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1994 Systematic Anatomy of Euphorbiaceae Subfamily Oldfieldioideae I. Overview W. John Hayden University of Richmond, [email protected]

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Recommended Citation Hayden, W. John. "Systematic Anatomy of Euphorbiaceae Subfamily Oldfieldioideae I. Overview." Annals of the Missouri Botanical Garden 81, no. 2 (1994): 180-202.

This Article is brought to you for free and open access by the Biology at UR Scholarship Repository. It has been accepted for inclusion in Biology Faculty Publications by an authorized administrator of UR Scholarship Repository. For more information, please contact [email protected]. SYSTEMATIC ANATOMY OF W.John Hayden2 EUPHORBIACEAE SUBFAMILY OLDFIELDIOIDEAE. I. OVERVIEW'

ABSTRACT

The biovulate subfamily Oldfieldioideaeof Euphorbiaceae, characterized by spiny pollen, is an otherwise apparently diverse assemblage of mostly Southern Hemisphere and that traditionally have been allied with genera of Phyllanthoideae and Porantheroideae sensu Pax and Hoffmann. Although fairly diverse anatomically, the following structures characterize the subfamily with only a few exceptions: pinnate brochidodromousvenation with generally randomly organized tertiary and higher venation; foliar and petiolar glands absent; unicellular or unbranched uniseriate ; absent; mucilaginous epidermis or hypodermis; brachyparacytic stomata; vessel elements with simple perforation plates and alternate, often very small, intervascular pits; thick-walled nonseptate imperforate tracheary elements; numerous narrowheterocellular rays; and abundantaxial xylem parenchyma in diffuse to somewhat banded patterns and often bearing prismatic crystals. Anatomically, the shrubby Australian ericoid genera a well-definedgroup with obvious affinities to the more arborescent Australasian genera, which show clear relationships to each other; the African and neotropical genera bearing compound form another distinct group; the remaining genera are somewhat more isolated and seem to represent, in various cases, elements that are primitive within the subfamily or elements derived from the group bearing compound leaves. Presence of theoid teeth and palmately compound leaves in Oldfieldioideaeare features consistent with Dilleniid origin for Euphorbiaceae.

As a taxonomic entity the euphorbiaceous sub- dendron was shown to be a member of Oldfieldioi- Oldfieldioideae K6hler & Webster dates deae (Hayden, 1977; see also Hayden et al., 1984, conceptually from the palynological studies of Punt and Hakki, 1985), an anatomical survey of the (1962) and K6hler (1965) who noted the spiny entire subfamily was initiated (Hayden, 1980) to pollen that characterizes the group; the assemblage assess relationships from data independent of re- recognized by pollen structure was subsequently productive (including pollen) morphology. Based in formalized nomenclaturally as a new subfamily part on these anatomical studies, classification of (Webster, 1967). In essence, pollen characters Oldfieldioideaehas been modified from Webster's circumscribed a group of genera that previously (1975) original proposal; two broadly similar clas- had been assigned to the biovulate subfamilies Phyl- sifications, one by G. L. Webster (the preceding lanthoideae and Porantheroideae in the system of issue) and another by G. A. Levin and M. G. Pax & Hoffmann (1931). Webster's first (1975) Simpson (this issue), are proposed elsewhere. classification of oldfieldioid genera contained sev- eral novel taxonomic associations at variance with HISTORY earlier classifications, notably those of Pax & Hoff- mann (1931) and Hutchinson (1969). Classifications of Euphorbiaceae from the first Interest in the anatomy of Oldfieldioideae half of the 19th century (e.g., Jussieu, 1824; End- stemmed from the need for comparative data to licher, 1836-1840) offer little insight into rela- aid placement of the problematic Picroden- tionships among oldfieldioid genera. At this for- dron Planchon (Hayden, 1977). Despite a number mative time in the definition of Euphorbiaceae of publications dealing with the anatomy of old- (Webster, 1987) the few oldfieldioidgenera known fieldioid genera (Appendix 2), detailed information were often scattered widely in the family; more- for most of the subfamily is lacking. Once Picro- over, some were referred to other families. Genera

' This study is based largely on a Ph.D. dissertation submitted to the University of Maryland, College Park. I thank W. L. Stern for assistance and guidance; H. K. Airy Shaw, L. J. Hickey, G. A. Levin, A. M. W. Mennega, and G. L. Webster were particularly helpful in providing specimens and/or comments; numerous others also provided specimens. 2 Department of Biology, University of Richmond, Richmond, Virginia 23173, U.S.A. ANN. MISSOURIBOT. GARD. 81: 180-202. 1994. Volume 81, Number 2 Hayden 181 1994 EuphorbiaceaeSubfamily Oldfieldioideae

of Pseudanthinae (or Caletieae in the traditional/ included, using current nomenclature, Dissiliaria, narrow sense) were the first to be classified to- Longetia, Austrobuxus, Hyaenanche, Mischo- gether, undoubtedly because of their shared ericoid don, Oldfieldia, Baillon, and only one xeromorphic habit and common provenance in nonoldfieldioidgenus, Bischofia Blume, within gen- . Baillon (1858) grouped Micrantheum era 46-54. Although these constituted three Desf. with Pseudanthus Sieber ex Sprengel, to discrete groups in his conspectus, Bentham (1878) which Agardh (1858) added Plan- expressed some doubt about their relatedness and chon, establishing the composition of Caletieae that he chose to associate Neoroepera and Petalostig- was followed in all subsequent studies until the ma with other phyllanthoid genera. Pax (1890) addition, first, of Neoroepera Muell. Arg. by Koh- treated oldfieldioidgenera much as had Bentham; ler (1965) and, now, the inclusion of all Austral- Engelm. ex C. Parry, however, was asian oldfieldioidsas proposed by Levin & Simpson included, and Pax & Hoffmann (1931) added Peta- (1994, this issue) and Webster (1994). During the lostigma, Androstachys Prain, and Aristogeiton- intervening years, however, the use of cotyledon ia Prain to various subtribes consisting largely of width as the primary criterion for subdivision of oldfieldioid genera. Perhaps the first clear indica- the family (Mueller, 1866; Pax, 1890; Pax & tion of the relatedness of oldfieldioid genera can Hoffmann, 1931) relegated the genera of Pseu- be found in Pax's (1925) essay on Euphorbiaceae, danthinae (as Caletieae) to the Stenolobeae, a small which includes the phylogenetic reproduced group of Australian xerophytes with narrow cot- in Figure 1. Although much of the detail in this yledons. Their somewhat isolated position in Sten- phylogenetic tree may be challenged seriously in olobeae minimizedassociation of Pseudanthinaewith the light of present knowledge, it does show old- other oldfieldioid genera. fieldioid genera (as usual, minus Pseudanthinae) Other oldfieldioidgenera similarly suffered early comprising a clade distinct from other biovulate taxonomic assignments that delayed consideration Euphorbiaceae. of relationshipswith the rest of the subfamily. Bail- In the disposition of genera, Hurusawa's (1954) lon (1858) submerged Klotzsch within classification of Euphorbiaceae essentially follows the phyllanthoidgenus Vahl, a disposition that of Pax & Hoffmann (1931) and thus contains followed well into this century. Oldfieldia Benth. no new insights on classification of oldfieldioidgen- & Hook. f. was temporarily considered sapinda- era. In light of Pax's (1925) phylogeny and because ceous (Mueller, 1866; Baillon, 1878). Worse, the of its disregard for the palynological data available relationships of Picrodendron were long obscured at the time (Punt, 1962; K6hler, 1965), Hutch- by a of misassignments at both the generic inson's (1969) classification was a retrograde de- and familial levels (Hayden et al., 1984). velopment; oldfieldioidgenera were widely distrib- Aside from Caletieae sensu stricto, the genera uted in five of 12 biovulate tribes, with three tribes of Oldfieldioideae were scattered widely in Muel- mixing oldfieldioid and phyllanthoid elements. ler's (1866) treatment of the family for the Prod- Hutchinson was the first, however, to associate romus; Mischodon Thwaites was included with Paradrypetes Kuhlm. with other oldfieldioid gen- uniovulate genera, following an earlier error of era. Baillon (1858), Oldfieldia was still banished to Airy Shaw (1965) entertained serious doubts , and the remaining five oldfieldioid about inclusion of several oldfieldioid genera in genera in his treatment were each assigned to dif- Euphorbiaceae. Accordingly, he proposed Andro- ferent subtribes of . Greater cohe- stachydaceae, of uncertain relationships,to accom- siveness is apparent in a later publication of Baillon modate Androstachys; he recognized Picroden- (1878). For example: Choriceras Baillon was in- draceae as distinct from but allied to Euphorbiaceae; cluded within Caletieae; Austrobuxus Miq. (as Bur- and he viewed Aristogeitonia, Calaenodendron aeavia Baill.), Longetia Baillon ex Muell. Arg., Standley, Mischodon, Oldfieldia, and Piranhea Petalostigma F. Muell., and Hyaenanche Lambert as occupying an intermediateposition between these formed a sequence; and Dissiliaria F. Muell. ex families (Airy Shaw, 1966, 1972, 1973). Airy Baill. followed Richeria (which included the old- Shaw (1983) continued to accept an isolated tax- fieldioidPodocalyx). (See Webster (1987) for com- onomic position for Stenolobeae (including Pseud- mentary on Baillon's peculiar "serial" system to anthinae), but he did, consistently, group the re- indicate relationships.) Additional elements were maining Australasian genera of Oldfieldioideae in gradually accreted to this loosely defined nucleus adjacent tribes in several of his informal or tentative of oldfieldioidgenera. Bentham (1880), in his treat- classification systems (e.g., Airy Shaw, 1975, ment of Euphorbiaceae in the Genera Plantarum, 1980b, 1983). 182 Annals of the Missouri Botanical Garden

WI ELAND IINAE

ANDRACHNINAE PS EUDOL ACH NOSTYLI DINAE

PETALOSTIGMATINAE ANTI DESM INAE Petalostigma

AMANOINAE DRYPETINAE DISCOCARPINAE HeywoodiaLingelsheimia Neoroepera Tetracoccus UAPACI NAE BISOHOFFIINAE PAIVAEUSINAE SAUROPODINAE/ Aristogeitonia Old fieldia Piranhea

PHYLLANTHINAE TOXICODENDRINAE Androstachys Hyaenanche

DISSILIA RIINAE GLOCHIDIINAE Dissiliaria Longetia (incl. Austrobuxus) Mischodon FIGURE 1. Relationships of subtribes of Phyllantheae, after Pax (1925). Right-hand clade is the earliest published phylogram of Oldfieldioideae.Generic composition of subtribes, where indicated, follows Pax & Hoffmann (1931); oldfieldioidtaxa are in bold italics. Other than Pseudantheae, Podocalyx (treated as a of Richeria [Anti- desminae]) is the only element of Oldfieldioideaeknown to Pax and not included in the phylogram.

DESCRIPTION, CIRCUMSCRIPTION,AND DISTRIBUTION of two to five carpels; styles are generally undi- Plants of Oldfieldioideaeare woody, ranging from vided; each locule houses a pair of pendulous anat- low depressed shrubs to tall trees. Latex is absent ropous ovules. are often carunculate and and vestiture consists of unicellular or uniseriate usually possess copious endosperm. Reports of n trichomes. Leaves are alternate, opposite, or whorled = 12 for Pseudanthus (Hassall, 1976), 2n = 48 *andmay be simple or palmately compound; petiolar for Picrodendron (Fritsch, 1972), n = 24 for and laminar glands are absent; may be Mischodon and Tetracoccus (Hans, 1973), and n present or absent. Leaves may be strongly reduced = 24, 2n = 48 for Mischodon (Sarkar & Datta, in xerophytic . Plants are typically dioe- 1980) collectively suggest a base number of x = cious. are apetalous, and most lack discs. 12 for the subfamily. range from three to many. Pollen is bi- The first comprehensive classification of Old- nucleate, with four to many brevicolporate to po- fieldioideae (Webster, 1975) included 21 genera, rorate apertures; the exine lacks a foot layer, bears but several changes in composition have occurred a discontinuous interstitium and thick perforate since then. Two newly discovered genera, Voata- tectum with prominent supratectal spines (Levin malo Capuron ex Bosser (1976) and Whyanbeelia & Simpson, 1994, this volume). Gynoecia consist Airy Shaw & B. Hyland (Airy Shaw, 1976), have Volume 81, Number 2 Hayden 183 1994 Euphorbiaceae Subfamily Oldfieldioideae

been referred to the subfamily. Two enigmatic gen- cations listed in Appendix 2 has been incorporated era, Croizatia Steyerm. (Webster et al., 1987) into the following account as appropriate. and Paradrypetes (Levin, 1992), have been as- signed to Oldfieldioideaefollowing discovery of di- ARCHITECTURE agnostic flowering material and, especially, after study of pollen from these plants. Kairothamnus For the most part, leaves are either simple or Airy Shaw (1980a) and Scagea McPherson (1985) palmately compound; however, interesting transi- have been segregated from Austrobuxus sensu lato, tional morphologies do exist. Leaves of Oldfieldia as has Canaca Guillaumin, if only tentatively are palmately compound, with 3-8 leaflets; those (Webster, 1994). In recent years Radcliffe-Smith of Celaenodendron, Picrodendron, and Piranhea has redefined generic limits for several Oldfieldioi- are trifoliolate; both palmately compound and sim- deae. He has included Paragelonium Leandriwith- ple leaves occur in Aristogeitonia; and leaves of in Aristogeitonia (Radcliffe-Smith, 1988), he seg- Parodiodendron Hunz. are unifolioate, as evi- regated Stachyandra R. -Sm. from Androstachys denced by the minute stipels at the apex of the petiole to accommodate several Madagascan species bear- (Hunziker, 1969) and by the frequent disarticu- ing compound leaves (Radcliffe-Smith, 1990), and lation of the lamina at the same point (Fig. 4). he expanded Pseudanthus to include Stachyste- Finally, leaves of Micrantheum, which occur in mon (Radcliffe-Smith, 1993). The number of gen- alternate groups of three (to five), have been in- era now stands at 27. (Solely because of the re- terpreted as the leaflets of a palmately compound cency of its reclassification, Stachystemon is herein leaf which, by loss of their common petiole, are treated as a distinct genus.) sessile on the stem (Baillon, 1858); alternatively, Genera of Oldfieldioideae are mostly mono- or this unique phyllotaxy has been attributed to foliate oligotypic. Austrobuxus, with perhaps 20 species, stipules (Griining, 1913; Webster & Miller, 1963). is the most speciose, followed by Pseudanthus (sev- For the most part, leaf margins are entire, the few en species) and Petalostigma (six species). The exceptional species being Austrobuxus cuneatus total number of species referable to the subfamily (Airy Shaw) Airy Shaw, A. swainii (de Beuzev. & is estimated at 86, approximately 1 percent of the C. T. White) Airy Shaw, Choriceras tricorne total number of species in Euphorbiaceae. (Benth.) Airy Shaw (Figs. 7, 8), Dissiliaria muel- Oldfieldioideaeis largely a southern hemisphere leri (Baill.) ex Benth., Paradrypetes ilicifolia group. Only three genera occur in areas not derived Kuhlm. (Levin, 1986), P. subintegrifolia G. Levin from the breakup of Gondwanaland;these are Ce- (Levin, 1992), Parry (only laenodendron, from western , Picroden- some leaves), and T. ilicifolius Coville & Gilman. dron, from and Greater Antilles, and Paradrypetes possesses irregularly spaced spinose Tetracoccus from Mexico and the southwest United teeth (Levin, 1986, 1992). Teeth of Tetracoccus States. Eight genera and 16 species occur in the ilicifolius are the largest in the subfamily: median New World, six genera and 16 species occur in veins of these teeth are derived from the looped and Madagascar, one monotypic genus oc- secondary veins; there are prominent brochidod- curs in southern India and Sri Lanka, and 13 romouslikeloops within the tooth itself; and median genera and 52 species are Australasian. No genus veins extend nearly to the apices, which in the of Oldfieldioideaehas a bicontinental distribution, specimens examined appear to possess apical caps, although Androstachys and Aristogeitonia occur at least in young leaves. Teeth of the remaining both in Madagascar and Africa. species are much smaller, consisting of a vein end- ing in a small protrusionof leaf tissue. Significantly, however, deciduous apical caps are also visible in MATERIALS Austrobuxus swainii and Choriceras tricorne (Figs. This report is based on first-hand examination 7, 8). Tooth morphology in Oldfieldioideae thus of 97 leaf and 87 wood specimens of 61 species conforms with the theoid type (Hickey & Wolfe, of Oldfieldioideae. Specimens examined are listed 1975). Excluding noninformative spinose teeth, in Appendix 1. The specimens available represent theoid teeth are the only type found in Phyllan- to some degree all genera of the subfamily except thoideae, specifically in the genera Drypetes Vahl, Croizatia and Paradrypetes; it should be noted Putranjiva Wall., and Bischofia; reduced theoid that leaves of Voatamalo and wood of Kairotham- teeth are also present in Aporuseae (Levin, 1986). nus, Scagea, and Stachystemon are lacking in this Venation is always pinnate, most frequently fes- study. Previous anatomical literature concerning tooned brochidodromous (Figs. 2, 3). In addition genera of Oldfieldioideae provided by the publi- to brochidodromy, however, leaves of Longetia 184 Annals of the Missouri Botanical Garden

Si n~~~S

MMW AW EW S NEW

!v x~~~~~~~~~~~~5

FIGURES2-8. Leafarchitectural features ofOldfieldioideae. 2. Austrobuxus rubiginosus (Baumann-Bodenheim 15010),cleared leaf, bar = 1 cm.-3. Celaenodendronmexicanum (Ortega 6367), clearedleaf, bar = 1 cm.- 4. Parodiodendronmarginivillosum (Hueek 469), clearedleaf, note disarticulation of petiole from base of lamina, bar= 5 mm.-5. Picrodendronbaccatum (Gillis 6963), notelack of veinorders beyond tertiaries, bar = 2.5 Volume 81, Number 2 Hayden 185 1994 Euphorbiaceae Subfamily Oldfieldioideae

exhibit a tendency toward eucamptodromy whereas Picrodendron (Fig. 5), and Piranhea (all New those of Dissiliaria, Petalostigma, Picrodendron, World genera with trifoliolate leaves) plus An- and Tetracoccus tend toward reticulodromy. Leaves drostachys; this character state is extremely rare of the Australian genera of Pseudanthinae (Cale- in the dicots as a whole (L. J. Hickey, pers. comm.) tieae sensu stricto) exhibit a continuum of increas- and is thus a potentially robust synapomorphy link- ing disorganization, presumably a consequence of ing these genera. Areoles are well developed in the xeromorphy: in Neoreopera leaves are weakly fes- genera with compound leaves (Figs. 5, 12) plus tooned brochidrodromous; in Micrantheum one can Dissiliaria, Mischodon, Parodiodendron (Fig. 6), find vestiges of brochidodromous venation as well and Podocalyx; otherwise, areoles are imperfectly as secondary veins that recurve and ramify or form developed. Areoles are usually arranged randomly, a weak reticulum; in Stachystemon the range is but are oriented in Celaenodendron and somewhat from reticulodromous to kladodromous; and in oriented in Picrodendron, Piranhea, and Dissilia- Pseudanthus leaves are all kladodromous (Fig. 9). ria. Veinlets are usually present and mostly simple Primary veins are mostly of moderate size, but, or branched; the degree of branching varies widely, especially in xeromorphic leaves, they may range tending to be most highly branched in leaves with to stout and massive, e.g., those of Hyaenanche, low regularity of tertiary and higher order veins. Tetracoccus, and the Australian Pseudanthinae (Fig. Veinlets are absent in Androstachys (Fig. 12), but 9). Intersecondary veins are usually absent, al- they may appear to be present upon superficial though one or two simple intersecondaries per in- examination because of the columnar sclereids lo- tercostal area occur occasionally in Austrobuxus cated in each areole (see below). and Mischodon, and routinely in Croizatia (Levin, 1986), Oldfieldia, Paradrypetes (Levin, 1986), LEAF ANATOMY Piranhea, and Podocalyx. Intersecondary veins are frequent in several primitive Phyllanthoideae, Trichomes have been observed in about two- namely, Aubl., Blotia Leandri, Hey- thirds of the genera of Oldfieldioideae. Many spe- woodia Sim, Petalodiscus Baill., Willd., and cies are glabrescent with age, although mature Baill. (Levin, 1986); their presence is leaves of Androstachys, Parodiodendron, and thus postulated to be primitive for Oldfieldioideae. species of Petalostigma, for example, are clearly Tertiary vein patterns are usually random reticu- pubescent. Trichomes are either simple unicellular late; ramified patterns occur in Hyaenanche, spe- or uniseriate, generally consisting of less than six cies of Austrobuxus, and those species of Austra- cells. Within Pseudanthinae, epidermal emer- lian Pseudanthinae that possess distinguishable gences range from small papillae to four-celled tertiaries; there is a slight tendency toward trans- uniseriate trichomes. The densely packed tri- verse tertiaries in Parodiodendron, Paradrypetes chomes of Androstachys johnsonii Prain, which (Levin, 1986), Petalostigma, and Podocalyx; and consist of a short cell and long curly terminal the tertiary veins of Piranhea have a slight ten- cell, have been suggested by Alvin (1987) to func- dency to form orthogonal patterns. Marginal ve- tion in absorption of atmospheric moisture (mists nation is incomplete (Fig. I 1) or looped (Fig. 6) in and drizzles) in the otherwise extremely arid en- many genera, "hemmed" with a fimbrial vein in vironment of southern Africa. Oldfieldia possesses the genera with compound leaves (Figs. 10, 12) trichomes similar to those of Androstachys, ar- plus Dissiliaria and Mischodon, or dominated by guing for some degree of relationshipbetween these a massive intramarginal vein in most Australian two genera despite their manifest differences in Pseudanthinae (Fig. 9). A distinctive furcate-fla- reproductive morphology. Depending on the spe- bellate form of marginal venation occurs in Hyae- cies, trichomes of Austrobuxus are either simple nanche. or bifurcate (malpighiaceous). Parodiodendron is High-order venation varies considerably within unique within the subfamily in possessing strongly Oldfieldioideae. Perhaps most notable is the oc- ciliate leaf margins (Fig. 6). Rao & Raju (1985) currence of ultimate reticula in which vein order reported uniseriate, stellate, and glandular hairs in is not distinguishable, a feature of Celaenodendron, Dissiliaria, characteristics reminiscent of uniovu-

mm.-6. Parodiodendron marginivillosum (Hueck 469), margin of cleared leaf, bar = 250 ,um.-7. Choriceras tricorne (Forman s.n.), tooth at margin of cleared leaf, bar = 250 ,um.-8. Choriceras tricorne (Forman s.n.), paradermal through tooth at leaf margin, note glandular apex, bar = 100 ,um. 186 Annals of the Missouri Botanical Garden

K~~~~~~~~~~~~~~~~~~~~~~~~~

$k17

FIGURES 9-12. Leaf architecture of Oldfieldioideae.-9. Pseudanthus orientalis (Clemens 44092), kladodromous venation, massive primary and intramarginal veins, bar = 250 gm.-10. Celaenodendron mexicanum (Ortega 6367), fimbrial vein (far right), bar = 250 ,um.-11. Petalostigma banksii (Perry 1981), branched veinlets with swollen ultimate tracheids, bar = 100 m. -12. Androstachys johnsonii (Wellcome Chemical Research Laboratory s.n.), well-developed areoles with columnar sclereids, veinlets absent, bar = 1 mm.

late euphorbs that would be unique to Oldfieldioide- cell or chamber thus formed contains mucilage, ae; however, neither trichomes nor their bases were which is common in other genera as well. Expansion detected in the leaves available to me. of the mucilaginous layer in Australian Pseudan- The epidermis is fundamentally uniseriate. How- thinae greatly distends the adaxial epidermis (Figs. ever, a single layer of hypodermis has been re- 18, 19); while the grossly expanded mucilaginous ported for Paradrypetes (Milanez, 1935) and some layer may well be an artifact of preparation, it is or all epidermal cells of the Australasian genera derived solely from the lower portions of subdivided have a horizontal partition resulting in a poorly to epidermal cells and is not thickly multicellular as well-defined hypodermis (Figs. 17-19). The inner depicted by Gaucher (1902), whose erroneous in- Volume81, Number2 Hayden 187 1994 EuphorbiaceaeSubfamily Oldfieldioideae

TB *;i.~~~~~~~~~~0 W T4P

FIGURES13-16. Leaf anatomyof Oldfieldioideae.-13. Longetia buxoides(Baumann-Bodenheim 5605), sto- mate from cross section, bar = 20 sum.-14. Scagea oligostemon(McKee 2352), surfaceview of stomatefrom paradermalsection, note crenulateinner anticlinal walls of subsidiarycells visiblethrough stomatal aperture, bar = 10 Mm.-15. Austrobuxushuerlimannii (McKee 4850), subdividedcrenulate subsidiary cells and trichomebases from paradermalsection, bar = 20 Mum.-16. Podocalyx loranthoides(Krukoff 811), tracheoididioblasts from maceratedmesophyll, bar = 20 ,um.GC = guardcell, SC = subsidiarycell, TB = trichomebase. terpretation has been reiterated by others (e.g., lem, L., Richeria, and Savia (Met- Metcalfe & Chalk, 1950; Raju & Rao, 1977). So calfe & Chalk, 1950). In surface view, anticlinal far, no mucilage has been detected in Aristogei- walls of epidermal cells are generally straight (Figs. tonia, Celaenodendron, Mischodon, Piranhea, and 14, 15), the only exceptions being Aristogeitonia, Podocalyx. Mucilaginous epidermis is known in Celaenodendron, Piranhea, (all members of Pi- several Phyllanthoideae, for example, crodendreae), and Dissiliaria, in which these walls Bl., L., Aporusa Bl., Amanoa, Bac- have a wavy outline; intriguingly, paradermal sec- caurea Lour., Willd., Hyeronima Fr. Al- tions of Aristogeitonia and Celaenodendron reveal 188 Annals of the Missouri Botanical Garden

PF _M) PF - (M)

FIGURES 17-21. Leaf anatomyand woodparenchyma of Oldfieldioideae.-17. Longetia buxoides(Baumann- Bodenheim5605), leaf crosssection, note chambered mucilaginous epidermal cells, bar = 100 Aum.-18. Pseudanthus orientalis (Wilson 679), leaf cross section, note grosslyexpanded mucilaginous hypodermis and prominentintra- marginalveins, bar = 100 um.- 19. Micrantheumhexandrum (McGillivray 3196), cross sectionof primaryvein, note grosslyexpanded mucilaginous hypodermis, bar = 100 um.-20. Hyaenancheglobosa (GodfreySH 1257), cross sectionof leaf, bar = 100 ,um.-21. (Ducke s.n., USw 31485), normaland chambered crystalliferousaxial xylem parenchymacells, bar = 15 Am.PF = phloemfibers. Volume 81, Number 2 Hayden 189 1994 Euphorbiaceae Subfamily Oldfieldioideae

the inner portions of epidermal cells to possess trast to most genera, subsidiary and guard cells straight anticlinal walls. are coplanar in Oldfieldia and Parodiodendron. Leaves are overwhelmingly hypostomatic, al- Mesophyll is bilateral except in some species of though both hypo- and amphistomatic conditions Petalostigma with isobilateral leaves; leaves of occur in species of Petalostigma and Tetracoccus. Hyaenanche approachan isobilateralcondition (Fig. Stomatal type is anomocytic in Podocalyx, para- 20). Spongy mesophyll with well-developed inter- cytic in Paradrypetes (Levin, 1986), but otherwise cellular spaces but a tendency toward vertical align- brachyparacytic (Fig. 14) or derived from a ment of cells occurs in Androstachys, Oldfieldia, brachyparacytic pattern. For example, intruding Picrodendron, and Piranhea, all members of Pi- lobes of adjacent cells tend to form an anomocytic crodendreae. Mesophyll usually contains scattered pattern in Tetracoccus as viewed from the surface; druses; prismatic crystals are also present in Ar- paradermal sections, however, reveal typical istogeitonia, Austrobuxus, Dissiliaria, Hyaenan- brachyparacytic configurations. The most frequent che, Longetia, and Micrantheum. Mesophyll of modification of stomatal type is the tendency for Paradrypetes contains raphide bundles (Milanez, one or both of the subsidiary cells to become sub- 1935; Levin, 1986), a structure otherwise un- divided into two or three smaller cells; subdivision known in Euphorbiaceae(Gaucher, 1902; Metcalfe of subsidiary cells may be a consistent feature in & Chalk, 1950). No crystals were observed in the a given taxon, or it may be sporadic, affecting only mesophyll of Celaenodendron, Parodiodendron, some stomata or only one subsidiary cell of a given and Piranhea. Except for Androstachys and pair. Subdivided brachyparacytic stomata occur in Stachyandra, foliar sclereids are absent; areoles Androstachys, where the pattern has been de- of these genera usually contain a single columnar scribed as incompletely cyclocytic (Alvin, 1987), sclereid with ramified tips that run parallel with Aristogeitonia, some species of Austrobuxus (Fig. the bases of epidermal cells and eventually inter- 15), Hyaenanche, Mischodon, Picrodendron, and mingle with bases and the bundle sheath Pseudanthus. The paracytic stomata of Paradry- extensions of the veins. Alvin (1987) has inter- petes are also subdividedin a similar fashion (Levin, preted the sclereids of Androstachys to function 1986). The distribution of subdivided subsidiary in apoplastic transport from its water-absorbant cells does not follow any obvious taxonomic group- trichomes. It is intriguing to speculate that the ing within the subfamily. Within Phyllanthoideae, vertically oriented spongy mesophyll cells of An- brachyparacytic stomata are characteristic of Bri- drostachys may have served as a preadaptation delieae, Drypeteae, Phyllantheae-Fleuggeinae, and for the evolution of its columnar sclereids. Another certain genera of Wielandieae; moreover, subdi- unique mesophyll feature is found in Podocalyx, vided brachyparacytic stomata occur in Lachnos- which bears unbranched, sinuous tracheoid idio- tylis Turcz. and Bridelia (Levin, 1986). Raju & blasts with spirallythickened, nonlignifiedwalls (Fig. Rao (1977) reported brachyparacytic stomata to 16). These elements, occurring most frequently be the most common type among woody genera between the junction of palisade and spongy layers, throughout Euphorbiaceae. are sufficiently abundant to obscure the presence In most genera subsidiary cells extend partially of veinlets in clearings; they are not, however, over the inner periclinal walls of adjacent guard directly connected to any vasculature. cells in a "semi-piggyback" fashion (Fig. 13); the Vasculature of the primary vein consists of ad- inner anticlinal walls of subsidiary cells thus delimit jacent (colateral) regions of xylem, phloem, and an inward extension of the stomatal pore. Within phloem fibers. Little taxonomic significance can be Phyllanthoideae, Levin (1986) noted a similar spa- read into the overall configuration of primary vein tial relationship of guard and subsidiary cells only vasculature, which ranges from broad shallow arcs in Drypetes. The inner anticlinal walls of "pig- to more tightly curved u-shaped arcs to closed gyback" subsidiary cells may have crenulate out- loops; reduced leaves of desert xerophytes, how- lines (Figs. 14, 15), a feature first observed by ever, tend to have patterns with minimal curvature Solereder (1908) in Micrantheum and Pseudan- (Figs. 18, 19). Phloem fibers of the primary vein thus that now proves characteristic of the Aus- in Petalostigma and the Australian Pseudanthinae tralasian genera (Mischodon and certain species are unlignified (Figs. 18, 19), in sharp contrast to of Austrobuxus excluded) plus the South African the usual lignified condition of these cells in the genus Hyaenanche; this feature defines a distinct rest of the subfamily. Smaller veins are frequently clade within the subfamily. Crenulate subsidiary associated with a parenchymatous bundle sheath cells are only weakly developed in the single spec- (Fig. 17). Bundle sheath extensions that are merely imen of T;hyanbeelia available for study. In con- parenchymatous occur in Longetia (Fig. 17); crys- 190 Annals of the Missouri Botanical Garden

tals are present in bundle sheath extensions of to reticulate). Tyloses and/or are common Aristogeitonia, Celaenodendron, Hyaenanche, in lumina of heartwood vessels; silica deposits occur Mischodon, Oldfieldia, Parodiodendron, Peta- in lumina of Whyanbeelia. lostigma, Picrodendron, and Piranhea; and at Imperforate tracheary elements bear either sim- least some fibrouselements are also present in those ple or bordered pits. Elements with simple pits, i.e., of Androstachys, Mischodon, and Piranhea. libriformwood fibers, characterize the genera with Overall, bundle sheath extensions seem best de- compound leaves (Aristogeitonia, Celaenoden- veloped in the genera bearing compound leaves, dron, Oldfieldia, Piranhea, and Picrodendron) but also occur sporadically elsewhere in the sub- plus Dissiliaria, Hyaenanche, and Petalostigma; family. Swollen terminal tracheids of veinlets occur some of these may also possess elements with bor- in some Austrobuxus, Choriceras, Hyaenanche, dered pits. The remaining genera possess only el- Longetia, Petalostigma (Fig. 11), and Tetracoc- ements with bordered pits; these cells are probably cus. best characterized as fiber-tracheids by virtue of their relatively small pit borders and thick walls. However, because intervascular pits in some old- WOOD ANATOMY fieldioidsare remarkably small, Androstachys, Ar- Growth rings are often absent or only faintly istogeitonia, and the Australian genera of Pseud- visible. Growth rings are present, however, in An- anthinae, for example, pits of imperforate elements drostachys, Celaenodendron (Fig. 23), Parodio- may be approximately equal to or slightly larger dendron, Petalostigma, Podocalyx, Tetracoccus, than intervascular pits in the same wood; by the and Australian Pseudanthinae (Fig. 24); except for criteria of Bailey (1936) such elements would be Podocalyx, from the upper Amazon and Orinoco tracheids, by definition, despite their thick walls drainage basins, these are plants of dry habitats and pit diameters of 5 gim or less. "Tracheid," with strongly seasonal availability of moisture. Pores with its connotation of primitive conducting ele- are evenly distributed (i.e., diffuse porous in species ment, hardly seems appropriate for such cells. On with growth rings), except in the ring porous wood the other hand, the tracheids of Podocalyx, with of Tetracoccus, which extends into desert regions pit diameters up to 13 tm, attest more convincingly of western North America. Pore outlines are mostly to primitive structure, and both fiber-tracheidsand circular, generally small, and usually less than 100 tracheids are present in Austrobuxus, distinguish- Atm diam.; pore diameters are often less than 50 able by both wall thickness (Fig. 22) and pit size. Atm in the genera mentioned above from dry hab- Bands of gelatinous fibers occur in woods of Aus- itats. Perforation plates are overwhelmingly simple, tralian Pseudanthinae (Fig. 24), Hyaenanche, and but scalariform plates are found in Paradrypetes Tetracoccus. Imperforate elements often possess (exclusively so according to Mennega (1987), mixed such thick cell walls that lumina appear completely with simple perforations according to Araujo & closed; Bamber(1974) noted that these thick-walled Mattos Filho (1984)) and mixed simple, scalariform fibers lack an easily detectable S3 layer in Aus- (Fig. 30), and reticulate plates characterize Podo- trobuxus, Dissiliaria, and Petalostigma. Fibers calyx. Intervascular pits are transitional in Par- are septate only in Parodiodendron. adrypetes and Podocalyx; otherwise they are al- Rays are numerous, generally more than 15 per ternate and mostly small, ca. 5 Aim or less. Very mm; however, there are more than 20 per mm in small intervascular pits (2-3 ,um) are found in Australian Pseudanthinae, and only 12 per mm in Aristogeitonia, Neoroepera, and Pseudanthus; Androstachys and Oldfieldia. High ray frequen- somewhat larger than usual pits (6-8 ,um) occur cies are probably related to the general narrowness in Austrobuxus, Celaenodendron, Parodioden- of individual rays. Rays are mostly 1-, 2-, or dron, Picrodendron, Piranhea, and Podocalyx. 3-seriate, but up to 4- or 5-seriate rays occur in Vessel element lengths for most genera fall within Choriceras, Dissiliaria, Aristogeitonia, and Tet- the range of 400-700 ,um; vessel elements are racoccus (Fig. 33). Polymerous (vertically fused) somewhat shorter in Picrodendron (ca. 300 Aim), rays are usually common (Fig. 32); however, they somewhat longer in Dissiliaria (ca. 800 gim), Aus- are infrequent or absent in Androstachys (Fig. 31), trobuxus (ca. 950 ,im), and Paradrypetes (ca. Choriceras, Parodiodendron, Tetracoccus, and the 1200 ,im), and longest in Podocalyx (ca. 1250 Australian Pseudanthinae. Aggregate rays were ob- ,im). Sculpture on the inner surface of vessels is served in Choriceras only. Rays are usually het- rare; some vessels of Choriceras possess spiral erocellular (Figs. 28, 29), which is generally con- thickenings; thickenings are characteristic of sidered the primitive condition. Homocellular Whyanbeelia (spiral only) and Tetracoccus (spiral procumbent rays are shared by Androstachys and Volume 81, Number 2 Hayden 191 1994 Euphorbiaceae Subfamily Oldfieldioideae

AMAMI

FIGURES22-27. Wood anatomy of Oldfieldioideae.-22. Austrobuxus swainii (deBeuzeville s.n., MADw 10449), note thin- and thick-walled fibers.-23. Celaenodendron mexicanum (Ortega 35, USw 3886), note long radial multiples of pores and boundariesof growth ring (top and bottom). -24. ( Whaite & Whaite 3536), note bands of gelatinous fibers.-25. Piranhea trifoliata (Ducke s.n., USw 31485), note banded distribution of axial xylem parenchyma.-26. Androstachys johnsonii (Pretoria UIND 2127, Uw 21991).-27. Oldfieldia africana (Cooper 88, USw 4517). All bars = 100 Am. 192 Annals of the Missouri Botanical Garden

TABLE 1. Wood structure of biovulate euphorbs, after Metcalfe & Chalk (1950).

Feature Aporusa-type "Other genera" -type Perforations scalariform, simple, or both simple simple Fibers nonseptate, thick-walled nonseptate, thick-walled septate, thin to moderately thick-walled Parenchyma abundant, diffuse or nar- abundant, diffuse to wide absent or scanty row bands bands some species of Oldfieldia, which serves to dem- Axial xylem parenchyma is mostly diffuse and onstrate that these woods are not as dramatically diffuse-in-aggregates (Fig. 27), with bands also distinct as Metcalfe & Chalk (1950) suggested. present in Aristogeitonia, Dissiliaria, Parodio- Homocellular square to erect rays are one of sev- dendron (strictly initial bands), Picrodendron, Pi- eral synapomorphiesthat mark the Australian gen- ranhea (Fig. 25), and Voatamalo; on the other era of Pseudanthinae as a distinct monophyletic hand, parenchyma is infrequent and restricted to group. Vessel to ray pits are of two forms that a few abaxial scanty paratracheal cells in Andro- appear to hold great systematic significance. The stachys, Stachyandra, and the Australian genera most distinctive pattern consists of highly irregular of Pseudanthinae (Fig. 24). Parenchyma strands pits that range from circular to elongate with the usually contain both ordinary cells and short scler- elongate pits at various orientations: vertical, hor- ified cells bearing a single prismatic crystal (Fig. izontal, or diagonal (Fig. 28). This irregularpattern 21); crystalliferous parenchyma is absent, how- is interpreted as primitive by virtue of its resem- ever, in Paradrypetes, Podocalyx, Petalostigma, blance to primitive transitional intervascular pit- Whyanbeelia, the Australian genera of Pseudan- ting, and by its occurrence in Paradrypetes and thinae, and most specimens of Tetracoccus. Since Podocalyx (see below); irregular vessel-ray pits sclerified crystalliferous axial xylem parenchyma have been retained by all arborescent Australasian cells are common in several phyllanthoid woods genera. All other genera possess uniform vessel- (e.g., Amanoa and Drypetes), presence of such ray pits that are circular and alternate. If circular, cells may be considered primitive for Oldfieldioi- alternate vessel-ray pits are indeed the derived deae; their loss may well be synapomorphous for character state, this feature evolved twice, since Petalostigma,f Whyanbeelia, and the Australian the Australian Pseudanthinae (i.e., Caletieae sensu genera of Pseudanthinae; loss in others (e.g., Par- stricto) are clearly derived from the lineage bearing adrypetes, Podocalyx, and most specimens of Tet- the arborescent genera of Australasia (see below), racoccus) may represent convergent develop- rather than the lineage of African and American ments. genera. Ray cells generally bear only tannins, but several exceptions occur: prismatic crystals are ORIGIN OF OLDFIELDIOIDEAE sporadic in Podocalyx, abundant in Paradrypetes EVIDENCE FROM WOOD ANATOMY (Araujo & Mattos Filho, 1984); silica deposits are common in Petalostigma; and sclerified cells bear- The analysis of wood structure of biovulate eu- ing a prismatic crystal are abundant in Aristogei- phorbs contained in Metcalfe & Chalk (1950) pro- tonia, Mischodon, and Tetracoccus fasciculatus; vides a convenient starting point for discussion of these crystalliferous cells are only rarely present relationships between Phyllanthoideae and Oldfield- in Voatamalo. Perforated ray cells are sporadic in ioideae. In this work, three groups of genera were Paradrypetes (Milanez, 1935), Podocalyx, and distinguished, as indicated in Table 1. At the most Hyaenanche, but have not been observed in other superficial of levels, woods of Oldfieldioideae, large- Oldfieldioideae.Perforated ray cells are fairly wide- ly included in Metcalfe & Chalk's "other genera," spread in Euphorbiaceae according to Giraud may be characterized as a combination of the vessel (1983), who recorded this feature in the following features of Glochidion-type woods and the fiber phyllanthoid genera: Aporusa, , Bri- and parenchyma features of Aporusa-type woods, delia, Hook. f. ex Planch., Drypetes, the latter two categories consisting primarily of Hyeronima, and Richeria. Perforated ray cells phyllanthoid genera. In some instances these three are also present in Putranjiva (Nazma et al., 1981) coarsely defined categories provide a useful per- and Amanoa (unpublished obs.). spective for placing genera; for example, the re- Volume 81, Number 2 Hayden 193 1994 Euphorbiaceae Subfamily Oldfieldioideae

moval of Neowawraea Rock, which has Glochidi- Aporusa-type structure, an ecologically restrictive on-type wood, from Drypetes, which has Aporusa- syndrome of xylem features. type wood, and its subsequent submergence into Within Phyllanthoideae, Aporusa- and Glochid- Willd., which also has Glochidion-type ion-type structure represent evolutionary ex- wood (Hayden & Brandt, 1984; Hayden, 1987). tremes, but numerous transitional forms can be However, as wood structure of biovulate eu- identified from Mennega's (1987) data. For ex- phorbs has become better known, genera with wood ample, tracking both perforation plates and de- that is transitional between the three categories velopment of septate fibers yields the following cloud what once appeared to be a clear picture. series of forms that may be viewed as intermediates For example, Mennega (1984) found tribal place- between Aporusa- and Glochidion-type structure: ment of Webster difficult, essentially Actephila, Urb., and Pentabrachi- because the wood of Jablonskia has an unusual um Muell. Arg. with exclusively scalariform per- combination of characters: specifically, vessel fea- forations and some septate fibers; Celianella Jabl., tures of Aporusa-type woods and fiber and paren- Didymocystis Kuhlm., and Jablonskia with mixed chyma features of Glochidion-type woods. In short, simple and scalariform perforations and some sep- Jablonskia represents the reverse of the combi- tate fibers; Rob. & Greenm. and Dis- nation that characterizes most oldfieldioids. Men- cocarpus Klotzsch with simple perforations, but nega (1987) has noted additional transitional gen- only some septate fibers. Similarly, within Apo- era in her extensive survey of wood structure in rusa-type woods, there is a clear transition of per- Phyllanthoideae; moreover, woods of some phyl- foration plates from exclusively scalariformin Apo- lanthoids, e.g., Turcz. and Savia, rusa, Heywoodia, Hyeronima, match the typical oldfieldioid pattern described Benth., and Putranjiva, to mixed simple and sca- above. Further, within Oldfieldioideae,Podocalyx lariform in numerous genera and, finally, to exclu- and Paradrypetes possess essentially typical ex- sively simple in Lachnostylis and Savia. Of course, pressions of Aporusa-type structure. Clearly, the such sequences of extant genera should not be simple rubric of three wood types for biovulate interpreted as the actual course of xylem evolution euphorbs requires modification. within Phyllanthoideae. An evolutionary perspective of anatomical char- In terms of the gross vessel, fiber, and paren- acters helps to clarify some of the complexity seen chyma features of Table 1, the evolutionary trans- in woods of biovulate euphorbs. In accord with formation of wood in Oldfieldioideaeseems parallel widely accepted hypotheses of wood evolution, to that noted for Aporusa-type woods. In com- Mennega (1987) has identified woods with long parison, Phyllanthoideae experienced a greater vessel elements, long scalariformperforation plates, range of wood diversification with the additional medium to large intervascularpits, long thick-walled development of Glochidion-type woods. nonseptate fibers with bordered pits on both radial Within Oldfieldioideae, Podocalyx and Para- and tangential walls, and diffuse or narrowly band- drypetes stand out as probably the most primitive ed axial xylem parenchyma to be primitive within woods by virtue of their very long vessel elements, Phyllanthoideae. Extant genera such as Aporusa, multiple perforation plates, and large transitional Blotia, and Hutch. retain these intervascular pits; presence of perforated ray cells features. Carlquist(1975) has argued convincingly in these genera may also be interpreted as primitive that primitive vessel features are adaptive only in features. Overall, their woods are comparable to uniformly moist forest environments that impose primitive phyllanthoid woods with Aporusa-type minimal demands for water conduction. It may be structure. The primitive woods of Paradrypetes assumed that adaptive radiation of primitive biovu- and Podocalyx excepted, Oldfieldioideaegenerally late euphorbs into drier, or seasonally drier, hab- have exclusively simple perforation plates and have itats would be accompanied by evolution of more lost perforated ray cells, but otherwise retain the advanced vessel features. Similarly, one may rea- features of Aporusa-type structure (cf. comments sonably suppose exploitation of nonforest and/or on Lachnostylis and Savia, above). Much of the seasonal habitats to be associated with modification diversity of oldfieldioid woods is restricted largely of mechanical and storage requirementsof the wood; to what are, perhaps, minor themes such as element such changes would be manifest in both fiber and size (Figs. 22-27), vessel grouping (Figs. 22-27), parenchyma features. Much of the diversity of ray dimensions (Figs. 31-33), vessel-ray pitting, biovulate euphorb wood structure may thus be in- and parenchyma distribution(Figs. 22-27). These terpreted in terms of divergence from primitive minor themes, however, are responsible for con- 194 Annals of the MissouriBotanical Garden

p ~ ~ ~ ~~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~~~~~~~~~~~adS~~~~~~~~~~~~~

FIGURES28-33. Wood anatomyof Oldfieldioideae.-28.Austrobuxus swain~ii(Symington s.n., Uw 2141 1), radial section, heterocellular ray and irregular slitlike vessel-ray pits. -29. Petalostigma sp. (SFCw R594-2), radial section, heterocellular rays and simple perforation plates.-30. Podocalyx loranthoides (Wurdack & Adderley 42 795, MADw 2242 9), radial section, scalariform perforation plate. - 31. Androstachys johnsonii (Pretoria UIND 2127, Uw 21991), tangential section, short and narrow rays.-32. Celaenodendron mexicanum (Ortega 35, USw 3886), tangential section. -33. Tetracoccus fasciculatus var. fasciculatus (Johnston 7783), tangential section, wide rays. All bars = 100 ,um. Volume 81, Number 2 Hayden 195 1994 Euphorbiaceae Subfamily Oldfieldioideae

siderable diversity of oldfieldioid woods; based on Phyllanthoideae and Oldfieldioideaeprecludes any wood features alone, it is entirely understandable simple statement about the point of divergence of that Metcalfe & Chalk (1950) sought to associate the two subfamilies. Both characater states of three oldfieldioidgenera with woods from other subfam- important characters (paracytic-brachyparacytic, ilies. entire-subdivided subsidiary cells, and coplanar- The presence of somewhat primitive woods (Par- "piggyback" subsidiary cells) are found in both adrypetes and Podocalyx) in Oldfieldioideaesug- groups. This situation may be viewed as an example gests that the divergence of Oldfieldioideae from of Cronquist's (1988) assertion that parallel ten- Phyllanthoideae occurred quite early in the evo- dencies are reasonably good indicators of relation- lution of Euphorbiaceae, from ancestral stocks with ships; a rigorous cladistic analysis of Phyllanthoi- relatively primitive Aporusa-type woods. The sym- deae and Oldfieldioideae should distinguish the plesiomorphousnature of wood features at the evo- synapomorphic stomatal characters from the par- lutionary transition between the subfamilies pre- allelisms. cludes the possibility of specifying one or another phyllanthoid group as closest to the origin of Old- ADDITIONALEVIDENCE fieldioideae based on this tissue alone. A number of anatomical characters such as the Septate fibers, common in phyllanthoids with occurrence of theoid teeth, intersecondary veins, Glochidion-type structure, occur in only one old- and mucilaginous epidermis in Oldfieldioideaeand fieldioid, Parodiodendron. One prominent differ- primitive Phyllanthoideae are consistent with the ence, however, between this wood and the Glo- former's derivation from the latter. Floral structure chidion-type phyllanthoids is its fairly abundant of Wielandieae is sufficiently generalized to be con- parenchyma present in initial bands, diffuse apo- sistent with ancestral status. However, plesiomor- tracheal and scanty paratracheal configurations. phous characters such as these do not present by Typical expressions of Glochidion-type structure themselves an overly compelling case for consan- include very little parenchyma at all. The occur- rence of septate fibers in Parodiodendron may guinity. On the other hand, the often reduced carpel thus represent convergence. number and drupaceous of Drypetes show greater (or, at least, different) specialization than EVIDENCE FROM STOMATALSTRUCTURE that found in many Oldfieldioideae.Further, chro- mosome numbers of n = 20 for Putranjiva (Gill Configuration of the stomatal apparatus is one et al., 1981) and 2n = 40 for Drypetes (Webster, of the most consistent features of leaves of Old- 1967) are difficult to resolve with the counts sug- fieldioideae. Most genera possess brachyparacytic gesting x = 12 for Oldfieldioideae (see above). patterns in which the subsidiary cells substantially Extant Drypeteae are thus unsuitable as progeni- overlie the adjacent guard cells. In this regard, tors for Oldfieldioideae,but it remains conceivable Levin (1986), upon whose data much of the fol- that these taxa may have shared a common an- lowing is based, has shown stomatal patterns of the cestor. phyllanthoid tribes to be fairly diverse; in fact, this Levin & Simpson (1988) noted that the spinules character provides important evidence in identi- and discontinuous exine foot layer in pollen of fying which phyllanthoids are closest to the origin Comm. ex Juss. sensu stricto suggested of Oldfieldioideae.As argued above, it will be nec- a close relationship with Oldfieldioideae. Despite essary only to consider tribes with Aporusa-type exclusively simple perforation plates, the wood of wood structure. Aporuseae may be eliminated from Securinega conforms well to the Aporusa-type further consideration by its consistently anisocytic (and thus may be out of place in Phyllantheae, stomata, a pattern never found in Oldfieldioideae. as pointed out by Mennega (1987)). Securinega Paracytic or brachyparacytic stomata are found in also possesses paracytic stomata (Gaucher, 1902). the remaining tribes under consideration, i.e., Further anatomical data would be most useful. In Amanoeae, , Drypeteae, and Wieland- our present state of ignorance, Securinega stands ieae, with brachyparacytic in only Drypeteae and as another possible near relative to Oldfieldioideae. some Wielandieae. Subsidiary cells in Drypetes, like those of most Oldfieldioideae,partially overlie SUMMARY the adjacent guard cells. The brachyparacytic sub- sidiary cells of Lachnostylis (tribe Wielandieae) Taken together, stomatal and wood characters are frequently subdivided (Levin, 1986), another suggest that Oldfieldioideaediverged from the early common character in Oldfieldioideae. Unfortu- differentiationof the primitive biovulate tribe Wie- nately, the distribution of stomatal characters in landieae perhaps along some of the same lines that 196 Annals of the Missouri Botanical Garden

ultimately led to the modern genera Drypetes and/ Tribe Picrodendreae (Small) Webster. The gen- or Securinega. In a larger context, presence of era with palmately compound leaves form the con- theoid teeth and palmately compound leaves in ceptual nucleus of tribe Picrodendreae. Bentham Oldfieldioideaelends support to Dilleniidrather than (1878) was the first to group together the biovulate Rosid derivation of Euphorbiaceae (cf. discussion euphorbs with compound leaves, associating Old- in Levin (1986)). fieldia and Piranhea with the non-oldfieldioidge- nus Bischofia. Later, Aristogeitonia (Prain, 1912; Pax & Hoffmann, 1922, 1931) and Celaenoden- RELATIONSHIPS WITHIN OLDFIELDIOIDEAE dron (Hutchinson, 1969) were added to this group, Classification of subfamily Oldfieldioideae has which (minus Bischofia) constituted subtribe Pai- been in a state of flux over the past three decades. vaeusinae of Webster (1975). (Presence of non- The following discussion focuses on anatomical data spiny pollen (K6hler, 1965) and Glochidion-type as indicators of relationships within Oldfieldioideae, wood structure (Mennega, 1987) shows Bischofia specifically, the role of anatomy in modification of to be better placed in Phyllanthoideae.) Webster early classifications of Oldfieldioideae (Khler, (1975) maintained Picrodendron in a monogeneric 1965; Webster, 1975) and the extent that anat- tribe, but anatomical evidence (Hayden, 1977, omy supports the most recent classifications of 1980, see also below) suggests a close relationship these plants (Levin & Simpson, 1994; Webster, among the oldfieldioidgenera with compoundleaves. 1994). Presently, Picrodendreae includes all oldfieldioids Tribe Croizatieae Webster. Croizatia, the only with compound leaves (e.g., Stachyandra), plus genus of the tribe, is anatomically unknown. several others with unifoliolate (Parodiodendron Tribe Podocalyceae Webster. The genera as- and species of Aristogeitonia) or evidently simple sociated with Podocalyx have undergone radical leaves (Androstachys, Mischodon, and Voata- revision in the brief history of Oldfieldioideae.K6h- malo) (Levin & Simpson, 1994; Webster, 1994). ler (1965) grouped Podocalyx with several genera Picrodendreae is characterized anatomically by al- of tribe Picrodendreae that have compound leaves ternate vessel-ray pits, bundle sheath extensions plus Tetracoccus, whereas Webster (1975) asso- bearing crystals, well-developed areoles, and fim- ciated it with some of the simple-leaved genera of brial veins at leaf margins. Picrodendreae plus, again, Tetracoccus. As dis- Anatomical data support a subdivision of Picro- cussed below, the genera of Picrodendreae, wheth- dendreae that has been adopted by Levin & Simp- er bearing simple or compound leaves, form a son (1994) and Webster (1994). The first group reasonably well-defined lade and are thus better is African-Madagascan-Sri Lankan and consists classified elsewhere. Of the two classifications pre- of And rostachys, Aristogeitonia, Mischodon, sented in this volume, both link Podocalyx with Stachyandra, and Voatamalo; these genera may Paradrypetes, albeit each in separate subtribes, be defined by stipules adnate to the petiole (Airy but only Webster continues to include Tetracoccus Shaw, 1970, 1972; Bosser, 1976; Radcliffe-Smith, in this tribe. There are no compelling anatomical 1988, 1990) and a strong tendency toward uni- synapomorphies that might serve to unite these foliolate or simple leaves. Further, Aristogeitonia, three genera. The primitive wood features of Par- Mischodon, and Voatamalo possess sclerified ray adrypetes and Podocalyx (see above) suggest that cells bearing prismatic crystals. at least these two genera are basal offshoots from Mischodon was included among the genera of the ancestral stem of Oldfieldioideae;as such, they Dissiliariinae by Pax & Hoffman (1931) (see also may not be expected to share many synapomor- Fig. 1) and K6hler (1965). I am in complete agree- phies with each other. Each genus of Podocalyceae ment with Raju (1984), who pointed out several bears at least one strikingly unique autapomorphy: differences in stomata and trichomes between the raphides of Paradrypetes, the tracheoid idio- Mischodon and genera of Dissiliariinae. Mischo- blasts of Podocalyx, and the ring porous wood of don thus bears no compelling anatomical resem- Tetracoccus. blance to any genus of tribe Caletieae sensu lato. The xeromorphic adaptations of Tetracoccus Placement in Picrodendreae is definitely superior might just as easily obscure an early or late di- to any previous classification of the genus, a con- vergence from ancestral oldfieldioidstocks. Tetra- clusion confirming,to some extent, suggestionsmade coccus does share alternate vessel-ray pitting with by Airy Shaw (1972) based on the similarity of Picrodendreae, and this character could be used stipules of Aristogeitonia and Mischodon. to argue for its inclusion in that tribe, as classified The second subgroup of Picrodendreae is neo- by Levin & Simpson (1994, this volume). tropical and consists of Celaenodendron, Picro- Volume 81, Number 2 Hayden 197 1994 Euphorbiaceae Subfamily Oldfieldioideae

dendron, and Piranhea; these genera are uni- western Cape of . Hyaenanche has formly trifoliolate, have alternate phyllotaxy, and no other obvious close relatives within Oldfieldioi- lack the epidermal mucilage which is so widespread deae. Anatomically, its marginal venation is re- in the family. Parodiodendron, also neotropical, markable, but, apparently, autapomorphic. It is presents an interesting situation. It shares with the perhaps best viewed as a remnant of the Austral- trifoliolate genera alternate phyllotaxy and unusu- asian stem of the subfamily, from which it has been ally large (for Oldfieldioideae) intervascular pits; separated since the breakup of Gondwanaland. but its leaves are unifoliolate and lack the fimbrial Placement of Hyaenanche in a separate mono- vein characteristic of all other members of the tribe. generic subtribe seems appropriate. Further, Parodiodendron is unique within the sub- Hyaenanche excluded, all other members of family by virtue of its septate wood fibers. Nev- Tribe Caletieae share another epidermal feature, ertheless, Parodiodendron seems best accommo- longitudinally chambered cells that bear copious dated among the other neotropical Picrodendreae, mucilage deposits in their lower halves. Taken to- especially if its discordant features are viewed as gether, crenulate subsidiary cells and mucilaginous autapomorphies. epidermis provide a robust definition of the Aus- Oldfieldia is not included in either of the above tralasian lade. The Australasian genera also tend groups. Anatomically, its trichomes and presence to have relatively low rank foliar venation and (in some species) of homocellular procumbent rays poorly defined areoles, but it seems these vein resemble these features in the otherwise rather features are best interpreted as plesiomorphic. The different genera Androstachys and Stachyandra. distinctive epidermal features of Caletieae sensu Oldfieldia may represent a relictual element de- lato are found in Scagea, which argues strongly rived early from the ancestors to Picrodendreae for its placement here and not in prior to its differentiation into otherwise distinct or Crotonoideaeas suggested by McPherson (1985); New and Old World lineages. the uniovulate carpels of Scagea may thus be Levin & Simpson (1994) include Tetracoccus homoplasious with Acalyphoideae, , in Picrodendreae, but aside from the alternate ves- and . sel-ray pits of these desert shrubs there is no com- Both Webster (1994) and Levin & Simpson pelling anatomical support for this placement. (1994) divide the Australasianoldfieldioids into three Tribe Caletieae Muell. Arg. With virtually no subtribes, Dissiliariinae, Petalostigmatinae, and contrary opinion on record, Micrantheum, Pseud- Pseudanthinae. anthus, and Stachystemon have been recognized Aside from the epidermal characters that define as close relatives for well over a century (Agardh, the entire Australasian lade of Oldfieldioideae,the 1858; Mueller, 1866; Bentham, 1880; Grining, genera of subtribe Dissiliariinae share few phylo- 1913; Pax & Hoffmann, 1931; Hutchinson, 1969). genetically significantanatomical structures. Woods These shrubby xerophytes of Australia constitute of Dissiliariinaehave irregular vessel-ray pits (Fig. the traditional circumscription of Tribe Caletieae. 28), but this is probably a plesiomorphic feature Their gross similarity and narrow "Stenolobeae"- in the subfamily. Leaf margins tend to be entire type cotyledons precluded serious comparison with in Oldfieldioideae,but, as noted above, exceptional other euphorbs prior to the utilization of pollen toothed leaves occur in species of Austrobuxus, characters in the systematics of Euphorbiaceae. Choriceras, and Dissiliaria, and this feature, too, Neoroepera was added to what was then a wholly is probably plesiomorphic. Austrobuxus, with a Australian tribe by Webster (1975) who was im- preponderance of solitary pores, long vessel ele- pressed, no doubt, by the numerous scattered ap- ments (often > 1 mm), occasional scalariform per- ertures (Punt, 1962; Kohler, 1965) shared by all forations, and abundant tracheids, seems to be the four genera. Additional palynological and anatom- least specialized genus of the subtribe in terms of ical studies have refined concepts of relationships wood anatomy. Anatomically, Dissiliaria stands to the extent that, now, all Australasian genera apart from the remainder of its tribe by virtue of except Mischodon are perceived to constitute a high rank venation, well-developed and somewhat single clade, the greatly expanded Tribe Caletieae oriented areoles, narrow ultimate tracheids in vein- sensu lato (Levin & Simpson, 1994; Webster, lets, fimbrial veins, wavy anticlinal walls of leaf 1994). epidermis cells, bundle sheath extensions, and libri- The presence of crenulate "piggyback" subsid- form wood fibers. iary cells is a particularly striking synapomorphy W'hyanbeelia lacks crystal-bearing axial xylem linking all Australasian genera of Oldfieldioideae, parenchyma; in this respect it resembles wood of plus the monotypic Hyaenanche, endemic to the Petalostigma and Pseudanthinae; its retention in 198 Annals of the Missouri Botanical Garden

Dissiliariinaemay be challenged on this character. taxa are quite similar anatomically and evidently Lack of wood material precludes determining very closely related. Levin & Simpson (1994) pro- whether Scagea and Kairothamnus are better in- vide further discussion of the relationships of Kair- cluded in Dissiliariinae (crystalliferous axial xylem othamnus, Neoroepera, Petalostigma, and Sca- parenchyma present) or either Petalostigmatinae gea with the other genera of Pseudanthinae. or Pseudanthinae (said crystals absent); pollen sug- gests relationship with Pseudanthinae (Levin & Simpson, 1994). Subtribe Dissiliariinae appears to LITERATURE CITED be a paraphyletic assemblage at the base of the AGARDH, J. G. 1858. Theoria Systematis Plantarum ... Australasian lade. C. W. K. Gleerup, Lund. Petalostigma is a distinctive genus of Australia AIRY SHAW, H. K. 1965. Diagnoses of new families, and southern New Guinea characterized, as its new names, etc., for the seventh edition of Willis's "Dictionary." Kew Bull. 18: 249-273. name suggests, by broad petaloid stigmas. The * 1966. A Dictionary of the Flowering Plants presence of crenulate subsidiary cells and cham- and Ferns, Ed. 7. Univ. Press, Cambridge. bered epidermal cells with mucilage shows the as- * 1970. The genus Androstachys Prain in Af- sociation of Petalostigma with Australasiangenera rica. Adansonia, ser. 2 10: 519-524. 1972. A second species of the genus Aris- of Oldfieldioideaeto be superior to its former as- togeitonia Prain (Euphorbiaceae),from East Africa. sociation with Androstachys (Webster, 1975; Kew Bull. 26: 495-498. Hayden, 1982); this realignment is also supported 1973. A Dictionary of the Flowering Plants biogeographically. and Ferns, Ed. 8. Univ. Press, Cambridge. Both Levin & Simpson (1994) and Webster . 1975. The Euphorbiaceae of Borneo. Kew Bull. Additional Series IV. Her Majesty's Stationery (1994) place Petalostigma in its own monogeneric Office, London. tribe, evidently because its pollen bears at least . 1976. New or noteworthy Australian Eu- some apertures out of the equatorial plane (Punt, phorbiaceae. Kew Bull. 31: 341-398. 1962; K8hler, 1965), thus differingfrom the pollen 1980a. New Euphorbiaceae from New Guin- ea. Kew Bull. 34: 591-598. of Pseudanthinae. Nevertheless, Petalostigma . 1980b. The Euphorbiaceae of New Guinea. shares some anatomical features with Pseudan- Kew Bull. AdditionalSeries VIII. Her Majesty's Sta- thinae: lack of crystalliferous axial xylem paren- tionery Office, London. chyma and the presence of nonlignified phloem 1983. Euphorbiaceae. Pp. 129-135 in B. D. Morley & H. R. Tolken (editors), Flowering Plants fibers in foliar veins. In Petalostigma the phloem in Australia. Rigby Publishers, Adelaide. fibers are thin-walled, whereas in Pseudanthinae ALVIN, K. L. 1987. Leaf anatomy of Androstachys the walls are so thick that lumina are almost com- johnsonii Prain and its functional significance. Ann. pletely occluded, so the similarity is only partial in Bot. 59: 579-591. this regard. & T. A. RAO. 1987. On the unusual distri- bution pattern of leaf sclereids in Androstachys john- From the numerous comments above in the an- sonii Prain (Euphorbiaceae). Bot. J. Linn. Soc. 95: atomical descriptions, it is clear that the four Aus- 55-60. tralian genera of subtribe Pseudanthinae (i.e., tribe ANONYMOUS. 1909. Makruss or Zimbiti. Bull. Misc. Caletieae in the traditional or narrow sense) are Inform. 1909: 201-204. [Probably attributable to united by a suite of characters involving leaf ar- D. Prain & L. A. Boodle.] ARAUJO, P. A. M. & A. MATTOS FILHO. 1984. Estrutura chitecture, leaf anatomy, and wood structure (see das madeiras brasileiras de dicotiledoneas. XXVI. also Hayden, 1981). Many of the anatomical char- Euphorbiaceae. Rodriguesia 36: 25-40. acters of these genera suggest a sequence of in- ASSAILLY, A. 1954. Contributiona la determinationdes creasing xeromorphy involving general reduction of Euphorbiaceespar la methode anatomique. Bull. Soc. Hist. leaf size, of the venation, Nat. Toulouse 89: 157-194. increasing disorganization BAILEY, I. W. 1936. The problem of differentiatingand and increasing prominence of a massive sclerenchy- classifying tracheids, fiber-tracheids, and libriform matous marginal vein. Neoroepera is particularly wood fibers. Trop. Woods 45: 18-23. interesting in that N. buxifolia Muell. Arg. is sim- BAILLON, H. 1858. Etude g6n6rale du groupe des Eu- ilar to Dissiliariinaein some characters (incomplete phorbiac6es. Victor Masson, Paris. . 1878. Euphorbiaceae. The Natural History marginal ultimate venation and lignified phloem of Plants. 5: 105-256. L. Reeve, London. fibers in foliar veins), whereas N. banksii Benth. BAMBER, R. K. 1974. Fibre types in the wood of Eu- conforms with other Pseudantheae (massive intra- phorbiaceae. Austral. J. Bot. 22: 629-634. marginal vein and unlignified phloem fibers). Rad- BENTHAM, G. 1878. Notes on Euphorbiaceae. J. Linn. Soc., Bot. 17: 185-267. cliffe-Smith's (1993) inclusion of Stachystemon 1880. Euphorbiaceae. In: G. Bentham & J. within Pseudanthus increases the diversity of ve- D. Hooker (editors),Genera Plantarum. 3: 239-340. nation patterns in the latter, but otherwise these L. Reeve, London. Volume 81, Number 2 Hayden 199 1994 Euphorbiaceae Subfamily Oldfieldioideae

BOLZA, E. & W. G. KEATING. 1972. African Timbers- & D. S. BRANDT. 1984. Wood anatomy and The Properties and Characteristics of 700 Species. relationshipsof Neowawraea (Euphorbiaceae).Syst. of Building Research, Commonwealth Sci- Bot. 9: 458-466. entific and Industrial Research Organization, Mel- , W. T. GILLIS, D. E. STONE, C. R. BROOME& bourne. G. L. WEBSTER. 1984. Systematics and palynology BOSSER, J. 1976. Voatamalo, nouveau genre d'Eu- of Picrodendron: Further evidence for relationship phorbiaceae de Madagascar. Adansonia 15: 333- with the Oldfieldioideae(Euphorbiaceae). J. Arnold 340. Arbor. 65: 105-127. CARLQUIST, S. 1975. Ecological Strategies of Xylem HEIMSCH,C., JR. 1942. Comparative anatomy of the Evolution. Univ. Press, Berkeley. secondary xylem in the "Gruinales" and "Terebin- CRONQUIST, A. 1988. Evolution and Classification of thales" of Wettstein with reference to taxonomic Flowering Plants, 2nd ed. New York Botanical Gar- grouping. Lilloa 8: 82-198. den, New York. HICKEY, L. J. & J. A. WOLFE. 1975. The bases of DAHLGREN, R. & A. E. VAN WYK. 1988. Structures angiospermphylogeny: Vegetative morphology. Ann. and relationships of families endemic to or centered Missouri Bot. Gard. 62: 538-589. in southern Africa. Monogr. Syst. Bot. Missouri Bot. HUNZIKER,A. T. 1969. Parodiodendron gen. nov.: Un Gard. 25: 1-94. nuevo genero de Euphorbiaceae (Oldfieldioideae)del DEHAY, C. 1935. L'appareil libero-ligneux foliare des noroeste Argentino. Kurtziana 5: 329-341. Euphorbiac6es. Ann. Sci. Nat. Bot. 17: 147-296. HURUSAWA,I. 1954. Eine nochmalige Durchsicht des ENDLICHER, S. 1836-1840. Genera Plantarum Secun- herk6mlichen Systems der Euphorbiaceen im wei- dum Ordines Naturales Disposita. Fr. Beck, Vienna. teren Sinne. J. Fac. Sci. Univ. Tokyo, Sect. 3, Bot. FRITSCH, R. 1972. Chromosomenzahlenvon pflanzen 6: 209-342. der insel Kuba. II. Kulturpflanze 19: 305-313. HUTCHINSON,J. 1969. Tribalism in the family Euphor- FROEMBLING, W. 1896. Anatomisch-systematischeUn- biaceae. Amer. J. Bot. 56: 738-758. tersuchung von Blatt und Axe der Crotoneen und JUSSIEU,A. DE. 1824. De Euphorbiacearumgeneribus Euphyllantheen. Bot. Centralbl.65: 129-139, 177- medisque earumdem viribus tentamen, ... Didot, 192, 241-249, 289-297, 321-329, 369-378, Paris. 403-411, 433-442, pls. 1-2. KOHLER, E. 1965. Die Pollenmorphologie der Biovu- GAMBLE, J. S. 1922. A Manual of Indian Timbers. laten Euphorbiaceaeund ihre Bedeutung fur die Tax- Reprint of ed. 2. Sampson, Low, Marston & Co., onomie. Grana Palynol. 6: 26-120. London. LEBACQ,L. & R. DECHAMPS. 1964. Essais d'identifi- GAUCHER, L. 1902. Recherches anatomiques sur les cation anatomique des bois de l'Afrique Centrale. Euphorbiacees. Ann. Sci. Nat. Bot, Ser. 8, 15: 161- Musee Royal de l'Afrique Centrale, Tervuren. 309. LEVIN, G. A. 1986. Systematic foliar morphology of GILL, B. S., S. S. BIR & Y. S. BEDI. 1981. Cytological Phyllanthoideae(Euphorbiaceae). I. Conspectus.Ann. studies on woody Euphorbiaceaefrom north and cen- Missouri Bot. Gard. 73: 29-85. tral India. New Botanist 8: 35-44. . 1992. Systematics of Paradrypetes (Eu- GIRAUD, B. 1983. Les cellules perforees des rayons phorbiaceae). Syst. Bot. 17: 74-83. ligneux chez les Euphorbiacees. Bull. Mus. Natl. Hist. & M. G. SIMPSON. 1988. Taxonomic impli- Nat. (Paris) ser. 4, sect. B, Adansonia 5: 213-221. cations of pollen ultrastructurein the Phyllanthoideae GRUNING, G. 1913. Euphorbiaceae-Porantheroideaeet and Oldfieldioideae(Euphorbiaceae). Amer. J. Bot. Ricinocarpoideae. Das Pflanzenreich IV. 147(Heft 75(6, part 2): 189-190. [Abstract.] 58): 1-97. & . 1994. Phylogenetic implications HAKKI, M. I. 1985. Studies on West Indian plants. 3. of pollen ultrastructure in the Oldfieldioideae (Eu- On floral morphology, anatomy, and relationship of phorbiaceae). Ann. Missouri Bot. Gard. 81: 203- Picrodendron baccatum (L.) Krug & Urban (Eu- 238. phorbiaceae). Bot. Jahrb. Syst. 107: 379-394. MATHOU,T. 1940. Recherches sur la famille des Bux- HANS, A. S. 1973. Chromosomal conspectus of the ac6es. Trav. Lab. Bot. Fac. M6d. & Pharmacol. Euphorbiaceae. Taxon 22: 591-636. Univ. Toulouse 1940: 130-136. HASSALL, D. C. 1976. Numerical and cytotaxonomic MCPHERSON,G. 1985. Scagea, a new genus of Eu- evidence for generic delimitation in Australian Eu- phorbiaceae from . Bull. Mus. Natl. phorbieae. Austral. J. Bot. 24: 633-640. Hist. Nat., B, Adansonia 3: 247-250. HAYDEN, W. J. 1977. Comparative anatomy and sys- MENNEGA, A. M. W. 1984. Wood structure of Ja- tematics of Picrodendron, genus incertae sedis. J. blonskia congesta (Euphorbiaceae). Syst. Bot. 9: Arnold Arbor. 58: 257-279. 236-239. - 1980. Systematic Anatomy of Oldfieldioideae 1987. Wood anatomy of the Euphorbiaceae, (Euphorbiaceae). Ph.D. Dissertation (unpublished). in particular of the subfamily Phyllanthoideae. Bot. University of Maryland, College Park. J. Linn. Soc. 94: 111-126. 1981. Systematic anatomy of Caletieae (Eu- METCALFE,C. R. & L. CHALK. 1950. Anatomy of the phorbiaceae-Oldfieldioideae).Bot. Soc. Amer. Misc. Dicotyledons. Clarendon Press, Oxford. Ser. Publ. No. 160: 69. [Abstract.] MILANEZ,F. R. 1935. Anatomie de Paradrypetes il- - 1982. Comparativeanatomy and relationships icifolia. Arq. Inst. Biol. Veg. 2: 133-156. of Androstachys Prain and Petalostigma F. v. MUELLER,J. (MUELLERARG.). 1866. Euphorbiaceae. Mueller(Euphorbiaceae subfam. Oldfieldioideae).Bot. In: A. de Candolle (editor), Prodromus systematis Soc. Amer. Misc. Ser. Publ. No. 162: 96. [Abstract.] naturalis regni vegetabilis. 15(2): 189-1286. Fortin 1987. The identity of the genus Neowawraea Masson, Paris. (Euphorbiaceae). Brittonia 39: 268-277. NAZMA, B. SUNDARSIVARAO& R. VIJENDRARAO. 1981. 200 Annals of the Missouri Botanical Garden

Occurrence of perforated ray cells in the wood of SOLEREDER, H. 1908. Systematic Anatomy of the Di- Drypetes roxburghii (Wall.) Hurusawa. I.A.W.A. cotyledons. (Translated by L. A. Boodle & F. E. Bull., n.s. 2: 201-203. Fritsch; revised by D. H. Scott.) Clarendon Press, PAX,F. 1884. Anatomieder Euphorbiaceen.Bot. Jahrb. Oxford. Syst. 5: 384-421. STERN, W. L. 1988. Index xylariorum. 3. Institutional . 1890. Euphorbiaceae. In: A. Engler & K. wood collections of the world. IAWA Bull. n.s. 9: Prantl (editors), Die Natiirlichen Pflanzenfamilien. 203-252. Ed. 1. Teil III. Abteilung 5: 1-119. Wilhelm En- STONE, H. 1904. The Timbers of Commerce and Their gelmann, Leipzig. Identification. William Rider & Son, London. * 1925. Die Phylogenie der Euphorbiaceae. WEBSTER, 1967. The genera of Euphorbiaceae in the Bot. Jahrb. Syst. 59: 9-182. southeastern United States. J. Arnold Arbor. 48: & K. HOFFMANN. 1922. Euphorbiaceae-Phyl- 303-430. lanthoideae-Phyllantheae.Das PflanzenreichIV. 147- 1975. Conspectus of a new classification of XV (Heft 81): 1-349. the Euphorbiaceae. Taxon 24: 593-601. & K. HOFFMANN. 1931. Euphorbiaceae. In: 1987. The saga of the spurges: A review of A. Engler & K. Prantl, Die Natiirlichen Pflanzen- classification and relationships in the Euphorbiales. familien. Ed. 2. 19c: 11-253. Wilhelm Engelmann, Bot. J. Linn. Soc. 94: 3-46. Leipzig. 1994. Synopsis of the genera and suprage- PRAIN, D. 1912. Aristogeitonia. Pp. 625-626 in W. neric taxa of Euphorbiaceae.Ann. MissouriBot. Gard. T. Thiselton-Dyer (editor), Flora of Tropical Africa, 81: 33-144. Vol. 6, sect. 1. L. Reeve, London. & K. I. MILLER. 1963. The genus Rever- PUNT, W. 1962. Pollen morphology of the Euphorbi- chonia (Euphorbiaceae). Rhodora 65: 193-207. aceae with special reference to . Wentia , L. GILLESPIE & J. STEYERMARK. 1987. Sys- 7: 1-116. tematics of Croizatia (Euphorbiaceae).Syst. Bot. 12: PYYKKO,M. 1979. Morphology and anatomy of leaves 1-8. from some woody plants in a humid tropical forest WORBES, M. 1989. Growth rings, increment and age of Venezuelan Guayana. Acta Bot. Fenn. 112: 1- of trees in inundation forests, savannas and a moun- 41. tain forest in the Neotropics. IAWA Bull. n.s. 10: RADCLIFFE-SMITH,A. 1988. Notes on Madagascan Eu- 109-122. phorbiaceae I. On the identity of Paragelonium and on the affinitiesof Benoistia and Claoxylopsis. Kew APPENDIX 1. Specimens of Oldfieldioideaeexamined. Bull. 43: 625-647. Xy- larium acronyms follow Stern (1988). 1990. Notes on Madagascan Euphorbiaceae. III. Stachyandra. Kew Bull. 45: 561-568. Androstachys johnsonii Prain. Leaf: Gomes & Sousa 1993. Notes on Australian Euphorbiaceae II: 2202 (K); Wellcome Chemical Research Laboratory Pseudanthus and Stachystemon. Kew Bull. 42: 165- s.n. (K). Wood: Capuron 3594.R.4, USw 27434 (= 168. CTFw 13817) (TAN); DDw 2385; Pardy s.n., USw RAJU, V. S. 1984. Notes on Mischodon zeylanicus 21255 (= Uw 14606); Pretoria UIND 2127, Uw Thwaites: A little-known euphorbiaceous plant from 21991; PRFw 20686. Sri Lanka and southern India. J. Econ. Taxon. Bot. Aristogeitonia monophylla Airy Shaw. Leaf: Bally & 5: 165-167. Smith B 14376 (K). Woody twig: Tanner 3386 (K). & P. N.RAo. 1977. Variation in the structure Aristogeitonia sp. Begue 727.R.1, CTFw 13770 (TAN). and development of foliar stomata in the Euphorbi- Austrobuxus brevipes Airy Shaw. Leaf: Stauffer & Blan- aceae. Bot. J. Linn. Soc. 75: 69-97. chon 5751 (K). Wood: McPherson 4579 (MO). RAO, P. N. & V. S. RAJU. 1985. Foliar trichomes in Austrobuxus carunculatus (Baill.) Airy Shaw. Leaf: Bau- the family Euphorbiaceae. Pp. 128-136 in C. M. mann-Bodenheim 16087 (US). Govil & V. Kumar (editors), Trends in Plant Re- Austrobuxus clusiaceus (Baill.) Airy Shaw. Leaf: McKee search. Bishen Singh & Mahendra Pal Singh, Dehra 2570 (US); Webster 14972 (DAV). Woody twig: Web- Dun. ster 14972 (DAV). RECORD,S. J. 1928. The "palo prieto" of west central Austrobuxus cuneatus (Airy Shaw) Airy Shaw. Leaf: Mexico. Trop. Woods 14: 8-12. McKee 12184 (K). . 1938. The American woods of the family Austrobuxus eugeniifolius (Guillaum.) Airy Shaw. Leaf: Euphorbiaceae. Trop. Woods 54: 7-40. Guillaumin & Baumann-Bodenheim 12908 (US); & R. W. HESS. 1943. Timbers of the New Hurlimann 1331 (US). World. Yale Univ. Press, New Haven. Austrobuxus horneanus (A. C. Smith) Airy Shaw. Leaf: ROTH, I. 1981. Structural patterns of tropical barks. A. C. Smith 6669 (US). Wood: A. C. Smith 6872, In: Encyclopedia of Plant Anatomy, Volume 9, Part Aw 28453 (= USw 30522), (A, US). 3. Borntraeger, Berlin. Austrobuxus huerlimannii Airy Shaw. Leaf: McKee 4850 ROTHDAUSCHER,H. 1896. Ueber die anatomischen Ver- (K). haltnisse von Blatt und Axe der Phyllantheen (mit Austrobuxus lugubris Airy Shaw. Leaf: McKee 25773 Ausschluss der Euphyllantheen). Bot. Centralbl. 68: (K). 65-79, 97-108, 129-136, 161-169, 193-203, Austrobuxus montanus (Ridl.) Airy Shaw. Leaf: Wray & 248-253,280-285,305-315,338-346,385-393. Robinson 5424 (K). SARKAR,A. K. & N. DATTA. 1980. Cytological assess- Austrobuxus nitidus Miq. Leaf: Chew & Corner RSNB ment of the family Euphorbiaceae. II. Tribe Phyl- 4107 (US); Chew & Corner RSNB 4608 (US). Wood: lantheae. Proc. Indian Sci. Congr. Assoc. (III, C) 67: FPAw DFP 30239; PRFw 21393 (SAR); PRFw 21395 48-49. (SAR); Si Boecca 7983, USw 29100 (MICH); Sy- Volume 81, Number 2 Hayden 201 1994 Euphorbiaceae Subfamily Oldfieldioideae

mington s.n., Uw 21411 (= KEPw 3602) (KEP); USw Cons. For. Tanganyika Territory 254, Uw 10951 30796, Uw 14635, (= SARFw 13234) (SAR). (PRFw 13495). Austrobuxus ovalis Airy Shaw. Leaf: McKee 26894 (K). Oldfieldia macrocarpa L6onard. Wood: Dechamps Austrobuxus paucifiorus Airy Shaw. Leaf: Baumann- (Comite Nat. du Kivu) s.n., TERVw 1605 (BR). Bodenheim 14113 (K); McPherson 3935 (MO).Wood: Oldfieldia somalensis (Chiov.) Milne-Redhead.Leaf: Per- McPherson 3923 (MO); McPherson 3935 (MO); Mc- due & Kibuwa 10005 (NA). Wood: Schlieben 6371 Pherson 4603 (MO). (wood no. 558), Uw 15635 (= MAD-SJRw 34030). Austrobuxus rubiginosus (Guillaum.) Airy Shaw. Leaf: Oldfieldia sp. Wood: Dechamps 330, TERVw 7522; Baumann-Bodenheim 15010 (US); Hurlimann 1486 Dechamps 335, TERVw 7527; Dechamps 655, (US). TERVw 8499 (BR). Austrobuxus swainii (de Beuzev. & C. T. White) Airy Parodiodendron marginivillosum (Speg.) Hunziker. Leaf: Shaw. Leaf: Boorman s. n. (NSW); Hewitt s. n. (NSW); Hueck 469 (US). Wood: Vervoorst & Cuezzo 7.610C Johnson & Constable s.n. (NSW). Wood: de Beuze- (LIL). ville s.n., MADw 10449 (= FPAw DFP 8606). Petalostigma banksii Britten & S. Moore. Leaf: Perry Austrobuxus vieillardii (Guillaum.) Airy Shaw. Leaf: 1981 (US); Perry 3531 (US); Perry 3562 (US). Wood: Schmid 2514 (K). Wood: McKee 25222, FPAw DFP Doherty s.n., USw 21280. 33881 (K). Petalostigma "glabrescens" (probably referable to P. Austrobuxus sp. Leaf: University of California, Davis pubescens or P. triloculare). Leaf: Clemens 42580 Greenhouse B73.173. Wood: Hyland 6918 (DAV); (US); Wilson 679 (US). Wood: SFCw R 594-2. Webster & Hyland 18927 (DAV). Domin. Leaf: White 12421 (US). Celaenodendronmexicanum Standley. Leaf: Ortega 4962 Wood: SFCw R 594-3; SFCw R 977-256; White s.n., (US); Ortega 6367 (US). Wood: Ortega 35, USw 3886 PRFw 17591. (= Aw 4494, MADw 29901, MAD-SJRw 1200); Or- Petalostigma quadriloculare F. v. Muell. Leaf: Clemens tega 6367 (US); Uw 21735 (= Aw 30657). 42561 (US); Lazarides 6669 (US). Wood: PRFw 2921; Choriceras tricorne (Benth.) Airy Shaw. Leaf: Forman PRFw 24259, (= Uw 10949); PRFw 10913, (= Uw s.n. (LAE, US). Wood: Pullen 7135, MADw 29097, 10948); Webster & Hyland 18879 (DAV). FPAw-Pullen 7135 (A, CANB, K, L, LAE). Piranhea longepedunculata Jablonski. Leaf: Breteler Dissiliaria baloghioides F. v. Muell. Leaf: Bailey s.n. 4969 (US). Wood: Breteler 4970, MAD-SJRw55650, (US); Francis & White s.n. (US). Wood: Bailey's (= Uw 12254) (MER, US); Breteler 5096, USw 35682, Woods 366, Aw 26736; PRFw 28015; ( Uw 12306, MAD-SJRw 55702) (MER, NY, U, USw 32037, Uw 14625 (= FPAw DFP 3127). US, WAG). Hyaenanche globosa (Gaertn.) Lam. Leaf: Bayliss BS- Piranhea trifoliata Baill. Leaf: Krukoff 5924 (US); Stey- BRI 576 (US); Godfrey SH-1257 (US); Werderman ermark 86615 (US). Wood: Capucho 493, USw 22377 & Oberdieck 528 (US). Wood: Bohmer & Verdoucq ( Aw 4526, MADw 30166, MAD-SJRw 23457) (F, s.n. (PRE); Botanical Research Institute Pretoria s.n. IAN); Ducke s.n., USw 31485 (MAD); Krukoff 6163, (PRE); Werderman & Oberdieck 528 (US). USw 7524 (US). Kairothamnus phyllanthoides (Airy Shaw) Airy Shaw. Podocalyx loranthoides Klotzsch. Leaf: Bernardi 1675 Leaf: Johns NGF 47324 (K); Streimann NGF 45108 (NY); Froes 21543 (NY); Krukoff 811 (NY); Williams (K). 14480 (US). Wood: Wurdack & Adderley 42795, Longetia buxoides (Baill.) Airy Shaw. Leaf: Baumann- MADw 22429 (= MAD-SJRw 54246) (NY, US). Bodenheim 5605 (US). Wood: Baumann-Bodenheim Pseudanthus divaricatissimus (Muell. Arg.) Benth. Leaf: 5605 (US). Constable 53354 (US); Ingram s.n. (NSW). Woody Micrantheum demissum F. v. Muell. Leaf: Hunt 2802 twig: Constable 53354 (US); Ingram s.n. (NSW). (US). Woody twig: Hunt 2802 (US). Pseudanthus orientalis F. v. Muell. Leaf: Clemens Desf. Leaf: Hotchkiss 428 (US); 44092 (US); Wilson 639 (US). Woody twig: Clemens Johnson & Constable 19095 (US). Woody twig: Cam- 44092 (US). bage 495 (NSW). Pseudanthus ovalifolius F. v. Muell. Leaf: Beauglehole Micrantheum hexandrum Hook. f. Leaf: Boorman s.n. & Orchards 30452 (NSW); Muir 906 (US). Woody (US); McGillivray 3196 (DAV); Schodde 1177 (US). twig: Beauglehole & Orchards 30452 (NSW); Muir Woody twig: Boorman s.n. (US); Whaite & Whaite 906 (US). 3536 (NSW). Pseudanthus pimelioides Sieb. ex Spreng. Leaf: Boor- Mischodon zeylanicus Thwaites. Leaf: Ripley 05 (US); man s.n. (US); Clemens 42750 (US). Woody twig: Wheeler 12079 (US). Wood: Jayasuriya 2434 (PDA); Boorman s.n. (US); Clemens 42750 (US); Constable Wheeler 12079 (US). NSW 55972 (NSW). Neoroepera banksii Benth. Leaf: Banks & Solander s. n. Scagea depauperata (Baill.) McPherson. Leaf: Franc (US). Woody twig: Horner & Taylor s.n. (NSW). 1642a (US). Neoroepera buxifolia White. Leaf: White 12095 (US). Woody twig: White 12095 (US). Scagea oligostemon (Guillaum.) Airy Shaw. Leaf: Guil- Oldfieldia africana Benth. & Hook. f. Leaf: Cooper 88 laumin & Baumann-Bodenheim 11808 (US); McKee (K, MAD, US); Cooper 439 (US). Wood: Commercial 2352 (US); McKee 2651 (US). sample, USw 19900; Cooper 88, USw 4517, Uw Stachyandra merana (Airy Shaw) A. Radcliffe-Smith. 14636 (= Aw 16930, MADw 30131, MAD-SJRw Leaf: Baron 6431 (K); Capuron 23335-5F (K). 13738) (K, MAD, US); Cooper 111, USw 4538, (= Stachyandra viticifolia (Airy Shaw) A. Radcliffe-Smith. Aw 16931, MADw 30132, MAD-SJRw 13761) (K, Leaf: Capuron 20975 SF (K). Wood: Capuron MAD); Cooper 295, USw 4882, (= Aw 16932, MAD- 1914.R.4, CTFw 9069 (TAN). SJRw 15207) (MAD). Stachyandra sp. Wood: Belin 218.R.6, CTFw 13786 Oldfieldia dactylophylla (Weiw. ex Oliv.) L6onard.Wood: (TAN). 202 Annals of the Missouri Botanical Garden

Stachystemon axillaris George. Leaf: Blackwell & Grif ou (1940); Heimsch (1942); MC; Bamber (1974); Rao fin 3132 (PERTH). & Raju (1985). Stachystemon brachyphyllus Muell. Arg. Leaf: George CelaenodendronStandley. Record (1928); Record (1938); 12928 (PERTH). Record & Hess (1943); Hayden (1977). Stachystemon polyandrus (F. Muell.) Benth. Leaf: Hna- Croizatia Steyerm. Levin (1986). tiuk 761262 (PERTH). Dissiliaria F. Mueller.MC; Dehay (1935); Bamber(1974); Stachystemon vermiculare Planch. Leaf: Pritzel s. n. (US); Rao & Raju (1985). Royce 5207 (PERTH). Hyaenanche Lambert & Vahl. Pax (1884); G; S; Dehay Tetracoccus dioicus Parry. Leaf: Moran 13170 (US); (1935); Assailly (1954). Terrell & Gordon 4004 (US); Webster & Hildreth Longetia Baillon. Much publishedanatomical information 7478 (DAV). Wood: Campbell 21484 (RSA). on "Longetia" pertains to Austrobuxus nitidus (= Tetracoccus fasciculatus (Wats.) Croizat var. fascicu- Longetia malayana); there appears to be no previous latus. Leaf: Johnston 7783 (GH, US); Webster,21221 anatomical study of Longetia buxoides (Baill.) Airy (DAV). Wood: Johnston 7783, Aw 23748 (GH, US). Shaw. Tetracoccus fasciculatus (Wats.) Croizat var. hallii Micrantheum Desfontaines. Pax (1884); G; S; MC; Rao (Brandegee) Dressler. Leaf: Webster & Hildreth 7460 & Raju (1985). (DAV); Wiggins 6617 (US). Wood: Webster & Hil- Mischodon Thwaites. G; Gamble(1922); Heimsch (1942); dreth 7460 (DAV). MC; Raju (1984); Rao & Raju (1985). Tetracoccus ilicifolius Coville & Gilman. Leaf: Gilman Neoroepera Mueller Arg. Rothdauscher (1896). s.n. (US); Gilman 2181 (US). Wood: Gilman 2181 Oldfieldia Bentham. Stone (1904); MC; Assailly (1954); (US). Lebacq & Dechamps (1964); Bolza & Keating (1972); Voatamalo eugenioides Capuron ex Bosser. Wood: SF Hayden (1977); Rao & Raju (1985). 198 R 259, (= CTFT 13816, Uw 23104); SF 5327 Paradrypetes Kuhlm. Milanez (1935); Araujo & Mattos R 4 (= CTFT 15079, Uw 23105). Filho (1984); Levin (1986); Mennega (1987). Whyanbeelia terrae-reginae Airy Shaw & Hyland. Leaf: Petalostigma F. Mueller. Froembling (1896); Roth- Irvine 1399 (K). Wood: Hyland 7945 (K). dauscher (1896); G; S; Dehay (1935); MC; Bamber (1974); Rao & Raju (1985). APPENDIX 2. Previous anatomical literature on Oldfieldioi- Picrodendron Planchon. Hayden (1977) (q.v. for earlier deae. Comprehensive works abbreviated as follows: G = references); Hakki (1985); Rao & Raju (1985). Gaucher (1902); S = Solereder (1908); MC = Metcalfe Piranhea Baillon. Dehay (1935); Record (1938); MC; & Chalk (1950). Hayden (1977); Pyykk6 (1979); Roth (1981); Worbes Androstachys Prain. Anonymous (1909); MC; Bolza & (1989). Keating (1972); Rao & Raju (1985); Alvin (1987); Pseudanthus Sieber ex Sprengel. Pax (1884); G; S; Rao Alvin & Rao (1987); Dahlgren & van Wyk (1988). & Raju (1985). Austrobuxus Miquel (often reported as "Longetia," see Stachystemon Planchon. Pax (1884); G; MC. below). Rothdauscher(1896); G; Dehay (1935); Math- Tetracoccus Engelman ex Parry. Heimsch (1942); MC.