Flora (1999) 194 1—12

© by Urban & Fischer Verlag Wood, stem, and anatomy of with relation to habit, systematics, and cambial variants

SHERWIN CARLQuIsT

Santa Barbara Botanic Garden, 1212 Mission Canyon Road, Santa Barbara, California 93105 U.S.A.

Accepted: June 24, 1997

Summary

Wood data from wider stem, root, and root-stem transition of a mature of baselloides are analyzed for quantita tive and qualitative features. Distinctive characters of A. baselloides include presence of successive cambia in wider stem, root, and root-stem transition; other types of cambial variants are newly reported for the family. Systematic distribution of successive cambia in does not parallel cladistic schemes for the order, and possible reasons are advanced. Wood features other than successive cambia are compatible with relationship to the other families of Portulacinae (Cactaceae, Didiereaceae, Hectorellacaeae, Portulacaeae) except for features related to habit, particularly the scandent habit. These features (mostly newly reported for Basellaceae) include restriction of vessels to central portions of fascicular areas (vessels thereby likely protected from torsion); some vessels wide but many narrow; all ray cells and ray-adjacent axial parenchyma with thin walls; (inter xylary) phloem strands in ray-adjacent axial parenchyma (with cambia that augment the phloem strands); and intraxylary phloem. Tubers contain pith phloem strands adjacent to which cambia produce secondary xylem and phloem. Druses and mucilage cells in cortex and rays and storying in axial xylem cells are newly reported for Basellaceae.

Key words: “Anomalous” secondary growth, cambial variants, Caryophyllales, Centrospermae, , successive cambia.

1. Introduction TH0RNE 1994, NowicKE 1994, 1996), which is usually construed as containing Cactaceae, Didiereaceae, Hec The family Basellaceae (4 genera, 40 species: CR0N- torellaceae, and Portulacaceae. R0DMAN et al. (1984) QUIST & TH0RNE 1994) is of special interest within and R0DMAN (1994) made a case for inclusion of Aizo Caryophyllales in a number of respects. All species are aceae in the same dade as the families of Portulacineae vining or lianoid, a habit relatively unusual in the order, (but see MANHART & RETTIG 1994). although found in agdestoid and petiverioid Phytolacca Cactaceae, Didiereaceae, Hectorellaceae, and Portu ceae, Bosea (Amaranthaceae), Bougainvillea (Nycta lacaceae lack successive cambia (METcALFE & CHALK ginaceae), and a few species of pereskioid cacti. The 1950, RAuH & DITTMAR 1970, GIBsoN 1994, CARL family is also distinctive in its tubers, which are not like QUIST 1998). Anredera baselloides (H. B. K.) BAILL0N, stems elsewhere in Caryophyllales. The stems, , rubra L., and tuberosus CALDA5 of and tubers are capable of indefinite longevity in some the Basellaceae were reported to have successive species, such as the one studied here, Anredera basello cambia (M0R0T 1884, PFEIFFER 1926), and successive ides, for which an unusually mature specimen was avail cambia are mentioned for the family by PANIKKAR & able. Numerous anatomical characteristics of wood, BHAMBIE (1974); more recent authors have not men stems, and roots are reported for the first time because tioned these reports. In addition, cambial variants other of the excellence of this material. Only stems of limited than successive cambia are present in A. baselloides diameter were available to METcALFE & CHALK (1950) and are described below. The distribution of successive and GIBsoN (1994). cambia in Caryophyllales is of considerable potential The likelihood that wood anatomy is strongly in phyletic significance: about half of the families and fluenced by the scandent habit of Basellaceae provides genera of the order have successive cambia, but the problems in systematic interpretation in wood anatomy. systematic distribution of these taxa does not cor Basellaceae have been placed in the suborder Portulaci respond in a parsimonious fashion with the position of neae (TH0RNE 1992, BEHNKE 1994, CR0NQuIsT & these taxa in cladograms. Therefore, successive cambia

0367-2530/99/194/01-001 $ 12.00/0 FLORA (1999) 194 1 present a curious situation in the interpretation of phy The mature specimen that forms the basis for the descrip lesis of Caryophyllales. Genetic, developmental, and tions below is clearly referable to Anredera base//aides functional nature of successive cambia in the order are = Boussingaultia base//aides H. B. K. and Anredera scandens in need of elucidation, and Basellaceae are central to (L.) M0Q.j. This plant was supplied to me by STEVE MoRGAN analysis of these questions. In Caryophyllales, succes (Botanic Garden, University of California at Riverside), it was probably at least 40 years old, and had been cultivated at a sive cambia can be found in succulent roots (Caryo residence in La Verne, California. The portions designated as phyllaceae, Chenopodiaceae, Nyctaginaceae: PFEIFFER “upper Stems” were not twigs but upper portions of the main 1926, METcALFE & CHALK 1950) as well as lianoid stem, about 2 cm in diameter. The root-stem transition features stems (Nyctaginaceae: EsAu & CHEADLE 1969) or in a swollen form, wider than the stem above this region and stems subshrubs (Halophyttim: GIBsoN 1978) or trees aboLit 10cm in diameter. The root selected for sectioning was (: WHEAT 1977, MIKEsELL 1979), so a portion of the main root about 5 cm in diameter. The tubers factors other than habit must be involved. Caryophylla are potato-like branches from the main stem at ground level, les in general, and Basellaceae in particular, are keys to and were about 3 cm in diameter in the plant studied. Stem and understanding of structure, functional significance, and root materials of relatively large specimens identified as Bous phylogenetic nature of successive cambia in vascular singaultia cordiftlia TEN0RE and B. gracilis MIERs were . available through the courtesy of the Los Angeles State and CountryArboretum, Arcadia, California. ULBRIcH (1934) con The materials studied here may all belong to a single cluded that these two taxa are conspecific with A. base//aides. species, A. haselloides (H. B. K.) BAILLON (see below). However, SPERLIN (1987) found that both B. cordij1ia and This is not regarded a limitation as to the present study, B . grad/is belong to a species separate from A. base//aides, the purpose of which is to establish the presence of par and that this species should be called Anredera cordi/ia ticular histological features father than to explore diver (TEN0RE) STEENIs. No anatomical differences (except those sity within the family. Anredera haselloides, however, due to dif-ferent degrees of maturity) were observed among may attain a large size than other species in the family, the col-lections studied here, so all are referred to A. hasel and thus may represent the nature of wood and cambial bides in accordance with ULBRIcH (1934). activity and other histological features in stems and Terms are according to the IAWA Committee on Nomen clature (1964). The term “vessel restriction pattern” roots better than immature material of other species. (CARL QUI5T 1983, 1988, CARLQuIsT & ZONA l988a) refers to pre New data on Basellaceae are important because a series sence of vessels in the central portions of fascicular areas, with of studies on Caryophyllales is in progress, and more libriform fibers adjacent to rays. In determining number of data on character states of these families are needed to vessels per mm2 of transection, ray areas were excluded from develop concepts of evolution of anatomical conditions the portions surveyed here. Had rays been included, the figu in the order. Data on Didiereaceae (RAuH & DITTMAR res for vessels per mm2 would have been much lower, especi 1970) and Cactaceae (several papers by GIBsON, see ally in tubers. Number of vessels per group is calculated as a GIBsoN 1994) have been contributed by others. The pre solitary vessel = 1.0, a pair of vessels in contact = 2.0, etc.; sent series includes a study of Caryophyllaceae (CARL however, the narrow vessels adjacent to wide vessels are so numerous that number of vessels cannot be accurately calcu QUIST 1995) and Portulacaceae (CARLQuIsT 1998), as lated. Vessel lumen diameter is measured an average well as a study of a family considered an outgroup of as be tween wide and narrow axes of a vessel lumen as seen in trans Caryophyllales, Plumbaginaceae (CARLQuIsT B0GGS & ection in order to present a more accurate image of the rheo 1996). logical capabilities of vessels. Both wide and narrow vessels were included in the means, although the two categories were also studied separately with respect to vessel element length. 2. Materials and methods Figs. 1—4. Photographs of sections of stem of Anredera base! All specimens were fixed in 50% aqueous ethanol; stems boides. 1—2. Transections. I. Section to show formation of a and roots of Basellaceae are too succulent for drying to be a second increment of vascular tissue (above) by a cambium feasible means of preservation. Liquid preservation is ad formed in the cortex; vascular tissue formed by the first cam vantageous in fixing thin-walled cells such as mucilage cells, bium below (sp = secondary phloem, sx = secondary xylem). phloem, and parenchyma, whereas woody dicotyledons have 2. Vascular tissue formed by cambium that originated in the wood that often consists wholly of cells with rigid lignified stem cortex; thin-walled axial parenchyma partially subdivi walls. Sections were prepared using the schedule of CARL des the fibrous portions of the secondary xylem. 3. Tangential QUIST (1982), in which ethylene diamine is employed as a sof section to show histology of fascicular area and ray portion tening agent prior to paraffin sectioning. Wide vessels and (dr = druse, lf= libriform fiber, mc = mucilage cell, wv = wider fibrous tissue embedded in a background of thin-walled tissue vessel). 4. Vessel wall from tangential section; grooves inter cannot be satisfactorily sectioned on a sliding microtome. Sec connect pit apertures (above). Fig. 1, scale above fig. 1 (finest tions were stained with a safranin-fast green combination. divsions= lOftm); Fig.2, scale above Fig.2 (divisions Macerations of secondary xylem were prepared with Jeffrey’s = l0l.tm); Fig.3, scale above Fig. 3 (divisions= bum); solution and stained with safranin. Fig.4, scale above Fig.4 (divisions = lOum).

2 FLORA (1999)194 Iii I liii Iii I I Ii I I I I

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FLORA (1999) 194 3 The term “pseudoscalariform” refers to lateral wall pits of ves ly square as seen in radial section, less commonly sels in which the pit is laterally elongate, like a scalariform pit upright or procumbent. Mucilage cells and cells bearing but derived from an alternate pattern (whereas ends of scalari a single druse each present in rays (Fig. 3). Vague story form pits are aligned to wall angles). All quantitative data are ing present in vessels, axial parenchyma, and libriform derived from products of the first cambium. fibers; storying clear in sieve-tube elements. Stem cor tex with scattered druse-bearing idioblasts and scattered 3. Anatomical descriptions idioblastic sclereids or sclereid nests. Sclerenchyma very rare in secondary phloem; and only present in older The anatomy of the upper stem (2 cm diameter) is secondary phloem. Sclerenchyma absent in periderm. described completely; the root and the root-stem transi Root (Figs. 5, 6). Vascular tissue produced by a tion descriptions omit items in which structural condi second (successive) cambium portions present in cortex, tions are identical to those of the upper stem. Illustra but the vascular tissue produced by them mostly orien tions prepared from the root and for the root-stem tran ted tangentially rather than radially. Vessel restriction sition are however, cited under those categories. present (Fig. 5, 6). Mean number of vessels per group, Upper stem (Figs. 1—4). Successive cambia present, > 15. Mean vessel diameter, 36 tm. Mean number of products of a second cambium observable in the mate vessels per mm2, 301. Mean vessel element length, rial available (Figs. 1, 2). Accumulation of secondary 206 tm; mean length of wider vessel elements, 173 tm; xylem and phloem much less than that produced by the mean length of narrower vessel elements, 243 tm. first cambium, but orientation similar. Intraxylary Mean wall thickness of vessels ranging from 2.6 tm phloem present adjacent to pith. Growth rings absent. (narrower vessels) to 7.5 tm (wider vessels). Lateral Mean number of vessels per group, > 15. Vessels dimor wall pitting commonly composed of pits circular, poly phic in diameter, the narrow vessels located mainly in gonal, or oval in outline, about 12 tm in diameter; radial strips interconnecting the groupings of wider ves pseudoscalariform pitting common in wider vessels. sels. The portions of fascicular areas adjacent to rays are Mean length of libriform fibers, 500 tm. Mean wall composed of libriform fibers and strips of thin-walled thickness of libriform fibers, 5.0 tm. Thin-walled axial axial parenchyma; the libriform fibers and thin-walled parenchyma adjacent to the rays appearing as indenta axial parenchyma may be described as ray-adjacent, tions in the fibrous margins of the fascicular areas therefore. Mean vessel diameter, 31 tm. Mean number (Fig. 5, upper right; Fig. 6, upper right). If fascicular of vessels per mm2, 251. Mean vessel element length, areas are narrow, thin-walled axial parenchyma may 221 tm; mean length of wide vessels, 182 tm; mean interrupt radial continuity of the radial bands of fibrous length of narrow vessels, 264 tm. Mean thickness of tissue (Fig. 5, left of center). Ray-adjacent axial paren vessel wall, 2.2 to 7.2 tm (wider vessels are thicker wal chyma frequently with phloem strands (Fig. 6, “rp”). led). All vessels with simple perforation plates. Lateral Rays (other than those that are extensions of primary wall pitting composed mostly of oval pits (Fig. 4), the rays) originate in an abrupt fashion, rather than as uni axial diameter of which is about 12 tm. Grooves inter senate or biseriate rays that widen. Mean width of rays, connect some pit apertures (Fig. 4, above), and some 6.0 cells. Ray cells most commonly upright or sqare, pits are quite elongate laterally (pseudoscalariform), less commonly procumbent.Occasional mucilage cells especially on the wider vessels. All imperforate trache and occasional sclereids or sclereid nests in cortex, pen ary elements are libriform fibers with minute slitlike derm free from sclerenchyma. simple pits. Mean length of libriform fibers, 405 tm. Root-Stem Transition (Figs. 7—13). Vascular strands Mean wall thickness of libriform fibers, 2.8 tm. Axial produced from the second cambium oriented either radi parenchyma present as scanty vasicentric cells with ally or tangentially. Growth rings absent (Fig. 7). Divi lignified walls formed in strands of two cells. Axial parenchyma also present as thin-walled cells adjacent to rays; in transection, these parenchyma zones appear as Figs. 5—8. Transections of secondary xylem of root (5—6) and indentations in the outlines of the fibrous fascicular root-stem transition (7—8) of Anredera baselloides. 5. Varied xylem (Fig. 2, bottom; see also Fig. 7, lower right). Ray- widths of fascicular areas; one near left appears discontinu adjacent axial parenchyma in strands of two cells or not ous because fibrous strands alternate with axial parenchyma, subdivided; a few strands subdivided into strands of 6. Two strands of ray-adjacent interxylary phloem (rp). 7. Fas cicular area four or more cells each of which contains a druse also in which abrupt origin of a multiseriate ray (above) has occurred. Section to show that libriform fibers (II) present in the ray-adjacent axial parenchyma. Phloem are adjacent to a ray, whereas narrow vessels (nv) lie in the strands present within some of the ray-adjacent axial central portion of a fascicular area, between wider vessels; parenchyma. Rays multiseriate only, mean width = 7.8 a strand of ray-adjacent phloem (light gray) is located above cells. Mean ray heigth >500 tim. Rays composed of the strand of libriform fibers. Fig. 5, 7, scale above Fig. 2; thin-walled nonlignified cells. Ray cells most common- Fig. 6, 8, scale above Fig. 3.

4 FLORA (1999) 194 —- _f1)--

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FLORA (1999) 194 5 .1j

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a. sions in parenchyma result in breakage and displace mm2, 247. Mean vessel element length, 218 tm; mean ment of fascicular areas (Fig. 10). Vessels dimorphic in length of narrower vessel elements, 265 tm; mean Diameter (Figs. 7, 8), the narrower vessels forming radi length of wider vessel elements, 187 tm. Vessel wall al chains interconnecting the larger vessels. Number of thickness ranging from 2.4 tm for narrower vessels to vessels per group, > 15. Mean diameter of vessels, 7.2 tm for wider vessels. Lateral wall pits of vessels 38 tm. Mean length of vessel elements, 184 tm; length oval in outline, 10 tm in axial diameter. Mean length of of wider vessel elements, 147 tm; length of narrower libriform fibers, 480 tm. Mean wall thickness of libri vessel elements, 208 tim. Lateral wall pits of vessels form fibers, 2.2 tm. Libriform fibers present in some circular, about 12 im in axial diameter with grooves secondary xylem, but relatively scarce compared with interconnecting pit apertures; pits laterally elongate other parts of the plant. Axial parenchyma pervasive, (pseudoscalariform) in some wider vessels (Fig. 12). present almost to the exclusion of libriform fibers Mean length of libriform fibers, 451 tm. Mean wall (Fig. 14). Axial parenchyma commonly not subdivided, thickness of libriform fibers, 2.8 tm. Thin-walled axial occasionally in strands of two cells, composed of thin- parenchyma adjacent to rays in strands separated from walled cells. Upright, square and procumbent cells each other by libriform fibers (Fig. 7—9). Thin-walled about equally abundant. Mean height of multiseriate axial parenchyma cells in strands of one or two cells rays, > 1 500 tm. Mean width of rays, 12 cells. Cortex (Fig. 11). Phloem present in some of the ray-adjacent with druse-containing idioblasts and mucilage idio parenchyma strands (Fig. 8, 9, 12). Cambial activity that blasts, but sclerenchyma lacking. Strands of vascular produces secondary phloem developing between libri tissue scattered throughout pith. Pith vascular tissue form fibers and the phloem strands (Fig. 9, “c”). Rays mostly composed of phloem (Figs. 15, 16). A cambium composed of procumbent, square, and upright cells in (Fig. 15, “c”) develops adjacent to these phloem strands about equal numbers. and adds secondary phloem to all of the strands and Multiseriate ray height, >500 tm. Mean width of secondary xylem to many of the strands (without xylem: multiseriate rays, 7.8 cells. Storying present in ray-adja Fig. 15; with xylem and phloem, Fig. 16). Topology of cent axial parenchyma (Fig. 11), some libriform fibers, the cambium varies in these pith strands from nearly flat phloem within ray-adjacent axial parenchyma (Fig. 12, and arclike (Fig. 15) to near-cylindrical (Fig. 16). left), narrow and wide vessels and vasicentric axial parenchyma (Fig. 12, right). Sclereids in older parts of secondary phloem only, appearing to be sclereids 4. Conclusions derived from phloem parenchyma, not phloem fibers. Intraxylary phloem present adjacent to the crushed pith, 4.1. Habit but no cambial activity adjacent to phloem strands observed (Fig. 13). Characteristics of wood anatomy of lianas and Tubers (Figs. 14—16). No cambium present in cortex, (as contrasted with that of trees) include presence of not and therefore no vascular tissue outside of the main ably wide vessels; dimorphism in diameter of ves cylinder. Only a single cylinder of bundles present, no sels; fibrous axial xylem relatively small in volume successive cambia observed. Secondary growth much compared to vessel elements; abundant axial paren greater in fascicular areas of the cylinder of bundles; chyma; and wide, tall rays (CAREQuIsT 1975, 1985). interfascicular cambium relatively inactive (Fig. 14, Although successive cambia certainly occur widely in “ic”). Mean number of vessels per group, > 15. Mean non-lianoid plants, they are relatively more common vessel diameter, 32 tm. Mean number of vessels per than “normal” (single) cambia in lianoid plants (CARL QuIsT 1985). This is illustrated clearly in Gnetales, in Figs. 9—12. Sections from root-stem transition region of An which all of the lianoid species have successive cambia redera baselloides. 9—10. Transections. 9. Fascicular area to (although one non-lianoid species, Welwitschia mirabi show wide vessels (upper right and lower left) interconnected us HooK. f., also has successive cambia). Anredera by narrow vessels; libriform fibers also present; ray-adjacent baselloides agrees with all of these characteristics, interxylary phloem strands at upper left and lower right with although in distinctive ways. For example, a sample of origin of a cambium (c) adjacent to one of these. 10. Fascicu vines and lianas (CARLQuIsT 1975, 206) showed a lar area broken and displaced by differential growth in ray p. mean vessel diameter of 157 tm; non-lianoid dicotyle parenchyma. 11—12. Tangential sections. 11. Section through dons with thin-walled ray-adjacent axial parenchyma, showing storied successive cambia had a mean vessel dia condition; some parenchyma cells in strands of two. 12. Sec meter of 68 tm. Anredera baselloides has a mean vessel tion through strand ray-adjacent interxylary phloem (sieve diameter less than either of these: from 31 tm in stems plates indicate storied nature of sieve-tube elements), narrow to 36 im in roots. The photographs suggest that vessels vessels (nv) and portions of a wide vessel (upper right). Fig. 9, are wider than 36 urn on average (Figs. 1, 5, 7, 13), but 11, 12, scale above Fig.3;Fig. 10, scale above Fig. I. the fact that there are numerous vessels is not so evident

FLORA (1999) 194 7 — I,: — ‘I

C at low as at high power (Fig. 8). Because both wide and The vessels of A. baselloides are far more numerous narrow vessels are present, one can say that vessels are per mm2 (246—301) of transection than in most lianas dimorphic (the wide vessels are shorter, another criteri because they are narrow and in much larger groups com on for dimorphism). If frequency were plotted against pared to the lianas sampled by CARLQuIsT (1975), either vessel diameter or vessel element length, a bi which average 19.1 per mm2. The high number in modal curve would not be obtained: narrow vessels are A. baselloides would be lowered had rays and conjunc numerous and would form a spike on a curve, but wide tive tissue been included in the areas sampled, but the vessels are relative few, and would create an attenuation number would be halved, at most. of the curve. The wide range of diameters is unusual Another distinctive feature of some lianas shared by except for instances of marked ring porosity (e.g., deci A. baselloides is the abrupt origin of wide rays. This duous species of Quercus). Narrow vessels (in addition phenomenon was illustrated in Aristolochia (CARL to wide ones) are not uncommon in lianas, and may con QUIST 1993). fer conductive safety (CARLQuIsT 1985). In more ‘typical’ woody species, procumbent cells Vessel elements do not elongate appreciably after are much more abundant than upright or square cells in derivation from fusiform cambial initials. The narrow later-formed wood. In A. baselloides, procumbent cells vessels of A. baselloides may elongate during matura are relatively less abundant, upright cells more ab tion, but probably not to a marked extent because greater undant. This ray histology often characterizes phylads in elongation of tracheary elements would likely create a which the ancestors were less woody (CARLQuIsT nonstoried appearance, but the tracheary elements of the 1988). species are storied (Fig. 12). The storied pattern of sieve In general, cambial variants are comparatively more tube elements (Fig. 12) is a little less evident than that of common in lianas and vines than in arboreal dicotyle vessel elements or axial parenchyma (Fig. 11). dons. The presence of successive cambia in Basellaceae Vessel restriction patterns, with libriform fibers adja might represent an adaptation to the habit rather than an cent to rays but vessels in the central portions of fasci indicator of phylogenetic relationship. However, one cular areas as seen in transection, were described in must take into account that there are several types of Valerianaceae (CARLQuIsT 1983), several Papaveraceae cambial variants other than successive cambia in Basel (CARLQuIsT & Z0NA 1988 a) and Launea of the Astera laceae. ceae (CARLQuIsT 1988). More significantly, several Intraxylary phloem (phloem adjacent to bundles, at types of vessel restriction can be seen in families that the periphery of the pith) is present in A. baselloides contain lianas, such as Convolvulaceae (CARLQuIsT & (VAN TIEiHEM 1891). However, no cambial action re HANSON 1991), Icacinaceae (BAILEY & HOWARD 1941), lated to intraxylary phloem could be detected. Cambia and in two genera of Acanthaceae, Mendoncia and form adjacent to intraxylary phloem in Convolvulaceae Thunbergia (OBATON 1960, CARLQuIST & ZONA (CARLQuIsT & HANSON 1991) and Cucurbitaceae 1988 b). If one surveys the examples of vessel restriction (CARLQuIST 1992) in species of lianoid habit. Intra patterns in lianas cited above, as well as patterns in xylary phloem potentially offers phloem strands in sites Anredera, one often sees that the imperforate tracheary less likely to experience torsion than phloem strands at elements (mostly libriform fibers) tend to surround ves the periphery of a lianoid stem. sels, and that fiber-sheathed units of vessel groups are Pith strands of phloem in tubers of A. baselloides separated from each other by soft-walled parenchyma, have cambial activity that produces both secondary either rays or axial parenchyma, or both. This suggests xylem and secondary phloem. Scattered strands of that fibrous tissue surrounded by soft-walled tissue xylem and phloem throughout the pith is a characteri serves in protecting vessels from torsion damage in stic of tubers or tuberous roots such as potatoes and lianas. sweet potatoes (METCALFE & CHALK 1950). Such strands potentially provide efficient input and with drawal of photosynthates and water in a highly paren Figs. 13—16. Transections ofAnredera baselloides. 13. Section chymatous storage structure. of root-stem transition, to show intraxylary phloem strands Initiation of phloem strands in axial parenchyma of (one labeled “ip”) adjacent to the pith, which is crushed. A. baseiloides is a structural feature not found in other 14—16. Sections from tuber. 14. Section of vascular tissue from Caryophyllales. Cambia eventually adjacent to them, main cylinder; interfascicular area shows the beginning of apparently adding cambial action (ic) that will produce ray cells. 15—16. Vascu secondary phloem to the strand. lar strands from pith of tuber. 15. Phloem strand to which a These phloem strands qualify as interxylary phloem cambium (c) is adding secondary phloem. 16. Strand to which (‘interxylary phloem’ here denotes phloem within a cambium is adding both secondary xylem (center) and secondary xylem, but excludes phloem produced to the secondary phloem. Fig. 13, scale above Fig.2; Fig. 14—16, outside of a stem or root by successive cambia). The scale above Fig. 3. phloem strands of A. baselloides are much like those of

FLORA (1999) 194 9

194 FLORA(1999) 10

series. this of paper story- cluding vague and initials cambial fusiform Short bium.

con a

in trees on graphically be shown will features cal cam a storied has baselboides A. and cambia, storied

anatomi

other in with changes along trees phylogenetic with species in elements vessel short notably found

on

presence cambium successive in changes state They (1918). TUPPER and by BAILEY hypothesized

character of placement possible The as Basellaceae. of specialization, of phyletic indicator an is likely more

origin to prior yet reinvented Portulacaceae, ly and taceae but 1985), (CARLQuIsT habit to relationship little

Cac

of

origin to and prior lost Aizoaceae to leading that relative bears probably lianas in length element Vessel

except order the in clades the of of all origin to prior sm. lost 334 (1975): CARLQUIsT in sample the of that

be

to have would cambia successive stock, this than From is shorter tm) 206 and tm 184 between ranging

Caryophyllales. of cladograms most in basally placed (means base/bides A. of length element vessel The

is that a family Stegnospermaceae, to prior order the

Basellaceae of Relationship 4.2. in been invented have would cambia succestive Thus,

1992). (PAx 1891, TH0RNE Plumbaginaceae in basal

considered usually not genus a 1996), & B0GGs LQUIST

Aegialitis in except (CAR cambia successive lack which laceae.

Plumbaginaceae, and Polygonaceae outgroups the from in Caryophyl cambia by successive produced tissue

Caryophyllales trace would one families, these of lesis vascular for function storage a to relationship a suggests

phy

true the represented (1994) of R0DMAN This cladogram 1995). CARLQuIsT 1950, CHALK & (METcALFE

the If them. lack and Portulacaceae Hectorellaceae, roots to restricted exceptions, no virtually with are,

Didiereaceae, Cactaceae, whereas cambia, successive Caryophyllaceae in cambia Successive function. that to

have Aizoaceae position. basal a in in dade this appear relate may vascularization additional thus and synthetas,

that Aizoaceae exception the above, with defined as photo and water of storage in serve may baselboides

to Portulacineae corresponding a dade showed A. (1994) in portions root and stem thicker These surface.

and (1984) R0DMAN of etaL. results The ceae. R0DMAN ground the above dm a stem the than thicker appreciably

Portulaca and Hectorellaceae, Didiereaceae, are taceae, base/bides A. of plant mature a in root and base stem

Cac

Basellaceae, of consists which 1994), the & structures: TH0RNE wide relatively of vascularization ing

Portulacineae (CR0NQuI5T Caryophyllales, of suborder provid for mechanism a be may baselboides in A. action

a in

placed are generally Basellaceae cambia. cessive cambial additional of products the Rather, explanation.

suc of presence precedes cambia successive of absence relevant only the be not may habit lianoid the to tion

that 1994) (e.g., made R0DMAN generally is adapta assumption that suggests cambium outer the of appearance

The Caryophyllales. of phylogeny and systematics late the the and parenchyma) by cortical separated plates

in

great interest of is cambia successive of role The cambium of series as a occurs but stem, the around

both. cylinder continuous a form not does (which cambium

to as sister a Portulacaceae with to close Didiereaceae, outer by the formed tissue of quantity limited The

Basellaceae shows (1994) R0DMAN Portulacaceae. understandable. is Basellaceae for reported been viously

and Cactaceae, Didiereaceae, to group as sister a pre laceae not have cambia successive that fact the therefore

Basel place (1994) & RETTIG and and (1992) MANHART root, or stem a of development the in late occurs

al. et of trees The RETTIG Didiereaceae. of thus groups action cambial additional The small. relatively is

sister as Basellaceae and Portulacaceae showed 1994b) event cambial additional this by produced phloem and

(1994a, & D0wNIE PALMER families. these involving xylem of amount the and material, this in occurs event

cladograms with conflicts This 1935). (KRIBs only cambium additional one only that so base/bides, A. in

rays multiseriate of presence than more primitive as cylinder vascular first the of outside forms tissue cular

regarded commonly is 1970), & ceae DITTMAR vas of (RAuH circle single a Only paper. present the in detail

Didierea in found as rays, uniseriate plus rays in senate described baselloides A. of plant large the for those

Multi- order. the in far thus obtained results than cladistic smaller were species those for available roots and

the

with compatible is type ray of this status phyletic stems the but observed, not were cambia successive studied,

whether but Caryophyllales, of family another in found gracilis” “A. and corthfolia” “A. of stems the In curious.

be can Basellaceae of those like rays whether is not is tion in Anredera cambia successive of occurrence The

ques the However, of Portulacaceae. that to similar also stems. the of periphery

is

base/bides A. in vessels of pitting The submitted). the at strands phloem are than torsion by damaged be

(CARLQuI5T, Portulacaceae all virtually to characterizes likely less are a stem in of phloem strands dispersed

condition that because is interesting, base/bides A. strands: phloem intraxylary to similar functionally

in

rays multiseriate exclusively of The as presence be regarded can baselloides A. in parenchyma axial

submitted). in (CAREQuIsT, strands phloem intraxylary The 1991). (CARLQuIsT

Portulacaceae family related the in occur also ing Curcurbitaceae of Coccinia genus, lianoid another The above imaginary sequences call attention to the BALF0uR, E. (1965): Anomalous secondary thickening in problems of interpretation of successive cambia in Chenopodiaceae, Nyctaginaceae and Amaranthaceae. Caryophyllales. As compared to other orders, relatively Phytomorphology 15: 111—122. numerous families of Caryophyllales have successive BEDELL, H. (1980): A taxonomic and morphological re-eva cambia (Aizoaceae, Amaranthaceae, Basellaceae, Che luation of Stegnospermaceae (Caryophyllales). Syst. Bot. 5:419—431. nopodiaceae, Nyctaginaceae, Stegnospermaceae, and BEHNKE, H.-D. (1994): Sieve-element plastids: their signifi some Caryophyllaceae and Phytolaccaceae and segre cance for the evolution and systematics of the order. In: gates of Phytolaccaceae); the families in which succes BEHNKE, H.-D., & MABRY, T. J. (eds.): Caryophyllales. sive cambia do not occur include Achatocarpaceae, Cac Springer Verlag, Berlin & Heidelberg, pp. 89—121. taceae, Didiereaceae, Hectorellaceae, and Portulacaceae CARLQuIsT, S. (1975): Ecological strategies of xylem evolu (BALF0uR 1965, BEDELL 1980, CARLQuIsT 1995. EsAu tion. University of California Press, Berkeley & Los & CHEADLE 1969, GrnsoN 1994, H0RAK 1981, MIKE- Angeles.

SELL 1979, WHEAT 1977). Cambial variants are repor — (1982): The use of ethylene diamine in softening hard plant ted in Barbeuia, Petiveria, Rivina, and possibly Agdestis structures for paraffin sectioning. Stain Technol. 57: 311—317. by PFEIFFER (1926), and these genera need additional — (1983): Wood anatomy of Calyceraceae and Valerianaceae, investigation. The distribution of successive cambia in with comments on aberrant perforation plates in predomi Caryophyllales is not congruent with proposed phylo nantly herbaceous groups of dicotyledons. Aliso 10: genies except for the pairing of Amaranthaceae and 413—425. Chenopodiaceae, regardless of whose phylogenies are — (1985): Observations on functional wood histology of vines considered. The phylogenies are not necessarily incor and lianas: vessel dimorphism, tracheids, vasicentric rect. The distribution of successive cambia may involve tracheids, narrow vessels, and parenchyma. 11: 139—157. developmental factors. For example, successive cambia — (1988): Comparative wood anatomy. Springer Verlag. Ber appear quite late in Basellaceae. In the branches of Steg lin & Heidelberg. nosperma, successive cambia appear relatively tardily — (1992): Wood anatomy of selected Cucurbitaceae and its relationship compared to their appearance in stems of other caryo to habit and systematics. Nord. J. Bot. 12: 347—355. phyllalean families (H0RAK 1981). A similar situation — (1993): Wood and bark anatomy ofAristolochiaceae; syste occurs in Menispermaceae, in which most genera have matic and habital correlations. IAWA Journal 14: been reported to have more than one cambium, but no 341—357. successive cambia have yet been reported in some gen — (1995): Wood anatomy of Caryophyllaceae: ecological, era of that family (METcALFE & CHALK 1950). Most habital, systematic, and phylogenetic correlations. Aliso wood samples of Menispermaceae are not basal stems 14: 1—17. of maximal diameter, so that we do not know whether — (199): Wood anatomy of Portulacaceae and Hectorel successive cambia might eventually appear in genera of laceae: ecological, habital, and systematic implications. Menispermaceae for which they have not yet been Alisol6: 131—153.

— reported. Perhaps the genetic information required for , & Booos, C. J. (1996): Wood anatomy of Plumba ginaceae. Bull. Torrey formation of successive cambia originated early in the Bot. Club 123: 135—147. — , & HNsoi’, M. A. (1991): Wood and stem anatomy order Caryophyllales, but relatively minor genetic of Convolvulaceae: a survey. Aliso 13: 5 1—94. changes might be needed to activate, inhibit, or delay — , & ZoNk, S. (l988a): Wood anatomy of Papaveraceae, formation of successive cambia. When more wood and with comments on vessel restriction patterns. IAWA Bull., stem data on other families of Caryophyllales have been n.s., 9: 253—367.

— , accumulated in the present series of papers, an attempt — (1988b): Wood anatomy of Acanthaceae: a survey. will be made to re-examine the systematic distribution, Aliso 12: 20 1—227. the diversity in types, and the phylogenetic status of suc CR0NQuI5T, A., & TH0RNE. R. F (1994): Nomenclatural and cessive cambia. taxonomic history. In: BEHNKE, H.-D., & MABRY, T. J. (eds.): Caryophyllales. Springer Verlag, Berlin & Heidel berg, pp. 5—25. D0wNIE, S. R., & PALMER, J. D. (1994 a): Phylogenetic rela References tionship using restriction site variation of the chloroplast DNA inverted repeat. In: BEHNKE, H.-D., & MABRY, T. J. BAILEY, I. W., & HowARD, R. A. (1941): The comparative (eds.): Caryophyllales. Springer Verlag, Berlin & Heidel morphology of the Icacinaceae. I. Anatomy of the node berg, pp. 223 —233.

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