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Botanical Journal of the Linnean Society, 2013, 173, 407–441. With 5 figures
Taxonomy and phylogenetics of Cuviera
(Rubiaceae–Vanguerieae) and reinstatement of
Globulostylis with the description of three new species
BRECHT VERSTRAETE1*, OLIVIER LACHENAUD2,3, ERIK SMETS
STEVEN DESSEIN3 and BONAVENTURE SONKÉ2,5,6
FMLS1,4,
1
Plant Conservation and Population Biology, KU Leuven, Kasteelpark Arenberg 31, PO Box 2437,
3001 Leuven, Belgium
2
Service d’Evolution Biologique et Ecologie, Université Libre de Bruxelles, CP 160/12, 50 Avenue F.
Roosevelt, 1050 Bruxelles, Belgium
3
National Botanic Garden of Belgium, Domein van Bouchout, 1860 Meise, Belgium
4
Naturalis Biodiversity Center, Leiden University, PO Box 9517, 2300 RA Leiden, The Netherlands
5
Plant Systematic and Ecology Laboratory, Higher Teachers’ Training College, University of Yaounde
I, PO Box 047, Yaounde, Cameroon
6
Africa and Madagascar Department, Missouri Botanical Garden, PO Box 299, St Louis, MO
63166-0299, USA
Received 19 May 2012; revised 12 November 2012; accepted for publication 19 April 2013
Generic circumscriptions in tribe Vanguerieae (Rubiaceae) have been under discussion for a long time. Recent
molecular studies, while providing new insights, have not yet solved all the problems. In this study, the taxonomy
and phylogenetics of the genus Cuviera s.l. are investigated. On the basis of molecular and morphological evidence,
Cuviera is restricted to a group of ten West and Central African species. Globulostylis, previously included in
Cuviera, is reinstated as a distinct genus, with eight species from Central Africa. Both genera are revised; the
latter includes three new species (G. dewildeana, G. rammelooana and G. robbrechtiana) and two new combinations (G. leniochlamys and G. uncinula). The close relationship of Cuviera s.s. and Globulostylis to Vangueriella is
shown. Six aberrant species (most from East Africa) are excluded from Cuviera, but further work is needed before
they can be confidently assigned to other genera. © 2013 The Linnean Society of London, Botanical Journal of
the Linnean Society, 2013, 173, 407–441.
ADDITIONAL KEYWORDS: Cameroon – Equatorial Guinea – Gabon – Tropical Africa.
INTRODUCTION
Tribe Vanguerieae are palaeotropical in distribution
and among the larger tribes in Rubiaceae, comprising
approximately 600 species in 25 currently accepted
genera (Govaerts et al., 2012). The tribe is delineated
by a set of morphological characteristics, in particular
the specialized hood-like structure of the stigma
(Lantz & Bremer, 2004), the valvate corolla lobes, the
*Corresponding author. E-mail:
brecht.verstraete@bio.kuleuven.be
pendulous ovules and the drupaceous fruits with oneseeded pyrenes in each locule. Generic delimitation in
the tribe is still problematic as several genera lack
good diagnostic characters. Not surprisingly, recent
molecular studies are partially in conflict with
morphological classifications (Lantz et al., 2002;
Lantz & Bremer, 2004, 2005). At present, molecular
sampling and tree resolution are insufficient to
answer all questions related to the generic delimitations in the tribe. Detailed molecular studies in
particular groups of the tribe are rare (e.g.
Razafimandimbison et al., 2009) and many taxonomic
problems are still to be solved. Furthermore, many
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
407
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B. VERSTRAETE ET AL.
species remain to be described from Central and West
Africa, but also from Madagascar and Asia.
The main aim of this study is to elucidate the
phylogenetic position of the African genus Cuviera
DC., especially in relation to Vangueriella Verdc.
Cuviera was described by de Candolle (1807) with one
species, C. acutiflora DC. It was regarded as closely
related to Vangueria Juss. because of the solitary
pendulous ovules in each locule. Further species were
added by various authors (Bentham in Hooker, 1849;
Hiern, 1877; Schumann, 1888, 1899, 1903; Krause,
1912; Wernham, 1914, 1918; Mildbraed, 1924;
Verdcourt, 1957, 1981; Hallé, 1960).
Wernham (1913) described the genus Globulostylis
Wernham with two species, G. minor Wernham and
G. talbotii Wernham, and later added a third species,
G. cuvieroides Wernham (Wernham, 1918). Although
Cuviera and Globulostylis clearly belong to the tribe
Vanguerieae, they were not addressed in the monograph of the tribe by Robyns (1928).
Hallé (1960) published a conspectus of Cuviera,
including studies of inflorescence, style and pyrene
morphology, and a key to the species then known. He
noted that certain Cuviera spp. have a hairy swelling
at the base of the style and suggested an infrageneric
group. Verdcourt (1987) saw the resemblance of these
species with Globulostylis and treated the latter as a
subgenus of Cuviera. More recently, Onana (2008)
presented a conspectus of subgenus Globulostylis.
Currently, Cuviera s.l. (including Globulostylis)
includes 24 accepted species (Govaerts et al., 2012).
The genus occurs mainly in the Guineo–Congolian
region of Africa, but four species, poorly known and of
questionable generic position, are found in East Tropical Africa (Verdcourt & Bridson, 1991; Bridson, 1998).
So far only C. physinodes K.Schum. (misidentified as
C. angolensis Welw. ex K.Schum.) has been included in
molecular studies (Lantz et al., 2002; Lantz & Bremer,
2004, 2005), and its position was unresolved.
Vangueriella, with 18 species in two sections
(section Vangueriella and section Stenosepalae
(Robyns) Verdc.), was erected by Verdcourt (1987)
when he raised Vangueriopsis Robyns subgenus
Brachyanthus Robyns (Robyns, 1928) to generic rank.
Verdcourt considered Vangueriella to be related to
Cuviera. Molecular analyses (Lantz et al., 2002; Lantz
& Bremer, 2004) rather suggested an affinity to Canthium Lam., but the only species included (V. spinosa
(Schumach. & Thonn.) Verdc.) is atypical. We therefore found it necessary to add data for Vangueriella
while investigating Cuviera.
The taxonomic problems in Cuviera do not only
involve generic delimitation, but frequent misidentifications between the species also occur in literature
and even more so in herbaria. For example, in the
Checklist of Gabonese vascular plants (Sosef et al.,
2006), three out of ten species were misidentified. The
names C. acutiflora DC., C. leniochlamys K.Schum.,
C. longiflora Hiern and C. minor C.H.Wright, in particular, have been commonly misapplied. A taxonomic
revision of this group was therefore necessary and is
provided here.
MATERIAL AND METHODS
To test the monophyly and systematic position of
Cuviera and Vangueriella, a molecular phylogenetic
study has been performed based on seven DNA
regions (trnTL, trnLF, rpl16, petD, ITS, rpl32-trnL
and accD-psaI). Ninety-two specimens of Vanguerieae
representing the different groups recognized in the
tribe were included in the phylogenetic analysis, as
well as three outgroup species. Detailed information
on the investigated taxa can be found in Appendix 1.
DNA of silica-dried and herbarium material was
extracted using the E.Z.N.A.TM HP Plant DNA Mini
Kit (Omega Bio-Tek). The primers for the amplification of the seven DNA regions can be found in Appendix 2, with their respective annealing temperatures.
Purified PCR products were sent to Macrogen for
sequencing (Macrogen Inc., Amsterdam, the Netherlands). The sequences were assembled, edited and
aligned using Geneious 5.4 (Drummond et al., 2011).
Gaps were coded following Simmons & Ochoterena
(2000). Maximum parsimony analysis was conducted
using PAUP* v.4.0b10a (Swoffort, 2002). Heuristic
searches were conducted with tree bisection–
reconnection (TBR) branch swapping on 10 000
random addition replicates, with five trees held at
each step. Non-parametric bootstrap analysis was
carried out to calculate the relative support for individual clades found in the parsimony analysis. For
each of 1000 bootstrap replicates, a heuristic search
was conducted with identical settings as in the original heuristic analysis. Phylogenetic trees were also
estimated using probabilistic methods under Bayesian in the CIPRES web portal (Miller, Pfeiffer &
Schwartz, 2010). Bayesian analysis was inferred
using MrBayes 3.1, running four Markov chains sampling every 100 generations for 5 million generations.
DNA substitution models for the individual markers
were selected by preforming jModelTest 0.1.1 (Posada,
2008) (Appendix 2). The concatenated data set was
partitioned and independent models were applied for
each of the partitions.
The taxonomic revision is based on the examination
of herbarium specimens in BM, BR, BRLU, E, HBG,
K, LBV, MPU, P, WAG and YA. Central African collections of Cuviera from all these herbaria and West
African collections from BM, BR, K and WAG, were
seen for this study. The distribution is based on the
specimens of the above-mentioned herbaria, comple-
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
mented with data from the literature in a few cases
(e.g. Hepper & Keay, 1963). Measurements, colours
and other details given in the descriptions are based
on living material, spirit and herbarium specimens
and data derived from field notes. The dimensions
given for the calyx do not include the ovary.
Phytogeographical considerations follow White
(1979), but we simplify his ‘(sub)centres of endemism’
into Domain and Region. Specimens are cited alphabetically first by country (with a further distinction
for Equatorial Guinea between Bioko Island and Rio
Muni) and then by collector, with the initials only
given in the case of ambiguity (e.g. J. J. F. E. de Wilde
and W. J. J. O. de Wilde). The conservation status was
assessed by calculating the extent of occurrence or the
area of occupancy using the geographic information
system (GIS) and applying the 2001 IUCN Red List
Categories and Criteria.
409
4. The focus of this study is on the Cuviera/
Vangueriella group. It includes three wellsupported subclades corresponding to Cuviera
subgenus Cuviera (excluding C. schliebenii Verdc.
and C. semseii Verdc.), Cuviera subgenus Globulostylis and Vangueriella (excluding V. spinosa). The
latter two subclades are weakly supported as
sister groups.
5. The Vangueria group includes Multidentia Gilli,
Pygmaeothamnus zeyheri (Sond.) Robyns, Robynsia Hutch., Vangueria (in the enlarged sense of
Lantz & Bremer, 2005), Vangueriopsis and two
East African species of Cuviera (C. schliebenii and
C. semseii). Vangueria is monophyletic with good
support but the rest of the clade is not well
resolved.
DISCUSSION
RESULTS
The analysis of the combined data set using maximum
parsimony and Bayesian inference yielded similar
trees, of which the consensus tree is shown in Figure 1.
Bootstrap values and posterior probabilities are indicated below the respective branches. Vanguerieae as a
whole is monophyletic and strongly supported. The
consensus tree is well resolved and contains several
strongly supported clades, in correspondence with the
findings of Lantz & Bremer (2004).
1. The earliest branching clade contains the genera
Afrocanthium, Keetia, Psydrax, Bullockia, Peponidium and Pyrostria, the last three forming the
dioecious group of Lantz & Bremer (2004). In our
analysis, Keetia is sister to the remainder of the
clade and Afrocanthium is sister to the dioecious
group, whereas Lantz & Bremer (2004) found
these two genera to be sister to each other. Relationships in the dioecious group are not well
resolved; for a detailed investigation of this group
see Razafimandimbison et al. (2009).
2. The so-called ‘spiny’ group of Lantz et al. (2002)
containing most Canthium Lam. spp., Plectroniella armata (K.Schum.) Robyns, Pygmaeothamnus chamaedendrum (Kuntze) Robyns and
Vangueriella spinosa (Schumach. & Thonn.) Verdc.
The name ‘spiny’ is somewhat misleading as spiny
taxa are not uncommon in other clades as well
(e.g. Cuviera and Rytigynia).
3. As in all previous studies of Vanguerieae, our
study finds the Fadogia Schweinf./Rytigynia
Blume group as a clear and distinct clade in the
tribe. The representatives of this group all have
unique indels in the investigated DNA regions.
The internal topology of this clade is still unclear.
Our phylogenetic tree indicates several suprageneric
groups with good support and these are not in contradiction with the findings of Lantz & Bremer
(2004). The molecular data show a supported clade
containing Cuviera s.l. (including subgenus Globulostylis) and Vangueriella (except V. spinosa) (Fig. 1). In
this clade three distinct groups are strongly supported: C. subgenus Cuviera, C. subgenus Globulostylis and Vangueriella.
In our opinion there are three possible options for
defining phylogenetic groups: (1) placing all species in
a large genus Cuviera containing three subgenera
Cuviera, Globulostylis and Vangueriella; (2) maintaining the taxonomy as it is now with the genera Cuviera
s.l. and Vangueriella; and (3) reinstating Globulostylis
as a genus and recognizing three genera. A major
inconvenience of an enlarged Cuviera is that it would
become quite heterogeneous and difficult to define
morphologically; for example, in relation to Vangueria. Even in the current sense, Cuviera is quite
heterogeneous and not easily separated from Vangueriella based on morphological characters. In addition, the monophyly of Cuviera + Globulostylis is not
supported by molecular data. We favour option 3,
which allows the formation of more homogeneous
(and molecularly well-supported) groups (see Table 1
for distinguishing characters); the problematic case of
Cuviera le-testui Pellegr. is discussed below. We therefore recognize three genera, Cuviera, Globulostylis
and Vangueriella. These are briefly discussed further,
as well as species excluded from Cuviera.
CUVIERA
SENSU STRICTO
Cuviera, now considered in a narrower sense, is
revised here and includes ten species from West and
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410
B. VERSTRAETE ET AL.
Figure 1. Strict consensus tree of the tribe Vanguerieae based on the combined analysis of seven DNA markers.
Bayesian posterior probabilities/bootstrap values are indicated below the branches.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
411
Table 1. Main distinguishing characters between Vangueriella, Globulostylis and Cuviera
Vangueriella
Globulostylis
Cuviera s.s.
C. le-testui
Ovary
Inflorescences
Bilocular
Many-flowered
Pentalocular
One- to five-flowered
Bilocular
Many-flowered
Bracts at lowest
node
Corolla lobes
(shape)
Present/absent
Present
Pentalocular
Three- to
many-flowered
Absent
Present
Narrow, at most equalling
tube (occasional
appendages not
included)
Plain green or yellow
Rather broadly triangular,
variously shorter or
longer than tube
Narrow, longer than
tube
Narrow, longer
than tube
Plain green or yellow
Plain green
Slender
Swollen in lower half
(sometimes slightly so)
Absent
Absent
Striped (see note under
C. trilocularis)
Slender, rarely
(C. pierrei) thickened
in upper two-thirds
Usually present
Corolla lobes
(colour)
Style
Ant holes
in twigs
Central Africa. Most of these species form a rather
homogeneous group that is well characterized, in particular by their striped petals, many-flowered inflorescences and (usually) ant holes in the twigs. The
bracts are recaulescent (Hallé, 1960), which means
they are moved to the upper node. Therefore, the first
node of the inflorescence is bare and the lowest bracts
are inserted at the second node (or on the lateral
pedicels if the inflorescence is unbranched).
Three species are more or less atypical and need
some discussion. Cuviera trilocularis Hiern lacks ant
holes in the twigs (which is sometimes also the case in
the type species, C. acutiflora) and has few-flowered
inflorescences, but matches Cuviera in other characters (e.g. style, bracts). We did not obtain enough
DNA data of this species to include it in the general
analysis, but when analysing the trnL-F marker,
C. trilocularis clearly belongs to the Cuviera s.s.
clade.
Cuviera pierrei also has few-flowered inflorescences
and the style is thickened in the upper two-thirds,
which is reminiscent of Globulostylis (although in the
latter the style swelling occurs in the lower half).
Presumably for these reasons, it was included in
subgenus Globulostylis by Onana (2008). However,
the striped corolla lobes, twigs with ant holes and the
lowest node of the inflorescence lacking bracts (these
are inserted halfway on the pedicels of the lateral
flowers) are clear differences with Globulostylis and
place this species in Cuviera s.s.
Cuviera le-testui is certainly the most aberrant
species (Table 1). It is presumably related to Cuviera
s.s. in having ant holes in the twigs, many-flowered
inflorescences and corolla lobes longer than the tube,
Slender
Present
but differs in its bilocular ovary, plain green corolla
lobes and in having a pair of bracts at the lowest node
of inflorescence (the other bracts are recaulescent and
therefore the second nodes of the inflorescence are
bare; Hallé, 1960). Its peculiar characters could well
justify the creation of a new genus, but we think this
would be premature given the lack of genetic data. We
therefore provisionally keep it in Cuviera s.s.
GLOBULOSTYLIS
Globulostylis is reinstated with eight species, including three newly described (G. dewildeana, Fig. 2;
G. rammelooana, Fig. 3; and G. robbrechtiana, Fig. 4)
and two newly transferred from Cuviera (G. leniochlamys (K.Schum.) Sonké, O.Lachenaud & Dessein
and G. uncinula (N.Hallé) Sonké, O.Lachenaud &
Dessein). The main characters of Globulostylis are the
few-flowered inflorescences with a pair of bracts at
the apex of the peduncle and the style with a swelling
(sometimes rather slight) in the lower half. The genus
is quite homogeneous; the only slightly atypical
species is G. cuvieroides Wernham, which has narrow
calyx lobes.
VANGUERIELLA
A remarkable finding is that Vangueriella is polyphyletic; most of the species studied [including V. laxiflora (K.Schum.) Verdc., the type of the genus] form a
well-supported clade related to Cuviera but V. spinosa
(Schumach. & Thonn.) Verdc. (the type species of
section Stenosepalae) is related to Canthium, as
already found by Lantz & Bremer (2004). This is not
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B. VERSTRAETE ET AL.
Figure 2. Globulostylis dewildeana. A, flowering twig. Bracts are represented by dotted lines. B, stipule. C, flower bud.
D, open flower. E, style. F, cross section of ovary. G, fruit. [Based on: J.J.F.E. de Wilde 7886 (A–F); Letouzey 9843 (G)].
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
413
Figure 3. Globulostylis rammelooana. A, flowering branch. Bracts are represented by dotted lines. B, stipule. C, flower
bud. D, open flower. E, style. F, cross section of ovary. G, fruit. H, pyrene. [Based on: Sonké & Simo 4671 (A, B); Sonké
& Simo 4711 (C–F); Sonké & Taedoumg 4464 (G, H)].
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
414
B. VERSTRAETE ET AL.
Figure 4. Globulostylis robbrechtiana. A, flowering branch. Bracts are represented by dotted lines. B, stipule. C, flower
bud. D, calyx. E, open flower. F, style. G, cross section of ovary. H, fruit. I, pyrene. [Based on: Elad et al. 1554 (A); Sonké,
Taedoumg & Simo 4868 (B–G); Lisowski 1571A (H, I)].
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
KEY
TO
CUVIERA
AND
415
GLOBULOSTYLIS
1. Inflorescence three- to many-flowered, the lowest node lacking bracts (except C. le-testui); style slender,
rarely (C. pierrei) thickened in the upper two-thirds; twigs frequently with ant holes; corolla lobes usually
with a median stripe ............................................................................................................Cuviera
1’. Inflorescence one- to five-flowered with a pair of bracts at lowest node (often caducous in fruit); style
swollen in the lower half (sometimes slightly so); twigs without ant holes; corolla lobes plain green or
yellow, not striped .........................................................................................................Globulostylis
so unexpected as V. spinosa (and several other species
of section Stenosepalae) differ quite markedly from
the rest of the genus in floral characters, lacking a
ring of deflexed hairs inside the corolla tube and
having vestigial or subulate (rather than foliaceous)
calyx lobes. Interestingly, Vangueriella rufa (Robyns)
Verdc., placed in section Stenosepalae by Verdcourt
(1987), is sister to V. discolor (Benth.) Verdc. of
section Vangueriella (which it indeed closely resembles in flower, leaf and fruit). This species has the
calyx lobes narrower than usual in section Vangueriella, but still clearly foliaceous, and the corolla tube
has a ring of deflexed hairs inside, as in section
Vangueriella.
This shows that the circumscription of Vangueriella
has to be redefined, which will be the object of a
future study. Most species of section Stenosepalae will
probably have to be transferred to Canthium. Lantz &
Bremer (2004) already transferred V. spinosa (as Canthium stenosepalum Lantz), but this has not been
widely followed in the literature (e.g. Hawthorne &
Jongkind, 2006 still used V. spinosa).
SPECIES
EXCLUDED FROM
CUVIERA
Six Cuviera spp. should be excluded from the genus
based on morphological and/or molecular data, but at
present cannot be transferred to other genera. These
are C. calycosa Wernham, C. nigrescens (Scott-Elliott
ex Oliv.) and the four East African species (C. midgeodii Verdc., C. schliebenii Verdc., C. semseii Verdc.
and C. tomentosa Verdc.). All these species differ from
both Cuviera s.s. and Globulostylis in having the
inflorescences borne on old woody twigs below the
leaves. However, they do not form a homogeneous
group and further studies, especially in the Vangueria
group, are crucial to understand their position.
Cuviera calycosa, C. nigrescens and C. semseii are
closely related and, in fact, may even be conspecific.
The first two were already indicated as the least
typical species of the genus by Hallé (1960). They
have a pentalocular ovary, as usual in Cuviera, but
differ in (1) inflorescence position, (2) pyrenes with a
sharp dorsal crest, (3) small, black-drying leaves with
tuft domatia in nerve axils, and (4) twigs that become
woody soon, with the bark peeling off. The molecular
data (for C. semseii only) suggest an affinity with
Vangueria. Further studies are required before these
species can be transferred to either Vangueria or a
new genus.
Cuviera schliebenii and C. tomentosa have a bilocular ovary and small flowers, two characters reminiscent of Vangueriella, but the molecular data for
C. schliebenii rather suggest an early branching position in the Vangueria group. Until the generic relationships in this group are better understood, we
cannot suggest a generic placement.
The last species, C. migeodii, is only known from
the poor type and is therefore difficult to place, but is
clearly not a Cuviera s.s. The small, black-drying
leaves with tuft domatia resemble C. nigrescens, but
the ovary is described as bilocular.
In conclusion, we here reinstate Globulostylis as a
genus and we describe three new species, bringing the
total to eight species. The remaining ten species are
placed in Cuviera s.s. Four East African species,
C. calycosa and C. nigrescens are aberrant and are
excluded from Cuviera. Vangueriella is shown to be
paraphyletic with V. section Stenosepalae related
to the ‘spiny’ group and V. section Vangueriella to
Globulostylis.
TAXONOMIC
TREATMENT
Keys to the genera Cuviera and Globulostylis to their
respective species and a detailed species list, including the description of the three new Globulostylis spp.
(G. dewildeana, G. rammelooana and G. robbrechtiana) are presented. Species excluded from Cuviera
are listed at the end.
CUVIERA DC., Ann. Mus. Hist. Nat. 9: 222. 1807. nom.
cons.
Type species: Cuviera acutiflora DC., Ann. Mus. Hist.
Nat. 9: 222. 1807.
Description: Small trees or shrubs, 1–14 m high, evergreen, with regular horizontal branching (Roux’s
architectural model); vegetative parts glabrous or
rarely puberulent; twigs usually with swollen and
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B. VERSTRAETE ET AL.
hollow internodes, inhabited by ants (solid in C. trilocularis and occasionally in C. acutiflora); young
plants and coppicing shoots frequently armed with
paired supra-axillary spines that sometimes persist
on the trunk. Leaves opposite, ± elliptic, shortly petiolate; stipules small, ± basally connate, not or shortly
(< 2 mm) awned, caducous to ± persistent. Inflorescences axillary and paired at each node on young
twigs, cymose, three- to many-flowered; bracts linear
to broadly elliptic, ± leafy, but absent at lowest node
of inflorescence (except in C. le-testui), inserted at the
base of pedicels (or towards the middle in C. pierrei).
Flowers hermaphrodite. Calyx lobes three to five, free
or shortly connate at base, ± leafy, linear to broadly
ovate and usually longer than the corolla, or rarely
truncate calyx (C. truncata). Corolla tube campanulate to nearly cylindrical, glabrous outside, with a
ring of reflexed hairs near the middle inside; lobes
five, longer than tube, elongate, acute to longapiculate at apex, spreading or reflexed, glabrous,
usually green with a white to pink median stripe
(apparently plain green in C. le-testui). Stamens five,
inserted in upper part of tube, anthers partly to fully
exserted (frequently reflexed between the lobes).
Ovary (bi-) pentalocular, obconic or turbinate, sometimes five-angled; ovules solitary in each locule, pendulous. Disk ± flat, glabrous or hairy in the centre.
Style exserted, narrowly cylindrical or (in C. pierrei)
thickened in the upper two-thirds, stiffly pubescent to
glabrous; stigmatic club ± mitriform, shortly (two-)
five-lobed. Fruits drupaceous, apparently remaining
green, large 2.0–3.7 × 1.8–3.3 cm, subglobose to
obovoid, smooth to variously lobed, with calyx
generally persistent (sometimes tardily caducous);
pyrenes (two-)five, one-seeded, shaped like a mandarin orange segment, usually with a faint dorsal crest,
and a slight ventral indentation towards the upper
third.
Distribution and ecology: Cuviera has ten species in
the Guineo–Congolian rainforest zone (including Bioko
Island). The centre of diversity is in Lower Guinea;
only two species occur in Upper Guinea (C. acutiflora
and C. macroura) and only one extends into Congolia
(C. angolensis). Most species are relatively light
demanding, favouring secondary or riverine forest,
although some can be found in the understory as
well. They are frequently gregarious, especially
C. physinodes that may form dense thickets locally.
Notes: The most important characters for species
identification in Cuviera are the calyx lobes, the
corolla and, to some degree, the fruits. Leaves are of
limited value, as in many species they are quite
variable; for example, the leaf base can be acute to
subcordate. However, an experienced researcher can
identify most of the sterile collections if the origin is
taken into account.
Several aspects of the biology of Cuviera would be
interesting to study in the field, in particular the
association with ants, which presumably play a role
in protecting the plant (although in our experience
they are not aggressive to humans). Whether different Cuviera spp. have different associated ants is not
known.
Not much is known about the pollination of the
flowers, which are quite attractive and often fragrant
(e.g. those of C. macroura smell of honeysuckle), or
about the dispersal of the fruits (although, considering the size of the pyrenes, large animals are presumably involved).
Cuviera spp. are rarely used by humans, although
at least two species (C. le-testui and C. longiflora)
have edible fruits, and the leaves of C. angolensis
subsp. latior are eaten as a vegetable in the Democratic Republic of the Congo (according to Pynaert 11,
BR).
1. CUVIERA ACUTIFLORA DC., Ann. Mus. Hist. Nat. 9:
222. 1807. Type: SIERRA LEONE. s.loc., Smeathman s.n. (type: BM, see Notes).
Synonyms: Cuviera africana Spreng., Syst. Veg. 1:
760. 1824. Type: not traced.
Vangueriopsis coriacea Robyns, Bull. Jard. Bot.
État 22: 319. 1952. Type: LIBERIA. 3 miles north-east
of Suacoco, Traub 299 (holotype: BR000000882973!;
isotypes: BM000903517!, BR000000882965!, MO n.v.).
Distribution: Lower and Upper Guinea Domain: Cameroon, Equatorial Guinea (Rio Muni), Ghana (see
Notes), Guinea, Ivory Coast, Liberia, Nigeria, Sierra
Leone and Togo (see Notes).
Notes: Cuviera acutiflora is closely related to
C. physinodes and C. truncata; the three species share
coriaceous leaves and glabrous, shortly exserted styles.
Cuviera acutiflora is a widespread and polymorphic
species, especially in West Africa where the leaf base
varies from cuneate to asymmetrically cordate; specimens from Cameroon and Equatorial Guinea always
have cordate leaf bases (which allows them to be
separated from C. physinodes). Ant holes in the twigs
can be present or absent, apparently irrespective of
locality. Some Nigerian specimens are intermediate
with C. truncata (see that species).
The species has been reported from Ghana (Hepper
& Keay, 1963) and Togo (Brunel, Hiepko & Scholz,
1984), which seems likely on geographical grounds,
but we have not seen the specimens. Records of
C. acutiflora from Gabon (Sosef et al., 2006) refer to
C. physinodes.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
KEY
TO THE
CUVIERA
417
SPECIES
1.
Ovary and fruits bilocular; inflorescence many-flowered with a pair of large bracts at the lowest node;
apex of flower buds with reflexed appendages (Gabon to south-west Democratic Republic of the Congo)
......................................................................................................................................C. le-testui
1’. Ovary and fruits pentalocular; no bracts at lowest node of inflorescence; flower bud appendages, if
present, never reflexed .................................................................................................................2
2. Calyx truncate or with short (< 2 mm) irregular lobes (Nigeria and south-west Cameroon) .C. truncata
2’. Calyx lobes conspicuous, 4 mm long at least (sometimes caducous on fruit) .................................... 3
3. Calyx lobes three(–four), the fourth lobe when present often slightly smaller; style hairy, long exserted
.................................................................................................................................................. .4
3’. Calyx lobes five ...........................................................................................................................5
4. Calyx lobes narrowly lanceolate, of about the same width throughout, 2.5–4.0 mm wide (west Angola and
south-west Democratic Republic of the Congo) ...................................C. angolensis subsp. angolensis
4’. Calyx lobes ovate, conspicuously widened above the base, 2.5–23.0 mm wide (Gabon to north-east
Angola) ...................................................................................................C. angolensis subsp. latior
5. Leaves thick and coriaceous, tertiary nerves invisible or lax; corolla lobes not (or shortly) apiculate ..
.................................................................................................................................................. .6
5’. Leaves not markedly thick, tertiary nerves apparent, usually dense (sometimes laxer in C. subuliflora);
corolla lobes often with a filiform appendage (lacking in C. pierrei) ............................................... .9
6. Inflorescence three- to five-flowered, very lax; twigs lacking ant holes (Nigeria and south-west Cameroon) .......................................................................................................................C. trilocularis
6’. Inflorescence many-flowered (but often with few fruits developing); twigs usually with ant holes,
sometimes lacking in C. acutiflora ................................................................................................7
7. Style hairy, exceeding corolla throat by 8–10 mm; corolla lobes 10–25 mm long; fruit large, 3.2–3.7 × 2.3–
3.3 cm when dry, on long (1.5–2.0 cm) and much-thickened pedicel (Nigeria to the Central African
Republic) .....................................................................................................................C. longiflora
7’. Style glabrous, exceeding corolla throat by 2–3 mm only; corolla lobes 5–9 mm long; fruit smaller,
2.0–3.2 × 1.8–2.2 cm when dry, on short pedicel (0.5–1.0 cm) .......................................................... 8
8. Corolla tube broad (throat 4–5 mm wide); flower buds conical, conspicuously broadening towards base;
anthers reflexed between corolla lobes; bracts and calyx lobes narrow, 0.5–2.0(−4.0) mm wide; fruit
broadly ellipsoid, 1.9–2.5 × 1.5–2.2 cm, drying generally lobed; leaf base variable, cuneate to subcordate
(Guinea to Rio Muni) ...................................................................................................C. acutiflora
8’. Corolla tube narrow (throat c. 2 mm wide); flower buds almost cylindrical, not broadening towards
base; anthers erect; bracts and calyx lobes ovate to lanceolate, broader, (2-)3–8 mm; fruit narrowly
ellipsoid, c. 3 × 2 cm, drying smooth; leaf base always cuneate (south Cameroon to south Gabon)
............................................................................................................................... ..C. physinodes
9. Calyx lobes almost filiform, 5–15 mm long, < 1 mm wide, fused at base into a short cup; domatia present
as small glabrous holes in axils of nerves; calyx lobes caducous on fruit (Guinea to Cameroon)
...................................................................................................................................C. macroura
9’. Calyx lobes broader, (12–)16–50 mm long, (1.2–)2.0–5.0 mm broad, not forming a cup at base; domatia
absent; calyx lobes persistent (but sometimes damaged) on fruit ................................................. .10
10. Inflorescence seven- to many-flowered (but only one fruit may develop); bracts long (> 2 cm), approximately equalling the sepals; corolla lobes ending in a filiform appendage; fruit broadly truncate at apex,
with the calyx lobes patent and star-like (Nigeria to south-west Democratic Republic of the Congo, also
Bioko) .......................................................................................................................C. subuliflora
10’. Inflorescence two- or three- (five-) flowered; bracts small (< 1 cm), much shorter than the sepals; corolla
lobes not appendaged; calyx lobes erect on fruit (Equatorial Guinea and Gabon) .................C. pierrei
The typification of C. acutiflora needs further investigation. Two Smeathmann sheets in BM are probably
part of the original gathering, but it is not clear
whether De Candolle saw them. There might be other
sheets in P, where De Candolle worked, so we have
not chosen a lectotype.
Additional specimens examined: CAMEROON.
Batanga, Apr 1895, Bates 98 (K); 9 km north of Kribi,
27 Feb 1969, Bos 4010 (P, WAG, YA); ibid., 30 Oct
1969, Bos 5556 (BR, K, P, WAG, YA); Ibid., 9 Nov
1970, Bos 6118 (BR, K, P, WAG, YA); km 20, CampoKribi, 10 Nov 1970, Bos 8706 (YA); ibid., 4 Dec 1975,
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
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B. VERSTRAETE ET AL.
J.J.F.E. de Wilde 8706 (BR, K, P, WAG); Bimbia–
Bonadikombo community forest, 27 Apr 2009, Dessein
et al. 2809 (BR, MO, YA); 8 km north of Kribi, 13 Feb
1997, Elad 530 (WAG); Limbe, 1904, Kalbreyer 29 (K);
Victoria [= Limbe], Nov 1929, Maitland 784 (BR, K);
Ambas Bay, Feb 1861, Mann 770 (K); Cameroon
Mountains, 1862, Mann 1211 (P); Bipindi, 25 Nov
2004, Sonké 3578 (BR); Douala–Nkongsamba road,
north Maleke, 17 Jan 1983, Van der Zon 2021 (P,
WAG, YA); Liwenyi, 31 Nov 1993, Watts 893 (K);
Bipindi, 1903, Zenker 2651 (BM, BR, HBG, K, P,
WAG); ibid., 1908, Zenker 3594 (BM, BR, HBG, K, P);
ibid., Jun 1913, Zenker 264 (BR, P).
EQUATORIAL GUINEA. Rio Muni: zona do Bairro
Ikundi, 23 Jun 1991, Carvalho 4749 (WAG); Rio
Ndote, 7 Jun 1999, Eneme 304 (BRLU, WAG).
IVORY COAST. Km 25 Sassandra–Gagnoa, 30 Oct
1968, Breteler 5860 (BR); near Abidjan, Banco Forest
Park, 9 Jan 1976, de Koning 6377 (BR); c. 140 km
north of Tabou, 10 Oct 1963, W.J.J.O. de Wilde 1054
(K); Abidjan, 24 Aug 1955, de Wit 801 (WAG); Adiopodoumé, Oct 1960, F. Hallé 188 (K); ibid., Oct 1960,
F. Hallé 198 (BR); Abouabou, 9 Jan 1959, Leeuwenberg 2348 (K); N Sékré, Oldeman 603 (K); Yapo, 28
Oct 1954, Roberty 15338 (K).
LIBERIA. Nimba, 8 Jan 1965, Adam 20500 (K);
near Tobli on the Tapeta–Chien road, 14 Jan 1967,
Bos 2769 (BR); Sinoe to port, 17 Jan 1969, Jansen
1129 (BR); Gibi Mountain, 5–10 miles south-east of
Salala, 15 Jan 1970, Jansen 1708 (BR); Bendu,
10 miles north of Robertsport, 30 Jan 1970, Jansen
1761, (BR); 4 miles north of Monrovia, 16 Nov 1970,
Jansen 2296 (BR); 6 miles from to Monrovia, 1904,
Johnston s.n. (K); Monrovia, 12 Nov 1926, Linder
1539 (K); Gola–Yoma National Forest, 12 Nov 1965,
van Meer 274 (BR); 27 km south of Zwedru, 22 Feb
1966, van Meer 481 (BR); Paynesville, 8 miles east of
Monrovia, 23 Oct 1960, Voorhoeve 95 (BR).
NIGERIA. Unnokoo, 5 Nov 1967, Ariwaodo 1080
(K); Epe, 28 Nov 1994, Daramola 589 (K); Milken
hill, Enugu, 11 Jul 1964, Daramola 55162 (WAG);
Ipe–Ikum road, 15 May 1978, Daramola & Ihe 420
(WAG); Shasha Forest Reserve, 10 Nov 1961,
Emwiogbon 43535 (WAG); Lagos, Oct 1905, Foster 25
(K); boundary of Nigerian College site, Ibadan (site
of new sports field), Nov 1960, Hambler 1100 (BR);
road from Imesi–Igtayo, 23 Oct 1972, Latilo &
Fagbeni 67515 (WAG); Enugu, 21 Feb 1973, Latilo &
Oguntayo 67624 (WAG); Kwanya, Dec 1892, Millen 6
(K); Unekpara road, 31 Jan 1974, Odewo 67030
(WAG); Akpaka Forest Reserve, 20 Nov 1958, Okele
& Latilo 38439 (WAG); Ibadan, south reserve, 14
Dec 1943, Onochie 7495 (P); Gambari Forest
Reserve, south-west Ibadan, 16 Jan 1958, Onochie &
de Wit 678 (WAG); W Lagos, Rowland s.n. (P); Udi
Forest Reserve (Enugu), Oct 1928, Smith 9 (K);
Eket, 1913, Talbot 3300 (K); Oban, Talbot 286b (K);
Owena Forest Reserve, 28 Oct 1948, Ujor 23920 (P);
Ibadan, 16 May 1966, van Eijnatten 1516 (WAG);
s.loc., van Meer 989 (WAG);
SIERRA LEONE. s.loc., Afzelius s.n. (BM); s.loc.,
Don s.n. (K000412059); Mount Aureol, Freetown, 2
Apr 1967, Gledhill 531 (BR); Freetown, 24 Jan 1883,
Johnston 50 (K); Leicester Peak, 4 Dec 1891, ScottElliott 3898b (K); Nyungeru, 5 Jan 1914, N.W.
Thomas 7232 (K); Bo, Jan 1914, N.W. Thomas 7418
(BR); Komana, 10 Jan 1914, N.W. Thomas 7648 (K).
2. CUVIERA ANGOLENSIS WELW. EX K.SCHUM., Nat.
Pflanzenfam. 4(4): 94. 1891. Type: ANGOLA.
Golungo Alto, Alta Queta, Apr 1855, Welwitsch
2564 (lectotype designated here: BM000903514!;
syntypes:
BM000903515!,
BM000903516!,
K000412037!,
K000412038!,
LISU208621!,
LISU208622!, LISU208623!, M0106328!).
Notes: Cuviera angolensis is closely related to C. longiflora, in particular in the long-exserted hairy style.
However, it is hard to understand why Hepper & Keay
(1963) synonymized the two species, which have different calyces (C. angolensis: three or four narrowly
lanceolate and acute lobes; C. longiflora: five broadly
elliptic and rounded lobes). The corolla lobes are also
generally longer and narrower in C. longiflora.
Cuviera angolensis is, however, closely related to
C. latior and, after reviewing all available material of
both taxa, we concluded that the latter is a subspecies
of the former. The only distinction between them
concerns the calyx lobes (see Key). The two subspecies
also have separate ranges.
The specimen McPherson 16297 referred to as
C. angolensis in previous phylogenetic studies (Lantz
et al., 2002; Lantz & Bremer, 2004, 2005) is actually
C. physinodes. Several Welwitsch collections made on
different dates were given the same number 2564, as
is usual with this collector (Albuquerque, Brummit &
Figueiredo, 2009). The lectotype chosen here was collected in April 1855 and a complete description of the
new species is attached to the specimen, hence the
lectotypification.
2A. CUVIERA ANGOLENSIS Welw. ex K.Schum. subsp.
ANGOLENSIS.
Distribution: Congolia Domain: north-west Angola,
Democratic Republic of the Congo (Bas–Congo).
Additional specimens examined: ANGOLA. Cuanza
Sul, Libollo Hochland, 1954–1955, Boss 5755 (BM);
Calandula Mountain, Libulo, 18 May 1915, Gossweiler 6314 (BM).
DEMOCRATIC REPUBLIC OF THE CONGO.
M’vuazi, Malanga Forest, 23 Sep 1951, Devred 727
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
(BR); M’vuazi, Mansiesie Forest, 25 Sep 1951, Devred
755 (BR, K); Massif of Matete (Mvuazi); Thysville, 15
Jun 1954, J. Dubois 23 (BR); Nzengi Nzengi forest, 1
Aug 1958, J. Dubois 328 (BR, K); Kisantu, 1900,
Gillet 1076 (BR); near N’Gidinga, bank of Mosi river,
Sep 1923, Gillet s.n. (BR, K).
2B. CUVIERA
ANGOLENSIS
SUBSP.
LATIOR
(WERNHAM) SONKÉ, O.LACHENAUD & DESSEIN
stat. nov. Basionym: Cuviera latior Wernham,
J. Bot. 56: 311. 1918. syn. nov. Type: DEMOCRATIC REPUBLIC OF THE CONGO. N
Boyeka, 31 Aug 1914, Nannan 139 (lectotype
designated here: BR0000008829580!; isolectotypes:
BM000903511!,
BR0000008829665!,
K000412047!).
Synonyms: Cuviera latior var. evorombila N.Hallé,
Bull. Soc. Bot. France 106: 344. 1960. syn. nov. Type:
GABON. Evorombil, 4 Jul 1934, Le Testu 9627 (holotype: P!; isotypes: BM!, BR!, MO!, WAG!).
Cuviera latior var. hispidula N.Hallé, Bull. Soc.
Bot. France 106: 344. 1960. syn. nov. Type:
CENTRAL AFRICA REPUBLIC. 60 km south-east
of Bambari, Gbongo river, Pudjeyo, 15 Jan. 1928,
Tisserant 2404 (holotype: P!; isotypes: BM!,
BR0000008846846!,
BR0000008829672!,
K000412046!, MO-391362!, P00553439!).
Distribution: Lower Guinea and Congolia Domains:
north-east Angola, Central African Republic, Democratic Republic of the Congo (widespread except in
south), north-east Gabon (Ivindo basin), Republic of
Congo.
Notes: Unlike the rather uniform subsp. angolensis,
subsp. latior is variable, especially in the width of the
calyx lobes (some specimens approaching subsp.
angolensis) and in the size of the corolla lobe appendages that vary from 6 mm long to nearly lacking.
The leaves are sometimes shortly pubescent on the
nerves beneath, which is unique in Cuviera. This
character may vary on a single specimen, so Hallé’s
(1960) var. hispidula has not been maintained, nor
var. evorombila (separated only on account of its less
pubescent style). The tertiary veins are typically
obscure, but in a few specimens (e.g. Gilbert 14345,
M. Laurent 669) they are apparent and rather dense.
Additional specimens examined: ANGOLA. Dundo, 2
Jun 1948, Gossweiler 14023 (BM, K, P).
CENTRAL AFRICAN REPUBLIC. near Bambari,
6 km on Alindao road, 20 Dec 1963, Descoings 11840
(MPU); hill near Bangui, 5 Jan 1961, Guigonis 2031
(P); 100 km south of Yalinga, road to Bangassou, 24
Nov 1922, Le Testu 4386 (BM, BR, P); Kpalata river,
419
Tisserant 437 (P); Boukoko, 14 Jan 1948, Tisserant
614 (BM, P); Boukoko, 8 Mar 1951, Tisserant 2030
(BM, P); Gbondo river, Pudjiya, 15 Jan 1928, Tisserant 2483 (P); Mbaïki, 5 Jan 1961, Tisserant 3692 (P).
DEMOCRATIC REPUBLIC OF THE CONGO.
Epulu, 27 Feb 1998, Amsini 097 (BR); Island of
Elelwa, 19 Apr 1960, Bamps 932 (BR, K); Metmas, 13
Jan 1915, Bequaert 160 (BR); Molima (Yambuya),
Bequaert 1358 (BR); Penghe, Bequaert 2461 (BR);
Masisi–Walikale, 31 Dec 1914, Bequaert 6429 (BR);
Manyema, 1909, Berger s.n. (BR); 5 km west of Kisangani, 9 Feb 1971, Bokdam 3085 (WAG); ibid., 1 May
1971, Bokdam 3180 (WAG); Yangambi–Yaselia road,
25 Jun 1963, Bolema 1144 (BR); Yangambi, 17 Jan
1961, Bolema 343 (BR); s.loc., Boone 57 (BR);
Namoya, Kabazimba to north, Bytebier 232 (BR);
Hemptinne St Benediktus, 1911, Callewaert s.n.
(BR); Mutakato, km 120 Kavumu–Walikale road, 10
Aug 1956, Christiaensen 1818 (BR, K); Eala,
Corbisier-Baland 1399 (BR); ibid., Corbisier-Baland
1524 (BR); ibid., Corbisier-Baland 1717 (BR);
Gangala na Bodio, 24 Mar 1943, Cornet D’ Elzius Du
Chenoy, Lauwers & Offermann 808 (BR); Yangambi,
1948, Gilbert 8424 (BR); Eala, 10 Sep 1937, Coûteaux
325 (BR); Kiyaka, 11 Jul 1955, Devred 2140 (BR);
Bas-Uele, 5 Oct 1934, Dewulf 203 (BR); ibid., 27 Dec
1934, Dewulf 523 (BR); Yangambi, 3 Oct 1950, Donis
2847 (BR); ibid., 8 Jan 1952, Donis 3336 (BR); ibid.,
30 Jan1952, Donis 3501 (BR); Boyagidigba, 23 Apr
1955, Evrard 755 (BR); Mangala (Terr. Isangi), 19
Mar 1957, Evrard 2252 (BR); Befale, 2 Jan 1958,
Evrard 3179 (BR, K); Eandja, 13 Feb 1958, Evrard
3423 (BR, K); Djolu (Bolomba), 20 Feb 1959, Evrard
5791 (BR, K); [Yionda], 15 km south of Mbandaka
(Zaire), 18 Feb 1987, Evrard 10688 (BR); Epulu, 16
Nov 1993, Ewango 199 (BR); s.loc., Flamigni 6122
(BR); km 37 Elundu-Kindu, 22 Jul 1957, Gaillez 65
(BR); Bambesa, 12 Feb 1953, Gerard 552 (BR); Likati,
22 Mar 1956, Gerard 2212 (BR); Madabu (Zobia), 6
Dec 1956, Gerard 2570 (BR); Bambesa, 31 Jan 1958,
Gerard 3232 (BR); Bambesa, 12 Nov 1957, Gerard
3300 (BR); Tukpwo, 12 Feb 1958, Gerard 3540 (BR);
Bambesa, 8 Jan 1960, Gerard 4015 (BR); ibid., 14 Nov
1963, Gerard 5706 (BR); around Yaosuka, Yangambi,
May 1937, Gilbert 26 (BR); ibid., May 1937, Gilbert 26
(BR); s.loc., Mar 1938, Gilbert 974 (BR); Yaosuka,
Gilbert 1341 (BR, K); ibid., Gilbert 1410 (BR);
Yangambi, INEAC Forest Reserve, 1948, Gilbert 9046
(BR); Yangambi, 1949, Gilbert 9961 (BR); Botaka,
Lake Leopold II, 4 Jul 1953, Gilbert 14345 (BR); Beni,
Gille 255 (BR); Bikoro, Dec 1920, Goossens 2321 (BR);
near Lula, Apr 1921, Goossens 2511 (BR); Lisala, Mar
1924, Goossens 4641 (BR); Busanga, Feb 1953, Gorbatoff 78 (BR); Manyema, Mutongo, 30 Oct 1957,
Gutzwiller 3321 (BR); Epulu, 6 Apr 1991, Hart 1114
(BR, K); ibid., 27 Feb 1983, Hart 382bis (BR);
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B. VERSTRAETE ET AL.
Bambesa, 11 Jan 1940, Hendrickx 869bot (BR);
Bolima, 31 Oct 1941, Hulstaert 471 (BR); Bokote,
1943, Hulstaert 953 (BR); Boende, 28 Jul 1944, Hulstaert 1354 (BR, K); s.loc., Jans s.n. (BR); bank of
Congo river, near Bolombe, 2 Jan 1904, M. Laurent
s.n. (BR); Eala (Ikakéma), 29 Jan 1904, M. Laurent
s.n. (BR); Isangi, 13 Jan 1904, E. Laurent & M.
Laurent 11 (BR); near Lié, 7 Jan 1904, M. Laurent 13
(BR); Eala, 1905, M. Laurent 669 (BR); ibid., 10 Oct
1906, M. Laurent 1216 (BR); ibid., 28 Oct 1906, M.
Laurent 1256 (BR); ibid., Jun 1906, M. Laurent 1571
(BR); Yaligimba, 1988, Le Jeune 60 (BR, K, WAG);
Bamania, Aug 1930, Lebrun 890 (BR); between
Libenge and Gemena, Lebrun 1871 (BR, K); ibid.,
Lebrun 2186 (BR); between Niangara and Wamba,
Jul 1931, Lebrun 3228 (BR); between Walikale and
Kalehe, Mar 1932, Lebrun 5240 (BR); Urega, Jun
1932, Lebrun 5634 (BR); between Kindu and Katakokombe, Lebrun 6073 (BR, K); Eala, 1936, Leemans
295 (BR); ibid., 1936, Leemans 475 (BR); Kisangani,
500 m SE Kabondo, 30 Apr 1977, Lejoly 1424 (BR);
Kisangani, near bac of Simi-Simi, Jun 1977, Lejoly
1928 (BR); Kisangani, Island of Mayele near Wagenia,
13 May 1978, Lejoly 3572 (BR); Kisangani, 13 Nov
1981, Lejoly 81/289 (BR); Kabunga, 17 Feb 1958,
A. Léonard 1717 (BR); Kamisuku, 18 Aug 1959,
A. Léonard 5946 (BR); between Coquilhatville
[= Mbandaka] and Ileko, 15 Nov 1946, J. Léonard
1020 (BR); Kikwit, 28 Jul 1904, Lescrauwaet 165
(BR); road Hemptinne-Kamwandu (Terr. Dibaya), 21
Jun 1957, Liben 3197 (BR); River Kateba (Terr.
Luisa), 16 May 1957, Liben 3314 (BR); Kisangani,
Tshopo, 22 Nov 1972, Lisowski 15482 (BR, K); Ibid.,
28 Jan 1973, Lisowski 16441 (BR, K); Haut Zaïre,
plantation Lale–Ekili, 14 Nov 1976, Lisowski 43225
(BR); Kisangani, Tshopo, 22 Nov 1972, Lisowski
B9565 (BR); Yangambi, 13 Dec 1935, J. Louis 823
(BR, K, P); île ‘Esali’, en face de Yangambi, 13 Feb
1936, J. Louis 1255 (BR, K); north-west Eala, 20 May
1936, J. Louis 1976 (BR); Yangambi, 26 Jun 1937, J.
Louis 4249 (BR); ibid., 29 Nov 1937, J. Louis 6810
(BM, BR); ibid., 12 Jul 1938, J. Louis 10309 (BR, K,
P); Island of Esali, 15 Oct 1938, J. Louis 11794 (BR);
Yangambi, île Yalututcha, 15 Nov 1938, J. Louis
12583 (BR, K); Opala, J. Louis 14137 (BR); Île
Lotumba, 5 Apr 1939, J. Louis 14483 (BR); Lokutu, 29
Oct 2004, Luke 10412Z (BR); Likimi, 13 Feb 1910,
Malchair 96 (BR); Kikwit/Erco, 21 Nov 1990, Masens
569 (BR); Bikoro, 8 Aug 1983, Nsola 229 (BR); Mabali,
7 Apr 1985, Nsola 845 (BR); Kapanga, 1934, Overlaet
1216 (BR); km 82 road Kavumu–Walikale, 27 Sep
1955, Pierlot 896 (BR); Tshinganda, Mount Kahusi,
km 42 Kavumu–Walikale, 13 May 1959, Pierlot 2904
(BR); Irebu, May 1904, Pynaert 397 (BR); Grelco,
Quarré 2595 (BR); Kikwit, 29 May 1946, Renier 35
(BR); Dundusana, Feb 1913, Reygaert 11 (BR); near
Mobwasa, Dec 1913, Reygaert 1464 (BR); Gandajika,
7 Nov 1957, Risopoulos 698 (BR); Eala, 25 Dec 1905,
Seret 392 (BR); near Eala, Seret 392BIS (BR); Eala,
Nov 1930, Staner 1538 (BR, P); road Weko–
Bengamisa, between Weko and Yalibutu, 14 Mar
1988, Szafranski 1345 (BR); Kisangani, Tshopo area,
km 8 old road to Buta, 5 Jul 1988, Szafranski 1439
(BR); Mobwasa (Itimbiri), 30 Jan 1909, Thonner 126
(BR); La Kulu, Van den Brande 340 (BR); s.loc., Van
Der Gucht 131 (BR); Saint Trudon, Van Kerkhoven
824 (BR); ibid., 18 Aug 1913, Van Kerkhoven s.n. (BR);
Ipamu, Jul 1922, Vanderyst 9804 (BR); ibid., Sep
1921, Vanderyst 10607 (BR); ibid., Sep 1921, Vanderyst 10907 (BR); ibid., Oct 1922, Vanderyst 12293 (BR);
between Lubue 1 and Luange, Oct 1922, Vanderyst
12486 (BR); Hemptinne Saint Benoît, Vanderyst
23677 (BR); Ibid., Vanderyst 23644/4 (BR); Mobwasa,
28 Apr 1914, Vermoesen 324 (BR); Bambesa, 11 Jan
1940, Vrydagh 68 (BR).
GABON. Ivindo, Makokou, 20 Nov 1985, Caraglio
56 (MPU); Ipassa, 10 km south of Makokou, 21 Jul
1978, Florence 1556 (P); Bélinga, Basse Nounah, 1
Dec 1964, N. Hallé 3381 (P).
REPUBLIC OF THE CONGO. Dongou, 28 Jan
1966, Bouquet 2099 (P); Odzala National Park, camp
Mboko, 9 Dec 1993, Diafouka 558 B (BRLU); ibid., 17
Nov 1994, Dowsett-Lemaire 1826 (BR); ibid., 21 Nov
1996, Lejoly 96/753 (BRLU); Kassa, 17 Dec 1926,
Linder 1726 (P); bank of Lekoli river, 6 Feb 1994,
Lisowski c-790 (BRLU, K).
3. CUVIERA LE-TESTUI PELLEGR., Bull. Soc. Bot.
France 81: 142. 1934. Type: GABON. Tchibanga, 13
Apr 1925, Le Testu 2053 (lectotype designated
here:
P00553438!;
isolectotypes:
BM!,
BR0000008846822!,
BR0000008846839!,
K000412042!, LISC002648 n.v., P00553436!,
P00553437!).
Distribution: Lower Guinea Domain: Deomacratic
Republic of the Congo (Bas–Congo), Equatorial
Guinea (Rio Muni), Gabon (Libreville area, Doudou
Mountains, Chaillu Mountains), Republic of Congo
(Mayombe).
Notes: Cuviera le-testui is an aberrant species standing well apart from its congeners in having a pair of
large bracts at the apex of the peduncle and a bilocular ovary. Another remarkable character is the red
exudate in the bark mentioned by two different collectors (A.M. Louis 1684 and Senterre & Obiang
4315). This is exceptional in Rubiaceae, although it
also occurs in a new species of Psydrax Gaertn. (currently under description).
Cuviera le-testui is newly reported from the Republic of Congo and Equatorial Guinea. Material from the
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REVISION OF CUVIERA AND GLOBULOSTYLIS
latter country is sterile, but the identification makes
little doubt.
Additional specimens examined: DEMOCRATIC
REPUBLIC OF THE CONGO. Kimbuya–Kingedi
road, 24 Aug 1959, Compère 154 (BR, K).
EQUATORIAL GUINEA. Rio Muni: Monte Bata,
1 km north of road Bata–Niefang at Santa Marta, 8
Aug 2003, Senterre & Obiang 4297 (BRLU); ibid., 9
Aug 2003, Senterre & Obiang 4315 (BRLU).
GABON. Mourindi, 15 Sep 2000, Bourobou Bourobou 247 (BR, K, P, WAG); Etéké, 15 May 1963, N.
Hallé & Cours 5907 (P); Tchibanga, 2 May 1914, Le
Testu 1720 (BR, BM, P); Mouloumbi, 1 Aug 1930, Le
Testu 8211 (BR); Malibé, 1 km toward west, 7 May
1985, A.M. Louis 1684 (WAG); near Igotchi–Mouenda,
11 May 1997, McPherson 16942 (K, MO); km 23 road
south-east of Igotchi–Mouenda, 19 May 1997,
McPherson 17047 (BR, K, MO); c. 10 km north of
Libreville, 23 Apr 1985, J.M. Reitsma & B. Reitsma
811 (WAG); Mourindi, 16 Apr 2000, Sosef 1312
(BRLU, WAG).
REPUBLIC OF THE CONGO. Sounda, bank of
Kouilou, 10 Jun 1987, de Foresta 1265 (P); Les Saras,
30 Jun 1989, Dechamps 13234 (BR); around M’vouti,
Pounga–Girard road, 10 Jun 1971, Sita 3095 (P).
4. CUVIERA LONGIFLORA HIERN, in D. Oliver, Fl. Trop.
Afr. 3: 157. 1877. Type: CAMEROON. Mount Cameroon, Jan 1862, Mann 1211 (lectotype designated
here: K000412049!; isolectotype: K000412050!).
Distribution: Lower Guinea Domain: Cameroon
(widespread in the west, centre and east), Central
African Republic (extreme west), Equatorial Guinea
(Bioko Island), north-east Gabon (Bélinga), east
Nigeria.
Notes: Cuviera longiflora is closely related to C. angolensis, but we cannot follow Hepper & Keay (1963) in
uniting them; they especially differ in the number of
calyx lobes (see C. angolensis) and also in the range.
The type of C. longiflora, Mann 1211 (K) has two
sheets, one of which is here selected as lectotype. Note
that Mann 1211 (P) represents another species,
C. acutiflora.
The species can be considered as new to Gabon, as
the two specimens cited for this country by Sosef et al.
(2006) are both misidentified: McPherson 16297 is
C. physinodes and McPherson 16332 is C. calycosa.
Additional specimens examined: CAMEROON.
Sanaga River near Goyoum, 29 Jan 1961, Breteler 963
(WAG); ibid., 29 Jan 1961, Breteler 963 (K, P); 6 km
south-west of Yaoundé, trail to Eloumden Mountain,
29 Dec 1962, Breteler et al. 2318 (BR, K, P, WAG);
421
Kupe village, 24 Jan 1995, Cable et al. 764 (K);
Nyasoso, 6 Feb 1995, Cheek et al. 7305 (K); Bafut–
Ngemba Reserve, 12 Mar 1959, Daramola 40537 (K,
P, WAG); Mount Kupe, above Nyasoso, 24 Apr 2009,
Dessein et al. 2713 (BR, MO, WAG, YA); Mount Kupe,
Etube village, 2 Feb 1995, Elad 101 (K); Aboh, Etuge
3410 (K); Laikom, 3 Dec 1998, Etuge 4538 (K); Ndikiniméki, 24 Dec 1927, Hédin 3 (P); Nkambe, 10 miles
west, 11 Feb 1958, Hepper 1916 (K, P); Mount Bama,
Jan 1939, Jacques-Félix 2986 (P); ibid., Jan 1939,
Jacques-Félix 3021 (P); Koutchankap, Feb 1939,
Jacques-Félix 3042 (P); Bafut–Ngemba Forest
Reserve, 7 May 1960, Keay 37925 (BR, K, YA); Kupe
village, 17 Jan 1995, Lane et al. 298 (K); Mount Kupe,
Ndum, 31 Jan 1995, Lane et al. 460 (K); km 17 Betaré
Oya–Meiganga, 5 km south-east of Ndokayo, 3 Nov
1966, Leeuwenberg 7697 (BR, K, P, WAG, YA); bank of
Sanaga, between Poute and Ebaka, 1 Feb 1960,
Letouzey 2901 (BR, P, YA); river Sanaga, N Goyoum,
20 Jan 1961, Letouzey 3304 (BR, P, WAG, YA); near
Ngoila, 7 Feb 1973, Letouzey 11903 (BR, HBG, P,
WAG, YA); track from Acha–Abaw towards lake Oku,
40 km north-east Bamenda, 5 Dec 1974, Letouzey
13450 (P, YA); Tinachong, 30 km west-north-west of
Bamenda, 10 Aug 1975, Letouzey 14234 (BR, K, YA);
bank of Boumba river, 14 km west-south-west of Kinsassa, 7 Mar 1971, Letouzey & Villiers 10525 (BR, P,
YA); Mount Oku, Lumutu Forest, 1 May 1998,
Maisels 116 (YA); Lakom, Bamenda, May 1938, Maitland 1361 (K); Mount Cameroon, Jan 1862, Mann
1212 (K); Mapanja, 16 Mar 1992, Mbani 55 (K);
between Yaoundé and Deng Deng, c. 170 km northwest of Yaoundé, 1 Mar 1914, Mildbraed 8410 (HBG);
Elak, 6 Nov 1996, Munyenyembe et al. 892 (K, YA);
80 km de Bertoua, route Ndemba II, 17 Jan 1956,
Nana 431 (BR, P, YA); Ekona, Mount Cameroon, 14
Jan 1985, Nkongmeneck 892 (YA); Bafut–Ngemba
Forest Reserve, 19 Mar 1955, Richards 530 (K, P);
Small Massaka (Rumpi hills), 19 Dec 2009, Sonké
et al. 5442 (BR, BRLU, K, MO, P, WAG, YA); National
Park Mbam Djerem, 23 Jan 2011, Sonké et al. 5510
(BR, BRLU, K, MO, YA); Bertoua–Batouri, 15 May
1905, Tchinaye 111 (P, YA); south slope of Mount
Cameroon, above Batoke, 29 Dec 1983, D.W. Thomas
2844 (BR, K, P, YA); above small Koto village, 6 Mar
1985, D.W. Thomas 4463 (MO, P, WAG, YA); Bafut–
Ngemba Forest Reserve, 24 Jan 1951, Tiku 22247 (K);
Bali–Nguemba Forest Reserve, 5 Jun 1951, Ujor
30416 (K); east slope Mount Cameroun, 6 km east of
Bomana, 34 km north-west of Limbe, 11 Dec 1984,
Villiers 2447 (BR, YA); Mapanja, 19 Feb 1992, Wheatley 14 (K).
CENTRAL AFRICAN REPUBLIC. near Baboua,
3 km along the road to Besson, Descoings 12703
(MPU); Berbérati, 28 Feb 1937, Tisserant 3478 (BM,
P).
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422
B. VERSTRAETE ET AL.
EQUATORIAL GUINEA. Bioko: Gran Caldeira de
Luba, along the river towards Mount Pisarro, Carvalho 4268 (K); s.loc., Fernandez Casas 12167-19 (K).
GABON. Bélinga hills, main ridge, 22 Nov 2007,
Leal et al. 2169 (BR, MO).
NIGERIA. Boshi extension Forest Reserve, 23 May
1971, van Meer 1771 (WAG).
5. CUVIERA MACROURA K.SCHUM., Bot. Jahrb. Syst.
33: 352. 1903. Type: NIGERIA. Lagos, Millen 159
(holotype: K000412062!).
Distribution: Lower and Upper Guinea Domains:
Benin, Cameroon (only along coast), Ghana, Guinea,
Ivory Coast, Liberia, Nigeria, Sierra Leone; a doubtful
record from Equatorial Guinea (Bioko).
Notes: Cuviera macroura is unique in the genus in
having small glabrous pits in the nerve axils (sometimes hard to see), a calyx with subulate lobes distinctly fused at the base, and stipules with a broad
rounded lobe (see photographs in Hawthorne &
Jongkind, 2006). The species is rather variable, specimens from Cameroon and Nigeria generally have
smaller leaves and fruits than those from West Africa.
Vogel 83, the type of C. subuliflora, has two sheets,
one of which is C. macroura (K000412044!). Both
sheets are labelled ‘Fernando Po’ [= Bioko], but their
origin is somewhat doubtful, for Bentham (in Hooker,
1849) states in the protologue of C. subuliflora: ‘Fernando Po, on the seashore, and, apparently the same
species, at Abòh, growing in the water, Vogel’. The
latter locality is in Nigeria. There are no other records
of C. macroura on Bioko and its occurrence there is to
be regarded as doubtful.
Cuviera djalonensis A.Chev. (in Explor. Bot. Afrique
Occ. Franç.: 331. 1920.) is a nomen nudum referring
to C. macroura (Hallé, 1960).
Additional specimens examined: BENIN. Lokoli, 18
Dec 2002, Dan 674 (BR); Lokoli/Sisimè, 20 Dec 2002,
Dan 684 (BR); Godomé, 20 Aug 1902, Estéve 115
(BM).
CAMEROON. Right bank of Lokoundjé river, near
Edéa, 26 km north of Kribi, 18 Apr 1965, Leeuwenberg 5620 (BR, K, P, WAG); left bank of Sanaga river,
near of the mouth, 6 Jan 1974, Letouzey 12631 (YA);
bank of Abo river, between Miang and Koki, 25 km
north of Douala, 9 4 1976, Letouzey 14751 (BR, P, YA);
Douala–Edéa Reserve, bank of Kombe river, 3 Aug
1978, D.W. Thomas 521 (K).
EQUATORIAL GUINEA. Bioko: locality doubtful
(see Notes above), Vogel 83 (K000412044).
GHANA. Boin River Forest Reserve, 2 Jul 1956,
Agbley 6263 (K); Obuasi, Jun 1936, Andoh 4218 (BR,
K); near Anyinakim, 13 Jul 1954, Darko 898 (K);
± 5 miles inland from Dixcove, 31 Mar 1954, Morton
A468 (K); Kumasi, Jun 1929, Vigne 1758 (K); s.loc.,
s.d., Vigne 3008 (BM).
GUINEA. Gouam–Geasso, 23 Apr 1956, Adam
12092 (K); Sérédou, Aug 1954, Jacques-Félix 7108 (K).
IVORY COAST. Lower Cavally, Prolo, 11 Aug 1909,
Chevalier 19869 (K); Reserve of Boulay Island, Ebrié,
18 Nov 1956, J.J.F.E. de Wilde 818 (WAG); between
Mount Nienokoue and Hana river, Taï–Tabou road, 11
Aug 1962, Guillaumet 1519 (BR); Adiopodoumé, 16
Aug 1961, F. Hallé 219 (BR, K); near the debarcation
of the ferry from Grand Bassam to Bingerville, 24 Jul
1969, Versteegh & Den Outer 575 (BR).
LIBERIA. Zeahtown, 1 Aug 1947, Baldwin 6967
(K); 10 miles west of Tapita, along the road to Ganta,
16 Jul 1968, Jansen 864 (BR, K); Peahtah, 13 Oct
1926, Linder 1035 (K).
NIGERIA. s.loc., Hambler 409 (K); Ibarapa, 22 Aug
1966, Latilo 58826 (K, P); 19 miles from Imo river, 12
Aug 1966, Okafor 60323 (K); Ikorodu, 29 Dec 1952,
Onochie 32038 (K); Degema, 1916, Talbot 3632 (BM,
K).
SIERRA LEONE. Mussaea, 31 Aug 1963, Haswell
150 (K); Loma Mountains, 20 Sep 1945, Jaeger 1959
(K); Tingi, 18 Dec 1965, Morton & Gledhill SL3223
(K); Binkolo, 25 Aug 1914, N.W. Thomas 1857 (K);
Bumbuna, 14 Oct 1914, N.W. Thomas 3189 (K);
Komorolai, 23 Dec 1915, N.W. Thomas 6914 (K).
6. CUVIERA PHYSINODES K.SCHUM., Pringsh. Jahrb.
19: 391. 1888. Type: GABON. Sibange Farm,
Munda, 27 Aug 1879, Soyaux 29 (lectotype designated
here:
P03818077!;
isolectotype:
K000412041!); Sibange Farm, Munda, 25 Oct
1881, Soyaux 307 (syntype: K000412040!).
Synonyms: Cuviera ledermannii K.Krause, Bot.
Jahrb. Syst. 48: 418. 1912. syn. nov. Type: CAMEROON. Nkolebunde [= Elephant Mountain], Oct
1908, Ledermann 725, 751 (holotype: B†); Elephant
Mountain, c. 20 km south-east of Kribi, 9 Mar 2007,
Chatrou et al. 572 (neotype designated here:
BR000000980675!).
Distribution: Lower Guinea Domain: south Cameroon
(north to Lake Tissongo), Equatorial Guinea (Rio
Muni), Gabon (widespread except in the east).
Notes: This species has been overlooked since its
description, possibly because the Index Kewensis
gives a wrong reference for the protologue. Cuviera
physinodes is closely related to C. acutiflora and frequently mistaken for that species (e.g. Sosef et al.,
2006); see key for differences in flower and fruit.
Sterile specimens from the area of sympatry (Cam-
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REVISION OF CUVIERA AND GLOBULOSTYLIS
eroon, Equatorial Guinea) can be set apart from
C. acutiflora by their cuneate leaf base (always
cordate in local populations of C. acutiflora).
The description of C. physinodes is based on two
syntypes, Soyaux 29 (with flower buds) and Soyaux
307 (with young fruits). The P sheet of the former
bears the number 23, which is evidently a copying
error: Soyaux 23 (K) was collected on 21 Aug and
is an isosyntype of Pavetta brachycoryne K.Schum.
(= Rutidea glabra Hiern). In spite of this, we select
this sheet as lectotype, as it is by far the better.
Krause (1912) already considered C. ledermannii as
closely related to C. physinodes and his good description actually leaves no doubt that they are conspecific.
The syntypes have probably been destroyed in Berlin,
so we designated a neotype from the same locality.
Additional specimens examined: CAMEROON. Lobe
river, above the Grand Batanga ferry, 24 Oct 1968,
Bos 3081 (BR, K, P, WAG, YA); 13.5 km from Kribi,
north of Ebolowa road, Bidou II plantation, 2 Dec
1968, Bos 3426 (BR, K, P, WAG, YA); near Mbikiliki
village, 11 Mar 2007, Dessein & Sonké 1513 (BR, YA);
near Bidjouka, track towards waterfall, 15 Mar 2007,
Dessein & Sonké 1593 (BR, YA); near lake Tissongo,
9 May 1977, McKey 53 (P, YA); Mangombe Forest
Reserve (Edéa), 21 Jan 1956, Mpom 183 (BR, YA);
near Ebodje, 50 km south of Kribi, 29 Oct 1984,
Nkongmeneck 822 (YA); Nkoltsia hill, 24 Apr 1974,
Villiers 870 (YA); Bipindi, 1898, Zenker 1797 (BM);
ibid., 1900, Zenker 2246 (BM, K, P).
EQUATORIAL GUINEA. Rio Muni: Monte Alén, 19
Apr 2001, Ngomo 916 (BRLU); south-west part of
Monte Alén National Park, 2 km north-east of Rio
Uolo, 24 June 2002, Senterre & Nguema 3018
(BRLU); Monte Alén National Park, 12.5 km east of
Mosumo, 8 Sept 2003, Senterre & Obiang 4071
(BRLU).
GABON. Toucan, 11 Oct 2002, Bourobou et al. 990
(WAG); km 34 Mouila–Yeno, 22 Sep 1986, Breteler
et al. 8100 (BR, K, P, WAG); Sibange (Monda), 1884,
Büttner 152 (K); Monts de Cristal, inselberg Milobo,
10 km north of Mbé Akélayong, 30 Nov 2001, Degreef
181 (BR); Benga, Klaine 82 (BR, K, P); Owendo, 10
Nov 1903, Klaine 3340 (K, P); road to Cap Estérias on
the right, 11 Sep 1985, A.M. Louis 1805 (WAG); Forêt
des Abeilles, east Lopé Reserve, 3 Dec 1993, McPherson 16297 (K, MO, WAG); c. 25 km north of Libreville,
13 Jul 1985, J.M. Reitsma & B. Reitsma 1261 (WAG);
Mondah Forest, c. 15 km north of Libreville, 30 Jul
1986, J.M. Reitsma & B. Reitsma 2463 (WAG);
Doudou Mountains National Park, c. 30 km south of
Mandji, 18 Nov 2005, Sosef 2373 (WAG); Pechoud
road, southwards, 27 Oct 1990, Van Nek 123 (WAG);
Cap Esterias, 1896, Klaine 538 (P); Mondah Forest,
30 Aug 1969, Villiers s.n. (P).
423
7. CUVIERA PIERREI N.HALLÉ, Bull. Soc. Bot. France
106: 344. 1960. Type: GABON. La Nkoulounga
(north-east of Libreville), 7 Jul 1959, N. Hallé 730
(holotype: P00553435!; isotypes: K000412048!,
P00553434!).
Distribution: Lower Guinea Domain: Equatorial
Guinea (Rio Muni), Gabon.
Notes: This species is unusual in Cuviera in having
(two-)three- (five-) flowered inflorescences and the
style thickened in the upper two-thirds (Hallé, 1960:
fig. 2L). It is presumably related to C. subuliflora,
which has similar leaves.
Cuviera pierrei also shows a superficial resemblance to Globulostylis cuvieroides, because of the
shape of the calyx lobes, however, the striped corolla
lobes, the position of the bracts (inserted halfway on
the pedicels of the lateral flowers rather than at the
apex of the peduncle), and the presence of ant holes in
the twigs are clear distinctions.
The species is newly reported from Equatorial
Guinea. A record from the Democratic Republic of the
Congo (Compère, 1962) is an error for C. subuliflora
(see that species).
Additional specimens examined: EQUATORIAL
GUINEA. Rio Muni: Abama (Nsork), 22 Aug 2001,
Esono, Merino & Gomez 289 (BRLU); Ngoma, 15 km
south-east de Etembue, 12 Aug 1998, Lejoly & Elad
98/158 (BRLU).
GABON. 9 km south of Kinguélé, 21 Sept 1994,
Breteler et al. 12980 (WAG); Mount Mela, 26 Aug
1978, Breteler & J.J.F.E. de Wilde 320 (BR, K, P,
WAG); around Libreville, 3 Dec 1899, Chalot 15 (P);
Kinguélé road, N. Hallé & Villiers 4588 (P); Libreville, 25 Mar 1904, Klaine 48 (BR, K, P, WAG); ibid.,
12 Feb 1896, Klaine 378 (P); ibid., 15 Oct 1896, Klaine
558 (P); ibid., 25 Jul 1897, Klaine 558bis (P); ibid., 24
Oct 1900, Klaine 2005 (P); ibid., Jul 1895, Thollon 216
(BR, P); Cocobeach road, 15 Jul 1986, D.W. Thomas &
Wilks 6361 (K); N’Koulounga, 23 Jun 1959, Touzet 157
(P); Ngoualé, 15 km south of Ekorado, 2 May 2001,
Walters et al. 582 (BR); Nombo, 22 May 1986, Wilks
1299 (WAG).
8. CUVIERA SUBULIFLORA BENTH., in W. J. Hooker,
Niger Fl.: 407. 1849. Canthium subuliflorum
(Benth.) Roberty, Bull. Inst. Franç. Afrique Noire
16: 60. 1954. Type: EQUATORIAL GUINEA.
Bioko, Vogel 83 (lectotype designated here:
K000412045!); Excluded isolectotype: Bioko, Vogel
83 (K000412044!) is Cuviera macroura.
Synonyms: Cuviera plagiophylla K.Schum., Bot.
Jahrb. Syst. 33: 353. 1903. Type: CAMEROON.
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424
B. VERSTRAETE ET AL.
Bipindi, 1897, Zenker 1350 (lectotype designated
here:
K000412043!,
isolectotypes:
BM!,
BR000000884676!, HBG, L0058090 n.v., MA311021
n.v., NY00131204 n.v., P!, S05-10683 n.v., WAG!).
Distribution: Lower Guinea Domain: Cameroon,
Democratic Republic of the Congo, Equatorial Guinea
(Bioko and Rio Muni), Gabon, Nigeria, Republic of
Congo.
Notes: The type of C. subuliflora, Vogel 83, has two
sheets, one corresponding to the species hitherto
named C. subuliflora, the other being C. macroura. To
preserve current usage, we select the former sheet
(K000412045!) as lectotype. The origin of these collections is somewhat doubtful (see note under
C. macroura).
The fruits of C. subuliflora, with their broadly truncate apex and the calyx lobes patent and star-like, are
unique in the genus. The style can be glabrous or
pubescent, which explains discrepancies between the
keys in Hallé (1960) and Hepper & Keay (1963). This
species is newly reported from the Democratic Republic of the Congo (see C. pierrei above). A record
from Ghana (Hepper & Keay, 1963) is probably an
error for C. macroura (Hawthorne & Jongkind, 2006:
628), but we could not verify the specimen. Two
different Talbot specimens bear the same number
222: one collected in 1911 (C. subuliflora), the other
from 1909 (C. truncata).
Additional specimens examined: CAMEROON. South
of Bakundu, 14 Feb 1956, Binuyo & Daramola 35530
(K, P); Onge, 28 Oct 1993, Cheek et al. 5172 (K); Konye,
Kumba–Mamfe road, 12 Sep 1986, Etuge & Thomas
257 (BR, K, MO, P, WAG); Boa, 1 Jun 1994, Fraser 469
(K); Nkongkengui, 12 km north-north-east of Makak,
17 Jul 1972, Letouzey 11524 (K, P, WAG, YA); chutes du
Ntem, 40 km east-south-east of Campo, 10 Dec 1979,
Letouzey 15342 (P, YA); Bimbia, Feb 1929, Maitland
417 (K); Limbe, Oct 1929, Maitland 740 (K); Fenda,
58 km east of Kribi, 1911, Mildbraed 6009 (HBG);
Bibundi, Nov 1928, Mildbraed 10662 (K); Bonjare, 1
May 1994, Ndam 1111 (K); Nndian–Dibonda–
Ekumbako road, 24 Nov 1986, Nemba & D.W. Thomas
398 (BR, K, MO, YA); Kumba–Mamfe road, 23 Jul
1987, Nemba & D.W. Thomas 616 (K, MO); Kumba
area, 13 Oct 1984, Nemba & D.W. Thomas 4049 (BR);
s.loc., Preuss 557 (BM); Meka’a (Dja Fauna Reserve),
12 Feb 1995, Sonké 1430 (BR, BRLU); Djomedjoh (Dja
Fauna Reserve), 23 Jul 1995, Sonké 1646 (BR);
Bejange, 23 Jan 2008, Sonké 4591 (BR, K, MO, P, WAG,
YA); Kumba area, 13 Oct 1984, D.W. Thomas & Nemba
4049 (K, MO, P, YA); 10 km Ikata–Munyenge (northeast of Muyuka), 26 Aug 1983, D.W. Thomas 2542 (BR,
K, MO, P, YA); Liwenyi, 31 Oct 1993, Watts 880 (K);
Upper Boando, 21 Feb 1992, Wheatley 19 (K);
Nkuambe, 1913, Zenker 346 (BR, P, WAG); Bipindi,
1911, Zenker 3985 (BM, BR, HBG, K); ibid., 1913,
Zenker 4977 (BM, K); s.loc., Unknown (SCA) 2264 (YA).
DEMOCRATIC REPUBLIC OF THE CONGO.
Kimetete, 23 Sep 1959, P. Compère 463 (BR).
EQUATORIAL GUINEA. Bioko: s.loc., 1986, Carvalho 2283-22 (K); s.loc., 1986, Carvalho 2521-3 (K);
s.loc., 1986, Fernandez Casas 11544-3 (K); s.loc., Dec
1860, Mann 87 (K); Rio Muni: Sendje, 13 Aug 2001,
Esono & Ndong 304 (BRLU); Monte Alen, Ngomo &
Ndong 232 (BRLU); Nkolentangan, 15 Feb 1908, Tessmann 204 (K).
GABON. Km 4 Mbigou–Mimongo, 1983, J.J.F.E. de
Wilde et al. 545 (BR, K, WAG); Rembo, on Guidouma–
Mouila road, 19 Feb 2008, Dessein et al. 2004 (BR,
LBV); 23 km south-west of Koumameyong, 3 Aug
1987, Dibata 274 (WAG); Moubigou 2, 21 May 1963,
N. Hallé & Cours 6138 (P); around Libreville, 13 Jul
1895, Klaine 302 (P); Libreville, 1904, Klaine 999 (K,
P); Ofoubou, c. 30 km west of Mandji, 24 Jun 1991,
Reitsma 3728 (WAG); c. 17 km NW Doussala, Monts
Doudou Reserve, 25 Mar 2000, Sosef 1004 (WAG);
Saint Martin, Jul 1939, Walker 2 (P).
NIGERIA. Oban Group Forest Reserve, 11 Sep
1960, Adebusuyi 44000 (K); ibid., 22 Nov 1961,
Binuyo 45423 (K); Aponmu Forest Reserve, 7 Aug
1963, Gillett 15279 (BR, K, P, WAG); ibid., Hunder 90
(WAG); Oban, 2 Dec 1911, Talbot 222 (BM, K); ibid.,
1912, Talbot 2036 (BM); Degema, Talbot 3383 (BM,
K); 12.5 miles Akure-Ondo, 13 Nov 1968, van Meer
892 (BR, K, WAG).
REPUBLIC OF THE CONGO. region of Kouilou
(Bas–Kouilou), 26 Aug 1990, Moutsamboté & DowsettLemaire 4499 (BR); Les Saras region, Congo–Cabinda
road, 8 Jun 1966, Sita 1376 (P); s.loc., Moutsamboté
1401 (BR).
9. CUVIERA TRILOCULARIS HIERN, in D. Oliver, Fl.
Trop. Afr. 3: 157. 1877. Type: NIGERIA. Old
Calabar, 11 Apr 1863, Thomson 122 (lectotype
designated here: K000412061!; isolectotypes:
E00193711!, E00259212!).
Distribution: Lower Guinea Domain: restricted to
extreme south-east Nigeria (Oban) and adjacent
south-west Cameroon (Korup National Park).
Notes: Hiern (1877) based his specific name on the
supposedly trilocular ovary, which seems to have been
a wrong observation. We dissected two ovaries (one
each from D.W. Thomas 6797 and van Meer 1357) and
found them to be pentalocular, as is usual in the
genus.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
Cuviera trilocularis is the only species of Cuviera in
which ant holes seem to be consistently absent; it is
also unusual in its few-flowered inflorescences. The
flower colour pattern of C. trilocularis needs checking
in the field: the label of van Meer 1357 describes the
corolla as ‘greenish white inside’, not mentioning
stripes but on the dried specimen the central zone of
the lobes is distinctly paler.
Additional specimens examined: CAMEROON.
Ekundu Kundu, 26 April 1996, Cheek et al. 8186 (YA);
Korup National Park, 15 Mar 1986, D.W. Thomas &
Mcleod 5783 (K, YA); ibid., Mar 1979, D.W. Thomas
1181 (K); ibid., 26 Feb 1985, D.W. Thomas 4312 (K,
YA); Mundemba, 28 Mar 1987, D.W. Thomas 6797
(BR, K, MO, WAG, YA); around Erat village (southwest Korup National Park), 10 Jun 1988, D.W.
Thomas 8120 (K, MO, P).
NIGERIA. Oban, 10 May 1912, Talbot 221 (BM, K);
ibid., 1911, Talbot 272 (BM); Oban, 14 Apr 1971, van
Meer 1261 (WAG); Oban Group Forest Reserve (west
block, cut line from Pillar 51), 19 Apr 1971, van Meer
1357 (BR, WAG).
10. Cuviera truncata Hutch. & Dalziel, Fl. W. Trop.
Afr. 2: 118. 1931.
Type: NIGERIA. Oban, 1911, Talbot 286 (lectotype
designated
here:
K000412060!;
isolectotype:
BM000903509!); Degema, 1916, Talbot 3686 (syntypes: BM000903507!, BM000903508!).
Distribution: Lower Guinea Domain: south-west
Cameroon, Nigeria.
Notes: Cuviera runcata is unique in the genus in
having the calyx truncate or with short (< 2 mm) and
irregular lobes. It further differs from C. acutiflora,
its closest relative, in having larger and broader
bracts. However, some Nigerian collections (Dalziel 45
and Elliott 198, both from Lokoja; Kennedy 2758 from
Sapoba; Thornewill 47 from Wamba river) are intermediate between the two species, either by combining
characters of both (large bracts and long calyx lobes,
or the reverse) or by having variable calyx lobes. They
could represent hybrids; fieldwork in Nigeria would
be needed to solve this question. Another Talbot 222
specimen belongs to C. subuliflora (see Note under
that species).
Additional specimens examined: CAMEROON. Kupe–
Muanenguba, Kodmin, 20 Jan 1998, Etuge et al. 4051
(YA); Eyumojock Forest Reserve (c. 42 km east of
Mamfe), 9 Feb 1985, Onana 107 (BR, YA); Mamfe
town, 22 Apr 1987, D.W. Thomas 7304 (BR, K, MO,
WAG).
425
NIGERIA. s.loc., Akete 64 (K); Ganglani, 23 Nov
1957, Hepper 1448 (BR, K, P); Sanga river, Dogon
Kurmi, 30 Nov 1957, Keay 37246 (K, P); Dogon
Kurmi, 17 Nov 1946, Keay & Onochie 21535 (K);
Gangumi (between Dondere and Yandere), 8 Dec
1954, Latilo & Daramola 28861 (K, P); Nimbia Forest
Reserve, 9 Apr 1963, Latilo 47417 (K, P, WAG); Boki
(c. 18 miles from Bende/Ayuk), 28 Feb 1973, Latilo
67754 (K, WAG); Dogon Kurmi, 10 Dec 1964, Olorunfemi 55130 (P); Oban, 1909, Talbot 222 (BM).
GLOBULOSTYLIS Wernham, Cat. Pl. Oban: 49. 1913.
Cuviera subg. Globulostylis (Wernham) Verdc., Kew
Bull. 42: 189. 1987.
Type species: Globulostylis talbotii Wernham (lectotype designated by Verdcourt, 1987: 189).
Description: Small trees or shrubs, 1.5–16.0 m high,
evergreen, with regular horizontal branches (Roux’s
architectural model); vegetative parts glabrous or
rarely shortly pubescent (in some specimens of
G. rammelooana and G. robbrechtiana); twigs without
ant holes; spines absent. Leaves opposite, ± elliptic;
stipules small, basally ± connate, with an awn
> 2 mm long (frequently damaged). Inflorescences
axillary and generally paired at nodes (or occasionally
terminal), on young twigs, cymose, umbelliform, oneto five-flowered, with a single pair of elliptic leafy
bracts at apex of peduncle (in G. cuvieroides and
G. minor rarely with some additional bracts on the
pedicels). Flowers hermaphrodite. Calyx lobes five,
almost free, leafy, broadly elliptic or more rarely lanceolate (G. cuvieroides). Corolla green or yellow; tube
broadly funnel-shaped; lobes five, triangular, acute to
shortly apiculate, spreading or reflexed; outside glabrous or with five rows of hairs on the lobes and
upper part of tube; inside with a ring of hairs in the
lower half of the tube. Stamens five, inserted in the
upper part of the tube, anthers partly to fully
exserted. Ovary pentalocular, obconic or turbinate,
smooth; ovules solitary in each locule, pendulous.
Disk ± flat, glabrous. Style shortly exserted, with a
pubescent swelling in the lower part (fusiform in
G. dewildeana and G. robbrechtiana, discoid to
globose in other species), otherwise glabrous; stigmatic club ± mitriform, shortly five-lobed. Fruit
drupaceous, maturing yellow to orange (but generally
seen green), large, 1.5–3.5 × 1.2–3.5 cm, subglobose to
ellipsoid, smooth to conspicuously five-lobed, with
calyx persistent (rarely caducous); pyrenes five, oneseeded, shaped like a mandarin orange segment, with
a slight ventral indentation towards the upper third.
Distribution and ecology: Globulostylis has eight
species in Central Africa, all endemic to the Lower
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
426
B. VERSTRAETE ET AL.
KEY
1.
1’.
2.
2’.
3.
3’.
4.
4’.
5.
5’.
6.
6’.
7.
7’.
TO THE
GLOBULOSTYLIS
SPECIES
Calyx lobes narrowly lanceolate, > 5 times longer than wide, 7–17 × 1.0–3.5 mm; tree 6–12(−16) m high
(south-east Cameroon and Gabon) ..............................................................................G. cuvieroides
Calyx lobes broadly elliptic, < 3 times longer than wide; smaller trees or shrubs, 1.5–6 m high ........2
Calyx ciliate on margin; corolla lobes pubescent outside on the midrib ...........................................3
Calyx entirely glabrous; corolla lobes glabrous outside ...................................................................4
Flowers small; calyx 5–7 mm long; corolla tube 4–5 mm, and shorter than the lobes (Nigeria and
south-west Cameroon) .....................................................................................................G. talbotii
Flowers large; calyx lobes 10–16 mm long; corolla tube 14.5–19.0 mm long, longer than wide, and longer
than the lobes (south Cameroon, around Ebolowa) ......................................................G. dewildeana
Corolla yellow, with tube 20–30 mm long, at least twice longer than calyx; style with a weak, fusiform
basal swelling; fruits strongly five-lobed and rather small, 15–22 × 12–19 mm when dry (Cameroon,
Equatorial Guinea, Gabon) ................................................................................... .G. robbrechtiana
Corolla green (possibly yellow in C. leniochlamys), with tube 2–15 mm long, not or shortly exceeding
calyx; style with a strong, globose to discoid swelling; fruits smooth to weakly five-lobed and generally
larger, 19–32 × 17–27 mm when dry ............................................................................................. 5
Calyx large, with lobes 11–22 mm long .........................................................................................6
Calyx smaller, with lobes 4–10 mm long ..................................................................................... ..7
Corolla tube c. 15 mm long, ± equalling calyx; inflorescence three- to five-flowered (but only one fruit
may develop) (south Cameroon) ...............................................................................G. leniochlamys
Corolla tube much shorter than calyx; inflorescence always one-flowered (Gabon to Democratic Republic
of the Congo) ............................................................................................................. ..G. uncinula
Corolla small, tube 2–5 mm long, lobes 3–5 mm long; calyx lobes patent (Fig. 5G), 4–7 × 2.5–5.0 mm;
leaves drying greyish–green below (Nigeria and south-west Cameroon) ................................G. minor
Corolla larger, tube 6–8 mm long, lobes 6–10 mm long; calyx lobes erect (Fig. 5E), 6–10 × 5.5–7.0 mm;
leaves drying olive–green to olive–brown below (Cameroon) ................................... ..G. rammelooana
Guinea Domain, except G. uncinula, which also
occurs in the Congolian Domain. The centre of diversity is in Cameroon (seven species, including three
endemics). All Globulostylis spp. are shrubs or small
trees of forest understory, never gregarious.
Notes: Globulostylis spp. are often difficult to separate
in the absence of flowers. The leaves in particular
show little variation between the species.
The inflorescences are most often axillary, but
terminal inflorescences, previously unrecorded in
Vanguerieae, are occasionally found in G. robbrechtiana (e.g. Nguema & Parmentier 446, Ngomo &
Ndong 439) and G. rammelooana (e.g. Sonké & Simo
4671).
As for Cuviera, the pollinators or dispersors of
Globulostylis are unknown. There are well-marked
differences in flower characters between species with
a long corolla tube, a generally weak style swelling,
and an internal ring of hairs close to the base
(G. dewildeana, G. leniochlamys and G. robbrechtiana) and those with a short corolla tube, a thick
style swelling and an internal ring of hairs near the
middle of the tube (the remaining five species), so it is
likely these two groups have different pollinators. The
function of the style swelling is unclear, although a
role in preventing nectar robbery has been suggested
(Verdcourt, 1987). No human uses of Globulostylis
have been recorded.
1. GLOBULOSTYLIS CUVIEROIDES WERNHAM, J. Bot.
56: 313. 1918. Cuviera cuvieroides (Wernham)
Onana, Kew Bull. 63: 402. 2008 publ. 2009. Type:
CAMEROON. Bitye, 1911, Bates 1016 (holotype:
BM000903506!).
Synonyms: Cuviera heisteriifolia Mildbr., Notizbl.
Bot. Gart. Berlin-Dahlem 9: 205. 1924. syn. nov.
Type: CAMEROON. Ebolowa, 17 Jun 1911, Mildbraed
5610 (lectotype designated here: HBG!).
Distribution: Lower Guinea Domain: south-east Cameroon, east Gabon.
Notes: Globulostylis cuvieroides stands well apart
from its congeners in having narrowly lanceolate
calyx lobes, a character more reminiscent of Cuviera.
For that reason it shows a superficial resemblance to
Cuviera pierrei (see that species).
An examination of the type of C. heisteriifolia
shows this to be conspecific with G. cuvieroides. The
original specimen has presumably been destroyed in
Berlin, so the HBG duplicate is selected as lectotype.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
427
Figure 5. Flowers of several Cuviera and Globulostylis spp. A, Cuviera angolensis subsp. latior. B, Cuviera subuliflora.
C–D, Cuviera longiflora. E, Globulostylis rammelooana. F, Globulostylis robbrechtiana. G, Globulostylis minor. H,
Globulostylis cuvieroides. Photographs by Quentin Luke (A), Steven Dessein (B), Murielle Simo (C–F) and Olivier Maurin
(G–H).
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
428
B. VERSTRAETE ET AL.
Additional specimens examined: CAMEROON. Lomié
region, 1911, Mildbraed 5404 (HBG); c. 15 km southeast of Somalomo (Dja Fauna Reserve), 9 Nov 2002,
Davis 3049 (BR, K); Bouamir, Dja Fauna Reserve,
Mar 1996, Fogiel 586 (K); Meyos Mela (32 km eastnorth-east Djoum), 9 Nov 1966, Letouzey 8325 (BR, P,
YA); Bouamir, 5 Sep 2001, Nguembou 146 (BR); Akom
sili-Bali (Dja Fauna Reserve), 28 Dec 2002, Nguembou 544 (BR, BRLU); track from Bouamir station
Mbassakok (Dja Fauna Reserve), 20 Apr 2001, Senterre & Kouob 1007 (BRLU); ibid., Senterre & Kouob
1020 (BRLU); ibid., 17 May 2001, Senterre & Kouob
1233 (BRLU); ibid., 20 May 2001, Senterre & Kouob
1408 (BRLU); Djolimpoum (Dja Fauna Reserve), 10
Dec 1994, Sonké 1296 (BR); Mékas (Dja Fauna
Reserve), 12 Jan 1995, Sonké 1405 (BR, WAG);
Meka’a (Dja Fauna Reserve), 15 Feb 1995, Sonké
1438 (BR); Djolimpoum (Dja Fauna Reserve), 13 Apr
1995, Sonké 1464 (BR); 27 km south of Djolimpoum,
26 Nov 1996, Sonké 1841 (BR, K); Haut-Nyong, Somalomo, 12 km east of Somalomo, 8 Nov 2002, Sonké
et al. 2882 (BR, K, YA).
GABON. c. 60 km south-south-west of Moanda, 16
Oct 1970, Breteler 6947 (BR, K, P, WAG); Oveng,
chantier Rougier–Ocean, 7 May 1985, Breteler & A.M.
Louis 859 (WAG); road Mouila–Yéno, 20 Feb 2008,
Dessein et al. 2017 (BR, LBV); Bélinga, Mayibout I, 9
Jun 1978, Florence 1220 (P); Levata, 29 Apr 1930, Le
Testu 8059 (BM, P); Oveng, km 19 forest exploitation
camp, 9 Nov 1983, A.M. Louis et al. 525 (BR, K, P,
WAG); eastern border of Lopé–Okanda Reserve, 15
Jan 1993, McPherson 16062 (BR, K, MO, WAG);
Oveng, c. 15 km north-west of forestry camp, 8 Feb
1987, J.M. Reitsma & B. Reitsma 2923 (WAG); Oveng,
c. 25 km west-south-west of Mintsic, 9 Nov 1986, J.M.
Reitsma, B. Reitsma. & Mezui 2571 (WAG); c. 40 km
north-east of Mitzic (forestry concession Bordamur),
10 Feb 2003, Sosef et al. 1961 (WAG); Langoue Bai
(Ivindo National Park), 27 Nov 2002, Stone &
Niangadouma 3529 (BR); Nombo village, 22 May
1986, Wilks 1301 (WAG).
2. GLOBULOSTYLIS
DEWILDEANA
SONKÉ,
O.LACHENAUD & DESSEIN sp. nov. Type: CAMEROON. between N’Kolandom and N’Koemvone,
680 m alt, 2°48′N, 11°09′E, 9 Jan 1975, J.J.F.E de
Wilde 7886 (holotype: WAG0114671!; isotypes: BR!,
K!, P!, WAG0114672!, WAG0114673!).
Diagnosis: Globulostylis dewildeana resembles G. talbotii in its ciliate calyx and dorsally pubescent corolla
lobes, but differs in the larger calyx lobes (10–16 mm
long vs. 5–7 mm long), the much longer corolla tube
(14.5–19.0 mm long vs. 4–5 mm long), and the style
with a weak and fusiform basal swelling (vs. thick
and subglobose in G. talbotii). Globulostylis dewil-
deana also resembles G. leniochlamys and G. robbrechtiana in corolla shape (tube longer than broad and
much exceeding lobes), but in these species the calyx
and outside of corolla are glabrous.
Description: Shrub, 2.5–4.5 m tall; twigs glabrous,
older ones with pale grey bark. Leaves with petiole
7–13 mm long, glabrous; lamina elliptic to oblong–
elliptic, (9.0–)17.0–23.5 × (4.3–)7.5–12.5 cm; apex
acuminate with acumen 6–13 mm long; base shortly
attenuate, acute or obtuse; leaf surface glabrous on
both sides; secondary veins brochidodromous, six to
eight on each side of the midrib, ascending, straight
to slightly curved at the base, strongly curved some
distance from the margin to join with the adjacent
vein; domatia absent. Stipules with a short triangular
base prolonged into an awn 4–9 mm. Inflorescences
axillary paired at node, two- to four-flowered; peduncle short, < 6 mm; bracts triangular, c. 5 mm long,
glabrous. Flowers 5-merous, subsessile; flower buds
16–24 mm long, apiculate. Calyx pale green; calyx
tube c. 1 mm; calyx lobes broadly elliptic to ovate,
10–16 × 6–9 mm, ciliate. Corolla pale yellow to pale
brownish–green; tube slightly funnel-shaped, 14.5–
19.0 × 6.0–9.5 mm;
lobes
narrowly
triangular,
7–13 mm long, keeled outside, shortly apiculate
(c. 2.5 mm); outside with five rows of hairs on the
median keel of the lobes, prolonged on the tube for the
upper third; inside with a ring of hairs near the base
of the tube. Stamens five, attached near the mouth of
the tube; filaments short, c. 0.5 mm; anthers
c. 2.5 mm, half-exserted. Ovary pentalocular, glabrous. Disc cylindrical, c. 0.3 mm high, glabrous.
Style, c. 23 mm long, with a pubescent fusiform swelling at the base, otherwise glabrous; stigmatic club
lobed, exserted, c. 2 mm long. Fruits yellow, oval–
obovate to subglobose, up to 35 × 30 mm when fresh
(25 × 20 mm when dry), glabrous, crowned by persistent calyx lobes; pyrenes unknown.
Distribution: Lower Guinea Domain: endemic to a
narrow range south-east of Ebolowa, Cameroon.
Habitat and ecology: Evergreen forest; 650–750 m in
altitude.
Phenology: Flowers in December and January; young
fruits in December, January and March; mature
fruits in April.
Etymology: The specific epithet honours Dr J. J. F. E.
de Wilde of Herbarium Vadense (Wageningen, the
Netherlands), a specialist on Begonia and Meliaceae,
who collected most of the specimens including the
type.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
429
Conservation status: IUCN Red List Category Critically Endangered [CR B1ab (i, ii, iii)]. The species is
found far away from protected areas. The region is
interspersed with several roads along which human
activities are intense, including housing, smallholder
farming and forest logging. The species is found in
only one location. The extent of occurrence is estimated to be < 100 km2. Based on the threats identified, a continuing decline can be inferred in EOO,
AOO and area, extent and quality of habitat.
Dessein & Sonké 1464 (BR); Mvilé (3 km west-northwest of Ngovayang), 29 Nov 2005, Sonké 4170 (BR,
BRLU, K, MO, WAG, YA); Bibondi, 21 Jan 2005,
Sonké & Nguembou 3722 (BR, K, YA); ibid., 29 Jan
2005, Sonké & Nguembou 3865 (BR, K, MO, YA);
3 km north-west of Mbikiliki, 21 Jan 2006, Sonké &
Djuikouo 4334 (K, MO, YA); Mbikiliki, 20 Jan 2008,
Taedoumg 210 (BR); Lokundje, Oct 1919, Zenker 89
(BM); Ibid., 1911, Zenker 4003 (BM, BR, HBG); ibid.,
19 Feb 1912, Zenker 4003b (K); Ibid., 1912, Zenker
4425 (BM, BR, HBG, K).
Notes: Globulostylis dewildeana has so far been confused with G. talbotii in herbaria, but has much a
larger corolla and calyx and a different range; it is not
sympatric with any of its congeners, except the distinct G. cuvieroides.
4. GLOBULOSTYLIS MINOR WERNHAM, Cat. Pl. Oban:
50. 1913. Cuviera minor (Wernham) Verdc., Kew
Bull. 42: 189. 1987, nom. illeg. (non C. minor
C.H.Wright). Cuviera wernhamii Cheek, Pl. Mount
Cameroon: 106. 1998. Type: NIGERIA. Oban,
Talbot 247 (holotype: BM000903505!).
Additional specimens examined: CAMEROON. hill
facing the village of N’Kolandom, 9 Apr 1975,
J.J.F.E. de Wilde 8159 (BR, K, P, WAG, YA); hill above
the village of N’Kolandom, 12 Dec 1974, J.J.F.E. de
Wilde 7831A (BR, K, WAG); hill Nkolomeyan on the
track Bihongboulou–Koungoulou, 25 km east-southeast of Ebolowa, Letouzey 9843 (BR, P, YA).
3. GLOBULOSTYLIS
LENIOCHLAMYS
(K.SCHUM.)
SONKÉ, O.LACHENAUD & DESSEIN comb. nov.
Cuviera leniochlamys K.Schum., Bot. Jahrb.
Syst. 28: 79. 1899. syn. nov. Type: CAMEROON.
Bipindi, 19 Oct 1897, Zenker 1571 (lectotype designated here: K000412051!; isolectotype: BM!).
Distribution: Lower Guinea Domain: endemic to the
Ngowayang massif in southern Cameroon.
Notes: This species has been much mistaken in herbaria, mostly with G. rammelooana and G. robbrechtiana that both occur in its range. It especially
resembles the latter in corolla shape, but differs in
having a larger calyx not or hardly exceeded by the
corolla tube, a subglobose (not fusiform) basal style
swelling, and the fruits larger, 24–28 × 17–26 mm
when dry, smooth or nearly so. From G. rammelooana, it differs in the larger corolla and calyx (see
Key).
The flower colour of C. leniochlamys needs checking
in the field; Schumann (1899) describes the corolla as
ochre yellow (‘ockergelb’), which could refer to a
fading flower. The original material has presumably
been destroyed in Berlin, so the K duplicate is
selected as lectotype.
Additional specimens examined: CAMEROON. from
Mbikiliki to basecamp, c. 1.5 km north-west of village,
9 Mar 2007, Dessein & Sonké 1448 (BR); near Mbikiliki village, from basecamp to top of hill, 10 Mar 2007,
Distribution: Lower Guinea Domain: restricted to
extreme south-east Nigeria (Oban) and neighbouring
Cameroon (Korup National Park, Mount Etinde).
Notes: When treated in Globulostylis, this species is
correctly named G. minor. However, if placed in
Cuviera, the replacement name C. wernhamii should
be used (Cable & Cheek, 1998), because C. minor
(Wernham) Verdc. is an illegitimate later homonym of
C. minor C.H.Wright (which is now a synonym of
C. nigrescens).
Globulostylis minor is closely related to G. rammelooana, which is locally sympatric (see that species
for differences). Records from Gabon (Sosef et al.,
2006) are an error for G. cuvieroides; the two species,
although quite dissimilar, have been much confused
in herbaria.
Additional specimens examined: CAMEROON.
c. 10 km west of Limbe, above the village of Batoke,
24 Oct 2002, Davis 3007 (BR); Mount Etinde, 29 Apr
2009, Dessein et al. 2876 (BR, YA); west Limbe, 15
Nov 1985, Gentry & D.W. Thomas 52842A (K, MO,
WAG); Upper Boando, 6 Dec 1993, Lighava 31 (K);
chimpanzee camp, 19 km from Mundemba village,
Korup National Park, CTFS forest dynamic plot, 28
Oct 2008, Parmentier & Mambo 5115 (BRLU); Mundemba (Korup National Park), 29 Dec 1992, Sonké
381 (BR); Liwenyi, 29 Oct 1993, Tchouto 1007 (K);
Idenau, 8 Nov 1993, Watts 969 (K); Limbe, 0.5 km
north-east of Etome, 23 Jan 1994, Wieringa 1990
(WAG).
5. GLOBULOSTYLIS
RAMMELOOANA
SONKÉ,
O.LACHENAUD & DESSEIN sp. nov. Type: CAMEROON. Nkolembonda, 476 m alt, 2°47′58,6”N,
10°01′15,9”E, 13 Mar 2008, Sonké & Simo 4671
(holotype: BR!; isotypes: K!, MO!, P!, WAG!, YA!).
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
430
B. VERSTRAETE ET AL.
Diagnosis: Globulostylis rammelooana is closely
related to G. minor, from which it differs in having a
larger calyx with erect lobes 6–10 × 5.5–7.0 mm (vs.
patent lobes 4–7 × 2.5–5.0 mm; see Fig. 5E and G for
comparison), and also a larger corolla, with tube
6–8 mm long and lobes 6–10 mm long (vs. tube
2–5 mm long and lobes 3–5 mm long in G. minor). In
addition, the leaf underside lacks the typical greyish
sheen of G. minor, but instead dries olive–green to
olive–brown. Globulostylis rammelooana is also
related to G. leniochlamys and G. robbrechtiana,
which have much larger flowers. Fruiting specimens
differ from G. leniochlamys in their smaller calyx, and
from G. robbrechtiana in the larger and less markedly
lobed fruits. The calyx lobes are more rounded and
overlapping than in G. robbrechtiana (compare
Figs 3G and 4H) and the corolla is green, not yellow.
Description: Shrub, 2–4 m tall; twigs glabrous. Leaves
with petiole 5–10 mm long, glabrous; lamina elliptic
to oblong–elliptic, (6.5–)8.7–20.2 × (2.5–)3.4–7.4 cm;
apex acuminate with acumen 7–17 mm long; base
shortly attenuate or acute; leaf surface glabrous on
both sides; secondary veins brochidodromous, five to
seven on each side of the midrib, ascending, straight
to slightly curved at the base, strongly curved some
distance from the margin to join with the adjacent
vein; domatia absent. Stipules deciduous, shortly triangular at base, prolonged into an awn of 4–7 mm.
Inflorescences axillary or, more rarely, terminal, twoor three-flowered (but usually with only one fruit
developing), peduncle 0–5 mm long; bracts ovate,
5–8 × 2.5–3.5 mm, glabrous. Flowers pentamerous;
pedicels 0–2 mm long; flower buds green, 10–13 mm
long, acute. Calyx pale green; calyx tube 1.5–2.0 mm;
calyx lobes broadly elliptic, erect, 6–10 × 5.5–7.0 mm,
glabrous. Corolla green; tube campanulate, 6–8 × 5–
8 mm, outside glabrous, inside with a ring of hairs
near the basal third of the tube; lobes triangular,
6–10 mm long. Stamens five, inserted in the throat;
filaments 1.5 mm; anthers c. 2 mm, just exserted,
reflexed between the lobes. Ovary pentalocular, glabrous. Disc cylindrical, c. 0.7 mm high, glabrous.
Style 8–10 mm long, with a conspicuous hairy globular swelling c. one fifth from the base, otherwise
glabrous; stigmatic club five-lobed, exserted, lobes
c. 3 mm long. Fruits subglobose to slightly ellipsoid,
weakly five-lobed when dry, 19–25 mm in diameter
when dry, glabrous, crowned by persistent calyx lobes,
on pedicel 2–4 mm long; pyrenes five per fruit,
2.4 × 0.7 mm.
Distribution: Lower Guinea Domain: endemic to Cameroon, occurring mostly in the South Region (Bipindi
to Nyabessan) with a smaller population in the
South-West Region (Mount Etinde).
Habitat and ecology: Evergreen forest; 40–476 m in
altitude.
Phenology: Flowers in November–January and
March–April; fruits in February–April and June.
Etymology: Named in honour of Professor Jan Rammeloo, retired director of the National Botanical
Garden of Belgium, to whom all authors are indebted
for the assistance and facilities offered by his
institute.
Conservation status: IUCN Red List Category Vulnerable [VU B2ab(i, ii, iii, iv, v)]. G. rammelooana is
restricted to Cameroon where it is mostly found
outside protected areas. Logging, deforestation and
urbanization are the major threats for this species.
This species is known from nine locations. The area of
occupancy is less than 500 km2 (72 km2). Based on the
threats identified, a continuing decline of EOO, AOO,
area, extent and quality of habitat, number of locations and number of mature individuals can be
inferred.
Notes: Globulostylis rammelooana has usually been
confused with G. leniochlamys in herbaria. Its range
overlaps those of G. leniochlamys and G. robbrechtiana in the South Region of Cameroon, and of
G. minor in the South-West Region. All these species
mostly differ in flowering characters, but the identification of fruiting specimens is difficult, although
possible with experience with the group (see Diagnosis and Key).
The collections from Mount Etinde lack flowers, but
as they fully match G. rammelooana in other characters, they are referred to this species.
Additional specimens examined: CAMEROON. East
of Mount Elephant, 5 km south of km 18 Kribi–
Ebolowa, 6 Mar 1970, Bos 6496 (WAG); near Bidjouka, track to basecamp, 13 Mar 2007, Dessein &
Sonké 1546 (BR); Mount Elephant, south-east of
Kribi, 28 Apr 1970, Bos 6871 (K, WAG); near Bidjouka, track towards waterfall, 15 Mar 2007, Dessein
& Sonké 1602 (BR); Boa, 2 May 1994, Ekema 852 (K);
Boa, 4 May 1994, Ekema 922 (K); Etinde, Fraser 347
(K); Mvini (Mivini), 35 km east of Campo, 1 Dec 1983,
Kaji 205 (YA); Etinde, Ndam 1132 (K); ibid., 2 May
1994, Ndam 1185 (K); ibid., Ndam 1244 (K); cañon of
Ntem, 29 km south-west of Nyabessan, 1 Dec 1982,
Nkongmeneck 422 (BR, YA); Bipindi, 25 Nov 2004,
Sonké & Nguembou 3585 (BR, BRLU, K, MO, WAG,
YA); Mingli II (6 km north of Bipindi), 15 Jan 2005,
Sonké & Nguembou 3656 (BR, BRLU, K, MO, WAG,
YA); west Ngoyang, 18 Sep 2005, Sonké 3988 (BR, K,
MO, YA); 3 km west-north-west of Bidjouka, 16 Jun
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REVISION OF CUVIERA AND GLOBULOSTYLIS
2006, Sonké & Taedoumg 4464 (BR, YA); Lambi,
massif of Ngovayang, 20 Feb 2008, Sonké 4650 (BR);
Nkolembonda, Mount Elephant, 13 Mar 2008, Sonké
& Simo 4680 (BR, K, MO, P, WAG, YA); Ibid., 16 Mar
2008, Sonké & Simo 4711 (BR, K, MO, P, WAG, YA);
Nkolembonda, 16 Jul 2007, Taedoumg 102 (BR);
South Province, Campo Ma’an area, Massif des
Mamelles, 20 Apr 2001, Tchouto MMX110 (WAG);
Mokoko Forest Reserve, Ekombe–Mofako, 23 May
1994, Watts 1164 (K, SCA); Bipindi, 1909, Zenker
3927 (BR, K).
6. GLOBULOSTYLIS
ROBBRECHTIANA
SONKÉ,
O.LACHENAUD, DESSEIN & DE BLOCK sp. nov.
Type: CAMEROON. Efoulan, Akom II, 894 m alt,
2°44′56.6”N, 10°32′03”E, 24 May 2008, Sonké, Taedoumg & Simo 4868 (holotype: BR!; isotypes: BR!,
K!, MO!, P!, WAG!, YA!)
Diagnosis: Globulostylis robbrechtiana differs from its
congeners in the long, 20- to 30-mm corolla tube,
which is at least twice as long as the calyx (vs. corolla
tube 2–19 mm long, not or shortly exceeding calyx)
and in the rather small and strongly five-lobed fruits,
15–22 × 12–19 mm when dry (vs. 19–35 × 17–35 mm
when dry). It further differs from all species (except
possibly G. leniochlamys) in having bright yellow
flowers.
Description: Shrub 2–4(−6) m tall; twigs brown, glabrous or sometimes sparsely hairy when young.
Leaves with petiole 5–10 mm long, glabrous; lamina
elliptic to oblong–elliptic, 7.3–18.8(−20.2) × 3.0–
7.8 cm; apex acuminate with acumen 7–10(−17) mm
long; base shortly acute to rounded; leaf surface glabrous, or sometimes pubescent on the midrib below;
secondary veins brochidodromous, prominent, (four–)
six to nine on each side of the midrib, ascending,
straight to slightly curved at the base, strongly
curved some distance from the margin to join with the
adjacent vein; domatia absent. Stipules shortly triangular at base, prolonged into an awn of 3–4 mm long,
glabrous outside, hairy inside. Inflorescences axillary
or occasionally terminal, two–four (–six)-flowered (but
usually with only one fruit developing); peduncle
4–7 mm long; bracts ovate–triangular, 5–10 × 2–
4 mm, glabrous. Flowers pentamerous; pedicels
2–4 mm long; flower buds 22–32 mm long, acute.
Calyx pale green; calyx tube 1–2(−4) mm; calyx lobes
ovate to elliptic, erect, 6–12 × 3.5–9.0 mm, glabrous.
Corolla yellow; tube funnel-shaped, 20–30 × 13–
20 mm at throat; lobes triangular, 5–10 mm long;
outside glabrous; inside with a ring of hairs near the
base of the tube. Stamens five, inserted near the apex
of the tube; filaments 1 mm; anthers c. 2.5 mm, halfexserted to included. Ovary pentalocular, glabrous.
431
Disc cylindrical, c. 0.5 mm high, glabrous. Style,
20–32 mm long, with a pubescent fusiform swelling
c. 1.5 mm above the base; stigmatic club five-lobed,
just exserted, c. 2.5 mm long. Fruits subglobose, conspicuously five-lobed, 15–22 × 12–19 mm when dry,
glabrous, crowned by persistent calyx lobes, on
pedicel 4–8 mm long; pyrenes five per fruit,
c. 17 × 5 mm.
Distribution: Lower Guinea Domain: restricted to
hilly ranges of southern Cameroon (Ngowayang
massif, Akom II area), Equatorial Guinea (Monte
Alén) and northern Gabon (Crystal Mountains).
Locally abundant in its range.
Habitat and ecology: Evergreen forest; 460–1110 m in
altitude.
Phenology: Flowers mostly from May to October, with
one record in March; fruits from July to December.
Etymology: Named in honour of Professor Elmar Robbrecht, retired head of the Vascular Plants Department at the National Botanic Garden of Belgium, who
made a major contribution to the knowledge of
African Rubiaceae and to whom all authors are
indebted for instruction in aspects of this family.
Conservation status: IUCN Red List Category Near
Threatened (NT). Despite the restricted EOO (11106,
36 km2), which qualifies for Vulnerable, and AOO
(72 km2), which meets the threshold for Endangered,
and a low number of locations (six), G. robbrechtiana
is here considered to be only Near Threatened. Most
collections have been made inside protected areas;
three collection sites are outside protected areas, but
the surrounding forest seems to be rather untouched
by human activities at present. This might change in
the future, the reason why we think the category NT
is the most appropriate.
Notes: The large yellow flowers of G. robbrechtiana
are distinctive, but specimens in bud or fruit can be
mistaken for G. leniochlamys or G. rammelooana (see
these species for differences). The ranges of the three
species overlap in Cameroon.
Globulostylis robbrechtiana is normally glabrous,
but some duplicates of Sonké, Taedoumg & Simo 4872
have short patent hairs on young twigs and the
underside of midrib, which is exceptional in the
genus.
Additional specimens examined: CAMEROON. Akom
II, 24 Apr. 2007, Droissart & Simo 438 (BRLU);
Ebianemeyong, 24 May 2002, Elad et al. 1558 (WAG);
ibid., 24 May 2002, Elad et al. 1574 (WAG); Engon,
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
432
B. VERSTRAETE ET AL.
south Efoulan, 6 Mar 2004, Sonké & Beina 3331 (BR,
BRLU, K, MO, WAG, YA); Akom II, Efoulan, 24 Mar
2008, Sonké et al. 4872 (BR, K, MO, P, WAG, YA);
Campo Ma’an area, Efoulan, 4 Dec 2000, Tchouto
3092 (WAG); Bipindi, Oct 1918, Zenker 13 (P).
EQUATORIAL GUINEA. Rio Muni: Monte Alen, 20
May 1992, Carvalho 5115 (WAG); Bata-Monte Alen,
Subida al Monte Alen, 27 May 1993, Carvalho 5310
(WAG); Transect of Monte Chocolate, 16 Nov 2002,
Desmet et al. 9 (BR); Engong, 9 May 2002, Esono &
Parmentier 589 (BRLU); Monte Chocolate, 11 Aug
2001, Esono & Senterre 272 (BRLU); Monte Mitra
(Monte Alen National Park), 30 Sep 2005, Leal et al.
806 (BR, MO); Ibid., 30 Sep 2005, M.E. Leal et al. 807
(BR, MO); between 0 and 1 km west of Alen (Monte
Alen National Park), 15 Oct 1993, Lejoly 93/315
(BRLU); ibid., 15 Oct 1993, Lejoly 93/339 (BRLU);
ibid., 21 Oct 1993, Lejoly 93/377 (BRLU); ibid., 21
Oct 1993, Lejoly 93/422 (BRLU); Monte Alen
National Park, 7 Oct 1994, Lejoly 94/168 (BRLU);
ibid., 7 Oct 1994, Lejoly 94/185 (BRLU); ibid., 22 Sep
1997, Lisowski 1554 (BRLU); ibid., 22 Sep 1997,
Lisowski 1571A (BRLU); ibid., 28 May 1997, Ngomo
0173 (BRLU); ibid., 16 Jun 1998, Ngomo & Ndong
348 (BRLU); ibid., 10 Aug 1998, Ngomo & Ndong 439
(BRLU); 5 km west of Engong (Monte Alen National
Park), 3 Jul 1999, N. Nguema & Parmentier 446 (BR,
BRLU); s.loc., 1 Dec 1997, Obama 347 (BRLU); S du
Rio Laña, près de la Cabaña Ecofac de Misergue
(south-east Monte Alen National Park), 13 Jul 2002,
Senterre & Obiang 3323 (BRLU); 2 km north-east of
Nkumékié (south-east Monte Alen National Park), 8
Dec 2002, Senterre & Obiang 3679 (BRLU); 8.5 km
east de la Cabaña de Mosumo (Monte Alen National
Park), 4 Jul 2003, Senterre & Obiang 3991 (BRLU);
Monte Alen, 10 Aug 2001, Sonké et al. 2501 (BR);
Transect Monte Chocolate (Monte Alen National
Park), 8 Jan 1998, Van Reeth 145 (BRLU).
GABON. Crystal mountains, 15 Nov 2000, N.
Nguema 1304, 1391 (WAG); Tchimbélé, 17 Dec 1998,
Wieringa 244 (WAG).
7. GLOBULOSTYLIS TALBOTII WERNHAM, Cat. Pl.
Oban: 50. 1913. Cuviera talbotii (Wernham)
Verdc., Kew Bull. 42: 189. 1987. Type: NIGERIA,
Oban, 4 Apr 1912, Talbot 2051 (lectotype designated
here:
BM000903503!;
isolectotypes:
BM000903504!, K000412052!, K000412053!).
Distribution: Endemic to Lower Guinea Domain:
restricted to extreme south-east Nigeria and adjacent
south-west Cameroon.
Notes: Globulostylis talbotii is closely related to
G. dewildeana, which has been previously mistaken
for it in herbaria, but has much smaller flowers and
a more north-westerly range. From the sympatric
G. minor and G. rammelooana, it can be told apart by
the ciliate calyx and the corolla pubescent outside on
the midrib of the lobes.
Additional specimens examined: CAMEROON. Boa,
Ekema 1131b (K, SCA); ibid., Ekema 1212 (K, SCA);
western side of Mount Koupé, near Mbule, 24 Jan
1972, Leeuwenberg 9275 (BR, P, WAG, YA); Mbu
Bakundu, Mamfe road, Nemba & Mambo 714 (K);
Boa, Pouakouyou 76 (K, SCA); Bonjare, Tchouto 1162
(K, SCA); Korup National Park, Jan 1972; D.W.
Thomas 593 (BR); south end of Korup National Park,
Mar 1986, D.W. Thomas & McLeod 5725 (K).
8. GLOBULOSTYLIS UNCINULA (N.HALLÉ) SONKÉ,
O.LACHENAUD & DESSEIN comb. nov. Cuviera
uncinula N.Hallé, Bull. Soc. Bot. France 106: 343.
1960. syn. nov. Type: GABON. La Nkoulounga
(north-east Libreville), 3 Jul 1959, N. Hallé 719
(holotype: P00553433!; isotype: P00553432!).
Distribution: Lower Guinea and Congolia Domains:
main range in Gabon and adjacent Republic of Congo,
with a smaller area in the central Democratic Republic of the Congo.
Notes: G. uncinula differs from other related species
(G. leniochlamys, G. minor, G. rammelooana and
G. robbrechtiana) in having consistently one-flowered
inflorescences and in combining a short corolla tube
with a large calyx. Fruiting specimens are difficult to
separate from G. leniochlamys, but the two species
have different ranges.
Globulostylis uncinula, until now regarded as a
Gabonese endemic, is newly reported from the Democratic Republic of the Congo and the Republic of
Congo.
Additional specimens examined: DEMOCRATIC
REPUBLIC OF THE CONGO. Imbow, 11 Feb 1959,
Evrard 5689 (BR); Mompono, 25 Feb 1959, Evrard
5834 (BR, K, WAG).
GABON. near Yombi (on Fougamou–Mouila road,
Koumounabouali ridge), 19 Sep 1990, Breteler 13993
(WAG); Mount Songou (between Poungui and
Dibandi), 23 Feb 2008, Dessein et al. 2116 (BR, LBV);
base of Mount Iboundji, 3 Mar 2008, Dessein et al.
2337 (BR, LBV); La Nkoulounga, 3 Jul 1959, N. Hallé
724 (P); Abanga chantier CEFA, 11 Jun 1963, N.
Hallé 2447 (P); Iméno Ivinzi, 23 Mar 1927, Le Testu
6446 (BM, BR, P); east chantier Mitendi, 21 Oct 1999,
Sosef et al. 583 (WAG); Mount Iboundji, 10 Feb 2000,
Sosef et al. 720 (BRLU, WAG); c. 40 km north-east of
Mitzic (forestry concession Bordamur), 6 Feb 2003,
Sosef et al. 1891 (WAG); c. 50 km south of Mandji
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
(Doudou Moutains), 17 Nov 2005, Sosef et al. 2367
(WAG); Shell oil-exploitation Rabi, 1 km south-east of
Shell camp., 8 Mar 1994, Wieringa 2416 (WAG); north
Ndouaniang (‘Sogacel’), 6 Aug 1984, Wilks 987 (WAG).
REPUBLIC OF CONGO. Maamar forest exploitation (towards N’Gongo-N’Dindi junction), 5 Feb 1974,
Sita 3648 (P, WAG); around junction N’Dindi-N’Gongo
and N’Tiétié, 10 Dec 1974, Sita 3816 (P); Bambama,
6 May 1983, Sita 4790 (BR, P).
SPECIES
EXCLUDED FROM
CUVIERA
1. CUVIERA AUSTRALIS K.Schum. – now a synonym of
Vangueria lasiantha (Sond.) Sond. (Bridson, 1998).
2. CUVIERA BOLO Aubrév. & Pellegr. – now a synonym
of Robynsia glabrata Hutch. (Hepper & Keay,
1963).
3. CUVIERA CALYCOSA WERNHAM, J. Bot. 52: 7. 1914.
Type: NIGERIA. Eket District, Talbot 3300 (lectotype designated here: BM000903513!; isolectotypes
designated here: BM000903512!, K000412057!,
K000412058!).
Distribution: Lower Guinea and Congolia Domains:
Cameroon, Democratic Republic of the Congo, Gabon,
Nigeria, Republic of the Congo.
Notes: This species is excluded from Cuviera, but not
otherwise placed (see Discussion). It differs from
C. nigrescens only (see below) in the size of calyx
lobes, so an intraspecific rank might be more appropriate. Mengé 5 (BR) is the first record from the
Democratic Republic of Congo.
4. CUVIERA MIGEODII VERDC., Fl. Trop. E. Afr.,
Rubiac. (3): 771. 1991. Type: TANZANIA. Tendaguru, Lindi District, 18 Dec 1930, Migeod 1052
(holotype: BM000903510!).
Distribution: South Tanzania (Lindi District).
Notes: This species is excluded from Cuviera, but not
otherwise placed (see Discussion).
5. CUVIERA NIGRESCENS (SCOTT-ELLIOTT EX OLIV.)
WERNHAM, J. Bot. 49: 321. 1911. Vangueria nigrescens Elliott ex Oliv., Bot. J. Linn. Soc. 30: 81.
1895. Type: SIERRA LEONE. Fabala, Mar 1892,
Scott-Elliot 5736 (lectotype designated here:
K000412056!); in forest near Kafogo, 6 Apr 1892,
Scott-Elliot 5610 (syntype: K00412055!).
Synonyms: Cuviera trichostephana K.Schum., Bot.
Jahrb. Syst. 23: 461. 1897. Type: SIERRA LEONE.
s.loc., Scott-Elliot s.n. (K).
Cuviera minor C.H.Wright, Bull. Misc. Inform.
433
Kew. 1906: 105. 1906. Type: GHANA. Kwahu, 2 Apr
1900, Johnson 646 (lectotype designated here:
K000412054!).
Distribution: Upper and Lower Guinea Domains:
Cameroon, Central African Republic, Democratic
Republic of the Congo, Gabon, Ghana, Guinea,
Guinea-Bissau, Ivory Coast, Liberia, Nigeria and
Sierra Leone.
Notes: This species is excluded from Cuviera, but not
otherwise placed (see Discussion). The original
description is based on two syntypes, one of which is
selected as lectotype.
6. CUVIERA SCHLIEBENII VERDC., Kew Bull. 33: 497.
1979. Type: TANZANIA. Lutamba See, Lindi District, 1 Nov 1934, Schlieben 5576 (holotype:
B100160713!;
isotypes:
BR0000008846815!,
EA000002930!, LISC002649!, PRE0593394-0!,
US00664144!).
Distribution: Mozambique and south Tanzania.
Notes: This species is excluded from Cuviera, but not
otherwise placed (see Discussion).
7. CUVIERA SEMSEII VERDC., Kew Bull. 12: 449. 1957.
Type: TANZANIA. Mchinjiri, Rondo Plateau, Lindi
District, 823 m, Jan 1952, Semsei 620 (holotype:
EA000002929!;
isotypes:
BR0000008846808!,
K000412039!).
Distribution:
Tanzania.
Malawi,
Mozambique
and
south
Notes: This species is excluded from Cuviera, but not
otherwise placed (see Discussion). It is close to
C. nigrescens and we are not convinced they are specifically distinct.
8. CUVIERA TOMENTOSA VERDC., Kew Bull. 36: 557.
1981. Type: TANZANIA. Kilwa District, Selous
Game Reserve, approximately 15 km south-west of
Kingupira, 8°35′S 38°27′E, 175 m, 21 Dec 1975,
Vollesen 3122 (holotype: K; isotypes: C, EA, WAG).
Distribution: North Mozambique (Niassa Province) to
south Tanzania (Lindi Region).
Notes: This species is excluded from Cuviera, but not
otherwise placed (see Discussion).
ACKNOWLEDGEMENTS
This research was supported financially by the
Research Foundation – Flanders (FWO, G.0343.09N),
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
434
B. VERSTRAETE ET AL.
the King Leopold-III Fund for Nature Exploration
and Conservation, the Sud Expert Plantes project (no.
375), the F.F.R.S.A. (Fondation pour Favoriser les
Recherches Scientifiques en Afrique), the Alberta
Mennega Stichting and SYNTHESYS. B.V. holds a
PhD research grant from the Agency for Innovation
by Science and Technology (IWT, no. 91158). O.L. is a
research fellow of the F.R.S.-F.N.R.S. (National Fund
for Scientific Research). B.S.’s visits to Belgium were
partly funded by the Université Libre de Bruxelles
and the F.R.S.-FNRS. We thank the curators of the
following herbaria for their help while working in
their institutions and/or the loan of material: BM,
BNRH, BR, BRLU, HBG, K, MPU, P, LBV, WAG and
YA. Dr Petra De Block is acknowledged for her help
in the description of Globulostylis robbrechtiana.
Murielle Simo, Quentin Luke and Olivier Maurin
kindly allowed us to reproduce their photographs.
B.S.’s visits to Belgium and France in 2012, during
which time this paper was finalized, were funded by
the ‘Institut de Recherche pour le Développement
(IRD)’, under the ISMOBIAC project. Thanks are due
to Dr Pierre Couteron (Institut de Recherche pour le
Développement IRD – AMAP), Dr Olivier Hardy
(Laboratoire d’Eco-éthologie évolutive, Université
Libre de Bruxelles) and Dr Tariq Stévart (Herbarium
et Bibliothèque de Botanique africaine, Université
Libre de Bruxelles) for their assistance. We are deeply
grateful to Dr Vincent Droissart, Yves Issembé, Dr
Steven Janssens, Thomas Nzabi, Murielle Simo,
Hermann Taedoumg and Lise Zemagho for help with
the collection of plant material.
REFERENCES
Albuquerque S, Brummit R, Figueiredo E. 2009. Typification of names based on the Angolan collections of Friedrich Welwitsch. Taxon 58: 641–646.
Bridson DM. 1998. Rubiaceae (Tribe Vanguerieae). In: Pope
GV, ed. Flora Zambesiaca, Vol. 5, part 2. Kew: Royal
Botanic Gardens, 211–377.
Brunel J-F, Hiepko P, Scholz H. 1984. Flore analytique du
Togo. Englera 4: 1–751.
Cable S, Cheek M. 1998. Plants of Mount Cameroon: a
conservation checklist. London: Kew Publishing.
de Candolle AP. 1807. Mémoire sur le Cuviera. Annales du
Muséum National d’Histoire Naturelle 9: 216–222.
Compère P. 1962. Observations sur la flore du Bas-Congo.
Bulletin du Jardin Botanique de l’État à Bruxelles 32:
199–211.
Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper
A, Duran C, Field M, Heled J, Kearse M, Markowitz S,
Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson
A. 2011. Geneious v5.4. Available at: http://www.geneious.
com
Govaerts R, Ruhsam M, Andersson L, Robbrecht E,
Bridson D, Davis A, Schanzer I, Sonké B. 2012. World
checklist of Rubiaceae. Facilitated by the Royal Botanic
Gardens, Kew. Published on the Internet. Available at:
http://apps.kew.org/wcsp Retrieved 2012-05-02.
Hallé N. 1960. Sur les Cuviera (Rubiacées) d’Afrique intertropicale et description pour ce genre de deux espèces et de
deux variétés nouvelles. Bulletin de la Société Botanique de
France 106: 342–348.
Hawthorne W, Jongkind C. 2006. Woody plants of western
African forests. A guide to the forest trees, shrubs and lianes
from Senegal to Ghana. Kew: Royal Botanic Gardens.
Hepper FN, Keay RWJ. 1963. Rubiaceae. In: Hepper FN, ed.
Flora of west tropical Africa, 2nd edn, Vol. 2. London: Crown
Agents, 104–223.
Hiern WP. 1877. Rubiaceae. In: Oliver D, ed. Flora of tropical
Africa, Vol. 3. London: Reeve & Co, 33–247.
Hooker WJ. 1849. Niger flora or an enumeration of the plants
of western tropical Africa collected by the late Dr Theodore
Vogel, botanist to the voyage of the expedition sent by her
Britannic Majesty to the river Niger in 1841. London: H.
Bailliere.
Krause K. 1912. Rubiaceae africanae. Botanische Jahrbücher
für Pflanzensystematik und Pflanzengeographie 48: 403–
433.
Lantz H, Andreasen K, Bremer B. 2002. Nuclear rDNA ITS
sequence data used to construct the first phylogeny of Vanguerieae (Rubiaceae). Plant Systematics and Evolution 230:
173–187.
Lantz H, Bremer B. 2004. Phylogeny inferred from morphology and DNA data: characterizing well-supported groups in
Vanguerieae (Rubiaceae). Botanical Journal of the Linnean
Society 146: 257–283.
Lantz H, Bremer B. 2005. Phylogeny of the complex Vanguerieae (Rubiaceae) genera Fadogia, Rytigynia, and Vangueria with close relatives and a new circumscription of
Vangueria. Plant Systematics and Evolution 253: 159–183.
Löhne C, Borsch T. 2005. Molecular evolution and phylogenetic utility of the petD group II intron: a case study in basal
angiosperms. Molecular Biology and Evolution 22: 317–332.
Mildbraed J. 1924. Additamenta africana I. Notizblatt des
Botanischen Gartens und Museums zu Berlin-Dahlem 9:
200–207.
Miller MA, Pfeiffer W, Schwartz T. 2010. Creating the
CIPRES Science Gateway for inference of large phylogenetic
trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE). New Orleans, USA, 1–8.
Onana JM. 2008. A new combination and key to the species
of Cuviera subgenus Globulostylis (Rubiaceae: Vanguerieae)
from Central Africa. Kew Bulletin 63: 401–403.
Posada D. 2008. jModelTest: phylogenetic model averaging.
Molecular Biology and Evolution 25: 1253–1256.
Razafimandimbison SG, Lantz H, Mouly A, Bremer B.
2009. Evolutionary trends, major lineages, and new generic
limits in the dioecious group of the tribe Vanguerieae (Rubiaceae): insights into the evolution of functional dioecy.
Annals of the Missouri Botanical Garden 96: 161–181.
Robyns W. 1928. Tentamen monographiae Vanguerieae
generumque affinium. Bulletin du Jardin Botanique de
l’État à Bruxelles 11: 1–359.
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
Schumann K. 1888. Einige neue Ameisenpflanzen. Jarbücher für Wissenschaftliche Botanik 19: 357–421.
Schumann K. 1899. Rubiaceae africanae. Botanische Jahrbücher für Pflanzensystematik und Pflanzengeographie 28:
55–113.
Schumann K. 1903. Rubiaceae africanae. Botanische Jahrbücher für Pflanzensystematik und Pflanzengeographie 33:
333–374.
Shaw J, Lickey EB, Schilling EE, Small RL. 2007. Comparison of whole chloroplast genome sequences to choose
noncoding regions for phylogenetic studies in angiosperms:
the tortoise and the hare III. American Journal of Botany
94: 275–288.
Simmons MP, Ochoterena H. 2000. Gaps as characters in
sequence-based phylogenetic analyses. Systematic Biology
49: 369–381.
Sosef MSM, Wieringa JJ, Jongkind CCH, Achoundong
G, Azizet Issembé Y, Bedigian D, Van Den Berg RG,
Breteler FJ, Cheek M, Degreef J, Faden RB, Goldblatt
P, Van Der Maesen LJG, Ngok Banak L, Niangadouma
R, Nzabi T, Nziengui B, Rogers ZS, Stévart T,
Van Valkenburg JLCH, Walters G, de Wilde JJFE.
2006. Checklist of Gabonese vascular plants. Scripta
Botanica Belgica 35. Meise: National Botanic Garden of
Belgium.
Swoffort DL. 2002. PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4. Sunderland, MA:
Sinauer Associates.
Tosh J, Davis AP, Dessein S, De Block P, Huysmans S,
Fay MF, Smets E, Robbrecht E. 2009. Phylogeny of
Tricalysia (Rubiaceae) and its relationships with allied
genera based on plastid DNA data: resurrection of the genus
Empogona. Annals of the Missouri Botanical Garden 96:
194–213.
Verdcourt B. 1957. Notes from the East African herbarium.
IV. Kew Bulletin 11: 445–454.
Verdcourt B. 1981. Notes on African Rubiaceae. Kew Bulletin
36: 493–557.
Verdcourt B. 1987. Notes on African Rubiaceae–
Vanguerieae. Kew Bulletin 42: 123–199.
Verdcourt B, Bridson DM. 1991. Flora of Tropical East
Africa. Rubiaceae (part 3). Rotterdam: A. A. Balkema.
Wernham HF. 1913. Globulostylis. In: Rendle AB, Baker EG,
Moore S, eds. Catalogue of the plants collected by Mr and
Mrs P. A. Talbot in the Oban district South Nigeria. London:
British Museum, 49–51.
Wernham HF. 1914. Cuviera calycosa. Journal of Botany,
British and Foreign 52: 7–8.
Wernham HF. 1918. New Rubiaceae from the Belgian Congo.
Journal of Botany, British and Foreign 56: 309–314.
White F. 1979. The Guineo–Congolian Region and its relationship to other phytochoria. Bulletin du Jardin botanique
national de Belgique 49: 11–55.
White T, Bruns T, Lee S-T, Taylor J. 1990. Amplification
and direct sequencing of fungal ribosomal RNA genes for
phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T,
eds. PCR protocols: a guide to methods and applications.
San Diego, CA: Academic Press, 315–322.
APPENDIX 1
ACCESSIONS
435
INCLUDED IN THE PHYLOGENETIC ANALYSIS
Taxon*
Voucher
trnTF
rpl16
petD
ITS
rpl32trnL
accDpsaI
Afrocanthium
gilfillanii (N.E.Br.)
Lantz
Afrocanthium
lactescens (Hiern)
Lantz
Afrocanthium
mundianum
(Cham. &
Schltdl.) Lantz
Bullockia
pseudosetiflora
(Bridson)
Razafim., Lantz &
B.Bremer
Bullockia setiflora
(Hiern) Razafim.,
Lantz & B.Bremer
Canthium ciliatum
(D.Dietr.) Kuntze
Lemaire &
Verstraete 32
(BR)
Kuchar 23003
(BR)
JQ958219
JQ958112
JQ958036
–
–
–
JQ958221
JQ958113
JQ958037
–
–
–
Lemaire &
Verstraete 33
(BR)
JQ958220
JQ958114
JQ958038
–
–
–
Bidgood et al.
4959 (BR)
JQ958222
JQ958115
JQ958039
JQ957968
–
–
Lemaire &
Verstraete 197
(BR)
Lemaire &
Verstraete 281
(BR)
JQ958223
JQ958116
JQ958040
JQ957969
–
–
JQ958230
JQ958122
JQ958049
–
–
–
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
436
B. VERSTRAETE ET AL.
APPENDIX 1 Continued
Taxon*
Voucher
trnTF
rpl16
petD
ITS
rpl32trnL
accDpsaI
Canthium
coromandelicum
(Burm.f.) Alston
Canthium glaucum
Hiern
Canthium inerme
(L.f.) Kuntze
Andreasen 36
(UPS)
AJ620122
AJ876810
–
AJ315081
–
–
Kuchar 17410
(BR)
Lemaire &
Verstraete 235
(BR)
Lemaire &
Verstraete 241
(BR)
Lemaire &
Verstraete 187
(BR)
Burrows &
Burrows 9858
(BNRH)
Dessein et al.
2809 (BR)
Amsini 97 (BR)
JQ958231
JQ958123
JQ958046
JQ957970
–
–
JQ958232
JQ958124
JQ958047
JQ957971
–
–
JQ958233
JQ958125
JQ958050
–
–
–
JQ958235
JQ958126
JQ958048
JQ957972
–
–
JQ958234
JQ958127
–
–
–
–
JQ958270
JQ958157
JQ958076
JQ957973
JQ958201
JQ957948
JQ958271
–
JQ958077
JQ957974
JQ958197
JQ957951
JQ958159
JQ958079
JQ957975
JQ958199
JQ957953
JQ958158
JQ958078
JQ957976
JQ958198
JQ957949
JQ958274
JQ958160
JQ958080
JQ957977
JQ958200
JQ957950
JQ958276
–
JQ958082
JQ957978
–
JQ957962
JQ958280
–
JQ958086
JQ957979
JQ958205
JQ957965
JQ958275
JQ958161
JQ958081
JQ957980
JQ958202
JQ957952
JQ958236
JQ958132
–
–
–
–
JQ958244
JQ958128
JQ958052
–
–
–
JQ958239
–
JQ958053
–
–
–
JQ958240
JQ958129
JQ958054
JQ957981
JQ958179
JQ957933
JQ958238
JQ958133
–
–
–
–
JQ958241
JQ958130
JQ958055
JQ957982
–
–
Canthium
kuntzeanum
Bridson
Canthium spinosum
(Klotzsch ex Eckl.
& Zeyh.) Kuntze
Canthium
suberosum Codd
Cuviera acutiflora
DC.
Cuviera angolensis
subsp. latior
(Wernham) Sonké,
O.Lachenaud &
Dessein
Cuviera longiflora
Hiern
Cuviera physinodes
K.Schum.
Cuviera physinodes
K.Schum.
Cuviera schliebenii
Verdc.
Cuviera semseii
Verdc.
Cuviera subuliflora
Benth.
Fadogia ancylantha
Schweinf.
Fadogia cienkowskii
Schweinf.
Fadogia fuchsioides
Schweinf. ex Oliv.
Fadogia homblei De
Wild.
Fadogia salictaria
S.Moore
Fadogia stenophylla
subsp. odorata (K.
Krause) Verdc.
Dessein et al.
JQ958272
2713 (BR)
Chatrou 572 (BR) JQ958273
Dessein et al.
1416 (BR)
Burrows &
Burrows 9839
(BNRH)
Burrows &
Burrows 11303
(BNRH)
Dessein et al.
2004 (BR)
Dessein et al.
1101 (BR)
Dessein et al. 258
(BR)
Dessein et al.
1083 (BR)
Lemaire &
Verstraete 22
(BR)
Malaisse 13490
(BR)
Lovett 2267 (BR)
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
437
APPENDIX 1 Continued
Taxon*
Voucher
trnTF
Fadogia tetraquetra
K.Schum. &
K.Krause
Fadogia triphylla
Baker
Fadogia verdickii
De Wild. &
T.Durand
Fadogiella
stigmatoloba
(K.Schum.)
Robyns
Globulostylis
leniochlamys
(K.Schum.) Sonké,
O.Lachenaud &
Dessein
Globulostylis minor
Wernham
Globulostylis
rammelooana
Sonké,
O.Lachenaud &
Dessein
Globulostylis
rammelooana
Sonké,
O.Lachenaud &
Dessein
Globulostylis
rammelooana
Sonké,
O.Lachenaud &
Dessein
Globulostylis
rammelooana
Sonké,
O.Lachenaud &
Dessein
Globulostylis
robbrechtiana
Sonké,
O.Lachenaud,
Dessein & De
Block
Globulostylis
uncinula (N.Hallé)
Sonké,
O.Lachenaud &
Dessein
Lemaire &
JQ958242
Verstraete 223
(BR)
Dessein et al. 226 JQ958237
(BR)
Schaijes 1502
JQ958243
(BR)
rpl16
petD
ITS
rpl32trnL
accDpsaI
JQ958131
JQ958056
–
–
–
JQ958134
–
–
–
–
JQ958135
–
JQ957984
–
–
Gillett 17403
(BR)
JQ958245
JQ958136
–
JQ957983
–
–
Dessein et al.
1448 (BR)
JQ958269
JQ958152
JQ958070
JQ957985
JQ958189
JQ957947
Dessein et al.
2876 (BR)
Dessein et al.
1546 (BR)
JQ958261
JQ958151
JQ958075
JQ957986
JQ958190
JQ957939
JQ958267
JQ958153
JQ958071
JQ957987
JQ958193
JQ957942
Sonké et al. 4650
(BR)
JQ958266
–
–
–
JQ958191
JQ957943
Sonké et al. 4671
(BR)
JQ958264
–
–
JQ957988
–
JQ957941
Sonké et al. 4711
(BR)
JQ958265
–
–
–
JQ958192
JQ957940
Sonké et al. 4868
(BR)
JQ958268
JQ958154
JQ958072
JQ957989
JQ958194
JQ957944
Dessein et al.
2116 (BR)
JQ958262
JQ958155
JQ958073
JQ957990
JQ958195
JQ957946
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
438
B. VERSTRAETE ET AL.
APPENDIX 1 Continued
Taxon*
Voucher
trnTF
rpl16
petD
ITS
rpl32trnL
accDpsaI
Globulostylis
uncinula (N.Hallé)
Sonké,
O.Lachenaud &
Dessein
Ixora finlaysoniana
Wall. ex G.Don
Dessein et al.
2337 (BR)
JQ958263
JQ958156
JQ958074
JQ957991
JQ958196
JQ957945
Van
Caekenberghe
54 (BR)
Lemaire &
Verstraete 97
(BR)
Dessein et al.
1261 (BR)
Dessein et al.
1085 (BR)
JQ958210
JQ958105
JQ958028
–
–
–
JQ958211
JQ958106
JQ958029
–
–
–
JQ958212
JQ958107
–
JQ957992
–
–
JQ958277
JQ958162
JQ958083
–
–
–
Dessein et al.
2949 (BR)
JQ958278
JQ958163
JQ958084
JQ957993
JQ958204
JQ957963
De Block et al.
2487 (BR)
Lemaire &
Verstraete 174
(BR)
Van
Caekenberghe
60 (BR)
Lemaire &
Verstraete 163
(BR)
JQ958224
JQ958117
JQ958041
–
–
–
JQ958229
JQ958121
JQ958051
JQ957994
–
–
JQ958208
JQ958104
JQ958026
–
–
–
JQ958213
JQ958109
JQ958030
JQ957995
–
–
JQ958214
–
JQ958031
–
–
–
JQ958215
JQ958108
JQ958032
JQ957996
–
–
JQ958216
JQ958110
JQ958033
JQ957997
–
–
JQ958217
–
JQ958034
JQ957998
–
–
JQ958218
JQ958111
JQ958035
JQ957999
–
–
JQ958228
JQ958120
JQ958045
JQ958000
–
–
JQ958279
–
JQ958085
JQ958001
JQ958203
JQ957964
JQ958225
JQ958118
JQ958042
JQ958002
–
–
Keetia gueinzii
(Sond.) Bridson
Keetia venosa (Oliv.)
Bridson
Multidentia crassa
(Hiern) Bridson &
Verdc.
Multidentia
dichrophylla
(Mildbr.) Bridson
Peponidium sp.
Plectroniella armata
(K.Schum.)
Robyns
Pseudomussaenda
flava Verdc.
Psydrax
fragrantissima
(K.Schum.)
Bridson
Psydrax kraussioides
(Hiern) Bridson
Psydrax livida
(Hiern) Bridson
Psydrax locuples
(K.Schum.)
Bridson
Psydrax obovata
(Klotzsch ex Eckl.
& Zeyh.) Bridson
Psydrax parviflora
(Afzel.) Bridson
Pygmaeothamnus
chamaedendrum
(Kuntze) Robyns
Pygmaeothamnus
zeyheri (Sond.)
Robyns
Pyrostria bibracteata
(Baker) Cavaco
Dessein et al.
1285 (BR)
Lemaire &
Verstraete 14
(BR)
Lemaire &
Verstraete 287
(BR)
Lemaire &
Verstraete 188
(BR)
Dessein et al.
1345 (BR)
Lemaire &
Verstraete 142
(BR)
Lemaire &
Verstraete 2
(BR)
Burrows &
Burrows 10784
(BNRH)
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
439
APPENDIX 1 Continued
Taxon*
Voucher
trnTF
rpl16
petD
ITS
rpl32trnL
accDpsaI
Pyrostria hystrix
(Bremek.) Bridson
Lemaire &
Verstraete 270
(BR)
De Block et al.
2423 (BR)
JQ958226
–
JQ958043
JQ958003
–
–
JQ958227
JQ958119
JQ958044
–
–
–
Tosh et al. 263
(BR)
JQ958209
–
JQ958027
–
–
–
Hall &
Amponsah
46545 (K)
Lachenaud et al.
739 (BR)
AJ620170
–
–
AJ617774
–
–
JQ958246
JQ958137
JQ958057
JQ958004
–
JQ957934
Niyongabo 53
(BR)
JQ958247
JQ958138
JQ958058
–
–
JQ957935
Dessein et al.
2961 (BR)
Dessein et al.
2541 (BR)
Lachenaud et al.
852 (BR)
JQ958248
JQ958139
JQ958060
JQ958005
–
JQ957936
JQ958249
JQ958140
JQ958059
JQ958006
JQ958180
JQ957938
JQ958250
JQ958141
JQ958061
JQ958007
–
JQ957937
JQ958281
JQ958164
JQ958087
JQ958008
–
–
JQ958284
Lemaire &
Verstraete 233
(BR)
Dessein et al. 202 JQ958282
(BR)
JQ958170
JQ958097
JQ958009
–
–
JQ958165
JQ958088
JQ958010
–
–
JQ958283
–
JQ958089
JQ958011
–
–
JQ958285
JQ958166
JQ958090
–
–
–
JQ958289
JQ958171
JQ958093
JQ958012
JQ958206
JQ957966
JQ958287
JQ958168
JQ958091
–
–
–
JQ958296
JQ958169
JQ958101
JQ958013
–
–
JQ958288
JQ958172
JQ958098
JQ958014
JQ958207
JQ957967
Pyrostria serpentina
Lantz, Klack. &
Razafim.
Razafimandimbisonia
humblotii (Drake)
Kainul. &
B.Bremer
Robynsia glabrata
Hutch.
Rytigynia
membranacea
(Hiern) Robyns
Rytigynia monantha
(K.Schum.)
Robyns
Rytigynia neglecta
(Hiern) Robyns
Rytigynia rubra
Robyns
Rytigynia
umbellulata
(Hiern) Robyns
Vangueria agrestis
(Schweinf. ex
Hiern) Lantz
Vangueria bowkeri
(Robyns) Lantz
Vangueria
cinerascens (Welw.
ex Hiern) Lantz
Vangueria discolor
(De Wild.) Lantz
Vangueria dryadum
S.Moore
Vangueria infausta
Burch.
Vangueria lasiantha
(Sond.) Sond.
Vangueria latifolia
(Sond.) Sond.
Vangueria
macrocalyx Sond.
Lejoly 82/390
(BR)
Bidgood et al.
6094 (BR)
Lemaire &
Verstraete 289
(BR)
Lemaire &
Verstraete 13
(BR)
Lemaire &
Verstraete 209
(BR)
Lemaire &
Verstraete 69
(BR)
Lemaire &
Verstraete 114
(BR)
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
440
B. VERSTRAETE ET AL.
APPENDIX 1 Continued
rpl16
petD
ITS
rpl32trnL
accDpsaI
–
JQ958094
–
–
–
JQ958173
–
–
–
–
Ntemi Sallu et al. JQ958293
309 (BR)
JQ958174
JQ958096
JQ958015
–
–
Lemaire &
Verstraete 265
(BR)
Lemaire &
Verstraete 42
(BR)
Lemaire &
Verstraete 98
(BR)
Lemaire &
Verstraete 285
(BR)
Lemaire &
Verstraete 25
(BR)
Lemaire &
Verstraete 53
(BR)
Dessein et al.
1632 (BR)
JQ958294
JQ958175
JQ958099
–
–
–
JQ958297
JQ958177
JQ958102
–
–
–
JQ958291
–
JQ958095
–
–
–
JQ958295
JQ958176
JQ958100
–
–
–
JQ958298
JQ958178
JQ958103
–
–
–
JQ958286
JQ958167
JQ958092
–
–
–
JQ958251
JQ958146
JQ958062
JQ958016
JQ958181
JQ957954
Dessein et al.
1654 (BR)
JQ958252
JQ958147
JQ958063
JQ958017
JQ958182
JQ957955
Jongkind 7887
(WAG)
Lachenaud et al.
689 (BR)
JQ958256
JQ958142
JQ958067
JQ958018
JQ958185
JQ957958
JQ958254
JQ958149
JQ958064
JQ958019
JQ958183
–
Jongkind 3089
(WAG)
JQ958258
JQ958144
JQ958068
JQ958020
JQ958186
JQ957959
Dessein et al.
1574 (BR)
JQ958253
JQ958148
JQ958066
JQ958021
–
JQ957956
Dessein et al.
2415 (BR)
JQ958255
JQ958150
JQ958065
JQ958022
JQ958184
JQ957957
Lachenaud et al.
1119 (BR)
Merello et al.
1494 (K)
JQ958257
JQ958143
–
JQ958023
JQ958188
JQ957960
AJ620182
–
–
AJ315085
–
–
Taxon*
Voucher
Vangueria
madagascariensis
J.F.Gmel.
Vangueria
micropyren
(Verdc.) Lantz
Vangueria
pallidiflora
(Bullock) Lantz
Vangueria parvifolia
Sond.
Lemaire &
JQ958290
Verstraete 189
(BR)
Dessein et al. 253 JQ958292
(BR)
Vangueria pygmaea
Schltr.
Vangueria randii
subsp. chartacea
(Robyns) Verdc.
Vangueria
soutpansbergensis
N.Hahn
Vangueria thamnus
(Robyns) Lantz
Vangueria triflora
(Robyns) Lantz
Vangueriella
chlorantha
(K.Schum.) Verdc.
Vangueriella
chlorantha
(K.Schum.) Verdc.
Vangueriella discolor
(Benth.) Verdc.
Vangueriella
laxiflora
(K.Schum.) Verdc.
Vangueriella
nigerica (Robyns)
Verdc.
Vangueriella
nigricans (Robyns)
Verdc.
Vangueriella
olacifolia (Robyns)
Verdc.
Vangueriella rufa
(Robyns) Verdc.
Vangueriella spinosa
(Schumach. &
Thonn.) Verdc.
trnTF
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441
REVISION OF CUVIERA AND GLOBULOSTYLIS
441
APPENDIX 1 Continued
Taxon*
Voucher
trnTF
rpl16
petD
ITS
rpl32trnL
accDpsaI
Vangueriella
vanguerioides
(Hiern) Verdc.
Vangueriella
vanguerioides
(Hiern) Verdc.
Vangueriopsis
shimbaensis
A.P.Davis &
Q.Luke
Jongkind 7855
(WAG)
JQ958259
–
–
JQ958024
–
–
Kpadeyeah 10
(WAG)
JQ958260
JQ958145
JQ958069
JQ958025
JQ958187
JQ957961
Luke 8316 (UPS)
AJ620183
AJ876875
–
AJ617778
–
–
*Information on taxon, voucher and GenBank numbers for trnT-F, rpl16, petD, internal transcribed spacer (ITS),
rpl32-trnL, accD-psaI.
–, not sequenced.
APPENDIX 2
DNA
MARKERS WITH THEIR RESPECTIVE PRIMER PAIRS, ANNEALING TEMPERATURE, SUBSTITUTION MODEL AND
REFERENCES TO THE SEQUENCES OF THE PRIMERS
Marker
Primer pairs
Annealing
Model
Reference
trnT-L
trnTFa1
trnTLi
trnLFc
trnLFf
L16exon1 (pcr)
RPL16-18R (seq)
1067F
petB1411
petD738
ITS1
ITS4
rpl32F
accD769F
psa175R
55 °C
GTR + G
Lantz & Bremer, 2004
55 °C
GTR + G
Lantz & Bremer, 2004
55 °C
GTR + I + G
Lantz & Bremer, 2005
55 °C
GTR + G
Löhne & Borsch, 2005
50 °C
HKY + G
White et al., 1990
55 °C
55 °C
F81 + I
GTR + I
Shaw et al., 2007
Tosh et al., 2009
trnL-trnF
rpl16
petD
Internal transcribed
spacer (ITS)
rpl32-trnL
accD-psaI
© 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 173, 407–441