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775
Int. J. Plant Sci. 164(5):775–792. 2003.
䉷2003 by The University of Chicago. All rights reserved.
1058-5893/2003/16405-0011$15.00
COMPARATIVE MORPHOLOGY AND SYSTEMATIC POSITION OF
AVERRHOIDIUM WITHIN SAPINDACEAE
Caroline S. Weckerle
1
and Rolf Rutishauser
Institute of Systematic Botany, University of Zurich, Zollikerstrasse 107, 8008 Zurich, Switzerland
The Neotropical genus Averrhoidium (Sapindaceae) is classified in Doratoxyleae (Radlkofer 1934) and
comprises four species with disjunct distribution: Averrhoidium dalyi is found in east Peru and northwest
Brazil, Averrhoidium gardnerianum in east Brazil, Averrhoidium paraguaiense in Paraguay, and Averrhoidium
spondioides in west Mexico. All species are dioecious subcanopy trees. Here we present for the first time
observations on living material and detailed morphological and anatomical data of leaves, flowers,and dehisced
fruits of A. dalyi. This information contributes to a more complete circumscription of the genus Averrhoidium.
The type of seed presentation observed for Averrhoidium is found to be unique and remarkable forSapindaceae:
the one-seeded capsules dehisce, allowing the placenta and parts of the septa to turn outward like a tongue,
while the single seed, with a conspicuous white sarcotesta, is still fixed to the placenta. It is dangling between
neighboring undehisced red capsules and presumably attracts birds. Comparison of the structural features of
the four Averrhoidium species shows that they are morphologically closely related, differing only in leaf
characters (size, leaflet number, margin, secondary vein number, anatomy) and in their distribution area. A
cladistic analysis of morphological data derived from literature and herbarium specimens confirms the position
of Averrhoidium within Dodonaeoideae-Doratoxyleae as proposed by Radlkofer (1934). However, Doratox-
yleae sensu Radlkofer (1934) appear to be paraphyletic, including two sapindoid taxa.
Keywords: Sapindaceae, Averrhoidium, flower and fruit morphology, cladistics.
Introduction
The Neotropical genus Averrhoidium Baill. comprises four
species with a disjunct distribution: Averrhoidium dalyi Acev.-
Rodr. & Ferrucci, recently found in east Peru and northwest
Brazil (Acevedo-Rodrı´guez and Ferrucci 2002); Averrhoidium
gardnerianum Baill., confined to east Brazil (Baillon 1874);
Averrhoidium paraguaiense Radlk., confined to Paraguay
(Radlkofer 1910; Ferrucci 1991); and Averrhoidium spon-
dioides (Standley) Acev.-Rodr. & Ferrucci, confined to west
Mexico (Acevedo-Rodrı´guez 1998). All species seem to be di-
oecious subcanopy trees, occurring in low land terra firme and
seasonally inundated forests as well as in submontane forests
(Reynel and Leon 1989; Ferrucci 1991; C. S. Weckerle, per-
sonal observation). Most species are not well known. Aver-
rhoidium paraguaiense is the only species for which flowering
specimens of female and male individuals as well as fruiting
specimens have been collected. Averrhoidium dalyi,A. gard-
nerianum, and A. spondioides are known only from a few
herbarium specimens of female individuals (flowering or fruit-
ing). The available literature is restricted to the protologues
(Baillon 1874; Radlkofer 1910; Standley 1927; Acevedo-
Rodrı´guez and Ferrucci 2002) and the morphological descrip-
tions of A. gardnerianum and A. paraguaiense in Radlkofer’s
(1934) monograph of Sapindaceae and that of A. paraguaiense
in Ferrucci (1991). In these treatments, the fruits of Aver-
1
Author for correspondence; telephone 41-1-634-84-38; fax 41-1-
634-84-03; e-mail weckerle@systbot.unizh.ch.
Manuscript received October 2002; revised manuscript received May 2003.
rhoidium are described as indehiscent, tardily dehiscent, or
irregularly dehiscent.
Previous studies of Averrhoidium were based on Radlkofer’s
(1933, 1934) classification in his monograph of Sapindaceae,
which is based on gynoecium and fruit characters. The two
subfamilies, which are still widely accepted (Klaassen 1999;
Savolainen et al. 2000b), are distinguished by ovule number:
Sapindoideae (105 genera) are characterized by one ovule per
locule and Dodonaeoideae (34 genera) by two or, rarely, more
ovules per locule. Ca. 30 genera of Sapindoideae and eight of
Dodonaeoideae occur in the Neotropics. The nine tribes of
Sapindoideae are distinguished by fruit, flower, leaf, and habit
characters and the five tribes of Dodonaeoideae by fruit, flower,
and leaf characters. Because of the two ovules per locule and
the supposed indehiscence of the fruits, Radlkofer (1934)
placed Averrhoidium in the tribe Doratoxyleae of the subfam-
ily Dodonaeoideae. This tribe comprises nine genera, each con-
taining very few species. They are scattered around the world;
four occur in the Neotropics, four in Africa and/or Madagas-
car, and one mainly in southeast Asia and Australia.
For a long time, systematists have dealt with the question
of whether the mainly temperate Aceraceae and Hippocasta-
naceae should be included in Sapindaceae. Radlkofer (1934)
treated them as separate families but described them as very
closely related to Sapindaceae and his decision therefore a
“matter of taste” (Radlkofer 1890, p. 108). Similar opinions
are found in several evolutionary classifications (Takhtajan
1959, 1980, 1997; Cronquist 1968, 1981, 1988; Thorne 1976,
1983, 1992b; Dahlgren 1980, 1983). However, in his most
776 INTERNATIONAL JOURNAL OF PLANT SCIENCES
Fig. 1 Averrhoidium dalyi. Stem, leaf, and inflorescence. Photographs by C. S. Weckerle. A, Stem of a ca. 25-m-tall tree with 0.5 m dbh.
m. B, Bark, shed in irregular plates. m. C, Uppermost lateral leaflets with entire (e) or slightly serrate (s) margin. ArrowheadBar p0.5 Bar p0.1
points to aborted rachis apex. cm. D, Shoot with female inflorescence in leaf axil. cm.Bar p2 Bar p1
recent classifications, Thorne (1992a, 2000) includes Acera-
ceae and Hippocastanaceae as subfamilies in Sapindaceae.
Muller and Leenhouts (1976) compared all sapindaceous
taxa using pollen and floral characters, which resulted in the
acceptance of the circumscription of the two subfamilies pro-
posed by Radlkofer (1933, 1934). They regarded Aceraceae
and Hippocastanaceae as closely allied to Sapindaceae and
suggested their inclusion into Dodonaeoideae.
In their phylogenetic analyses based on morphological data
of selected taxa (19 genera, 27 characters) from Sapindaceae,
Aceraceae, and Hippocastanaceae, Judd et al. (1994) conclude
that Sapindaceae are paraphyletic with Aceraceae and Hip-
pocastanaceae nested within them. Sapindoideae plus Acera-
ceae form a monophyletic group, Dodonaeoideae and Hip-
pocastanaceae form one clade, and Hypelate is cladistically
basal and sister to the rest.
In recent molecular studies, Aceraceae and Hippocastana-
ceae are sister to Sapindaceae (Gadek et al. 1996; Savolainen
et al. 2000a, 2000b; Soltis et al. 2000). In the study by Sa-
volainen et al. (2000b), on the basis of rbcL sequences, Do-
donaeoideae (three taxa sampled) is paraphyletic with respect
to Sapindoideae (four taxa sampled). In the other studies
(Gadek et al. 1996; Savolainen et al. 2000a; Soltis et al. 2000),
only few sapindaceous taxa were sampled, and therefore noth-
ing can be said about the infrafamilial classification.
The aim of this study is to examine the morphology and
anatomy of fruits, flowers, and leaves of Averrhoidium and to
compare the four species currently described. To elucidate the
position of Averrhoidium within Sapindaceae, we conducted
a cladistic analysis based on our own observations of mor-
phological characters and data from the literature. Relying on
the recent molecular analysis mentioned above, we chose Acer
and Aesculus as outgroups. Xanthoceras, basal in two molec-
ular analyses (Savolainen et al. 2000b; Soltis et al. 2000), was
not considered for this study because of its aberrant gynoecium
characters for Sapindaceae s.l.
Material and Methods
Morphological and Anatomical Investigations
of Averrhoidium
Morphological studies were carried out on living and fixed
(70% EtOH) material of Averrhoidium dalyi Acev.-Rodr. &
Ferrucci as well as herbarium specimens of Averrhoidium gard-
nerianum Baill., Averrhoidium paraguaiense Radlk., and Av-
errhoidium spondioides (Standley) Acev.-Rodr. & Ferrucci.
Leaf terminology of morphological characters follows Hickey
(1973). The following specimens or photographs of specimens
were examined: A. dalyi, Daly et al. 7531, W Brasil, US (fr);
A. dalyi, Mitchel 2587, Peru, MOL (fr); A. dalyi, Silveira 494,
W Brasil, US (fr); A. dalyi, Weckerle & Igersheim 000318–1/
1 and 010127–1/1, Peru, eastern Andean slopes of the de-
partment Pasco, in an old coffee plantation with remnants of
the primary vegetation as shading trees, 1550 m, Z, MOL
(female fl, fr); A. gardnerianum, do Cavalo 945, E Brasil, US
(male fl); A. gardnerianum, Davidse & D’Arcy 11674, E Brazil,
SP (photograph) (fr); A. gardnerianum, Gardner 1260, E Bra-
zil, W, SP (photograph) (female fl); A. gardnerianum, Lyra-
Lemos & Esteves 1811, E Brazil, SPF (photograph) (fr); A.
gardnerianum, de Queiroz et al. 3056, E Brazil, SPF (photo-
graph) (female fl); A. paraguaiense, Bernardi 19100, Paraguay,
WECKERLE & RUTISHAUSER—SYSTEMATICS OF AVERRHOIDIUM 777
Fig. 2 Averrhoidium spp. Transverse sections of leaflets (lamina, midrib). A,B,Averrhoidium dalyi.C,D,Averrhoidium gardnerianum.E,
F,Averrhoidium paraguaiense.A,C,E, Transverse sections of the lamina. Arrowheads indicate mucilaginous cells. B,D,F, Transverse sections
of the midrib (polarized light), with sclerenchyma sheath (ss) and rhomboidal crystals (rc). mm.Bar p0.1
Z (fr); A. paraguaiense, Ferrucci, Schinini & Dematteis 1353,
Paraguay, SPF (photograph) (fr); A. paraguaiense, Hassler
10648, Paraguay, M, US (male fl); A. paraguaiense, Hatsch-
bach & Cervi 52413, S Brasil, US (male fr); A. spondioides,
Lott, Rothschild & Upson 3803, Mexico, US (fr); A. spon-
dioides, Acevedo & Martinez 956, Mexico, US (fr). Illustra-
tions were prepared from the following collections: Weckerle
& Igersheim 010127–1/1 (fig. 1; fig. 2A,2B; figs. 3, 4, 5A–
5E, 6–8) and Weckerle & Igersheim 000318–1/1 (fig. 9); Gard-
ner 1260 (fig. 2C,2D); Hassler 10648 (fig. 5F,5G); Bernardi
19100 (fig. 2E,2F).
For microtome sections, the dehydrated samples were em-
bedded in 2-hydroxyethyl methacrylate (KULZER’s Technovit
7100) and cut at 3–5 mm with a rotary microtome. For detailed
description, see Igersheim (1993) and Igersheim and Cichocki
(1996). Mucilaginous secretions of pectic nature were identi-
fied with ruthenium red (Gerlach 1984); for contrast enhance-
ment, ruthenium red staining was poststained with toluidine
blue (Weber and Igersheim 1994).
For scanning electron microscopy, the specimens were
sputter-coated with gold. The micrographs were taken with a
Hitachi S4000 scanning electron microscope at 20 kV. All light
microscope micrographs were prepared with an Olympus
BX50 microscope and a PM10 ADS camera system and Agfa
Pan 25.
Cladistic Analysis of Averrhoidium
The relationships of Averrhoidium were investigated with a
cladistic analysis of 21 terminals. Reference genera were cho-
sen (table 1) on the basis of the classification systems of Radl-
kofer (1933, 1934) and Judd et al. (2002). Representatives of
all five tribes of Dodonaeoideae (including all genera of Do-
ratoxyleae) and selected tribes of Sapindoideae were used. In-
stead of genera, type species were coded for the analysis as
terminals. For Averrhoidium,A. dalyi was used as terminal
instead of the type species. On the basis of results from mo-
lecular analyses (Gadek et al. 1996; Savolainen et al. 2000b),
Aesculus and Acer were chosen as outgroup.
Overall, 34 morphological and anatomical characters from
778 INTERNATIONAL JOURNAL OF PLANT SCIENCES
Fig. 3 Averrhoidium dalyi. Leaf epidermis. A, Adaxial epidermis
with polygonal cells. B, Abaxial epidermis with anomocytic stomata.
mm.Bars p20
Fig. 4 Averrhoidium dalyi. Female flowers and their aestivation.
A, Young partial inflorescence with bract seen from the side. B, Female
anthetic flower from the side. Base of gynoecium and stamens sur-
rounded by nectar disk (d). C, Anthetic flower from above with re-
moved gynoecium and stamina, showing continuous transition from
sepals (1–5) to petals (6,7). D, Same flower from below.E,F, Diagrams
of two female flowers, with trilocular ovary and eight staminodes.
Note quincuncial aestivation of perianth. Innermost members (black)
are viewed as petals. mm.Bar p2
habit, leaves, flowers, and fruits were coded (tables 2, 3). Most
of the characters are based on the descriptions by Radlkofer
(1933, 1934), Capuron (1969), Reynolds and West (1985),
Adema et al. (1994), and Davies and Verdcourt (1998) and
were verified using herbarium specimens (table 4). The mor-
phological data set of 19 sapindaceous genera, compiled by
Judd et al. (1994), was chosen as the working basis for our
data matrix. Autapomorphies were excluded, the scoring of
other characters was modified in many cases, and 15 new
characters were added. All characters were equally weighted
and treated as unordered.
The cladistic analysis was conducted using the branch-and-
bound algorithm as implemented in PAUP (version 4.0b8a;
Swofford 2001) and standard search options. Bootstrap values
and decay indices were estimated for different clades. Boot-
strap analysis was based on 1000 replicates, and decay indices
were determined with inverse constraint analysis. MacClade,
version 4.0 (Maddison and Maddison 2000), was used to de-
termine character transitions and to check alternative topol-
ogies with Acctran option.
Results
Morphology and Anatomy of Averrhoidium dalyi
Habit, stems, and leaves (fig. 1).Averrhoidium dalyi is a
15–25-m-tall subcanopy tree with up to 0.5 m dbh. The bark
is dark brown to grayish brown and shed in irregular plates.
The stems are grayish brown, terete, glabrescent, and minutely
lenticellate at maturity. The leaves, up to 22 cm long, are al-
ternate and pinnately compound. An aborted rachis apex is
always present. The eight to 10 chartaceous leaflets are op-
positely to alternately arranged. They are elliptic or slightly
asymmetrical, 5.5–8 cm long and 1.6–3 cm wide. The leaflet
margin is entire, slightly undulate, or serrate.
Leaflet surface and anatomy (figs. 2, 3). The leaflets are
mostly glabrous on both sides except for the puberulent mid-
vein but might be sparsely puberulent on the abaxial surface.
The indument consists of solitary unicellular hairs.
The epidermal cells are polygonal, with straight to undulate
walls. The stomata, confined to the abaxial side, are anomo-
cytic and up to 20 mm long.
Blade anatomy is dorsiventral. The epidermal cells are
square to flat-rectangular, larger on the adaxial surface, and
usually erect over the midrib and along the margin of the
leaflet. Mucilaginous cells occur in the adaxial and abaxial
epidermis. The palisade tissue is composed of one to two (sel-
dom three) layers of elongate cells; the spongy tissue is rather
compact. The midrib is raised strongly on the abaxial side and
slightly on the adaxial side. A sclerenchyma sheath is present
around the vascular system. Rhomboidal oxalate crystals occur
around the veins. No secretory cells were observed.
Inflorescences (figs. 1, 4). Thyrses arise in the axils of the
leaves of young branchlets and are 8–11 cm long (shorter than
the leaves). They consist of six to 10 partial inflorescences with
few flowers each. Cincinni with three or two flowers or some-
times reduced to one flower occur. The axes are slender, terete,
Fig. 5 Averrhoidium dalyi and Averrhoidium paraguaiense. Floral structures. SEM micrographs.A–E,Averrhoidium dalyi.F,G,Averrhoidium
paraguaiense.A, Female flower during anthesis with staminodes surrounded by a glabrous nectary disk (d); note gynoecium with an oblique
style. mm. B, Fused and twisted stigma branches. mm. C, Close-up of unicellular papillae of the stigma. mm.Bar p1.5 Bar p500 Bar p50
D, Ventral view of staminode of female flower. mm. E, Close-up of disk with basal portion of staminode. mm. F, MaleBar p300 Bar p250
flower from above with prominent filaments and rudimentary gynoecium. Note prominent nectary disk. mm. G, Close-up of rudimentaryBar p1
gynoecium. mm.Bar p200
780 INTERNATIONAL JOURNAL OF PLANT SCIENCES
Fig. 6 Averrhoidium dalyi. Schematic drawing of median longitudinal section of anthetic gynoecium. Levels A–Kcorrespond to the transverse
sections. Morphological surfaces drawn with uninterrupted line; outline of free parts outside the median plane drawn with dotted lines. Mucilage
of pollen tube transmitting tract shaded in gray. A–K, Transverse section series of anthetic gynoecium. Vascular bundles indicated with thin
lines. Mucilage of pollen tube transmitting tract shaded in gray. A, Stigma. B, Style. C–E, Symplicate zone. F–J, Synascidiate zone. F–H, Ovary
at level of ovule insertion. K, Below ovarial cavity. mm for all transverse sections.Bar p1
slightly striate, and puberulent. The bracts are subulate, pu-
berulent, and deciduous.
Flowers (figs. 4, 5). The species of the genus Averrhoidium
produce female flowers with a reduced androecium and male
flowers with a reduced gynoecium. For A. dalyi, only female
flowers could be examined. The observations on male flowers
are based on the flowers of Averrhoidium paraguaiense.
The female flowers are actinomorphic, 4–5 mm long, 4–5
mm wide, greenish to whitish, and scentless. The pentamerous
calyx is persistent. The outer three sepals are smaller, up to
WECKERLE & RUTISHAUSER—SYSTEMATICS OF AVERRHOIDIUM 781
Fig. 7 Averrhoidium dalyi. Ovules. SEM micrographs. A, Abaxial view of ovule pair showing nucellus (n), inner integument (ii) and outer
integument (oi) of upper ovule, and median region of concave side of ovule (m). mm. B, Adaxial view of ovule pair. Note rudimentaryBar p200
aril (ra) of upper ovule. mm. C, Adaxial view of upper ovule. Note rudimentary aril (ra). mm. D, Abaxial view of upperBar p200 Bar p150
ovule. Note median region of concave side of ovule (m). mm. E, Close-up of median region. mm. F, Abaxial view of lowerBar p150 Bar p50
ovule with micropyle adjacent to insertion area. mm.Bar p150
1.3 mm long, 1.5–1.8 mm wide, and greenish; the inner two
are up to 1.8 mm long, 2.0–2.2 mm wide, and more whitish.
Minute unicellular hairs occur on the outer surface and along
the margin of the sepals, whereas the inside surface is glabrous.
Aestivation of the sepals in bud is quincuncial.
A continuous gradation from sepals to petals exists. One or
two (rarely three or four) petals are developed. These are whit-
ish, 2 mm long, up to 1.4 mm wide, and glabrous. Anatom-
ically the petals differ from the sepals chiefly by more papillate
adaxial epidermal cells and fewer chlorenchymatic cells.
In the female flowers, the eight (seldom seven) stamens have
short, up to 0.3 mm long, glabrous filaments and sterile an-
thers. The anthers are ca. 0.7 mm long, hooded, glabrous,
introrse, and basifixed. For the male flowers, much longer fil-
aments are expected, as observed for A. paraguaiense.
The stamens and the base of the gynoecium are surrounded
by a regular, glabrous nectary disk, which is slightly raised
between the stamens. The nectary disk is persistent and is still
visible at the base of the mature fruits.
Gynoecium (figs. 5–8). The syncarpous, tricarpellate, su-
perior ovary is spherical to triangular, up to 2 mm long and
wide, with short unicellular hairs at the base and the edges.
Three stigmas arise from a short style. They are twisted around
each other and postgenitally united even during anthesis. The
three sutures are unicellular papillate. In bud stage, the style
is bent downward, and during anthesis, it is suberect. The inner
canal from the stigma down to the ovary has a large inner
surface but a small lumen and is filled with mucilaginous se-
cretion. The carpels are synascidiate up to the upper third of
the ovary and symplicate up to the stigmas, which are asym-
782 INTERNATIONAL JOURNAL OF PLANT SCIENCES
Fig. 8 Averrhoidium dalyi. Longitudinal and transverse sections of ovules in anthetic flowers. A–E, Longitudinal section series of one locule
of ovary. Vascular bundles indicated with thin lines; mucilage of pollen tube transmitting tract shaded in gray. A,B, Sections through nucellus
(n), median region of concave side of ovule (m), and inner (ii) and outer integument (oi) of upper ovule. C, Insertion of upper ovule with
rudimentary aril (ra) and pollen tube transmitting tissue (pt). D,E, Insertion of lower ovule. F, Median longitudinal section of upper ovule
showing median region (m) and rudimentary aril (ra). G–I, Transverse section series of one locule of ovary. Vascular bundles indicated with
thin lines. G, Upper ovule. H, Insertion area of both ovules. I, Lower ovules. mm.Bars p250
plicate. The ovary wall is provided with several minor vascular
bundles, which occur between the major dorsal bundles of the
three carpels. Few oxalate crystals are found in the paren-
chymatous tissue. The three locules are more or less filled by
the ovules. Two ovules per locule occur, born on the axile
placenta. They are superposed and fixed more or less at the
same level in the upper half of the locule. The ovules are cam-
pylotropous, crassinucellar, and bitegmic. A rudimentary aril
exists around the short funicle of the upper ovule. The micro-
pyle of the lower ovule is formed by the annular outer integ-
ument, whereas in the upper ovule, the semiannular outer in-
tegument does not cover the nucellus apex. The vascular
bundle that serves the ovules ends in the chalaza.
Fruits and seeds (fig. 9). The red, elliptical to subglobose
capsules are up to 1.7 cm long and up to 1.4 cm wide. They
are slightly asymmetrical because usually only one seed is de-
veloped. The pericarp is coriaceous, glabrous, and ca. 1 mm
thick with three furrows, corresponding to the dorsal dehis-
cence lines of the locules. Only one (seldom two) of the six
ovules develop to a mature seed; the aborted ovules are still
detectable in the mature fruit. During development, the pro-
longed septa are pressed toward the pericarp, pushing aside
the two sterile locules. The seed and the aborted ovules are
fixed in the apical portion of the capsule, and therefore the
seed becomes a pendant position. During capsule dehiscence,
the valves fall off and the seed tips down, dangling between
the not yet opened red fruits.
The epidermis of the pericarp consists of small, erect cells.
The exocarp (the tissue outside the ring of vascular bundles)
is compact. Sclerenchymatous fibers and groups of cells with
a conspicuously larger lumen occur (secretory cells?). The
mesocarp is rather spongy, and the innermost layer is made
up of elongated, thin cells.
The seeds are oblong, ovoid, and up to 1.5 cm long and 1.1
cm wide. They possess a fleshy white sarcotesta that consists
of parenchymatous, polygonal, more or less isodiametric cells.
The endotesta consists of a small-celled tissue layer. The cot-
yledons of the embryo are curved and plicate. The radicula is
situated in a “radicle pocket,” a deep fold of the testa.
WECKERLE & RUTISHAUSER—SYSTEMATICS OF AVERRHOIDIUM 783
Fig. 9 Averrhoidium dalyi. Fruit, seed, and embryo. A, Dorsal view of undehisced fruit. Level Ecorresponds to the transverse section below.
B,C, Dorsal and lateral view of fruit after removal of capsule valves. Arrowhead indicates aborted ovules. The square corresponds to F.E,
Transverse section of undehisced fruit. Arrowheads point to dehiscence lines of the three capsule valves. F, Close-up of aborted ovules of the
two rudimentary locules. D, Side view of dangling seed after dehiscence of the fruit. Arrowhead points to the aborted ovules. G,H, Abaxial
and adaxial view of the embryo with radicula (r). I, Side view of the embryo. J, Polar view of the embryo. cm for all except F, whereBar p1
mm.bar p1
Comparative Morphological Features of Averrhoidium
dalyi,Averrhoidium gardnerianum,Averrhoidium
paraguaiense, and Averrhoidium spondioides
The morphological and anatomical characters of leaves,
fruits, seeds, and flowers of the four Averrhoidium species are
listed in table 5. Differences are mainly found in leaflet and
leaf anatomical characters (see “Discussion”).
Generic Description of Averrhoidium Baill.
Tree: up to 25 m, subcanopy tree, (probably) dioecious.
Leaves: spirally arranged, no stipules, paripinnate, up to 22
cm long, rachis puberulent, up to 16 leaflets, leaflets ca. 1–11
cm long and 1–5 cm wide, elliptic to oblong, margin entire to
serrate, leaflet apex obtuse to acuminate, seven to 15 secondary
nerves, indument glabrous to sparsely puberulent, epidermis
with mucilaginous cells. Inflorescences: thyrses, 3–16 cm long.
784 INTERNATIONAL JOURNAL OF PLANT SCIENCES
Table 1
Species Included in the Cladistic Analysis
Classification Genus, number of species, and distribution Type species
Sapindaceae sensu lato:
Aceroideae Acer 111; Europe 14, N America, Asia A. pseudoplatanus L.
Hippocastanoideae Aesculus 13; SE Europe 1, India and E Asia 5, N America 7 A. hippocastanum L.
Dodonaeoideae:
Cossinieae Cossinia 4; Mascarenes 1, New Caledonia 1, Fiji 1, Australia 1 C. pinnata Comm. ex Lam.
Dodonaeeae Distichostemon 6; Australia D. phyllopterus F. Muell.
Loxodiscus 1; New Caledonia L. coriaceus Hook. f.
Doratoxyleae Averrhoidium 4; Central America 1, S America 3 A. dalyi Acev.-Rodr. & Ferrucci
Doratoxylon 6; Madagascar 5, Mascarenes 1 D. apetalum (Poir.) Radlk.
Euchorium 1; Cuba E. cubense Ekman & Radlk.
Exothea 3; Florida, Central America, West Indies E. paniculata (A.L. Juss.) Durand
Filicium 3; Madagascar, Comores 2, E India 1 (pantrop ornam) F. decipiens (Wight & Arn.) Thw.
Ganophyllum 2; SE Asia and Australia 1, trop Africa 1 G. falcatum Blume
Hippobromus 1; SE Africa H. alatus (Thunb.) Ecklon & Zeyher
Hypelate 1; Antilles, Florida H. trifoliata Sw.
Zanha 3; Madagascar 1, trop Africa 2 Z. golungensis Hiern
Harpullieae Delavaya 1; SW China D. toxocarpa Franch.
Majidea 4; Madagascar 1, trop Africa 3 M. zanguebarica Kirk
Koelreuterieae Koelreuteria 3 (–7); E Asia K. paniculata Laxm.
Sapindoideae:
Nephelieae Nephelium 22; SE Asia N. lappaceum L.
Paullinieae Paullinia ca. 180; Central and S America P. pinnata L.
Serjania ca. 220; Central and S America, S United States (few) S. sinuata Schumacher
Sapindeae Sapindus 10; Central America and S United States 2, Hawaii 1, SE Asia 6, pantropic 1 S. saponaria L.
Note. Classification following Radlkofer (1934) and Judd et al. (2002); species number and distribution following Mabberley (1997) and the corresponding flora;
type species following the Index Nominum Genericorum (Farr et al. 1979) and the corresponding flora. For Averrhoidium,A. dalyi was chosen as terminal instead
of the type species A. gardnerianum.
Flowers: actinomorphic, ca. 4 mm in diameter, five greenish
sepals, zero to four whitish petals, both spirally arranged, per-
sistent extrastaminal nectary disk, male flower with eight sta-
mens and rudimentary gynoecium, female flower with eight
staminodes and trimerous ovary, three papillate stigmas
twisted around each other, three locules with two superposed
ovules each. Fruits: one- or two-seeded red capsules, asym-
metrically subglobous to obovoid, ca. 1–2.5 cm long and 0.5–
2 cm wide, seeds with white sarcotesta, pendant position in
undehisced fruit, hanging on the placenta and parts of the septa
after dehiscence.
Cladistic Analysis
The branch-and-bound search of the morphological data set
resulted in six equally parsimonious trees of 101 steps (con-
sistency index excluding uninformative , re-characters p0.50
tention ). The strict consensus of the six trees isindex p0.63
shown in figure 10. Two major clades, denoted as A and B,
were found. Clade A comprises all Doratoxyleae taxa as well
as a subclade encompassing two sapindoid taxa. Filicium is
sister to this subclade. Clade B comprises dodonaeoid taxa as
well as Paullinia and Serjania. The trees differ in the position
of Distichostemon: this taxon occurs either at the base of clade
A or at the base of clade B. Bootstrap values ≥50% and decay
values are shown on the branches. Four clades receive mod-
erate to strong support: the Paullinieae group (92% bootstrap
[BS], +6 decay value), the Cossinia group (57% BS, no decay
value), the Euchorium group (56% BS, no decay value), and
the Zanha group (56% BS, no decay value).
Discussion
Morphology and Anatomy of the Genus Averrhoidium
Leaves. Morphological and anatomical leaf characters
seem to be the only structural features that allow a distinction
of the Averrhoidium species (Radlkofer 1934; Acevedo-
Rodrı´guez and Ferrucci 2002). Averrhoidium gardnerianum
and Averrhoidium spondioides have somewhat smaller leaves
than the remaining two species. Averrhoidium paraguaiense
differs in having more leaflets and more secondary veins (16
vs. 10 and 15 vs. nine, respectively), and attenuate leafletapices
may occur. Averrhoidium dalyi often has an entire or subentire
leaflet margin, whereas the other species are serrate (A. par-
aguaiense) or coarsely serrate.
Anatomically, the leaves of A. dalyi and A. paraguaiense
differ from A. gardnerianum in the presence of a lignified scle-
renchyma sheath around the rachis vascular bundles and the
presence of rhomboidal oxalate crystals along the vascular
system. They are characterized by abundant mucilaginous epi-
dermal cells, which are mostly lacking in A. gardnerianum.
The presence or absence of a sclerenchyma sheath and muci-
laginous epidermal cells seems to be of systematic value at the
infrageneric level in Sapindaceae, often limited to certain
closely related species (Radlkofer 1890; Solereder 1899, 1908;
Metcalfe and Chalk 1950; Buijsen 1995). However, Radlkofer
(1890) did not mention these characters in Averrhoidium. The
frequency and distribution of oxalate crystals as well as the
crystal type (mainly rhomboidal to mainly druses) may vary
WECKERLE & RUTISHAUSER—SYSTEMATICS OF AVERRHOIDIUM 785
Table 2
Characters and Their States
Character State
1 Sepal number 5 (constant) (0); 4–7 (variable) (1)
2 Calyx aestivation Imbricate, including quincuncial (0); valvate (1)
3 Fusion
a
≤One-third calyx length (0); 1one-third calyx length (1)
4 Petal number 0 (0); 1–3 (1); 4 (2); 5 (3)
5 Petals
a
Flat, ovate to elliptic (0); two auricle-like basal lobes (1); scale across adaxial surface (2);
with raised marginal ridges (3)
6 Petal base
b
Clawed (0); unclawed (1)
7 Stamen number
a
(4–) 5 (0); 8 (1); 4–10 (variable) (2)
8 Stamens
a
Glabrous (0); pilose (1)
9 Anther appendages
a
Absent (0); present (1)
10 Pollen
b
Spherical to round-prolate (0); triangular-oblate (1)
11 Carpel number
a
3 (0); 2 (1); 6–8 (2)
12 Ovary
b
Sessile (0); slightly stipitate (1)
13 Stigma
b
Lobed (0); unlobed (1)
14 Style shape Curved (0); erect (1)
15 Style length (female flower) ≤One-half ovary length (0); 1one-half ovary length (1)
16 Ovules
b
1 per locule (0); 2 per locule (1)
17 Ovule insertion
a
ⳲMidlevel (0); apical (1); basal (2)
18 Flower symmetry
a
Actinomorphic (0); zygomorphic or obliquely zygomorphic (1)
19 Sex distribution Monoecious (0); dioecious (1)
20 Fruit type Dehiscent (0); indehiscent (1); schizocarpous (2)
21 Pericarp Fleshy (0); crustaceous (1); membranaceous (2); coriaceous (3)
22 Pericarp 2 Always all carpels part of pericarp (0); usually not all carpels part of pericarp (1)
23 Endocarp Coriaceous to woody (0); membranaceous (1)
24 Locules Inflated (0); not inflated (1)
25 Seed number 1 (0); 1–3 (1); 2 (2); 3 (3); 3–6 (4)
26 Seed insertion Pendant (0); not pendant (1)
27 Testa With fleshy structure (0); without fleshy structure (1)
28 Embryo shape
a
Cotyledons curved (0); fairly straight (1); spiral-like (2)
29 Phyllotaxis
b
Alternate (0); opposite (1)
30 Leaf 1
a
Pinnate (0); palmately compound or palmately lobed (1)
31 Leaf 2
b
Not paripinnate (including simple) (0); paripinnate (1)
32 2⬚venation
a
Brochidodromous (0); eucamptodromous (1); craspedodromous (2); bohlenioid (3)
33 Stipules
b
Absent (0); present (1)
34 Tendrils Absent (0); present (1)
a
Characters modified after Judd et al. (1994).
b
Characters as defined by Judd et al. (1994).
considerably and seem not to be valuable characters at species
level (van Welzen 1989; Adema 1991).
Flowers. Actinomorphic flowers with a pentamerous im-
bricate calyx and a reduced number of petals, as found in
Averrhoidium, are widespread in Sapindaceae. Actinomorphic
flowers occur in the tribes Aphanieae, Doratoxyleae, Meli-
cocceae, Nephelieae, and Schleichereae, and petals are reduced
in number or totally lacking in eight out of 14 tribes (Radlkofer
1933, 1934).
No differences in floral structures could be found among
the Averrhoidium species. However, Acevedo-Rodrı´guez and
Ferrucci (2002) mention the pubescent nectary disk as the main
distinguishing character of their newly described species A.
dalyi. In the plant material, we found that the nectary disk
was glabrous. Nevertheless, our collection (Weckerle & Iger-
sheim 000318–1/1 and 010127–1/1) is presumed to belong to
A. dalyi because of its leaf characters and its locality in east
Peru.
Gynoecium and ovules. The gynoecium of the genus Av-
errhoidium is syncarpous and trilocular, with two ovules per
locule. Style and stigma are curved and unlobed. These features
are generally found within the Sapindaceae. However, in the
tribe Doratoxyleae, five of nine taxa have a bicarpellate ovary
with a bilobed style.
Little is known about ovule characters within sapindaceous
taxa (Mauritzon 1936; Kadry 1946; Baehni and Bonner 1953;
van der Pijl 1957; Corner 1970, 1976; Batygina 1985; Ronse
Decraene et al. 2000). In Averrhoidium, ovule characters have
only been described for A. dalyi and, in the tribe Doratoxyleae,
additionally for Filicium decipiens. The ovules of A. dalyi are
campylotropous with a rudimentary aril. In F. decipiens, Gulati
and Mathur (1977) found campylotropous ovules with a nu-
cellar beak and an obturator with loosely arranged mucilag-
inous cells. Campylotropous ovules with obturator occur in
several other sapindaceous taxa, whereas a rudimentary aril
was never described. However, certain structures illustrated by
van der Pijl (1957; e.g., fig. 10) could be interpreted as a ru-
dimentary aril.
Seeds and fruits. The fruits of Averrhoidium are usually
one- and seldom two-seeded, although there are six ovules in
Table 3
Data Matrix with 34 Morphological Characters of 21 Sapindaceous Taxa
1234 5
12 3
67890123456789012345678901234
Aesculus
hippocastanum 0012/31 01110001011010030110/4110110200
Acer pseudoplatanus 00030 11000100111000220112110110300
Averrhoidium dalyi 0001 0 1101000101100101/30110000001100
Cossinia pinnata 0002 0 02000011?1101001/20104112001000
Delavaya toxocarpa 00030 110000/11101100001/30102110000200
Distichostemon
phyllopterus 1000……201? 20101100002/3010411 ?0…0100
Doratoxylon
apetalum 0000/10 12000101101101100110010001000
Euchorium cubense 00030 11000001001001 ?????????001?00
Exothea paniculata 0003 0 11000100001101100110011001000
Filicium decipiens 0003 0 10000101010100100110/2?10001000
Ganophyllum
falcatum 110/10……2000100?11100100010/2010001000
Hippobromus alatus 0003 0 11000001001001100?10 ?100011/200
Hypelate trifoliata 0003 0 1100?001111000100110010000000
Koelreuteria
paniculata 0002 2 01100000111010020104112000200
Loxodiscus coriaceus 00020 1100001101101 ?02010? 1? ?001200
Majidea zanguebarica 00020 1200 ?011011010020103/4110001000
Nephelium
lappaceum 0/10/10/10/13 0210?11011020 ?111110101001100
Paullinia pinnata 0002 2 11101010110210030111100000311
Sapindus saponaria 00031/2/30/1110?001110200201110/1110001000
Serjania sinuata 0002 2 111010?0 ?10210220113110000311
Zanha golungensis 10/110……0000101111101100010011001000
Note. Aesculus and Acer are defined as outgroup. Ellipsis indicates inapplicable character; question mark indicates state unknown. The epithet of the type species is given for all genera.
WECKERLE & RUTISHAUSER—SYSTEMATICS OF AVERRHOIDIUM 787
Table 4
Specimens Examined for the Coding of Morphological Characters
for the Cladistic Analysis
Taxa Collection data
Aesculus hippocastanum W.A. Rietmann s.n., 10.5.1930, cult. Zurich (fl)
C. Schroeter s.n., 9.5.1894, cult. Zurich (fl)
Acer pseudoplatanus I. Nielson & P. Pedersen 419, 30.5.1968, Denmark (fl)
I. Nielson & P. Pedersen 482, 8.8.1968, Denmark (fr)
Cossinia trifoliate M. Balansa 3172, (1868–1872), New Caledonia (fl, flb)
Delavaya toxocarpa A. Henry 9090B, —, China (male fl, fr)
Distichostemon sp. v. Balgooy/Byrnes 1381, 26.7.1971, Australia (fr immature)
Distichostemon phyllopterus M. Holtze s.n., 1891, Port Darwin (fr)
Doratoxylon apetalum L. Bernardi 14507, 20.10.1973, La Re´union (fr immature)
L. Bernardi 14758, 12.1974–1.1975, Mauritius (male fl)
H.J. Schlieben 10923, 15.11.1966, Mascarenes (female fl)
Exothea paniculata M. Fuertes 1312, 10.1911, St. Domingo (flb, fl)
M. Fuertes 1534, 4.1912, St. Domingo (flb, fl)
Picarda 1357, 12.1894, Haiti (flb, fl)
Filicium decipiens H.J. Schlieben 1725, 3.2.1932, O Africa (male and female fl)
Ganophyllum falcatum M. Holtze s.n., 1891, Port Darwin (male fl)
Hippobromus alatus P. MacOwau 82, —, S Africa (fr immature)
F.A. Rogers 23784, 4.1920, Transvaal (fr)
H. Rudatis 1692, 30.9.1912, S Africa (male fl)
Hypelate trifoliata M. Fuertes 45, 5.1911, St. Domingo (female fl)
Koelreuteria paniculata J. Fru¨ h s.n., 23.7.1918, cult. Zurich (male and female fl)
E. Landolt s.n., 2.8.1998, cult. Zurich (fr)
A.K. Schindler 131, 7.1907, China (male fl)
Loxodiscus coriaceus I. Franc 2417, 1.11.1929, New Caledonia (fr immature)
R. Schlechter 14973, 9.10.1902, New Caledonia (male fl)
Majidea forsteri A.J.M. Leeuwenberg 2663, 4.11.1959, W Afrika (fr)
Nephelium lappaceum A. Meebold 15389, 4.1911, Burma (fr)
V. Schiffner 54, 2.7.1894, Java (fl, flb)
Paullinia pinnata M. v. Balthazar, J. Scho¨ nenberger & J. Smedmark A154, 8.2.2000,
Madagascar, fixed material (male fl, fr)
Sapindus saponaria Broadway 3389, 7.1909, Tobago (female fl)
G. Hatschbach 60872, 10.6.1994, Bolivia (male fl)
G. Hatschbach 60955, 12.6.1994 (fr)
Serjania sinuata M. Fuertes 1361, 1911, St. Domingo (male fl)
Zanha golungensis R.P. Berhaut 1499, 4.1951, Senegal (veg)
Kersting 155, 5.1905, Togo (fr, fl)
Note. If not mentioned otherwise, the specimens are from Z/ZT. buds, ,flb pflower fl pflowers fr p
.fruits
the gynoecium. This feature is characteristic for the tribe Do-
ratoxyleae. It is unknown which of the ovules develops to a
mature seed. Parallel studies carried out in the genus Aesculus
showed that normally one but occasionally up to six seeds
may develop per fruit. The position of the ovule that develops
into a seed seems to be random, and abortion does not result
from a previous morphological degeneration of ovules or parts
of the placenta (Hardin 1955).
Averrhoidium is the only genus within Doratoxyleae known
to have a dehiscent fruit and seeds with a sarcotesta. The other
genera have a fleshy pericarp but no sarcotesta. The same fruit
opening mechanism as observed in A. dalyi (dangling white
seed fixed on the placenta and parts of the septa) is expected
for the other Averrhoidium species, which possess a very sim-
ilar fruit structure only slightly differing in size.
Dangling seeds seem to be rare in Sapindaceae, and seeds
displayed by their own placenta, as found in A. dalyi, are, to
our knowledge, not yet described for the family. Some genera
of east Asia—e.g., Guioa (van Welzen 1989), Mischocarpus
(van der Ham 1994), or Sarcopteryx (van Welzen 1994)—have
an aril with a pseudofunicle, an outgrowth, extending to the
base of the locule as a long, narrow, folded tongue (Corner
1976). After dehiscence, the seeds fall out of the capsule and
remain hanging on this pseudofunicle. The movable seeds and
the color contrast (red and white in the case of Averrhoidium)
are an extra stimulus for birds to eat them (van der Pijl 1982;
van Welzen 1998).
Systematics
In the cladistic analysis, type species were coded as repre-
sentatives for genera. This seems appropriate because most of
the selected genera comprise few species or are monotypic (ta-
ble 1). Therefore, little polymorphism is to be expected. Even
the three larger genera, Nephelium,Paullinia, and Serjania,
are quite consistent regarding the coded characters.
788 INTERNATIONAL JOURNAL OF PLANT SCIENCES
Table 5
Morphological and Anatomical Characters of Averrhoidium dalyi,Averrhoidium gardnerianum,
Averrhoidium paraguaiense, and Averrhoidium spondioides
A. dalyi A. gardnerianum A. paraguaiense A. spondioides
Leaves:
Length (cm) 5–22 4–12 6–18 6–18
Petiole (cm) 2.5–6.5 1.5–3 1.5–3.5 1–3.5
Leaflets:
Leaflets nr 4–10 4–10 8–16 8–10
Length (cm) 3–10.5 1–5 2–6 2–8
Width (cm) 1.5–4.5 0.8–2 0.8–1.8 0.8–3.5
Petiolule (mm) 2–5 Ca. 1 (subsessile) Up to 2 Up to 2
Shape Elliptic Elliptic Elliptic (less often ovate),
sometimes slightly
asymmetrical
Elliptic-oblong or elliptic,
sometimes
asymmetrical
Margin Entire, subentire, or
coarsely serrate
Coarsely serrate (less often
entire or subentire)
Serrate (less often subentire) Subentire or coarsely
serrate
Leaflet apex Acuminate (less often
acute-mucronate)
Obtuse or acute-mucronate Acuminate-mucronate,
acute, or attenuate
Obtuse, acute, or
acuminate
2⬚nerves (of uppermost leaflets) 8–10 7–9 13–15 8-10
Leaflet indument abax Sparsely puberulent to
glabrous
Sparsely puberulent Sparsely puberulent to glabrous Sparsely puberulent
Indument leaf rachis Puberulent Puberulent to densely
puberulent
Puberulent to densely
puberulent
Puberulent
Leaf anatomy:
Epidermis with mucilaginous cells Present Few mucilaginous cells Present Present
Sclerenchyma sheath around
vascular system Present Absent Present Present
Crystals around veins Present Absent Present Present
Secretory cells in mesophyll Absent Present Present Present
Fruit:
Shape Asymmetrically subglobose,
ellipsoid, or obovoid
Asymmetrically subglobose,
ellipsoid, or obovoid
Obovoid Obovoid-globose
Length (cm) 1.5–2.3 0.8–1.5 1.1–1.8 1–1.2
Width (cm) 1.2–1.9 0.6–1 0.8–1.1 Ca. 1.0
Pedicel (cm) 0.2–0.5 0.2–0.5 0.1–0.3 0.5
Fruit surface Puberulent to glabrous … Glabrous Sparsely puberulent
Seed:
Seed (often solitary) Pendant with fleshy testa Pendant with fleshy testa Pendant with fleshy testa Pendant with fleshy testa
Length (cm) Up to 1.5 0.8 1 Up to 1
Width (cm) Up to 1.1 0.7 0.6 Up to 0.7
Thyrses:
Length (cm) 9–16, simple 2.5–6 4–14 Flowers unknown
Flowers:
Nectary disk (persistent) Glabrous or pubescent (as
observed in fruits)
Glabrous Glabrous Glabrous (as observed in
fruits)
Sepals and petals (often reduced) Sepals up to 2.2, slightly
hairy; petals up to 2.0
Sepals up to 2; petals
slightly smaller
Sepals up to 2, hairy; petals
slightly smaller
Flowers unknown
Other characters:
Tree (m) 15–32 4–20 5–12 7–8
Distribution W Brazil, E Peru E Brazil Paraguay, S Brazil W Mexico
Note. Characters are based on herbarium specimens (see “Material and Methods”) and the species descriptions of Acevedo-Rodrı´guez and Ferrucci (2002) for
A. dalyi, Baillon (1874) and Radlkofer (1934) for A. gardnerianum, Radlkofer (1910) and Ferrucci (1991) for A. paraguaiense, and Standley (1927) and Acevedo-
Rodrı´guez (1998) for A. spondioides. Ellipsis indicates no information available.
In our cladistic analysis, Averrhoidium is placed at the base
of the Doratoxyleae group (clade A), despite its dehiscent fruit
with the coriaceous to crustaceous pericarp. This supports the
systematic position of the genus as proposed by Radlkofer
(1934). Averrhoidium is linked to clade A by the presence of
one seed in pendant position (fig. 9). The fleshiness of the seed
is shown to be homoplastic in Sapindaceae. Three independent
origins are indicated (two in clade A and one in clade B). To
invoke a single origin requires an additional 12 steps on the
tree.
The members of Doratoxyleae sensu Radlkofer (1934) are
restricted to clade A. They represent a paraphyletic group,
which includes two sapindoid taxa (Sapindus and Nephelium).
Clade A and clade B are characterized mainly by fruit char-
acters: clade A (Doratoxyleae group) mainly comprises inde-
hiscent taxa with a fleshy pericarp or seed structure and with
usually only one pendant seed. Clade B includes taxa with
dehiscent, inflated fruits with a membranaceous or coriaceous
pericarp and more than one seed. Both clades have represen-
tatives in America, Africa, Asia, and Australia. The members
of the dodonaeoid tribes Dodonaeeae (Loxodiscus) and Har-
pullieae (Delavaya and Majidea), respectively, are scattered
within clade B.
The sapindoid taxa are grouped in two subclades, which
WECKERLE & RUTISHAUSER—SYSTEMATICS OF AVERRHOIDIUM 789
Fig. 10 Strict consensus tree of six mp trees based on 34 morpho-
logical characters coded for 21 sapindaceous taxa (101 steps, consis-
tency , retention ). Bootstrap values ≥50%index p0.50 index p0.63
and decay indices are given on the branches. The two major clades of
the ingroup ( of the tribe Doratoxyleae mainly,Apmembers Bp
dodonaeoid taxa mainly) as well as the position of Averrhoidiumother
(gray shading) and the two sapindoid subclades (grayish open boxes)
are indicated. Important morphological characters discussed in the text
are mapped on the tree: number: one seed; seed insertion:apseed
pendant. insertion: not pendant. : with fleshy struc-
∗
apseed bptesta
ture. type: indehiscent with fleshy pericarp.
∗
cpfruit cp
with crustaceous pericarp. : inflated; seed num-indehiscent dplocules
ber: three to six seeds. : not inflated. : mem-
∗
dplocules eppericarp
branaceous. : coriaceous.
∗
eppericarp
are nested within the two major clades A and B. Paullinia
clusters robustly with Serjania. They are characterized by the
following synapomorphies: triangular to oblate pollen (char-
acter 10), one ovule per locule (character 16), basal insertion
of the ovule (character 17), not inflated locules (character 24),
a character state widespread in clade B, bohlenioid secondary
venation (character 32), and the presence of stipules (character
33) and tendrils (character 34). Koelreuteria is the sister of
Paullinia and Serjania, sharing pilose stamens (character 8)
and a lobed and erect stigma (characters 13 and 14). Paullinia
and Serjania are both Neotropical lianas (except one species),
whereas Koelreuteria is an eastern Asian tree. The other sap-
indoid clade comprises Nephelium and Sapindus. They are
characterized by the following synapomorphies: petals with
marginal ridges (Sapindus is polymorphic for this state) (char-
acter 5), pilose stamens (character 8), basal insertion of the
ovule (character 17), a fruit consisting of one and seldom up
to three carpels (character 22), and basal seed insertion (char-
acter 26). An interesting result is that Filicium is more closely
associated with the Nephelium group (Sapindoideae) than with
the other members of the Doratoxyleae group. Originally, Fil-
icium was placed in Doratoxyleae (Dodonaeoideae) (Radlkofer
1934), although it only has one ovule per locule. Muller and
Leenhouts (1976) assert that the genus does not belong to this
tribe but rather to Sapindoideae, probably Thouinieae. In ad-
dition, this cladistic analysis supports monophyletic Sapin-
daceae as circumscribed by Radlkofer (1890), Cronquist
(1988), Gadek et al. (1996), and Takhtajan (1997).
Conclusions
(1) Dangling sarcotestal seeds, displayed hanging on their
placenta as described here for Averrhoidium, is a new seed
presentation type within Sapindaceae. (2) The four species of
Averrhoidium (Averrhoidium dalyi,Averrhoidium gardner-
ianum,Averrhoidium paraguaiense, and Averrhoidium spon-
dioides) turn out to be very similar and closely related. They
only differ in leaf characters (size, leaflet number,margin, anat-
omy) and in their distribution area. (3) The cladistic analysis
of the morphological data indicates a basal position of Av-
errhoidium in Doratoxyleae. This tribe turns out to be
paraphyletic.
Acknowledgments
We thank the Instituto Nacional de Recursos Naturales
(INRENA) for permit 006-2000-INRENA-DGF-DTCF to col-
lect plants and Aurora Albengring and her family in Pusapno
for support and the possibility to work on her property. We
also thank the curators and staff of the following herbaria for
loans or assistance during study visits: M, MOL, US, W, Z/
ZT. Moreover, we thank A. Igersheim for the photographs
from SP and SPF and for his help in many aspects of the field
work; R. Nyffeler for his patient help with the cladistic anal-
ysis; and P. Acevedo-Rodrı´guez, P. K. Endress, and R. Nyffeler
for critical comments on the manuscript. This project has been
partly funded by the Marie-Louise-Splinter-Legat and the
Georges-und-Antoine-Claraz-Schenkung.
790 INTERNATIONAL JOURNAL OF PLANT SCIENCES
Appendix
Character States of Characters 1–34
1. Sepal number is scored as constant (5; state 0) or variable
(4–7; state 1).
2. Calyx aestivation is scored as imbricate (state 0) or valvate
(state 1).
3. The sepals may be free or connate to different degrees.
Because a continuous transition between free and connate
sepals exists, character 7 of Judd et al. (1994) (sepals distinct
or connate) was modified to allow a clear differentiation:
fusion ≤one-third length of calyx (state 0) and fusion 1one-
third length of calyx (state 1). For Nephelium lappaceum, four
to six sepals are reported (Adema et al. 1994), but usually a
constant number of five sepals is found. The sepals are nearly
free and imbricate to halfway connate and valvate (Adema et
al. 1994). The characters are therefore scored as polymorphic.
The same is found in Ganophyllum falcatum, but for this
taxon, the sepals are reported to be always valvate (Adema et
al. 1994). In Distichostemon phyllopterus, the number of the
sepals varies between five and seven (Reynolds and West 1985).
The sepals of Zanha golungensis vary between four and five
and are valvate or slightly imbricate and more or less halfway
united (Capuron 1969; Davies and Verdcourt 1998). In
Aesculus hippocastanum, the five sepals are united (Eichler
1878; Hardin 1957).
4. Petal number is scored as four states: absent (state 0), one
to three (state 1), four (state 2), or five (state 3). Aesculus
hippocastanum has five petals with a tendency of having four
(Hardin 1957) and is therefore scored as polymorphic. In N.
lappaceum and Doratoxylon apetalum, the petals are usually
absent but may occur with reduced number, i.e., one to three
(Adema et al. 1994; Friedmann 1997). The feature is scored
as polymorphic. For D. phyllopterus,G. falcatum, and Z.
golungensis, the petals are reported to be completely absent
(state 0) (Radlkofer 1934; Capuron 1969; Reynolds and West
1985; Adema et al. 1994; Davies and Verdcourt 1998).
5. The shape of petals is scored following characters 8 and
9 of Judd et al. (1994). However, state 3 of their character 8
(petals with a prolonged basal hornlike, digitate, or hooded
appendage) was integrated into our state 2. Sapindus saponaria
is polymorphic for petal shape. Ovate petals with marginal
ridges or auricles or scales are found (Tomlinson 1980; Adema
et al. 1994). The feature is scored as 1/2/3.
6. The petal base follows the distinctions used by Judd et
al. (1994) (their character 9) and is scored as clawed (state 0)
or unclawed (state 1).
7. Stamen number varies considerably. In D. apetalum and
N. lappaceum, four to nine; in Cossinia pinnata, five to eight;
in G. falcatum, five to seven; in Majidea zanguebarica, seven
to 10; and in D. phyllopterus, eight to 10 stamens are found
(Capuron 1969; Adema et al. 1994; Friedmann 1997). The
other taxa show a constant number of eight or, more rarely,
five or four to five stamens. The feature is scored as (four to)
five (state 0), eight (state 1), or variable (four to 10; state 2).
8. Scoring of the indument of the filaments is modified after
Judd et al. (1994). It is scored as glabrous (state 0) or pilose
(state 1). The character state papillose, mentioned by Judd et
al. (1994) for, e.g., Acer, could neither be verified for Acer
pseudoplatanus nor be found in other taxa of our data set and
was therefore excluded.
9. Scoring of the anther appendages is modified after Judd
et al. (1994). Apical anther and basal thecal appendages are
found in A. hippocastanum (Hardin 1957) and apical
appendages in Averrhoidium dalyi and D. phyllopterus
(Reynolds and West 1985). The feature was scored as absent
(state 0) or present (state 1); thus, states 1 and 2 of Judd et
al. (1994) (apical or apical and basal) were integrated in one
state.
10. Scoring of pollen shape follows Judd et al. (1994):
spherical to round prolate (state 0) or triangular-oblate (state
1). The data are based on Radlkofer (1933, 1934) and Muller
and Leenhouts (1976).
11. Carpel number is scored as three states: three (state 0),
two (state 1), and variable with six to eight carpels (state 2).
It is slightly modified after Judd et al. (1994) (character 17:
five, three, or two carpels). Most of the taxa have threecarpels,
presumed to be a plesiomorphic state (Muller and Leenhouts
1976). In a smaller number of taxa, two carpels are found.
Distichostemon phyllopterus is the only taxon with up to eight
carpels (Reynolds and West 1985), an autapomorphy in our
data set. Delavaya toxocarpa has two or three carpels and is
scored as polymorphic (state 0/1) (Radlkofer 1934).
12. Ovary position follows Judd et al. (1994) and is scored
as sessile (state 0) or stipitate (state 1).
13. Following Judd et al.’s (1994) character 18, the stigma
is scored as lobed (state 0) or unlobed (state 1). Approximately
half of the taxa have an unlobed style.
14. Style shape was scored as curved (state 0) or erect (state
1).
15. Style length was scored as ≤one-half ovary length (state
0) or 1one-half ovary length (state 1). In the majority of the
taxa, the style is curved and longer than one-half of the
gynoecium.
16. Ovule number per locule is scored as one (state 0) or
two (state 1), following Judd et al. (1994). For Hippobromus
alatus, Radlkofer (1934) mentioned the occasional occurrence
of three ovules, which is not considered in our data matrix.
Filicium decipiens,N. lappaceum,Paullinia pinnata,S.
saponaria, and Serjania sinuata have only one ovule per locule.
17. The information about ovule insertion is based on
Radlkofer (1934). Scoring is slightly modified after Judd et al.
(1994): their state 0 (medial to apical) is scored as two different
states: ovule (state 0), apical (state 1), orinsertion Ⳳmidlevel
basal (state 2). In most taxa, the ovules are inserted at
midheight of the locule or slightly above. In N. lappaceum,P.
pinnata,S. saponaria, and S. sinuata, the ovules are basally
inserted, and in F. decipiens apically (Gulati and Mathur 1977).
In H. alatus, the ovules are usually inserted at midheight but
occasionally at the apex of the locule (Radlkofer 1934).
However, it is scored as 0.
18. Flower symmetry is modified after character 12 (disk/
stamen insertion) of Judd et al. (1994) and is scored as
actinomorphic (state 0) or zygomorphic (state 1). More than
half of the taxa have actinomorphic flowers.
WECKERLE & RUTISHAUSER—SYSTEMATICS OF AVERRHOIDIUM 791
19. Sex distribution is scored as monoecious (state 0) or
dioecious (state 1). Actually, this is a simplification caused by
the lack of sufficient data available on our taxa. A higher
variability of floral sexuality may be expected as could be
shown for Acer spp. (Hall 1951; Scholz 1960; de Jong 1976),
Aesculus spp. (Hardin 1956), Cupania spp. (Bawa 1977), or
Serjania sp. (C. S. Weckerle, personal observation). Dioecious
trees are restricted to the tribe Doratoxyleae.
20. Five characters are used to describe the fruits, differing
from the three characters defined by Judd et al. (1994). The
fruit type is scored as dehiscent (state 0), indehiscent (state 1),
or schizocarp (state 2).
21. The pericarp is scored as fleshy (state 0), crustaceous
(state 1), membranaceous (state 2), or coriaceous (state 3).
About half of the taxa have dehiscent fruits (capsules).
Schizocarps are found in A. pseudoplatanus,S. saponaria, and
S. sinuata (Acevedo-Rodrı´guez 1993; Adema et al. 1994).
Most of the indehiscent fruits are drupes. However, the
indehiscent fruit of N. lappaceum has a crustaceous pericarp,
and the fleshy structure is part of the seed. A membranaceous
pericarp is found in taxa with samaras or inflated capsules.
22. Usually all carpels are part of the ripe pericarp (state 0).
In N. lappaceum, only one carpel (the other two are
rudimentary); in S. saponaria, one, two, or three carpels are
part of the mature fruit (Adema et al. 1994). Both taxa are
scored as state 1.
23. The endocarp is scored as coriaceous to woody (state
0) or membranaceous (state 1). A coriaceous to woody
endocarp is found in G. falcatum and Z. golungensis (Capuron
1969; Adema et al. 1994).
24. The locules may be inflated (state 0) or not inflated (state
1). For Euchorium cubense, the fruits are unknown.
25. Seed number varies considerably between the different
taxa. In Doratoxyleae, usually only one (state 0) or, more
rarely, two seeds (state 2) are developed; the remaining four
to five ovules are aborted (Radlkofer 1934). Nephelium
lappaceum and S. saponaria often have one-seeded fruits,
because only one carpel with a single ovule develops to a ripe
fruit. In C. pinnata,Koelreuteria paniculata, and M.
zanguebarica, up to six seeds (state 4) may ripen (in D.
phyllopterus, even more may be found, depending on the
variable number of carpels). In A. hippocastanum, usually one
but up to six seeds occur (Hardin 1955). The capsule of P.
pinnata normally contains three seeds, but one- or two-seeded
capsules also are found. In the samaroid taxa, one seed per
samara is developed.
26. Seed insertion is scored as pendant (state 0) or not
pendant (state 1). Pendant seeds are restricted to taxa of the
tribe Doratoxyleae (Radlkofer 1934).
27. The testa is scored as with fleshy structure (state 0) or
without fleshy structure (state 1). Fleshy seed structures
(sarcotesta or aril-like structure) are found in only three taxa:
Averrhoidium gardnerianum,N. lappaceum, and P. pinnata.
28. The scoring of the character states of embryo shape is
based on Radlkofer (1933, 1934) and modified after character
27 of Judd et al. (1994). According to the different position
of the cotyledons, the states are scored as cotyledons curved
(state 0), fairly straight (state 1), or spiral-like (state 2).
29. Phyllotaxis is scored as alternate (state 0) or opposite
(state 1), following Judd et al. (1994). Opposite leaves are only
found in A. pseudoplatanus and A. hippocastanum.
30, 31. Leaf architecture follows Judd et al. (1994) (their
characters 2 and 3: leaf type). In our data set, paripinnate
leaves are found in the majority of the taxa. Ternate leaves
occur in D. toxocarpa,Hypelate trifoliata, and S. sinuata,
although in the latter, taxon five-foliate or biternate leaves are
occasionally found (Radlkofer 1933; Tomlinson 1980). In D.
phyllopterus, simple leaves occur (Reynolds and West 1985).
Koelreuteria paniculata and P. pinnata have imparipinnate
leaves.
32. Scoring of secondary venation follows Judd et al. (1994).
However, their state 4 (billioid 2⬚venation) does not occur in
our data set and has therefore been excluded.
33, 34. Stipules and tendrils within Sapindaceae are restricted
to Paullinieae and accordingly are found in P. pinnata and S.
sinuata only.
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