IAWA Bulletin n.s., Vol. 9 (3),1988: 253-267

WOOD ANATOMY OF PAPAVERACEAE, WITH COMMENTS ON VESSEL RESTRICTION PATTERNS

by

Sherwin Carlquist and Scott Zona Rancho Santa Ana Botanic Garden and Department of Biology, Pomona College, Claremont, California 91711, U. S.A.

Summary Qualitative and quantitative features are California, Dendromecon is a conspicuous reported for Bocconia, Dendromecon, Di­ shrub or small tree to 6 m (Munz 1974). Boc­ centra, Hunnemannia, and Romneya. Boc­ conia, native to montane Mesoamerican and conia differs from the other genera by its Andean regions, is even taller (to 8 m: Fedde wide vessels, few per group, and few per 1936, Cumbie 1983), although the succulent mm2; it shows paedomorphosis in vessel ele­ cortex and pith suggest a degree of herbace­ ment length and ray histology. In respects ousness. Romneya is a shrub to 2.5 m, in other than these, it agrees with features com­ chaparral and coastal sage associations of Ca­ mon to woody Papaveraceae; these features lifornia and northern Baja California (Munz in turn occur in families of Papaverales (Ber­ 1974); the sterns branch from the base, and beridaceae, Lardizabalaceae, Ranunculaceae): last only for several years each, so that wood vessels in diagonal groups; presence of both accumulation is less than in Dendromecon. libriform fibres and vasicentric tracheids; nu­ Hunnemannia, which occurs on the Mexican cleated nature of libriform fibres; rays almost Plateau, is a small to medium-sized shrub, exclusively multiseriate; rays wide, tall, and woody at the base (the specimen in the pres­ composed mostly of procumbent cells; wood ent study was collected in Hawaii, where it is storied to various degrees. Additional fea­ adventive). Much less woody is Dicentra tures show resemblance between one or more chrysantha. Although most species of Dicen­ genera of Papaveraceae and other families of tra are relatively herbaceous, the rhizomes Papaverales. Bocconia is distinctive among and lower sterns of D. chrysantha and D. Papaveraceae in its relatively mesomorphic ochroleuca Enge1m. are conspicuously stout wood, which may in part be explainable on and woody; upright innovations from these the basis of stern succulence. The occurrence rhizomes are woody at bases. Degree and of avessei restriction pattern - vessels in the kind of woodiness are relevant to the study centre of fascicular areas (axial portions of of wood anatomy; Cumbie (1983), by study­ secondary xylem between rays) not in contact ing wood ontogeny of Bocconia vulcanica, with rays - in Dicentra and Hunnemannia is believes Bocconia wood to exemplify pae­ like that of other genera of Papaverales such domorphosis. Dendromecon is, as Cumbie as Nandina. An explanation for the signifi­ (1983) notes, probably not closely related to cance of vessel restriction, involving genera Bocconia, and therefore there is a possibility other than those of Papaverales (Launea, Va­ that it may be primarily rather than secondar­ leriana), is attempted. ily woody. This concept seems more plau­ Key words: Ecological wood anatomy, sys­ sible than the earlier phylogeny offered by tematic wood anatomy, vessel restriction Fedde (1936: 18, 58) in which he postulates patterns, Papaveraceae. a linear series leading from Corydalis to Eschscholzia to Dendromecon to Bocconia Introduction (and thence on to Glaucium and other herba­ Papaveraceae are not generally considered ceous genera). In addition to primary versus woody to any appreciable degree, although in secondary woodiness, degree of woodiness

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is a concern; for example, the sterns studied ly attained consensus, despite the presence of Dendromecon rigida subsp. rhamnoides of quite different views in earlier literature. are much larger than those of D. rigida The treatment of Dahlgren (1980), Takhtajan subsp. rigida (Table 1, colurnn 1). Likewise, (1987), and Thorne (1976) group together the differences between stern and root wood the fartlilies Papaveraceae (including Fuma­ in Dicentra offer interesting comparisons. riaceae in the present study), Berberidaceae, Papaveraceae that are essentially herbaceous, Circaeastraceae, Kingdoniaceae, Lardizabala­ with only very thin woody cylinders at bases ceae, Menispermaceae, Ranunculaceae, and at most (e.g., Argemone) have not been in­ Sargentodoxaceae (as weil as such segregate cluded in the present study. farnilies as Glaucidiaceae, Nandinaceae, and None of the Papaveraceae in the present Podophyllaceae). Recent data are at hand on study occur in wet forest habitats. Bocconia wood anatomy of some of these families, is a tree in shrubby montane forest; however, such as Lardizabalaceae (Carlquist 1984a) bark and pith succulence in Bocconia suggest and Ranunculaceae (Sieber & Kucera 1980). the existence of features that modify xylary Wood anatomy of Papaveraceae can be com­ adaptation to dry conditions. The roots and pared with that of these other families in an stern hases of Dicentra chrysantha are also attempt to see to what degree wood anatomy succulent and rich in starch. Dendromecon reinforces the idea that the families named and Romneya are not at all succulent, and in form a natural grouping. these genera one may expect wood anatomy Little data have been accumulated on to reflect ecology more directly. wood anatomy of Papaveraceae. As the sum­ Although only a single species of Dendro­ mary of Fedde (1936) shows, most work on mecon is recognised here, in accordance with the anatomy of the farnily emphasised study the treatment of Munz (1974), that species of laticifers or leaf anatomy. Harvey-Gibson does possess considerable ecological ampli­ and Bradley (1917) commented only briefly tude. Dendromecon rigida subsp. rhamnoides on features of wood anatomy (e.g., helical occurs in the moderate climate of offshore is­ thickenings in tracheids of Romneya). The lands of California, whereas D. rigida subsp. brief account of wood of Papaveraceae con­ rigida can be found in summer-hot chaparral tains virtually all of what we know. Data on areas with less than 30 cm annual rainfall. Dendromecon and Romneya were provided The term 'vessel restriction patterns' has recently by Carlquist and Hoekman (1985). been applied to those instances in which ves­ sels are confined (to various degrees) to the Materials and Methods central portions of fascicular areas and do not Wood sampies were available in dried contact ray cells. Attention was called to an form except for Dendromecon rigida subsp. instance in Valeriana (Carlquist 1988). The rigida and Dicentra chrysantha; portions of phenomenon has been illustrated in Launea these were preserved in formalin-acetic-alco­ (Asteraceae), and the term invented in that hol. Woods were sectioned on a sliding mi­ instance (Carlquist 1988). The occurrence of crotome except for Dicentra. Sections of vessel restriction in certain of the Papavera­ greater thickness (e.g., 30~) were prepared ceae studied here has led to an assessment of for Bocconia and Hunnemannia in order to this phenomenon in terms of its occurrence minimise collapse of vessels in transections. systematically and with respect to habit. The Thick sections were not disadvantageous be­ phenomenon of vessel restriction does not cause cell size is greater in these genera than seem related to the 'isolation' syndrome of in the other genera. For the sterns and roots rays (e.g., the wide or aggregate rays in Fa­ of Dicentra chrysantha, an alternative meth­ gaceae), which Braun (1970) described from od involving softening in ethylene diamine woody species quite unlike Papaveraceae in followed by sectioning portions in paraffin habit. on a rotary rnicrotome (Carlquist 1982a) was The systematic affinities of Papaveraceae employed. Sections were stained in safranin; and the constitution of an order that may be formost collections, sections were also coun­ called Papaverales or Berberidales have near- terstained in fast green. Macerations were

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prepared with Jeffrey's fluid and stained with Anatomical results safranin. Photographs utilising scanning elec­ tron microscopy (SEM) were derived from Growth rings sliding microtome sections with the use of an Growth rings are absent or nearly so in ISI WB-6 electron microscope. The mottled Bocconia (Fig. 1), Dicentra (Hg. 10), and appearance of SEM photographs presented Hunnemannia (Fig. 15). In contrast, Dendro­ here is not the result of charging; it repre­ mecon (Fig. 11) and Romneya (Fig. 16) are sents natural depositions on the vessel walls ring-porous to varying degrees. The ring po­ illustrated. rosity of these two genera takes the form of The means in Table 1 are based upon 25 largervessels in earlywood; the larger vessels measurements per feature except for vessel tend to be in smaller groupings than the late­ wall thickness, libriform fibre diameter at wood vessels, and vasicentric tracheids are widest point (as seen in transection), libri­ less abundant in earlywood than in latewood, form fibre wall thickness, and diameter of pits although they are present throughout growth on lateral walls of vessels. For these features, rings in Dendromecon and Romneya. means were derived from a few carefully se­ lected measurements. Vessel diameter was Quantitative vessel features taken at widest point within a vessel and is The number of vessels per group has been the lumen diameter. The presence of very computed in Table 1, colurnn 2. A difference narrow vessels that are elose to vasicentric between Bocconia (2.1 or fewer vessels per tracheids in diameter presented a problem, group: Fig. 1) and the other genera (3.6 or and some narrow vessels may have been in­ more vessels per group) is evident. Because advertently omitted from ca1culations. Ter­ very narrow vessels may have been missed tpinology follows the IAWA Committee on durlng measurements, the number of vessels Nomenelature (1964), except for vasicen­ per group in Dendromecon and Romneya tric tracheids, where the usage of Carlquist may be slightly higher than those recorded in (1985) and Carlquist and Hoekman (1985) is Table 1. The large groupings of vessels in followed; this usage is much like that of Met­ the latewood of Dendromecon (Fig. 11) con­ calfe and Chalk (1950). If the usage of Met­ tain an almost indefinite number of vessels calfe and Chalk (1950) and Carlquist (1985) pergroup. is not entirely uniform, that is because the Vessels wider than 100 ~m in diameter representation of vasicentric tracheids varies characterise Bocconia (Fig. 1). Next in mean somewhat from one family to another. The vessel diameter of the genera is Dicentra reader' s attention is called to the fact that (Fig. 10), in which vessel diameter is greater some authors apply the term 'vascular tra­ in roots than in stems (Table 1, colurnn 3). cheids' to what are called vasicentric tra­ Lowest in vessel diameter are Dendromecon cheids here. Vascular tracheids, in the usage rigida subsp. rigida (Fig. 11) and Romneya of Carlquist and Hoekman (1985) and Carl­ coulteri (Hg. 16). The vessels of Hunneman­ quist (1985) are restricted to latewood and nia (Fig. 15) are narrow but fluctuate season­ do not tend to surround vessels. Reasons for ally in diameter less than do those of Dendro­ adoption of the terrninology employed here mecon and Romneya. The small vessel diam­ will be found discussed by Carlquist (1985). eter of large numbers of latewood vessels in Preparation of many of the sections and the lauer two genera account for the low collection of quantitative data represent the figures (Table 1, colurnn 3). Similar results work of the junior author; the senior author were obtained for Dendromecon and Rom­ prepared photographs, text, and made addi­ neya earlier (Carlquist & Hookman 1985). tional observations on wood characteristics. Vessel density (Table 1, colurnn 4) is Some of the sampies were collected by the roughly inversely proportional to vessel di­ senior author in Peru with the aid of agrant ameter in dicotyledons at large; this tends to from the National Science Foundation, BSR- be illustrated also in Papaveraceae. Bocconia 8109910. The taxonomy of Dendromecon (Fig. 1) has the lowest number of vessels per andRomneya follows Munz (1974). mm" whereas Dendromecon rigida subsp.

Downloaded from Brill.com10/07/2021 01:25:31AM via free access Table 1. Wood characteristics of Papaveraceae. I~

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Species Colleclion 2 3 4 5 6 7 8 9 10 11 12

Bocconia arborea S. Watson Carlquist 2393 (RSA, RSAw) 18 2.0 132 13.5 357 3.5 23 726 2.8 1758 7.9 3491 Wiens 2535 (RSA, RSAw) 4 2.1 127 24.1 409 3.5 19 598 3.5 1067 4.7 2155 B.frutescens L. Davidson 5131 (RSA, RSAw) 24 2.0 129 9.2 269 2.6 30 715 4.0 1730 11.0 3772 B. integrifolia H. & B. Carlquist 7044 (RSA, RSAw) 25 1.7 135 11.6 241 3.4 16 614 3.0 1404 6.0 2805 Carlquist 7068 (RSA, RSAw) 17 1.9 143 6.7 360 3.5 32 711 3.5 1443 5.0 7684 -> Carlquist 7111 (RSA, RSAw) 14 1.5 144 7.7 386 3.4 19 731 4.0 1533 4.3 7219 ~ Downloaded fromBrill.com10/07/2021 01:25:31AM Davidson 5046 (RSA, RSAw) 11 1.7 107 17.4 270 3.5 19 585 3.0 1556 8.9 1660 OJ B. vulcanica Donn. Smith Davidson 3317 (RSA, RSAw) 18 2.0 182 9.2 308 2.7 29 677 3.7 1213 5.7 6093 E. Dendromecon rigida Benth. ;-" g. subsp. rhamnoides (Keil.) Raven Thorne 34845 (RSA, RSAw) 38 6.4 63 89.3 330 2.5 19 514 3.5 1385 5.1 233 ? D. rigida subsp. rigida R.S.A.B.G. prop. no. 5865 6 14.7 43 256.0 302 2.5 13 474 3.2 1630 4.5 51 Diantra chrysantha (H. & A.) Walp. STEM Carlquist 15940 (RSA) r 15 3.6 87 36.2 200 2.4 17 294 2.1 > 1 cm >10 481 <: ROOT Carlquist 15940 (RSA) 10 5.0 100 38.6 277 2.6 24 514 2.5 > 1 cm >10 718 ?- Hunnemannia fumariaefolia Sweet Carlquist 2392 (RSA, RSAw) 14 14.4 54 80.0 142 3.5 19 307 2.0 > 1 cm >10 96 1.0 Romneya coul/eri Harv. R.S.A.B.G. prop. no. 6549 4 17.4 37 227.8 196 2.5 '""'w 12 391 2.8 > 1 cm 5.6 32 ::--

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* vessel diameter limes vessel element length divided by number of vessels per mm2• I~ 00 Carlquist & Zona - W ood anatomy of Papaveraceae 257 rigida and Romneya coulteri have the high­ Forms of helical sculpture occur on vessel est values. walls of Papaveraceae. In Dicentra and Hun­ Vessel element length (Table 1,column 5) nemannia, shallow grooves interconnect pit ranges from 409 llIl1 in Bocconia arborea to apertures. These grooves are not readily vis­ 142 11m in Hunnemanniafumariaefolia. Ves­ ible, and can be demonstrated where portions sel elements in Papaveraceae are relatively of vessel walls are shaved away by section­ short compared to those in dicotyledons at ing in such a way that depressions on the in­ large (mean = 649 11m: Metcalfe & Chalk, ner wall surface are revealed as slitlike ap­ 1950: 1360). The majority of Papaveraceae pearances in the wall sections. In Dendro­ have vessel elements ranging from 200 to mecon and Romneya, pronounced thicken­ 360 11m in length. In view of the ontogenetic ings occur on vessel walls. In Dendromecon, changes in vessel element length found by these thickenings may be wide (Fig. 13) or Cumbie (1983) in Bocconia vulcanica, these narrow (Fig. 14), and may tend to anasto­ results are worthy of examination. mose (Fig. 14). The thickenings do not tend Vessel wall thickness (Table 1, column 6) to ron predorninantly between pit apertures; ranges from 2.4 11m to 3.9 11m in Papaver­ rather, the thickenings may overlie pits (Fig. aceae. This range is small. Bocconia, the 13, thickenings overlie most pits; Fig. 14, genus with the widest vessels, also has the thickenings over some pits). Pit apertures do greatest vessel wall thickness, although not penetrate the thickenings. In Romneya, the conspicuously so (Fig. 1). thickenings are more densely crowded (Fig. 18), so that only slitlike portions of the wall Qualitative vessel features are not covered by them. No helical sculpture Perforation plates are simple throughout was observed on vessel walls of Bocconia. Papaveraceae. Lateral wall pitting consists of Thin-walled tyloses were observed in three alternate circular to somewhat elliptical pits. collections of Bocconia integriJolia (Fig. 1). Intervascularpits are similar in size to vessel­ parenchyma pits; mean diameters for the for­ ImperJorate tracheary elements mer are shown in parentheses in the follow­ As reported by Metcalfe and Chalk (1950), ing: Dendromecon (6 11m); Dicentra (7 11m); borders are not present on pits of the ordinary Hunnemannia (6 11m); Romneya (5 11m). In imperforate tracheary elements; following the Bocconia, vessel-parenchyma pits are about IAWA Committee on Nomenclature (1964) 50% greater in horizontallength than the in­ usage, these cells are termed libriform fibres tervascular pits (compare Fig. 3 with Figs. 4, here. In Table 1, column 7, mean diameter of 5); intervascular pits are as follows in mean libriform fibres at widest point (as seen in diameter: B. arborea (8 11m); B. Jrutescens transection) is given. The figure for Bocconia (14 11m); B. integriJolia (11 11m: Fig. 3); B. (Fig. 1) ranges upward from 19 11m, whereas vulcanica (15 11m). In Bocconia, vessel-pa­ Dendromecon (Fig. 11) and Romneya (Fig. renchyma pits have much wider apertures 16) have libriform fibres less than 19 11m in (Figs. 3, 4) than do intervascular pits (Fig. diameter. Hunnemannia (Fig. 15) is interme­ 3). Intervascular pits in Papaveraceae have diate.Libriform fibres are wider in roots (Fig. pit aperture shape that ranges from nearly 10) of Dicentra chrysantha than in sterns. circular to markedly elliptical. With respect to libriform fibre length Some pits on lateral vessel walls of Boc­ (Table 1, column 8), one finds the range in conia vulcanica appear to be vestured when Bocconia is from 585 11m to 731 11m. The viewed with a light microscope. Examination shortest libriform fibres occur in Dicentra of these with SEM reveals that these pits have chrysantha roots and in the sterns of Hunne­ somewhat irregular outlines to their margins, mannia and Romneya. The fact that libriform and a tendency of pit aperture margins to be fibres are nearly twice as long in sterns as bent into the pit cavities (Fig. 9). This has they are in roots of Dicentra chrysantha is also been figured (with a different photo­ noteworthy, because the difference in length graph) for this species elsewhere (Carlquist of vessel elements between the two organs in 1988). this species is not so great.

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Librifonn fibre wall thickness is shown in con rigida subsp. rigida, in which strands of Table 1, column 9. Although fibre walls are two cells are also common. thickest in Bocconia (Fig. 1), these fibres do Quantitative features of rays not appear thick because the diameter of li­ In Table 1, column 10, multiseriate ray brifonn fibres in Bocconia is relatively great. height is given. Within Bocconia, the range is Relatively thin walled librifonn fibres can from 1067 J.lID to 1758 J.lID - a relatively small be seen in Dendromecon (Fig. 11), Dicentra range. The rays shown for B. integrifolia (Fig. 10), Hunnemannia (Fig. 15) and Rom­ (Fig. 2) are typical for the genus. The height neya (Fig. 16). of multiseriate rays in Dendromecon (Fig. With the aid of liquid preserved material, 12) lies within the range given for Bocconia. one can demonstrate nuclei in the librifonn The rays of Dicentra, Hunnemannia, and fibres of Dendromecon rigida subsp. rigida. Romneya (Fig.17) are much taller; estimat­ One can find starch in librifonn fibres of ing the height of rays in these genera proved Bocconia (not liquid preserved) and Dicentra difficult because many rays in the sections (liquid preserved). Thus, living (or nucleat­ studied are Ion ger than the seetion; this ac­ ed) fibres can be claimed for three genera. counts for the approximate values in Table 1. The fact that materials of Hunnemannia and If one computes multiseriate ray width in Romneya were dried may account for ab­ tenns of cell number at widest point (Table 1, sence of contents in librifonn fibres of these column 11), one obtains figures for the spe­ two genera. A small amount of fibre dimor­ cies of Papaveraceae that tend to parallel ray phism occurs in Bocconia and Hunneman­ height. Multiseriate rays of Bocconia (Fig. 2) nia, in which shorter, wider fibres (resem­ and Dendromecon (Fig. 12), which range bling narrow vessel elements in length and from 5.0 to 8.9 cells, are less wide than those diameter at widest point) occur near vesse1s. of Dicentra, Hunnemannia, and Romneya Vasicentric tracheids were reported earlier (Fig. 17), in which mean ray width at widest for Dendromecon and Romneya (Carlquist point exceeds 10 cells. 1985; Carlquist & Hoekman 1985). Vasicen­ Uniseriate rays are so scarce in Papaver­ tric tracheids occur in the collections of these aceae that they have been omitted from two genera in the present study. Vasicentric Table 1. tracheids occur in smaller numbers in the woods of Dicentra and Hunnemannia, and Qualitative ray features were not observed in Bocconia. In Dendro­ Multiseriate rays in Papaveraceae consist mecon and Romneya, vasicentric tracheids of upright or square cells on lateral surfaces are more abundant in latewood than in early­ (sheathing cells) of the rays (Figs. 12, 17). wood, although present in appreciable num­ Upright cells are more common in rays of bers in earlywood. Bocconia (Fig. 2), where they are present not merely on surfaces but throughout rays; Axial parenchyma some procumbent cells are present in small Paratracheal axial parenchyma fonning numbers in Bocconia rays. In Hunnemannia, sheaths one to three cells in thickness occurs markedly elongate cells fonn the central por­ in Bocconia (Fig. 1). In Dendromecon, Di­ tion of a ray, while upright cells comprise the centra, Hunnemannia, and Romneya, axial periphery and square to moderately procum­ parenchyma is sparser and is scattered among bent cells occur between. The abundance of the vessels, which are typically in large upright cells in rays of most Papaveraceae groups in these genera; the distribution can be exceeds that specified in the definition by considered vasicentric scanty (this tenn used Kribs (1935) of Heterogeneous Type 11; uni­ by Kribs, 1937, and other authors). seriate rays, present in that type, are absent Axial parenchyma most commonly occurs or nearly so in Papaveraceae. Because of the in strands of two cells in Papaveraceae; pa­ abundance of upright cells in rays in Papav- renchyma not subdivided into strands was encountered commonly only in Dendrome- (text continued on page 263)

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1111111 I

Figs. 1-5. Wood section of Bocconia integrifolia, Carlquist 7111. - 1: Transeetion; tyloses present in vessels. - 2: Tangential section; rays contain a large proportion of upright cells. - 3-5: Pitting in vessel walls from radial seetions. - 3: Intervascular pitting. - 4: Vessel-axial parenchyma pitting with narrowly elliptical pit apertures. - 5: Vessel-axial parenchyma pitting with wide apertures. - Figs. 1,2, magnification scale above Fig. 1 (divisions = 10 J.1m); Figs. 3-5, scale above Fig. 3 (divisions = 10 ~m).

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Figs. 6-10. Wood sections of Bocconia and Dicentra. - 6: B. arborea, Carlquist 2393, crystals in ray cell, tangential section. - 7: B.frutescens, Davidson 5131, rhomboidal crystal in ray cell, radial section. - 8: B. integrifolia, Carlquist 7111, cluster of crystals, radial section. - 9: B. vul­ canica, Davidson 3317, vessel-axial parenchyma pitting from tangential section, showing ir­ regular pit margins. - 10: D. chrysantha, Carlquist 15940, transection of root; vessels are re­ stricted to centre of fascicular zones. - Figs. 6-8, scale above Fig. 3; Fig. 9, scale at upper left (bracket = 10 11m); Fig. 10, scale above Fig. 1.

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Figs. 11-14. Sections of Dendromecon rigida subsp. rigida, R.S. A.B.G. prop. no. 5865. -11: Transection; vessels in diagonal aggregations. - 12: Tangential section; upright, square, and procumbent cells present in about equal numbers. - 13 & 14: SEM photographs of vessel walls from tangential section; mottled appearance is caused by deposits on wall. - 13: Wider helical thickenings in wide vessel plus (left) narrow vessel. - 14: Narrower helical thickenings in wide vessel. - Figs. 11 & 12, scale above Fig. 1; Fig. 13 & 14, bracket in Fig. 9.

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Fig. 15. Wood section of Hunnemanniafumariaefolia, Carlquist 2392; vessels restricted to cen­ tral portions of fascicular areas. - Figs. 16-18: Wood seetions of Romneya coulteri, R.S.A.B.G. prop. no. 6549. - 16: Transeetion; latewood with many narrow vessels and vasi­ centric tracheids 1/5 distance from top of photograph. - 17: Tangential seetion; narrow vessels and vasicentric tracheids (darker staining areas) are storied. - 18: SEM photograph of vessel from tangential section; helical thickenings are narrow, crowded. - Figs. 15-17, scale above Fig. 1; Fig. 18, bracket = 10 Ilm.

Downloaded from Brill.com10/07/2021 01:25:31AM via free access Carlquist & Zona - Wood anatomy of Papaveraceae 263 eraceae, they should be designated Paedo­ very limited local portions of tangential sec­ morphic Type II, according to the scheme of­ tions in Bocconia and Hunnemannia. Storied fered by Carlquist (1988), or transitional to cells in these two genera may inc1ude wider that type. fibres, axial parenchyma, narrow vessels, Mean ray cell wall thickness is moderate and vasicentric tracheids. in Papaveraceae: Bocconia, 1.6-2.2 ~m; Dendromecon, 2.2 ~m; Dicentra, 1.4 ~m Conclusions (root) to 2.0 ~m (stern); Hunnemannia, 2.3 ~; Romneya, 2.0 ~m. Pits among ray cells Vessel restrietion patterns are predominantly simple, although some The term 'vessel restriction patterns' was bordered pits were observed on ray cells of devised to descrlbe instances in Valeriana of all genera except Dicentra. the Valerianaceae (Carlquist 1983) and Lau­ Starch was seen in ray cells of Bocconia nea of the Asteraceae (Carlquist 1988) in andDicentra (root, lower stern, but not upper which vessels occur in eentral portions of stern). Crystals (nature confirmed with polar­ fascicular secondary xylem, and thus only ised light), are present in ray cells of Bocco­ libriform fibres but not vessel elements are in nia, but were not seen in wood of the other contact with rays. The oceurrenee of this genera. In B. arborea (Fig. 6), various num­ phenomenon in Dicentra (Fig. 10) and, to a bers of smaller rhomboidal crystals occur in lesser extent (occasional vessels touching a minority of ray cells. They vary from clear­ rays), in Hunnemannia (Fig. 15) leads one to ly angular to somewhat rounded in outline; ask if this occurs in other genera of the order rounded outlines of crystals have occasional­ Papaverales. Most Berberidaceae have large ly been observed in various dicotyledons. In vessel groupings which eome into contaet ß. Jrutescens, slightly larger and clearly with rays here and there. However, in Nan­ rhomboidal crystals occur in solitary fashion dina domestica Thunb., several layers of li­ in a scattering of ray cells (Fig. 7). A few ray briform fibres lie between the groupings of cells of B. integrifolia have minute rhomboi­ vessels (including some vasieentric tracheids) dal crystals, which tend to be grouped (Fig. and the rays. A figure of a wood transeetion 8). The difference between modes of occur­ of Berberis darwinii Hook. by Metcalfe and rence in B. arborea and B. integrifolia is not Chalk (1950: 60) shows no vessels in contact great. Crystals have not been reported hither­ with rays. The photographs by Sieber and to in wood of Papaveraceae, although Met­ Kucera (1980) of Clematis vitalba L. and my calfe and Chalk (1950) report crystals in plant own materials of C. lasiantha Nutt. indicate portions other than wood for the family. few vessels in contaet with rays in that genus Dadswell and Record (1936) report a few of Ranuneulaceae. large open radial canals in rays of Bocconia. However, the oceurrenee of vessel re­ No such canals were observed in the present striction patterns in Asteraeeae and in Valeri­ study, despite abundance of material; the pos­ anaeeae may indicate that vessel restriction sibility must be taken into account that the patterns are less of phyletie than of physio­ canals reported by Dadswell and Record were logical signifieanee. If one compares the spe­ traumatic in nature or the result of shrinkage eies that show vessel restrietion patterns most patterns due to drying. No laticifers were ob­ clearly, all have sterns of limited diameter or served in rays of any of the Papaveraceae duration; they are either woody herbs, short­ studied here, nor have any been found in lived shrubs, or, as in the case of Nandina, a wood of the family previously. shrub with canelike sterns each of which lasts for only a few years. In vessel restrietion, Storied structure vessels contact axial parenchyma but do not In Romneya (Fig. 17), one finds storying have direct contact with radial parenehyma. If in narrow vessels and vasicentric tracheids as contacts between axial and ray parenehyma, weIl as in vessels and axial parenchyma in eommon in most dicotyledonous woods, zones where tracheids are abundant. Small form a system for transferring photosynthates numbers of storied cells were observed in both radially and vertieally within the wood,

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vessel restriction may represent minimal se­ secondary xylem for various periods of time lective value for radial translocation of photo­ of features characteristic of metaxylem; this synthates in a plant. Minimal contact between phenomenon occurs in particular herbs and vertical and horizontal parenchyma systems is herblike growth forms such as succulents, assumed here because the parenchyma in Pa­ rosette trees, and annuals. Cumbie (1983) paveraceae (as in the other groups with vessel has rightly identified features of the wood of restriction patterns) is vasicentric; thus the ra­ Bocconia vulcanica as exemplifying paedo­ dial photosynthate-conduction system (rays) morphosis; he uses the age-on-Iength curve is unlikely to form contacts with the vertical (Carlquist 1962) which shows a descending photosynthate-conducting system (axial pa­ length of vessel element length in instances of renchyma). This is reminiscent of rayless­ paedomorphosis (as opposed to an ascending ness, in which radial translocation of photo­ pattern for typical woody species). Length of synthates must be very low (axial parenchy­ libriform fibres in Bocconia vulcanica neither ma is not prominent either in most instances increases nor decreases. Cumbie (1983) also of raylessness). If there is not a selective identifies as paedomorphic the tendency in B. value for radial translocation of photosyn­ vulcanica forfew rays to be initiated after the thates in taxa with vessel restriction patterns, onset of secondary growth, and the tendency one would still need to explain why vessel for few horizontal divisions to occur in ray restriction is of any value. One possibility is initials (thus upright cells continue to pre­ found in the tendency of vessels to be sheath­ dominate in rays and procumbent cells remain ed by libriform fibres in certain plants. For comparatively few). The present study con­ example, in scandent species of Thunbergia, firms these features and their interpretation in rays may be absent, but axial parenchyma Bocconia. Although the present study has not (which may contain phloem strands) occurs developed length-on-age curves, it is notable as islands or strips in the secondary xylem; that the collection of Bocconia with the long­ the vessels, however, are invariably sheathed est vessel elements, B. arborea, Wiens 2535, by fibres. Vessel restriction may have the has the least accumulation of secondary xy­ same effect as sheathing of vessels by fibres. lem. The large pit apertures of vessel-paren­ One ean imagine that sheathing ofvessels by ehyma pits in Bocconia may be associated fibres might have some positive value. For with lowered mechanieal strength of wood, example, in a vine such as Thunbergia, the which appears to characterise certain woods wide vessels are relatively vulnerable and with paedomorphosis (Carlquist 1975). might experienee fewer failures in their water Dendromecon, Hunnemannia, and Rom­ eolurnns when sheathed by fibres (Carlquist neya show relatively few features related to & Zona 1988). Alternatively, one eould ima­ paedomorphosis, and Cumbie (1983) is justi­ gine that if vessels were restrieted to the een­ fied in suggesting that Dendromecon could tral portion of a faseieular area of secondary have had a woody ancestry, whereas Bocco­ xylem (axial secondary xylem zones between nia may have had herbaceous or more nearly rays), there would be a greater tendency for herblike ancestors and may not be c10sely re­ radial chains of vessels to form, increasing lated to Dendromecon. The storied wood pat­ the potential degree of vessel grouping, tern of Romneya is probably an indication of which is c1aimed to enhance conductive safe­ a nonpaedomorphic wood, because storying ty (Carlquist 1984b). The concept ofisolation is not common in woods with paedomorpho­ rays entirely composed of procumbent cells sis (although Piperaceae are an exception: (Braun 1970) represents a different phenom­ Carlquist 1962). Storying may develop over enon (one which may enhance efficient radial time in a wood, ratherthan shortly after on set conduction of photosynthates), and should of secondary growth. Although woody rela­ not be confused with vessel restriction. tives of Papaveraceae, such as Berberidaceae and Decaisnea (Lardizabalaceae), are shrubs Paedomorphosis branched from the base rather than subarbor­ The theory of paedomorphosis (Carlquist eal, they must be c1assified as woody, just as 1962) was devised to explain occurrence in must Dendromecon.

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Relationships primitive wood features among the families As cited in the Introduction, Papaveraceae and genera. are generally conceded by recent phylogenists to be c10sely related to Berberidaceae, Lardi­ Ecology zabalaceae, Menispermaceae, Ranunculaceae, Within Papaveraceae, computation of the and Sargentodoxaceae, as weIl as several fa­ Mesomorphy ratio (Table 1, column 12) re­ milies that are herbaceous (Circaeastraceae, veals that Bocconia and Dicentra have rela­ Glaucidiaceae, Kingdoniaceae). The wood tively mesomorphic woods. Both of these anatomy of Papaveraceae contains aseries of genera have markedly succulent cortex and features that validate this relationship (data pith, as weIl as, to a limited extent, rays. from Metcalfe & Chalk 1950; Sieber & Kuce­ Dendromecon and Romneya show wood ra 1980; Carlquist 1984a): vessels with sim­ xeromorphy in ways other than the density of ple perforation plates (scalariform in Decais­ vessel elements and their narrowness and nea); lateral wall pitting of vessels alternate shortness, as reflected in the Mesomorphy (intervascularpitting similarto vessel-ray pit­ ratio. Degree of grouping of vessels has been ting); helical thickenings present in vessels cited, in families with libriform fibres or (presentinBerberis of Berberidaceae, Akebia fibre-tracheids (as opposed to true tracheids) of Lardizabalaceae, Clematis of Ranuncula­ as indicative of degree of xeromorphy (Carl­ ceae); libriform fibres present (fibre-tracheids quist 1966, 1984b). Using vessel grouping in Lardizabalaceae, tracheids in Menisperma­ figures (Table 1, column 2) as an indicator of ceae); libriform fibres nucleated (some sep­ xeromorphy, one can arrange the genera of tate); axial parenchyma vasicentric scanty Papaveraceae from most mesomorphic to (absent in Berberidaceae); rays exc1usively most xeromorphic: Bocconia, Dicentra, Hun­ multiseriate or nearly so, tall and wide, com­ nemannia, Dendromecon, Romneya. This se­ posed mostly of procumbent cells. ries corresponds to ecology of these genera: Several wood features unite Papaveraceae Dendromecon and Romneya occur in chapar­ with some but not all of the woody families ral or coastal sage. Dicentra chrysantha does cited above. For example, vasicentric tra­ occur in sites that are like these, but its rela­ cheids, common in Dendromecon and Rom­ tively mesomorphic wood can be explained neya, occur in Berberis (inc1uding Mahonia), on the basis of the succulence of roots and Nandina, and Clematis (Carlquist 1985). lower sterns, and the fact that upper sterns Crystalsoccurin raycells of Stauntonia (Lar­ die back annually. dizabalaceae) as weIl as those of Bocconia. Vasicentric tracheids are abundant in Den­ In addition to Dendromecon and Romneya, dromecon and Romneya, supporting the idea papaveralean genera with diagonal aggrega­ that these genera should be regarded as the tions of vessels inc1ude Berberis, Nandina, most xeromorphic in the family. Vasicentric and Clematis. tracheids and narrow vessels are moderately If one is to rank Papaveraceae with respect common in Hunnemannia, less common in to degree of primitiveness in Papaverales on Dicentra. Vasicentric tracheids prove to be a the basis of wood features, one finds that two key to understanding diagonal aggregations families have somewhat more primitive wood ofvessels (Baas etal. 1984; Carlquist 1987). features: fibre-tracheids may be found in Lar­ The occurrence of these vessel aggregations dizabalaceae (one genus of which, Decaisnea, can be considered a maximal form of xero­ has scalariform perforation plates); true tra­ morphy (orconductive safety) in phylads that cheids are present in Menispermaceae. Papa­ possess vasicentric tracheids (Carlquist 1987, veraceae retains axial parenchyma, the ab­ 1988). sence of which in Berberidaceae must be The systematic and ecological distribution counted a specialisation. Thus, Papaveraceae of helical thickenings in vessels of dicotyle­ can be considered of medium advancement dons suggests adaptation both to cold (as in within Papaverales. The hypothesis that Pa­ Ilex: Baas 1973) and drought (Carlquist paverales as an order is primitively woody 1982b). Helical thickenings are present in seems to be supported by the distribution of vessels of Dendromecon even in frost free

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localities, such as Santa Catalina Island, and Braun, H. J. 1970. Funktionelle Histologie in montane areas where frost occurs, but one der sekundären Spross achse. I. Das Holz. must note that even in the most extreme Den­ Handbuch der Pflanzenanatomie IX (1): dromecon and Romneya localities with re­ 1-190. Borntraeger, Berlin, Stuttgart. spect to winter cold, frost is probably too Carlquist, S. 1962. A theory of paedomor­ mild to account for selective value of helical phosis in dicotyledonous woods. Phyto­ thickenings in vessels. Adaptation to drought morphology 12: 30-45. may explain these cases of helical sculpture. - 1966. Wood anatomy of Compositae: a Presence of helical thickenings does not seem summary, with comments on factors in­ to be a relictual feature in dicotyledons be­ fluencing wood evolution. Aliso 6: 25-44. cause one can find many families (even gen­ - 1975. Ecological strategies of xylem evo­ era) in which some species possess helical lution. Univ. Calif. Press, Berkeley, Los thickenings (the species of colder or drier Angeles, London. areas) whereas the species from less extreme - 1982a. The use of ethylenediamine in sof­ sites lack the thickenings. tening hard plant structures for paraffin Thus, Papaveraceae show a wide diversity sectioning. Stain Tech. 57: 311-317. in ecoiogical adaptation. The wood features - 1982b. Wood anatomy of Onagraceae: of Dendromecon and Romneya are much like further species; root anatomy; significance those of Berberis (including Mahonia) from of vestured pits and allied structures in di­ comparable habitats. Bocconia, however, is cotyledons. Ann. Missouri Bot. Gard. 69: notably more mesomorphic, and does not 755-769. correspond to any other genus of Papaverales - 1983. Wood anatomy of Calyceraceae in its growth form. Comparable in habit and and Valerianaceae, with comments on degree of wood xeromorphy are such genera aberrant perforation plates in predomi­ as Wigandia (Hydrophyllaceae) or arbores­ nantly herbaceous groups of dicotyle­ cent species of Nicotiana (Solanaceae). dons. Aliso 10: 413-425. These two examples are very pertinent be­ - 1984a. Wood and stern anatomy ofLardi­ cause in both cases, the plants have an An­ zabalaceae, with comments on the vining dean habitat much like that of localities habit, ecology, and systematics. Bot. J. where Bocconia could be found. Linn. Soc. 88: 257-277. The fact that Dendromecon rigida subsp. - 1984b. Vessel grouping in dicotyledons: rigida from cultivation has wood that ranks significance and relationship to imperfor­ as much less mesomorphic on a quantitative ate tracheary elements. Aliso 10: 505- basis than that of a specimen of D. rigida 525. subsp. rhamnoides collected from the wild - 1985. Vasicentric tracheids as a drought shows that the genetic nature of wood in survival mechanism in the woody flora of these two subspecies is weIl fixed, and culti­ southern California; review of vasicentric vation (with water availability greater than in tracheids. Aliso 11: 37-68. the wild) evidently has not altered the xero­ - 1987. Diagonal and tangential vessel ag­ morphic nature of the wood appreciably. gregations in wood: function and relation­ ship to vasicentric tracheids. Aliso 11: References 451-462. Baas, P. 1973. The wood anatomical range in - 1988. Comparative wood anatomy. Sprin­ Ilex (Aquifoliaceae) and its ecological ger Verlag, Heidelberg (in press). and phylogenetic significance. Blumea - & D.A. Hoekman.1985. Ecological wood 21: 193-258. anatomy of southern Californian woody - , P.M. Esser & M.E. T. van der Westen. plants. IAWA Bull. n.s. 6: 319-347. 1984. Systematic andecologicalwood anat­ - & S. Zona. 1988. Wood anatomy of omy of the Oleaceae with special refer­ Acanthaceae: a survey. Aliso 12: 201-227. ence to dendriticvessel patterns. In: S. Sudo Cumbie, B.G. 1983. Developmental changes (ed.), Pacific Regional Wood Conference, in the wood of Bocconia vulcanica Donn. Tsukuba, Ibaraki,Japan: 153-155. Smith. IAWA Bull. n.s. 4: 131-140.

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Dadswell, H.E. & S.J. Record. 1936. Iden­ - 1937. Salient lines of specialization in the tification of woods with conspicuous rays. wood parenchyma of dicotyledons. BuH. Trop. Woods 48: 1-30. Torrey Bot. Club 64: 177-186. Dahlgren, R. M. T. 1980. A revised system of Metcalfe, C.R. & L. Chalk. 1950. Anatomy classification of the angiosperms. Bot. J. of the dicotyledons. Clarendon Press, Ox­ Linn. Soc. 80: 91-124. ford. Fedde, F. 1936. Papaveraceae. In: A. Engler Munz, P.A. 1974. A flora of southern Cali­ & K. Prantl (eds.), Die natürlichen Pflan­ fornia. Univ. Calif. Press, Berkeley, Lon­ zenfamilien ed. 2, 17b: 5-145. Engel­ don, Los Angeles. mann, Leipzig. Sieber, M. & L.J. Kucera. 1980. On the stern Harvey-Gibson, R.J. & M. Bradley. 1917. anatomy of Clematis vitalba L. IAW A Contribution towards a knowledge of the Bull. n.s. 1: 49-54. anatomy of the lower dicotyledons. I. The Takhtajan, A. L. 1987. Systema magnolio­ anatomy of the stern of the Papaveraceae. phytorum. Officina Editoria 'NAuKA', Trans. Roy. Soc. Edinburgh 51: 589- 608. Leningrad. IAWA Committee on Nomenclature. 1964. Thorne, R.F. 1976. A phylogenetic classifi­ Multilingual glossary of terms used in cation of the Angiospermae. Evol. Biol. wood anatomy. Konkordia, Winterthur. 9: 35-106. Kribs, D.A. 1935. Salient lines of structural specialization in the wood rays of dicoty­ ledons. Bot. Gaz. 96: 547-557.

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