Systematic Botany (2004), 29(3): pp. 569–586
q Copyright 2004 by the American Society of Plant Taxonomists
A Morphological Cladistic Analysis of Olacaceae
VALÉRY MALÉCOT,1,4 DANIEL L. NICKRENT,2 PIETER BAAS,3 LEEN
DANIELLE LOBREAU-CALLEN1
VAN DEN
OEVER,3 and
Equipe d’Accueil 3496 Classification Evolution et Biosystématique, Laboratoire de Paléobotanique et
Paléoécologie, Université Pierre et Marie Curie, 12 rue Cuvier, 75005 Paris, France;
2
Department of Plant Biology, Southern Illinois University, Carbondale, Illinois 62901-6509;
3
National Herbarium, Leiden University, P.O. Box 9514, 2300 RA Leiden, Netherlands;
4
Author for Correspondence. Present address: UMR A 462 SAGAH, Institut National d’Horticulture,
2 rue Le Nôtre, 49045 Angers Cedex 01, France (valery.malecot@inh.fr)
1
Communicating Editor: Gregory M. Plunkett
ABSTRACT. A cladistic study based on morphological characters is presented for all 28 genera of Olacaceae as well as
26 representative genera from five other families of Santalales: Loranthaceae, Misodendraceae, Opiliaceae, Santalaceae, and
Viscaceae. The data matrix consists of 80 macro-morphological, palynological, and anatomical characters. The phylogenetic
trees obtained show a paraphyletic Olacaceae with four main clades. Some of these clades are congruent with previously
recognized tribes, but all of subfamilies are para- or polyphyletic. Examination of character transformations confirms several
assumptions of evolutionary trends within Olacaceae and Santalales, but others appear to be more complex than expected.
Optimization of trophic mode on the consensus tree shows that root hemiparasitism had a single origin in Santalales.
Whatever the optimization procedure used, the basal-most clade of Olacaceae consists of 12 genera, among which five are
known to be autotrophs, whereas the remaining three clades (15 genera) contain four genera known to be root parasites.
Olacaceae (ca. 28 genera and 200 species) constitute
a small family of tropical, woody, autotrophic or root
hemiparasitic plants (Breteler et al. 1996). Two genera,
Erythropalum and Octoknema, are sometimes considered to belong to this family or to represent the monogeneric families Erythropalaceae and Octoknemaceae.
Together with Loranthaceae, Misodendraceae, Opiliaceae, Santalaceae (including Eremolepidaceae, Nickrent et al. 1998), and Viscaceae, Olacaceae belong to
the order Santalales and are considered the basalmost
family in this order (Engler and Gilg 1924; Fagerlind
1948; Kuijt 1968, 1969). Such a basal position is supported by molecular phylogenies for Santalales proposed by Nickrent and Franchina (1990), Nickrent and
Duff (1996), Nickrent et al. (1998), Nickrent and Malécot (2001), and in phylogenies of all angiosperm (Savolainen et al. 2000; Soltis et al. 2000).
In the first edition of ‘‘Natürlichen Pflanzenfamilien’’ (Engler 1897), the family included three subfamilies and six tribes and since this publication, modification of the infrafamilial classification consists primarily of newly described genera as listed by Sleumer
(1984b) and Breteler et al. (1996) (Table 1). The main
distinction between the subfamilies Anacolosoideae
(formerly known as Dysolacoideae), Olacoideae, and
Schoepfioideae, was the presence or absence of ovule
integuments and the micropyle position, but according
to Sleumer (1984b), the sampling on which these observations were made was too limited to justify the use
of these characters at such a level of classification.
Moreover, Bouman and Boesewinkel (in Breteler et al.
1996) showed that numerous observations of integument number in the literature were doubtful, and
probably erroneous. Tribes as defined by Engler (Anacoloseae, Aptandreae, Couleae, Heisterieae, Olaceae,
Ximenieae) are distinguished mainly by the type of
endosperm reserve (starch or lipid) and by the degree
of fusion of the stamens. But as with ovule integument
number, the endosperm reserve character (composed
of just two states, either starch or lipid) is too simplistic, plus this feature is not known for about 20% of the
genera in the family. Given these facts, previous authors have regularly expressed doubts on the validity
of this classification (Gagnepain 1910; Reed 1955; Sleumer 1984b), and some have suggested that Olacaceae
be split (Kuijt 1969) or have actually split it into several
families (van Tieghem 1896; Gagnepain 1910; Hutchinson 1969; Takhtajan 1997). Specific studies of palynology (Feuer 1977; Lobreau-Callen 1980), leaf anatomy (Baas et al. 1982), and wood anatomy (van den
Oever 1984), resulted in groupings that differed considerably from older classifications and highlighted the
huge diversity of characters among the various genera
of this family. More recently, molecular phylogenetic
studies of Santalales, using nuclear small-subunit
(SSU) ribosomal DNA (rDNA) sequences alone (Nickrent and Duff 1996) or together with the chloroplastencoded gene rbcL (Nickrent et al. 1998), revealed the
polyphyletic nature of the family. These studies sampled relatively few genera, hence no classification was
suggested for the entire family. A broader sampling
(17 genera of Olacaceae and 58 species of Santalales)
was used by Nickrent and Malécot (2001), in a phylogenetic study based on SSU rDNA and rbcL, but incomplete sampling similarly prevented proposing a
classification for the entire family.
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TABLE 1. Infrafamilial classification of Olacaceae based on Engler (1897) with modification and additions by Sleumer (1984b)
and Breteler et al. (1996).
Subfamily Anacolosoideae Airy-Shaw
Tribe 1. Couleae Engl.
Coula Baill.
Maburea Maas
Minquartia Aubl.
Ochanostachys Mast.
Tribe 2. Heisterieae Dumort.
Chaunochiton Benth.
Heisteria Jacq.
Tribe 3. Anacoloseae Engl.
Anacolosa (Blume) Blume
Brachynema Benth.
Cathedra Miers
Diogoa Exell and Mendonca
Engomegoma Breteler
Phanerodiscus Cavaco
Scorodocarpus Becc.
Strombosia Blume
Strombosiopsis Engl.
Tetrastylidium Engl.
Tribe 4. Ximenieae Engl.
Ximenia L.
Subfamily Olacoideae Sond.
Tribe 5. Olaceae Horan.
Curupira G.A.Black
Douradoa Sleumer
Dulacia Vell.
Malania Chun and S.K.Lee
Olax L.
Ptychopetalum Benth.
Tribe 6. Aptandreae Engl.
Aptandra Miers
Harmandia Pierre ex Baill.
Ongokea Pierre
Subfamily Schoepfioideae Engl.
Tribe 7. Schoepfieae Miers
Schoepfia Schreb.
Dubious affinities
Erythropalum Blume
Octoknema Pierre
Distinguishing genera in the family is relatively
straightforward owing to the monographic studies of
Sleumer for Asia (Sleumer 1980), Malaysia (Sleumer
1984a) and Latin America (Sleumer 1984b), as well as
those of African Olacaceae by Michaud (1962, 1966).
Among the 28 genera,13 are monospecific, and only
six consist of more than ten species. Moreover, four
genera have been described within the last 20 years:
Malania from China (Lee 1980), Douradoa from Brazil
(Sleumer 1984b), Maburea from Guyana (Maas et al.
1992), and Engomegoma from Gabon (Breteler et al.
1996). Some genera show disjunct distributions (afroamerican, afro-asiatic or asiatic-american) and consideration of morphological, anatomical, and chemical
characters suggest an origin of the family during the
Lower Cretaceous (Ling 1982) or Upper Cretaceous
(Sleumer 1984b; Haron and Ping 1997). This biogeographic hypothesis is reinforced by the presence of fossil pollen from the Maestrichtian assigned to the pollen
form genus Anacolosidites, which is similar to pollen of
the current genera Anacolosa, Cathedra, and Phanerodiscus (Krutzsch 1989; Askin 1989; Malécot 2002).
The goal of this work is to use a cladistic approach
to examine the phylogeny of Olacaceae and putatively
related taxa using morphological, palynological, and
anatomical (leaf and wood) characters. To take into account the risk associated with the study of a probable
paraphyletic or polyphyletic group (Nickrent and Duff
1996; Nickrent et al. 1998; Nickrent and Malécot 2001),
members of other families of Santalales (Loranthaceae,
Misodendraceae, Opiliaceae, Santalaceae, and Viscaceae) have been included. A revised classification of
the family will not be presented here but will be published after inclusion of results from molecular phylogenetic analyses (see Malécot 2002; Nickrent and
Malécot, in prep.). A second objective is to study evolutionary trends in selected characters of the family
and order inferred in previously published works.
MATERIALS
AND
METHODS
Taxa. The studied taxa include all genera that have at one time
or another been classified in Olacaceae (Table 1), with the exception of Brachynema which is only doubtfully assigned to Santalales.
Placentation in Santalales consists of a few ovules inserted on the
top of a free-central column (or as a ‘mamelon’ in Opiliaceae, Loranthaceae, and Viscaceae). Placentation in Brachynema is axile in a
4–5 loculate ovary, i.e. clearly not santalaceous. In addition, other
morphological characters such as glandular toothed leaves, apiculate stamen connectives, and convolute aestivation, are unknown
in Santalales. For these reasons, Brachynema was excluded from this
analysis and may be best placed among Ericales (Malécot 2002).
In addition to Olacaceae, six genera of Opiliaceae, one genus of
Misodendraceae, four genera of Loranthaceae, 11 genera of Santalaceae, and four genera of Viscaceae were included. For a few
genera where some characters show variability between species
(e.g., Heisteria, Phoradendron, Viscum), two species have been included as terminal taxa for this cladistic analysis. When character
state variability (polymorphism) existed among species of a genus,
both states were recorded in the data matrix.
Recent molecular phylogenetic analyses (Savolainen et al. 2000;
Soltis et al. 2000) have suggested various putative sister clades for
Santalales, in particular Saxifragales and Caryophyllales. Therefore, Daphniphyllum, a primitive member of Saxifragales, and Rhabdodendron from Caryophyllales were chosen as outgroups.
Characters. Macromorphological characters for all taxa were
scored from specimens housed in various herbaria (e.g., K, KUN,
L, MO, P), or taken from previously published descriptions (e.g.,
Malania, Douradoa, and Curupira). Voucher information is included
in Lobreau-Callen (1980, 1982), Baas et al. (1982), and Kooek-Noorman and van Rijckevorsel (1983). Palynological characters were
taken from Feuer (1977), Lobreau-Callen (1980, 1982, in Sleumer
1984b), as well as new observations by Lobreau-Callen. Leaf anatomical characters for Olacaceae have been obtained from Baas et
al. (1982) and Baas and Koel (1983), whereas those for Opiliaceae
were taken from Koek-Noorman and van Rijckevorsel (1983).
Wood anatomical characters were obtained from publications by
van den Oever (1984) and van den Oever et al. (1993) for Olacaceae, and from Koek-Noorman and van Rijckevorsel (1983) for Opiliaceae. Most of the data (morphology, palynology, leaf and wood
anatomy) for Engomegoma and Maburea were taken from the very
comprehensive papers by Breteler et al. (1996) and Maas et al.
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MALÉCOT ET AL.: OLACACEAE PHYLOGENY
(1992), respectively. Data for other Santalales and the outgroup
genera were obtained from herbarium samples or were gleaned
from the literature (particularly from Metcalfe 1935; Reed 1955;
Metcalfe and Chalk 1957; Puff and Weber 1976; Bhatnagar and
Garg 1977; Carlquist 1982, 1985, 2001; Zavada and Dilcher 1986;
Norverto 1993; Huang 1996). The 80 characters used for this cladistic analysis are described in Appendix 1. Data matrices are
available on TreeBASE (study accession number S1022, matrix accession number M1730). Parasitism was not included as a character in this cladistic analysis because the available data for Olacaceae were too poor and because we wished to study this character by optimizing it on the consensus tree obtained.
Data Analysis. Cladistic analysis of the data was conducted
using PAUP* (Swofford 2000). Heuristic searches for most parsimonious trees used 100 random addition sequences and TBR
branch swapping. Characters were unweighted and character state
transformations of binary and multistate characters were unordered. Node specific support was assessed using bootstrap analysis (Felsenstein 1985) with 1,000 replications and ‘‘Bremer support’’ (Bremer 1988, 1994; Donoghue et al. 1992) was calculated
using Autodecay (Eriksson 1999). MacClade (Maddison and Maddison 1997) and Winclada (Nixon 1999) were used to optimize
character state distributions.
RESULTS
A total of 80 parsimony informative characters was
identified for use in this cladistic analysis of Santalales.
The data matrix consisted of 58 binary and 22 multistate characters. Of these, 32 were derived from anatomy, 14 from palynology, and 34 from floral and vegetative morphology, with 9.1% of the cells coded as
missing. The data matrix used for this cladistic analysis is presented in Appendix 2.
Maximum parsimony analysis resulted in 33 most
parsimonious trees (length 5 457 steps, consistency index (CI) 5 0.33, retention index (RI) 5 0.69). The strict
consensus of those trees is presented in Fig. 1. Relatively few nodes showed bootstrap (BS) values above
50%. Bremer support values above one are commonly
associated with nodes that had bootstrap values above
50%. Santalales are monophyletic (BS 90%), with a
clade of 13 Olacaceae genera sister to the remaining
Santalales. As a family, Olacaceae are paraphyletic and
four lineages (Clades 1–4 on Fig. 1) can be identified.
Clade 1 is composed of 13 genera including members
of tribe Couleae (Coula, Ochanostachys, Minquartia, Maburea), Heisterieae (Heisteria), Anacoloseae sensu Breteler et al. (1996) (Diogoa, Engomegoma, Strombosia,
Strombosiopsis, Tetrastylidium), as well as two problematic genera Erythropalum and Octoknema. Clade 2 consists of four genera: Ximenia (tribe Ximenieae), Curupira, Douradoa, and Malania, the latter three genera
doubtfully placed in tribe Olaceae by Sleumer (1984b).
Clade 3 is composed of ten olacaceous genera from
tribes Olaceae, Aptandreae, Anacoloseae (in part) and
Chaunochiton. This clade is sister to one with Schoepfia
and the remaining Santalales families: Misodendraceae, Opiliaceae, Loranthaceae, Santalaceae, and Viscaceae. Clade 4 consists solely of the genus Schoepfia
which appears as sister to the other families of Santalales. A clade consisting of Misodendraceae plus Op-
iliaceae is sister to a clade that includes Loranthaceae,
a paraphyletic Santalaceae, and Viscaceae. Opiliaceae
are monophyletic (BS 64%), as are Loranthaceae (BS
85%).
DISCUSSION
In general, the relationships obtained from this cladistic analysis of Santalales are quite similar to those
obtained following analyses of SSU rDNA and rbcL
sequences (Nickrent and Malécot 2001), despite differences in taxon sampling. This study also demonstrates
the paraphyly of Olacaceae as first suggested by molecular analyses (Nickrent and Duff 1996; Nickrent et
al. 1998; Nickrent and Malécot 2001). As traditionally
circumscribed, Olacaceae is paraphyletic, but four
groups (clades) can be recognized (Fig. 1). A Templeton test (as implemented in PAUP*) in which the
monophyly of the four clades of Olacaceae was constrained shows that this hypothesis was significantly
worse than the most parsimonious trees.
Comparison to Previous Subfamilial and Tribal
Delimitations. Neither of the two multigeneric subfamilies recognized by Sleumer (1984b) and Breteler et
al. (1996), Anacolosoideae and Olacoideae (Table 1),
are monophyletic and indeed Olacoideae are polyphyletic. Three genera of tribe Olaceae, Curupira, Douradoa,
and Malania, are placed in a clade with Ximenia of tribe
Ximenieae (subfamily Anacolosoideae). The remaining
six genera of subfamily Olacoideae (Aptandra, Dulacia,
Harmandia, Olax, Ongokea, Ptychopetalum), together
with Chaunochiton (tribe Heisterieae) and Anacolosa, Cathedra, and Phanerodiscus of tribe Anacoloseae, constitute Clade 3. As with Olacoideae, subfamily Anacolosoideae is thus polyphyletic and is not the basalmost
subfamily as suggested by Ling (1982). Most members
of Anacolosoideae form a clade at the base of Santalales, including the two genera with doubtful affinities:
Erythropalum and Octoknema.
Only some of the tribes defined by Engler (1897)
appear to be monophyletic, such as Couleae (Coula,
Minquartia, Ochanostachys), Aptandreae (Aptandraceae
of Takhtajan 5 Aptandra, Ongokea, Harmandia), and
Olaceae (Olax, Ptychopetalum, Dulacia). However, other
genera that were included within this last tribe by
Sleumer (1984b), e.g., Malania, Curupira, and Douradoa,
or Maburea, placed in tribe Couleae by Maas et al.
(1992), are excluded. Tribes Ximenieae (Ximenia) and
Schoepfieae (Schoepfia) were both monogeneric, but
Ximenieae are included here in a larger clade with Malania, Douradoa, and Curupira. Tribe Heisterieae, composed of Heisteria and Chaunochiton, is polyphyletic, as
already suggested by Reed (1955). Members of tribe
Anacoloseae are scattered in various positions on the
tree with members in both Clades 1 and 3 (Fig. 1). Baas
et al. (1982), Lobreau-Callen (1980), and van den Oever
(1984) have already highlighted this heterogeneity,
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SYSTEMATIC BOTANY
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FIG. 1. Phylogenetic relationships of Olacaceae and Santalales based on anatomical and morphological characters. Branch
support is given above the branches in the following format: decay index / bootstrap percentage (1000 replications). Circled
numbers indicate major clades of Olacaceae (see text). For nutritional mode character state transformations (using either ACCTRAN or DELTRAN optimizations): black 5 hemiparasitism absent; grey 5 root hemiparasitism; black dashed 5 aerial hemiparasitism. For trophic conditions: ? 5 trophic status unknown; 0 5 autotrophs; R 5 root hemiparasites; A 5 aerial hemiparasites. The subfamilial and tribal names for Olacaceae correspond to the infrafamilial classification shown in Table 1.
which is confirmed here. Relationships within and
among the clades as shown on Fig. 1 will be discussed
in the following section.
Clades of Olacaceae. The basalmost member of
Clade 1 is Erythropalum, a genus with doubtful olacaceous affinity based on anatomy (Reed 1955; Baas et
al. 1982) but whose embryology clearly place it in Santalales (Fagerlind 1946, 1948). Its wood structure (van
den Oever, unpublished) and pollen morphology suggest an affinity with Santalaceae (Lobreau-Callen
1982). Ling (1982) considered this genus as the most
derived subfamily of Olacaceae (Erythropaloideae).
The remaining genera of Clade 1 form a polytomy
of three poorly to well-supported clades. One of these
consists of Octoknema, which is frequently placed in its
own family, Octoknemaceae. Fagerlind (1948) showed
that the genus has typical santalaceous placentation
and proposed a relationship with tribe Couleae. From
its wood anatomy, Reed (1955) linked it to Heisteria
and Couleae. The same relationship has been proposed
2004]
MALÉCOT ET AL.: OLACACEAE PHYLOGENY
by Feuer (1977) on the basis of palynology, whereas,
according to Lobreau-Callen (1982), its pollen is similar to Opiliaceae. The second clade of the polytomy
received strong support (BS 85%, Bremer support 5
3) and is composed of Diogoa, Engomegoma, Tetrastylidium, and Strombosiopsis (hereafter the Diogoa clade).
Unambiguous changes for this clade are the occurrence of epidermal druse crystals and a constricted
furrow in the pollen ectoaperture. In most previous
classifications (Reed 1955; Feuer 1977; Lobreau-Callen
1980; Baas et al. 1982), a group was recognized that
included not only these genera (minus Engomegoma,
then undescribed) but also Strombosia and several other
genera in tribe Anacoloseae. In another case (van den
Oever 1984), two groups were distinguished, one with
Diogoa and Strombosiopsis, the other with Tetrastylidium
and Strombosia. Molecular analyses of Nickrent and
Malécot (2001) showed that Diogoa and Strombosiopsis
are associated with Strombosia and Scorodocarpus, with
strong support (BS . 90%). This relationship is not
supported here, but nodes between these genera are
also not well supported. Breteler et al. (1996), who described the genus Engomegoma, indicated rather ambiguous affinities within Olacaceae near Diogoa, Strombosia, Strombosiopsis, and Tetrastylidium. This relationship
is supported here.
The third subclade of the polytomy of Clade 1 is
composed of seven genera. For the genera or clades
included in this polytomy, different patterns of relationships have been proposed based on different organs or on molecular data. For Maburea, wood anatomical data link it to Heisteria (Maas et al. 1992), leaf anatomy to Scorodocarpus and Brachynema (Maas et al. 1992)
and the pollen apertures (analyzed by Hiepko and
Lobreau-Callen, in Maas et al. 1992) to Minquartia, Coula, and Heisteria. On the basis of both palynology and
anatomy, Strombosia is placed near Diogoa and Scorodocarpus (Feuer 1977; Lobreau-Callen 1980; Baas et al.
1982; van den Oever 1984). Molecular analyses by
Nickrent and Malécot (2001) indicated a strong relationship (BS . 90%) among Diogoa, Strombosia, Strombosiopsis, and Tetrastylidium. According to wood anatomy, Scorodocarpus is closest to Couleae (van den Oever
1984). Leaf anatomy links it to members of the Diogoa
clade and Strombosia, but also to Heisteria (Baas et al.
1982). Palynology suggests a relationship with Strombosia (Feuer 1977; Lobreau-Callen 1980). The genus
Heisteria has been considered the most primitive member of Olacaceae by Reed (1955), mainly on the basis
of wood anatomical features. In his wood anatomical
study of the family, van den Oever (1984) placed this
genus in the same group as Brachynema, likely because
of shared ancestral features. The rather homogeneous
tribe Couleae (Coula, Minquartia, Ochanostachys) has
long been recognized (van Tieghem 1899a, 1899b;
Stauffer 1961). Fagerlind (1948) suggested a basal po-
573
sition of this tribe within the family, a relationship that
was supported by Michaud (1962, 1966) but not the
present study. Couleae are unique among all dicotyledons because they possess both laticifer and secretory cavities in their leaves. Unambiguous changes in
this tribe also include the acquisition of libriform fibers
(also in Scorodocarpus), two or more cycles of stamens,
and thyrsoid inflorescences.
The composition of Clade 2 (Ximenia, Malania, Curupira, and Douradoa; BS 5 63%, Bremer support 5 2)
is exactly the same as proposed by van den Oever
(1984). According to Sleumer (1984b), Ximenia constitutes a monogeneric tribe (Ximenieae) within subfamily Anacolosoideae, whereas Curupira, Malania, and
Douradoa were doubtfully placed within tribe Olaceae
of subfamily Olacoideae. An affinity between Malania
and Ximenia corresponds with the proposal made by
Lee (1980) in his generic description, and was found
by Nickrent and Malécot (2001) in their molecular
study. This association was supported by Ling (1982),
but was never pointed out in the later synthesis by
Sleumer (1984b) and Breteler et al. (1996). Curupira was
placed close to Ptychopetalum because of the absence of
staminodes or an accrescent calyx (Black and Murça
Pires 1948). In the present study, the clade composed
of Ximenia and Malania as well as the two Brazilian
genera Curupira and Douradoa can be attributed to their
shared umbellate inflorescences, flowers with two stamen cycles, lipid reserves in the fruit, and several
wood anatomical features.
Clade 3 received less support (,50% BS, Bremer
support 5 1) but is here composed of ten genera, arranged in three major subclades. Three members of
one subclade (Olax, Ptychopetalum, and Dulacia) have
long been recognized for their morphological (Sleumer
1984b), anatomical (Reed 1955; Baas et al. 1982; van
den Oever 1984), and palynological (Feuer 1977; Lobreau-Callen 1980) homogeneity. This group was
strongly supported (100% BS) in the molecular analysis of Nickrent and Malécot (2001). According to van
Tieghem (1896), this group is equivalent to family Olacaceae sensu stricto. Unambiguous character changes
for this clade include heterogeneous type I rays, a pollen foot-layer in masses, and the loss of endexine in
the mesocolpium of the pollen. Bootstrap support for
a clade composed of the three genera coinciding with
tribe Aptandreae (Harmandia, Aptandra, and Ongokea)
was strong (BS 95%, Bremer support 5 6). The homogeneity of this group has long been known, and
indeed van Tieghem (1896), Pierre (1897), and Gagnepain (1910) all suggested that these genera be recognized at the family level (Aptandraceae). Several
morphological features link these three genera, particularly the very peculiar fused androecium and the anthers that dehisce by means of flaps. Molecular data
(Nickrent and Malécot 2001) provide strong support
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SYSTEMATIC BOTANY
(BS 5 82%) for a relationship between two representatives of this group (Aptandra and Ongokea). The third
component of Clade 3 (Chaunochiton, Phanerodiscus, Cathedra, and Anacolosa) received BS support below 50%
but Bremer support 5 3. A clade minus Chaunochiton
received higher support (BS 5 77%, Bremer support
5 5), thus in agreement with the assignment of the
three genera to tribe Anacoloseae sensu stricto as recognized by Reed (1955) and Baas et al. (1982). Floral
features of this smaller clade include petals inserted
on the top of a disk and poricidal stamens. Chaunochiton has been more commonly associated with Aptandreae (‘‘Chaunochitoneae’’ of Fagerlind 1948), based
on ovary morphology. The molecular analysis by Nickrent and Malécot (2001) also supported a clade composed of Chaunochiton and Aptandreae (BS 5 81%).
Relationships between Anacoloseae s.s. and Aptandreae have been proposed by Baas et al. (1982) on the
basis of leaf anatomy. Despite an early association with
tribe Heisterieae (Engler 1897), affinities of Chaunochiton are clearly not with Heisteria as stated by Fagerlind
(1948) and subsequent workers (Feuer 1977; LobreauCallen 1980; Baas et al. 1982; van den Oever 1984,
1990).
Engler (1894) placed the genus Schoepfia in its own
tribe in Olacaceae (Schoepfieae) and later (Engler 1897)
proposed a monogeneric subfamily (Schoepfioideae).
This genus was previously assigned to Loranthaceae
(de Candolle 1830). Van Tieghem (1896) and Gagnepain (1910) both proposed raising this genus to the
family level (Schoepfiaceae). According to wood anatomy, Reed (1955) noted that this genus was the most
specialized among all Olacaceae, noting further that its
pollen was comparable to that of some Santalaceae. In
molecular phylogenetic analyses (Nickrent and Duff
1996; Nickrent et al. 1998; Nickrent and Malécot 2001),
Schoepfia was separated from other Olacaceae and
placed in a clade together with Misodendrum and Loranthaceae. In our study, this genus occurs in Clade 4
and is sister to all the remaining Santalales families.
Compared to the traditional infrafamilial classification of Olacaceae, these results suggest that relatively
few characters can be used to distinguish subfamilies
Olacoideae and Anacolosoideae, such as integument
number (1 or 2 for Anacolosoideae, 0 for Olacoideae)
and an accrescent calyx (absent in Anacolosoideae,
mostly present in Olacoideae) (Sleumer 1984b). Moreover, some genera have been assigned to subfamily
based on erroneous data (e.g., Bouman and Boeswinkel
in Breteler et al. 1996, comments on ovule integument
number). Aside from those genera described after
1948, tribal characteristics appear more pertinent, except for tribes Anacoloseae and Heisterieae, in which
genera were grouped based on non-homologous characters. For the genera described during the second part
of the 20th century, some tribal assignments may have
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been the consequence of the absence of data (e.g. Curupira placed in Olaceae because it lacks an accrescent
calyx and staminodes). Moreover, some genera were
classified based on data not initially used for delimitating the tribes, such as Douradoa and Malania, which
were placed in Olaceae because they are morphologically close to Curupira, and Maburea, which waas
placed in Couleae based on flower morphology.
Other Santalalean Families. Of the major clades
sister to Schoepfia, the first is Opiliaceae, a monophyletic and moderately well-supported family (BS 64%,
Bremer support 5 2). This family was recognized as
distinct from Olacaceae by Valeton (1886) and it is
commonly divided into two tribes: Agonandreae and
Opilieae. According to Sleumer (1935), the first tribe
contains Agonandra and Gjellerupia, whereas Hiepko
(1984) includes only Agonandra therein, placing Gjellerupia with Urobotrya and Lepionurus. Anatomical data
presented by Koek-Noorman and van Rijckevorsel
(1983) place these latter three genera together in one
group and Champereia, Melientha, Opilia, and Rhopalopilia (and possibly Cansjera) in another group; Agonandra showed uncertain affinities. Molecular results
support a monophyletic Opiliaceae but the topology
differs from the above treatments. According to the
combined analysis of SSU rDNA and rbcL by Nickrent
and Malécot (2001), Lepionurus is basalmost in the family followed by Agonandra and the four other genera in
the family (Champereia, Cansjera, Opilia, and Pentarhopalopilia). Although additional sampling is called for,
the presence of Agonandra near the base for the family
is supported by this morphological cladistic analysis
because this genus has the highest number of plesiomorphies. Dividing the family into two tribes seems
premature at this time, even though six characters state
transformations (characters 2, 42, 50, 75, 76, 78) separate Agonandra from the remaining Opiliaceae.
Misodendrum of the monogeneric mistletoe family
Misodendraceae is placed here as sister to Opiliaceae.
The genus has a large number of autapomorphies, such
as wood features (peculiar/highly modified rays, fibers and parenchyma), or palynological characters (polyporate, echinulae) (Skottsberg 1914; Metcalfe and
Chalk 1957; Feuer 1981; Carlquist 1985). This position
as sister to Opiliaceae is not stable as indicated by a
BS value of less than 50% (Bremer support 5 1) for
this clade. Molecular data (Nickrent and Soltis 1995;
Nickrent and Duff 1996; Nickrent et al. 1998; Nickrent
and Malécot 2001) always link Misodendrum and
Schoepfia, a relationship also recovered in some morphological cladistic analyses (data not shown) where
fewer genera of Santalaceae and Loranthaceae were
used.
The four genera sampled from Loranthaceae (Dendrophthoe, Ligaria, Tripodanthus, and Tupeia) are monophyletic and this well-supported (BS 85%, Bremer sup-
2004]
MALÉCOT ET AL.: OLACACEAE PHYLOGENY
port 5 2) clade is sister to Santalaceae and Viscaceae.
Santalaceae appear paraphyletic in this study. One
clade consists of members of tribe Thesieae of Pilger
(Acanthosyris, Scleropyrum, Pyrularia) and is relatively
similar in composition to Santalaceae clade c of Nickrent and Malécot (2001). Okoubaka, also considered to
belong to this tribe based on habit, fruit morphology,
wood anatomy, and palynology (Stauffer 1957; Lobreau-Callen 1982; Hallé 1987), is here placed as sister
to Viscaceae, an anomalous position supported by a
single character (37, long ray cells). The remaining Santalaceae form a poorly-supported clade that includes
members of Santalaceae clades d, e and f of Nickrent
and Malécot (2001), mainly from tribes Santaleae and
Antholobeae. The four genera of Viscaceae are monophyletic, but with low BS support Bremer support 5
1, thus few intergeneric relationships are resolved.
Character Transformations. This discussion of
character transformations will concentrate mostly on
Olacaceae, although some characters more particularly
concern the other families. The unambiguous character
optimizations are presented in Fig. 2. Alternate (character 1) and developed (character 3) leaves are plesiomorphic within Santalales, and opposite and/or
squamate leaves appear independently derived several
times in non-olacaceous families (Loranthaceae, Misodendraceae, Santalaceae, Viscaceae). Such evolution appears consistent with morphological reduction associated with the parasitic habit. The presence of tomentum, whether on twigs (character 2) or leaves (characters 7, 8), is a derived feature. Dendritic leaf hairs is
a synapomorphy of tribe Couleae. Regarding venation,
the variability of the states for the outgroups prevent
any decision regarding plesiomorphic and apomorphic
features as secondary (character 4) and tertiary (character 5) venation distinguish Clade 1, (with camptodromous leaves and reticulate tertiary venation) from
the remaining clades (Clades 2, 3, 4). Mesh shape
(character 6) is primarily polygonal and flabellate
meshes are a synapomorphy for Coula and Ochanostachys.
Evolution of leaf anatomical features commonly follows the assumptions of Baas et al. (1982), with derived features being sclerification or lignification of
epidermal cells (character 9), lignification of guard
cells (character 10), wide lumina of stomata (character
11), and the presence of cuticular ledges on guard cells
(character 12). Occurrence of paracytic (character 13)
or cyclocytic (character 15) stomata separate Clade 1
(cyclocytic stomata) from the remaining Santalales
(with paracytic stomata). However, according to Baas
et al. (1982), the presence of paracytic stomata may be
plesiomorphic. Regarding stomatal features, Couleae
strangely show a reversal compared with other members of Clade 1. Contrary to Baas et al. (1982), the presence of laticifers (character 17) is a derived feature,
575
whereas schizogeneous cavities (character 16) are a
synapomorphy of Couleae, in agreement with them.
The presence of druses in epidermal cells (character
18), silicified walls of mesophyll and epidermal cells
(character 19), mesophyll sclereids (character 20), and
leaf cystoliths (character 21) are all apomorphic within
Santalales. The presence of mechanical tissues of the
vascular system, e.g. sclerenchyma fibers (character 22)
and astrosclereids (character 23) in the petiole and median vein, appear to be plesiomorphic within Santalales, in agreement with Baas et al. (1982); the absence
of such mechanical tissue is a specialization achieved
through reduction.
General trends for wood anatomical features mostly
conform to the hypotheses put forth by Bailey (1957),
but occurrence of the derived state does not imply a
close relationship. For example, ray organization (character 36) follows Bailey’s hypothesis, with heterocellular rays being plesiomorphic, whereas homocellular
rays are apomorphic. Clade 1 consists only of taxa
with heterocellular rays with several rows of erect or
square cells. Clades 2 and 3 consist of taxa with heterocellular rays with a single row of erect or square
cells. For the remaining santalalean families the picture
is not so clear and several reversals from homocellular
to heterocellular rays (whether with one or several
rows of erect or square cells) have occurred in the Opiliaceae and Exocarpos/Santalum clades. Presence of
wood cystoliths (character 38) is a possible synapomorphy for two genera of Opiliaceae (Champereia and
Opilia), and the presence of silica bodies (character 39)
is a synapomorphy for the three genera of tribe Olaceae (Ptychopetalum, Olax, Dulacia).
Tetramerous (character 44) flowers with oval buds
(character 43), partially fused sepals (character 45), accrescent calices (character 46), fused petals (character
47) and pubescent petals (character 48) occur commonly in a few unrelated clades, thus suggesting that
parallel morphological evolution may be linked with
pollination syndromes. The primitive androecial condition appears to be five (character 49), epipetalous
(character 51) stamens organized in a single (character
50) cycle. Such an organization contradicts the hypothesis of Michaud (1962, 1966) who proposed that the
two-cycled androecium as occurs in Heisteria and tribe
Couleae is primitive. Duplication of the androecium
occurs independently in Clade 1 (Couleae, Heisteria,
Scorodocarpus, Maburea), Clade 2 (all genera except
Douradoa), and Clade 3 (tribe Olaceae). The presence
of staminodia (character 52), of fused filaments (character 53), or of a modified anther connective (character
54) are all synapomorphies of small clades, commonly
regarded as tribes within Clades 1 or 3. Anthers are
primitively basifixed (character 55) with a transformation to dorsifixed in Clade 1, and to oblique in
Clade 3. Anther dehiscence mode (character 56) and
576
SYSTEMATIC BOTANY
[Volume 29
FIG. 2. Optimization of morphological characters on cladogram given in Fig. 1. Open boxes indicate homoplastic characters,
filled boxes non-homoplastic characters.
orientation (character 57) appear to be linked, with longitudinal and introrse (or lateral) anther dehiscence as
plesiomorphies. In contrast, extrorse dehiscence is almost always associated with porous or valvate dehiscence, as occurs in Chaunochiton and tribes Aptandreae
and Anacoloseae of Clade 3.
The accrescent disk (character 58) is a synapomorphy of Anacolosa and Cathedra within Clade 3. The
glandular tissue (character 59) is primitively located
between the stamens and ovary. Its location between
the stamens and petals is a synapomorphy for members of Aptandreae. The absence of glandular tissue
occurs in several independent lineages. A short cylindrical style (character 60) seems to be plesiomorphic
within Santalales. Style shape modifications are common in Clade 1, but are uninformative. Conversely,
2004]
MALÉCOT ET AL.: OLACACEAE PHYLOGENY
long conical styles appear as a clear synapormophy for
Clade 2 and a long cylindrical style as a synapomorphy for Clade 3.
The inferior ovary (character 62) is a synapomorphy
of non-olacaceous families and Schoepfia, but within
Olacaceae, semi-inferior ovaries arose several times independently. The ovary locule number of two (character 63) is plesiomorphic within Clade 1, and increases (to four or five) in the Diogoa clade. For the remaining Santalales (Clades 2, 3 etc.), the plesiomorphic state
is a single locule, with an increase of up to two in
Anacoloseae, or to three in Olax. Such patterns contradict common assumptions on the prevalence of reduction in locule number evolution in Santalales (Sleumer
1984b), but new observations may be necessary for
some taxa as some reports date to Valeton (1886).
Breviaxial pollen (character 67) is a synapomorphy
for Clade 3, whereas heteropolarity (character 68) has
occurred independently in various groups. A concave
mesocolpium (character 69) and concave apocolpium
(character 70) are synapomorphies for members of Aptandreae, the former occurring also in a few unrelated
genera. Apertures are primitively three or four and zonoaperturate (character 71); duplication of the number
occurs independently in Ptychopetalum and in Anacoloseae s.s. (Anacolosa, Cathedra, Phanerodiscus). Round
or elliptic ectoapertures (character 73) are a synapomorphy for Clade 3 (with a reversal for Chaunochiton),
as stated by Lobreau-Callen (1980). The occurrence of
granules on the apertural membrane (character 73)
does not constitute a synapomorphy for any group of
Olacaceae, but granules in the endoaperture (character
76) are synapomorphies of Clade 3. The endoaperture
and ectoaperture of identical size (character 75) are
mainly synapomorphies of Clade 3, with few independent occurrences in other Santalales. Mesocolpium ornamentation (character 77) is primitively smooth or
microperforate, but derived states occur several times
independently. The presence of granules in the infratectum (character 78) is a synapomorphy for members
of Couleae and Opiliaceae, but this feature appears to
be independently derived in these two groups. Formation of a columella in the infratectum (character 79)
also appears independently in a few clades (Aptandreae and Anacoloseae s.s.; Opiliaceae p.p.) suggesting
these features are not always homologous. A smooth
foot layer (character 80) is plesiomorphic in Santalales,
but contrary to the assumptions of Lobreau-Callen
(1980), an irregular foot layer surface is not homologous in all Olacaceae. An irregular foot-layer is a synapomorphy for two groups, Couleae (Coula, Ochanostachys) and Olaceae (Ptychopetalum, Dulacia, Olax).
Parasitism. The occurrence of root hemiparasitic
and autotrophic taxa in Olacaceae has been known for
decades, but the evolution of this ecological specialization remains poorly understood. Only four genera of
577
Olacaceae are known to contain species that possess
haustoria on their roots: Ximenia (Heckel 1899), Olax
(Barber 1907), Schoepfia (Piehl 1973; Werth et al. 1979),
and Ptychopetalum (Anselmino 1932). The absence of
haustoria has been documented only for Heisteria (Kuijt
1969), Ochanostachys, Strombosia, Scorodocarpus, and Erythropalum (Ping 1997). No data are available for the
remaining 19 genera in the family. Haustoria have
been recorded for eight of the ten genera of Opiliaceae.
Gjellerupia and Pentarhopalopilia are the only genera for
which parasitism has not yet been confirmed, but all
Opiliaceae are assumed to be root parasites (Kubat
1987). All Santalaceae are considered to be either aerial
or root hemiparasites, including Okoubaka, a 40 meter
high African tree whose parasitic mode was only recently reported (Veenendaal et al. 1996). Hemiparasitism has been documented in Acanthosyris (Barroso
1969), Colpoon (Visser 1981), Pyrularia (Leopold and
Muller 1983), Scleropyrum (van Rheede 1688; Arnott
1836; Nicolson et al. 1988) and for Santalum, Thesium,
Exocarpos, Osyris, and Buckleya (see references in Kuijt
1969). Among the 11 genera of Santalaceae used in this
study, documentation of parasitism is lacking only for
Rhoiacarpos. The three genera of Loranthaceae included
here are all aerial hemiparasites (mistletoes), as is Misodendrum and all Viscaceae. On the basis of molecular
results, Nickrent (2002) showed that aerial hemiparasitism arose independently in Santalales at least five
times, but the evolution of root hemiparasitism was not
addressed.
Positive documentation of hemiparasitism and nonparasitism have been plotted on the tree obtained from
this cladistic analysis (Fig. 1). When those taxa with
an unknown parasitic state are coded with ‘‘?’’, root
hemiparasitism arises only once in Santalales, in the
common ancestor of Clade 1 (Olacaceae) and its sister
group (remaining Santalales). This result is obtained
using both ACCTRAN (accelerated transformation)
and DELTRAN (delayed transformation) optimization
strategies. Aerial hemiparasitism appears in three independent lineages among the taxa studied here: Misodendraceae, Loranthaceae and Viscaceae (an aerial
parasite from Santalaceae was not included). Moreover, an additional appearance of root parasitism can
be assumed at the base of Loranthaceae (Atkinsonia,
Gaiadendron, and Nuytsia, none of which were sampled
here). If taxa coded as unknown are considered root
parasites or autotrophs (‘‘R’’ or ‘‘0’’), ancestral states
for Santalales are ambiguous, thus leaving the possibility open that root parasitism arose numerous times.
From the topology of the tree shown in Fig. 1, it may
be assumed that, in addition to the five olacaceous
genera documented as lacking haustoria, eight other
genera are autotrophs: Coula, Diogoa, Engomegoma,
Minquartia, Maburea, Octoknema, Strombosiopsis, Tetrastylidium. Furthermore, eleven genera not known to be
578
SYSTEMATIC BOTANY
parasites may, based on our optimizations, be root
hemiparasites: Anacolosa, Aptandra, Cathedra, Chaunochiton, Curupira, Douradoa, Dulacia, Harmandia, Malania,
Ongokea and Phanerodiscus. If the tree topology is correct, and any of these genera are later found to be autotrophic, such cases would represent reversals from
the parasitic mode. Such reversals, however, have never
been reported for any parasitic plant and seem unlikely given the selective advantage conferred by this trophic mode.
Perspectives. Several previous works based on
morphological or molecular data suggested a paraphyletic or polyphyletic Olacaceae. The present study
reaches the same conclusion, but the positions of genera such as Maburea, Strombosia, and Scorodocarpus remain uncertain when compared with available molecular data. This cladistic analysis demonstrates that the
infrafamilial classification of the family is in need of
revision. The existing classification is based on the
work of Engler from the 19th century (Engler 1894,
1897). Subsequent work during the last century mainly
provided amendments, such as the description of new
taxa, but the overall structure of the classification remained relatively unchanged. In the present analysis,
the subfamilies Olacoideae and particularly Anacolosoideae are polyphyletic and only a few of the named
tribes appeared monophyletic. A revised classification
of the family will not be presented here but will be
published after consideration of results from molecular
phylogenetic analyses (Nickrent and Malécot, in prep.).
Regarding parasitism, if states are inferred for unknown taxa, this study suggests a single origin of root
hemiparasitism within Santalales, whereas aerial hemiparasitism appeared independently in at least three of
the lineages sampled here. The evolution of hemiparasitism appears to have been a major event in Olacaceae, one that can be used to distinguish two groups
in the family. Character optimization for parasitism allows a prediction, for the first time, of the nutritional
mode for nineteen genera of Olacaceae.
ACKNOWLEDGEMENTS. We thanks the curators and staff of K,
KUN, L, MO and P for making specimens available for study
through visit or loans. The first author (V. Malécot) is indebted to
Jean Broutin and staff of the Equipe Classification Evolution et
Biosystématique at University Pierre & Marie Curie, Paris, for support and advice during the preparation of his PhD dissertation
from which much of this work is derived. We are also grateful to
P. Herendeen (as editor and reviewer), G.M. Plunkett (as editor)
and an anonymous reviewer for helpful comments on the manuscript.
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APPENDIX 1
List of characters used in this cladistic analysis of Olacaceae
with discussion of character state assignments.
Stem
1. Phyllotaxy: alternate (0): opposite (1). All species of Olacaceae have alternate phyllotaxy, but various Santalaceae and Loranthaceae have opposite leaves. In rare cases (e.g., Okoubaka), phyllotaxy varies near the proximal ends of shoots within an individual, thus such species were coded as polymorphic.
2. Twig tomentum: none (0): simple hairs (1): stellate hairs (2).
According to Reed (1955), Coula and Minquartia, as well as Octoknema, could be allied by the presence of branched hairs on the
young branches. Diverse Opiliaceae also have pubescent young
branches, albeit with simple hairs. We interpreted the pubescence
on young growth among Opiliaceae and Couleae as non-homologous and coded the states accordingly.
Leaf
The majority of foliar anatomical characters result from work of
Baas et al. (1982) who studied infrageneric variation in leaf anatomical characteristics of Olacaceae. They also proposed assumptions as for the homology and the taxonomic utility of these attributes while taking into account the other families of Santalales.
For Opiliaceae, Koek-Norman and van Rijckvorsel (1983) did similar work.
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MALÉCOT ET AL.: OLACACEAE PHYLOGENY
3. Leaf size: developed (0): squamate (1).
4. Secondary venation: camptodromous (0): brochidodromous
(1). The venation of the leaves of Olacaceae shows some diversity.
The secondary venation is always pinnate, either of a festooned
brochidodromous, or a festooned eucamptodromous type (Mouton 1972). In the genera with three clear basal veins (Maburea,
Curupira, etc.), the secondary veins are widely spaced at the base,
and much closer towards the top, and the type of secondary venation remains identifiable starting from these final veins.
5. Tertiary venation: plagiodromous (parallel) (0): reticulate (1).
The tertiary venation is of a simple plagiodromous type (parallel
veins between them, at oblique angles to the secondary veins), or
reticulate and irregular.
6. Quarternary venation (areolation): meshes flabellate (0):
meshes polygonal (1). The meshes (areoleae) are either flabellate
in a direction parallel with the tertiary veins or polygonal.
7. Leaf dentritic hairs: absent (0); present (1). Baas et al. (1982)
recognized three types of hairs: dendritic, unicellular, and uniseriate. The simultaneous presence of hairs of two types in certain
genera (e.g. Ochanostachys) led us to independently code for each
hair type rather than to use only one character with four states
(hairs absent, dendritic, unicellular, uniseriate). Moreover, according to Baas et al. (1982), the presence of uniseriate hairs does not
make it possible to characterize any genus of Olacaceae, and this
character varies between leaves of the same individual. Consequently, only two characters will be defined, one for dentritic hairs
and a second one (character 8) for unicellular hairs.
8. Leaf unicellular hairs: absent (0); present (1).
9. Epidermal cell lignification: none (0); weakly lignified (1); lignified (2). The secondary walls of the ‘‘ordinary’’ epidermal cells
(excluding guard cells and stomatic cells) can be sclerified—a very
rare phenomenon in angiosperms (Baas et al. 1982). Such cells are
found on the entire abaxial surface of the leaves of the genera of
tribe Couleae, as well as occasionally on the leaves of Heisteria p.p.,
Harmandia, and Aptandra. For these last three genera, a very weak
sclerification is observed, thus the phenomenon may not be homologous with that observed in Couleae. Thus weakly lignified
epidermal cells was treated as distinct.
10. Guard cell lignification: not lignified (0); lignified (1). According to Baas et al. (1982), there is no link between the sclerification of the epidermal cells and the lignification of the guard
cells. The majority (more than 60%) of the guard cells are lignified
in the genera Aptandra, Cathedra, Maburea, and Phanerodiscus. Taking into account the small percentage (lower than 10%) of lignified
guard cells mentioned for Heisteria p.p., Chaunochiton, Harmandia
and Dulacia, these genera were scored with a question mark.
11. Lumina of guard cells: narrow (0); wide (1). Seen in cross
section, the guard cells of the stomata are of very different form
and size in Olacaceae. Two extreme types were defined by Baas
et al. (1982): 1) guard cells with a broad lumen and equally thick
walls above and below and 2) guard cells with a narrow lumen
with the inner wall (facing the mesophyll) much thicker than the
outer wall. They found that the guard cells with broad lumens are
constantly associated with marked cuticular ledges, whereas the
guard cells with narrow lumens generally occur (but not always)
in the species with paracytic stomates. However, exceptions to this
relationship exist. Thus, two characters will be defined, one corresponding to the size of the lumen of the guard cells, the other
to the presence of cuticular ledges (character 12).
12. Cuticular ledges of guard cells: inconspicuous (0); thick (1).
13. Paracytic stomata: absent (0); present (1). Olacaceae show a
great diversity of stomate types (Baas et al. 1982), and different
types can be present on the same individual. Thus, in an effort to
avoid using a polymorphic characters, each stomatal type was coded independently (characters 13–15) except anomocytic stomata
which occur in all genera.
14. Cyclocytic stomata: absent (0); present (1).
15. Anisocytic stomata: absent (0); present (1).
581
16. Schizogenous cavities in leaf. absent (0); present (1).
17. Laticiferous channel in leaf: absent (0); present (1). The laticifers present in the leaves of certain species of Olacaceae are not
ramified, and have a diameter ranging between 8 and 45 mm (Baas
et al. 1982). Their presence has been used to delimit tribe Couleae
(Sleumer 1935), however, they are also present in species of Heisteria, Chaunochiton, Harmandia, and Aptandra.
18. Druses in epidermal cells: absent (0); present (1). Druses are
considered by Baas et al. (1982) to be an apomorphy for the genera
Diogoa, Strombosia, Strombosiopsis, and Tetrastylidium. Other types
of crystals listed by Baas et al. (1982) were recorded in only some
species of the same genus, thus only druses will be used in this
phylogenetic analysis.
19. Silicified walls of mesophyll and epidermal cells: absent or
extremely infrequent (0); present (1). In various genera of Olacaceae and the majority of the other families of Santalales the walls
of certain cells of the mesophyll and epidermis are silicified, more
particularly those associated with the stomatal complex or vein
endings. Baas et al. (1982) consider that this is a derived condition
in Olacaceae.
20. Mesophyll sclereids: absent (0); present (1). Idioblastic sclereids are morphologically variable in the species of Heisteria (Baas
et al. 1982; Baas and Kool 1983), but not so in the other genera of
the family. Only the presence of this type of mesophyll sclereid
will be coded here.
21. Leaf cystoliths: absent (0); present (1). Mesophyll cystoliths
are observed only for Opiliaceae and could constitute an apomorphy for this family (Koek-Noorman and van Rijckevorsel 1983).
22. Petiole and median vein sclerenchyma fibers: absent (0); present (1). Baas et al. (1982) considered that the presence of sclerenchyma fibers is strongly related to the type of vascularization. The
presence of such fibers is common in angiosperms, but the linkage
with the type of vascularization is not so strong in other families.
On the other hand, the absence of sclerenchymatous fibers (more
exactly their substitution by collenchyma) as supportive tissue in
the median vein is not very common in angiosperms (Baas et al.
1982). Moreover, this absence from the median vein does not automatically correspond to an absence near the other veins. Baas et
al. (1982) identified a particular type of nonlignified fiber near the
margin of the leaf in Strombosia, Strombosiopsis, and Diogoa. The
difficulty in observing this type of fiber makes it impossible to
determine if its absence in the other families of Santalales is real
or simply a lack of observation. Thus, only the presence or absence
of sclerenchyma fibers in the petiole and median vein will be coded, but not in other veins.
23. Petiole and median vein astrosclereids: absent (0); present
(1). With the exception of Phanerodiscus, these sclereids are present
in the majority of Anacoloseae s.l., such as Heisteria, Maburea, Engomegoma, Curupira, and Douradoa, and sporadically in Malania and
Ximenia (Baas et al. 1982). These sclereids are morphologically
close (groups of isodiametric and slightly ramified sclereids) and
have an identical position in the central tissue of the petiole and
the median vein (Baas et al. 1982).
Vascularization of nodes and petiole
24. Vascularization of the nodes: unilacunar (0); trilacunar (1);
pentalacunar or more (2). The genera for which information is
available derives from Reed (1955), otherwise taxa were coded
with missing data. A possible correlation (although unconfirmed)
between the vascularization of the petiole and the median vein
may exist (Baas et al. 1982). Thus, the unilacunar nodes would be
generally associated with a simple type of vascularization of the
petiole and principal vein. However, trilacunar nodes can be associated with a closed vascular cylinder or a simple arc. For Octoknema, the vascularization of the nodes was described by van
Tieghem (1905).
25. Basal petiole vascularization: simple bundle (0); incomplete
vascular cylinder (1); simple vascular cylinder (2). This type of
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SYSTEMATIC BOTANY
vascularization is constant in a genus and sometimes in a tribe
(Baas et al. 1982). Variation exists, however, in the condition of the
vascular system between the base of the petiole, the top of the
petiole (character 26), and the median vein in the center of the
lamina (character 27).
26. Distal petiole vascularization: simple bundle (0); complex
vascular cylinder and one or more adaxial or enclosed strands (1);
simple vascular cylinder (2).
27. Median vein vascularization: simple bundle (0); complex
vascular cylinder and one or more adaxial or enclosed strands (1);
simple vascular cylinder (2).
Wood anatomy
The diagnostic characteristics of wood in Olacaceae were outlined by van den Oever (1984). Moreover, Herendeen and Miller
(2000) proposed a phylogenetic coding for characters traditionally
used for wood anatomical data and this coding will be used here.
28. Vessel grouping: solitary (0); grouped in multiples (1). Vessels can be exclusively solitary, or can be grouped in multiples of
two to four (and even up to 15 in Anacolosa). A frequency of solitary vessels higher than 60% was coded as wood with solitary
vessels, following van den Oever (1984).
29. Perforation plate type: scalariform (0); simple (1). The type
of perforation was studied by van den Oever (1984) on mature
wood. Heisteria scandens, a lianescent species, has simple and scalariform perforations in young wood, then exclusively simple perforations in older wood (van den Oever in prep.). Herendeen and
Miller (2000) proposed using a more complex coding that does
not have utility in this study. The number of bars of the scalariform perforations could also be introduced into the analysis. Van
den Oever (in prep.) mentions that scalariform perforations of the
genera Coula, Minquartia, Ochanostachys, Scorodocarpus, and Engomegoma always have more than ten bars.
30. Vessel member length: below 900 mm (0); over 900 mm (1).
Two distinct non-overlaping length classes for vessel elements exist in the wood of Olacaceae (van den Oever 1984; in prep.).
31. Intervascular pits (if present): alternate (0); opposite (1); scalariform (2). Although used by van den Oever (1984),this character
may not be independent of character 28. Solitary vessels obviously
never have intervascular pits. However, taking into account the
occasional presence of two adjacent vessels (and coding ‘‘solitary
vessels’’ when at least 60% of them are solitary), the type of intervascular pitting can be easily observed (van den Oever in prep.).
This coding corresponds to that recommended by Herendeen and
Miller (2000) when character states inapplicable in Santalales are
removed.
32. Vascular tracheids associated with the vessels: absent (0);
present (1). This character was defined by van den Oever (1984).
These tracheids are rare but can be observed in certain cases in
macerations. The coding used corresponds to that of Herendeen
and Miller (2000).
33. Fibers: fiber-tracheids (0); libriform fibers (1). The terminology used for this character is that of Baas (1986), and coding is
that proposed by van den Oever (1984, in prep.). Usually one observes either fiber tracheids or libriform fibers. An exceptional case
is the septate libriform fibers in Octoknema, which were coded as
libriform fibers.
34. Axial parenchyma frequency: abundant (0); rare or absent
(1). The abundance of axial parenchyma was recorded by van den
Oever (1984; in prep.). This type of tissue is very rare in Heisteria
and Maburea and some other genera.
35. Axial parenchyma strand width: less than seven cells (0);
more than seven cells (1). Two classes of axial parenchyma strand
width can be distinguished in Olacaceae: less than seven cells
broad (narrow bands of axial parenchyma), and greater than seven
cells broad (broad bands of axial parenchyma) (van den Oever
1984, in prep.). Taxa with rare or absent axial parenchyma (character 34 state 1) have been coded as inapplicable ‘‘-’’. This coding
[Volume 29
corresponds to one of the four characters suggested by Herendeen
and Miller (2000) to code parenchyma.
36. Ray type: all cells procumbent (homogeneous) (0); heterocellular, one row of erect cells (1); heterocellular, several rows of
erect or square marginal cells (2). Various types of rays can be
distinguished that correspond to the heterogeneous rays I, II, III
types (van den Oever 1984, in prep.) and with the homogeneous
rays of Kribs (1968). Herendeen and Miller (2000) recommend coding the composition of the rays in the following way: first, homogeneous rays, all cells procumbent (homogeneous I II and III
of Kribs 1935 5 homogeneous of Kribs 1968): second, heterocellular rays, a file of erect cells (heterogeneous I of Kribs 1935 and
Kribs 1968): third, ray heterocellular, only one row of erect or
square marginal cells (heterogeneous IIA and IIB of Kribs 1935 5
heterogeneous II and III of Kribs 1968). Such coding will be used
here.
37. Ray height: long (over 1,000 mm) (0); short (below 1,000 mm)
(1). The height of the rays varies from 94 mm to 4300 mm, and van
den Oever (1984) determined a threshold value equal to 1 mm,
making it possible to distinguish two non-overlaping groups within Olacaceae.
38. Wood cystoliths: absent (0); present (1). Various genera of
Opiliaceae have cystoliths in the wood rays, that are apparently
independent of their presence in leaves (Koek-Noorman and van
Rijckevorsel 1983). It is possible that this character could be used
to distinguish groups within Opiliaceae.
39. Silica bodies in ray cells: absent (0): present (1). van den
Oever (1984) mentions only their presence in three genera, Olax,
Ptychopetalum, and Dulacia.
Inflorescence and flowers
40. Inflorescence bracts: absent (0); present (1).
41. Floral and inflorescence trichomes: absent (0); present (1).
42. Flower sexual condition: bisexual (0); unisexual (1).
Perianth
43. Floral bud shape: spherical (0); oval (1). In Olacaceae, floral
buds are either spherical, measuring 2–3 mm in diameter (e.g.,
Coula), or lengthened, and reaching more than 5 cm in length (e.g.,
Chaunochiton). The length and width of floral buds before anthesis
were measured on rehydrated flowers from herbarium specimens.
The flowers for which the length/width ratio was between 0.9 and
1.1 were regarded as spherical, whereas those with values higher
than 1.1 were regarded as oval.
44. Flower merosity: five (0); four (1); six (2). The number of
parts per floral cycle was determined directly or obtained from
the literature (Douradoa). The number of stamens was not used to
code this character because of the simultaneous and variable presence, in certain genera, of stamens and staminodes. Within a genus, the number of parts per cycle does not vary, except for Phanerodiscus and Olax spp. Sometimes the number of floral parts per
flower varies on the same branch. Olax is often regarded as having
only three petals (Linné 1753; Sleumer 1984a, 1984b), but the anatomical studies of Argawal (1963) and Patil and Pai (1984), the
observations of Capuron (1968), and our own observations of herbarium samples indicate that these flowers are pentamerous with
varying degrees of fusion between the more or less distinct petals.
45. Sepals: developed, partially fused (0); developed, completely
fused (1); calyculus (2); absent (3). Among genera of Olacaceae,
the petals are more or less fused. In Opiliaceae, Santalaceae, Viscaceae, and Loranthaceae various and contradictory interpretations of the floral parts have been proposed. Here we scored Misodendraceae and Opiliaceae as lacking a calyx (a ‘torus’ is present
in Opiliaceae according to Hiepko 2000), whereas we interpreted
Santalaceae and Viscaceae as having only a developed calyx (Eichler 1878; Kuijt 1968). In Loranthaceae, a calyculus is generally
present. Among Olacaceae, Schoepfia and Octoknema were regarded
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MALÉCOT ET AL.: OLACACEAE PHYLOGENY
as lacking a calyx, although very small sepals are present on the
female flowers of Octoknema orientalis.
46. Accrescent calyx: absent (0); present (1). Identification of an
accrescent structure around the fruit was based on the study of
herbarium samples of ripe and unriped fruits. Taking into account
the problems of homology and the difficulty in considering the
development relative to certain organs, each tissue that can be
accrescent was coded independently, and only the accrescence of
the calyx and of the disc/receptacle (character 58) were taken into
account. In Erythropalum, one observes no accrescent structure
around the fruit, but at maturity the mesocarp tears into four to
five parts, revealing a black, sclerified endocarp, and a bright red,
internal mesocarp face. This structure has sometimes been regarded as an accrescent calyx (particularly given its radial pseudosymmetry), but it is not at all homologous. In santalaceous families
treated here as lacking a calyx (character 45 state 3) this character
was coded as inapplicable.
47. Corolla connation: apopetalous (0); sympetalous at base
only (1); sympetalous with a floral tube (2). If one considers that
Santalaceae have only one cycle of floral parts (monochlamydous)
and this is interpreted to represent the calyx, the present character
cannot be coded for that family, and was scored as inapplicable.
For our purposes, we considered petals fused by less than half
their length to be connate at their base, whereas those fused by
more half their length to have a floral tube. In the case of variation
in the degree of fusion between petals of the same flower (Olax),
we took account of the measured minimal value.
48. Petal pubescence: petal glabrous (0); petal with hairs in upper third (1); petal with 1 row of hairs (2). Pubescence is particularly variable on the external as well as the internal surfaces of
the petals. External pubescence was very variable on the same
individual at anthesis and was thus not taken into consideration.
The exact nature of the trichomes occupying the internal face was
not established with precision but in Anacolosa, Cathedra, and Phanerodiscus they appear as two types. Those adjacent to the stamens
are likely glandular (but were not coded here), whereas the uniserial trichomes were coded.
Androecium
49. Stamen number: three (six including staminodes) (0); four
(eight including staminodes) (1); five (ten including staminodes)
(2); twelve to twenty (3).
50. Stamen whorls: one (0); two (1); three (2). The number of
staminal cycles was calculated by taking into account possible
staminodes and the merosity of the flowers. In the case of Olax,
the total number of stamens and staminodes is in general not proportional to the number of petals (five), but always lies between
seven and ten. The flowers of this genus were regarded as having
an androecium composed of two cycles.
51. Stamen position relative to corolla: alternate and opposite
(0); opposite only (1). For Olacaceae we tried to identify epipetalous stamens and alternipetalous stamens, but, in various genera
this distinction proved to be impossible to realize in the absence
of fresh material and a study of floral development. Thus, for flowers of Scorodocarpus, two stamens are fused with each petal and
are placed at equal distance from the edges of the petal. For Olax,
a similar phenomenon is observed, which becomes complicated
because of the probable absence of certain parts of the androecium. In these last two cases, stamens were regarded as only opposite.
52. Staminodia: absent (0); present (1). The presence of staminodia provides a means of distinguishing the genera of tribe Olaceae. Other genera (e.g. Ongokea) have at the base of the staminal
column either staminodia or a divided disc, depending upon interpretation. Similarly, the condition in Opiliaceae can be interpreted as staminodia (Kuijt 1969) or a divided disc (Hiepko 2000).
In all such cases, our coding follows the latter interpretation.
53. Filament: free (0); fused (1). The mutual fusion of the fila-
583
ments of stamens (synadelphous or monadelphous) is characteristic of a small number of genera: Aptandra, Harmandia, and Ongokea.
54. Anther connective: typical (0); prolonged to a point or thicken (1). The top of the stamen connective is generally blunt and
without excrescenses, but for Anacolosa and Cathedra it is pubescent, whereas for Diogoa, Tetrastylidium, and Engomegoma it is
pointed.
55. Anther attachment: dorsifixed (0); basifixed (1); oblique (2);
other (3). The state ‘‘oblique’’ was applied to the very short anther
of Chaunochiton whereas ‘‘other’’ was applied to members of tribe
Aptandreae where stamens are fused by their filaments.
56. Anther dehiscence: slit (0); pores (1); flaps (2); disaggregation (3). Anther dehiscence is generally longitudinal but poricidal
for tribe Aptandreae. For Anacoloseae and Chaunochiton, dehiscence is valvate. Curupira has a curious short longitudinal dehiscence that does not appear to be the result of mechanical tearing
but a disaggregation of the tissue that exposes the interior of the
thecae.
57. Direction of anther dehiscence: introrse or lateral (0); extrorse (1).
Gynoecium
58. Accrescent disk: absent (0); present (1). The disc corresponds either to glandular tissue surrounding the ovary (Strombosia), or located below it (Olax), or with a cup into which the
petals and stamens are inserted (Anacolosa, Cathedra, Phanerodiscus). Thus, the disc is a descriptive term used to indicate an often
glandular structure of the flower (see also character 59). Accrescence of the ‘‘disk’’ applies only to a cup into which the corolla
and androcium are inserted. For Phanerodiscus, Capuron (1968)
and Malécot et al. (2003) showed that neither the calyx nor the
disk are accrescent, but a structure indiscernable in the flower at
anthesis.
59. Glandular tissue (disk): between stamens and ovary (0); between stamens and petals (1); none (2). In this analysis, we code
only glandular tissue that correspond to structures of reduced
size, that areseparate from the ovary (not fused as in Strombosiopsis), and that are not being used as support for the stamens and
the petals (as in Anacolosa, Cathedra, and Phanerodiscus) (see also
character 58).
60. Style shape: long conical (0); cylindrical short (1); cylindrical
long (2); short conical (3). Although style shape may be influenced
by the position of the ovary (inferior or superior), the relative
length of the style was established by taking into account the relationship between the distance from the top of the locules of the
ovary to the stigma and the diameter below the stigma. When this
ratio is lower than six, the style was regarded as short. The values
used were measured on rehydrated floral material at anthesis
(long-styled flowers in the case of the genera with heterostylous
flowers). Heterostyly is mentioned or supposed for several genera
of Olacaceae (Michaud 1966; George 1984; Sleumer 1984a, 1984b),
in which case only longistylous material was used for coding.
61. Stigma length: small globular (0); elongated (1). The length
of the stigmas was measured on the same material used for coding
character 60. The elongated character state occurs only in the outgroup (stigmas of more than 1 mm in length). The micromorphology of the stigmas was not studied.
62. Ovary position: hypogynous (0); epigynous (1); half inferior
(2). The position of the ovary was observed on rehydrated flowers
obtained from herbarium samples or was determined from the
literature (Douradoa). Schoepfia, sometimes described as having a
half inferior ovary, was regarded as having an inferior one.
63. Ovary locule number: five (0); four (1); three (2); two (3);
one (4). The number of locules at the base of the ovary is based
on the data available in the literature, in particular Fagerlind (1946,
1947, 1948) and Sleumer (1984a, 1984b). The reliability of this information is doubtful for some and unknown for other genera.
584
SYSTEMATIC BOTANY
64. Integument number: two (0); one (1); none (2). Given varying accounts in the old literature, only the indications provided by
Bouman and Boesewinkel (in Breteler et al. 1996) were used in
coding. The genera for which variation exists (cf. Sleumer 1984b)
were coded as polymorphic.
Fruit
65. Starch in fruit: absent (0); present (1). The nature of the reserves of the fruit was coded according to the data available in the
literature (Michaud 1966; Hegnauer 1966, 1969, 1973, in Sleumer
1984a, 1984b). This character was used by Engler (1897) to distinguish the subfamilies of Olacaceae. In general, starch and/or lipid
quantity is not known and, according to Sleumer (1984b), varies
in the same genus and even in the same species. Thus some taxa
that were recorded as lacking either starch or lipid may contain
these, as well as other types of seed reserves. Despite the absence
of data for some taxa, the presence/absence of starch and lipid
(character 66) was coded.
66. Lipids in fruit: absent (0); present (1).
Pollen
67. Pollen shape: equiaxial (0); longiaxial (1); breviaxial (2). The
ratio of the distance between the poles and the equatorial diameter
of the pollen grains results from the observations of Lobreau-Callen (1980, 1982). The values used to distinguish the three character
states are those recommended by Punt et al. (1994).
68. Pollen symmetry: isopolar (0); heteropolar (1). Work by
Feuer (1977), Lobreau-Callen (1980, 1982, in Sleumer 1984b, in Breteler et al. 1996) and Hiepko and Lobreau-Callen (in Maas et al.
1992) showed that the pollen of certain Olacaceae was asymmetrical.
69. Mesocolpium shape: flat or convex (0); concave (1). According to Lobreau-Callen (1980), the pollen of Aptandreae has a concave mesocolpium, a unique feature in Santalales.
70. Apocolpium shape: convex (0): concave (1). Concave apocolpium is a distinctive feature of tribe Aptandreae.
71. Aperture number: three to four, zonoaperturate (0); six, diploporate (1); more than six, periaperturate (2). In Santalales, the
number and position of the apertures are linked: pollen grains
with three or four apertures are always zonoaperturate, those with
six apertures are always diploporous, and those with more than
six apertures (Misodendrum) are periaperturate. In some genera,
the number of apertures varies between three or four for pollen
derived from the same anther, but these are zonoaperturate pollens.
72. Ectoaperture shape: ellongate (furrow) (0); round (porous)
[Volume 29
or elliptic (1). The ectoaperture of Olacaceae can either be lengthened perpendicular to the equator (furrow), or circular or elliptic.
73. Apertural membrane: smooth or scabrous (0); granular or
verucose (1).
74. Endoaperture shape: elliptic (0); circular (1). The endoaperture can be lengthened perpendicular to the equator, or circular.
The absence of endoapertures for certain Opiliaceae prevented
coding this character for some taxa, and they were scored as inapplicable.
75. Relative size of the endo- and ectoaperture: ecto- and endoaperture of distinct size (0); ecto- and endoaperture of identical
size (1).
76. Endoaperture granules: none and endoaperture smooth (0);
present and endoarpeture smooth (1); none and endoaperture
with endosculpture (2). Lobreau-Callen (1980, 1982) showed that
the pollen endoapertures of Olacaceae could be ornamented. Presence of granules in the endoaperture was coded but not other
modifications of the nexine (such as endosculpted nexine instead
of a true endoaperture).
77. Exine in mesocolpium: smooth or microperforate tectum (1);
reticulate exine (1); echinulate tectum (2); other (3). In the mesocolpium and apocolpium the exine can correspond to a continuous
tectum with rare perforations, with a microperforate or perforated
tectum or with a network (Lobreau-Callen 1980, 1982). However,
the transition between these various types is almost continuous
and combines two elements, the size of the perforations and the
density of the perforations. The terminology used here corresponds to extremes but is not easily applicable to certain intermediate forms.
78. Granules in infratectum: absent (0); present (1). According
to Lobreau-Callen (1980), the structure of the infratectum makes
it possible to distinguish various groups of Olacaceae. In certain
genera this layer consists of individualized grains laid out in several layers, in others only one layer of grains exist, which tend to
form columellae (Anacolosa, Aptandra, Ptychopetalum), or individualized columellae (Chaunochiton). Homology among these features
is not clear and two characters were defined, one for the presence
of granules whatever the number of layers, and one for the coding
presence of columellae-like structures (character 79).
79. Columella in infratectum: absent (0); present (1).
80. Foot layer surface: smooth (0); irregular with masses (1).
Lobreau-Callen (1980) use the foot-layer as a distinctive feature to
separate two main set of Olacaceae. Despite the relatively low
number of taxa for which this information was available, it appears
useful for characterizing some groups among Olacaceae. Various
other structural characteristics of the plate and the endexine were
highlighted by Feuer (1977) and Lobreau-Callen (1980). These
characters are available only for the small number of genera that
have been studied using transmission electron microscopy.
2004]
APPENDIX 2. Data matrix analyzed in this study. Abbreviations: A 5 0 or 1; B 5 1 or 2; C 5 0 or 2.
2222222222
0123456789
3333333333
0123456789
4444444444
0123456789
5555555555
0123456789
6666666666
0123456789
77777777778
01234567890
Viscaceae
Korthalsella complanata
Notothixos leiophyllus
Phoradendron californicum
Phoradendron serotinum
Viscum album
Viscum articulatum
101???002
100011002
10A011002
10A011002
10A011002
10A011002
00?1000010
00?1000010
00?1000011
00?1000011
00?1000010
00?1000010
?0??000000
?0??000000
?011000000
?011000000
?011000000
?011000000
10?1000000
10?1000000
10?01-0000
10?01-0000
10?1001000
10?1001000
??10110000
??10110000
??10110000
??10110000
??1011000A
??1011000A
01000?0002
01000?0002
01000?0002
01000?0002
01000?0002
01000?0002
?014201000
?014201000
?014201000
?014201000
?014201000
?014201000
0001?002???
0001?002???
0001?002???
0001?002???
0001?002???
0001?002???
Santalaceae
Acanthosyris asipapote
Buckleya distichophylla
Colpoon compressum
Exocarpos bidwillii
Okoubaka aubrevillei
Osyris lanceolata
Pyrularia pubera
Rhoiacarpos capensis
Santalum album
Scleropyrum pentandrum
Thesium humifusum
000111002
100011012
100???002
001011102
100011002
000???002
000111012
100???002
100A11002
000???002
000?11002
00?1000010
00?1000010
00?1000010
00?1000010
00?1000010
00?1000010
00?1000010
00?1000010
00?1000010
00?1000010
00?1000010
?011000000
?011000000
?0??000010
?0??000010
?0??000010
1011000010
?0??000000
?0??000010
?0??000010
?0??000010
10??000010
11001-A101
11101-010?
1?101-110?
1?101-1100
1?001-0000
1?101-1100
10001-210?
1?101-110?
1?101-1100
1?001-210?
1?101-110?
??00010002
??10010001
??00010001
??10010002
??10010012
??1001000A
??10010002
??0001000B
??00010001
??00010002
??0011001B
01000?0000
01000?0002
01000?0002
01000?0002
01100?0000
01000?0002
01000?0002
01000?0002
01000?0002
01000?0002
01000?0002
?014201000
?014201000
?014201000
?014201100
?014201000
?014201100
?014201010
?014201000
2014201100
?014201000
?014201011
0011?100???
0001?005???
0001?001???
0001?005???
0000100010?
0001?000???
00A1?100???
0001?000???
00110104???
00A1?100???
0011?101???
Opiliaceae
Agonandra macrocarpa
Champereia manillana
Opilia amentacea
Pentarhopalopilia marquesii
Rhopalopilia umbellata
Urobotrya siamensis
010011000
000011000
010011000
000011000
000011010
000011010
0011000000
0011000001
0011000000
0011000000
0011000001
0011000001
0100?00010
0100?00010
0110?00010
0100?00010
0100?00010
0100?00000
1000001100
1000001110
1010001110
1000001100
1000001100
1000001100
??1013--01
??0003--02
??0003--02
??0003--02
??0013--01
??0013--02
01000?0000
01000?0000
01000?0000
01000?0000
01000?0000
01000?0000
1014201000
1014201000
1014201000
1014201000
1014201200
1014201200
00010?20000
0001-001010
00011001010
0001-001010
00010021010
00010001010
Loranthaceae
Dendrophthoe lepidota
Ligaria cuneifolia
Tripodanthus flagellaris
Tupeia antarctica
100011002
100???002
100???002
100011002
00?1000010
00?1000010
00?1000010
00?1000010
1000000000
?0??000000
?0??000000
1000000000
1001000100
1001000100
100?000100
1????????0
??01020202
??01020202
??0102020?
??1??20?0?
01000?0002
01000?0002
01000?0002
01??0??002
?014201200
?014201201
?014201201
?014201200
0101?00????
0001?005???
0001?002???
0101?00????
Misodendraceae
Misodendrum brachystachyum
000011010
00?1000001
0110?00000
1101000100
??1013--00
01100??002
1014201000
0211211200?
Olacaceae
Anacolosa frutescens
Aptandra tubicina
Cathedra acuminata
Chaunochiton kappleri
000111010
000111001
000111010
000111010
1001000001
0001000101
1111000001
0111000101
0011000000
0000000000
1011000000
0011000000
101101A000
1010001000
101101A000
1011001100
0000010112
0001110001
A000010012
1001011112
0100111012
0101032101
0100101012
0100022102
20031?1200
2003B11211
2003110200
2003B?1200
01111110110
10111110110
0111111010?
00000003010
585
1111111111
0123456789
MALÉCOT ET AL.: OLACACEAE PHYLOGENY
123456789
586
APPENDIX 2. Continued
1111111111
0123456789
2222222222
0123456789
3333333333
0123456789
4444444444
0123456789
5555555555
0123456789
6666666666
0123456789
77777777778
01234567890
Coula edulis
Curupira tefeensis
Diogoa zenkeri
Douradoa consimilis
Dulacia candida
Engomegoma gordonii
Erythropalum scandens
Harmandia mekongensis
Heisteria concinna
Heisteria parvifolia
Maburea trinervis
Malania oleifera
Minquartia guianensis
Ochanostachys amentacea
Octoknema dinklagei
Olax subscorpioidea
Ongokea gore
Phanerodiscus perrieri
Ptychopetalum petiolatum
Schoepfia schreberi
Scorodocarpus borneensis
Strombosia javanica
Strombosiopsis tetrandra
Tetrastylidium peruvianum
Ximenia americana
010000102
000111000
000001000
000111000
000111010
000???000
000001000
000111001
000001000
000AA1000
010001000
000111000
010001102
000000102
020001000
000111010
000111000
000111000
000111000
000111010
000001000
000001000
000001A00
000001000
000111000
0011001100
0001000001
0110110010
0001000001
0011000001
0111110010
1000010000
0101000101
0110110100
0110110100
1010110000
0110000001
0111001100
0111001100
0010010000
0000000001
0001000001
1001000000
0001000001
0001000001
0110110000
0110100010
0110110010
0110110010
0001000001
0011121101
0001110010
0011?21111
0001?10010
0000100010
0011?21111
0011?22001
0000000010
1011122211
0011122211
0011?21111
0001?10010
0011122201
0011121101
0011222201
0000000000
0000000010
0000?00000
0000100000
0000000000
0011222201
1011122201
1011121101
1011121101
0001110010
0001012000
1010001100
0100012100
10101-1000
1010001101
0?00012000
A00A112000
1011001100
0B00112000
0B00112000
0000012000
1010001100
0001012000
0001012000
0101112000
1011001101
1010001100
101101A100
1011001101
1011000100
0001012000
0101012000
0101012000
0101012000
10001-1100
1100010003
1100110011
1000010002
1100110011
1101211100
100011000B
1000000A12
1011110201
0000001A22
0000001A22
1100000112
1100100001
0100010112
1100110001
?110020002
1101211120
1?01110002
1100C00012
1001010012
??00020222
1101010012
1101010012
1001110101
0000110101
1001110011
B000000002
1000013002
0100010002
0000010?02
0110000002
0100110002
0100010002
0101032101
1000000002
1000000002
1000000002
1000000002
1000000002
B000000000
0100000000
1010010000
0111032101
0100111102
100001000?
01000?0000
1100010000
0100000002
0100110000
0100100002
1000010002
3002011010
0001?01000
30001??000
000?101000
2002B1A200
30011??0A0
1002101000
2004B01211
3002011???
3002011010
10020??010
000???1210
3001010000
3002010010
3002A??000
2002B01200
2004B?1211
2003??1201
2004201200
1012101010
2002A10010
2024110010
30211??000
1001101000
00040010A0
0000-000001
0001-000??0
00010001100
00010001100
00111110101
00010001010
00010000101
10111110110
00?????????
00010000100
00010001???
00000000???
00000000000
0001-000001
0001-110110
00111110101
10111110111
01111110110
01111110101
00011000100
00010000100
00010010101
00010001100
00010000100
00010000111
outgroups
Daphniphyllum pentandrum
Rhabdodendron amazonicum
000???100
020???101
0000001001
0000001001
10??2???11
1011222210
02001-1000
0210002000
?????00???
0000010003
?00?0??00?
2000110002
?1000?????
11140??000
00?????????
0001???1???
SYSTEMATIC BOTANY
123456789
[Volume 29