Flora (1982) 172: 403 —491

Wood Anatomy of : Correlations with Ecology and Phylogeny

SHERWIN CARLQuIsT

Claremont Graduate School, Pomona College, and Raneho Santa Ana Botanic Garden

Summary

The family l3uxaceee consists of four genera, with the desert Ssrnmonds’em dubiously mcludcd in the family as a fifth . (Andean rain forest) has the most niesomorphic and primitive wood features, followed by &rrcococce and then by , which can be grouped closely with Notohuxus in terms of wood anatomy. Pachysormdra was excluded from this study because of its essentially herbaceous habit. For a small family, Buxaceae have a wide span in expression of wood features. Characters in Buxeceae s.c. which show a range within the family probably explainable in terms of ecology include vessel element length, number of vessels per muimc, vessel diameter, number of bars per perforation plate, presence or absence of helical thickenings in vessels and tracheids, and presence or absence of growth rings. The woods in the family can be ranked as highly mnesic (Stytoceras, Scmrcococca) to moderately mesic (Buxus, Notobuxus), with a few species in the latter pair of genera notably more mesomorphic in wood construction. Retention -of scalariform perforation plates throughout- Bmexoceee s.s. may be due to compensatory low transpiration capabilities of the foliage, which may have very thick cuticles and tend toward microphylly. Features which are susceptible to evolutionary interpreation but which do not bear as direct a relationship to ecology include ratio of tracheicl length to vessel element length, presence of tracheids with fully bordered pits, degree of aggregation of axial pamenchymna cells (diffuse, diffuse-in-aggregates, abaxial) and degree of cellular heterogeneity in ray histology. The ray types of Sercococce reflects a type of juvenilism, and scarcity of axial parenchyma in the genus also seems related to innovation of numerous shoots, each •with limited duration. Simrnondsia differs from Buxoceae s.s. in its desert habitat, its successive camnbia, and its anemophuily. i)istinctive features of wood anatomy (lack of acial parenchyma, juvenilisnu in ray histology, and presence of very short vessel elements with helical thickenings) can be attributed to the first two factors. No features of wood anatomy clearly rule out relationship to Buxeceae. Presence of tracheids in wood of $irnrnondsice may be related to the high selective value for tracheids in a desert environment; this feature (and the encyclocytic stomata) suggest affinity to Buxnceae, even if the genus is segregated in Sirnrnondsiaceae. Buxuceae have been claimed to be related to four major groups of dicotyleclons: Gelastro-les, E-uphorbioles, Hurncmnrelidaies, and 1-httosporeles. Of these, Euphorbiales shows the least degree of resemblance to Bnxaceee in terms of wood anatomy. The placement of the isolated Madagascan genus Diclyrneles may be related to the problem of placement of Buzoceae, and is discussed in this context.

Introduction

Wood anatomy of Buxaceae has been reported in condensed form by METCALFE & CHALK (1950). Their account and that of RECORD & GARRATT (1925) are generally 464 S. CARLQTT1ST accurate, and the present paper may be regarded as an amplification in several directions. Wood descriptions presently available are brief, or consist of a single species only, as in GREnuss’s (1959) account of B’uxus sempervrens. The present paper has been essayed as part of a survey of anatomy of families included by TH0RNE (1977) in Pittosporales. The genera of Buxaceae. as noted by METcALFE & CHALIC span a range in wood structure unusual for a single small family. This range is do cumented in quantitative form here (Table 1). The pattern of characteristics which emerges is compared to ecology of the species in the family. The family ranges from wet rain forest to moderately moist scrub, if one excepts the desert genus Simmondsia, often excluded from Buxaceae. Because the wood of Buxaceae ranges from strongly primitive to moderately specialized (highly specialized in Simmondsia), the comparison between evolutionary status of characters and their ecological distribution forms the basis for an inviting project. The relationships of Buxaceae have not been at all well understood. The traditional placement of B’uxaceae in Euphorhiales (or similar groupings) has yielded to a diversity of thought, with various authors opting for placement in such groups as Ha,ncrmeiidales (most recently TAKHTAJAN 1980), (‘elastrales (DAHLOREN 1977). or in a rosoid alliance such as Pittosporales (TH0RNE 1976). I)ata from wood anatomy are mostly inter pretable in terms of levels of wood evolution rather than indicators of affinity. There is growing appreciation of this among phylogenists. However, data from wood ana tomy can be expected to be usable to a limited extent in the construction of the natural system. The details of placement of the family are given in a later section of this paper. Buxaceae s.s. consists of five genera (distributions modified from Pa.x 1926-.-.-1928). Buxus frequently occurs on limestones and ranges from tropical meso-America into the West Indies, and from southern Europe and North Africa eastwards to Asia and offlying islands (Japan, Taiwan, Philippines. Borneo). Notobuxus is closely related to Buxus and consists of subsaharan African and Madagascan species which differ from .Buxus by having no pistillodes in male flowers, stamens without filments, and stamens four to eight as compared to four in Bu.xus s.s. (ADAMs0N. EsTERHUYsEN & PHILLIPS 1943). is a genus of understory , sprouting from near the base, native to southeast Asia (including Java. Sumatra. India, China, and Burma). A single species, S. conzattii (STANDLEY) JOHNsToN was recognized by JoHNsTON (1938, 1939). This species has baccate . as in •S’a,cococca, but male flowers si.ir rounding a female flower as in Buxus (Sarcococca otherwise has bisexual flowers). More needs to be learned about this interesting situation. (southeast Asia and the eastern U.S.A.) is a genus of prostrate herbs, probably closely related to Sarcococca, which never develops much wood and has therefore been omitted from this study. The above genera are epresentative of temperate climates chiefly, and occur mostly in the northern hemisphere. They form a subfamily. Buxoideae. of Buxaceae. A second subfamily, Styloceratoideae, is formed by the genus Styloceras. native to warm tropical forests of Colombia, Ecuador, .Peru, and Bolivia. Simmondsia, variously Wood Anatomy of Buxaceae 465 included in Buxaceae or excluded as a genus incertae.sedis (TH0RNE 1976) is a shrub of southernmost California and adjacent Sonora and Baja California. It is listed at the end of Table 1 on account of its isolated features, and is discussed in a terminal section of this paper.

Materials and Methods

In other studies of wood anatomy, I have often been able to stuely wood anatomy from samples .1 collected in the field. in the present study, wood samples have been obtained from other cources, listed in Table 1 (herbarium abbreviations from H0LIemEEN & KNuKEN 1974; xylarium abbrevia tions from STERN 1978). The specimen of (a species described from cultivation) was from material culti voted in the University Botanic Garden of Cambridge, England, and was collected for me through the kindness of P. F. YR0. The specimen of S. rvscifoliu, a species native to China, was collected from a cultivated shrub in Claremont, California. The wood of Simmoredsie was collected by James HanaicKsoN in Baja California, Mexico, a native habitat for this species whose specific- epithet is misleading. The remaining wood samples were obtained from wood collections, to whose curators I am grateful. The wood sample from the SJRw collection were PrOvided by MAI)w, where a set of Rrcoan’s wood collection is now housed. The locality data on these specimens is minimal. Provenances are as follows: Buxu$ beleurrcu, Balearic Islands; B. qio,nereta (MADw.205G9), Cuba; B. qlonrerete (USw-4300), Haiti; B. ha-rl-u.ndi-e, China; B. inicrophgliu var. netermed?e, Taiwan; B. microphyllee var. japoeeeca, Japan; B. sempc’rcirens, no

collection data but probably European; B. wollichieene, India; Notob u.rus acuminate, \V . Africa; N. macowaaii, S. Africa (presumably the East London area); N. n-eetclensis, S. Africa (presumably the area from Pondoland to Durban, Natal); Styloceras laurifof turn, E. Ecuador. The Himalayan population termed Buxrrs wellichiana here is regarded by moSt authors as B. sempervirens. How ever, because of the distinctive nature of the wood, which doubtless reflects a more mesic habitat (1,800—3,000 in, Simla to Kumaon) than in typical B. semperviren.s, the segregate species name is used here for convenience. The comments on ecology of the various species. based on data gleaned from numerous finristic works, lint cannot be considered more than approximate because ireicroelirnatic conditions are all too often not specified when the habitat of a is given in floras. The best habitat data for the family is offered by RECoRD & GARO-url (1925), wood samples were boiled and then macerate(l and sectioned according to the usual techniques. Prior to sectioning, wood samples were soaked in ethylene diamine according to the general method outlined by KuKACUICA (1977), with variations in times dependent- upon the hardness of the wood. For aid in microtechnique, 1 un grateful to Mr. Vixca ECEHART.

Anatomical Data

The main basis for discussion is formed by the data in Table 1. Additional quali tative data are cited below, however, and comparisons between the results of the present study and those of earlier workers are offered. Because of the isolated nature of the genus uSimmondsia, all aspects of that genus are considered in a terminal section of the paper.

Vessel Elements

Vessel element length ranges from a mean of 440 tm in one collection of Noto bu.xws mac-owanii to a mean of 1,579 tm in one collection of S’tyioceras laurifolium. 466 s. CARLQIn5T

This remarkable range is paralleled by other wood features of the family. However, quite noteworthy is the uniformity in vessel element length in Buxus and Notobuxus: mean values fall mostly between 450 and 550 m. This can be attributed to similarity among the collections in ecology, with the exception of two species. Buxus wallichiana, from moister forests in montane India, has longer vessel elements than the samples of B. sempervirens. Likewise. Notobuxus natalensis, from subtropical regions of South Africa. has longer vessel elements than N. macowanhi, from temperate regions. The correlation between greater vessel element length and more nesic habitats has been noticed repeatedly (WEBBER 1936: CARLQUIsT 1966, 1975). Vessel element length in Sarcococca would, in this regard, seem an indicator of the moist understory habitats of that genus, and the exceptionally long vessel elements of Styloceras correlate with the tropical rain forest habitat of that genus (see WEEERBAUER 1945, for notes on. habitats). The length of vessel elements in Buxus and Notohuxus cor responds to the mean for dicotyledons as a whole figures by ME’roALFE & CHALK (1950, xxiv). However, vessel element length in Sarcococca and Styloceras exceeds that mean. The long vessel elements in these two genera should probably be regarded as a primitive feature, owing to an unbroken occupation of mesic sites. Perforation plates are uniformly scalariform throughout the family; the report of simple perforation plates by Tirro (1938) relates only to extremely rare instances where bars were lacking on perforation plates, and such instances are so infrequent as to be aberrations, the mean number of bars per perforation plate is shown for each species in Table 1. Buxus and Notobuxus are notable in that the mean bar number is rather close to 10 (Figs. 4, 7—9, i9—2l). Ouly a few dicotyledon groups have stabilized, at a low nuin her of bars per perforation plate. The relatively low number of bars per perforation plate in most species of Buxus and Notobuxus, probably an indicator of moderately mesic conditions. contrasts with the long scalariform per foration plates of Sarcococca and Styloceras (Table 1 Figs. 25, 26, 32, 35, 36). Excep tions within Buxus and Notobuxus include B. wallichiana and N. natalen.sis (Figs. I 4—16), species from more mesic habitats than those of congeners studied here. The correlation within Buxaceae between vessel element length and bars per perfora tion plate is remarkably close (see Table 1). If one were to plot these two features on a graph, a straight-line relationship with very little deviation would result. S0LERE- DER (1908) reported 30 or more bars per perforation plate of Buxus subcolumnar’is l1uell. Arg. S0LEREDER’s material was probably what should now be called B. muel lerianci Urb., a macrophyllous species from wet forest areas of Cuba. Bars are occasionally forked in perforation plates of Buxaceae (e.g., Fig. 26). In Notobuxus natalen.sis (Figs. 14—16), interconnections between bars are so frequent that one might term the plates multiperforate. While one may regard such inter connections as a form of strengthening in some groups (CARLQUIsT 1975), the total picture of correlations of multiperforate perforations (which probably represent more than a. single phenomenon) is not yet clear. Bars on perforations of Buxaceae are bordered, at least on either side of the plate, with borders narrow in the central portion of each bar. Bars are most clearly bordered in Styloceras (Fig. 36). S Table 1. Wood characteristics of B12xoceoe

Species Collection 1 2 3 4 5 (1 7 8 9 10 11 12 13 LAM. SjRw-7475 523 32 14 2.8 532 775 10.2 185 61 2.7 1.46 0.09 32 B. gloaierata MuELJ. Ann. MADw-20569 156 33 10 4.1 408 029 8.7 321 168 3.9 1.34 0.21 98 iJ$w-4300 187 33 17 5.3 351 457 9.5 288 109 3.2 1.30 (I.ln 63 B. harlandii HANC’n SJRw-20049 221 33 16 4.6 491 751 14.7 152 86 2.1 1.53 (1.15 72 B. microphylia S. and Z. var. TAIFSw-H162 198 35 16 4.1 544 783 10.5 207 81 3.1 1.44 o.1% 98 intermedia (KANEieJRA) Li B. rn. var. japonica (MuEr.r.. ARc.) MADw-20404 378 31) 17 4.1 632 782 12.7 327 199 2.1 1.24 ((.08 50 REHD. & WTL5. MADw-27860 323 29 16 5.8 914 915 12.7 353 159 2.2 1.49 0.09 55 B. sempervirens L. ZTw.46 296 29 16 5.5 447 615 8.0 220 123 2.7 1.38 0.10 44 0 0 IjSw-3867 329 34 19 5.5 666 648 12.5 248 139 2.0 1.49 ((.10 (19 IJSw-13105 224 29 18 4.6 492 725 9.3 18 68 2.3 1.47 ((.12 59 B. wailichiana BAILL. tJSw.6658 242 43 23 4.6 562 886 17.5 214 146 2.4 1.52 ((.18 103 0 Notobuxus acnniinoto HuTCrnNSON FHOw-7125 184 30 16 3.2 540 715 9.9 193 124 2.1 1.32 ((.16 86 N. macouapu (OLIVER) PHILLIPS MADw.14198 295 29 14 3.7 444) 5s0 9.1 114 41 2.0 1.31 ((.10 44 0 PFL’w, s.u. 206 36 1(1 4.1 469 611) 5.6 138 52 2.0 1.3)) ((.17 82 N. natalensis OLIvER S,lliw-7477 94 38 18 6.9 7$)) 9(15 52.3 539 167 2.1 1.16 ((.4(1 312 Sareococca con/usa SEALY Palmer 37—65 81 29 18 4.4 1,125 1,267 45.3 879 466 2.0 1.13 0.35 394 S. ruse ifolia STAPF C1lLQu1sT 176 29 18 3.7 94(9 1,098 51.6 1,267 381 3.5 1.13 0.16 155 15.636 (RSA) Styloeeras iaurifoliuin H.B.K. MADw-2781i5 46 (18 30 5.8 1,579 1,772 10.1 939 41$ 2.1 1.12 1.49 2,264 FHOw-11709 24 76 30 5.8 1,151 1,298 45.2 899 366 3.5 1.13 3.25 3,740 Simmondsia chinensis (LINK) C. K. HENiucKsoN 133 28 12 4.1 132 292 0 222 89 2.3 2.21 0.21 26 SCHNEID. 2,345 (RSA)

Key: 1 = mean number of vessels pet 2mm 2 = mean vessel diameter, pm; 3 = mean tracheid diameter, pm; 4 = mern tracheid wall thickness, urn; 5 mean vessel element length, pm;; 6 = mean tracheid length, pm; 7 = mean number of bars per perforation plate; 8 = Illean height of niultiseriate rays, urn; 9 = mean height of uniseriate rays, pm; 10 = mean ray width at widest point, cells; 11 = mean tracheiil lcngth/niean vessel elementlength; 12 = ‘vulnerability” index (vesseldiameter/vessels pet sq. mm); 13 = “mesomorphy” index (vulnerability X vesacl element length). I 111111 III II II 111111 IIIlIIIIl !

SIlôillV) • 9t Wood Anatomy of Bnxaceae 469

Vessels are mostly solitary in Buxaceae (Figs. 3, 10, 22, 27, 37; see also low power transections). As a result, vessel-to-vessel contacts are few. Where such contacts do occur, pitting tends to he opposite in Buxaceae, as noted by M.ETeA1FE & CHALK (1950). Pitting on vessel walls which face rays is predominantly opposite in Buxws balearica. B. qlomera.ta. B. harlandli. B. in icrophzjiia, B. .sempervirens ..B. wallichian.a. Aotohua-us natalen.i.s. Sarc;ococca con fusa, and S. muscfoiia. Vessel-ray pitting is scalariform to opposite in. the Styioceras collections studied. Alternate pitting was observed in vessel-ray contacts in Notobuxu.s acorn inata and N. macowanii, and in one collection (USw-131(15) of Baxus .seinpervirea.s. Pitting on vessel walls which face axial parenchyma was observed to be alternate in all species of Biwraceac. except for some scalariform pitting seen in Stytoceras laurifoliuni. (FHOw-11709). \essels are round in outline as seen in transection (Figs. 3. 10. 22, 27). or somewhat angular in tyloceras (Fig. 37). Vessel walls are approximately 3 ,urn in thickness throughout the family, except in $tyloceras, where they are i—--2 ni in thickness. Greater wall thickness of vessels has been claimed to be correlated with xeromorphy in some instances (CARLQU1sT 1975). Helical thickenings on vessel walls occur onl in Sarcococca (Fig. 25) and also on vessels of Sirninondsia (Figs. 42. 43). These th ickenings are not pronounced. In that respect they resemble those of Jilicium (CARLQUIsT 1982). The function of helical thicken.ings such as these is not clear, although in Illiciurn, they occur in species from climates more likely to have pronounced frost, and the thickenings in So.rcococca might relate to such a climatic regime. In other groups. such as Astera ceae. there seems to be a correlation with increased xeromorphv (CARLQUIsT 1966). The number of vessels per sq. mm. tends to he roughly inversely related t.o vessel diameter (Table 1, columns 1 & 2). Buxaceae. with the exception of Styloceras, are notable for the narrow diameter of vessels, numerous per sq. mm. (Figs. 1, 3, 5, 10, 11, 17, 22, 23, 27, 28). Relatively low numbers of vessels per mm occur in the more mesic of t.he B’u..raceae studied here: Notobu.rus nataiensis (Fig. 10), $arcococca ruscifolia. arid S’tyioceras laurifoiiunr (Fig. 33). Vessel diameter in ;Stioceras is notably wide (Fig. 37), although wood. cell size in general is large in that genus. Buxaceae are notable for having relatively long vessel elements, but narrow ones numerous per unit transection. If my (1975) correlations are accepted, adaptation to xero morphy in this family may be said to involve primarily shift in vessel diameter and abundance rather than vessel shortening (although vessel elements are appreciably longer in ,Sarcococca and Styloceras, the most mesic genera, than itt Buxus and Noto banns).

Figs. 1—4. Wood sections of Buxus. 1, 2. B. bulectrseo, SJRw-7475. 1. Transection, showing growth rings. 2. Tangential section. Rays mostly biseriate. 3. B. sernpervirens, USw-13105. Transection, showing end of one growth ring, transition upward into earlywood of next ring. 4. B. microphylia var. upon ic,i, liA1)w-20404. Perforation plate from radial section. Figs. 1, 2. Magnification scale above Fig. 1 (finest divisions = 10 ion). Fig. 3. Scale above Fig. 3 (divisions 10 urn). Fig. 4. Scale above Fig. 4 (divisions = 10 pm). 32* LSE1V) • OLT’ Wood Anatomy of Buxaceae 471

Tracheids

Imperforate tracheary elements in Buxaceae must be termed tracheids. Pit borders on tracheids are reported to he sometimes ‘indistinct” in Buxus and Notobuxus according to METCALFE & CHALK (1950). However, careful observation of imperforate elements reveals that tracheid pits of all Bttxaceae studied are fully bordered, with pit apertures not longer than diameters of pit cavities. Most of the pits are about 3 im in diameter or slightly less. Tracheid pits 4.5 um in diameter were observed in Sarcococca (both species), while pits 7—8 urn in diameter were seen on tracheids of Styloceras. All species of Buxus studied except B. glomerata and B. harlandii and all species studied of Notobuxus were observed to have splits in tracheid walls (Fig. 4, 13). These splits, which occur at pit apertures and thus greatly lengthen theni, do obscure pit borders, which thereby are not noticed except on pits which lack splits based on the pit apertures. The splits in tracheid walls may not occur on all tracheids in a given section. The splits are no doubt related to gelatinous wall structure which, in turn, is related to compression wood. Compression wood has been reported and figured for by H5sTER & L1EsE (1966). Tracheids of both species of Sarcococca examined hear helical thickenings (Fig. 30). These thickenings are essentially the same as the t.hickenings. mentioned above, present in vessel elements of Sarcococca. Figures for tracheid diameter and tracheid wall thickness are given in Table 1 (columns 3 & 4). Several features are evident. Tracheids are not notably narrower than vessels, they are in approximately the same range of magnitude; their walls are a little thicker than those of vessels, however. The sirnilarty between the two eli types accounts for the extraordinary uniformity in texture in the wood, a uni formity upon which the use of buxaceous wood for woodcuts is based. The differentia tion between. vessels and tracheids in Styloceras (Fig. 37) is much more marked, however. Figures are given in Table 1 (column 11) for the ratio in length between trachoid length and vessel element length for each species. Buxus and lVotohuxus have ratios berween 1.3 and 1.5 mostly, whereas Sarcococca and Styloceras are close to 1.12. Simmondsia. with a ratio of 2.2, offers a marked contrast.

Axial Parenchyma

Axial parenchyma in Styloceras is diffuse (Figs. 33. 37), and rather abundant, so that inevitably some parenchyrna cells are adjacent to each other. In the remainder

Figs. 5—10. Wood sections of Buxus. 5.—- 8. B. giomeruta, USw-4306. 5. Transection. Growth rings are absent. 6. Tangential section. Multiseriate lays mostly four cells wide. 7, 8. Perforarion plates from radial sections. Bars are bordered at ends. 9.- 10. B. wallichiano, USw-6658. 9. Perforation plate from radial section, showing slender bars. 10. Transection. Parenchyina mostly abaxial to vessels. Figs. 5, 6. Scale above Fig. 1. Figs. 7—9. Scale above Fig. 4. Fig. 10. Scale above Fig. 3.

S. 472 CARLQiIsT Wood Anatomy of Buxaceae 473

of Buxaceae s.s., small groupings of axial parenchvrna cells with each other (diffuse in-aggregates) and small groups aba.xial to each vessel (“abaxial”) are present in addition to a few diffuse cells. These three axial paren.chvrna expressions occur in .Buxus (Figs. 3, 10) rather uniformly. in Notobuxus, axial parenchyrna cells are mostly abaxial (Fig. 22). In Sarcococca (Fig. 27). axial parenehyma cells are scarce, with oni a sparse representation of diffusely arranged cells: scarcity of axial paren chvma may be related to the short. duration of sterns in Sarcococca, in which lateral sterns are continually innovated. Strands of two to four cells in axial parenchyma are common in the Notobuxus species studied, and in Bu.tus balearica, B. glomerata, and B. harlaadii. Strands of five to eight are most common in B. ,n icrophylla, B. sempervirens, B. wailichiana, and Stjioceras iaurifoliirm.

Ray Parencityrna

If one views tangential and radial sections of the woods of Boxes (Figs. 2, 6) and Notobu,rus (Figs. 12, 8), one finds rather uniform ray histology patterns. [iii senate rays are at. least as frequent as multiseriate rays. usually more numerous. lJniseriate rays are composed of erect cells. Multiseriate rays are composed primarily of procumbent cells. No erect cells are present sheathing the sides of multiseriate rays. Occasional erect ra cells are present as wings on multiseniate rays. rghese wings seem merely a consequence of the abundance of uniseriate rays, a consequence of the likelihood that tips of multiseriate rays will, here and there, intercept uniseniate rays and conjoin them. This ray histology corresponds roughly to KRIBS’s (1935) ‘I’ype L[A. The claim by METCALFE & CHALK (1950) that rays of J\Totol)nxuS macowanii (Fig. 1$) correspond to KEIBs’s Homogeneous Type I could not he confirmed. because both of the collections I studied conformed to the type described above, with only erect cells in uniseriate rays. Rays of (Fig. 34), in contrast, correspond clearly to Krib’s Heterogeneous Type I, with both procument and erect cells in both multiseriate and uniseriat.e rays. Procumbent cells are much less common than erect cells in uniseniate rays, however. Erect cells are present as sheathing cells on multiseniate rays, and uniseriate wings composed of erect cells may commonly be found on multi- senate rays.

Rays of •S’arcococca (Figs. 24. 29) do not correspond to au of KRIBS’s types. Rather, they correspond to a type shown in a schematic drawing (CARLQU Tsr 1961, Figs. 4—12). and later described as one of the wood features referable to the concepts of paedomorphosis (CARLQUIsT 1962). Uniseriate rays are entirely composed of erect

Figs. 11—- 16. Wood sections of Notobnrtis. 11—13. N. nrnonnutn, FHOw-7125. 11. Transection. Growth rings absent. 12. Tangential section. Rays scarce, narrow. 13. Tangential section; splits in tracheid at right. 14—16 .V. nataic,cns, SJ Rw-7477. Perforation plates finn radial section, showing variations in size, degree of interconnection among bars. Figs. ] 1, 2. Scale above ‘Fig. 1. Figs. 13 .15. Scale above Fig. 4.

S. 474 CARLQuIST Wood Anatomy of Buxacoae 475 cells. Multiseriate rays are composed of square to erect cells, with very few procumbent cells. These ray conditions are much like those in Styloceras, but with greater erectness of ray cells. Such preponderance of erect ray cells may be an ontogenetic matter. Procumbent ray cells tend to increase in abundance with age of stem (BARCH00RN 1941). The type of rays found in Sarcococca might therefore be expected to yield the Heterogeneous Type I of K.RIBs if stems increased sufficiently in diameter and horizontal subdivision of ray initials occurred with time. However, stems of Sarco cocca mostly do not increase much in diameter because new shoots are continually innovated and older shoots cease active addition of secondary xylem. Therefore, occurrence of a more juvenilistic ray type in the stems of Sarcococca, which can be licked to “sucker shoots”, is understandable. The stems of Sarcococca confusa showed such juvenilism quite clearly, since they were smaller than the stems studied of S. ruscifoiia. As shown in Fig. 24, rays of S. confusa are almost all uniseriate, and the few multiseriate rays are only two cells wide at most. Ontogenetic origin of the ray system wholly as uniseriates, or nearly so. can also be seen in Illiciurn (BAIIEY & NA5T 1948; CARLQUIsT 1982). This feature is regarded as a specialization by BAILEY & NAs’r. As seen in radial section, walls of ray cells in sectional view have some bordered pits. in all species of Buxus and Notobuxus studied, at least a few bordered pits on ray cells were seen. Bordered pits in ray cells are much more common that generally realized (e.g. CARLQuIsT 1980a). Ray cells throughout Buxaceae have lignified se condary walls. Rays of Buxaceae tend to parallel in height the length of tracheary elements, so that the tallest rays are in Stylocera.s, Sarcococca. and Notobuxus natalensis (Table 1, columns 8 & 9). Fluctuation in height of multiseriate rays among species of Buxus is related to abundance of uniseriate rays, since as noted above, when uniscriate rays are frequent in. a species, more numerous multiseriate rays tend to terminate in uniseriate wings and thus be taller. Horizontally subdivided ray cells were not observed in Buxaceae.

With respect to ray width, interesting differences among species may be seen (Table 1, column 10). Rays of Buxus glomerata (Fig. 6) are notably wider than those of other species of Buxus (Fig. 2). Differences in ray width between the two species of Saicococca (Figs. 24. 29) doubtless is related to the ontogenetic situation described above; originating as uniseriate rays composed of erect cells only, procum bent cells, forming progressively wider rays, gradually increase in number with age. Ray cell size is appreciably greater in Sarc30000ct (Figs. 24. 29) and Styloceras (Fig. 34) than in Buxu.s (Figs. 2, 6) and Notobuxus (Figs. 12, 18). The rays in Noto

Figs. 17—22. Wood sections of Notobnxus. 17—21. N. macowenji, MADw-14198. 17. Ti.ansection. Growth ring evident. 18. Tangential section. Rays numerouS, narrow. 19—21. Perforation plates from radial section. 19. Double perforation plate. 20. Typical perforation plate. 21. Perforation plate with few bars. 22. N. natolensis, SJRw-7477. Transection; parenchyma mostly abaxial to vessels, clearly visible by virtue of contrast with the thick-walled tracheids. Figs. 17, 18. Scale above Fig. 1. Figs. 19, 20. Scale above Fig. 4. Fig. 22. Scale above Fig. 3. ICI4 j

1S]YfliVO 9k1 Wood Anatomy of Buxaceae 477 buxus acuminata (Fig. 12) are notably less abundant than in other species of Buxaceae (except for Simmondsia, Fig. 39).

Crystals and, i)eposits Crystals were not observed in woods of Buxaceae s.s., nor were they reported by S0LEREDER (1908) or METcALE & CHALK (1950), although of Buxaceae do contain crystals. Buxaceous woods are free from dark-staining compounds or gummy deposits. The pale color of buxaceous woods as seen in gross aspect betokens this lack of deposits.

Growth Rings Growth rings are absent from. specimens studied of B. lomerata (Fig. 5), which occurs in Cuba and Haiti. Other subtropical or tropical Buxaceae in which growth rings were not observed include Notobuxus acuminata (Fig. ii), N. natalensis. and Styloceras laurifolium (Fig. 33). Not surprisingly, species of Buxacea.e from higher latitudes show growth rings. Where growth rings occur iii Buxus and Notobuxus, they can be described as con sisting of wide vessels of fairly uniform length until the rather sudden onset of late- wood, in which narrower vessels are briefly formed. followed by a. band of latewood nearly devoid of vessels. This tendency is shown in Fig. 3 for Buxus sempervirens, but it may also he seen in B. balearica (Fig. 1) and Notobuxus macowanii (Fig. 17). Gxxuuss (1959) oversimplifies somewhat when he says that earlywood cannot be distinguished from latewood in B. seinpervirems because vessels are of the same dia meter throughout.. The fluctuation in diameter is certainly small. Likewise, contrary to GREouss. occasional vessels may he seen in the terminal band of latewood, although in limited numbers, so that as a generalization his observation is essentially correct. The growth rings of Buxus and Notobuxus would therefore he referable to Type VA in my (1980 h) categorization of growth rings. In Sarcococca. the patterns are similar to those in Buxus, but latewood instead of lacking vessels merely grades fairly abruptly into zones with slightly fewer and slightly narrower vessels (Figs. 23, 28). The Sarcococca growth rings fall in Type ID according to my (1980b) scheme. The first growth ring in Sarcococca stems studied is larger than the second, which is, in turn, wider than the third (Fig. 23). The short and relatively finite duration of shoots in Sarcococca accounts for this: less wood is added as the shoot becomes inactive.

Figs. 23—27. Wood sections of Sarcococca confwee, Palmer 37—55 (Cambridge). 23. Transection, showing progressively narrower growth rings. 24. Tangential section. Ray cells large. 25. Radial section showing helical thickenings on vessel walls (left); tracheids; and perforation. plate of vessel (right). 26. Radial section with typical perforation plate in its entirety. 27. Transection. Growth ring evident; axial pa.renchyina scarce. Figs. 23, 24. Scale above Fig. 1. Figs. 25, 26. Scale above Fig. 4. Fig. 27. Scale above Fig. 3. mci

LS1YITV) •S SLT Wood Anatomy of Buxaceae 479

indicators of Evolutionary Advancement: Summary Buxaceaes.s. qualifyasarela.tively primitive familyonthe basis of wood characters, with a rather remarkable span of features expressed in the few genera. While many features are susceptible to ecological interpretation, many others cannot be specifi cally discussed in that context; these latter are considered in this section. Vessel element length can be related to ecology, but the ratio between tracheid length and vessel element length (Table 1, column ii) has a broader phyletic signi ficance. This ratio was cited as a sensitive indicator — within limits — of wood specialization. More particularly, it is an indicator of division of labor between vessel elements and imperforate tracheary elements (CARLQUIsT 1975). In Sarcococca and Styloceras. the ratio hovers just above 1.10, which is approximately the lowest ratio one expects in woods with very primitive vessels. In Buxus and Notobuxus, the ratio lies mostly between 1.3 and 1.5, despite fluctuation in vessel element length among the species. That range shows moderate advance, but not nearly as much as that of Simmoncisia, in which the ratio is 2.2. The precise parallel between number of bars per perforation plate and vessel element length is interesting. If Buxaceae were plotted for these two features, a straight line would result; in dicot ledons as a whole, the correlation is much looser. More numerous bars per perforation plate are interpreted as a primitive condition by FRosT (1930); undoubtedly there is little reversion from few to many bars, so that this trend is, within reasonable limits, not subject to reversion. Certainly no bars are added phyletically to a simple perforation plate, at least not in an orderly scalariform manner (CARLQuI5T 1980b). The values for bars per perforation plate in Table 1 can be interpreted in terms of phyletic progression rather closely, although the two different values for the two collections of Styloceras cannot be so interpreted: where bar number is very great, accurate determination of bar number is very diffi cult, and representative samples are difficult to obtain. Alternate pitting predominates on lateral vessel walls of Buxaceae. On the rare vessel-vessel contacts and on some vessel-ray contacts, opposite pitting may be found. Thus, using the criteria of FRoST (1931), Buxus has specialized lateral wall pitting on vessels, with vestiges of moderately primitive expressions. Buxaceae qualify as primitive with respect to imperforate elements. All species studied have fully bordered pits on the tracheids, and no elements which could be termed fiber-tracheids or libriform fibers can be designated. Axial parenchyma is diffuse throughout the family, but with modifications. Diffuse axial parenchyma is the primitive type for dicotyledons (KRIB8 1937). Modest degrees of grouping of axial parenchyma cells with each other (diffuse-in-aggregates) and with vessel elements (abaxial) may be found in Buxus and Notobuxus, indicating

Figs. 28—32. Wood sections of , CARLQUIsT 15636. 28. Transection. Faint growth ring evident. 29. Tangential section. Rays vary in width. 30—32. Radial sections. 30.

Helical thickenings on tracheid walls. 31. Scalariform — opposite lateral wall pitting on vessel; tracheids showing bordered pits at right. 32. Portion of perforation plate. Figs. 28, 29. Scale above Fig. 1. Figs. 30—32. Scale above Fig. 4. 11.1

III

U,

Dji 2 Wood Anatomy of Buxaceae 481 moderate specialization in these two genera; Styloceras and Sarcococca qualify as more primitive in retaining the diffuse condition. Ray histology of Styioceras qualifies it as having the most primitive type for the family, a type comparable to that in primitive dicotyledonous woods at large, ac cording to the scheme of KRms (1935). From this type, the rays in Buxus and Note buxus show specializations in loss of procumbent cells in uniseriate rays and loss of erect ray cells (except for the short wings, where present) in multiseriate rays. The rays of Sarcococca are of the more primitive type but are modified by juvenilism, so that they are composed mostly of erect cells. Rays of Buxus and Notobuxus are moderately specialized, as is the case in axial parenchyma in those genera. Origin of rays near the pith as uniseriate rays only, as seen in S’arcococca, should be regarded as a specialization, in accordance with that interpretation in fiticium (BAILEY & NAsT 1948; CAIILQuIsT 1982). Bordered pits on ray cells of Buxaceae do not connote primitiveness so much as enhanced mechanical strength combined with optimum conductive ability.

Summary of Ecological Aspects of Wood Anatomy

Most Buxaceae have vessel elements in the modal range for dicotyledons as. a whole; Sarcococca and Styloceras have vessel elements longer than that modal cotidition. Certainly shortening of vessel elements is a phylesis that occurs with relation to drier conditions (WEBBER 1936; CARLQU1sT 1966), and Buxaceae demon strate this. However, as with Illicium (CARLQuIs’r 1982), Buxaceae s.s. represent only moderate shortening of vessel elements, and thus moderate adaptation by this measure to drier conditions. Much more marked adaptation is shown by other vessel features, perhaps because alteration of vessel element length is evolutionarily a more difficult process, based as it is on length of fusiform cambial initials. Much more readily modified, as growth rings demonstrate amply, are vessel diameter and density of vessels per unit transection. Vessel elements in Buxaceae are relatively narrow and numerous per mm2 of transection. Those two measures were used to construct an index, “vulnerability” (see Table 1, column 12) for dicotyledonous woods (CARLQTIsT 1977). Vulnerability ratios of below 0.2 may be said to connote xero morphy in a group of woody with evergreen leaves (and thus comparable with Buxaceae), for example., .Pittosporaceae (CARLQUIsT 1981). Buxus and Notobuxus generally fall below the 0.2 level, while Sarcococca an.d Styloceras lie well above it. The numerous narrow vessels in the former two genera offer great redundancy, which theoretically would permit functioning of the conductive system even if numerous vessels were blocked by air embolisms.

Figs. 33 37. Wood sections of Stytoceras laurifolium, MADw-27865. 33. Transection. Vessels much larger than in other genera. 34. Tangential section. Strands of axial parenchyma at lower right. 35. Radial section showing most of a perforation plate. 36. Portion of a perforation plate showing bordered condition of bars. 37. Transection. Axial parenchyma is abundant. Figs. 33, 34. Scale above Fig. 1. Figs. 35, 36. Scale above Fig. 3. Figs. 317. Scale above Fig. 36. LsnThmvO Wood Anatomy of Buxaceae 483

The vulnerability ratio multiplied by mean vessel element length produces an index, “mesornorphy” (CARLQUI5T 1977), in which Buxaceae as a whole appear some what less xeromorphic. Species of Buxus and Notobuxus mostly fall within the range from 30 to 80 for this index. Species of Pittosporurn from open scrub (P. tobira) or from alpine localities (P. turneri) have comparable ranges in this index (CARL QTJIST 1981), but most species in Pittosporurn have mesomorpity index values over 100. In the present study, Sarcococca and especially Styloceras have such higher values. Styloceras qualifies on the basis of this index as a rain forest plant, which it is: according to WEBERBAUER (1945). Sarcococca is peculiar in that its habit (especially in S. confusa) of innovating short-lived branches from near the base permits its foliage presentation to die back during unfavorable seasons, while growing for longer periods if seasons are favorable. Sarcococca is thus like Balanops pancheri (CARLQU1sT 1980a, p. 216) in having a mesomorphic xylem but in also having a growth form which can compensate for that conformation, altering the amount of branch system presented from year to year. The lowest snesomorphy index value in the family (excepting Sirninondsia) is found in Buxus halearica, which occupies what may be the driest sites exploited by Buxaceae s.s. Within Buxws and Notobuxus. the higlist mesomorphv index values are exhibited by B. wailichiana and N. natalensis, species which occupy moister and more tropical areas than their congeners. These two species are exceptional in their genera not only in having longer vessel elements (included in the index), but also more numerous bars per perforation plate, a feature correlated with meso morphy (CARLQUI5T 1975). Buxus muelleriana, reported (as B. subcolumnari.s) to have more than 30 bars per perforation plate by S0LEREDER (1908), has remarkably large leaves and a clearly more mesic habitat than other Buxus species. One must hypothesize that the mesomorphic wood features of Buxaceae cited above persist (in the case of scalariform perforation plates and long vessel elements) during unbroken occupancy of mesic sites (assuming that these features are irreversi ble). The diameter of vessel elements and their density are reversible features. If, however, the xylem of Buxaceae represents persistence of some old and mesomorphic features. the nature of the foliage may be responsible in pa.rt. size tends toward microphylly in Buxus and Notobuxus species in drier areas. These species also have remarkably thick leaf cuticles and sunken stomata. With respect to potentially compensating effect of leaf cuticle and stomata in a group with primitive and meso morphic wood, Buxaceae may be likened to Balanopaceae (CARLQuIsT 1980a). The persistence of bars on perforation plates in both families — fewer bars in species from areas where transpiration rates are likely to be higher is notable.

Figs. 38--43. Wood sections of Simmoncisia cijinensis, HENRIcKs0N 2345. 38. Transection, showing products of successive cambia. 39. Tangential section of xylem band; rays inconspicuous. 40. Transection; a xylem baud and, near bottom, preceding parenchyma band. 41. Transection; a rare axial parenchyma cell, upper right; thick-walled vessel below. 42, 43. Portions of vessel walls from radial sections, showing helical thickneings. Figs. 38, 39. Scale above Fig. 1. Fig. 40. Scale above Fig. 3. Figs. 41—43. Scale above Fig. 4. 32a 484 S. Cuiuis

Vessel walls in Sarcococca (as well as tracheids in that genus) bear helical thickenings If these thickenings were indicative of resistance to drought in the family, one might have expected them in Bar us. However, Burns does not approach the desert habitats of shrubs which so frequently show these thickenings, as in Asteraceae (CARLQUI5T 1966) and others (WEBBER 1936; see Simmondsia also, Figs. 43 and 44). However, helical thickenings in dicotyledon vessels have originated numerous times, and probably not always for identical reasons. The species of lUicium which grow in areas where frost is more prevalent have such thickenings on vessel walls (CARL QUIST 1982), and that factor may account for innovation of these thickenings in Sarcococca. Buxaceae are also interesting in. the persistence of a primitive imperforate element type (tracheid). Tracheids are ideal as a cell type which prevents the spread of air embolisms in xylem. That may account for presence of tracheids in a remarkably high proporiion of woods in deserts of southern California (CARLQuIs’r 1980b). Buxa ceae (and especially Simmondsia) may survive in moderately dry areas on this account, Furthermore, growth ring phenomena in Buxaceae s.s. may be keyed to the value of tracheids during periods of drought.. In those species of Buxaceae s.s. with growth rings, latewood lacks vessels. Conduction in latewood can therefore be on an all tracheid basis, a potential phenomenon noted earlier (CARLQuIsT 1978, 1980 b). The lumina of tracheids in Buxaceae are not notably wide (e.g., Fig. 3), but tracheids would be a conductive system subsidiary to vessels at best, and the volumes of water conveyed during drought periods ought to be much less than during growth periods. The grouping of axial parenchyrna cells (diffuse-in-aggregates, abaxial) and the specialization in ray histology in Buxaceae (procumbent cells prodominant in multi senate rays) appear to denote moderate levels of specialization. These specializations in parenchyma can also be interpreted ecologically (CARLQuIsT 1975). Specialization in wood parenchyma seems to maximize potential conductive rates of photosyni thate-bearing solutions within wood. Buxaceae s.s. exemplify this in ray cell shape and grouping. The presence of bordered pits in ray cells in many Buxaceae would connote maintenance of mechanical strength of cell walls combined with maximiza tion of conductive rates across those walls. Procumbent cells offer fewer cross walls (a potential hindrance to horizontal conduction) per unit radial length of ray.

Phylogenetic Relationships of Buxaceae

Four main affinities have been claimed for Buxaceae. These can be cited in terms of ordinal names: Celastrales, Euphorbiale.s, Hamarnelidales, and Pittosporales. The evidence for each of these placements is discussed below primarily in terms of wood anatomy, but other features are also included. Assessing evidence from wood anatomy is not easy because similarity does not necessarily indicate relationship. Rather, similarity may indicate independent attainment of (or retention of) similar evolution ary levels. Consequently, one should be very careful about the similarities claimed by JANssoNIus (1950) among dicotyledon families. On the other order, where Wood Anatomy of Buxaceae 485 an entire order contains woods much more specialized than woods of Buxaceae, the order can be ruled out as providing a probable progenitor. One is left with, at. most, a hypotherical common ancestor in such a case. Celastrales have been the choice of a scattering of botanists speculating on the affinities of Buxaceae. These authors include BAILL0N (1887); BEssEY (1915); P(LLE (1952); Soó (1967) and DAHLQREN (1977). With respect to wood comparisons, one may concentrate on Celastraceae (data from METCALFE & CHALK 1950). Vessels in Cdaefrac.eae have only alternate lateral wall pitting patterns, with no vestiges of opposite, as in Buxaceae. Perforation plates in Celaetracae with more than 10 bars are infrequent. Perhaps more significantly, axial parenchyma is very rarely diffuse (which is reported from only three genera), and is generally present in bands, a type unknown in Buxaceae. Buxaceae show transitions from diffuse to diffuse-in-aggre gates and more particularly, abaxial, a type lacking in Celastraceae, apparently. Ray histology in Oelastraceae shows a range very similar to the range in Buxaceae. Tracheids and fiber-tracheids are the imperforate elements in Oelastraceae. Septate fibers, unknown in Buxaceae, occur in Celastraceae. Crystals are frequent in rays of Gdastraceae, whereas they are absent in woods of Buxaceae. If these differences do not rule out possible relationship between Buxaceae and Celastraceae, they do not strengthen the claimed affinity. Euphorbiaceae and a few small families constitute Eupliorbiales. A euphorbialean alliance for Buxaceae is supported by many authors, such as ENDLIcHEB (1841), who included the family in Euphorbiaceae. Among recent adherents of Euphorbialean affinity for Buxaceae are CR0NQUIsT (1968); HEYwoon (1978); BENsoN (1979) and, on the basis of pollen morphology, ERDTMAN (1952) and KöHLER (1980). Tricarpellary gynoecia and presence of caruncles are cited as resemblances between Euphorbiaceae and Buxaceae. The caruncle in Buxaceae is probably a mvrmecochore. and such myr mecochores may evolve independently in dicotyledous more than once. With respect to wood anatomy of Euphobiales, we may neglect Daphniphyliaceae, which probably is not closely related to Euphorbiaceae, and concentrate on Euphorbiaceae itself. Although Euphorbiaceae is a heterogeneous families, its wood expressions are in the specialized to highly specialized range. Vessel elements have simple perforation plates, except for a few genera listed by METcALFE & CHALK (1950). Imperforate tracheary elements have pits which are simple or nearly so. Rays are of two distinct sizes (with rare exceptions), the larger 4—17 cells uide (METcALFE & CHALK 1950). These at their lower limit would exceed the width of multiseriate rays of most Buxa ceae (see Table 1, column 10). Axial parenchyma is composed of short bands in Euphor biaceae and contains crystals. This constellation of wood features not only is markedly different from those of Buxaceae, it is appreciably more specialized in evolutionary level. Buxaceae could not be derived from Euphorbiaceae as presently known, and one would have to invoke at best a hypothetical common ancestor. Hamamelidales as a placement for Buxaceae has been advocated by several authors, most notably HUTCHIN50N (1926, 1969); Tipro (1938); CoRNER (1976), and TAKHTAJAN (1980). One can use Hamai elidaceae as the base for comparison in wood anatomy, 486 S. C.iir.uis’r

because the small families usually associated with Hamameiidaceae (Cercidiphyl laceae, Eupteleaceae, Platanaceae} have very similar wood features. Vessel elements have scalariform perforation plates, often with numerous bars (plates often simple in Piataniis). Lateral wall pitting is calariform or opposite (METCALFE & CHALK 1950). Imperforate tracheary elements are all tracheids. Axial parenchyma is diffuse. but diffuse-in-aggregate and banded (small aggregations) also occur; truly paratracheal parenchyma is apparently not usually present. Rays are narrow, and follow KRTBS’s (1935) Heterogeneous Type II and III; they rather infrequently conform to Hetero geneous Type I. Thus rays of Hamarnelidaceae are comparable to those of Buxus often. Crystals are infrequent in rays and axial parenchyma of Ham arnelidaceae, but may be found prominently in some species (CARLQUIsT 1980a). Thus woods of Hamamelidaceae are comparable in level of evolution to woods of Buxaceae, and have few features alien to Buxaceae. The banded parenchyma of Hctmamelidaceae is a minor departure from diffuse-in-aggregates, and crystal presence characterizes a minority of hamamelidaceous woods. Buxaceae has also been placed in recent years in Pittosporales. an order invented by HITCHINs0N. but much revised and expanded by TH0RNE (1977), who places Buxaceae in a separate suborder of Pittosporales, emphasizing its distinctness from other pittosporalea.n families. TH0RNE’s Pittosporales falls into his superorder Rosi J’lorae, and thus lie emphasize,s a rosoid or saxifragoid affinity for the order. This order is quite heterogeneous in terms of wood anatomy, but can be characterized basically as having rather primitive woods. By virtue of primitiveness in wood, &yloceras and. to a lesser extent, Buxus compare rather closely to TH0RNES Pitto sporales. Lack of crystals characterizes Roridulaceae (CARLQuIST 1976), but most of the families of TH0RNE’s Pittosporales have them. However, one may note that in each of these families, crystals are more abundant in species in dry localities, whereas species in quite wet localities lack them (CARLQUIST 1981). The gummy deposits and horizontally subdivided ray cells characteristic of pittosporalean families (CARL QfIST 1978, 1981) do not occur in Buxaceae. However. Pittosporaceae. once thought distiuctive by virtue of having exclusively simple perforation plates, now proves to have scalariform perforation plates in at least one species (CARLQUIsT 1981), so that a potential contrast with Buxaceae is slightly lessened. In sum, if one compares wood anatomy of B’uxaceae to that of the four main orders claimed to bear some resemblance to Buxaceae, one finds that Hamarnelidales and Pittosporales offer the closest comparisons, although Buxaceae has a few features (axial parenchyma abaxial to vessels in part) not observed in those groups. The diversity of Pittosporales as recognized by TH0RNE makes exclusion of Buxaceae difficult, but hamamelidoids, if a less diverse group with respect to woods, resemble Buxaceae to an equal degree. Celastrareae seems a little more removed than those two groups from Buxaceae on the basis of wood anatomy, with Euphorbiales the least similar to Buxaceae of the four with respect to xylem. One may add one curious plant to this discussion: Didymeles, a monotypic genus endemic to Madagascar. The systematic position of Didymeles, usually placed in Wood Anatomy of Buxaceae 4S7

a monogenerie family, has been uncertain. ERDTIAN (1952) found resemblance be tween Didyineles and Euphoibiaceae, a resemblance in pollen also noted by KöHLER (1980). However, in order to match features of the Didymeles pollen grain in Euphor biaceae, one must select pollen characters from various Eephorbiaceae: the tricolpate condition with central exine strip in colpi of crotonoids, the oroid colpi (but without the central strip) in Breynia (ERDTMAN 1952). KöHLER (1980) places Didymeles next to Buxaceae because of similar reasoning with respect to pollen: no genus of Buxaceae has the colpus structure of Didymeles; exine patterns of Pachysandra and Sarcococca, if “crotonoid” (polyporato with triangular exine ornaments around apertures), do not have the tricolporoid condition of Buxaceae. No single genus of Buxaceae matches Didymeles closely in pollen. However, Buxaceae and Didyrnele.s do share “eucyclocytic” stomata (for an illustration, see CARLQUIs’r 1961). Thus, Didymeles may be related to Buxaceae. but the situation is not at all clear yet. TAKHTAJAN (1980) claimed that “the genus Didymeles is related to Ilamamelidales, but the stomata, pollen grains, and ovules are different, the gynoecium is mono carpellate, and the leaves are exstipulate. Moreover. the coat anatomy of Did, ineles is sharply distinct, from that of the Hamamelidales and related orders”. The numerous differences between Ilamamelidales and Didymeles would perhaps cause one to question TAKHTAJAN’s reasoning. The wood anatomy of Didymeles is at about the same level of primitiveness as Styloceras, judging from TAKHTAJAN’s description, but the alleged lack of axial parenchyma in Didymeles is curous.

Simmondsia: wood, ecology, and relationships

Traditionally, Simmondsia has been placed in Buxaceae. METcALFE & CHALK (1950) give Simmondsia a separate section within their discussion of Bu.raceae on account of the occurrence of successive cambia in the genus. A review of Simmondsia wood seems warranted, for minor amplifications of METCALFE & CHALK’s (1950) account can be offered, and the question of relationships of the genus can be re-exam ined. The wood of Simmondsia (Figs. 38—44) results from production of narrow xylem increments, accompanied by phloem strands, by means of successive cambia which also add intervening parenchyma bands. The xylem bands do not have indefinite tangential extent, and arcs of yxiem separated from each other by radially-oriented parenchyma sheets may be seen (Fig. 38, center). Vessels are solitary, as in Buxaceae. Perforation plates of vessel elements are invariably simple, as one might expect in a xeromorphic shrub, according to my earlier considerations (CARLQuIsT 1975). Vessels are thick-walled, a feature also found in xeromorphic shrubs. Vessels are narrow, as one might also expect in a dry environment (Table 1. column 2). The number of vessels per sq. mm. (Table 1, column 1) is not exceptionally low, because the fields viewed to obtain this figure did not exclude parenchyma bands. Thus the vulnerability index (Table 1, column 12) is not as low as one would ordinarily expect for a desert shrub. The vessel elements 33 Flora. Bd. 172 488 5. C.xuis in Simmondsia are exceptionally short, however (Table 1, column 5). Thus the meso rnorphv index value is quite low (Table 1, column 13) and does fall in the range of a desert shrub. Vessel elements of Simmondsia (but not tracheids) bear helical thicken. ings (Figs. 42, 43). These are probably an innovation independent of the helical thickenings in Sarcococca. Many desert shrubs have helical thickenings in vessels (WERBER 1936; CARLQuIsT 1966). Imperforate tracheary elements in Simmondsia are all tracheids, as in Buxaceae s.s. Pits are fully bordered, about 3 m in diameter. Although presence of tracheids might at first glance seem unusual where wood is otherwise rather specialized, the retention of tracheids in woods of the southern California deserts can be hypothesized to have a high selective value, and is indeed present in many such woods (CARL. QUIST 1980b). The ratio of tracheid length to vessel element length (2.21) is higher than in the genera of Buxaceae s.s. (Table 1, column 11) and may be taken as an ac curate index of the specialization of Simmondsia wood, perhaps accelerated in adap - tation to desert conditions. Axial parenchyma occurs only in the xylem bands in the form of very infrequent cells (Fig. 41), not subdivided into strands. Absence of axial parenchyma is probably related to the compensatory presence of the parenchyma bands which intervene between xylem arcs (Fig. 40). Vascular rays are likewise few in number (Fig. 39). A few rays can be traced from one xylem arc to another, but most cannot. The uni senate rays consist of erect cells. Multiseriate rays are rather narrow and are composed almost wholly of square to erect cells, like those of Sarcococca. Near absence of pro cumbent ray cells may be explained as a j uvenilism as in Sarcococca, but for a different reason: each cambium in Simmondsia operates only for a short period, only a por tion ofa year. The rays of Simmondsia are within the histological range ofBuxaceac s.s. Although not mentioned by METCALFE & CHALK (1950), Simmondsia does have crystals in the wood. These crystals are not present in the xylem arcs themselves, but in the intervening parenchyma bands. The crystals are rhomboidal, borne singly in cells, and occur in idioblastic form, rather sparsely. The pattern of vessel dimensions in Simmondsia is not related to the xylem arcs: a xylem band may begin with narrow vessels or with wide ones (Fig. 38). Annual increment of growth include more than one xylem band, and possibly a growth season might begin by completion of a xylem band rather than initiation of a new arc. This topic needs further investigation.

The problem in assessing wood anatomy of Simmondsia with regard to relationships of the genus lies in the modification of the wood with reference to xeromorphy and with reference to the occurrence of successive ca.mbia, as noted above. If one takes these factors into account, nothing in the wood of Simmondsia, highly specialized though it is, positively rules out inclusion of the genus in Buxaceae. That statement could also be made with relation to any affinity advanced between Simmondsia and a family other than Buxaceae also. The data on subsidiary cell patterns of leaves of Simmondsia is uncertain; BARA xovA (quoted in TAKHTAJAN 1980) claims Simmondsia has an encyclocytic pattern WoOd Anatomy of Buxaceae 489 like that of &yloceras, whereas METcALFE & CHALK (1950) claimed a ranunculaceous pattern for Simmondsia. The absence of nectaries in Simmondsia is easily related to the shift to anemophily by the genus, and that also may explain the distinctive ectexine (CHANG 1964). The distinctive chromosome number of Fimmondsia cannot rule out relationship; that number (x = 13) can be found in Pachysandra also (RAvEN 1975). That is also true of the large with cotyledons rich in liquid oils and the lack of endosperm in the mature seed. With respect to chemical constituents (BRowN 1976), Simmondsia differs appreciably from Buxaceae s.s.; however, it does not approach any other family closely in these respects either. One may well choose to recognize the many distinct features of Simmondsia by placing it in a family by itself, in common with DARLGREN (1977) and TAEHTAJAN (1980). With respect to relation ships, one may agree with TH0RNE (1976) that at present it should he regarded as a genus incertae sedis. In order to clarify the questions about subsidiary cell occurrence in Simmondsia

Didymeles, and Buxaceae, I prepared leaf sections and epidermal peels of the two former genera and of Sarcococca. Didymeles does not have subsidiary cells at all; subsidiary cells could be defined by virtue of greater tannin content, but not in any other way. Also, Didymeles has small peltate non-glandular trichomes which are not matched in Buxaceae. Therefore, relationship of Didymeles to Buxaceae seems improbable. Simmondsia also does not have encyclocytic subsidiary cells its condi tion is apparently just a slightly modified ranunculaceous condition and not at all the precise series of six cells seen aroundguard cells in Sarcococca and other Buxaceae. According to my observations, such genera of Ramamelidales as Tetracentron have encyclocytic subsidiary cells, and relationship between Buxaceae and Hamamelidales seems likely. The relationships of Simmondsia may well proved to be with Euphor biaceae; one can cite recent phytochemical evidence in this regard (ScoGIN 1980).

References

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Received October 20, 1981

Author’s address: S. CARi.QuxsT, Rancho Santa Ana Botanic Garden, Claremont, California 91711, U.S.A. Reihe ,,Einfuhrung in die Hydrobiologie”

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