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Biology
1994
Systematic Anatomy of Euphorbiaceae Subfamily
Oldfieldioideae I. Overview
W. John Hayden
University of Richmond, jhayden@richmond.edu
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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.
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SYSTEMATIC ANATOMY OF
W.John Hayden2
EUPHORBIACEAE
SUBFAMILY
OLDFIELDIOIDEAE.
I. OVERVIEW'
ABSTRACT
The biovulate subfamily Oldfieldioideaeof Euphorbiaceae, characterizedby spiny pollen, is an otherwise apparently
diverse assemblage of mostly Southern Hemisphere trees and shrubs 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 order venation; foliar and petiolar glands absent; unicellular or unbranched
uniseriate trichomes; latex absent; mucilaginous epidermis or hypodermis; brachyparacytic stomata; vessel elements
with simple perforation plates and alternate, often very small, intervascular pits; thick-wallednonseptate imperforate
tracheary elements; numerous narrowheterocellularrays; and abundantaxial xylem parenchyma in diffuse to somewhat
banded patterns and often bearing prismatic crystals. Anatomically, the shrubby Australian ericoid genera form a
well-definedgroup with obvious affinitiesto the more arborescent Australasiangenera, which show clear relationships
to each other; the African and neotropical genera bearing compoundleaves 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 subfamily Oldfieldioideae K6hler & Webster dates
conceptually from the palynological studies of Punt
(1962) and K6hler (1965) who noted the spiny
pollen that characterizes the group; the assemblage
recognized by pollen structure was subsequently
formalized nomenclaturally as a new subfamily
(Webster, 1967). In essence, pollen characters
circumscribed a group of genera that previously
had been assigned to the biovulate subfamilies Phyllanthoideae and Porantheroideae in the system of
Pax & Hoffmann (1931). Webster's first (1975)
classification of oldfieldioid genera contained several novel taxonomic associations at variance with
earlier classifications, notably those of Pax & Hoffmann (1931) and Hutchinson (1969).
Interest in the anatomy of Oldfieldioideae
stemmed from the need for comparative data to
aid placement of the problematic genus Picrodendron Planchon (Hayden, 1977). Despite a number
of publications dealing with the anatomy of oldfieldioid genera (Appendix 2), detailed information
for most of the subfamily is lacking. Once Picro-
dendron was shown to be a member of Oldfieldioideae (Hayden, 1977; see also Hayden et al., 1984,
and Hakki, 1985), an anatomical survey of the
entire subfamily was initiated (Hayden, 1980) to
assess relationships from data independent of reproductive (includingpollen) morphology. Based in
part on these anatomical studies, classification of
Oldfieldioideaehas been modified from Webster's
(1975) original proposal; two broadly similar classifications, one by G. L. Webster (the preceding
issue) and another by G. A. Levin and M. G.
Simpson (this issue), are proposed elsewhere.
HISTORY
Classifications of Euphorbiaceae from the first
half of the 19th century (e.g., Jussieu, 1824; Endlicher, 1836-1840) offer little insight into relationships among oldfieldioid genera. At this formative time in the definition of Euphorbiaceae
(Webster, 1987) the few oldfieldioidgenera known
were often scattered widely in the family; moreover, 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
1994
EuphorbiaceaeSubfamilyOldfieldioideae
of Pseudanthinae (or Caletieae in the traditional/
narrow sense) were the first to be classified together, undoubtedlybecause of their shared ericoid
xeromorphic habit and common provenance in
Australia. Baillon (1858) grouped Micrantheum
Desf. with Pseudanthus Sieber ex Sprengel, to
which Agardh (1858) added Stachystemon Planchon, establishingthe composition of Caletieae that
was followed in all subsequent studies until the
addition, first, of Neoroepera Muell. Arg. by Kohler (1965) and, now, the inclusion of all Australasian oldfieldioidsas proposed by Levin & Simpson
(1994, this issue) and Webster (1994). During the
intervening years, however, the use of cotyledon
width as the primary criterion for subdivision of
the family (Mueller, 1866; Pax, 1890; Pax &
Hoffmann, 1931) relegated the genera of Pseudanthinae (as Caletieae) to the Stenolobeae, a small
group of Australian xerophytes with narrow cotyledons. Their somewhat isolated position in Stenolobeae minimizedassociationof Pseudanthinaewith
other oldfieldioidgenera.
Other oldfieldioidgenera similarly suffered early
taxonomic assignments that delayed consideration
of relationshipswith the rest of the subfamily. Baillon (1858) submerged Podocalyx Klotzsch within
the phyllanthoidgenus Richeria Vahl, a disposition
followed well into this century. Oldfieldia Benth.
& Hook. f. was temporarily considered sapindaceous (Mueller, 1866; Baillon, 1878). Worse, the
relationships of Picrodendron were long obscured
by a series of misassignments at both the generic
and familial levels (Hayden et al., 1984).
Aside from Caletieae sensu stricto, the genera
of Oldfieldioideaewere scattered widely in Mueller's (1866) treatment of the family for the Prodromus; Mischodon Thwaites was included with
uniovulate genera, following an earlier error of
Baillon (1858), Oldfieldia was still banished to
Sapindaceae, and the remaining five oldfieldioid
genera in his treatment were each assigned to different subtribes of Phyllantheae. Greater cohesiveness is apparent in a later publicationof Baillon
(1878). For example: Choriceras Baillon was included within Caletieae;Austrobuxus Miq. (as Buraeavia Baill.), Longetia Baillon ex Muell. Arg.,
Petalostigma F. Muell., and Hyaenanche Lambert
formed a sequence; and Dissiliaria F. Muell. ex
Baill. followed Richeria (which included the oldfieldioidPodocalyx). (See Webster (1987) for commentary on Baillon's peculiar "serial" system to
indicate relationships.) Additional elements were
gradually accreted to this loosely defined nucleus
of oldfieldioidgenera. Bentham (1880), in his treatment of Euphorbiaceae in the Genera Plantarum,
181
included, using current nomenclature, Dissiliaria,
Longetia, Austrobuxus, Hyaenanche, Mischodon, Oldfieldia, Piranhea Baillon, and only one
nonoldfieldioidgenus, Bischofia Blume, within genera 46-54. Although these plants constituted three
discrete groups in his conspectus, Bentham (1878)
expressed some doubt about their relatedness and
he chose to associate Neoroepera and Petalostigma with other phyllanthoid genera. Pax (1890)
treated oldfieldioidgenera much as had Bentham;
Tetracoccus Engelm. ex C. Parry, however, was
included, and Pax & Hoffmann (1931) added Petalostigma, Androstachys Prain, and Aristogeitonia Prain to various subtribes consisting largely of
oldfieldioid genera. Perhaps the first clear indication of the relatedness of oldfieldioid genera can
be found in Pax's (1925) essay on Euphorbiaceae,
which includes the phylogenetic tree reproduced
in Figure 1. Although much of the detail in this
phylogenetic tree may be challenged seriously in
the light of present knowledge, it does show oldfieldioid genera (as usual, minus Pseudanthinae)
comprising a clade distinct from other biovulate
Euphorbiaceae.
In the dispositionof genera, Hurusawa's (1954)
classification of Euphorbiaceae essentially follows
that of Pax & Hoffmann (1931) and thus contains
no new insights on classification of oldfieldioidgenera. In light of Pax's (1925) phylogeny and because
of its disregard for the palynological data available
at the time (Punt, 1962; K6hler, 1965), Hutchinson's (1969) classification was a retrograde development; oldfieldioidgenera were widely distributed in five of 12 biovulate tribes, with three tribes
mixing oldfieldioid and phyllanthoid elements.
Hutchinson was the first, however, to associate
Paradrypetes Kuhlm. with other oldfieldioidgenera.
Airy Shaw (1965) entertained serious doubts
about inclusion of several oldfieldioid genera in
Euphorbiaceae. Accordingly, he proposed Androstachydaceae, of uncertain relationships,to accommodate Androstachys; he recognized Picrodendraceae as distinctfrom but alliedto Euphorbiaceae;
and he viewed Aristogeitonia, Calaenodendron
Standley, Mischodon, Oldfieldia, and Piranhea
as occupying an intermediatepositionbetween these
families (Airy Shaw, 1966, 1972, 1973). Airy
Shaw (1983) continued to accept an isolated taxonomic position for Stenolobeae (including Pseudanthinae), but he did, consistently, group the remaining Australasian genera of Oldfieldioideae in
adjacent tribes in several of his informalor tentative
classification systems (e.g., Airy Shaw, 1975,
1980b, 1983).
182
Annals of the
Missouri Botanical Garden
WI ELAND IINAE
ANDRACHNINAE
PS EUDOL ACH NOSTYLI DINAE
PETALOSTIGMATINAE
Petalostigma
ANTI DESM INAE
AMANOINAE
DRYPETINAE
Drypetes
DISCOCARPINAE
UAPACI NAE
Heywoodia
Lingelsheimia
Neoroepera
Tetracoccus
BISOHOFFIINAE
SAUROPODINAE/
PHYLLANTHINAE
PAIVAEUSINAE
Aristogeitonia
Old fieldia
Piranhea
TOXICODENDRINAE
Androstachys
Hyaenanche
GLOCHIDIINAE
DISSILIA RIINAE
Dissiliaria
Longetia
(incl. Austrobuxus)
Mischodon
FIGURE 1.
Relationshipsof 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 subgenus of Richeria [Antidesminae]) 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 undiPlants of Oldfieldioideaeare woody, ranging from vided; each locule houses a pair of pendulous anatlow depressed shrubs to tall trees. Latex is absent ropous ovules. Seeds 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; stipules 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 species. Plants are typically dioe- 1980) collectively suggest a base number of x =
cious. Flowers are apetalous, and most lack discs. 12 for the subfamily.
Stamens range from three to many. Pollen is biThe first comprehensive classification of Oldnucleate, 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, Voatatectum 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
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Hayden
Euphorbiaceae Subfamily Oldfieldioideae
been referred to the subfamily. Two enigmatic genera, Croizatia Steyerm. (Webster et al., 1987)
and Paradrypetes (Levin, 1992), have been assigned to Oldfieldioideaefollowing discovery of diagnostic flowering material and, especially, after
study of pollen from these plants. Kairothamnus
Airy Shaw (1980a) and Scagea McPherson (1985)
have been segregated from Austrobuxus sensu lato,
as has Canaca Guillaumin, if only tentatively
(Webster, 1994). In recent years Radcliffe-Smith
has redefined generic limits for several Oldfieldioideae. He has included Paragelonium Leandriwithin Aristogeitonia (Radcliffe-Smith, 1988), he segregated Stachyandra R. -Sm. from Androstachys
to accommodate several Madagascan species bearing compound leaves (Radcliffe-Smith, 1990), and
he expanded Pseudanthus to include Stachystemon (Radcliffe-Smith, 1993). The number of genera now stands at 27. (Solely because of the recency of its reclassification,Stachystemon is herein
treated as a distinct genus.)
Genera of Oldfieldioideaeare mostly mono- or
oligotypic. Austrobuxus, with perhaps 20 species,
is the most speciose, followedby Pseudanthus (seven species) and Petalostigma (six species). The
total number of species referable to the subfamily
is estimated at 86, approximately 1 percent of the
total number of species in Euphorbiaceae.
Oldfieldioideaeis largely a southern hemisphere
group. Only three genera occur in areas not derived
from the breakup of Gondwanaland;these are Celaenodendron, from western Mexico, Picrodendron, from the Bahamas and Greater Antilles, and
Tetracoccus from Mexico and the southwest United
States. Eight genera and 16 species occur in the
New World, six genera and 16 species occur in
Africa and Madagascar, one monotypic genus occurs in southern India and Sri Lanka, and 13
genera and 52 species are Australasian. No genus
of Oldfieldioideaehas a bicontinental distribution,
although Androstachys and Aristogeitonia occur
both in Madagascar and Africa.
cations listed in Appendix 2 has been incorporated
into the following account as appropriate.
MATERIALS
This report is based on first-hand examination
of 97 leaf and 87 wood specimens of 61 species
of Oldfieldioideae. Specimens examined are listed
in Appendix 1. The specimens available represent
to some degree all genera of the subfamily except
Croizatia and Paradrypetes; it should be noted
that leaves of Voatamalo and wood of Kairothamnus, Scagea, and Stachystemon are lacking in this
study. Previous anatomical literature concerning
genera of Oldfieldioideae provided by the publi-
183
LEAF ARCHITECTURE
For the most part, leaves are either simple or
palmately compound; however, interesting transitional morphologies do exist. Leaves of Oldfieldia
are palmately compound, with 3-8 leaflets; those
of Celaenodendron, Picrodendron, and Piranhea
are trifoliolate;both palmately compound and simple leaves occur in Aristogeitonia; and leaves of
Parodiodendron Hunz. are unifolioate, as evidenced by the minute stipelsat the apex of the petiole
(Hunziker, 1969) and by the frequent disarticulation of the lamina at the same point (Fig. 4).
Finally, leaves of Micrantheum, which occur in
alternate groups of three (to five), have been interpreted as the leaflets of a palmately compound
leaf which, by loss of their common petiole, are
sessile on the stem (Baillon, 1858); alternatively,
this unique phyllotaxy has been attributedto foliate
stipules (Griining, 1913; Webster & Miller, 1963).
For the most part, leaf margins are entire, the few
exceptional species being Austrobuxus cuneatus
(Airy Shaw) Airy Shaw, A. swainii (de Beuzev. &
C. T. White) Airy Shaw, Choriceras tricorne
(Benth.) Airy Shaw (Figs. 7, 8), Dissiliaria muelleri (Baill.) ex Benth., Paradrypetes ilicifolia
Kuhlm. (Levin, 1986), P. subintegrifolia G. Levin
(Levin, 1992), Tetracoccus dioicus Parry (only
some leaves), and T. ilicifolius Coville & Gilman.
Paradrypetes possesses irregularly spaced spinose
teeth (Levin, 1986, 1992). Teeth of Tetracoccus
ilicifolius are the largest in the subfamily: median
veins of these teeth are derived from the looped
secondary veins; there are prominent brochidodromouslikeloops within the tooth itself; and median
veins extend nearly to the apices, which in the
specimens examined appear to possess apical caps,
at least in young leaves. Teeth of the remaining
species are much smaller, consisting of a vein ending in a small protrusionof leaf tissue. Significantly,
however, deciduous apical caps are also visible in
Austrobuxus swainii and Choriceras tricorne (Figs.
7, 8). Tooth morphology in Oldfieldioideae thus
conforms with the theoid type (Hickey & Wolfe,
1975). Excluding noninformative spinose teeth,
theoid teeth are the only type found in Phyllanthoideae, specifically in the genera Drypetes Vahl,
Putranjiva Wall., and Bischofia; reduced theoid
teeth are also present in Aporuseae (Levin, 1986).
Venation is always pinnate, most frequently festooned brochidodromous(Figs. 2, 3). In addition
to brochidodromy, however, leaves of Longetia
Annals of the
Missouri Botanical Garden
184
Si n~~~S
S NEW
MMW
!v
AW
EW
x~~~~~~~~~~~~5
2. Austrobuxus
ofOldfieldioideae.
(Baumann-Bodenheim
features
architectural
FIGURES2-8. Leaf
rubiginosus
mexicanum
(Ortega6367), clearedleaf,bar= 1 cm.15010),clearedleaf,bar= 1 cm.-3. Celaenodendron
of petiolefrombaseof lamina,
4. Parodiodendron
(Hueek469), clearedleaf,notedisarticulation
marginivillosum
bar= 2.5
baccatum(Gillis6963), notelackof veinordersbeyondtertiaries,
bar= 5 mm.-5. Picrodendron
185
Volume 81, Number 2
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Hayden
Euphorbiaceae Subfamily Oldfieldioideae
exhibit a tendency toward eucamptodromy whereas
Picrodendron (Fig. 5), and Piranhea (all New
World genera with trifoliolate leaves) plus Androstachys; this character state is extremely rare
in the dicots as a whole (L. J. Hickey, pers. comm.)
and is thus a potentially robust synapomorphylinking these genera. Areoles are well developed in the
genera with compound leaves (Figs. 5, 12) plus
Dissiliaria, Mischodon, Parodiodendron (Fig. 6),
and Podocalyx; otherwise, areoles are imperfectly
developed. Areoles are usually arranged randomly,
but are oriented in Celaenodendron and somewhat
oriented in Picrodendron, Piranhea, and Dissiliaria. Veinlets are usually present and mostly simple
or branched; the degree of branching varies widely,
tending to be most highly branched in leaves with
low regularity of tertiary and higher order veins.
Veinlets are absent in Androstachys (Fig. 12), but
they may appear to be present upon superficial
examination because of the columnar sclereids located in each areole (see below).
those of Dissiliaria, Petalostigma, Picrodendron,
and Tetracoccus tend toward reticulodromy. Leaves
of the Australian genera of Pseudanthinae (Caletieae sensu stricto) exhibit a continuum of increasing disorganization, presumably a consequence of
xeromorphy: in Neoreopera leaves are weakly festooned brochidrodromous; in Micrantheum one can
find vestiges of brochidodromous venation as well
as secondary veins that recurve and ramify or form
a weak reticulum; in Stachystemon the range is
from reticulodromous to kladodromous; and in
Pseudanthus leaves are all kladodromous (Fig. 9).
Primary veins are mostly of moderate size, but,
especially in xeromorphic leaves, they may range
to stout and massive, e.g., those of Hyaenanche,
Tetracoccus, and the Australian Pseudanthinae (Fig.
9). Intersecondary veins are usually absent, although one or two simple intersecondaries per intercostal area occur occasionally in Austrobuxus
and Mischodon, and routinely in Croizatia (Levin,
1986), Oldfieldia, Paradrypetes (Levin, 1986),
Piranhea, and Podocalyx. Intersecondary veins
are frequent in several primitive Phyllanthoideae,
namely, Amanoa Aubl., Blotia Leandri, Heywoodia Sim, Petalodiscus Baill., Savia Willd., and
Wielandia Baill. (Levin, 1986); their presence is
thus postulated to be primitive for Oldfieldioideae.
Tertiary vein patterns are usually random reticulate; ramified patterns occur in Hyaenanche, species of Austrobuxus, and those species of Australian Pseudanthinae that possess distinguishable
tertiaries; there is a slight tendency toward transverse tertiaries in Parodiodendron, Paradrypetes
(Levin, 1986), Petalostigma, and Podocalyx; and
the tertiary veins of Piranhea have a slight tendency to form orthogonal patterns. Marginal venation is incomplete (Fig. I 1) or looped (Fig. 6) in
many genera, "hemmed" with a fimbrial vein in
the genera with compound leaves (Figs. 10, 12)
plus Dissiliaria and Mischodon, or dominated by
a massive intramarginal vein in most Australian
Pseudanthinae (Fig. 9). A distinctive furcate-flabellate form of marginal venation occurs in Hyae-
nanche.
High-order venation varies considerably within
Oldfieldioideae. Perhaps most notable is the occurrence of ultimate reticula in which vein order
is not distinguishable, a feature of Celaenodendron,
LEAF ANATOMY
Trichomes have been observed in about twothirds of the genera of Oldfieldioideae.Many species are glabrescent with age, although mature
leaves of Androstachys, Parodiodendron, and
species of Petalostigma, for example, are clearly
pubescent. Trichomes are either simple unicellular
or uniseriate, generally consisting of less than six
cells. Within Pseudanthinae, epidermal emergences range from small papillae to four-celled
uniseriate trichomes. The densely packed trichomes of Androstachys johnsonii Prain, which
consist of a short basal cell and long curly terminal
cell, have been suggested by Alvin (1987) to function in absorption of atmospheric moisture (mists
and drizzles) in the otherwise extremely arid environment of southern Africa. Oldfieldia possesses
trichomes similar to those of Androstachys, arguing for some degree of relationshipbetween these
two genera despite their manifest differences in
reproductive morphology. Depending on the species, trichomes of Austrobuxus are either simple
or bifurcate (malpighiaceous). Parodiodendron is
unique within the subfamily in possessing strongly
ciliate leaf margins (Fig. 6). Rao & Raju (1985)
reported uniseriate, stellate, and glandular hairs in
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 section through tooth at leaf margin, note glandular apex, bar = 100 ,um.
Annals of the
Missouri Botanical Garden
186
K~~~~~~~~~~~~~~~~~~~~~~~~~
$k17
Leaf architecture of Oldfieldioideae.-9. Pseudanthus orientalis (Clemens 44092), kladodromous
FIGURES 9-12.
Celaenodendron mexicanum (Ortega
venation, massive primary and intramarginal veins, bar = 250 gm.-10.
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 Oldfieldioideae; however, neither trichomes nor their bases were
detected in the leaves available to me.
The epidermis is fundamentally uniseriate. However, a single layer of hypodermis has been reported for Paradrypetes (Milanez, 1935) and some
or all epidermal cells of the Australasian genera
have a horizontal partition resulting in a poorly to
well-defined hypodermis (Figs. 17-19). The inner
cell or chamber thus formed contains mucilage,
which is common in other genera as well. Expansion
of the mucilaginous layer in Australian Pseudanthinae greatly distends the adaxial epidermis (Figs.
18, 19); while the grossly expanded mucilaginous
layer may well be an artifact of preparation, it is
derived solely from the lower portions of subdivided
epidermal cells and is not thickly multicellular as
depicted by Gaucher (1902), whose erroneous in-
Volume81, Number2
1994
Hayden
187
EuphorbiaceaeSubfamilyOldfieldioideae
TB
*;i.~~~~~~~~~~0
W
T4P
FIGURES13-16.
Leaf anatomyof Oldfieldioideae.-13. Longetia buxoides(Baumann-Bodenheim
5605), stomate from cross section,bar = 20 sum.-14. Scagea oligostemon(McKee2352), surfaceview of stomatefrom
paradermal
section,note crenulateinneranticlinalwallsof subsidiarycells visiblethroughstomatalaperture,bar =
10 Mm.-15. Austrobuxushuerlimannii(McKee4850), subdividedcrenulatesubsidiarycells and trichomebases
from paradermalsection, bar = 20 Mum.-16.Podocalyx loranthoides(Krukoff811), tracheoididioblastsfrom
maceratedmesophyll,bar = 20 ,um.GC = guardcell, SC = subsidiarycell, TB = trichomebase.
terpretation has been reiterated by others (e.g.,
Metcalfe & Chalk, 1950; Raju & Rao, 1977). So
far, no mucilage has been detected in Aristogeitonia, Celaenodendron, Mischodon, Piranhea, and
Podocalyx. Mucilaginous epidermis is known in
several Phyllanthoideae, for example, Actephila
Bl., Antidesma L., Aporusa Bl., Amanoa, Baccaurea Lour., Bridelia Willd., Hyeronima Fr. Al-
lem, Phyllanthus L., Richeria, and Savia (Metcalfe & Chalk, 1950). In surface view, anticlinal
walls of epidermal cells are generally straight (Figs.
14, 15), the only exceptions being Aristogeitonia,
Celaenodendron, Piranhea, (all members of Picrodendreae), and Dissiliaria, in which these walls
have a wavy outline; intriguingly, paradermal sections of Aristogeitonia and Celaenodendron reveal
Annals of the
Missouri Botanical Garden
188
PF
_M)
PF
-
(M)
-17. Longetia buxoides(BaumannFIGURES17-21. Leaf anatomyand woodparenchymaof Oldfieldioideae.
-18. Pseudanthus
Bodenheim5605), leafcrosssection,notechamberedmucilaginous
epidermalcells,bar= 100 Aum.
orientalis(Wilson 679), leaf cross section, note grosslyexpandedmucilaginoushypodermisand prominentintramarginalveins, bar = 100 um.- 19. Micrantheumhexandrum(McGillivray3196), crosssectionof primaryvein,
note grosslyexpandedmucilaginoushypodermis,bar = 100 um.-20. Hyaenancheglobosa (GodfreySH 1257),
cross sectionof leaf, bar = 100 ,um.-21. Piranhea trifoliata(Duckes.n., USw 31485), normaland chambered
axialxylemparenchymacells, bar = 15 Am.PF = phloemfibers.
crystalliferous
189
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Hayden
Euphorbiaceae Subfamily Oldfieldioideae
the inner portions of epidermal cells to possess
straight anticlinal walls.
Leaves are overwhelmingly hypostomatic, although both hypo- and amphistomatic conditions
occur in species of Petalostigma and Tetracoccus.
Stomatal type is anomocytic in Podocalyx, paracytic in Paradrypetes (Levin, 1986), but otherwise
brachyparacytic (Fig. 14) or derived from a
brachyparacytic pattern. For example, intruding
lobes of adjacent cells tend to form an anomocytic
pattern in Tetracoccus as viewed from the surface;
paradermal sections, however, reveal typical
brachyparacytic configurations.The most frequent
modification of stomatal type is the tendency for
one or both of the subsidiary cells to become subdivided into two or three smaller cells; subdivision
of subsidiary cells may be a consistent feature in
a given taxon, or it may be sporadic, affecting only
some stomata or only one subsidiary cell of a given
pair. Subdividedbrachyparacytic stomata occur in
Androstachys, where the pattern has been described as incompletely cyclocytic (Alvin, 1987),
Aristogeitonia, some species of Austrobuxus (Fig.
15), Hyaenanche, Mischodon, Picrodendron, and
Pseudanthus. The paracytic stomata of Paradrypetes are also subdividedin a similarfashion (Levin,
1986). The distribution of subdivided subsidiary
cells does not follow any obvious taxonomic grouping within the subfamily. Within Phyllanthoideae,
brachyparacytic stomata are characteristic of Bridelieae, Drypeteae, Phyllantheae-Fleuggeinae, and
certain genera of Wielandieae; moreover, subdivided brachyparacytic stomata occur in Lachnostylis Turcz. and Bridelia (Levin, 1986). Raju &
Rao (1977) reported brachyparacytic stomata to
be the most common type among woody genera
throughout Euphorbiaceae.
In most genera subsidiary cells extend partially
over the inner periclinal walls of adjacent guard
cells in a "semi-piggyback" fashion (Fig. 13); the
inner anticlinal walls of subsidiary cells thus delimit
an inward extension of the stomatal pore. Within
Phyllanthoideae, Levin (1986) noted a similar spatial relationship of guard and subsidiary cells only
in Drypetes. The inner anticlinal walls of "piggyback" subsidiary cells may have crenulate outlines (Figs. 14, 15), a feature first observed by
Solereder (1908) in Micrantheum and Pseudanthus that now proves characteristic of the Australasian genera (Mischodon and certain species
of Austrobuxus excluded) plus the South African
genus Hyaenanche; this feature defines a distinct
clade within the subfamily. Crenulate subsidiary
cells are only weakly developed in the single specimen of T;hyanbeelia available for study. In con-
trast to most genera, subsidiary and guard cells
are coplanar in Oldfieldia and Parodiodendron.
Mesophyll is bilateral except in some species of
Petalostigma with isobilateral leaves; leaves of
Hyaenanche approachan isobilateralcondition(Fig.
20). Spongy mesophyll with well-developed intercellular spaces but a tendency towardvertical alignment of cells occurs in Androstachys, Oldfieldia,
Picrodendron, and Piranhea, all members of Picrodendreae. Mesophyll usually contains scattered
druses; prismatic crystals are also present in Aristogeitonia, Austrobuxus, Dissiliaria, Hyaenanche, Longetia, and Micrantheum. Mesophyll of
Paradrypetes contains raphide bundles (Milanez,
1935; Levin, 1986), a structure otherwise unknown in Euphorbiaceae(Gaucher, 1902; Metcalfe
& Chalk, 1950). No crystals were observed in the
mesophyll of Celaenodendron, Parodiodendron,
and Piranhea. Except for Androstachys and
Stachyandra, foliar sclereids are absent; areoles
of these genera usually contain a single columnar
sclereid with ramified tips that run parallel with
the bases of epidermal cells and eventually intermingle with trichome bases and the bundle sheath
extensions of the veins. Alvin (1987) has interpreted the sclereids of Androstachys to function
in apoplastic transport from its water-absorbant
trichomes. It is intriguing to speculate that the
vertically oriented spongy mesophyll cells of Androstachys may have served as a preadaptation
for the evolution of its columnar sclereids. Another
unique mesophyll feature is found in Podocalyx,
which bears unbranched, sinuous tracheoid idioblasts with spirallythickened, nonlignifiedwalls (Fig.
16). These elements, occurring most frequently
between the junction of palisade and spongy layers,
are sufficiently abundant to obscure the presence
of veinlets in clearings; they are not, however,
directly connected to any vasculature.
Vasculature of the primary vein consists of adjacent (colateral) regions of xylem, phloem, and
phloem fibers. Little taxonomic significance can be
read into the overall configuration of primary vein
vasculature, which ranges from broad shallow arcs
to more tightly curved u-shaped arcs to closed
loops; reduced leaves of desert xerophytes, however, tend to have patterns with minimal curvature
(Figs. 18, 19). Phloem fibers of the primary vein
in Petalostigma and the Australian Pseudanthinae
are unlignified (Figs. 18, 19), in sharp contrast to
the usual lignified condition of these cells in the
rest of the subfamily. Smaller veins are frequently
associated with a parenchymatous bundle sheath
(Fig. 17). Bundle sheath extensions that are merely
parenchymatous occur in Longetia (Fig. 17); crys-
190
Annals of the
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tals are present in bundle sheath extensions of
Aristogeitonia, Celaenodendron, Hyaenanche,
Mischodon, Oldfieldia, Parodiodendron, Petalostigma, Picrodendron, and Piranhea; and at
least some fibrouselements are also present in those
of Androstachys, Mischodon, and Piranhea.
Overall, bundle sheath extensions seem best developed in the genera bearing compound leaves,
but also occur sporadically elsewhere in the subfamily. Swollen terminal tracheids of veinlets occur
in some Austrobuxus, Choriceras, Hyaenanche,
Longetia, Petalostigma (Fig. 11), and Tetracoccus.
to reticulate). Tyloses and/or tannins are common
in lumina of heartwoodvessels; silica deposits occur
in lumina of Whyanbeelia.
Imperforate tracheary elements bear either simple or borderedpits. Elements with simple pits, i.e.,
libriformwood fibers, characterize the genera with
compound leaves (Aristogeitonia, Celaenodendron, Oldfieldia, Piranhea, and Picrodendron)
plus Dissiliaria, Hyaenanche, and Petalostigma;
some of these may also possess elements with bordered pits. The remaining genera possess only elements with bordered pits; these cells are probably
best characterized as fiber-tracheids by virtue of
their relatively small pit borders and thick walls.
However, because intervascular pits in some oldfieldioidsare remarkably small, Androstachys, Aristogeitonia, and the Australian genera of Pseudanthinae, for example, pits of imperforate elements
may be approximately equal to or slightly larger
than intervascular pits in the same wood; by the
criteria of Bailey (1936) such elements would be
tracheids, by definition, despite their thick walls
and pit diameters of 5 gim or less. "Tracheid,"
with its connotation of primitive conducting element, hardly seems appropriate for such cells. On
the other hand, the tracheids of Podocalyx, with
pit diameters up to 13 tm, attest more convincingly
to primitive structure, and both fiber-tracheidsand
tracheids are present in Austrobuxus, distinguishable by both wall thickness (Fig. 22) and pit size.
Bands of gelatinous fibers occur in woods of Australian Pseudanthinae (Fig. 24), Hyaenanche, and
Tetracoccus. Imperforate elements often possess
such thick cell walls that lumina appear completely
closed; Bamber(1974) noted that these thick-walled
fibers lack an easily detectable S3 layer in Austrobuxus, Dissiliaria, and Petalostigma. Fibers
are septate only in Parodiodendron.
Rays are numerous, generally more than 15 per
mm; however, there are more than 20 per mm in
Australian Pseudanthinae, and only 12 per mm in
Androstachys and Oldfieldia. High ray frequencies are probablyrelated to the general narrowness
of individual rays. Rays are mostly 1-, 2-, or
3-seriate, but up to 4- or 5-seriate rays occur in
Choriceras, Dissiliaria, Aristogeitonia, and Tetracoccus (Fig. 33). Polymerous (vertically fused)
rays are usually common (Fig. 32); however, they
are infrequent or absent in Androstachys (Fig. 31),
Choriceras, Parodiodendron, Tetracoccus, and the
AustralianPseudanthinae. Aggregate rays were observed in Choriceras only. Rays are usually heterocellular (Figs. 28, 29), which is generally considered the primitive condition. Homocellular
procumbent rays are shared by Androstachys and
WOOD ANATOMY
Growth rings are often absent or only faintly
visible. Growth rings are present, however, in Androstachys, Celaenodendron (Fig. 23), Parodiodendron, Petalostigma, Podocalyx, Tetracoccus,
and Australian Pseudanthinae (Fig. 24); except for
Podocalyx, from the upper Amazon and Orinoco
drainage basins, these are plants of dry habitats
with strongly seasonal availability of moisture. Pores
are evenly distributed (i.e., diffuse porous in species
with growth rings), except in the ring porous wood
of Tetracoccus, which extends into desert regions
of western North America. Pore outlines are mostly
circular, generally small, and usually less than 100
Atm diam.; pore diameters are often less than 50
Atmin the genera mentioned above from dry habitats. Perforation plates are overwhelmingly simple,
but scalariform plates are found in Paradrypetes
(exclusively so according to Mennega (1987), mixed
with simple perforations according to Araujo &
Mattos Filho (1984)) and mixed simple, scalariform
(Fig. 30), and reticulate plates characterize Podocalyx. Intervascular pits are transitional in Paradrypetes and Podocalyx; otherwise they are alternate and mostly small, ca. 5 Aim or less. Very
small intervascular pits (2-3 ,um) are found in
Aristogeitonia, Neoroepera, and Pseudanthus;
somewhat larger than usual pits (6-8
,um) occur
in Austrobuxus, Celaenodendron, Parodiodendron, Picrodendron, Piranhea, and Podocalyx.
Vessel element lengths for most genera fall within
the range of 400-700
,um; vessel elements are
somewhat shorter in Picrodendron (ca. 300 Aim),
somewhat longer in Dissiliaria (ca. 800 gim), Austrobuxus (ca. 950 ,im), and Paradrypetes
(ca.
1200 ,im), and longest in Podocalyx (ca. 1250
,im). Sculpture on the inner surface of vessels is
rare; some vessels of Choriceras possess spiral
of
are characteristic
thickenings;
thickenings
Whyanbeelia (spiral only) and Tetracoccus (spiral
Volume 81, Number 2
1994
Hayden
Euphorbiaceae Subfamily Oldfieldioideae
191
AMAMI
Wood anatomy of Oldfieldioideae.-22. Austrobuxus swainii (deBeuzeville s.n., MADw 10449),
FIGURES22-27.
note thin- and thick-walled fibers.-23. Celaenodendron mexicanum (Ortega 35, USw 3886), note long radial
multiplesof pores and boundariesof growth ring (top and bottom). -24. Micrantheum hexandrum ( Whaite & Whaite
3536), note bands of gelatinous fibers.-25. Piranhea trifoliata (Ducke s.n., USw 31485), note banded distribution
Oldfieldia
of axial xylem parenchyma.-26. Androstachys johnsonii (Pretoria UIND 2127, Uw 21991).-27.
africana (Cooper 88, USw 4517). All bars = 100 Am.
Annals of the
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192
TABLE 1.
Wood structure of biovulate euphorbs, after Metcalfe & Chalk (1950).
Feature
Aporusa-type
"Other genera"
Glochidion-type
Perforations
Fibers
scalariform, simple, or both
nonseptate, thick-walled
simple
nonseptate, thick-walled
simple
septate, thin to moderately
thick-walled
Parenchyma
abundant, diffuse or narrow bands
abundant, diffuse to wide
bands
absent or scanty
some species of Oldfieldia, which serves to demonstrate that these woods are not as dramatically
distinct as Metcalfe & Chalk (1950) suggested.
Homocellular square to erect rays are one of several synapomorphiesthat mark the Australiangenera of Pseudanthinae as a distinct monophyletic
group. Vessel to ray pits are of two forms that
appear to hold great systematic significance. The
most distinctive pattern consists of highly irregular
pits that range from circular to elongate with the
elongate pits at various orientations: vertical, horizontal, or diagonal (Fig. 28). This irregularpattern
is interpreted as primitive by virtue of its resemblance to primitive transitional intervascular pitting, and by its occurrence in Paradrypetes and
Podocalyx (see below); irregular vessel-ray pits
have been retained by all arborescent Australasian
genera. All other genera possess uniform vesselray pits that are circular and alternate. If circular,
alternate vessel-ray pits are indeed the derived
character state, this feature evolved twice, since
the Australian Pseudanthinae (i.e., Caletieae sensu
stricto) are clearly derived from the lineage bearing
the arborescent genera of Australasia (see below),
rather than the lineage of African and American
genera. Ray cells generally bear only tannins, but
several exceptions occur: prismatic crystals are
sporadic in Podocalyx, abundant in Paradrypetes
(Araujo & Mattos Filho, 1984); silica deposits are
common in Petalostigma; and sclerified cells bearing a prismatic crystal are abundant in Aristogeitonia, Mischodon, and Tetracoccus fasciculatus;
these crystalliferous cells are only rarely present
in Voatamalo. Perforated ray cells are sporadic in
Paradrypetes (Milanez, 1935), Podocalyx, and
Hyaenanche, but have not been observed in other
Oldfieldioideae.Perforated ray cells are fairly widespread in Euphorbiaceae according to Giraud
(1983), who recorded this feature in the following
phyllanthoid genera: Aporusa, Baccaurea, Bridelia, Cleistanthus Hook. f. ex Planch., Drypetes,
Hyeronima, and Richeria. Perforated ray cells
are also present in Putranjiva (Nazma et al., 1981)
and Amanoa (unpublished obs.).
Axial xylem parenchyma is mostly diffuse and
(Fig. 27), with bands also
diffuse-in-aggregates
present in Aristogeitonia, Dissiliaria, Parodiodendron (strictly initial bands), Picrodendron, Piranhea (Fig. 25), and Voatamalo; on the other
hand, parenchyma is infrequent and restricted to
a few abaxial scanty paratracheal cells in Androstachys, Stachyandra, and the Australian genera
of Pseudanthinae (Fig. 24). Parenchyma strands
usually contain both ordinary cells and short sclerified cells bearing a single prismatic crystal (Fig.
21); crystalliferous parenchyma is absent, how-
ever, in Paradrypetes, Podocalyx, Petalostigma,
Whyanbeelia, the Australian genera of Pseudanthinae, and most specimens of Tetracoccus. Since
sclerified crystalliferous axial xylem parenchyma
cells are common in several phyllanthoid woods
(e.g., Amanoa and Drypetes), presence of such
cells may be considered primitive for Oldfieldioideae; their loss may well be synapomorphous for
Petalostigma,f Whyanbeelia, and the Australian
genera of Pseudanthinae; loss in others (e.g., Paradrypetes, Podocalyx, and most specimens of Tetracoccus) may represent convergent developments.
ORIGIN OF OLDFIELDIOIDEAE
EVIDENCE FROM WOOD ANATOMY
The analysis of wood structure of biovulate euphorbs contained in Metcalfe & Chalk (1950) provides a convenient starting point for discussion of
relationships between Phyllanthoideae and Oldfieldioideae. In this work, three groups of genera were
distinguished, as indicated in Table 1. At the most
superficial of levels, woods of Oldfieldioideae, largely included in Metcalfe & Chalk's "other genera,"
may be characterized as a combination of the vessel
features of Glochidion-type woods and the fiber
and parenchyma features of Aporusa-type woods,
the latter two categories consisting primarily of
phyllanthoid genera. In some instances these three
coarsely defined categories provide a useful perspective for placing genera; for example, the re-
193
Volume 81, Number 2
1994
Hayden
Euphorbiaceae Subfamily Oldfieldioideae
moval of Neowawraea Rock, which has Glochidion-type wood, from Drypetes, which has Aporusatype wood, and its subsequent submergence into
Flueggea Willd., which also has Glochidion-type
wood (Hayden & Brandt, 1984; Hayden, 1987).
However, as wood structure of biovulate euphorbshas become better known, genera with wood
that is transitional between the three categories
cloud what once appeared to be a clear picture.
For example, Mennega (1984) found tribal placement of Jablonskia Webster difficult, essentially
because the wood of Jablonskia has an unusual
combination of characters: specifically, vessel features of Aporusa-type woods and fiber and parenchyma features of Glochidion-type woods. In short,
Jablonskia represents the reverse of the combination that characterizes most oldfieldioids. Mennega (1987) has noted additional transitional genera in her extensive survey of wood structure in
Phyllanthoideae; moreover, woods of some phyllanthoids, e.g., Lachnostylis Turcz. and Savia,
match the typical oldfieldioid pattern described
above. Further, within Oldfieldioideae,Podocalyx
and Paradrypetes possess essentially typical expressions of Aporusa-type structure. Clearly, the
simple rubric of three wood types for biovulate
euphorbs requires modification.
An evolutionary perspective of anatomical characters helps to clarify some of the complexity seen
in woods of biovulate euphorbs. In accord with
widely accepted hypotheses of wood evolution,
Mennega (1987) has identified woods with long
vessel elements, long scalariformperforationplates,
mediumto large intervascularpits, long thick-walled
nonseptate fibers with bordered pits on both radial
and tangential walls, and diffuse or narrowly banded axial xylem parenchyma to be primitive within
Phyllanthoideae. Extant genera such as Aporusa,
Blotia, and Protomegabaria Hutch. retain these
features. Carlquist(1975) has argued convincingly
that primitive vessel features are adaptive only in
uniformly moist forest environments that impose
minimal demands for water conduction. It may be
assumed that adaptive radiation of primitive biovulate euphorbs into drier, or seasonally drier, habitats would be accompanied by evolution of more
advanced vessel features. Similarly, one may reasonably suppose exploitation of nonforest and/or
seasonal habitats to be associated with modification
of mechanicaland storage requirementsof the wood;
such changes would be manifest in both fiber and
parenchyma features. Much of the diversity of
biovulate euphorb wood structure may thus be interpreted in terms of divergence from primitive
Aporusa-type structure, an ecologically restrictive
syndrome of xylem features.
Within Phyllanthoideae, Aporusa- and Glochidion-type structure represent evolutionary extremes, but numerous transitional forms can be
identified from Mennega's (1987) data. For example, tracking both perforation plates and development of septate fibers yields the following
series of forms that may be viewed as intermediates
between Aporusa- and Glochidion-type structure:
Actephila, Chascotheca Urb., and Pentabrachium Muell. Arg. with exclusively scalariform perforations and some septate fibers; Celianella Jabl.,
Didymocystis Kuhlm., and Jablonskia with mixed
simple and scalariform perforations and some septate fibers; Astrocasia Rob. & Greenm. and Discocarpus Klotzsch with simple perforations, but
only some septate fibers. Similarly, within Aporusa-type woods, there is a clear transition of perforation plates from exclusively scalariformin Aporusa, Heywoodia, Hyeronima, Maesobotrya
Benth., and Putranjiva, to mixed simple and scalariform in numerous genera and, finally, to exclusively simple in Lachnostylis and Savia. Of course,
such sequences of extant genera should not be
interpreted as the actual course of xylem evolution
within Phyllanthoideae.
In terms of the gross vessel, fiber, and parenchyma features of Table 1, the evolutionary transformation of wood in Oldfieldioideaeseems parallel
to that noted for Aporusa-type woods. In comparison, Phyllanthoideae experienced a greater
range of wood diversification with the additional
development of Glochidion-type woods.
Within Oldfieldioideae, Podocalyx and Paradrypetes stand out as probably the most primitive
woods by virtue of their very long vessel elements,
multiple perforation plates, and large transitional
intervascular pits; presence of perforated ray cells
in these genera may also be interpreted as primitive
features. Overall, their woods are comparable to
primitive phyllanthoid woods with Aporusa-type
structure. The primitive woods of Paradrypetes
and Podocalyx excepted, Oldfieldioideaegenerally
have exclusively simple perforationplates and have
lost perforated ray cells, but otherwise retain the
features of Aporusa-type structure (cf. comments
on Lachnostylis and Savia, above). Much of the
diversity of oldfieldioidwoods is restricted largely
to what are, perhaps, minor themes such as element
size (Figs. 22-27), vessel grouping (Figs. 22-27),
ray dimensions (Figs. 31-33), vessel-ray pitting,
and parenchyma distribution(Figs. 22-27). These
minor themes, however, are responsible for con-
194
Annalsof the
MissouriBotanicalGarden
p
FIGURES28-33.
~ ~ ~ ~~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~ ~~~~~~~~~~~
S~~~~~~~~~~~~~
ad
Wood anatomyof Oldfieldioideae.-28.Austrobuxusswain~ii(Symingtons.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
1994
siderable diversity of oldfieldioid woods; based on
wood features alone, it is entirely understandable
that Metcalfe & Chalk (1950) sought to associate
oldfieldioidgenera with woods from other subfamilies.
The presence of somewhat primitivewoods (Paradrypetes and Podocalyx) in Oldfieldioideaesuggests that the divergence of Oldfieldioideae from
Phyllanthoideae occurred quite early in the evolution of Euphorbiaceae, from ancestral stocks with
relatively primitiveAporusa-type woods. The symplesiomorphousnature of wood features at the evolutionary transition between the subfamilies precludes the possibility of specifying one or another
phyllanthoid group as closest to the origin of Oldfieldioideae based on this tissue alone.
Septate fibers, common in phyllanthoids with
Glochidion-type structure, occur in only one oldfieldioid, Parodiodendron. One prominent difference, however, between this wood and the Glochidion-type phyllanthoids is its fairly abundant
parenchyma present in initial bands, diffuse apotracheal and scanty paratracheal configurations.
Typical expressions of Glochidion-type structure
include very little parenchyma at all. The occurrence of septate fibers in Parodiodendron may
thus represent convergence.
EVIDENCE FROM STOMATALSTRUCTURE
Configuration of the stomatal apparatus is one
of the most consistent features of leaves of Oldfieldioideae. Most genera possess brachyparacytic
patterns in which the subsidiary cells substantially
overlie the adjacent guard cells. In this regard,
Levin (1986), upon whose data much of the following is based, has shown stomatal patterns of the
phyllanthoidtribes to be fairly diverse; in fact, this
character provides important evidence in identifying which phyllanthoids are closest to the origin
of Oldfieldioideae.As argued above, it will be necessary only to consider tribes with Aporusa-type
wood structure. Aporuseae may be eliminated from
further consideration by its consistently anisocytic
stomata, a pattern never found in Oldfieldioideae.
Paracytic or brachyparacytic stomata are found in
the remaining tribes under consideration, i.e.,
Amanoeae, Antidesmeae, Drypeteae, and Wielandieae, with brachyparacytic in only Drypeteae and
some Wielandieae. Subsidiary cells in Drypetes,
like those of most Oldfieldioideae,partially overlie
the adjacent guard cells. The brachyparacytic subsidiary cells of Lachnostylis (tribe Wielandieae)
are frequently subdivided (Levin, 1986), another
common character in Oldfieldioideae. Unfortunately, the distribution of stomatal characters in
Hayden
Euphorbiaceae Subfamily Oldfieldioideae
195
Phyllanthoideae and Oldfieldioideaeprecludes any
simple statement about the point of divergence of
the two subfamilies. Both characater states of three
important characters (paracytic-brachyparacytic,
entire-subdivided subsidiary cells, and coplanar"piggyback" subsidiary cells) are found in both
groups. This situationmay be viewed as an example
of Cronquist's (1988) assertion that parallel tendencies are reasonably good indicators of relationships; a rigorous cladistic analysis of Phyllanthoideae and Oldfieldioideae should distinguish the
synapomorphic stomatal characters from the parallelisms.
ADDITIONALEVIDENCE
A number of anatomical characters such as the
occurrence of theoid teeth, intersecondary veins,
and mucilaginous epidermis in Oldfieldioideaeand
primitive Phyllanthoideae are consistent with the
former's derivation from the latter. Floral structure
of Wielandieae is sufficiently generalized to be consistent with ancestral status. However, plesiomorphous characters such as these do not present by
themselves an overly compelling case for consanguinity.
On the other hand, the often reduced carpel
number and drupaceous fruits of Drypetes show
greater (or, at least, different) specialization than
that found in many Oldfieldioideae.Further, chromosome numbers of n = 20 for Putranjiva (Gill
et al., 1981) and 2n = 40 for Drypetes (Webster,
1967) are difficult to resolve with the counts suggesting x = 12 for Oldfieldioideae (see above).
Extant Drypeteae are thus unsuitable as progenitors for Oldfieldioideae,but it remains conceivable
that these taxa may have shared a common ancestor.
Levin & Simpson (1988) noted that the spinules
and discontinuous exine foot layer in pollen of
Securinega Comm. ex Juss. sensu stricto suggested
a close relationship with Oldfieldioideae. Despite
exclusively simple perforation plates, the wood of
Securinega conforms well to the Aporusa-type
(and thus may be out of place in tribe Phyllantheae,
as pointed out by Mennega (1987)). Securinega
also possesses paracytic stomata (Gaucher, 1902).
Further anatomical data would be most useful. In
our present state of ignorance, Securinega stands
as another possible near relative to Oldfieldioideae.
SUMMARY
Taken together, stomatal and wood characters
suggest that Oldfieldioideaediverged from the early
differentiationof the primitive biovulate tribe Wielandieae perhaps along some of the same lines that
196
Annals of the
Missouri Botanical Garden
Tribe Picrodendreae (Small) Webster.The genultimately led to the modern genera Drypetes and/
or Securinega. In a larger context, presence of era with palmately compound leaves form the contheoid teeth and palmately compound leaves in ceptual nucleus of tribe Picrodendreae. Bentham
Oldfieldioideaelends supportto Dilleniidrather than (1878) was the first to group together the biovulate
Rosid derivation of Euphorbiaceae (cf. discussion euphorbs with compound leaves, associating Oldin Levin (1986)).
fieldia and Piranhea with the non-oldfieldioidgenus Bischofia. Later, Aristogeitonia (Prain, 1912;
Pax & Hoffmann, 1922, 1931) and CelaenodenRELATIONSHIPS WITHIN OLDFIELDIOIDEAE
dron (Hutchinson, 1969) were added to this group,
Classification of subfamily Oldfieldioideae has which (minus Bischofia) constituted subtribe Paibeen in a state of flux over the past three decades. vaeusinae of Webster (1975). (Presence of nonThe followingdiscussion focuses on anatomical data spiny pollen (K6hler, 1965) and Glochidion-type
as indicators of relationshipswithin Oldfieldioideae, wood structure (Mennega, 1987) shows Bischofia
specifically, the role of anatomy in modification of to be better placed in Phyllanthoideae.) Webster
(1975) maintained Picrodendron in a monogeneric
early classifications of Oldfieldioideae (Khler,
1965; Webster, 1975) and the extent that anat- tribe, but anatomical evidence (Hayden, 1977,
1980, see also below) suggests a close relationship
omy supports the most recent classifications of
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
several others with unifoliolate (Parodiodendron
genus of the tribe, is anatomically unknown.
Tribe Podocalyceae Webster. The genera as- and species of Aristogeitonia) or evidently simple
sociated with Podocalyx have undergone radical leaves (Androstachys, Mischodon, and Voatarevision 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 alof 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 fimciated it with some of the simple-leaved genera of brial veins at leaf margins.
Anatomical data support a subdivision of PicroPicrodendreae plus, again, Tetracoccus. As discussed below, the genera of Picrodendreae, wheth- dendreae that has been adopted by Levin & Simpson (1994) and Webster (1994). The first group
er bearing simple or compound leaves, form a
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 unifoliolate or simple leaves. Further, Aristogeitonia,
synapomorphies that might serve to unite these
three genera. The primitive wood features of ParMischodon, and Voatamalo possess sclerified ray
cells bearing prismatic crystals.
adrypetes and Podocalyx (see above) suggest that
Mischodon was included among the genera of
at least these two genera are basal offshoots from
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 agreephies 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. Mischoblasts of Podocalyx, and the ring porous wood of don thus bears no compelling anatomical resemblance to any genus of tribe Caletieae sensu lato.
Tetracoccus.
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 convergence from ancestral oldfieldioidstocks. Tetra- clusionconfirming,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.
The second subgroup of Picrodendreae is neoto argue for its inclusion in that tribe, as classified
tropical and consists of Celaenodendron, Picroby Levin & Simpson (1994, this volume).
197
Volume 81, Number 2
1994
Hayden
Euphorbiaceae Subfamily Oldfieldioideae
dendron, and Piranhea; these genera are uniformly trifoliolate, have alternate phyllotaxy, and
lack the epidermalmucilage which is so widespread
in the family. Parodiodendron, also neotropical,
presents an interesting situation. It shares with the
trifoliolate genera alternate phyllotaxy and unusually large (for Oldfieldioideae) intervascular pits;
but its leaves are unifoliolate and lack the fimbrial
vein characteristic of all other members of the tribe.
Further, Parodiodendron is unique within the subfamily by virtue of its septate wood fibers. Nevertheless, Parodiodendron seems best accommodated among the other neotropical Picrodendreae,
especially if its discordant features are viewed as
autapomorphies.
Oldfieldia is not included in either of the above
groups. Anatomically, its trichomes and presence
(in some species) of homocellular procumbent rays
resemble these features in the otherwise rather
different genera Androstachys and Stachyandra.
Oldfieldia may represent a relictual element derived early from the ancestors to Picrodendreae
prior to its differentiation into otherwise distinct
New and Old World lineages.
Levin & Simpson (1994) include Tetracoccus
in Picrodendreae, but aside from the alternate vessel-ray pits of these desert shrubs there is no compelling anatomical support for this placement.
Tribe Caletieae Muell. Arg. With virtually no
contrary opinion on record, Micrantheum, Pseudanthus, and Stachystemon have been recognized
as close relatives for well over a century (Agardh,
1858; Mueller, 1866; Bentham, 1880; Grining,
1913; Pax & Hoffmann, 1931; Hutchinson, 1969).
These shrubby xerophytes of Australia constitute
the traditional circumscription of Tribe Caletieae.
Their gross similarity and narrow "Stenolobeae"type cotyledons precluded serious comparison with
other euphorbs prior to the utilization of pollen
characters in the systematics of Euphorbiaceae.
Neoroepera was added to what was then a wholly
Australian tribe by Webster (1975) who was impressed, no doubt, by the numerous scattered apertures (Punt, 1962; Kohler, 1965) shared by all
four genera. Additional palynological and anatomical studies have refined concepts of relationships
to the extent that, now, all Australasian genera
except Mischodon are perceived to constitute a
single clade, the greatly expanded Tribe Caletieae
sensu lato (Levin & Simpson, 1994; Webster,
1994).
The presence of crenulate "piggyback" subsidiary cells is a particularly striking synapomorphy
linking all Australasian genera of Oldfieldioideae,
plus the monotypic Hyaenanche, endemic to the
western Cape of South Africa. Hyaenanche has
no other obvious close relatives within Oldfieldioideae. Anatomically, its marginal venation is remarkable, but, apparently, autapomorphic. It is
perhaps best viewed as a remnant of the Australasian stem of the subfamily, from which it has been
separated since the breakup of Gondwanaland.
Placement of Hyaenanche in a separate monogeneric subtribe seems appropriate.
Hyaenanche excluded, all other members of
Tribe Caletieae share another epidermal feature,
longitudinally chambered cells that bear copious
mucilage deposits in their lower halves. Taken together, crenulate subsidiary cells and mucilaginous
epidermis provide a robust definition of the Australasian lade. The Australasian genera also tend
to have relatively low rank foliar venation and
poorly defined areoles, but it seems these vein
features are best interpreted as plesiomorphic. The
distinctive epidermal features of Caletieae sensu
lato are found in Scagea, which argues strongly
for its placement here and not in Acalyphoideae
or Crotonoideaeas suggested by McPherson (1985);
the uniovulate carpels of Scagea may thus be
homoplasious with Acalyphoideae, Crotonoideae,
and Euphorbioideae.
Both Webster (1994) and Levin & Simpson
(1994) dividethe Australasianoldfieldioidsinto three
subtribes, Dissiliariinae, Petalostigmatinae, and
Pseudanthinae.
Aside from the epidermal characters that define
the entire Australasian lade of Oldfieldioideae,the
genera of subtribe Dissiliariinae share few phylogenetically significantanatomicalstructures. Woods
of Dissiliariinaehave irregular vessel-ray pits (Fig.
28), but this is probably a plesiomorphic feature
in the subfamily. Leaf margins tend to be entire
in Oldfieldioideae,but, as noted above, exceptional
toothed leaves occur in species of Austrobuxus,
Choriceras, and Dissiliaria, and this feature, too,
is probably plesiomorphic. Austrobuxus, with a
preponderance of solitary pores, long vessel elements (often > 1 mm), occasional scalariform perforations, and abundant tracheids, seems to be the
least specialized genus of the subtribe in terms of
wood anatomy. Anatomically, Dissiliaria stands
apart from the remainder of its tribe by virtue of
high rank venation, well-developed and somewhat
oriented areoles, narrow ultimate tracheids in veinlets, fimbrial veins, wavy anticlinal walls of leaf
epidermis cells, bundle sheath extensions, and libriform wood fibers.
W'hyanbeelia lacks crystal-bearing axial xylem
parenchyma; in this respect it resembles wood of
Petalostigma and Pseudanthinae; its retention in
198
Annals of the
Missouri Botanical Garden
Dissiliariinaemay be challenged on this character.
Lack of wood material precludes determining
whether Scagea and Kairothamnus are better included in Dissiliariinae(crystalliferous axial xylem
parenchyma present) or either Petalostigmatinae
or Pseudanthinae (said crystals absent); pollen suggests relationship with Pseudanthinae (Levin &
Simpson, 1994). Subtribe Dissiliariinaeappears to
be a paraphyletic assemblage at the base of the
Australasian lade.
Petalostigma is a distinctive genus of Australia
and southern New Guinea characterized, as its
name suggests, by broad petaloid stigmas. The
presence of crenulate subsidiary cells and chambered epidermal cells with mucilage shows the association of Petalostigma with Australasiangenera
of Oldfieldioideaeto be superior to its former association with Androstachys (Webster, 1975;
Hayden, 1982); this realignment is also supported
biogeographically.
Both Levin & Simpson (1994) and Webster
(1994) place Petalostigma in its own monogeneric
tribe, evidently because its pollen bears at least
some apertures out of the equatorial plane (Punt,
1962; K8hler, 1965), thus differingfrom the pollen
of Pseudanthinae. Nevertheless, Petalostigma
shares some anatomical features with Pseudanthinae: lack of crystalliferous axial xylem parenchyma and the presence of nonlignified phloem
fibers in foliar veins. In Petalostigma the phloem
fibers are thin-walled, whereas in Pseudanthinae
the walls are so thick that lumina are almost completely occluded, so the similarity is only partial in
this regard.
From the numerous comments above in the anatomical descriptions, it is clear that the four Australian genera of subtribe Pseudanthinae (i.e., tribe
Caletieae in the traditional or narrow sense) are
united by a suite of characters involving leaf architecture, leaf anatomy, and wood structure (see
also Hayden, 1981). Many of the anatomical characters of these genera suggest a sequence of increasing xeromorphyinvolving general reduction of
leaf size, increasing disorganizationof the venation,
and increasing prominence of a massive sclerenchymatous marginal vein. Neoroepera is particularly
interesting in that N. buxifolia Muell. Arg. is similar to Dissiliariinaein some characters (incomplete
marginal ultimate venation and lignified phloem
fibers in foliar veins), whereas N. banksii Benth.
conforms with other Pseudantheae (massive intramarginal vein and unlignified phloem fibers). Radcliffe-Smith's (1993) inclusion of Stachystemon
within Pseudanthus increases the diversity of venation patterns in the latter, but otherwise these
taxa are quite similar anatomically and evidently
very closely related. Levin & Simpson (1994) provide further discussion of the relationshipsof Kairothamnus, Neoroepera, Petalostigma, and Scagea with the other genera of Pseudanthinae.
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SOLEREDER,
APPENDIX 1. Specimens of Oldfieldioideaeexamined. Xylarium acronyms follow Stern (1988).
Androstachys johnsonii Prain. Leaf: Gomes & Sousa
2202 (K); Wellcome Chemical Research Laboratory
s.n. (K). Wood: Capuron 3594.R.4, USw 27434 (=
CTFw 13817) (TAN); DDw 2385; Pardy s.n., USw
21255 (= Uw 14606); Pretoria UIND 2127, Uw
21991; PRFw 20686.
Aristogeitonia monophylla Airy Shaw. Leaf: Bally &
Smith B 14376 (K). Woody twig: Tanner 3386 (K).
Aristogeitonia sp. Begue 727.R.1, CTFw 13770 (TAN).
Austrobuxus brevipes Airy Shaw. Leaf: Stauffer & Blanchon 5751 (K). Wood: McPherson 4579 (MO).
Austrobuxus carunculatus (Baill.) Airy Shaw. Leaf: Baumann-Bodenheim 16087 (US).
Austrobuxus clusiaceus (Baill.) Airy Shaw. Leaf: McKee
2570 (US); Webster 14972 (DAV). Woody twig: Webster 14972 (DAV).
Austrobuxus cuneatus (Airy Shaw) Airy Shaw. Leaf:
McKee 12184 (K).
Austrobuxus eugeniifolius (Guillaum.)Airy Shaw. Leaf:
Guillaumin & Baumann-Bodenheim 12908 (US);
Hurlimann 1331 (US).
Austrobuxus horneanus (A. C. Smith) Airy Shaw. Leaf:
A. C. Smith 6669 (US). Wood: A. C. Smith 6872,
Aw 28453 (= USw 30522), (A, US).
Austrobuxus huerlimannii Airy Shaw. Leaf: McKee 4850
(K).
Austrobuxus lugubris Airy Shaw. Leaf: McKee 25773
(K).
Austrobuxus montanus (Ridl.) Airy Shaw. Leaf: Wray &
Robinson 5424 (K).
Austrobuxus nitidus Miq. Leaf: Chew & Corner RSNB
4107 (US); Chew & Corner RSNB 4608 (US). Wood:
FPAw DFP 30239; PRFw 21393 (SAR);PRFw 21395
(SAR); Si Boecca 7983, USw 29100 (MICH); Sy-
Volume 81, Number 2
1994
mington s.n., Uw 21411 (= KEPw 3602) (KEP); USw
30796, Uw 14635, (= SARFw 13234) (SAR).
Austrobuxus ovalis Airy Shaw. Leaf: McKee 26894 (K).
Austrobuxus paucifiorus Airy Shaw. Leaf: BaumannBodenheim 14113 (K); McPherson 3935 (MO).Wood:
McPherson 3923 (MO);McPherson 3935 (MO);McPherson 4603 (MO).
Austrobuxus rubiginosus (Guillaum.) Airy Shaw. Leaf:
Baumann-Bodenheim 15010 (US); Hurlimann 1486
(US).
Austrobuxus swainii (de Beuzev. & C. T. White) Airy
Shaw. Leaf: Boorman s. n. (NSW); Hewitt s. n. (NSW);
Johnson & Constable s.n. (NSW). Wood: de Beuzeville s.n., MADw 10449 (= FPAw DFP 8606).
Austrobuxus vieillardii (Guillaum.) Airy Shaw. Leaf:
Schmid 2514 (K). Wood: McKee 25222, FPAw DFP
33881 (K).
Austrobuxus sp. Leaf: University of California, Davis
Greenhouse B73.173. Wood: Hyland 6918 (DAV);
Webster & Hyland 18927 (DAV).
Celaenodendronmexicanum Standley. Leaf: Ortega 4962
(US); Ortega 6367 (US). Wood: Ortega 35, USw 3886
(= Aw 4494, MADw 29901, MAD-SJRw 1200); Ortega 6367 (US); Uw 21735 (= Aw 30657).
Choriceras tricorne (Benth.) Airy Shaw. Leaf: Forman
s.n. (LAE, US). Wood: Pullen 7135, MADw 29097,
FPAw-Pullen 7135 (A, CANB, K, L, LAE).
Dissiliaria baloghioides F. v. Muell. Leaf: Bailey s.n.
(US); Francis & White s.n. (US). Wood: Bailey's
Queensland Woods 366, Aw 26736; PRFw 28015;
USw 32037, Uw 14625 (= FPAw DFP 3127).
Hyaenanche globosa (Gaertn.) Lam. Leaf: Bayliss BSBRI 576 (US); Godfrey SH-1257 (US); Werderman
& Oberdieck 528 (US). Wood: Bohmer & Verdoucq
s.n. (PRE); Botanical Research Institute Pretoria s.n.
(PRE); Werderman & Oberdieck 528 (US).
Kairothamnus phyllanthoides (Airy Shaw) Airy Shaw.
Leaf: Johns NGF 47324 (K); Streimann NGF 45108
(K).
Longetia buxoides (Baill.) Airy Shaw. Leaf: BaumannBodenheim 5605 (US). Wood: Baumann-Bodenheim
5605 (US).
Micrantheum demissum F. v. Muell. Leaf: Hunt 2802
(US). Woody twig: Hunt 2802 (US).
Micrantheum ericoides Desf. Leaf: Hotchkiss 428 (US);
Johnson & Constable 19095 (US). Woody twig: Cambage 495 (NSW).
Micrantheum hexandrum Hook. f. Leaf: Boorman s.n.
(US); McGillivray 3196 (DAV); Schodde 1177 (US).
Woody twig: Boorman s.n. (US); Whaite & Whaite
3536 (NSW).
Mischodon zeylanicus Thwaites. Leaf: Ripley 05 (US);
Wheeler 12079 (US). Wood: Jayasuriya 2434 (PDA);
Wheeler 12079 (US).
Neoroepera banksii Benth. Leaf: Banks & Solander s. n.
(US). Woody twig: Horner & Taylor s.n. (NSW).
Neoroepera buxifolia White. Leaf: White 12095 (US).
Woody twig: White 12095 (US).
Oldfieldia africana Benth. & Hook. f. Leaf: Cooper 88
(K, MAD, US); Cooper 439 (US). Wood: Commercial
sample, USw 19900; Cooper 88, USw 4517, Uw
14636 (= Aw 16930, MADw 30131, MAD-SJRw
13738) (K, MAD, US); Cooper 111, USw 4538, (=
Aw 16931, MADw 30132, MAD-SJRw 13761) (K,
MAD); Cooper 295, USw 4882, (= Aw 16932, MADSJRw 15207) (MAD).
Oldfieldia dactylophylla (Weiw. ex Oliv.)L6onard.Wood:
Hayden
Euphorbiaceae Subfamily Oldfieldioideae
201
Cons. For. Tanganyika Territory 254, Uw 10951
(PRFw 13495).
Oldfieldia macrocarpa L6onard. Wood: Dechamps
(Comite Nat. du Kivu) s.n., TERVw 1605 (BR).
Oldfieldia somalensis (Chiov.) Milne-Redhead.Leaf: Perdue & Kibuwa 10005 (NA). Wood: Schlieben 6371
(wood no. 558), Uw 15635 (= MAD-SJRw 34030).
Oldfieldia sp. Wood: Dechamps 330, TERVw 7522;
Dechamps 335, TERVw 7527; Dechamps 655,
TERVw 8499 (BR).
Parodiodendron marginivillosum (Speg.) Hunziker.Leaf:
Hueck 469 (US). Wood: Vervoorst & Cuezzo 7.610C
(LIL).
Petalostigma banksii Britten & S. Moore. Leaf: Perry
1981 (US); Perry 3531 (US); Perry 3562 (US). Wood:
Doherty s.n., USw 21280.
Petalostigma "glabrescens" (probably referable to P.
pubescens or P. triloculare). Leaf: Clemens 42580
(US); Wilson 679 (US). Wood: SFCw R 594-2.
Petalostigma pubescens Domin. Leaf: White 12421 (US).
Wood: SFCw R 594-3; SFCw R 977-256; White s.n.,
PRFw 17591.
Petalostigma quadriloculare F. v. Muell. Leaf: Clemens
42561 (US); Lazarides 6669 (US). Wood: PRFw 2921;
PRFw 24259, (= Uw 10949); PRFw 10913, (= Uw
10948); Webster & Hyland 18879 (DAV).
Piranhea longepedunculata Jablonski. Leaf: Breteler
4969 (US). Wood: Breteler 4970, MAD-SJRw55650,
(= Uw 12254) (MER, US); Breteler 5096, USw 35682,
( Uw 12306, MAD-SJRw 55702) (MER, NY, U,
US, WAG).
Piranhea trifoliata Baill. Leaf: Krukoff5924 (US); Steyermark 86615 (US). Wood: Capucho 493, USw 22377
( Aw 4526, MADw 30166, MAD-SJRw 23457) (F,
IAN); Ducke s.n., USw 31485 (MAD); Krukoff 6163,
USw 7524 (US).
Podocalyx loranthoides Klotzsch. Leaf: Bernardi 1675
(NY); Froes 21543 (NY); Krukoff 811 (NY); Williams
14480 (US). Wood: Wurdack & Adderley 42795,
MADw 22429 (= MAD-SJRw 54246) (NY, US).
Pseudanthus divaricatissimus (Muell. Arg.) Benth. Leaf:
Constable 53354 (US); Ingram s.n. (NSW). Woody
twig: Constable 53354 (US); Ingram s.n. (NSW).
Pseudanthus orientalis F. v. Muell. Leaf: Clemens
44092 (US); Wilson 639 (US). Woody twig: Clemens
44092 (US).
Pseudanthus ovalifolius F. v. Muell. Leaf: Beauglehole
& Orchards 30452 (NSW); Muir 906 (US). Woody
twig: Beauglehole & Orchards 30452 (NSW); Muir
906 (US).
Pseudanthus pimelioides Sieb. ex Spreng. Leaf: Boorman s.n. (US); Clemens 42750 (US). Woody twig:
Boorman s.n. (US); Clemens 42750 (US); Constable
NSW 55972 (NSW).
Scagea depauperata (Baill.) McPherson. Leaf: Franc
1642a (US).
Scagea oligostemon (Guillaum.)Airy Shaw. Leaf: Guillaumin & Baumann-Bodenheim 11808 (US); McKee
2352 (US); McKee 2651 (US).
Stachyandra merana (Airy Shaw) A. Radcliffe-Smith.
Leaf: Baron 6431 (K); Capuron 23335-5F (K).
Stachyandra viticifolia (Airy Shaw) A. Radcliffe-Smith.
Leaf: Capuron 20975 SF (K). Wood: Capuron
1914.R.4, CTFw 9069 (TAN).
Stachyandra sp. Wood: Belin 218.R.6, CTFw 13786
(TAN).
202
Annals of the
Missouri Botanical Garden
ou (1940); Heimsch (1942); MC; Bamber (1974); Rao
& Raju (1985).
CelaenodendronStandley. Record(1928); Record (1938);
Record & Hess (1943); Hayden (1977).
Croizatia Steyerm. Levin (1986).
Dissiliaria F. Mueller.MC;Dehay (1935); Bamber(1974);
Rao & Raju (1985).
Hyaenanche Lambert & Vahl. Pax (1884); G; S; Dehay
(1935); Assailly (1954).
Longetia Baillon. Much publishedanatomical information
on "Longetia" pertains to Austrobuxus nitidus (=
Longetia malayana); there appears to be no previous
anatomical study of Longetia buxoides (Baill.) Airy
Shaw.
Micrantheum Desfontaines. Pax (1884); G; S; MC; Rao
& Raju (1985).
Mischodon Thwaites. G; Gamble(1922); Heimsch (1942);
MC; Raju (1984); Rao & Raju (1985).
Neoroepera Mueller Arg. Rothdauscher (1896).
Oldfieldia Bentham. Stone (1904); MC; Assailly (1954);
Lebacq & Dechamps (1964); Bolza & Keating (1972);
Hayden (1977); Rao & Raju (1985).
Paradrypetes Kuhlm. Milanez (1935); Araujo & Mattos
Filho (1984); Levin (1986); Mennega (1987).
Petalostigma F. Mueller. Froembling (1896); Rothdauscher (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
(1989).
Androstachys Prain. Anonymous (1909); MC; Bolza &
Pseudanthus Sieber ex Sprengel. Pax (1884); G; S; Rao
Keating (1972); Rao & Raju (1985); Alvin (1987);
& Raju (1985).
Alvin & Rao (1987); Dahlgren & van Wyk (1988).
Stachystemon Planchon. Pax (1884); G; MC.
Austrobuxus Miquel (often reported as "Longetia," see
below). Rothdauscher(1896); G; Dehay (1935); Math- Tetracoccus Engelman ex Parry. Heimsch (1942); MC.
Stachystemon axillaris George. Leaf: Blackwell & Grif
fin 3132 (PERTH).
Stachystemon brachyphyllus Muell. Arg. Leaf: George
12928 (PERTH).
Stachystemon polyandrus (F. Muell.) Benth. Leaf: Hnatiuk 761262 (PERTH).
Stachystemon vermiculare Planch. Leaf:Pritzel s. n. (US);
Royce 5207 (PERTH).
Tetracoccus dioicus Parry. Leaf: Moran 13170 (US);
Terrell & Gordon 4004 (US); Webster & Hildreth
7478 (DAV). Wood: Campbell 21484 (RSA).
Tetracoccus fasciculatus (Wats.) Croizat var. fasciculatus. Leaf: Johnston 7783 (GH, US); Webster,21221
(DAV). Wood: Johnston 7783, Aw 23748 (GH, US).
Tetracoccus fasciculatus (Wats.) Croizat var. hallii
(Brandegee) Dressler. Leaf: Webster & Hildreth 7460
(DAV); Wiggins 6617 (US). Wood: Webster & Hildreth 7460 (DAV).
Tetracoccus ilicifolius Coville & Gilman. Leaf: Gilman
s.n. (US); Gilman 2181 (US). Wood: Gilman 2181
(US).
Voatamalo eugenioides Capuron ex Bosser. Wood: SF
198 R 259, (= CTFT 13816, Uw 23104); SF 5327
R 4 (= CTFT 15079, Uw 23105).
Whyanbeelia terrae-reginae Airy Shaw & Hyland. Leaf:
Irvine 1399 (K). Wood: Hyland 7945 (K).