are not common in species cambial initials (Bailey and Tupper 1918) with successive cambia. Instead, one tends to and rays (Barghoorn 1941) do not have time find such conditions as (1) permanently to occur. In fact, there is little change in juvenilistic rays; (2) raylessness; or (3) rays fusiform cambial length (as judged from vessel produced from a master cambium rather than element lengths observed in study of radial from a vascular cambium. Occasionally, one sections) over time in species with successive sees the occurrence of unusually wide rays in cambia (Carlquist. unpublished data). Simi­ species with otherwise rayless secondary xy­ larly, there is little change in type (procum­ lem. as in Suaeda (Lev-Yadun and Aloni bent, square, upright) of ray cells over time. In 1991). This assemblage of ray phenomena most species with successive cambia, each has provoked diverse reactions. Baird and vascular cambium undergoes little tangential Blackwell (1980) refer to "'radial conjunctive increase cell number because of its limited life tissue*' (as opposed to "tangential conjunctive span (although Gnetum africanum, Fig. 29, is tissue") in Halogeton (Chenopodiaceae), al­ an exception). The limited tangential increase though they figure (p. 271) what any wood of the vascular cambium is associated with the anatomist would identify as biseriate and phenomenon that vascular cambia are so triseriate rays. In Beta. Artschwager (1926) frequently juvenilistic in species with succes­ does not mention rays in vascular increments sive cambia. Increase in tangential extent of after the first one. Similarly, rays are not meristematic layers occurs mostly in the mentioned by Esau and Cheadle (1969) in master cambium. Tangential sections of cam­ Bougainviilea. Esau and Cheadle are evidently bia in plants with successive cambia are

conjunctive tissue, p = parenchymatous conjunctive tissue, psx = extensive background of parenchymatous conjunctive tissue, ri = raphide idioblast. sc = secondary cortex, sp = secondary phloem, sx = secondary xylem. v = vessel, arrow = vascular cambium, pointers = master cambium. Figs. 22. 24-25. scale in Fig. 2; Fig. 23. scale in Fig. 21. 318 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

FIGS. 26-29. Stem transections of Gneiuni (Gnetaceae). Figs. 26-27. G. schwackeaman. Fig. 26. Area showing portions of two vascular increments: there is a marked disjunction in the histological composition of the two increments (in ray number and size, for example). Fig. 27. Outer portion of a vascular increment: a probable master cambium forming just outside of the phloem libers. Figs. 28 29. G qfricanum. Fig. 28. A single vascular increment, showing marked dilation in both ray and fascicular tissue with secondary growth. Fig. 29. Origin of a new vascular increment (narrow cells) by subdivision of a few (perhaps two) cortical 2007] CARLQU1ST: SUCCESSIVE CAMBIA 319 infrequently illustrated: Esau and Cheadle (1935). There is a notable correlation involved. (1969, P. 3) present an excellent section. A In Guapira and allied genera all rays are section of a master cambium should look produced from the master cambium, not from much like a section of a vascular cambium vascular cambia. where lengths of fusiform cells are concerned. Raylessness in woods is a form of paedo- Three-Dimensional Aspects. The discussion morphosis. or protracted juvenilism (Carlquist to this point is based mostly on transactions, 1970. 2001) in which rays may never develop with passing reference to tangential or radial or, if they do, are characterized by mostly sections. The tissues in successive vascular upright cells. Not surprisingly, raylessness increments, in order to be function, must be occurs in a number of species with successive connected with each other, but single sections cambia. especially in Caryophyllales. Virtually do not illustrate this well. Only a few workers the entire family Aizoaceae is rayless (Carl­ have examined the three-dimensional patterns quist 2007). involved in species with successive cambia. The ontogeny of rays in Pisonia and allied Fahn and Schchori (1967) have made a notable genera (Guapira, Neea, Torrubia) is unusual in contribution based on study of Chenopodia- that rays are formed from the master cambi­ ceae. Conceivably, there are different patterns um, not from the vascular cambium (Carlquist in different families. Three-dimensional pat­ 2004). The rays in these genera are narrow terns can be studied with a variety of (uniseriate or biseriate), well defined (Fig. 11), techniques, ranging from serial sections (Fahn and not like the rays of other Nyctaginaceae. and Schchori 1967, Fahn and Zimmermann Vessels and some fibers but no rays are 1982) to dye injection (Fisher and Ewers produced by the vascular cambia in the 1992). Fahn and Schchori (1967) make the Pisonia alliance (Figs. 10, 12, 13). This di­ fascinating observation that the pathways of vision of labor between master cambium and phloem strands are not identical with those of vascular cambium is one clear line of evidence xylem strands in a given axis, but run in­ for the existence of both a master cambium dependently of each other in the material they and vascular cambia. rather than a single study. The degree to which this is widespread cambium, in species with successive cambia. in plants with successive cambia needs studied. This interpretation should have been offered Esau and Cheadle (1969) note points of long ago, because the figure of the stem of fusion between "old" cambia and "new" Pisonia nigricans by Solereder (1899, 1908, cambia in transactions of Bougainvillea. Their 648: reproduced by Metcalfe and Chalk 1950, figures suggest that what they are describing p. 1064) has stood without comment or may represent ontogenetic starting points in explanation for about a century. formation of anastomoses between vascular Ray cambium is difficult to discern in increments. species with successive cambia that do have In my account of cambial variants (2001), I rays. Divisions are relatively few (Fig. 3) made a distinction between instances of compared with divisions in fascicular areas. "successive cambia" and examples of "wood Much radial growth is accomplished by radial portions dispersed or separated in divisions in cell elongation in rays, hence the infrequency parenchyma or parenchyma expansion." The of periclinal divisions. latter list, in fact, contains a number of Although the rays of species with vascular examples in which formation of successive cambia are predominantly upright, leading cambia is present in addition to other meri- them to be termed paedomorphic. exceptions stematic phenomena. One genus notable in can be found in the genera Guapira, Neea, this regard is Bauhinia of the Fabaceae (Handa Pisonia. and Torrubia (Nyctaginaceae). Met­ 1937, Wagner 1946, Machado et al. 1966, calfe and Chalk (1950) refer rays in these Basson and Bierhorst 1967. Roth and Ascen- genera to Homogeneous Type II of Kribs scio 1977, Fisher and Ewers 1994, Vieira

cells. Labels: c = cortex, ct = conjunctive tissue, p r = phloem ray, r = ray, re = ray cambium, sp = secondary phloem, sx = secondary xylem. arrows = v ascular cambium, pointer = master cambium. Fig. 26, scale in Fig. 2; Fig. 27. scale in Fig. 3; Fig. 28, scale = 200 urn; Fig. 29, scale = 20 urn. 320 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

MF^K FIGS. 30-33. Stem transections of species with successive cambial activity. Fig. 30. Chrysanthemoides monilifera (Asteraceae). Portions of two vascular increments and the conjunctive tissue between them. Fig. 31. Anamirta coccuhts (Menispermaceae). A vascular increment and the preceding and following bands of conjunctive tissue, which contain tangential bands of sclereids. Figs. 32-33. Mendoncia gigas (Acanthaceae). Fig. 32. Area representing most of a vascular increment, radiating from point of origin (osx) and an isolated vessel with associated fibers at top. left of center. Fig. 33. Area from outside of stem 2007] CARLQUIST: SUCCESSIVE CAMBIA 321

1994). To this may be added Rourea of the in Simmondsia and Stegnosperma, as well as Connaraceae (Fisher and Ewers 1992), Men- evidence from molecular studies (Downie and doncia of the Acanthaceae (Carlquist and Palmer 1994. Downie et al. 1997) reinforce the Zona 1988), and Triphyophyllum (Dioncophyl- idea, presented earlier, that the plan of master lum) of the Dioncophyllaceae (Gottwald and cambia and vascular cambia in the two genera, Parameswaran 1968). There is little or no represents a basic condition in centrosper- action of a master cambium in these examples, moids with successive cambia. There has been because origin of new vascular cambia occurs no previous evolutionary sequence of succes­ as points (single cells) rather than as sheets of sive cambia types within Caryophyllales hith­ parenchyma. erto proposed.

Comparative Themes Nyctaginaceae: apomorphies in master cam­ bia and rays. Esau and Cheadle (1969) do not Simmondsia and Stegnosperma: symplesio- mention rays (or for that matter, raylessness) morphies in the centrosperms. Downie and in their account of Bougainvillea. and thus Palmer (1974) and Downie et al. (1997) have present an incomplete picture of meristematic presented DNA-based trees of Caryophyllales. activity in the genus. In the transaction shown These trees refine the phylogenetic construc­ here (Fig. 5), the right five radial cell files tions by Rodman et al. (1984). The positioning are best interpreted as a ray. The area in of the monogeneric families Simmondsiaceae a tangential section (Fig. 6) designated -*jr'" and Stegnospermaceae in these trees suggests forms an elliptical area typical of rays, and that one might expect character states primi­ since there is radial continuity of such areas tive for Caryophyllales in these two families. (Fig. 5), they should be considered as rays. Indeed, tracheids, a feature symplesiomorphic Ray cells (Fig. 7, r) embedded in a background for dicotyledon woods at large (Carlquist of fibers (Fig. 7, fx) are readily identifiable as 2001). occur in these two genera but in few rays, certainly, even though most of the ray other centrospermoid Caryophyllales. In con­ cells are upright. The presence of upright cells trast, Phytolaccaceae (Carlquist 2000) and and storying does not disqualify these struc­ Amaranthaceae (Carlquist 2003) have libri- tures from being rays. Paedomorphosis in ray form fibers in wood. Simmondsia (Bailey 1980, cells has long been recognized (Carlquist Carlquist 2002) and Stegnosperma (Carlquist 1962). Storying is evident in all cell types in 1999a) have uniseriate to triseriate rays, as well Bougainvillea. This is the action of increase in as a few wider rays (Fig. 2). The rays in both girth by the master cambium rather than the genera are paedomorphic in having a prepon­ vascular cambium. Attention should be drawn derance of upright cells, they are otherwise not to this phenomenon because accounts of unlike those of other dicotyledon woods (most storying in vascular plants are based on of which have Heterogeneous Type II rays of "normal*' vascular cambia rather than on Kribs, 1935), and thus are best interpreted as plants with successive cambia (e.g., Bailey symplesiomorphic for the centrospermoid 1923). Areas of fiberlike parenchyma in Caryophyllales. This contrasts, for example, Bougainvillea (Fig. 7, pb) and thin-walled to the raylessness that predominates in Aizoa- conjunctive tissue (ct) are distinguishable from ceae (Carlquist 2007). Both genera have ray areas. There is some division of labor in diffuse axial parenchyma (Carlquist 1999. parenchyma cells in Bougainvillea. Some have 2002). a primitive condition in dicotyledons thin secondary walls and contain starch (Kribs 1937). The majority of Caryophyllales (Fig. 5, upper left). have scanty vasicentric parenchyma (original data). These several wood symplesiomorphies Pisonia (Figs. 10. 11, 17) and Guapira (Figs. 12, 13) are genera of Nyctaginaceae

including periderm (top), showing two vascular increments that have formed recently from cortical parenchyma. Labels: ct = conjunctive tissue, ctp = conjunctive tissue parenchyma, cts = conjunctive tissue sclerenchyma, osx = origin of secondary xylem increment, pb = parenchyma band, pe = periderm, rs = ray sclereid. sp = secondary phloem, spf = secondary phloem fiber area, ssc = sclerilled secondary cortex, sx = secondary xylem, sxf = fibrous secondary xylem, sxp = secondary xylem parenchyma, v = vessel, arrow = vascular cambium, pointers = master cambium. Figs. 30, 32-33, scale in Fig. 2; Fig. 31, scale in Fig. 28. 322 JOURNAL OF THE TORREY BOTANICAL SOCIETY [Voi 1 34 that represent a greater degree of differentia­ conjunctive tissue fibers with production of tion, compared to Bougainvillea, between axial a relatively small number of secondary xylem and radial tissues. In these genera, there are no fibers is not a morphogenetic problem. The ray initials in the vascular cambia and thus no use of the term "fiber" here contains some rays in secondary xylem and secondary intentional vagueness. If fibers are formed phloem. Examination of the sections of from a vascular cambium, they should be Guupira (Figs. 12, 13) makes this especially termed libriform fibers if they have simple clear. Rays occur only in the background pits—as they do in Pisonia and allied genera. tissue of conjunctive tissue, which consists Because fibers formed from vascular cambia mostly of fibers. The arcs of thin-walled and from the master cambium are identical in parenchyma around the secondary phloem of Pisonia, there is no contrast that can be made, the vascular increments also contain rays and there is no reason why the term "fiber" (Fig. 13). but rays do not occur in the thin- should not be used. However, the terminolog­ walled parenchyma directly external to the ical consequences of shift in mode of ray origin secondary phloem. Distinctive rays may be and fiber origin in Nyctaginaceae have not seen in tangential sections (Fig. 11). No plant been noted by plant anatomists—who are anatomist would fail to recognize these as likely to neglect such minor problems. rays. The reader may note that the term The presence of arc-like zones of conjunc­ "vascular ray" is avoided here, and may not be tive tissue parenchyma in Guapira (Fig. 12; applicable because the rays do not originate Fig. 13. ctp) and Pisonia (Fig. 10, pet) repre­ from a vascular cambium. The distribution sents an interesting division of labor in and nature of the rays in Pisonia is not entirely conjunctive tissue. The arcs of parenchyma clear in the drawing of P. nigricans by contrast markedly with the Fibers. The walls Solereder (1899, 1908), and has not received are thin, and a few raphide idioblasts may be comment by other workers. Metcalfe and found in this tissue. The parenchyma cells do Chalk (1950) accurately describe the rays of not have intrusive growth, as do the fibers. Neea, Pisonia, and Torrubia without noticing The arcs of parenchyma are not part of the their distinctive distribution within the stems secondary phloem and do not contain any of these genera. The production of rays by sieve elements. The parenchyma arcs do a master cambium, which is the meristematic contain rays (but not opposite the strips of layer that drives increase in girth of the axis, vessels). The parenchyma arcs are derived and their absence in the vascular cambia from the master cambium, not from the shows a fascinating division of labor. vascular cambia. The observant reader will have noticed that An obvious corollary to the above is that in there are a few fibers in secondary xylem areas, Guapira and allied genera, the master cambi­ adjacent to vessels in these genera (Fig. 10), um extends in a cylinder around the stem, fibers identical to those in the "background" whereas the vascular cambia are tangentially fiber tissue. How can there be two sources for narrow strips. A single master cambium per fibers, with such precise and seamless co­ stem (or root) is active indefinitely in Guapira. ordination of production of the fibers from the Pisonia, etc., whereas the vascular cambia. two sources? The answer is that unlike the although they may produce secondary phloem master cambium in most species with fusiform for indefinite period of time, very likely cambia initials, the master cambium in Guu­ eventually cease functioning in older parts of pira (see points in Fig. 13) consists of narrow a stem or root. The production of vessels plus fusiform cells like those of the vascular a few fibers by vascular cambia is limited by cambia. Thus both master cambium and the fact that the vascular increments are vascular cambia have a template for pro­ encased in fibers. Although a vessel or two duction of fibers. In most species with may be added over time (see vascular in­ successive cambia, the cells of the master crement. Fig. 10. upper right), such additions cambium are tangentially wider than cells of are very minor. a vascular cambium, and production of The sequence of events hypothesized by vascular cambia from the master cambium Esau and Cheadle (1969) in Bougainvillca (a therefore involves anticlinal divisions (e.g.. single cambium giving off conjunctive tissue Fig. 15 above the letter d). Thus the co­ and secondary phloem externally, conjunctive ordination of simultaneous production of tissue and secondary xylem internally) is 2007] CARLQUIST: SUCCESSIVE CAMBIA 323 inapplicable to Guapira. Neea, Pisonia. and strips of vessels figured for Charpentiera of the Torrubia. Their proposed interpretation is. in Amaranthaceae (Carlquist 2003, his Figs. 23, fact, inapplicable to Bougainvillea. The condi­ 24). In Charpentiera. the radial vascular tion represented by Bougainvillea may be flanges are interconnected laterally by ray cells considered apomorphic to those in Phytolacca with lignified cell walls. or Stegnosperma in that near-raylessness is Amaranthaceae (including Chenopodia- being achieved in Bougainvillea. This is in line ceae) are like Nyctaginaceae in that some with the ray phylesis plan hypothesized earlier genera, such as Nototrichium (Fig. 9) and (Carlquist 2001. p. 188). Grayia are entirely rayless, whereas others Heimerlioderuiron of the Nyctaginaceae may have some wide ray areas (Lev-Yadun (Figs. 8, 14-16) has achieved complete ray- and Aloni. 1991). The conjunctive tissue of lessness, which is clearly an apomorphy as well Nototrichium (Fig. 9) could easily be confused as a form of permanent juvenilism. or with ray tissue in radial sections because paedomorphosis. The lack of rays can be horizontal subdivision of ray cells occurs. clearly seen in a tangential section of fibrous The master cambium of Nototrichium consists tissue (Fig. 8. fx). Derivatives of the master wholly of fusiform cells, as does that of cambium (pointers. Fig. 14) subdivide anti- Heimerliodendron. clinally, thereby creating narrow cells destined to become fibers. Subdivisions in the deriva­ Aizoaceae: diversification of conjunctive tis­ tives of the master cambium also lead to sue within a rayless clade. The structural mode fusiform cambial initials (Fig. 15 above the of alternating concentric rings of fibrous letter d) and to secondary phloem (Fig. 15, conjunctive tissue and parenchymatous con­ po). Early stages in maturation of fibers junctive tissue, and with localized strands of around vessels or vessel groups (Figs. 15, 16) xylem and phloem, as seen in Heimerlioden­ appear as islands or strands in a background dron, occurs in many Aizoaceae. This condi­ of undifferentiated cells. Strands of secondary tion is readily seen in Aptenia (Fig. 22). All of phloem are present radially outside of these the Aizoaceae illustrated in the present paper zones of vessels (Figs. 15. 16). but not at all are rayless, as are those figured earlier points opposite fibers (Fig. 14). In the mature (Carlquist 2007). As in Heimerliodendron. stems of Heimerliodendron. concentric rings of master cambium derivatives in Aizoaceae, at conjunctive tissue fibers (about seven to eight first tangentially wider (Fig. 21). subdivide to cells thick) alternate with cylinders of paren­ become much narrower tangentially (Fig. 22). chymatous conjunctive tissue fibers about four In stems of Trichodiadema. a master cambi­ or five cells thick. This situation has been um (Fig. 18, top) yields radial rows of excellently illustrated by Meylan and Butter- secondary cortical cells to the outside. In­ field (1978). wardly, it produces radial rows of parenchy­ A terminological question is presented by ma, some of which are raphide idioblasts the bands of conjunctive tissue fibers: Do (Fig. 18. cells with gray contents). Here and fibers originate from a vascular cambium or there, vascular increments are evident. These a master cambium in areas where no second­ vascular increments mostly have fiber strands ary phloem is evident (Fig. 14)? The answer is on their inner faces (Figs. 18-20). The radial that they are derived from the master cambi­ rows of vessels are not embedded in fibers, but um Vascular cambia are claimed here to be rather in axial parenchyma produced from the operative only where strands of secondary vascular cambium (Fig. 19). As more second­ phloem and vessels are evident. Thus, Hei­ ary phloem is added, earlier secondary phloem merliodendron (sometimes regarded as a species is crushed (Fig. 19). A small number of vessels of Pisonia) is really very similar to Pisonia, (with associated axial parenchyma) are added differing only in raylessness and in differenti­ by vascular cambia, although no fibers are ation of conjunctive tissue parenchyma into added. As with Pisonia. the master cambium concentric bands of fibers and parenchyma extends around the stem, whereas vascular rather than a background that consists almost cambia are, tangentially, narrow strips. The entirely of fibers. As shown by Meylan and vascular strands appear almost randomly Butterfield (1978. Fig. 198), radial chains of distributed (Fig. 18), so that the origin of vessels and associated fibers are produced as vascular cambia from the master cambia must radial flanges, much like the curious radial vary spatially through time. In a very small 324 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

number of fiber strands, no vessels or phloem derived from a master cambium. As in Pisonia. are present (Fig. 20). Just to the inside of the the master cambium consists of narrow cells. master cambium in Trichodiadema, fiber bands The only change in derivatives of these cells is are evident (Fig. 18). I am interpreting these, vertical (intrusive) elongation, no lateral sub­ and therefore the fiber strands elsewhere, as division is required as they mature into fibers. conjunctive tissue. Phloem is not associated There are a few thin-walled parenchyma cells with the fibers at all points in Trichodiadema, external to the secondary phloem in Stavneria nor are vessels. Thus, the stems of Trichodia­ (Fig. 26). Interestingly, the stem of Stavneria dema are similar to those of Heimerliodendron is thus identical to that of Pisonia in histolog­ in histology, except for the fact that the fibers ical patterns except for the absence of rays in strands do not extend tangentially for in­ Stavneria. Stavneria represents a maximum of definite distances around the stem. mechanical strength in stem structure in In Aptenia (Figs. 21-23). the master cambi­ Aizoaceae. Marlothistella a minimum. These um derivatives subdivide into more numerous patterns are best interpreted in terms of habit cell files as fibers, secondary xylem, and and ecophysiology (below). secondary phloem. The conjunctive tissue differentiates not as parenchyma and fiber Gnetum: parenchyma as a stem patterning de­ strands associated with secondary xylem, as in vice. Gnetum schwackeanum (Figs. 26-27) is Trichodiadema, but as alternating concentric typical of New World species of Gnetum bands of fibers and thin-walled parenchyma, (Carlquist 1996b) in having wide bands of as in Heimerliodendron. The strands of sec­ conjunctive tissues and wide rays. The patterns ondary xylem and phloem are formed on the of development in stems of these species abaxial faces of the fiber bands. As with suggest that a given master cambium may Heimerliodendron. the most obvious interpre­ not function indefinitely, but may be sup­ tation is that the there is a master cambium planted by a new master cambium formed by around the stem that produces conjunctive tangential divisions in parenchyma outside of tissue. The conjunctive tissue shows distinct the secondary phloem of the secondary patterns, and the vascular strands are pro­ phloem fibers (Fig. 27). This pattern is not duced by tangentially narrow bands of vascu­ markedly different from those of the families lar cambial cells. Heimerliodendron and Apte­ and genera considered before, because even in nia do show a specialized placement of vascular them, master cambia can sometimes cease cambia: always along the abaxial face of the functioning and can be supplanted by others. fiber bands, whereas vascular cambia are The idea that master cambia may be formed spatially scattered in Trichodiadema. more frequently in Gnetum is based on Marlothistella (Fig. 24) provides an example apparent disjunction in cell lineages involved of absence of mechanical tissue. A small in one or more bands of vascular increments. strand of fibers (fsx) is present in the trans­ Such a disjunction may be present between the action illustrated, but fiber strands are ex­ two vascular increments shown in Fig. 26, tremely infrequent in this plant. Vascular although identifying such a disjunction is not increments, looking like small vascular bun­ easy. These might merely be distinctive pro­ dles, are scattered widely throughout the ducts of a single master cambium over time. conjunctive tissue parenchyma background. More study of the meristematic action in stems A few raphide idioblasts (ri) are present in the of Gnetum is needed, but is hindered by the conjunctive tissue parenchyma. The stem of lack of availability of liquid-preserved material Marlothistella represents a maximization of and of workers interested in studying ontog­ parenchyma and a minimization of fibers and eny of successive cambia. Amazingly, the of vascular tissue. sections of G schwackeanum were derived Stavneria (Fig. 25) shows a pattern that from dried specimens, treated so that soft- contrasts markedly with that of Marlothistella. walled tissue would remain intact. In any case, Almost the entire conjunctive tissue consists the basic pattern in G schwackeanum is the of fibers. Vascular increments, like the one point at hand: strands of secondary xylem plus (arguably two close to each other) shown. Two fibers and secondary phloem (capped by chains of vessels can be seen in Fig. 25. As in fibers) are isolated from each other by thin- Pisonia, there is no difference between fibers walled ray parenchyma and conjunctive tissue derived from a vascular cambium and those parenchyma, a kind of cable construction. 2007] CARLQUIST: SUCCESSIVE CAMBIA 325

Parenchymatization in Gnetum africamon one condition to the other can be readily (Figs. 28-29) takes the form of rays, which achieved. become dilated as growth proceeds (Fig. 28). In any case, successive cambia clearly have The African species of Gnetum thus contrast occurred as apomorphies in some clades, so with the New World species by having several one must ask why they arise, why they do not long-lived cambia per stem (Carlquist and arise more often (or less frequently, for that Robinson 1995). As the rays dilate and the matter), and whether they all represent a single outer surface of the vascular tissue increases, plan. The first two questions relate to function the vascular cambium splits into fragments (analwed in the last section of this paper). Hie (Fig. 28. arrows), each of which may survive second question probably cannot be answered, and produce an ever-widening wedge of except for the speculation that successive vascular tissue. There are occasional bands cambial plans are modifications (from a sin­ of axial parenchyma in the fascicular xylem of gle-cambium plan) that are generally not easily G. africamon (Fig. 28). These bands, which achieved in genetic terms. But the third represent secondary xylem not conjunctive question can be answered affirmatively al­ tissue, are much less pronounced than are though one must take into account some very the conjunctive tissue parenchyma bands in G. diverse examples, and explain that diversity. schwackeanum. One can say that there are no Apparently there is a limited number of ways master cambia in G. africanum. However, in which vascular cambia can be formed and there is division in cortical parenchyma cells. included within the structural plan of a stem At infrequent intervals, new vascular cambia or root. arise as a group of cells, rather than a sheet, in Chrysanthemoides is a genus of calenduloid the cortical parenchyma (Fig. 29). As seen in Asteraceae. It was formerly considered a spe­ three dimensions, there are interconnections cies of Osteospermum. When it and its closest between the vascular increments, but such relatives are analyzed, all of the Calenduleae interconnections are not apparent in a single chosen (Nordenstam et al. 2006) prove to be transaction. basal to Chrysanthemoides. Thus, with Chry- Thus, the rapid increase in tangential extent anihemoides the only genus of Asteraceae in of the a cambium in G. africanum achieves which successive cambia are known to exist a broad wedge of vascular tissue, a mechanism (Adamson 1934, Carlquist 1966), successive at a polar opposite from the development of cambia are clearly an apomorphy in Aster­ a master cambium that extends around a stem aceae. Wood of all genera and species close to (or root) in a complete cylinder (G schwack- Chrysanthemoides (using the tree of Norden­ eanurri) or a series of interconnected arcs stam et al. 2006) has not been examined yet, {Bougainvi/lea), followed by production of but even if some of these prove to have vascular cambia. Gnetum africanum and rep­ successive cambia. the situation remains the resent different ontogenies, but both exemplify same. Fibers occur in secondary phloem the idea that more than one cambium—and (Fig. 30. spf) of Chrysanthemoides. Secondary thus successive cambia—are functioning in xylem. however, is like that of other Calendu­ a given stem at any particular time. leae (Carlquist 1966). The growth form of Chrysanthemoides may demonstrate an inter­ Chrysanthemoides and Chloanthaceae ( = esting correlation with presence of successive Dicrastylidaceae): examining apomorphies. cambia. A young plant of Chrysanthemoides Successive cambia have originated in about has a single terminal head, as though it were 15 clades. The numerous occurrences of an annual. Then, by lateral branching it can successive cambia in families of centrosper- become a large shrub or, if water is available, moid Caryophyllales suggest that in that a small tree. Thus, successive cambia may order, successive cambia might not be apo­ represent a mechanism for innovation of morphies- the number of reversions one must secondary growth in a non-woody lineage. hypothesize to explain the single-cambium A second family of dicotyledons suggests taxa as the primitive state may be fewer than a similar story. Chloanthaceae (= Dicrastyli­ the number of conversions from a single daceae), an Australian family of plants (some­ cambium to successive cambia in the centro- times subfamily Chloanthoideae of Verbena- spermoids. Perhaps the centrospermoids con­ ceae), have successive cambia (Carlquist 1981). tain a gene system in which switching from As in Chrysanthemoides, young plants in 326 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

Chloanthaceae have terminal inflorescences known: Avicennia (Studholme and Philipson and increase in size (some of them are shrubs 1996, Carlquist 2001) and Forchhammeria to 1 m or so) by lateral branching. Why pallida (Carlquist, original data). Most species Chryanthemoides and Chloanthaceae have de­ of Forchhammeria lack such sclereid bands. veloped successive cambia, rather than mere protracted secondary xylem production from Mendoncia (Acanthaceae) and other lianas: a single cambium, is an intriguing question. cambial fracture and parenchyma proliferation. Worth noting is that even if included in The portion of a Mendoncia gigas stem Verbenaceae, Chloanthaceae probably do not (Fig. 32) shown here is not unlike that figured form a sister group to Avicennia. which has earlier (Carlquist and Zona 1988, Fig. 29); it traditionally been thought to be close to or is. however, more extensive and includes most included within Verbenaceae. Recent results of a secondary xylem increment that began show that Avicennia is in the same clade of (center left) with a small number of cambial Acanthaceae that includes thunbergioids, to initials and then widened markedly. This which Mendoncia belongs (Schwarzbach and increment in that respect resembles the sec­ McDade 2002). The types of successive ondary xylem illustrated for Gnetum africanum cambial activity of chloanthoids, Mendoncia. (Fig. 28). The widening of the vascular in­ and Avicennia, respectively, are rather differ­ crement, achieved by increase in number of ent, and conceivably each of these instances of fusiform cambial initials and ray initials, successive cambial occurrence could represent frequently results in fragmentation of the an apomorphy. cambium (Fig. 32). Thus, the vascular in­ crement becomes lobed as seen in transection. Menispermaceae: cambial protraction; scler- From bands of parenchyma within the in­ eids. Successive cambia in Menispermaceae crement of secondary xylem (Fig. 32. pb), new (Carlquist 1996c) doubtless represent an apo­ parenchyma may develop. A single isolated morphy in the ranunculoid ("basal eudicot") vessel, with associated fibers (Fig. 32, top) is clade. Some Menispermaceae. such as Legno- associated with long files of parenchyma in phora moorei Miers, although woody, have two directions; this isolated strand does not only a single cambium as far as known, seem like a typical vascular increment. Xylary whereas others have numerous successive expansions are permitted by the compressibil­ cambia. Some vascular increments in Meni­ ity of older secondary phloem, which may be spermaceae can develop several centimeters of identified by scattered fibers (Fig. 32, spf; secondary xylem, but others are much thinner. Fig. 33, sp). What was not noted by Carlquist Unfortunately, these patterns and their poten­ and Zona (1988) is the innovation of new tial correlations can be clarified only when cambia in Mendoncia gigas. By definition these more extensive material is collected in the are successive cambia (Fig. 33). The radial field. Information on stems of Menisperma­ files of cells involved in the origin of vascular ceae has been derived almost exclusively from cambia. Fig. 33, suggest that limited portions xylarium material. We need liquid-preserved of master cambium activity may be involved. material from field-collected specimens. The However, origin of vascular cambia without improved histological results are less impor­ master cambial activity appears to be charac­ tant than the documentation of habit, size, etc. teristic of lianas such as Mendoncia and of the specimens. There is virtually no such Bauhinia. just as it is in Gnetum africanum. information on xylarium specimens, and thus we have no key to possible correlations between extent of secondary xylem within Ecophysiological Themes each vascular increment and other histological The majority of genera and species with features of stems as they might be related to successive cambia belong to the centrospermoid plant size and habit. clade of Caryophyllales. The growth forms and The tangential bands of sclerenchyma in habitats of these genera are so highly varied that AiHiniirta cocculus (Fig. 31) are considered correlations might not seem possible. However, here to be the last-matured cells of an individual genera offer possible interpretations. increment of conjunctive tissue between vas­ When one adds examples from outside of cular increments. Only a few other species with Caryophyllales, correlations become clearer. sclerenchyma bands in conjunctive tissue are Caryophyllales are used as a prime example 2007] CARLQUIST: SUCCESSIVE CAMBIA 327 here, after which comparisons from other (Pfeiffer 1926, Carlquist 1995). Labbe (1962) groups with successive eambia are added. reported this condition in Limoniastrum. Limonium. and Plumbago (Plumbaginaceae). Storage and Retrieval of Photosynthates A few genera in these two families have and Water. The alternation of vascular incre­ successive eambia in both roots and stems ments with parenchyma provided by the (Pfeiffer 1926. Labbe 1962). successive cambial mode of construction offers Dispersion of vascular tissue throughout an ideal histological plan for storage and storage organs does occur in plants that do not retrieval of photosynthates and water. The have successive eambia: examples from mono- roots of Beta (Artschwager 1926) and Mir­ cots (Dioscorea) and dicots (Ipomoea, Solanum) abilis (Mikesell and Popham 1976) have thin are familiar. The vascular plan of the typical cylindrical vascular increments spaced from monocotyledon needs no modification other each other by relatively wide zones of paren­ than increase in parenchyma amount to achieve chyma. Sugar is stored abundantly in roots of such a configuration. In dicotyledons with Beta, starch in those of Mirabilis. In both storage organs that do not have successive genera, more recent vascular increments lack eambia. diversification of bundle placement or vessels, although vessels do eventually differ­ vascular tissue placement within a stem or root entiate in earlier-formed vascular increments. (e.g., pith bundles) has achieved results similar This seems clearly correlated with adaptation to those than that can result from slight to photosynthate storage and retrieval rather alteration of the successive cambial template. than water storage. Some Aizoaceae. such as Mestoklema and Promotion of Mechanical Strength: a Para­ Trichodiadema, have thick tuberlike roots but digm for Prolonged Conductive Capabilities. relatively slender stems. The vascular incre­ Guapira, Neea, Pisonia, and Torrubia are ments are more widely spaced from each other tropical or subtropical nyctaginaceous trees. in stems of those two genera than they are All of these genera have slender vascular in roots (Carlquist 2007). Unlike Beta and increments embedded in a background of Mirabilis, Mestoklema and Trichodiadema fibers. This configuration suggests optimal have xylem as well as phloem in all increments. mechanical strength. Even the rays in these This seems to be correlated primarily with genera contribute to mechanical strength by storage of water in the underground struc­ having secondary walls and by being vertically tures, although small amounts of starch can be short and laterally narrow, so that they occupy observed in the roots. a small proportion of stem tissue. To be sure, Marlothistella is an interesting example of there are arcs of parenchyma around the adaptation by the successive cambial plan to phloem strands in these four genera, and these water storage in a stem. The stems of Mar­ arcs would represent a slight departure from lothistella are short and thick, and bear a plan of optimal mechanical strength. These numerous very short branches. The main stem parenchyma arcs could provide zones that is clearly succulent. The vascular increments could accommodate increased volume of are slender and sparsely distributed (resembling secondary phloem as it is produced outwardly vascular bundles) in a background tissue that from vascular eambia. The parenchyma arcs consists almost entirely of thin-walled paren­ are somewhat larger in Guapira than in chyma. The stem of Marlothistella represents Pisonia, but these arcs contain raphide idio- a version of the successive cambial plan in blasts that could afford protection from pre- which water storage is maximized and mechan­ dation of phloem. ical strength in minimized. The occurrence of Phloem in dicotyledons with a single cam­ similar configurations in roots (Beta, Mirabilis) bium mostly lasts only a single season. is not unexpected, because roots show minimal Functional phloem is represented in the new­ adaptations for mechanical strength. est bark tissue. This is matched by the tact An interesting confirmation of the suitabil­ that, as dye analyses show, only the current ity of the successive cambial plan for storage is year's accumulation of secondary xylem is found in genera of Caryophyllales that have functional (Braun 1970). However, in a tree a single cambium in the stem but successive such as Guapira, each of the numerous strands eambia in the root. This condition has been of secondary phloem, scattered throughout the reported for several genera of Caryophyllaceae stem (or root) is functional, as evidenced by 328 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134 the continued production of secondary phlo­ increase in mechanical strength as well as em in each of these vascular increments. A prolonging the activity of the vascular path­ logical corollary is that secondary xylem the ways formed earlier in the stem. Each of these vascular increments in which vascular cambia radial flanges is capped by secondary phloem, are continuing to form secondary phloem is formed for an indefinite period of time by each also functional. Thus, a much greater area of vascular cambium. the stem is potentially available for conduction Fahn and Schchori (1967) claim that phloem by secondary phloem and secondary xylem strands of Chenopodiaceae are long-lived. than in a dicotyledon with a single cambium. Presumably the basis for that statement could The consequences of prolonged conductive be found in continued production of secondary activity in the vascular increments are mani­ phloem by vascular cambia, a characteristic of fold. All of a stem's vascular increments are numerous species as noted above. This is true potentially conductive, especially in species o\~ the Californian desert shrub Grayia spinosa where water stress from drought or freezing of the Chenopodiaceae as well (original data). does not disable earlier-formed vessels. Cer­ The secondary xylem strands of Grayia spinosa tainly in Guapira and allies, the warm humid probably have considerable duration and re­ habitats without strong extremes in moisture sistance to embolism formation, because they availability make vessel embolism occurrences have not only narrow vessels, but vasicentric relatively unlikely. The capability for pro­ tracheids as well (Carlquist 1985). longed conductive activity of vessels, matched Some Aizoaceae, such as Aptenia, have ex­ as it is by continual production of secondary tended secondary xylem production from each phloem by vascular cambia means that pro­ vascular cambium, as noted above for Char- duction of large numbers of vessels, especially pentieraand Heinieriiorfendron. In Aptenia. very narrow ones that would have greater embo­ few Fibers are produced in this later-formed lism resistance (a phenomenon established by secondary xylem (Carlquist 2007). Thus, me­ Hargrave et al. 1994 in Salvia) is unnecessary. chanical strength is not increased, but xylem Indeed, the vessel density of Guapira and allied conductive area is either maintained or in­ genera is very low compared with vessel creased. This structural mode seems related to density in wood of dicotyledons with a single the flexibility of the sprawling stems of Aptenia. cambium. In turn, this permits a higher pro­ Interestingly. Stayneria o\' the Aizoaceae has portion of the stem tissue to be devoted to a stem anatomical plan virtually identical to mechanical tissue. This situation actually that of Pisonia. except that Stayneria lacks represents a maximum economy in use of rays. Stayneria even has small arcs of con­ photosynthates to produce wall material, junctive tissue parenchyma abaxial to phloem because fibers represent a kind of mechanical strands. Stayneria is a shrub larger than most strength superior to vessels: in vessels, me­ other Aizoaceae. and thus a structural mode chanical strength is present, but is much less that features mechanical strength is adaptive. than that of fibers. In a sampling of species The various anatomical plans above have with successive cambia. vessel density was obvious correlations with respect to mechan­ shown to be lower than in woody dicotyledons ical strength and longevity of conductive with a single cambium (Carlquist 1975). tissues in stems (and presumably roots, which The vascular cambia of Charpentiera are studied much less frequently than are (Amaranthaceae) produce not only radial stems). These distinctive plans have not been rows of vessels over a prolonged period, they studied by plant physiologists. Such study produce associated fibers as well, resulting in would reveal whether anatomical formulations the formation of radial flanges of vessels offer differences from those of single-cambium sheathed in fibers (Carlquist 2002. his Figs. species in their conductive and their mechan­ 22, 23). The occurrence of wide concentric ical characteristics. If successive cambial spe­ bands of conjunctive tissue parenchyma per­ cies were more common in dicotyledons at mits these additions of secondary xylem. large, they would doubtless have received such which intrude outwardly into the conjunctive study. The fact that successive cambial species tissue. This tendency can also be observed in are not sources of lumber does not make them older parts of HeimerHodendron stems. In both of less physiological interest, but it may be one of these genera, addition of fibers alongside reason why wood physiologists have studied vessels by the vascular cambium assures them so little. 2007] CARLQUIST: SUCCESSIVE CAMBIA 329

The Liana Syndrome: Flexibility and Fiber above with respect to three-dimensionaliza- Distributions That Protect Vessels. Lianas have tion, in which successive cambia are accom­ less mechanical tissue per unit transaction panied by other phenomena: rapid dilation of than self-supporting woody plants (Schenck vascular increments through tangential expan­ 1893. Carlquist 1991). They do have apprecia­ sion of cambia, fracturing of vascular cambia ble quantities of fibers in stems, however. into segments, production of axial parenchy­ Transections of lianas show that the fibers are ma bands, production of wide rays, and often disposed as sheaths of individual vessels proliferation of cells in the axial parenchyma or sheaths of a group of vessels often vessels and ray areas. The result of this syndrome of with relatively large diameter. Conferring interrelated ontogenetic changes is production mechanical strength that safeguards the in­ of anastomosing strands of wood varied with tegrity of water columns by preventing rup­ respect to transactional area and shape. One turing of vessels may be the primary function advantage where habit is concerned seems to of these vessel sheaths. Jacobsen et al. (2005) be mechanical flexibility, as hypothesized long find that presence of fibers around vessels ago by Schenck (1893) and experimentally contributes to cavitation resistance. demonstrated by Putz and Holbrook (1991). Successive cambial modes of structure make Stems of lianoid Bauhinia species, as well as possible various patterns of fiber disposition those of other lianas, frequently deviate from with respect to distributions of thin-walled a cylindrical form and often assume a flat­ parenchyma. Some of these predispose toward tened, bandlike form (Vieira 1994). The flexibility of stems simultaneously with sheath­ adaptation represented by this widened form ing of vessels. The centrosperm families may represent a conformation suited to Agdestidaceae (Carlquist 1999b) and Base- maximal surface contact with the surface of llaceae (Carlquist 1999c) are lianoid families the branch of the supporting tree. Such that satisfy that description, but in different a possibility is difficult to demonstrate exper­ ways. In Amaranthaceae, Bosea has thin- imentally. The multiplicity of ontogenetic walled parenchyma in ray areas as well as actions, which make a stem transaction of thin-walled conjunctive tissue between vascu­ a liana seem irregular with comparison to that lar increments (Solereder 1908. Metcalfe and of a self-supporting tree, may also be a more Chalk 1950). Bosea is a shrub that can become rapid way to achieve change in three-dimen­ markedly scandent (to 10 m). The fact that sional stem shape and achievement of the Charpentiera densiflora. also of Amarantha­ advantages of cable construction than would ceae, has lignified ray cells interconnecting eccentric growth of a single cambium. plates of fibrous secondary xylem (Carlquist Although not lianoid, the structure of 2003) correlates with the fact that Charpentiera sprawling stems in Aptenia. Carpohrotus, and densiflora is a tree, whereas Bosea is lianoid. Tetragonia is instructive. These plants have Soft (parenchymatous) conjunctive tissue be­ strong but very flexible stems that feature tween successive vascular increments offers concentric cylinder of alternating thin-walled flexibility, even to the point of tearing while and fibrous conjunctive tissue, with vessels vascular tissues remain intact. That this abaxial and secondary phloem on the abaxial happens has been shown experimentally by faces of the fiber cylinders (Carlquist 2007). Putz and Holbrook (1991) in Securidaca. Some of these genera grow on sand dunes or Bougainvillea offers wide ray areas, as well other places subject to soil level shift: Carpo­ as parenchymatous conjunctive tissue, that brotus is often planted in order to stabilize seem to correlate with potential flexibility of sand dunes. Another correlation of this kind this lianoid plant. The starch-rich nature of the of stem structure in Aizoaceae is with the parenchyma of rays and of conjunctive tissue, tendency of sprawling plants in this family to as well as the storage of starch in fibrous be able to bend toward the ground without tissue, suggests a distinctive function that can damage and thereby reroot. This strategy be related to its habit: rapid seasonal pro­ enlarges the plant without the expenditure duction of large inflorescences at tips of involved in mechanical strength production branches that reach the canopy or similarly such as one finds in a typical shrub. sunny sites. In all of the examples of lianoid or There are a number of lianas (Bauhinia sprawling plants cited above, one can consider offers the best known example), as mentioned the various anatomical plans to represent 330 JOURNAL OF THE TORREY BOTANICAL SOCIETY [VOL. 134

kinds of "cable construction," as opposed to the form of dried specimens (see papers cited in the rodlike or cylindrical structure we associ­ materials and methods) through the courtes) ate with dicotyledons that have a single of Regis Miller and Alex C. Wiedenhoeft of the cambium. In addition to combining flexibility U.S.D.A. Forest Products Laboratory. Madi­ with increased strength, cable construction son, Wisconsin. Thanks are extended to Dr. offers the potential advantage of redundancy. Bruce Kirchoff for his thoughtful reading of Because lianoid plants and sand dune plants the manuscript and his valuable editorial work. are subject to torsion, and thus to potential injury, ground plans that feature redundancy Literature Cited in conductive pathways and spatial separation ADAMSON, R. S. 1934. Anomalous secondary thick­ of those pathways are of especial value. ening in Compositae. Ann. Bot. 48: 505-514. Disposition of fibers as sheaths around vessels AR rsc HWAGER, E. 1926. Anatomy of the vegetative is a mechanism that helps safeguard water organs of the sugar beet. J. Agric. Res. 33: 143-176. columns from embolism formation. Successive BAILEY, D. C. 1980. Anomalous growth and cambial plans may prove to offer degrees of vegetative anatomy of Simmondsia chinensis. redundancy safety equal to if not greater than Am. J. Bot. 67: 147-161. those of woods of single-cambium species BAILEY, I. W. 1923. The cambium and its derivative tissues. IV. The increase in girth o\' the cambium. when comparable materials of each are studied Am. J. Bot. 10: 499-509. experimentally. Although successive cambia BAILEY, I. W. AND W. W. TUPPER. 1918. Size are represented by a relatively small number of variation in tracheary cells. I. A comparison species compared with the number of species between the secondary xylems of vascular with single cambia. the multiple origins of cryptogams, gymnosperms. and angiosperms. Proc. Am. Acad. Arts Sci. 54: 149-204. successive cambial plans within vascular BAIRD, M. V. AND W. H. BLACKWELL. 1980. plants—and the varied growth forms repre­ Secondary growth in the axis of Halogeton sented by successive cambial plants—provides ylomeratus (Bieb.) Meyer (Chenopodiaceae). a kind of circumstantial evidence of the Bot. Gaz. 141: 269-276. adaptational values of these plans. BARGHOORN. E. S. 1941. The ontogenetic develop­ ment and phylogenetic speci;ili/;ition of rays in The lesson provided by the many above the xylem of dicotyledons. II. Modification of examples that tend to show sensitive adapta­ multiseriate and uniseriate rays. Am. J. Bot. 26: tions to habit, ecology, and physiology is 273-276. BASSON. P. AND D. W. BIERHORST. 1967. An analysis obvious: they should be studied in those nl differential lateral growth in the stem of contexts. Too often, comparative studies in Bauhinia swtnamensis. Bull. Torrey Bot. Club 94: plant anatomy are limited to a description of 404-411. the histology of the group of species under BflAUN, H. J. 1970. Funktionelle Histologic der sekundaren Sprossachse. 1. Das Holz. Handbuch study and have recognition of diagnostic der Pflanzenanatomie 9(1): 1 190. Gebriider features as the sole goal. Potential structure- Borntraeger, Berlin. function correlations are all too frequently CARLQUIST, S. 1962. A theory of paedomorphosis in avoided, and thus comparative anatomy fails dicotyledonous woods. Phytomorphology 12: to provide questions worth answering. In the 30-45. CARLQUIST, S. 1966. Wood anatomy of Anthemi- case of plants with successive cambial struc­ deae, Ambrosieae, Calenduleae. and Arctotideae ture, the problems have been compounded (Compositae). Aliso 6: 1-23. because of the complexity of the histological CARLQUIST, S. 1970. Wood anatomy of insular patterns, their microtechnical difficulty, and species of Planiago and the problem of rayless- the strong desirability of liquid-preserved ness. Bull. Torrey Bot. Club 97: 353-361. CARLOLIST, S. 1975a. Wood anatomy of Onagra- material. Although these may be considered ceae. with notes on alternative modes of photo- reasons for avoiding study of successive synthate movement in dicotyledonous woods. cambial plants, they are precisely reasons Ann. Mo. Bot. Gard. 62: 386-424. why study of these plants offers so many CARLOLIST, S. 1975b. Ecological strategies of xylem evolution. University of California Press. Berke­ opportunities. ley and Los Angeles. CA. CARLQUIST. S. 1981. Wood anatomy of Chloanlha- Acknowledgements ceae (Dicrastylidaceae). Aliso 10: 19-34. Appreciation is expressed for the work of CARLQUIST, S. 1982. The use of ethylenediamine in softening hard plant structures for paraffin John Garvey in providing graphic design sectioning. Stain Technol. 57: 311-317. features for the illustrations. Some of the CARLQUIST, S. 1985. Vasicentric tracheids as specimens mentioned here were provided in a drought survival mechanism in the woody 2007] CARLQUIST: SUCCESSIVE CAMBIA 331

flora of southern California and similar regions; suggested by phylogenetic analyses of partial review of vasicentric tracheids. Aliso 11: 37-68. chloroplast DNA ORG280 homolog sequences. CARLQUIST, S. 1991. Anatomy of vine and liana Am. J. Bot. 84: 253-273. stems: a review and synthesis, p. 53-71. In F. E. DOWNIE. S. R. AND J. D. PALMER. 1994. A Putz and H. A. Mooney [eds.]. The biology of chloroplast DNA phylogeny of the Caryophyl­ vines. Cambridge University Press. Cambridge. lales based on structural and inverted repeat CARLQUIST. S. 1995. Wood anatomy o\' Caryophyl- restriction site variation. Syst. Bot. 19: 236- laceae: ecological, habital, systematic, and phy- 252. logenetic implications. Aliso 14: 1-17. ESAU. K. AND V. I. CHEADLE. 1969. Secondary CARLQUIST, S. 1996a. Wood. bark, and stem growth in Bougainvillea. Ann. Bot. 33: 807-819. anatomy of Gnetales: a summary. Int. J. Plant FAUN. A. AND Y. SCHCHORI. 1967. The organization Sci. 157(6 suppl.): S58-S76. of the secondary conducting tissues in some CARLQUIST, S. 1996b. Wood, bark and stem anato­ species of the Chenopodiaceae. Phytomorphol- my of New World species of Gnetum. Bot. J. ogy 17: 147-154. Linn. Soc. 120: 1-19. FAHN. A. AND M. H. ZIMMERMANN. 1982. De­ CARLQUIST, S. 1996C. Wood and stem anatomy of velopment of the successive cambia in A triplex Menispermaceae. Aliso 14: 155-170. halimus (Chenopodiaceae). Bot. Gaz. 143: CARLQUIST, S. 1999a. Wood and stem anatomy of 353-357. Stegnospcrma (Caryophyllales); phylogenetic re­ FISHER, J. B. AND F. W. EWERS. 1992. Xylem lationships: nature of lateral meristems and pathways in liana stems with variant secondary successive cambial activity. IAWA J. 20: growth. Bot. J. Linn. Soc. 108: 181-202. 149-163. GOTTWALD. H. AND N. PARAMESWARAN. 1968. Das CARLQUIST, S. 1999b. Wood anatomy of Agdestis sekundiire Xylem und die systematische Slellung (Caryophyllales): systematic position and nature der Ancistrocladaceae und Dioncophyllaceae. of the successive cambia. Aliso 18: 35-43. Bot. Jahrb. 85: 410-508. CARLQUIST. S. 1999C. Wood, stem and root anatomy GREGUSS, P. 1968. Xylotomy of the living cycads. of Basellaceae with relation to habit, systematics, Academiai Kiado, Budapest. and cambial variants. Flora 194: 1-12. HANDA. T. 1937. Anomalous secondary growth in CARLQUIST. S. 2000. Wood and stem anatomy of Bauhinia japonica Maxim. Jap. J. Bot. 9: 37-53. phytolaccoid and rivinoid Phytolaccaceae (Car­ yophyllales): ecology, systematics. nature of HARGRAVE. K. R.. K. KOLB, F. W. EWERS, AND S. D. successive cambia. Aliso 19: 13-19. DAVIS. 1994. Conduit diameter and drought- induced embolism in Salvia mellifera Greene CARLQUIST, S. 2001. Comparative wood anatomy. (1 abiatae). New Phytol. 126: 695-705. Edition 2. Springer Verlag. Berlin and Heidel­ berg. IAWA COMMITTEE. 1989. IAWA list of microscopic features for hardwood identification. IAWA J. CARLQUIST, S. 2002. Wood anatomy and successive cambia in Simmondsia (Simmondsiaceae): evi­ 10: 221-332. dence for inclusion in Caryophyllales s. 1. JACOBSEN. A.. F. W. EWERS, R. B. PRATT. W. A. Madrono 49: 158-164. PADDOCK III. AND S. D. DAVIS. 2005. Do xylem CARLQUIST, S. 2003. Wood and stem anatomy of fibers affect cavitation resistance? Plant Phys. woody Amaranthaceae s. s.: ecology, systematics 139: 546-556. and the problems of defining rays in dicotyle­ KlRCHOFF, B. K. AND A. FAHN. 1984. Initiation and dons. Bot. J. Linn. Soc. 143: 1-19. structure of the secondary vascular system in CARLQUIST, S. 2004. Lateral meristems, successive Phytolacca dioica (Phytolaccaceae). Can. J. Bot. cambia and their products: a reinterpretation 62: 2580-2586. based on roots and stems of Nyctaginaceae. Bot. KRIBS. D. A. 1935. Salient lines of structural J. Linn. Soc. 146: 129-143. specialization in the wood ravs of dicotyledons. CARLQUIST, S. 2007. Successive cambia in Aizoaceae: Bot. Gaz. 96: 547-557. products and process. Bot. J. Linn. Soc. 154: KRIBS. D. A. 1937. Salient lines of structural 141-155. specialization in the wood parenchyma of CARLQUIST. S. AND A. A. ROBINSON. 1995. Wood and dicotyledons. Bull. Torrey Bot. Club 64: 177- bark anatomv of the African species of Gnetum. 187. Bot. J. Linn. Soc. 118: 123-137. L.ABBI:. A. 1962. Les plombagjnacees. Structure, CARLQUIST, S. AND S. ZONA. 1988. Wood anatomy of developpement. repartition, consequences en Acanthaceae: a survey. Aliso 12: 201-227. systematique. Thesis. Grenoble. COCKRELL, R. A. 1941. A comparative study of the LEV-YADUN, S. AND R. ALONI. 1991. Polycentric wood of several south American species of vascular rays in Suaeda monoica and the control Strychnos. Am. J. Bot. 28: 32^1. of ray initiation and spacing. Trees 5: 22-29. COSTEA. M. AND D. DEMASON. 2001. Stem morphol­ M.ACHADO. R. D.. A. MATTOS FILHO, AND J. M. B. ogy and anatomy in Amaranthus L. (Amarantha­ DE PEREIRA. 1966. Estrutura microscopica e ceae)—taxonomic significance. J. Torrev Bot. submicroscopica de madeira de Bauhinia for- Soc. 128: 254-281. flcata Link. (Leguminosae: Caesalpinoideae). DE BARY, A. 1884. Comparative anatomy of the Rodriguesia 25: 313-334. vegetative organs of phanerogams and ferns. MENNEGA. A. 1980. Anatomy of the secondary Clarendon Press, Oxford. xylem, p. 112-161. In A. J. M. Leeuwenberg DOWNIE. S. R.. D. S. KATZ-DOWNIE, AND K.-J. CHO. [ed.]. Angiospermae: Ordnung Gentianales fam. 1997. Relationship in the Caryophyllales as Logtaniaceae. Die natiirlichen Pflanzenfamilien. 332 JOURNAL OF THE TORREY BOTANICAL SOCIETY [Voi. 134

second edition, vol. 28b(l). Ducnker and Hum- su relacion con la filotaxis. Acta Bot. Venezue- blot. Berlin. lana 12: 23-77. METCALFE, C. R. AND L. CHALK. 1950. Anatomy of SCHENCK, H. 1893. Beitriige zur Biologic und the dicotyledons. Clarendon Press. Oxford. Anatomie der Lianen. II. Schimpers Biol. Mit- MEYLAN, B. A. AND B. G. BLTTERFIELD. 1978. The theil. Trop. 5: 1-271. structure of New Zealand woods. DSIR Buill. St mvARZBACH, A. AND L. A. MCDADE. 2002. 122: 1 120. N. Z. DSIR. Wellington. Phyiogenetic relationships of the mangrove Miki si i I . J. E. AND R. H. POPHAM. 1976. Ontogeny family Avicenniaceae based on chloroplast and and correlative relationship of the primary nuclear ribosomal DNA sequences. Syst. Bot. 27: thickening meristem in four-o'clock plants (Nyc- 84-98. taginaceae) maintained under long and short SOLEREDER, H. 1899. Systematischen Anatomie der photoperiods. Am. J. Bot. 63: 427-437. Dikotyledonen. F. Enke. Stuttgart. SOLEREDER, H. 1908. Systematic anatomy of the NORDENSTAM. B.. M. KALLERSJ6, AND P. ELDENAS. 2006. Nephrotheca, a new monotypic genus of the dicotyledons (trans, by L. A. Boodle and F. E. Compositae-Calenduleae from the southwestern Fritsch). Clarendon Press, Oxford. UK. Cape Province. Compositae Newsletter 44: STEVENSON, D. W. AND R. A. POPHAM. 1973. 32-37. Ontogeny of the primary thickening meristem I'I i II i ER. H. 1926. Das abnorme Dickenwachstum. in seedlings of Bougainvillea spectabilis. Am. J. Bot. 60: 1 9. Handbuch der Pflanzenanatomie 9(2): 1-272. STUDHOLME, W. P. AND W. R. PHILIPSON. 1966. A Gebriider Borntraeger. Berlin. FRG. comparison of the cambium in two woods with PUTZ, F. E. AND M. HOLBROOK. 1991. Biomechanical included phloem: Heimerliodendron brtmonianum studies of vines, p. 73-97. In F. E. Putz and H. A. and Avicenma resinifera. N. Z. J. Bot. 4: 355-365. Mooney [eds.]. The biology of vines. Cambridge VANVLIET. G. J. C. M. 1979. Wood anatomy of the University Press. Cambridge. LIK. Combretaceae. Blumea 25: 141-223. RODMAN. J.. M. K. OLIVER. R. R. NAKAMIRA, J. U. VIEIRA, R. C. 1994. Estrutura do caule de Bauhinia MCCLAMMER JR. AND A. H. BLEDSOE. 1984. A radiate Veil, em diferentes ambientes. Rev. Bras. taxonomic analysis and revised classification of Biol. 54: 293-310. Centrospermae. Syst. Bot. 9: 297-323. WAGNER, J. A. 1946. Notes on the anomalous stem ROTH, L. AND J. ASCENSIO. 1977. Crecimiento structure of species of Bauhinia. Am. Midi. Nat. anomalo del eje de varias especies de Bauhinia y 36: 251-256.