IAWA Journal, Vol. 15 0), 1994: 51~63

STEM DEVELOPMENT, MEDULLARY BUNDLES, AND WOOD ANATOMY OF GLANDULOSUS VAR. SEPTENTRIONALIS ()

by

Sheila M. Hayden and W. John Hayden Department of Biology, University of Richmond, Richmond, 23173, U. S. A.

Summary Anatomy and development of vascular tis­ onomically complex assemblage of some 21 sues in the annual stems of Croton glanduZo­ described varieties found from eastern North sus var. septentrionaZis are described. In pri­ America, the West Indies, and mary stages of growth the stem possesses a to southern Brazil and northern Argentina; it eustele of bicollateral bundles; internal phloem has been classified in section GeiseZeria (Web­ is notably more extensive than the external. ster 1993). The northernmost element of this In addition to a vascular cambium and sec­ complex is Croton glanduZosus var. ondary xylem that form in the usual fashion, septentrionaZis Muell. Arg. (Fig. 1), a vigor­ additional cambia add cells to the internal ous weedy annual herb found from Mary­ phloem portion of the bicollateral bundles, land, to , , and Texas. The forming well-marked medullary bundles at grow one to two feet tall and branch freely. the perimeter of the pith. At first, the peri­ Stems of most species of Croton are note­ medullary cambial strands produce only in­ worthy for the presence of internal phloem ternal secondary phloem; later, internal sec­ (Pax 1884; Froembling 1896; Gaucher 1902; ondary xylem is also formed in some stems. Leandri 1939). In addition to these plants, When internal secondary xylem is present, Metcalfe and Chalk (1983) list nine more the medullary bundles have an inverted orien­ genera of Euphorbiaceae said to possess this tation, i.e., phloem innermost (towards centre feature and earlier literature indicates that of pith) and xylem outermost (near proto­ internal phloem or bundles of phloem-like xylem). Cells of the medullary bundles in­ cells are widespread in uniovu1ate members of clude sieve tube elements, vessel ekments, the family (e.·g, Pax 1884; Froembling 1896; and fibres. Normal (external) secondary phlo­ Gaucher 1902, Pax & Hoffmann 1931). The em is weakly developed. Normal secondary most comprehensive descriptions of stem xylem contains short vessel elements with anatomy for Croton and related genera are simple perforation plates and alternate inter­ found in Froembling's (1896) survey (sum­ vascular pits, libriform fibres, narrow hetero­ marised in Solereder 1908 and Metcalfe & cellular rays, and lacks axial parenchyma. Chalk 1950, 1983), but there appears to have Key words: Croton, Euphorbiaceae, internal been no previous study of stem development phloem, medullary bundles, stem devel­ in this . Preliminary observations of opment, wood anatomy stems of Croton glandulosus var. septentrio­ naZis confirmed the presence of medullary Introduction bundles containing phloem, but also revealed, Croton L. is a large genus of Euphorbia­ for the first time, some with secondary xylem ceae comprising nearly 1000 species of trees, as well. Thus, the present study was under­ shrubs, and herbs found throughout the taken to provide a detailed first report of stem warm regions of the globe and achieving ontogeny of this species, with an emphasis great diversity in the neotropics (Webster on its vascular tissues, especially the unusual 1992, 1993). Croton glanduZosus L. is a tax- structures encountered in the pith region.

Downloaded from Brill.com10/07/2021 03:30:22AM via free access 52 IAWA Journal, Vol. 15 0),1994

Materials and Methods Specimens were collected from the au­ thors' residence in the suburbs of Richmond, Virginia. A series of spring-collected seedling stems provided developmental stages from shortly after expansion of the cotyledons through primary growth, and early stages of secondary growth. Summer and autumn-col­ lected plants yielded stout pencil-thick stems with late stages of secondary growth. Col­ lection data and voucher specimens are as follows: U.S.A., Virginia, Chesterfield Co.: Hayden 2082 (9 July 1988) (URV); Hayden 2634 (26 May 1990) (URV); Hayden 2892 (23 Sept. 1990) (URV). All tissues were fixed in FAA. A total of 15 seedling and herbaceous stems were de­ hydrated in tertiary butanol, embedded in paraffin, and sectioned at 10 11m on a rotary microtome. Paraffin sections were stained in aniline blue and counter-stained with safranin. Six larger stems were sectioned at 30 11m on a sliding microtome and stained in various com­ binations of hematoxylin, aniline blue and safranin. Secondary xylem from the basc of two of the larger stems was macerated by means of Jeffrey's fluid (equal volumes of 10 percent nitric acid and 10 percent chromic acid). Numerical values reported in the wood description are derived from these two sets of macerations as well as sections prepared from the same stems; these values are based on 50 measurements per specimen of vessel element length, diameter, and fibre length, 30 mea­ surements per specimen of end wall angle, and 10 measurements or counts per specimen for all other features. SEM observations were made from sections cut on a sliding micro­ tome at 50 11m, dehydrated in ethanol, critical point dried with liquid C02, and sputter coated with a gold/palladium mixture. The epicotyl of Croton glandulosus var. septentrionalis ascends through several nodes, eventually terminating in a flower cluster sub­ tended by a verticil-like group of smaller flower-bearing stems (Fig. 1). In order to con­ trol for potential ontogenetic variation, i.e., variation with position along the stem, our anatomical observations were routinely fo­ Fig. 1. Croton glandulosus var. septentrio­ cused on the basal portion of the epicotyl, nalis. habit, shortly after onset of flowering. specifically, the most proximal (i.e., first) Scale bar = 2 cm. node and internode above the cotyledons; un-

Downloaded from Brill.com10/07/2021 03:30:22AM via free access Hayden & Hayden - Stem anatomy of Croton 53

less stated otherwise all descriptions pertain Nodes conform to the three-trace trilacu­ to this region. Two of the six mature stems nar configuration (Fig. 5). Each trace remains were sectioned at multiple (four or five) inter­ bicollateral as it diverges from the stele and vals spaced evenly between the cotyledons enters the (Fig. 4). Longitudinal sec­ and the first distal cluster of branches to pro­ tions of young stems reveal the presence of vide information on potential developmental sieve tube elements in both internal and ex­ (i.e., positional) variation. ternal phloem. Sieve tube elements are identi­ fiable by virtue of their simple sieve plates stained darkly with aniline blue and conspicu­ Results ous mucous slime plugs (Fig. 11). To the cx­ Primary growth tent detectable in our light microscope prepara­ Primary growth in the stem of Croton glan­ tions, sieve cells of the internal and external dulosus var. septentrionalis produces a eustele primary phloem are structurally similar. Sieve composed of bicollateral bundles (Figs. 2- pores were not observed, probably a conse­ 5). Epidermis is uniseriate and bears few sto­ quence of their presumed small size and the mates but has numerous stellate hairs (Fig. 1, failure to control fixation for optimal preserva­ inset) with multiseriate stalks. Cortex consists tion of fine details in phloem. No lateral sieve of collenchyma and parenchyma cells; in older areas were observed on sieve tube elements. stems, groups of thick-walled laticifers bear­ We assume that small cells among the sieve ing clear latex are prominent in the cortex (Fig. tubc elements of both internal and external 12). Each vascular bundle consists of three phloem are companion cells, but the prepara­ groups of cells, external primary phloem, pri­ tions made do not permit positive confirma­ mary xylem, and internal primary phloem tion of this assumption. (Fig. 3). In the mature primary body, internal phloem is generally more extensive than ex­ Secondary growth ternal phloem (Fig. 3). Internal and external The origin of the vascular cambium locat­ phloem are similar in their total lack of scle­ ed between the last-formed cells of metaxylem renchyma, but external primary phloem has and the external phloem proceeds in a com­ scattered tannin-bearing idioblasts that are pletely normal fashion; the same can be said absent in the internal phloem (Figs. 2, 4, 5). of the accumulation of secondary xylem (Figs. Primary xylem development is exarch and 13, 15). The amount of externally produced consists of single or double files of lignified secondary phloem is sparse and, like the pri­ conducting elements separated by unlignified mary phloem, it lacks sclerenchymatous ele­ xylem parenchyma. Protoxylem walls of ments (Fig. 12), but otherwise its mode of tracheary elements are helically thickened development seems normal. However, an a­ (Fig. 11); scalariformly thickened or pitted typical secondary ontogeny occurs between elements are frequent in the metaxylem. In­ the protoxylem and internal phloem. The com­ ternal phloem excluded, the pith consists bined activity of normal and atypical cambia solely of parenchyma cells (Figs. 2-5). Drus­ transforms the vascular system of the es occur scattered throughout the cortex and from a eustele of bicollateral bundles to a pith (Figs. 3-5). Through maturation of the vascular cylinder of normal secondary xylem primary body, pith cells are generally devoid and phloem with the addition of anomalous of starch (Fig. 3). Pith cells from stems with medullary bundles. The anomalous medullary secondary growth, however, are densely bundles consist of the original cells of inter­ packed with starch grains (Figs. 8, 10). nal primary phloem plus additional secondary Developmentally, internal phloem is first vascular tissues. In order to distinguish be­ detectable as a small clump of densely cyto­ tween normal secondary growth and events plasmic cells that differentiate shortly after that occur in the vicinity of the internal phloem, the first elements of protoxylem and external the latter will be referred to as perimedullary phloem. Additional internal phloem forms in­ secondary growth. ternally adjacent to the protoxylem as primary The cambia responsible for perimedullary growth continues. secondary growth occur as discrete strands

Downloaded from Brill.com10/07/2021 03:30:22AM via free access 54 IAWA Journal, Vol. 15 (I), 1994

Figs. 2-5. Seedling stems of Croton glandulosus var. septentrionalis (Hayden 2634) just after expansion of first true leaf. - 2: Eustele at upper portion of first node. - 3: Bicollateral bundles, same section as Fig. 2. - 4: Bicollateralleaf traces in petiole base of first true leaf. - 5: Departure of bicollateralleaf traces below first node. - Scale bars of 2 & 5 = 150 11m; of 3 = 100 11m; of 4 = 250 !lm. - dr =druse; epp =external primary phloem; ipp =internal primary phloem; It =leaf trace; px = primary xylem.

Downloaded from Brill.com10/07/2021 03:30:22AM via free access Hayden & Hayden - Stem anatomy of Croton 55 ------that arise between the earliest-formed proto­ eases it appears that multiple clumps of phlo­ xylem elements and outermost cells of the in­ em cells are the result of the vagaries of which ternal primary phloem. Perimedullary sec­ cells succumb to crushing by the forces re­ ondary growth is restricted to the medullary sulting from formation and expansion of new bundles. Cells of the interfascicular regions cells in the bundle; in this fashion, the inner­ (areas formerly between bundles of internal most phloem elements may become isolated primary phloem) are passive and either remain from the remainder of the bundles. In other unchanged (Figs. 6-8) or, in robust older cases, especially bundles with complex pat­ stems, become crushed by proliferation of terns of intact and crushed phloem elements cells formed in the inner portion of the bi­ (Fig. 8), we cannot rule out the possibility of collateral bundle (Fig. 9). multiple cambia. We have observed stages of perimedullary In some stems, there is a second phase of secondary growth only in stems that had at perimedullary secondary growth that produces least some normal secondary xylem. In early internal secondary xylem elements in addition stages of perimedullary secondary growth di­ to the internal secondary phloem cells previ­ visions apparently produce only internal (cen­ ously described. The newly formed xylem tripetal) derivatives which mature as internal elements are produced centrifugally, i.e., to­ secondary phloem; internal secondary xylem wards the protoxylem elements. Consequent­ is not formed in early stages. The new cells ly, the positions of xylem and phloem in formed by perimedullary secondary growth perimedullary bundles at this stage of devel­ are constrained to develop within the confin­ opment are inverted relative to that of normal ed space of the pith which, at this stage, is stem bundles in dicotyledons. Initiation of this completely surrounded by a cylinder of wood. second phase of development is highly vari­ One readily observable consequence of peri­ able from specimen to specimen. The earliest medullary secondary growth is the oblitera­ stage observed, a single xylem element in a tion (crushing) of primary phloem cells to­ perimedullary bundle, was found in a spring­ ward the interior of the medullary bundle collected seedling stem that had surpassed 3 (Figs. 6-8). The accumulation of crushed cm in height and had produced approximately cells becomes ever greater as perimedullary a 0.5 mm radius of normal secondary xylem, secondary growth proceeds. but had not yet initiated flowering. Some late The cambial nature of perimedullary summer collections of flowering stems with growth is evident from the radial alignment as much as a 3 mm radius of normal secondary of the derivative cells (Figs. 7, 10). The xylem are completely devoid of internal sec­ observation of slime plugs in radial files ondary xylem (Figs. 6, 13), while others of (Fig. 7) further indicates that each sieve cell comparable size and collected at the same time of the group developed at the same height in may have one to several perimedullary sec­ the stem, a further confirmation of the cam­ ondary bundles bearing internal secondary bium-like nature of perimedullary secondary xylem. In one late summer stem the perime­ growth. Unlike the normal cambium, how­ dullary bundles had expanded to occupy vir­ ever, we have seen no evidence of the pro­ tually the entire volume of the former pith, duction of ray tissue in perimedullary sec­ the original pith parenchyma being crushed ondary growth. Further, we have seen no evi­ along with early-formed cells of the internal dence of anticlinal (multiplicative) divisions in primary phloem (Fig. 9). Internal secondary cambia of medullary hundles. xylem consists of vessel elements and fibres; The phloem-only stage of peri medullary ray and axial parenchyma are absent. secondary growth may he restricted to a sin­ Sections taken at various heights along the gle source of camhium-like cells as implied main stem reveal expected aspects of develop­ by the above description. However, as many mental/positional variation. Qualitatively, the as half the internal hundles of a given stem structure of all upper portions of the stem cor­ section may possess multiple clumps of phlo­ respond to that of the base, but one finds suc­ em cells separated from each other by parti­ cessively earlier developmental stages as one tions of crushed cells (Figs. 6, 8). In some progresses apically. Another difference is re-

Downloaded from Brill.com10/07/2021 03:30:22AM via free access 56 IAWA Journal, Vol. 15 (1), 1994

Downloaded from Brill.com10/07/2021 03:30:22AM via free access Hayden & Hayden - Stem anatomy of Croton 57 lated to the normal slight increase in primary stem diameter that occurs from seedling stages to maturity; thus, pith diameter and the num­ ber of perimedullary bundles is smaller at the base of the plant than in apical regions.

Periderm A thin periderm was observed in older stems. Periderm arises from cortical cells im­ mediately subjacent to the epidermis (Fig. 12). Phellem cells are thin-walled and devoid of deposits. In addition to periderm formation, accommodation to increasing stem diameter in secondary growth is also accomplished by diffuse growth, evidenced by numerous par­ titions encountered in cells of the outer cortex (Fig. 12).

Wood anatomy Vessels are distributed more or less even­ ly across the single growth ring present in the annual stems, however, vessels are less fre­ quent and somewhat smaller in later formed secondary xylem than that formed early in the season (Figs. 13, 15). Vessel distribution is 45 percent solitary, 32 percent radial multiples, Fig. 10. Scanning electron micrograph of xy­ and 23 percent clusters; clusters are usual­ lem, phloem-only medullary bundleJlnd pith ly radially elongate (Fig. 16). Vessel outlines of Croton glandulosus var. septentrionalis range from rounded to somewhat angular, (Hayden 2892). Scale bar =' 100 ~m. the latter condition being found in clusters. Vessel walls have an average thickness of 2.6 ~m. Average tangential diameter of ves­ (170-600 ~m) for the other. Vessel elements sels is 26 ~m (10-51 )lm). Perforation plates are often ligulate, the ligules averaging 71 )lm are predominantly simple (Fig. 17); however, long. a few scalariform perforations with only 2 or Imperforate tracheary elements are pre­ 3 bars can be found near the protoxylem. On dominantly libriform fibres that have an aver­ average, end walls are inclined 59 degrees age length of 582 )lm (300-820 )lm). Fibre from the horizontal (25-85 degrees). Inter­ lumens occupy more than half of the cell's vascular pits are circular to elliptical, alternate, diameter. Fibres with gelatinous walls are and have an average vertical diameter of 6 Jlffi; common, occurring in broad tangential arcs vessel to ray pits are similar. Vessel element (Fig. 15) in most specimens examined. Some length varied notably in the two specimens for of the small diameter elements of pore groups which this feature was measured: an average prove to be vascular tracheids (Figs. 14, 16), of 237 ~m (78-362 ~m) for one, and 396 ~m but these cells are, overall, rare.

Figs. 6-9. Medullary bundles in mature stems of Croton glandulosus var. septentrionalis (Hayden 2892). - 6: Pith and phloem-only bundles. - 7: Phloem-only medullary bundle with radial alignment of slime plugs in sieve tube elements. - 8: Complex phloem-only medullary bundles. - 9: Inverted medullary bundles containing secondary xylem, pith nearly occluded. - Scale bar of 6 = 150 ~m; of 7 = 50 ~m; of 8 = 100 )lm; of 9 = 250 ~m. - sp = slime plug; st = starch grains.

Downloaded from Brill.com10/07/2021 03:30:22AM via free access 58 IAWA Journal, Vol. 15 (1), 1994

(Legend on page 60)

Downloaded from Brill.com10/07/2021 03:30:22AM via free access Hayden & Hayden - Stem anatomy of Croton 59

(Legend on page 60)

Downloaded from Brill.com10/07/2021 03:30:22AM via free access 60 IAWA Journal, Vol. 15 (1), 1994 ------

Axial xylem parenchyma is essentially ab­ nal phloem in Croton glandulosus and several sent. other species; none was observed in this study Rays are heterocellular and consist pri­ except, of course, the fibrous component of marily of erect cells with occasional procum­ the xylem formed in medullary bundles in bent cells toward the centre of the ray (Fig. late developmental stages. Froembling's ref­ 17). Rays are 66 percent uniseriate and 34 erence to fibres may be attributable to taxo­ percent multiseriate (Fig. 18). Uniseriate rays nomic differences in the material studied, or, have an average width of 10 11m and are gen­ possibly, failure to interpret the fibres as com­ erally less than 10 cells or 350 11m in height, ponents of internal secondary xylem. Fibres although a few rays more than twice this have been reported as components of the in­ height were encountered. Multiseriate rays ternal phloem of several other euphorbiace­ are mostly biseriate, less commonly 3-seriate, ous genera (Pax 1884; Gaucher 1902). and have an average width of 18 11m. Multi­ Available literature indicates the existence seriate rays routinely range up to 35 cells high, of some subtle differences in the structure of rarely higher, and have an average height of internal phloem of various species of Croton. 572 11m. Perforated ray cells are regularly In addition to presence or absence of fibres encountered (Fig. 14). Starch was observed discussed above, Uandri (1939) noted that in ray cells only in regions near the primary tanniniferous cells (cf. those observed in the xylem. Neither secretory canals nor laticifers external phloem in this study) are often, but were observed in the ray system. not always present in the internal phloem of Croton species. The amount of internal phlo­ em in any given stem is also reported to vary Discussion from species to species (Gaucher 1902), but Internal phloem and medullary bundles it is clear from our studies that age of the stem Previous literature (Froembling 1896) pro­ may affect such assessments. Finally, internal vides only limited information on stem struc­ phloem is reported to be absent in several spe­ ture of Croton glandulosus (variety unspeci­ cies of Croton section Astraea (Froembling fied). Froembling (1896) noted internal phlo­ 1896). em at the periphery of the pith, but he did not The occurrence of internal phloem, medul­ describe the successive addition of phloem lary bundles, or other phloem-like tissues at elements to the medullary bundle, neither did the periphery of the pith is widespread among he mention internal secondary xylem nor the uniovulate members of Euphorbiaceae (Gau­ inverted orientation of xylem-containing bun­ cher 1902; Solereder 1908; Metcalfe & Chalk dles. Froembling did mention the occurrence 1983). In addition to Croton and its closest of sclerenchyma fibres associated with inter- relatives, well-developed internal phloem has

f-- f-- Figs. 11-14. Stem features of Croton glandulosus var. septentrionalis. - 11: Longitudinal sec­ tion through pith, internal phloem, and protoxylem, note sieve plates and slime plugs (Hayden 2634). - 12: External phloem, cortex, epidermis, and periderm of a mature stem; note laticifers; same section as Fig. 15 (Hayden 2892). - 13: Phloem-only medullary bundles, primary xylem, and secondary xylem (Hayden 2892). - 14: Transverse section of wood with perforated ray cell (Hayden 2892). - Scale bars of 11 & 14 = 50 11m; of 12 = 100 11m; of 13 = 150 11m. -la = lati­ cifer; pd = periderm; pp = pith parenchyma; prc = perforated ray cell; sp = slime plug. f-- Figs. 15-18. Wood of Croton glandulosus var. septentrionalis (Hayden 2892). - 15: Transverse section; same section as Fig. 12. - 16: Transverse section. - 17. Radial section. - 18: Tangential section. - Scale bar of 15 = 500 11m; of 16 & 17 = 100 11m; of 18 = 200 11m. - gf = gelatinous fibres.

Downloaded from Brill.com10/07/2021 03:30:22AM via free access Hayden & Hayden - Stem anatomy of Croton 61

been recorded in Alchornea Swartz, Caelebo­ 1929; Maheshwari & Singh 1942); and also gyne J. Smith, Conceveiba Aublet, Mabea Campsis (Bignoniaceae) (Handa 1936). The AubL, Pera Mutis, Sebastiana Spreng., Sene­ case of Gentiana is notable in that external feldera Martius, and some species of Mallotus phloem is described as weakly developed, Loureiro (Gaucher 1902; Metcalfe & Chalk much as was found in Croton glandulosus 1983). Medullary bundle cells in some uni­ var. septentrionalis. ovulate euphorbs appear phloem-like but lack As noted by Maheshwari (1929), in his sieve areas (Pax 1884; Gaucher 1902). Such discussion of Rumex, the inverted medullary apparently vestigial phloem tissue has been bundles of all the genera named above, having described as 'cambiform' (Pax 1884; Pax & developed in the perimedullary region by cam­ Hoffmann 1931), suggesting the persistence bium-like proliferation from bieollateral bun­ of perimedullary secondary growth in plants dles, seem to constitute a special category of with poorly developed sieve plates in their in­ medullary bundle. The type of bundle found ternal 'phloem'. It is noteworthy that both ves­ in these plants and in Croton may bear no ho­ tigial and well-developed internal phloem are mology with deeply seated medullary bundles reported in all three subfamilies of uniovulate of other plants, especially bundles with the Euphorbiaceae, i.e., Acalyphoideae, Croton­ normal orientation of xylem and phloem. For oideae, and Euphorbioideae in the classifica­ example, the medullary bundles of cacti which tion of Webster (1975). The systematic poten­ are found throughout the pith and develop tial of this anatomical feature seems obvious, from discrete procambial strands (Mauseth but to apply it meaningfully would require 1993) differ fundamentally from the bundles much more data on stem structure in uniovu­ of Croton which form by perimedullary sec­ late euphorbs than is presently available. ondary growth. Bicollateral bundles occur in stems of a Physiological studies of internal phloem in number of dicotyledons, in some cases, char­ various plants offer a basis for hypotheses acterising entire families, in other cases re­ concerning the function of the structures found stricted to isolated genera or species (see lists in Croton glandulosus var. septentrionalis. A in Metcalfe & Chalk 1950, 1983). Perhaps number of studies employing radioactive trac­ the best known examples include Cucurbita­ ers and/or fluorescent dyes have indicated ceae, the families of Myrtales, and several that internal phloem may exhibit directional or families of Asteridae (as classified by Cron­ temporal differences in translocation com­ quist 1981). Based on the summaries in Met­ pared to the external phloem of the same plant calfe & Chalk (1950), it is interesting to note (Bonnemain 1969; Fredon & Bonnemain that cambial conversion of the inner portion 1970; Couillault & Bonnemain 1973). Fur­ of bicollateral bundles into medullary bundles ther, observation of preferential feeding by is not known in Cucurbitaceae and Myrtales, aphids has suggested differences in the com­ but does occur in some members of Apocyna­ position of the cell sap between internal and ceae, Asclepiadaceae, Convolvulaceae, Genti­ external phloem (Botha et aL 1975; Botha & anaceae, Loganiaceae (Buddleioideae exclud­ Evert 1978). Judging by its accumulation of ed), Solanaceae, and one non-asterid family, starch, pith of Croton glandulosus var. sep­ Polygonaceae. Among these families, ano­ tentrionalis is evidently a storage organ of malous xylem production resulting in the for­ considerable significance for the plant. Our mation of inverted medullary bundles has light microscope illustrations of woody stems been reported sporadically, including the fol­ grossly under-represent starch content since lowing (Metcalfe & Chalk 1950; and others, large quantities of starch were released during as cited): Apocynum (Holm 1910) and Wil­ sectioning. Somewhat better retention of lughbeia (Apocynaceae); Leptadenia (Asclepi­ starch is visible in the SEM image (Fig. 10), adaceae) (Singh 1943); many genera of Con­ but starch has been lost from this section, volvulaceae (Mikesell & Schroeder 1984; too. The internal phloem of bicollateral and Carlquist & Hanson 1991); Gelsemium (Lo­ medullary bundles is efficiently located for ganiaceae); Gentiana (Gentianaceae); Rumex transport of assimilates to and from the pith, (Polygonaceae) (Joshi 1936; Maheshwari which we hypothesize to be its major function.

Downloaded from Brill.com10/07/2021 03:30:22AM via free access 62 IAWA Journal, Vol. 15 (1), 1994 ------

Such a direct gathway to cells of the pith is mature stems, their relation to branches, and presumably more efficient than the pathway presumed assimilate sinks such as flowers and available to plants with only external phloem, fruits remains unknown, but must be consid­ i. e., through the cambium and across the sec­ ered before the function of these bundles can ondary xylem via ray cells. The predominance be understood thoroughly. Similarly, a de­ of upright ray cells would render radial trans­ tailed cytological examination of the phloem port in Croton glandulosus var. septentrio­ of Croton glandulosus would seem necessary naZis inefficient and, in fact, starch grains in this regard. Also, our knowledge of the were noticeably absent from xylem ray cells medullary cambium itself is, at best, rudi­ (except for a few cells near the pith) even mentary; additional structural and physiologi­ though all specimens were fluid preserved. cal studies are indicated. As mentioned ear­ Since this species is an annual it has no win­ lier, Croton is a large genus, and thus affords ter dormancy and no need for subterranean many opportunities for comparative anatomi­ storage of reserve assimilates; the relatively cal study beyond Froembling's (1896) origi­ weak development of external phloem may nal survey. The perspective provided by the well be sufficient to support growth and meta­ present study highlights the necessity of ex­ bolism of the root system. amining multiple stages of stem development in any comparative study of Croton or, for Wood anatomy that matter, any plant with perimedullary sec­ Although Croton is, essentially, a genus ondary growth. of woody plants, only a minority of species are actually arborescent and few of these Acknowledgements produce timber that has come to the attention This study was initiated as a graduate class of wood anatomists. Several aspects of wood project by Lydia Rogers who brought the structure reported for various species of Cro­ wood and medullary bundles of several Cro­ ton in Janssonius (1934), Record (1938), ton species to our attention. Uand.ri (1939), and Metcalfe & Chalk (1950) conform with the above description of C. References glandulosus var. septentrionalis: numerous, Bonnemain, J. L. 1969. Le phloeme interne narrow vessels frequently in radial alignment; et Ie phloeme inclus des Dicotyledones: libriform fibres with frequently gelatinous leur histogenese et leur physiologie. Rev. walls; and strongly heterocellular uni- or bi­ Gen. Bot. 76: 5-36. seriate rays that are generally less than 25 cells Botha, C.E.J. & R.F. Evert. 1978. Obser­ tall (sometimes taller, as reported here and in vations of preferential feeding by the aphid, Janssonius 1934). Croton glandulosus var. Rhopalosiphum maidis, on abaxial phlo­ septentrionalis is noteworthy, however, in its em of Cucurbita maxima. Protoplasm a 96: virtual absence of axial xylem parenchyma, in 75-80. contrast to the diffuse, banded, and aliform Botha, C.E.J., R.F. Evert & R.D. Walms­ patterns reported for other species. Record ley. 1975. Studies on Gomphocarpus phy­ (1938) and Carlquist (1988) report the pres­ socarpus: further evidence of preferential ence of secretory canals in rays of Croton feeding by the aphid, Aphis nerii, on the (species not mentioned) and Rudall (1987, internal phloem. Protoplasm a 84: 345- 1989) has noted laticifers in rays of C. con­ 356. duplicatus H.B.K., C. panamensis Muell. Carlquist, S. 1988. Comparative wood anat­ Arg., and an unidentified species, but no omy. Springer-Verlag, Berlin. such structures were observed in Croton glan­ Carlquist, S. & M.A. Hanson. 1991. Wood dulosus var. septentrionalis. anatomy of Convolvulaceae: a survey. Aliso 13: 51-94. Suggestions for further study Couillault, 1. & 1. L. Bonnemain. 1973. Results of the present study suggest several Transport et distribution des assimilats avenues for further investigation. The three­ chez Trapa natans L. Physiologie Vegetale dimensional pattern of medullary bundles in 11: 45-53.

Downloaded from Brill.com10/07/2021 03:30:22AM via free access Hayden & Hayden - Stem anatomy of Croton 63

Cronquist, A 1981. An integrated system of Metcalfe, C.R. & L. Chalk. 1950. Anatomy classification of flowering plants. Colum­ of the dicotyledons. Clarendon Press, Ox­ bia University Press, New York. ford. Fredon, J. J. & J. L. Bonnemain. 1970. Metcalfe, C.R. & L. Chalk. 1983. Anatomy Transport du 14C assimile chez Ie radis of the dicotyledons. 2nd ed., vol. 2. Cla­ a divers stades de son developpement. rendon Press, Oxford. Compt. Rend. Acad. Sci. ser. D 270: Mikesell, J. & AC. Schroeder. 1984. Inter­ 354-357. nal phloem development in Pharbitis nil Froembling, W. 1896. Anatomisch-systema­ Chois. (Convolvulaceae). Bot. Gaz. 145: tische Untersuchung von Blatt und Axe 196-203. der Crotoneen und Euphyllantheen. Bot. Pax, F. 1884. Anatomie der Euphorbiaceen Centralbl. 65: 129-139, 177-192,241- in ihrer Beziehung zum System derselben. 249, 289-297, 321-329, 369-378, Bot. Jahrb. Syst. 5: 384-421. 403-411, 433-442, pis. 1-2. Pax, F. & K. Hoffmann. 1931. Euphorbia­ Gaucher, L. 1902. Recherches anatomiques ceae. In: A Engler & K. Prantl, Die na­ sur les Euphorbiacees. Ann. Sci. Nat. tiirlichen Pflanzenfamilien. Ed. 2, 19c: 11- Bot., Ser. 8, 15: 161-309. 253. Wilhelm Engelmann, Leipzig. Handa, J. 1936. Abnormal vascular bundle Record, S.J. 1938. American woods of the in the stem of Campsis grandiflora K. family Euphorbiaceae. Trop. Woods 54: Schum. Jap. J. Bot. 8: 47-57. 7-40. Holm, T. 1910. Medicinal plants of North Rudall, P.J. 1987. Laticifers in Euphorbia­ America. 44. Apocynum cannabinum. ceae - a conspectus. Bot. J. Linn. Soc. Merck's Rep. 19: 277-280. 94: 143-163. Janssonius, H.H. 1934. Euphorbiaceae. In: Rudall, P.J. 1989. Laticifers in cambium and Mikrographie des Holzes der auf Java Vor­ wood of Croton spp. (Euphorbiaceae). kommenden Baumarten 5: 442-812. IAWA Bull. n.s. 10: 379-383. Joshi, AC. 1936. The anatomy of Rumex Singh, B. 1943. The origin and distribution with special reference to the morphology of inter- and intraxylary phloem in Lepta­ of the internal bundles and the origin of denia .. Proc.lndian Acad. Sci. 18, Sect. B: the internal phloem in the Polygonaceae. 14-19. Amer. J. Bot. 23: 362-369. Solereder, H. 1908. Systematic anatomy of Leandri, M.J. 1939. Les "Croton" de Mada­ the dicotyledons. (Translated by L. A. gascar et des ties voisines. Ann. Mus. Boodle & F.E. Fritsch; revised by D.H. Colon. Marseille ser. 5, 7: 1-100. Scott.) Clarendon Press, Oxford. Maheshwari, P. 1929. Origin and develop­ Webster, G.L. 1975. Conspectus of a new ment of internal bundles in the stem of classification of the Euphorbiaceae. Taxon Rumex crispus. J. Indian Bot. Soc. 8: 24: 593-601. 89-117. Webster, G.L. 1992. Realignments in Ameri­ Maheshwari, P. & B. Singh. 1942. On the in­ can Croton (Euphorbiaceae). Novon 2: ternal bundles in the stem of Rumex patien­ 269-273. ta L. Proc. Indian Acad. Sci. 45: 153-157. Webster, G.L. 1993. A provisional synopsis Mauseth, J.D. 1993. Medullary bundles and of the sections of the genus Croton (Eu­ the evolution of cacti. Amer. 1. Bot. 80: phorbiaceae). Taxon 42: 793-823. 928-932.

Downloaded from Brill.com10/07/2021 03:30:22AM via free access