Bota,ümt Jsernat of the Linnean Society t984), 88: 257—277. With 26 figures

Wood and stem anatomy of , with comments on the vining habit, ecology and systematics

SHERWIN CARLQUIST, F.L.S.

Claremont Graduate School, Pomona College, and Rancho Santa Ana Botanic Garden, Claremont. Ca4fornia 91711, U.S.A.

Received October /983, acceptedfor publication March 1984

CARLQUIST, S., 1984. Wood and stem anatomy of Lardizabalaceae, with comments on the vining habit, ecology and systematics. Qualitative and quantitative data, based mostly upon liquid- preserved specimens, are presented for , Bsquila, , Hslboeltia, JJardi.abala, Sinofranchetsa and Stauntonta. Because Decazsnea is a whereas the other genera are vines, anatomical differences attributable to the scandent habit can be considered. These include exceptionally wide vessels, a high proportion of vessels to trachcids (Or other imperforate tracheary elements) as seen in transection, simple perforation plates, multiseriate rays which are wide and tall, and pith which is partly or wholly scierenchymatous. With respect to ecology, two features are discussed: spirals in narrower vessels may relate to adaptation to freezing in the of colder areas, and crystalliferous sclereids seem adapted in morphology and position to deterrence of phytophagous insects or herbivores. The wood may provide mechanisms for maintaining conduction even if wider vessels are deactivated tethporarily by formation of air embolisms. Wood and stem anatomy of Lardizabalaceae compare closely to those of Berberidaeeae and of Clematis (), as well as to other families of Berberidales. Decaisnea is more primitive than these in having consistently scalariform perforation plates and in having scalariform pitting on lateral walls of vessels. A tentative listing of anatomical features which may correspond to generic limits is given.

KEY WORDS:—Ecological — anatomy — Lardizahalaceae — vegetative anatomy —

vines — wood anatomy.

CONTENTS

Introduction 257 Material and methods 259 Anatomical descriptions of wood 259 Anatomical descriptions of bark and pith 270 Anatomy and the vining habit 271 Ecological conclusions 273 Systematic and evolutionary conclusions 274 References 276

INTRODUCTION Only one of Lardizabalaceae, Decaisnea, is shrubby; the remainder are vines. Because wood of neither vines nor has been studied as much as 257 0024—4074/84/040257+21 503.00/0 © 1984 The Linnean Society of London 13 258 S. CARLQUIST that of , the lack of a monographic account of wood anatomy in the family to date is understandable. The summary of Metcalfe & Chalk (1950) represents the best summary to date. An excellent study of anatomy of Lardizabalaceae by Réaubourg (1906) has been little cited because of its limited availability. Réaubourg’s study deals with the vegetative and floral anatomy of the family but slights wood anatomy, presumably because of lack of material. Réaubourg’s monograph includes cuneata (Oliver) Rehd. & Wilson under the name curteata Oliver. Because Sargentodoxa is placed in its own family by various authors, it is omitted from the present study. Various papers give oblique mention to the wood of Lardizabalaceae. The tracheids and fibriform vessels of the family were viewed by Lemesle (1974a, b, 1955, 1956) largely because of his attempt to incorporate tracheary elements of those types in this and other families into a phylogenetic context which could include cycadophytes as well as flowering . A paper by Schönfeld (1954) on a fossil genus of uncertain age from Patagonia, Lardiabaloxjlon5 compares the wood of that fossil and of , and offers some comments on wood features of the other genera. The family Lardizabalaceae consists of about 30 species in eight genera (Cronquist, 1981). However, the geographical distribution of these genera and species makes assemblage of a liquid-preserved collection of stem portions difficult. Fortuitous travels provided me with species in all but one of the genera. Material of Franch. was provided by the Botanic Garden of Lund. The Goteborg Botanic Garden kindly contributed material of chinensis Hemsley. During the summer of 1982, travel in Japan under the auspices of the Japan Society for the Promotion of Science permitted collection in natural habitats of Akebia trfoliata (Thunb.) Koidz. (near Hakone, Honshu), A. quinata Decne. (near Nagasaki, Kyushu), and hexaphyl1a Decne. (summit of Ishigaki I., Ryukyu Is.). During October 1982 field work in Chile yielded trfo1iata Decne. and Lardiaba1a biternata R. & P. (both in Concepcion Province). Wood and stem anatomy of Lardizabalaceae provide potential aids for placing the family in a phylogenetic system, although the systematic location of the family does not seem controversial. Cronquist (1981), Dahlgren (1980), Thorne (1968) and Takhtajan (1980) place Lardizabalaceae in an order, variously termed Berberidales or , in which other families are Ranunculaceae, Berberidaceae, Sargentodoxaceae, and . This group of families exhibits numerous primitive floral features, so the question arises as to whether wood features are similarly primitive and whether distinctive habits of some genera in these families (herbs, vines) alter the assemblage of primitive features. As dicotyledonous families containing vining species become better known with respect to wood structure, we can develop further concepts of how the vining or lianoid habit is related to wood anatomy and stem anatomy. Because Decaisnea is a shrub whereas the other genera of the family are vines, Lardizabalaceae is a key family for study in this respect. Wood and bark anatomy prove to be varied within Lardizabalaceae, inviting explanations for this diversity. On this account, discussions are offered concerning ecological factors which could account for these features. The anatomical diversity within the family invites comparison with the taxonomic ANATOMY OF LARDIZABALACEAE 259 system, although the fact that fewer than half of the species in the family could be included in the present studies makes such commentary preliminary at best.

MATERIAL AND METHODS The wood samples of Decaisnea fargesii and Holboellia la4folia Wall. were available dried; the remainder of the taxa were preserved in 50% ethanol. No herbarium specimen was preserved for Decaisrzea fargesii. The wood of Holboellia 1atfo1ia was removed from the specimen Mukerji & Santapan 160 in the Makino Herbarium of Tokyo Metropolitan University. For the remaining Lardizalabaceae studied here, voucher specimens are located in the herbarium of the Rancho Santa Ana Botanic Garden. Material of the dried specimens was boiled and stored in 50% ethanol preparatory to sectioning. An attempt was made to section material of all collections on a sliding microtome prior to any softening. This proved successful in some instances. Specimens with larger vessels did not section well, nor did those with large quantities of bark scierenchyma. Consequently, an alternative procedure described earlier (Cariquist, 1982) was invoked. This softening technique obviated difficulties. Histological details were not altered, although the basic nature of ethylene diamine, which is employed in that method, resulted in hydrolysis of portions of starch grains. Sections were stained with safranin or with a safranin-fast green combination. The latter staining method permitted easy observation of pit borders, sieve plates, and other details involving primary walls. Quantitative data are based on 25 measurements per feature unless scarcity of structures (e.g. rays are few in some species) necessitated use of a smaller sample. Number of vessels per mm2 was based on arbitrary scanning transections of wood. Rays were not excluded from this scanning, even if any particular field of view proved to contain rays and no vessels; the mean for this feature is correspondingly lowered by the wide rays prevalent in the vining Lardizabalaceae.

ANATOMICAL DESCRIPTIONS OF WOOD Because Decaisnea is a shrub, its wood is considered separately from that of the remaining genera. Within the vining genera, the Asiatic genera are presented before the South American genera.

Decaisneafargesii5 Lund Botanic Garden, s. n. (Figs 1—7). Growth rings present, latewood distinguished by narrower and fewer vessels, fibre-tracheids slightly narrower radially (Fig. 1). Vessels mostly solitary, most groupings consist of a pair of vessels. Number of vessels per mm2 of transection, = 93. Vessel diameter,

= 63 tm (range: 46—69 tm). Vessel wall thickness. .‘ 1.8 JIm. Vessel elements with scalariform perforation plates (Fig. 3), bars slender and minimally bordered. Number of bars per perforation plate, . = 12.8. Vessel to vessel pitting scalariform (Fig. 4). Vessel to fibre-tracheid pitting scalariform to opposite (Fig. 5). Vessel to axial parenchyma pitting scalariform chiefly (Fig. 7). Spirals lacking in all vessels. All imperforate tracheary elements may be termed fibre-tracheids by virtue of presence of borders on the pits. Pits are small 260 S. CARLQUIST

d

Figures 1—7. Decaisneafargeszi (Lund Botanical Garden, sn.), wood sections. Fig. 1. Transection: vessels comparatively narrow. Fig. 2. Tangential section: multiseriate rays narrow. Figs 3—7. details from radial sections. Fig. 3. Typical scalariform perforation plate. Fig. 4. Scalariform intervascular pitting. Fig. 5. Scalariform-opposite vessel to tracheid pitting. Fig. 6. Opposite pitting between vessels and axial parenchyma cells. Fig. 7. Scalariform vessel-ray pitting. Figs 1—2, magnification scale above Fig. 1 (finest divisions = 10 jsm). Figs 3—7, magnification scale above Fig. 3 (divisions = 10 pm). ANATOMY OF LARDIZABALACEAE 261 (2 tm in diameter) and sparse, otherwise tracheids would be said to be present. Some fibre-tracheids are septate. Tracheid length, = 768 rim. Fibres-tracheid diameter at widest point, i = 18 jim. Fibre-tracheid wall thickness, 2.8 jim. Axial parenchyma mostly vasicentric (sheaths one cell thick, incomplete around vessels or vessel groups), only a few cells distributed in diffuse fashion. Axial parenchyma in strands of five or six cells, rarely four. Rays both multiseriate and uniseriate; multiseriate rays more abundant (Fig. 2). Width of multiseriate rays, = 6.1 cells. Height of multiseriate rays, i = 1248 jim. Height of uniseriate rays, i = 255 jim. Muitiseriate portion of multiseriate rays composed of procumbent cells, with erect sheathing cells present on margins. Uniseriate wings (where present) of multiseriate rays and uniseriate rays composed of erect cells. The rays of Decaisneafargesii could be said to belong to the Heterogeneous Type hA of Kribs (1935). Pits between adjacent ray cells are bordered. Ray cells with moderately thin, lignified walls. Wood non-storied. No crystals or other deposits noted.

Akebia quinata, Carlquist 15658 (Figs 8—14). Growth rings present, vessels fewer and narrower in latewood (Fig. 8), although narrow vessels may also be present mixed with wide vessels in the earlywood; tracheids radially narrower in latewood. Vessels solitary or, in the case of narrower vessels in earlywood, in pore multiples by virtue of the large number present per unit of transection. Number of vessels = per mm2, 178. Vessel diameter, . = 46 jim (range: 28—150 jim, the majority narrower than 38 jim in diameter). Many of the narrower vessels are fibriform (for a discussion of this term, see Carlquist, l984a), fusiform in shape with small subterminal perforation plates; some of these vessel elements have perforation plates at only one end. Although the longer vessel elements are narrow, narrow but short vessel elements are not uncommon. Mean vessel wall thickness, 2.6 jIm. Perforation plates simple, although scalariform plates may be seen in the narrow vessels of late metaxylem or earliest secondary xylem. Vessel pits alternate, the pits elliptical in shape (shape and distribution holds for vessel contacts with all kinds of cells), 5—7 jim in diameter. Spiral thickenings present in narrower vessels (Fig. 11), but absent in the widest vessels. Imperforate tracheary elements are all tracheids, pits on tracheids about 5 jIm in diameter. Spirals present on walls of many tracheids. Tracheid length, = 346 jim. Tracheid diameter at widest point, = 18 Jim. Tracheid wall thickness, i = 4.5 jim. Air spaces observed among some tracheids. Axial parenchyma vasicentric scanty with a few diffuse cells (vasicentric common because of the great density of the narrower vessels). Axial parenchyma composed of four to six cells per strand. Rays multiseriate only (Fig. 9). Width of multiseriate rays, = 18 cells. Ray height i > 5 mm. rays composed of procumbent cells except for a layer of sheathing cells on margins. Margins of rays have lignified cells earlier in ontogeny than does the central portion (Figs 8, 9). Cambium of the stem is sunken toward the interior of the stem in ray areas compared to fascicular areas, so that scierenchyma formed in phloem ray areas may appear to extend into xylem rays (Fig. 8). Intercellular spaces observed among ray cells. Wood obscurely storied (Fig. 9), but cambium and secondary phloem (Fig. 10) clearly storied. Crystals and amorphous deposits not observed.

3. Fig. above scale magnification Fig. 1. 11, above Fig. scale magnification

8—10, Figs thickenings. spiral showing wood, of section radial from Vessel 11. Fig. elements.

sieve-tube in

evident storying phloem: secondary of section Tangential 10. Fig. unlignified.

left

at is ray of portion Central section. tangential 9. Wood Fig. rings. growth wide vessels,

transection: Wood 8. Fig. sections. stem and wood 15658), (Carlquist quinata Akebia 8—il Figures

ff.

: k.

•j A,•

rj 1 .

‘I

•

U

1 •l’Ii

•.

•.1l

S. CARLQUIST 262 ANATOMY OF LARDIZABALACEAE 263

FLgures 12—15. Akebia wood and stem sections. Figs 12—14. A. qunata (Carlquist 15658), transections of bark. Fig. 12. Section from secondary xylem to outside of stem; dark-staining zones of sclerenchyma and periderm evident. Fig. 13. Inner portion of periderm and subperidermal crystalliferous sciereids. Fig. 14. Crystal containing protophloem fibres (below, right) and interstitial crystal-containing sclereids (remainder of photograph). Fig. 15. A. trfo1iata (Cariquist 15698), transection of wood. Large earlywood vessel, right, is accompanied by numerous narrower vessels. Fig. 12, magnification scale above Fig. I. Figs 13, 14, magnification scale above Fig. 3. Fig. 15, magnification scale above Fig. 15 (divisions = 10 pm).

Wood

bordered. are cells ray Pits among 23). (Fig. radially elongate markedly

not are which cells

procumbent

are cells ray of majority The 5 mm. rays, 1>

of

Height

cells. 10.5 I point, widest at rays of Width only. multiseriate Rays

simple.

pits with and fusiform than rather blunt ends with cells subdivided)

once- (or

single as but strands as chiefly formed not is bands of parenchyma

The

cells.

4—6 of strands in present is parenchyma vasicentric The present. also

bands but

scanty, vasicentric parenchyma Axial tracheids. of surfaces inner on

observed

not sculpture Spiral septate.

tracheids Some 3 jim. I thickness, = wall

Tracheid jim. 25 I point, widest at = diameter Tracheid jim. 566 I length,

Tracheid diameter. in jim 3—5 bordered, fully pits tracheids, are elements

tracheary imperforate All jim. 416 I length, element Vessel vessels. narrower

in present

Spirals diameter. in jim 5—7 shape, in elliptical pits alternate

with

vessels of

walls Lateral simple. plates

Perforation jim. 1.6 I thickness, =

wall

Vessel jim). 28—94 (range: p.m 47 1 vessels, of 23). Diameter (Fig.

groups

small in or

solitary Vessels 246. I mm 2 per = vessels of Number

phenomena.

ring growth with coordinated not apparently parenchyma of

bands

tracheids; narrow radially and vessels by narrower distinguished latewood

present,

rings Growth 23). (Fig. 160 Mukerji & Santapan 1atfolia, Holboellia

cells.

other in as as well vessels some in compounds brightly-staining of deposits

Massive

cells. ray in observed grains Starch storied. clearly phloem secondary

and cambium but storied, vaguely Wood mm. 5 1> height, Ray cells. ray

interconnect pits bordered Some ray margins. at cells erect of layer a single with

cells

of procumbent consist Rays quinata. in A. as only, at margins cells lignified

have cambium near

portions slowly,

lignified become cells Ray 21 cells, I =

point, widest at width ray Multiseriate only. multiseriate Rays cells. six to

four

of composed strands parenchyma Axial in strands. cells parerichvma axial

adjacent

interconnect pits Bordered small. is very vessel a with contact in being

without formed be can parenchyma that likelihood the that so abundant are

vessels smaller vasicentric; parenchyma Axial 15). (Fig. 3—5 jim 1 thickness,

wall

Tracheid 20 jim.

I point,

widest = at diameter Tracheid jim. 589 I =

length, Tracheid pronounced. less but elements, vessel narrower the

of

that resembling sculpture helical bear tracheids Some septate. are tracheids

Some

diameter. in 5 jim about pits bordered fully bearing tracheids are elements

tracheary

imperforate All jim. 498 length, element = Vessel vessels. widest the

on

absent but vessels, on narrower present thickenings Spiral a vessel. of portion

particular any to adjacent type cell of regardless diameter, in jim 7 about

pits alternate elliptical with of vessels walls Lateral vessels. xylem secondary

early and metaxylem late in seen plates perforation scalariform a few but

plates,

perforation simple with elements Vessel plates. perforation subterminal

and

shape fusiform with fibriform, are vessels narrow the of Many jim). 40

than

narrower vessels of majority the jim, 25—240 (range: 52 jim diameter,

Vessel sampling). from excluded been rays had higher much been have would

number (the 143 transection, £ of mm 2 = per vessels of Number transection.

of

area unit per present number large the of because groups large in commonly

more solitary, Vessels latewood. in narrower radially tracheids 15); (Fig.

also

earlywood in numerous are vessels narrow although latewood, in fewer and

narrower vessels present,

rings Growth 15). (Fig. 15698 Cariquist trfo1iata, Akebia

S. CARLQUIST 264 ANATOMY OF LARDIZABALACEAE 265

I

Figures l6— 19. Stauntonia hexaphyl1a (Carlquist 15681), sections of stem. Fig. 16. Trangential section of wood. Large vessel at left, multiseriate ray at right. Fig. 17. Tracheids from radial section of wood. Fig. 18. Ray area from transection of wood; about a quarter of the ray cells contain rhomboidal crystals. Fig. 19. Transection of pith: cells have moderately thick lignified walls; some cells contain rhomboidal crystals. Fig. 16, magnification scale above Fig. 3. Fig. 17, magnification scale above Fig. 3. Figs 18, 19, magnification scale above Fig. 15. 266 S. CARLQUIST

..- :fE

Figures 20—23. Sections of wood and stems of Boquila and Holboellia. Figs 20—22. Boquila tqfoliata (Carlquist 7225). Fig. 20. Radial section of stem, showing crystal-bearing sclereids located in zones between protophloem fibres. Fig. 21. Wood transection: growth rings evident. Fig. 22. Wood transection to show nature of growth ring and parenchyma (1—2 layers of cells sheathing vessels and vessel groups). Fig. 23. Holboellia latifolia (Santapan & Mukerji 160), wood transection: conspicuous parenchyma bands above and below centre. Fig. 20, magnification scale above Fig. 3. Fig. 21, magnification scale above Fig. I. Figs 22, 23, magnification scale above Fig. 15. ANATOMY OF LARDIZABALACEAE 267 storied, clearly in many places but vaguely in others. Neither amorphous deposits nor crystals observed.

Sinofranchetia chinensis5 Garlquist 15653 (Figs 26—27). Growth rings are not sharply demarcated, but evident in the smaller diameter of latewood vessels and in the narrower radial diameter of latewood tracheids. Vessels solitary, occasionally in small groups (Fig. 26). Number of vessels per mm2, i = 283. Vessel diameter, = 116 p.m. Vessel wall thickness, i = 2 p.m. Perforation plates simple, a few scalariform perforation plates seen in metaxylem vessels and in vessels of earliest secondary xylem. Lateral wall pitting of vessels consisting wholly of alternate elliptical pits. No spiral thickenings observed in vessels. Vessel element length, 352 p.m. Imperforate tracheary elements may all be termed tracheids, although sometimes pits are smaller or sparser than would typically be expected for tracheids. Tracheid length, . = 604 p.m. Diameter of tracheids at widest points, i = 23 p.m. Tracheid wall thickness, . = 3.5 p.m. Modal diameter of pits on tracheids varies between 5 and 7 p.m, pits fully bordered. No spiral thickenings present inside tracheids. Septa seen in about half of the tracheids. Axial parenchyma vasicentric scanty (sheaths a single layer thick but incomplete sheaths present around vessels and vessel groups) plus a few diffuse cells. Axial parenchyma strands composed of four to six cells, usually five. Rays both multiseriate and uniseriate (Fig. 27), uniseriate rays a little more common. Width of multiseriate rays at widest point, = 11.2 cells. Height of multiseriate rays, > 5 mm. Height of uniseriate rays, i = 284 p.m. Multiseriate portion of multiseriate rays composed of procumbent cells. Erect cells comprise uniseriate rays and tips of multiseriate rays; a few erect cells are present as sheathing cells on margins of multiseriate rays (Fig. 27). Most pits between ray cells are bordered (pits viewed in sectional view in radial sections). Wood vaguely storied in some places. No deposits of amorphous brightly-staining compounds nor crystals observed.

Stauntonia hexapy11a, Gariquist 15681 (Figs 16—19). Growth rings present as narrower vessels and radially narrower tracheids in latewood. also evident as absence of conspicuously wide vessels in latewood; narrower vessels are scattered throughout the remainder of the growth ring. Vessels are more numerous in earlywood than in latewood, and the last few layers of latewood are poor in vessels. Number of vessels per mm2, = 166. Vessels mostly solitary. Diameter of vessels, = 52 p.m (range: 25—140 p.m). Thickness of vessel walls, i = 2—4 p.m. Perforation plates simple. Lateral wall pitting of vessels consists wholly of elliptical alternate pits 5—7 p.m in diameter. Spiral thickenings present in medium-width and narrow vessels, absent only in the widest vessels. Vessel element length, = 564 p.m. Spiral thickenings present in most tracheids. Some tracheids septate. Axial parenchyma vasicentric scanty (about two cell layers present around largest vessels, fewer layers around narrower vessels) plus a few diffuse cells. Axial parenchyma strands consisting of four to seven cells. Rays multiseriate only. Width of rays at widest point, I = 22 cells (Fig. 16). Ray height, I> 5 mm. Rays composed of procumbent cells except for upright sheathing cells which form an interrupted single layer at the margins of rays. Many of the pits between ray cells are bordered. Wood storied with respect to vessels and axial parenchyma, storying in tracheids not evident. Rhomboidal 268 S. CARLQUIST

25

—I J27 Figures 24—27. Wood sections of Lardizabala and Sinofranchetia. Figs 24, 25. Lardizabala biternata (Carlquss 7219), sections of wood. Fig. 24. Transection: no growth rings present. Fig. 25. Tangential section. Multiseriate rays are relatively narrow. Figs 26, 27. Sinofranchetia chinensis (Cariquist 15653), wood sections. Fig. 26. Transection. Growth ring activity is not pronounced; notably wide vessels are visible. Fig. 27. Tangential section. Both multiseriate and uniseriate rays are evident. Figs 24-27, magnification scale above Fig. I. ANATOMY OF LARD EZABALACEAE 269 crystals abundant in rays (Fig. 18). Starch observed in ray cells which do not contain crystals.

Boquila trfo1iata, Carlquist 7225 (Figs 20—22). Growth rings varying from vague to marked (Figs 21, 22), definable by narrower vessels and radially narrower fibre tracheids in latewood; examination shows that narrow vessels occur in earlywood as well as in latewood (Fig. 22); some of these are only a little wider than tracheids. Vessels solitary or grouped variously (Figs 21, 22). Number of vessels per mm2, = 78. Vessel diameter, = 67 jim (range: 28—97 jim). Vessel wall thickness, i = 2.2 jim. Perforation plates simple. Lateral wall pitting of vessels composed of alternate elliptical pits 5—7 jim in diameter. No spiral thickenings like those of Akebia present, but grooves interconnecting apertures of two or three pits in a helix occur in vessel walls. Vessel element length, = 328 jim. All imperforate tracheary elements may be termed fibre-tracheids because pits, although fully bordered, are somewhat smaller (2—4 jim) and sparser than is typical of true tracheids. Fibre-tracheid length, ? = 449 jim. Fibre-tracheid diameter at widest point, i = 24 jim. Fibre-tracheid wall thickness ranges from 1.5 to 5 jim; fibre-tracheids vary considerably in pit density and diameter. Septa were observed in about half of the fibre-tracheids. Parenchyma is vasicentric, forming a sheath one or two cells wide around vessels or vessel groups (Fig. 22). Some diffuse axial parenchyma is also present. Axial parenchyma in strands of four to six cells. Borders present on pits interconnecting axial parenchyma cells. Rays multiseriate only (Fig. 21), showing very little alteration in number from primary rays. Width of rays at widest point, t 19.8 cells. Ray cells procumbent, with one or two layers of erect sheathing cells at ray margins. Air spaces observed among ray cells. Some pits among ray cells bordered. Wood storied in places with respect to vessels and axial parenchyma; storying not evident with relation to fibre-tracheids. Brightly-staining amorphous deposits observed in vessels and fibre-tracheids (Figs 21, 22), crystals not observed.

Lardizabala biternata, Cariquist 7219 (Figs 24—25). Growth rings absent, no fluctuations visible (Fig. 24). Number of vessels per mm2 of transection, i = 50. Vessel diameter, i 87 jim (range: 45—133 jim). Vessel wall thickness, = 3 jim. Vessels solitary, less frequently in groups of two to three (Fig. 24). Perforation plates simple. A few scalariform perforation plates seen in late metaxylem and earliest secondary xylem vessels. Lateral wall pitting of vessels consists of alternate elliptical pits 5—7 jim in diameter but vessel wall is highly sculptured. Grooves interconnect pit apertures on vessel walls; pairs of ridges accompany the grooves. Vessel element length, = 394 jim. Imperforate tracheary elements may be termed fibre-tracheids because pits, although fully bordered, range from 4 to 6 jim in diameter and may be sparse. Fibre-tracheid length, ? = 649 jim. Fibre-tracheid diameter at widest point, i = 24 jim. Fibre tracheid wall thickness, = 2—5 jim, but wall thickness not varying with relation to position in growth rings. Many of the fibre-tracheids are septate. No spiral sculpture present on inner surfaces of tracheids. Axial parenchyma is vasicentric scanty (incomplete sheaths one cell layer wide around vessels or vessel groups) plus a very few diffuse cells. Bordered pits present between axial parenchyma cells. Axial parenchyma in strands of three to six cells. Rays both

biternata. Lardizabala in as

pith, the of portion central the in thinner slightly walls with but periphery,

pith the at walls lignifled thick moderately with spherical, are cells Pith

19). (Fig. and Stauntonia Boquila, as Akebia, in throughout,

walls

lignified thick moderately with outline, in spherical are cells Pith

fargesii. Decaisnea

in as walls, unlignified thin with in outline polygonal cells of consists Pith

structure: of modes several illustrates here studied Lardizabalaceae the of Pith

simple. typically are plates Sieve 10). (Fig. evident clearly is

structure

Storied lacking. are fibres parenchyma; and cells, companion elements,

tube

sieve of composed is Lardizabalaceae vining of phloem secondary The

stem. the of exterior the toward be oriented to

tends

wall thin The unlignified. usually but thinner, merely be not to tends cell

sclereid each of wall one 20), (Fig. strands fibre protophloem interconnecting

those and

14) (Fig. periderm the beneath immediately sclereids the of

case the In

walls. lignified thick moderately have cells sclerenchyma these fibres,

phloem the for Except 20). 14, 13, (Figs. lumina their in crystals rhomboidal

contain

fibres, protophloic the even sclerenchyma-types, the of All

12. Fig. seen in be may sclerenchyma of kinds four All

13). (Fig.

wall outer the than thicker to be tending wall the inner with sciereids

represent that cortex outer the in cells of patches are phelloderm the Beneath

stem. the around cylinder

complete a them with to form as so fibres protophloem the interconnect

they because above) and left 14, (Fig. sclereids of bands interstitial termed

be

may which sclereids are fibres protophloem of strands the Connecting

12, below). Fig. above; 8, (Fig. scierenchyma cortical with

outwardly interconnected often sclerenchyma, of plates contain rays Phloem

bundles.

of

poles outer the at formed are right) lower 14, (Fig. fibres Protophloem

Lardizabalaceae: of stems the in of sclerenchyma kinds four are There

old. relatively were stems that fact the despite observed,

not

were

periderms successive study, present the in included samples bark In

present. are deposits amorphous dark-staining which in layers phelloderm and

phellem of consists Lardizabalaceae of periderm The family. latter the in origin

periderm

deeper-seated claims who (1906), Réaubourg of data the from judging

Sargentodoxaceae, from Lardizabalaceae distinguishes layer, subepidermal

a from

originates which periderm, The 12-14). (Figs periderm thick moderately

a exhibit Lardizabalaceae

all of stems older transection, in seen As

PITH AND OF BARK DESCRIPTIONS ANATOMICAL

evident. materials

brightly-staining of deposits amorphous or No crystals storied. clearly not wood

but fibre-tracheids, of groups some in 25). visible Storying (Fig. rays of margins

lateral on cells sheathing as occur and rays, multiseriate of tips rays, uniseriate

compose cells erect chiefly; cells procumbent of composed rays multiseriate

of 25). Width

(Fig. uncommon relatively latter the uniseriate, and multiseriate

S. CARLQUIST 270 ANATOMY OF LARDIZABALACEAE 271 Pith cells are spherical with moderately thick walls at the pith periphery, but with appreciably thinner walls in the centre of the pith, as in Sinofranchetia chinensis. The pith of Slauntonia hexapy11a (Fig. 19) is distinctive among the species studied here in presence of crystals in all cells. Réauborg (1906) figures scattered bundles and thereby a monocotyledon-like condition for the stem of Holboellia latfo1ia. My material of this species did not show scattered bundles.

ANATOMY AND THE VINING HABIT The Lardizahalaceae is of interest with regard to the evolution of the vining habit because within the family one genus (Decaisnea) is a shrub whereas the others are scandent. Other families in which both growth forms coexist, such as Trimeniaceae (Carlquist, 1984b), Dilleniaceae, and Fabaceae are of potential importance for showing correlations between wood anatomy and habit. Caution must be expressed about the generalizations on anatomical consequences of the vining habit when studies are based on a limited number of families. If one analyses a group of vines and lianas from various families (Cariquist, 1975), one finds that they have unusually wide vessels. Although number of vessels per mm2 is relatively small, the vessel diameter of at least some vessels is so exceptional that the lianas in that sample had, as a group, a greater total vessel area per mm2 than did the other growth forms and ecological categories with which lianas were compared in that study. In the sample cited, the vessel element length of scandent species was short, but not exceptionally so compared with that of other woody plants. Indeed, some scandent groups do not show notably short vessel elements at all. There are only two genera in Trimeniaceae; of these, the scandent Piptocayx does not show vessel elements shorter than those of the arboreal or shrubby genus Trimenia (Carlquist, 1984b). To be sure, Piptocayx is not highly specialized in the scandent habit and may be only partially adapted in wood features to this growth-form. Vining Lardizabalaceae do not show a high mean vessel diameter, although in some species vessels do have a high mean diameter figure (e.g., Sinofranchetia chinensis). However, the number of vessels per mm2 in the Lardizabalaceae studied here is much greater than that of the vines and lianas quoted in Carlquist (1975). Perhaps the prime characteristic of wood of vining plants is expressed neither by vessel diameter nor number of vessels per mm2 but by a combination of them: area of vessels per mm2 of transection. The area of vessels per mm2 in the vining Lardizabalaceae ranges from 0.27 to 0.43 with a mean of 0.34 (compared with 0.36 for the lianas in Carlquist (1975), whereas the area of vessels per mm2 in Decaisneafargesii is 0.21 (compared to 0.24 for the primitive woody mesic species in Carlquist (1975). Thus the picture in Lardizabalaceae reinforces that offered for dicotyledons as a whole with respect to conductive area of stems. The fact that number of vessels per mm2 is elevated in Lardizabalaceae compared with other vining dicotyledons means that Lardizabalaceae have greater potential safety in their conductive systems, a fact considered below in relation to ecology. In the vining genus ]‘/epenthes narrower vessels were termed a product of vessel dimorphism (Carlquist, 1981), denoting the tendency for formation of a few 272 S. CARLQUIST very wide vessels to preclude enlargement of the majority of vessels. The narrower vessels of J’.Iepenthes can be considered fibriform vessels with respect to form according to recent terminology (Cariquist, l984a) because of the tendency of these vessels to be fusiform in shape with subterminal perforation plates (these cells in Lardizabalaceae have been termed “tracheides ouvertes” by Lemesle, 1947b). Fibriform vessels can be said to characterize all of the vining genera of Lardizahalaceae. They are most abundant in Akebia and Slauntonia. Loss of bars on perforation plates in the vining genera (scalariform plates present only in metaxylem and first-formed secondary xylem) as compared with Decaisnea seems a consequence of the vining habit. This is a clear tendency in those families in which non-scandent genera have scalariform perforation plates. This tendency is evident in Piptocayx of the Trimeniaceae (Cariquist, 1984b) and in Davilla, Doliocarpus, and Tetracera of Dilleniaceae (Metcalfe & Chalk, 1950). Evolutionary loss of bars on vessels in vining genera presumably represents removal of an impedance to the water flow, which is characteristically rapid in vines in terms of volume per unit time as well as velocity (Carlquist, 1975). Rays of vines tend to be wide compared to those of related shrubby species (Carlquist, 1984b). This is clearly shown in Lardizabalaceae, in which the rays of Decaisnea are much shorter and narrower than those of the vining genera. In Lardizabalaceae, the rays are wide and tall in the vining genera, differing only in relatively small degrees among these genera. Sinofranchetia and Lardizabala retain uniseriate rays, but still possess the wide high rays characteristic of vines. My material of Boquila and Holboellia shows almost no innovation of rays during secondary growth: the primary rays account for nearly all rays present during the growth of the stem. Wide tall rays in vines may be related to flexibility, the ability of vines to bend and withstand torsion. The function of rays in vines as storage zones is probably of secondary importance. With respect to bark structure of Lardizabalaceae, the presence of sciereids interstitial between protophloem fibres and forming thereby an uninterrupted cylinder around the stem may have a mechanical function. The phloem ray scierenchyma plates may also serve in this capacity; both plates and scierenchyma cylinder tend to be absent in roots (Réaubourg, 1906). Alternatively, the presence of scierenchyma in stems of Lardizabalaceae may contribute to herbivore deterrence. That a complete cylinder of sclerenchyma does not form in stems of Decaisnea (réaubourg, 1906), seems related to its non vining habit: rapid increase in diameter of the wood would result in breakage of such a scierenchyma cylinder, whereas vining Lardizabalaceae evidently show such a slow increase of stem diameter as the stem ages, that a sclerenchyma cylinder can exist in the bark with little breakage. The simple sieve plates of vining Lardizabalaceae presumably are related to the high conductive efficiency claimed for phloem of vines (Carlquist, 1975). Presence of sclerenchyma in pith of vines as compared with presence of thin- walled parenchyma in Decaisnea pith may relate to mechanical strength of vining stems. In vines, the volume of wood devoted to mechanical tissue is smaller than that in shrubs or trees, so that presence of mechanical tissue outside the secondary xylem might be a compensatory device. In ray areas of Akebia, cambium is sunken into the xylem cylinder (Fig. 8). This can be described as the result of slower activity of the cambium in ray areas ANATOMY OF LARDIZABALACEAE 273 compared with fascicular areas. This behaviour may be seen in some other vines, such as Arislolochia. However, in other genera of Lardizabalaceae, such as Boquila, the cambium is not sunken into ray areas and thus this is not a characteristic feature of vines in general. Ogariezova (1975) has claimed that in Berberidales, the lianoid habit is primitive, followed by the shrubby and arboreal growth forms, with annual and perennial herbs more specialized. One cannot doubt that the vining habit is widespread in Berberidales (most Lardizabalaceae; Clematis of the Ranunculaceae; the majority of Menispermaceae; Sargentodoxaceae). However, the scalariform perforation plates of Decaisnea would seem to argue against the idea that the lianoid habit is primitive within the Lardizabalaceae. IfDecaisnea were derived from vining ancestors, one would expect that it would retain the simple perforation plates characteristic of lianas, since there seems to be no selective pressure for restoration of scalariform perforation plates once they have been lost in the course of evolution.

ECOLOGICAL CONCLUSIONS The nests of sclereids immediately beneath the periderm and the bands of sclereids which lie between protophloem fibre strands in members of the Lardizabalaceae are noteworthy in having a thin wall facing outward. These sclereids are also notably rich in rhomboidal crystals, which otherwise are absent in cortical parenchyma. These crystal-bearing sclereids of Lardizabalaceae are thus like the cristarque cells found in Ochnaceae, Quiinaceae, and Scytopetalaceae (Metcalfe & Chalk, 1950) as well as in Balanopaceae (Carlquist, 1980). However, cristarque cells have a druse in each cell, whereas the crystal-bearing sclereids of Lardizabalaceae contain non- aggregated crystals. In either kind of crystal-bearing cell, the array of crystal edges facing the exterior of the plant body may deter predation by phytophagous insects and possibly herbivores. If so, the rays and pith of Stauntonia hexaph3’ila, many cells of which contain rhomboidal crystals, represent optimal adaptation to resistance to predation. Vines and lianas are typically mesomorphic plants, common in wet areas but rare in deserts. Wood of vines might be expected to be mesomorphic adapted to high conductive rates. Therefore the kind of wood seen in desert plants, in which the confining of air embolisms is achieved by the presence of great numbers of very narrow vessels and tracheids, would not be expected in vines. Although the imperforate tracheary elements in wood of Lardizabalaceae are all tracheids or fibre-tracheids, some or many of these cells are septate, indicating the presence of living contents. Therefore these tracheids would not have an appreciable role in conduction. Pits on tracheids of Decaisneafargesii are, in any case, too small for tracheids of that genus to have any very great conductive function. Spirals occur in vessels of Akebia, Holboellia, and Stauntonia, although the wider vessels lack spirals; spirals tend, in at least some species of these genera, to occur inside tracheids as well. The grooves on vessel walls of Lardiabaia may represent a similar but independently evolved phenomenon, represented in a number of dicotyledons and recently illustrated excellently for A/yrsine and Alectryon by Meylan & Butterfield (1978). Spiral thickenings in vessels may represent one of 14 274 S. CARLQUIST several devices which intensify water bonding to walls of conductive cells. In theory, this could have one of several effects. It could reduce the likelihood of occurrence of air embolisms in case of physiological drought, which would include both dry and cold conditions: either would tend to increase tensions in vessels markedly when transpiration occurs but soil water is not available. If these conditions occurred, air embolisms would probably disable wider vessels in a vine quickly, but smaller vessels (and tracheids) which possess spiral thickenings would tend not to be disrupted by air embolisms and could suffice for conduction until lowered transpiration, coupled with greater availability of soil water (and perhaps action of root pressure) might result in expelling of air from the larger vessels, returning them to the active conductive system. Such a pattern of events has been demonstrated to occur in some angiosperms daily (Milburn, 1973). An alternative explanation for the occurrence of spiral thickenings would involve their functioning to induce refilling of cavitated vessels and tracheids once those cells are disabled. However, a mechanism which works only after the conductive system of the plant has been. seriously disabled would not be as selectively advantageous as one which prevents the occurrence of extensive cavitations. The occurrence of marked growth rings in .Akebia, Holboellia, and Stauntonia suggests that they do experience fluctuations in physiological drought. However, Lardizabala biternata does not have growth rings, a condition which suggests absence of marked frost and drought in its habitats. What function might the grooves and ridges on vessels walls have in that species? Conceivably some frost or drought might result in breaks of water columns of vessels even if growth rings are not present. Grooves and ridges might function much like spirals, resisting breakage of water columns in vessels or even conceivably aiding in refilling of vessels which contain air (Carlquist, 1983).

SYSTEMATIC AND EVOLUTIONARY CONCLUSIONS If Lardizabalaceae are to be included in Berberidales (Ranunculales), comparisons must be made between Lardizabalaceae and those families in which woody species occur: Berberidaceae, Menispermaceae, and Ranunculaceae (Clematis). Because Clematis is a vine, it may offer parallels to the vining Lardizabalaceae in anatomy, although monophylesis of the vining habit within Berberidales is quite unlikely. Within Ranunculaceae, there is no shrubby ancestral type to which we could compare Decaisnea (Paeonia is accepted here as belonging to its own family, Paeoniaceae, which is not close to Berberidales). Menispermaceae mostly have successive cambia, but little is known in detail about the anatomy of genera with normal cambium (Metcalfe & Chalk, 1950; Mennega, 1982). Thus by default Berberidaceae offers more numerous pertinent comparisons with Lardizabalaceae. Berberidaceae have vessels with scalariform perforation plates like those of Decaisnea as well as simple perforation plates (Solereder, 1908). The lateral wall pitting of vessels in Decaisnea is without parallel in Berberidaceae, so the hypothesis must be that the scalariform lateral pitting of Decaisnea vessels represents a more primitive condition than that exhibited by the Berberidaceae. The Berberidaceae is reported to have imperforate tracheary elements with ANATOMY OF LARDIZABALACEAE 275 simple pits except for J’Iandina, which Solereder (1908) pairs with Holboellia in that both have tracheids with bordered pits as well as simply-pitted “prosenchyma”. The latter undoubtedly corresponds to the parenchyma bands reported above for Holboellia la4folia; this also accounts for the report by Metcalfe & Chalk (1950) of fibres with simple pits in Holboellia. Otherwise they cite only bordered pits in imperforate tracheary elements of Lardizabalaceae, in agreement with the present study. Metcalfe & Chalk (1950) report bordered as well as simple pits in imperforate tracheary elements of Clematis. Tracheids with fully bordered pits occur in Sargentodoxa (Lemesle, 1943, 1947b), a genus regarded as close to Lardizabalaceae in most respects. Spiral thickenings are reported for vessels and tracheids of Berberis and jVandina (Solereder, 1908; Shen, 1954), so this feature of the vessels in Akebia, Holboellia, and Stauntonia is represented in Berberidaceae. Rays of Lardizabalaceae are matched by those of Berberidaceae (including Jfandina: Shen, 1954), which are often wide, and which have a distribution of erect and procumbent cells like that in Lardizabalaceae. The Lardizabalaceae has both paratracheal and apotracheal parenchyma, as does J’fandina (Shen, 1954). Paratracheal parenchyma is reported to occur in Clernatis (Metcalfe & Chalk, 1950), apotracheal axial parenchyma characterizes the Menispermaceae (Mennega, 1982), whereas in Berberidaceae, axial parenchyma is absent (Metcalfe & Chalk, 1950). Storying is not evident in the wood of Decaisnea. The vining genera of Lardizabalaceae show various degrees of storying (conspicuously expressed in phloem and cambium of Akebia, Fig. 10). Since storied wood structure is considered a specialization in dicotyledons (Bailey, 1923), Decaisnea must be regarded as more primitive than the rest of the family in this respect. Storying has been reported in woods of Berberidaceae and Ranunculaceae (Metcalfe & Chalk, 1950), underlining the list of similarities between that pair of families and Lardizabalaceae. Rhomboidal crystals which are present either singly or in groups in cells, both of which conditions occur in Lardizabalaceae, have been reported in Berberidaceae, Menispermaceae, and Ranunculaceae (Metcalfe & Chalk, 1950). Other indications of berberidalean placement for Lardizabalaceae may be found in bark anatomy. The uninterrupted cylinder of scierenchyma, composed of protophloem fibres plus interstitial sclereids, which occurs in all vining Lardizabalaceae, has been reported by Solereder (1908) in Mahonia (Berberidaceae) as well as Clematis. Because most stems of Mahonia do not enlarge markedly in diameter, a closed cylinder of cortical sclerenchyma in that genus is comprehensible. Generic characters in Lardizabalaceae cannot be cited definitively because the present study does not include all the known species for every genus. However, in a preliminary way the following features may be cited, excluding in the listing below features closely related to ecology and to the vining habit and discussed above. Decaisnea: scalariform lateral wall pitting of vessels; tracheids with very small pits; more than half of the rays uniseriate. Akebia: marked growth rings, numerous narrow vessels present; all rays multiseriate, newer central portions of rays consisting of unlignified cells. 276 S. CARLQUIST Holboellia: bands of parenchyma present; rays multiseriate only. Sinofranchetia: exceptionally wide vessels present; uniseriate rays not conspicuous but more numerous than multiseriate rays. Stauntonia: all rays multiseriate, wide, crystals present in rays as well as in pith. Boquila: axial parenchyma in sheaths one or two cells wide around vessels (more scanty in other genera); rays multiseriate only, almost all extensions of primary rays. Lardiaba1a: multiseriate rays much more frequent than uniseriate rays; multiseriate rays narrower than in the other genera.

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