Botanical Journal of the Linnean Society, 2010, 163, 447–472. With 9 figures
Amphistemon and Thamnoldenlandia, two new genera
of Rubiaceae (Spermacoceae) endemic to Madagascar
INGE GROENINCKX1*, PETRA DE BLOCK2, ELMAR ROBBRECHT2, ERIK E. SMETS1,3
and STEVEN DESSEIN2
1
Laboratory of Plant Systematics, K.U.Leuven, Kasteelpark Arenberg 31, P.O. Box 2437, BE-3001
Leuven, Belgium
2
National Botanic Garden of Belgium, Domein van Bouchout, BE-1860 Meise, Belgium
3
National Herbarium of the Netherlands, Leiden University Branch, P.O. Box 9514, NL-2300 RA
Leiden, the Netherlands
Received 4 March 2010; revised 21 May 2010; accepted for publication 21 May 2010
Amphistemon and Thamnoldenlandia are described as two new genera of Rubiaceae endemic to Madagascar. The
two novelties belong to the predominantly herbaceous tribe Spermacoceae. Amphistemon is unique within the tribe
in having its stamens inserted at two levels in the corolla tube. The genus includes two species: the subshrub A.
humbertii and the geoxylic herb A. rakotonasolianus. Thamnoldenlandia includes only one species, T. ambovombensis, which differs from most other Spermacoceae in being a medium-sized shrub with winged seeds. We
present a detailed description of Amphistemon and Thamnoldenlandia, including observations of pollen and seeds.
A molecular phylogenetic study based on atpB-rbcL, petD, rps16 and trnL-trnF sequences demonstrates that the
two new genera belong to the Hedyotis–Oldenlandia complex of tribe Spermacoceae. Amphistemon and Thamnoldenlandia are sister taxa and share a common ancestor with the Madagascan endemic genus Astiella. A second,
but not closely related, Madagascan clade includes the endemic genera Lathraeocarpa and Gomphocalyx and the
Afro-Madagascan genus Phylohydrax. This indicates that the Madagascan endemic members of Spermacoceae are
the result of at least two independent colonization events, most likely by long-distance dispersal from the African
mainland. © 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472.
ADDITIONAL KEYWORDS: Astiella delicatula – long-distance dispersal – molecular phylogenetics – scanning electron microscopy – taxonomy.
INTRODUCTION
Madagascar has a unique and spectacularly rich flora
with a high percentage of endemism. The island is
home to more than 10 000 plant species, 90% of which
occur nowhere else in the world (Moat & Smith,
2007). With natural vegetation varying from rainforest to unique spiny forest, Madagascar shows a huge
plant diversity, making it one of the most important
biodiversity hotspots (Moat & Smith, 2007).
On this island hotspot, Rubiaceae are the secondlargest family of flowering plants with approximately
*Corresponding author.
E-mail: inge.groeninckx@bio.kuleuven.be
650 described species and c. 95 genera (Davis &
Bridson, 2003). More than 30% of the genera (Davis &
Bridson, 2003) and 91% of the species (Davis et al.,
2009) are endemic. The inventory of the Madagascan
Rubiaceae is advancing rapidly. In recent years, many
genera have been studied taxonomically, including
Bertiera Aubl. (Wittle & Davis, in press), Breonia
A.Rich ex DC. (Razafimandimbison, 2002), Coffea L.
(Davis & Rakotonasolo, 2001; Davis et al., 2006;
Davis & Rakotonasolo, 2008), Coptosperma Hook.f.
(De Block, Degreef & Robbrecht, 2002), Gyrostipula
J.-F.Leroy (Emanuelsson & Razafimandimbison,
2007), Hymenodictyon Wall. with Paracorynanthe
Capuron (Razafimandimbison & Bremer, 2006), Ixora
L. (De Block, in press), Lathreaocarpa Bremek.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
447
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I. GROENINCKX ET AL.
Table 1. Genera of Spermacoceae present in Madagascar and their diagnostic features
Total no. of species/
Malagasy species/
species endemic to
Madagascar
Genus
Diagnostic feature(s)
Agathisanthemum
Perennial herbs. Inflorescences terminal, many-flowered cymes, corymbs
subglobose heads. Stigma usually one-lobed. Capsules dehiscing
loculicidal and septicidal
Herbs or subshrubs. Stamens inserted at two levels in the corolla tube
Herbs. Isostylous flowers with anthers and style both included. Only two
calyx lobes. Ovaries with uni-ovulate locules. Fruits boat-shaped and
distinctly beaked. Pollen pluri-colporate
Erect or straggling herbs. Ovaries with uni-ovulate locules. Fruits
dehiscing into two indehiscent one-seeded mericarps. Pollen
pluri-colporate
Herbs. Stipules almost truncate, with a few short fimbriae. Ovaries with
uni-ovulate locules. Fruits dry and indehiscent. Pollen pluri-colporate
Herbs. Inflorescences terminal. Flowers isostylous with anthers and style
included. Style with one stigma lobe held below the anthers
(Sub)shrub. Stipules almost truncate, with one short stipular tooth.
Ovaries tri- or tetra-locular, with uni-ovulate locules. Stigma three- to
four-lobed. Fruits indehiscent drupes. Pollen pluri-colporate
Herbs. Flowers often with two large and two small calyx lobes. Ovaries
with uni-ovulate locules. Fruits dehiscing circumscissile. Seeds with
X-shaped ventral groove. Pollen pluri-colporate
Herbs. Capsules distinctly beaked, dehiscing both loculicidally and
septicidally
Herbs. Heterogeneous assemblage of species. No synapomorphies present
Herbs. Flowers five-merous, organised in very lax elongated axillary
inflorescences
Herbs. Ovaries with uni-ovulate locules. Fruits dry and indehiscent.
Pollen pluri-colporate
Herbs. Flowers three-, four- or six-merous. Ovaries with uni-ovulate
locules. Fruits schizocarps, splitting into cocci. Pollen pluri-colporate
Mainly herbs. Heterogeneous assemblage of species. Ovaries with
uni-ovulate locules. Pollen pluri-colporate
Medium-sized shrub. Seeds distinctly winged
Amphistemon
Astiella
Diodella
Gomphocalyx
Kohautia
Lathraeocarpa
Mitracarpus
Mitrasacmopsis
Oldenlandia
Pentodon
Phylohydrax
Richardia
Spermacoce
Thamnoldenlandia
(Groeninckx et al., 2009b), Mantalania Capuron ex
J.-F.Leroy (De Block & Davis, 2006), Paederia L.
(Puff, 1991), Paracephaelis Baill. (De Block, 2003)
and Tricalysia A.Rich ex DC. (RanariveloRandriamboavonjy et al., 2007).
Rubiaceae comprise predominantly shrubs and
trees, which are mostly restricted to the tropics
(Davis et al., 2009). Only a few evolutionary lineages
of Rubiaceae include herbaceous species, of which
most belong to supertribe Rubiidinae of subfamily
Rubioideae (Robbrecht & Manen, 2006). The largest
herbaceous lineage is tribe Spermacoceae Cham. &
Schltd. ex DC. sensu lato (s.l.), uniting the former
tribes Spermacoceae sensu stricto (s.s.), Manettieae
Bremek. and the Hedyotis L.–Oldenlandia L. complex
(including most taxa of the former tribe Hedyotideae
4/1/0
2/2/2
1/1/1
16/1/0
1/1/1
32/2/0
2/2/2
58/1/0
1/1/0
c. 240/6/0
2/1/0
2/1/1
16/1/0
250(300)/6(10)/1?
1/1/1
Cham. & Schlecht.) (Kårehed et al., 2008; Groeninckx
et al., 2009a).
Madagascan Spermacoceae are still under revision.
Table 1 lists all genera of Spermacoceae currently
known to be present in Madagascar with their diagnostic features and number of (endemic) species. Of
the 15 genera listed in Table 1, two genera are newly
described in this paper, i.e. Amphistemon Groeninckx
and Thamnoldenlandia Groeninckx. Their fimbriate
stipules, tetramerous heterostylous white flowers,
two-lobed styles, bilocular ovaries, fleshy multiovulate placentas attached to the middle of the
septum and beaked capsules point to a position in the
Hedyotis–Oldenlandia complex of Spermacoceae.
Amphistemon includes two species, A. humbertii
Groeninckx and A. rakotonasolianus Groeninckx,
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
TWO NEW RUBIACEAE GENERA ENDEMIC TO MADAGASCAR
which are unique within Spermacoceae in having
their anthers positioned at two levels in the corolla
tube. Thamnoldenlandia Groeninckx is described as a
monospecific genus. Its only species T. ambovombensis Groeninckx differs from most other Spermacoceae
in being a medium-sized shrub with winged seeds.
Besides a detailed description (including pollen and
seed observations) of the two new genera, we also
present the results of a molecular phylogenetic study
illuminating the taxonomic position of Amphistemon,
Thamnoldenlandia and the monospecific Madagascan
genus Astiella Jovet. To date, no molecular data have
been available for Astiella and its taxonomic position
has remained controversial.
MATERIAL AND METHODS
DESCRIPTIONS
Amphistemon humbertii, A. rakotonasolianus, Thamnoldenlandia ambovombensis and Astiella delicatula
Jovet were collected and studied in the field in
January–February 2007 (De Block et al., 2294; Groeninckx et al., 147; De Block et al., 2328; De Block et al.,
2173, respectively). Fieldwork in March–April 2010
resulted in two more collections of Thamnoldenlandia
ambovombensis (De Block et al., 2386; Groeninckx
et al., 330). Herbarium material of the three new
species was consulted at BR, K, MO, P and TAN
(abbreviations after Holmgren, Holmgren & Barnett,
1990). Terminology in the descriptions follows Stearn
(1966). Measurements, colours and other details
given in the descriptions are based on spirit and
herbarium specimens and data derived from field
notes. Maps for the Madagascan endemics were made
with the software programme iMap (Schols, Dessein
& Smets, 2001).
CONSERVATION
ASSESSMENTS
Geo-referenced specimen data were imported into
ArcView™ geographic information software to calculate area of occupancy (AOO) and extent of occurrence
(EOO) for each species using Cats 1.2 (Moat, 2007).
AOO and EOO figures were used in conjunction with
field observations to produce conservation ratings
based on the IUCN Red List Categories criteria
(IUCN, 2001).
MICROMORPHOLOGICAL
OBSERVATIONS
Pollen grains from herbarium material were acetolysed according to Reitsma’s (1969) ‘wetting agent’
method. Using scanning electron microscopy (SEM),
external features were observed on grains that had
been suspended in 70% ethanol and left to dry.
Glycerin jelly slides were observed under a light
449
microscope. Untreated pollen grains from anthers
preserved in 70% ethanol were also studied following
the method of Halbritter (1998), but using
dimethoxymethane (DMM) instead of dimethoxypropane (DMP). Polar axis length (P) and equatorial
diameter (E) were measured on 20 grains from thrum
(brevistylous) and 20 from pin (longistylous) flowers
using the software program Carnoy (Schols et al.,
2002). Pollen terminology follows Punt et al. (2007).
Seeds from herbarium specimens were directly
mounted on aluminium stubs, coated with gold and
observed under the SEM as described above.
MOLECULAR
STUDY
To reveal the taxonomic position of the three new
species and Astiella delicatula, a molecular analysis
was carried out using sequence data of atpB-rbcL,
petD, rps16 and trnL-trnF from previous studies
within Spermacoceae (Andersson & Rova, 1999;
Andersson, Rova & Alzate, 2002; Dessein et al.,
2005; Kårehed et al., 2008; Groeninckx et al., 2009a,
b). DNA of the three new species and Astiella delicatula was isolated from silica dried leaf material
collected in the field (see above for voucher information). Methods for DNA extraction, PCR amplification, sequencing, sequence assembly, alignment
and gap coding are as described by Kårehed et al.
(2008). Our sampling includes 111 species representing 37 of the c. 62 genera currently recognized
within Spermacoceae (including the two new
genera). The Appendix lists all taxa included in the
molecular phylogenetic study, with author names,
voucher information and GenBank accession
numbers.
Equally weighted parsimony analyses were performed using Nona 2.0 (Goloboff, 1993) launched
through WinClada 1.0 (Nixon, 2002). The four plastid
regions were first analysed separately and then combined using a total evidence approach. Heuristic
searches for the shortest trees were performed using
the parsimony ratchet (Nixon, 1999). Ratchet runs of
200 iterations each, holding one tree per iteration and
randomly weighting 10% of the potentially informative characters, were carried out until the most parsimonious trees (MPTs) were repeatedly found. A
strict consensus tree was calculated using the trees
obtained in the parsimony ratchet analyses. In order
to evaluate the relative support of the clades, jackknife (JS) and bootstrap (BS) analyses were executed
using 1000 replicates with 100 initial trees holding
one tree per random addition, carrying out tree
bisection–reconnection (TBR) to hold 1000 trees and
calculating a consensus on each repetition. Frequency
values (> 65%) were plotted onto the consensus of the
MPTs.
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I. GROENINCKX ET AL.
RESULTS
TAXONOMIC
TREATMENT OF NOVELTIES
Amphistemon Groeninckx, gen. nov. (Fig. 1)
Type species: Amphistemon humbertii Groeninckx,
sp. nov.
Number of species: 2
Fide analysis molecularis genus novum generi
Astiellae gregis Hedyotis-Oldenlandiae affine, in hac
grege singulare propter stamina in corollae tubo ad
altitudines duas distinctas inserta, stamina inferiora
filamentis antherisque brevioribus, stamina superiora
illis longioribus.
According to molecular analysis, a new genus allied
to the genus Astiella of the species-group Hedyotis–
Oldenlandia, unique in this species-group because of
the stamens inserted at two distinct levels in the
corolla-tube, the lower stamens with filaments and
anthers shorter than those of the upper stamens.
Erect perennial herb or subshrub. Leaves sessile,
linear, narrowly elliptic to elliptic, somewhat fleshy,
with secondary veins indistinct. Stipules fimbriate.
Inflorescences terminal or pseudo-axillary (initially
terminal but pushed aside during anthesis by the
developing shoot in one of the axils, making them
axillary), simple or compound dichasia, three- to
many-flowered. Flowers pedicellate, heterostylous;
calyx tube reduced; calyx lobes narrowly triangular to
triangular; corolla tube cylindrical to funnel-shaped;
corolla lobes elliptic, broadly elliptic to broadly ovate;
stamens dimorphic, two lower ones smaller and
always included, inserted in the upper half of the
corolla tube in brevistylous flowers, inserted in the
lower half of the corolla tube in longistylous flowers,
two upper ones mostly larger, inserted near the base
of the corolla lobes and exserted in brevistylous
flowers, inserted in the middle or lower half of the
corolla tube and included in longistylous flowers;
anthers narrowly ellipsoid to ellipsoid, with mucronate apex; pollen tricolporate, bireticulate; ovary
obovate or transversely broadly obovate, bilocular;
placenta attached near the middle of the septum,
stalked, globose, bearing numerous ovules; style
included in brevistylous flowers, exserted in longistylous flowers; stigma bilobed, pubescent; nectary disc
bipartite. Capsules broadly obovate to transversely
broadly obovate; dehiscence loculicidal, later on septicidal in the apex. Seeds numerous, elliptic, ovoid or
broadly ovoid in outline, brown or dark brown; wing
absent or reduced; seed-coat surface reticulate, sometimes with undulating radial cell walls, smooth or
with rugulose microsculpturing.
Etymology: The genus name is based on the Greek
‘amphi-’ (= double or of two kinds) and ‘stemon’
(= stamen) referring to the dimorphic stamen position
characteristic for the genus.
Habitat: South-western dry spiny forest–thicket and
coastal bushland (Moat & Smith, 2007).
Distribution: South-west and west Madagascar, Province Toliara: Region Menabe (District Morondava);
Region Atsimo-Andrefana (District Betioky, Toliara I,
Toliara II, Sakaraha).
AMPHISTEMON HUMBERTII GROENINCKX, SP.
(FIGS 1A–E, 2, 3A–D, 4A–C AND 5A)
NOV.
Oldenlandia humbertii Homolle, nomen in herb.
Type specimen: La Table, Toliara, De Block, Dessein,
Groeninckx and Rakotonasolo 2294 (Holotype: BR.
Isotypes: MO, P, TAN).
Species habitu fruticosa, inflorescentiis paucifloris
et seminum testa in alam irregulariter expansa ab
altera hujus generis specie bene distincta.
A species of shrubby habit, well distinct from the
other species [singular] of this genus in its fewflowered inflorescences and the seed-coat irregularly
extended into a wing.
Much-branched subshrub with main branches
erect, up to 0.5 m tall; stems quadrangular, brownish
when young, greyish–brown in older stages, covered
with hairs when young, glabrescent in older stages.
Leaves decussate, sessile, fused with the stipule base
forming a sheath around the stem, somewhat fleshy;
leaf blades narrowly elliptic to elliptic, 2.2–22.5 (–39)
mm long, 1.0–4.1 mm wide, mucronate at the apex,
slightly narrowed at the base, glabrous on both surfaces or with sparse short hairs above or on both
surfaces; leaf margins revolute, minutely scabrid to
pubescent; mid-vein prominent underneath, pubescent above, glabrous to pubescent below; secondary
veins indistinct. Stipules fimbriate, persistent, becoming somewhat papery with age; stipule base 0.7–
0.9 mm long, pubescent; fimbriae 0.3–2.5 mm long,
shortly pubescent on the margins, not colleter-tipped.
Inflorescences terminal or pseudo-axillary, simple or
compound dichasia, three- to many-flowered. Flowers
heterostylous; pedicels 0.5–12.0 mm long, glabrous.
Calyx green; tube reduced; lobes triangular, 0.8–
1.9 mm long, 0.4–1.1 mm wide, glabrous or pubescent,
minutely scabrid on margins. Corolla white with vertical purple lines; tube cylindrical to funnel-shaped,
2.5–4.9 mm long, 0.9–1.8 mm wide at base, 1.8–
3.2 mm wide at throat, glabrous or with sparse hairs
outside, pubescent at the corolla throat inside; lobes
elliptic, 2.2–4.2 mm long, 0.8–1.4 mm wide, glabrous
or with sparse hairs outside, papillate to pubescent
inside. Stamens dimorphic, two lower ones smaller
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
TWO NEW RUBIACEAE GENERA ENDEMIC TO MADAGASCAR
451
Figure 1. Amphistemon humbertii (A–E) and Amphistemon rakotonasolianus (F–I). A, habit. B, brevistylous flower. C,
inflorescence with longistylous flowers. D, longistylous flower, note purple lines on the corolla tube. E, brevistylous flower,
note the dimorphic position of the stamens. F, habit. G, longistylous flower. H, brevistylous flower, note the dimorphic
position of the stamens. I, lateral view of longistylous flower. Photographs by Steven Dessein.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
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I. GROENINCKX ET AL.
Figure 2. Amphistemon humbertii. A, habit. B, brevistylous flower. C, ovary dissected to show placentation in each locule.
D, open longistylous flower. E, open brevistylous flower. F, capsule. G, capsule rotated to display loculicidal dehiscence.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
TWO NEW RUBIACEAE GENERA ENDEMIC TO MADAGASCAR
453
Figure 3. Scanning electron microscopy (SEM) micrographs of pollen of Amphistemon humbertii (A–D), Amphistemon
rakotonasolianus (E–H) and Thamnoldenlandia ambovombensis (I–L). A, polar view of tricolporate brevistylous pollen. B,
detail of apocolpium of brevistylous pollen. C, equatorial view of brevistylous pollen. D, detail of apocolpium of longistylous
pollen. E, polar view of tricolporate brevistylous pollen. Note the pollen buds (intine protrusions) in the apertural regions.
F, detail of apocolpium of brevistylous pollen. G, equatorial view of brevistylous pollen. H, detail of mesocolpium of
brevistylous pollen. I, polar view of tricolporate pollen. J, detail of apocolpium. K, equatorial view. L, detail of
mesocolpium. Pollen (A)–(D) and (I)–(L) were acetolysed following the method of Reitsma (1969). Pollen (E)–(H) were not
acetolysed, but treated with dimethoxymethane following the method of Halbritter (1998).
and always included, inserted in the upper half of the
corolla tube in brevistylous flowers, inserted in the
lower half of the corolla tube in longistylous flowers,
two upper ones mostly larger, inserted near the base
of the corolla lobes and exserted for 1–1.5 mm in
brevistylous flowers, inserted in the middle of the
corolla tube and included in longistylous flowers;
anthers narrowly ellipsoid to ellipsoid, with mucr-
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I. GROENINCKX ET AL.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
Figure 4. Scanning electron microscopy (SEM) micrographs of seeds of Amphistemon humbertii (A–C), Amphistemon rakotonasolianus (D–F) and Thamnoldenlandia ambovombensis (G–I). A, ventral view of seed, note hilum in the middle. B, dorsal view of seed, note narrow seed wing. C, detail of reticulate seed-coat
surface. D, lateral view of seed, note hilum above. E, ventral view of seed, note hilum in the middle. F, detail of reticulate seed-coat surface with undulating radial
cell walls. G, dorsal view of seed, note seed wing. H, ventral view of seed, note hilum in the middle. I, detail of reticulate seed-coat surface.
TWO NEW RUBIACEAE GENERA ENDEMIC TO MADAGASCAR
455
Figure 5. Distribution map of Amphistemon humbertii (A), Amphistemon rakotonasolianus (B) and Thamnoldenlandia
ambovombensis (C).
onate apex, white; upper pair of anthers 1.6–1.8 mm
long in brevistylous flowers, 1.0–1.2 mm long in longistylous flowers; lower pair of anthers c. 1.2 mm long
in brevistylous flowers, 0.8–1.0 mm long in longistylous flowers; filaments 1.5–2.0 mm long in brevistylous flowers, 0.2–0.5 mm long in longistylous flowers.
Pollen tricolporate, oblate spheroidal, sometimes
prolate spheroidal in both brevistylous and longistylous flowers; E 26–30 mm in brevistylous and longistylous flowers; P 25–29 mm in brevistylous and
longistylous flowers; ectocolpi long; endoaperture
endocingulum; tectum in brevistylous flowers microornate with granules on the muri, in longistylous
flowers microreticulate with granules in the lumina
(bireticulate). Ovary obovate, 0.6–1.6 mm long, 0.4–
1.6 mm wide, green, glabrous or pubescent; placenta
attached near the middle of the septum, stalked,
globose, bearing numerous ovules; style 2.7–3.0 mm
long and included in brevistylous flowers, 6.5–9.0 mm
long and exserted for c. 3 mm in longistylous flowers,
white; stigma bilobed, pubescent; stigma lobes 0.6–
1.2 mm long in brevistylous flowers, 1.0–1.5 mm long
in longistylous flowers; nectary disc bipartite. Capsules broadly obovate, 1.9–3.0 mm long, 2.1–3.0 mm
wide, crowned with the persistent calyx lobes, glabrous or with hairs; dehiscence loculicidal, later on
septicidal at the apex. Seeds elliptic, ovate or broadly
ovate in outline, 0.5–0.8 mm long, 0.40–0.65 mm
wide, dark brown; wing present as narrow, irregular
extension of the testa around the seed edge; seed-coat
surface reticulate, with rugulose micro-sculpturing.
Etymology: Amphistemon humbertii is named after H.
Humbert, one of the first collectors of the species.
Habitat: South-western dry spiny forest–thicket:
xerophyllous scrubland, on calcareous substrates;
2–740 m.
Distribution: South-west Madagascar, Province
Toliara: Region Atsimo-Andrefana (District Betioky,
Toliara I, Toliara II, Sakaraha).
Preliminary conservation assessment: The extent of
occurrence equals 6997.36 km2 and the area of occupancy equals 99.86 km2 (cell size set at 3.16 km).
Despite the restricted EOO and AOO, falling within
the IUCN threshold of Vulnerable and Endangered,
respectively, we consider the species as not threatened at present. Amphistemon humbertii is rather
common locally and large areas of undisturbed
similar vegetation remain in the distribution area of
the species.
Specimens investigated: MADAGASCAR PROVINCE
TOLIARA: REGION ATSIMO-ANDREFANA: DISTRICT
BETIOKY: Vallée de l’Onilahy près de Tongobory,
vallon d’Andranolahy, forêt tropophile et bush xérophile sur rocailles calcaires, 50–200 m, 5 February
1947, Humbert 20149 (BR, MO, P). DISTRICT
TOLIARA I: La Table, Toliara, January 1963, Chauvet
389 (BR, K, MO, P); La Table, 15 km from Toliara
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I. GROENINCKX ET AL.
on RN7, 4 January 1999, De Block, Leyman, Dessein,
Rakotonasolo and Randriamboavonjy 541 (BR, K,
MO, P, TAN); La Table, Toliara, 94 m, 2 February
2007, De Block, Dessein, Groeninckx and Rakotonasolo 2294 (BR, MO, P, TAN); La Table, Tuléar, s.d.,
Dequaire 27325 (P, TAN); Pied de la Table, Tuléar,
sol calcaire, s.d., Dequaire 27557 (BR, P, TAN); La
Table, Toliara, s.d., Dequaire 27582 (P, TAN); Colline
de La Table près de Tuléar, bush xérophile sur
rocailles calcaires, 100–140 m, March 1934, Humbert
14404 (MO, P). DISTRICT TOLIARA II: Route des 7
lacs, au nord de Tuléar vers Ambohimahavelona, 6
February 2001, Allorge and Rakotozafy 2609 (P);
Miary (Tuléar), bush sur calcaire, November 1956,
Bosser 10411 (P); Tuléar (route de St. Augustin par
la côte), bush xérophile sur calcaire, Bosser 14022
(TAN); 8–16 km east of Tulear, on road to Tananarive, forested slopes, 50 m, 7 February 1975, Croat
30992 (MO, P, TAN); Vallée de Fiherenana à
15–25 km en amont de Tuléar, bush xérophile,
coteaux calcaires de la rive droite, 200 m, March
1934, Humbert 14375 (P); Environs de Tuléar, delta
de Fiherenana, 2–10 m, 14–26 September 1924,
Humbert and Perrier de la Bâthie 2505 (BR, K, MO,
P); Tuléar, 1955, Pernet 86 (TAN). DISTRICT
SAKARAHA: Beraketa, Table de la Sakondry, 20 April
1922, Poisson 488 (P); 35 km east of Sakaraha on
route 7 East of Tulear, edge of road, prairie, 740 m,
4 February 1975, Croat 30644 (MO, TAN); Sud environs de Tuléar, km 30 route de Sakaraha, 5 February 1957, Descoings 2298 (P, TAN). LOCALITY
UNKNOWN: s.d., Homolle 13 (P).
AMPHISTEMON RAKOTONASOLIANUS GROENINCKX,
NOV. (FIGS 1F–I, 3E–H, 4D–F, 5B, 6)
SP.
Type specimen: RN35, c. 22 km from Morondava on
road to Tana, site ‘Dunes des Belges’, in shadow of
shrubs, white sand dune, Groeninckx, De Block,
Dessein and Rakotonasolo 147 (Holotype: BR. Isotypes: K, MO, P, TAN).
Herba perennis cum inflorescentiis late ramosis
multiflorisque et seminibus non alatis ab altera hujus
generis specie bene distincta.
A perennial herb, well distinct from the other
species [singular] of this genus in its broadly
branched and many-flowered inflorescences and
unwinged seeds.
Erect perennial herb, slender, c. 30 cm tall; stems
green with reddish–brown spots on upper surface,
rounded in cross section, glabrous, with swollen nodes;
well-developed tap root up to more than 40 cm long.
Leaves sessile, fused with the stipule base forming a
sheath around the stem; leaf blades linear, 4–34 mm
long, 0.3–0.7 mm wide, rounded in cross section, acute
at the apex, slightly narrowed at the base, green with
reddish–brown spots above, glabrous except for midvein above; leaf margins indistinct; mid-vein prominent below, sparsely pubescent above, glabrous below;
secondary veins indistinct. Stipules fimbriate; stipule
base reduced, 0.3 mm long, glabrous; fimbriae up to
0.3 mm long, glabrous, not colleter-tipped. Inflorescences terminal, compound dichasia, many-flowered.
Flowers heterostylous; pedicels 3.5–8.5 mm long, glabrous. Calyx tube reduced, green; lobes narrowly triangular to triangular, 0.2–0.4 mm long, 0.1–0.2 mm
wide, reddish–brown, glabrous. Corolla white in upper
half, greenish below, with purple tint inside; tube
funnel-shaped, 3.0–4.2 mm long, 0.6–1.0 mm wide at
base, 1.0–2.4 mm wide at throat, glabrous or with
sparse papillae or short hairs in the corolla throat;
lobes broadly elliptic to broadly ovate, 2.0–2.5 mm
long, 1.3–1.7 mm wide, glabrous outside, papillate
inside. Stamens dimorphic, two lower ones always
included, inserted in the upper half of the corolla tube
in brevistylous flowers, inserted in the lower half of
the corolla tube in longistylous flowers, two upper
ones mostly larger, inserted near the base of the
corolla lobes and exserted for 1.0–1.3 mm in brevistylous flowers, inserted in the lower half of the corolla
tube and included in longistylous flowers; anthers
ellipsoid, 0.7–0.9 mm long; filaments 0.3–0.8 mm long.
Pollen tricolporate, oblate spheroidal in brevistylous
flowers, prolate spheroidal to oblate spheroidal in
longistylous flowers; E 18–19 mm in brevistylous
flowers, 13–15 mm in longistylous flowers; P 17–19 mm
in brevistylous flowers, 13–15 mm in longistylous
flowers; ectocolpi long; endocolpi with acute endings;
tectum bireticulate, more or less identical in brevistylous and longistylous flowers; suprareticulum microreticulate to reticulate, smooth; infrareticulum
microreticulate, granulate to spinulate, less developed
in longistylous flowers. Ovary transversely broadly
obovate, 0.4–0.7 mm long, 0.5–0.8 mm wide, glabrous;
placenta attached near the middle of the septum,
stalked, globose, bearing numerous ovules; style 1.5–
2.0 mm long and included in brevistylous flowers, c.
5 mm long and exserted for 1.0–1.5 mm in longistylous flowers, white, glabrous; stigma bilobed; stigma
lobes with short hairs; nectary disc bipartite. Capsules
broadly obovate to transversely broadly obovate, 1.3–
2.1 mm long, 1.6–2.2 mm wide, crowned with the persistent calyx lobes, glabrous; dehiscence loculicidal,
later on septicidal at the apex. Seeds numerous, elliptic in outline, 0.4–0.6 mm long, 0.3–0.4 mm high, 0.3–
0.4 mm wide, brown; wing absent; seed-coat surface
reticulate, with undulating radial cell walls.
Etymology: This species is dedicated to Dr F. Rakotonasolo, who accompanied us on our field trip in Madagascar (January–February 2007) and who was the
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
TWO NEW RUBIACEAE GENERA ENDEMIC TO MADAGASCAR
457
Figure 6. Amphistemon rakotonasolianus. A, habit. B, brevistylous flower. C, detail of corolla lobe nervature. D, ovary
dissected to show placentation in each locule. E, open longistylous flower. F, open brevistylous flower. G, capsule. H,
capsule rotated to display loculicidal dehiscence.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
458
I. GROENINCKX ET AL.
first to spot this species growing in the white sand
dunes of ‘Dunes des Belges’ close to Morondava.
Habitat: South-western coastal bushland (Moat &
Smith, 2007): white sand dunes, in the shadow of
shrubs; 19 m.
Distribution: West Madagascar, Province Toliara:
Region Menabe (District Morondava).
Preliminary conservation assessment: Known from
three collections, only one with a locality. Grows on
sand dunes that until now received little attention
from collectors and might therefore be undercollected. However, at the locality we collected
Amphistemon rakotonasolianus (Groeninckx et al.
147); the species was not abundant and was only
found in one spot. Given its apparent rarity and
following the recommendation of Callmander, Schatz
& Lowry (2005) to avoid the Data Deficient category,
we consider the species as Vulnerable (VU) based on
its restricted area of occupancy (D2).
Specimens investigated: MADAGASCAR. PROVINCE
TOLIARA: REGION MENABE: DISTRICT MORONDAVA:
RN35, c. 22 km from Morondava on road to Tana, site
‘Dunes des Belges’, in shadow of shrubs, white sand
dune, 19 m, 24 January 2007, Groeninckx, De Block,
Dessein and Rakotonasolo 147 (BR, K, MO, P, TAN).
LOCALITY UNKNOWN: May 1955, Descoings 830 (P,
TAN); Descoings 781 (P, TAN).
THAMNOLDENLANDIA GROENINCKX,
(FIG. 7)
Type species: Thamnoldenlandia
Groeninckx, sp. nov.
GEN. NOV.
ambovombensis
Number of species: 1
Genus novum frutice parvo ostensum, teste analysis molecularis Amphistemoni soror, sed ab illo genere
staminibus omnibus in corollae tubo ad eandem altitudinem insertis differt.
A new genus represented by a small shrub, on the
evidence of molecular analysis sister to Amphistemon,
but differing from that genus in all the stamens being
inserted at the same level in the corolla tube.
Shrub. Leaves linear to narrowly elliptic, rarely
elliptic, somewhat fleshy. Stipules fimbriate. Inflorescences terminal or pseudo-axillary on lateral
branchlets, one- to two-flowered. Flowers pedicellate,
heterostylous; calyx tube reduced; calyx lobes narrowly triangular to triangular; corolla tube funnelshaped; corolla lobes elliptic to ovate; stamens
completely or almost completely included in longistylous flowers, exserted in brevistylous flowers; anthers
narrowly elliptic; pollen tricolporate, bireticulate;
ovary obovate; placenta attached near the middle of
the septum, stalked, globose, bearing numerous
ovules; style included in brevistylous flowers,
excluded in longistylous flowers; stigma bilobed, papillose; nectary disc bilobed. Capsules broadly obovate
to transversely broadly obovate, crowned with the
persistent calyx lobes; dehiscence loculicidal, later on
septicidal in the apex. Seeds numerous, elliptic, ovate
to broadly ovate in outline, winged, with reticulate
seed-coat surface, black.
Etymology: The genus name combines the Greek word
‘thamn’ (= shrub) and the genus name Oldenlandia,
referring to the shrubby habit of the genus.
Habitat: South-western dry spiny forest–thicket
(Moat & Smith, 2007).
Distribution: South Madagascar, Province Toliara:
Region Androy (District Ambovombe); Region Anosy
(District Amboasary Atsimo).
THAMNOLDENLANDIA AMBOVOMBENSIS GROENINCKX,
SP. NOV. (FIGS 3I–L, 4G–I, 5C, 7, 8)
Type specimen: 24 km from Ambovombe on road to Fort
Dauphin, De Block, Dessein, Groeninckx and Rakotonasolo 2328 (Holotype: BR. Isotypes: K, MO, P, TAN).
Hujus generis species unica in turma HedyotiOldenlandia singularis propter seminum testae in
alam extensae.
The only species of this genus, unique in the
species-group Hedyotis–Oldenlandia because of the
seed-coat [being] extended into a wing.
Much-branched shrub up to 1.5 m tall; stems
woody, greyish–brown, densely covered with short
stiff hairs, glabrenate in older stages. Leaves decussate, sessile, fused with the stipule base forming a
sheath around the stem, somewhat fleshy; leaf blades
linear to narrowly elliptic, rarely elliptic, 2.0–
21.6 mm long, 1.4–4.0 mm wide, mucronate at the
apex, gradually narrowed towards the base, green
above, light green below, glabrous or sparsely scabrous particularly towards the margins above, glabrous below except for mid-vein; leaf margins slightly
revolute when fresh, strongly revolute in dry state,
often lighter coloured, minutely scabrid; mid-vein
prominent underneath, scabrid, rarely glabrous; secondary veins indistinct. Stipules fimbriate, persistent,
becoming somewhat papery with age; stipule base
0.4–1.5 mm long, with sparse short or long hairs;
fimbriae up to 1.5 mm long but often much shorter,
colleter-tipped. Inflorescences terminal or pseudoaxillary on lateral branchlets, one- to two-flowered.
Flowers heterostylous; pedicels 2–12 mm long, green,
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TWO NEW RUBIACEAE GENERA ENDEMIC TO MADAGASCAR
459
Figure 7. Thamnoldenlandia ambovombensis. A–C, longistylous flower. D–E, capsule. Photographs by Steven Dessein
(D–E) and Inge Groeninckx (A–C).
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
460
I. GROENINCKX ET AL.
Figure 8. Thamnoldenlandia ambovombensis. A, habit. B, brevistylous flower. C, open longistylous flower. D, open
brevistylous flower. E, ovary dissected to show placentation in each locule. F, capsule. G, capsule rotated to display
loculicidal dehiscence.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
TWO NEW RUBIACEAE GENERA ENDEMIC TO MADAGASCAR
glabrous or with sparse hairs. Calyx green; tube
reduced; lobes narrowly triangular to triangular, 0.9–
3.5 mm long, 0.4–1.3 mm wide, glabrous or with
sparse hairs, with short hairs on margins. Corolla
white; tube funnel-shaped, 3.8–5.2 mm long in brevistylous flowers, 2.2–3.5 mm long in longistylous
flowers, 0.6–1.5 mm wide at base, 1.0–2.5 mm wide at
throat, glabrous or with sparse hairs outside, pubescent inside particularly at the corolla throat; lobes
elliptic to ovate, 2.2–5.5 mm long, 0.8–1.6 mm wide,
glabrous or with sparse hairs outside, glabrous to
papillate inside. Stamens inserted just below the
throat of the corolla tube and exserted for 1.2–1.6 mm
in brevistylous flowers, inserted in the lower half of
the corolla tube and completely included in longistylous flowers or only with the apex protruding from the
corolla tube; anthers narrowly elliptic, 1.0–1.8 mm
long, 0.2–0.5 mm wide; filaments dorsimedifixed, 0.7–
1.2 mm long. Pollen tricolporate, prolate spheroidal to
prolate, mostly subprolate; E 20.5–23.5 mm; P
23–29 mm; ectocolpi long; endocolpi with fish-tail
endings; tectum bireticulate; suprareticulum microreticulate to reticulate, smooth; infrareticulum
reduced, present as an extension of the muri of the
suprareticulum, covered with granules. Ovary
obovate, 0.8–1.4 mm long, 0.8–1.8 mm wide, green,
glabrous or sparsely beset with hairs; placenta
attached near the middle of the septum, stalked,
globose, bearing numerous ovules; style 2.2–3.5 mm
long in brevistylous flowers, 5.2–8.5 mm long in longistylous flowers; stigma bilobed; stigma lobes 0.5–
1.5 mm long, papillose; nectary disc bipartite.
Capsules broadly obovate to transversely broadly
obovate, 2.0–4.5 mm long, 1.8–5.5 mm wide, crowned
with the persistent calyx lobes, glabrous; dehiscence
loculicidal, later on septicidal in the apex. Seeds
numerous, elliptic, ovate to broadly ovate in outline,
1.0–1.5 mm wide, 0.8–0.9 mm long, black; wing
present; seed-coat surface reticulate.
Etymology: The specific epithet ambovombensis refers
to the location where the species was collected,
Ambovombe.
Habitat: South-western dry spiny forest–thicket
(Moat & Smith, 2007): on orange–brown sand, calcareous hills; 150–190 m.
Distribution: South Madagascar, Province Toliara:
Region Androy (District Ambovombe); Region Anosy
(District Amboasary Atsimo).
Preliminary conservation assessment: Only known
from six collections close to Ambovombe and
restricted to calcareous hills covered by dry, spiny
forest–thicket. The extent of occurrence is estimated
461
at 249.39 km2 and the area of occupancy (with cell
size set at 3.16 km) at 99.86 km2. Given the continuing decline of natural habitats and the small number
of locations, the species can be considered Endangered under B1 (a,b) and B2 (a,b). Probably a local
endemic; presumably threatened, as its known distribution range falls outside protected areas.
Specimens investigated: MADAGASCAR. PROVINCE
TOLIARA: REGION ANDROY: DISTRICT AMBOVOMBE:
24 km from Ambovombe on road to Fort Dauphin,
190 m, 8 February 2007, De Block, Dessein, Groeninckx and Rakotonasolo 2328 (BR, K, MO, P, TAN);
hill between Ambovombe and Amboasary, dry forest,
limestone, 5 April 2010, Groeninckx, De Block and
Rakotonasolo 330 (BR, K, MO, P, TAN); Ambovombe,
endroits ensoleillés, calcaire, 19 August 1924, Decary
2989 (P); Ampasimpolaka, à l’est d’Ambovombe, sur
les calcaires, 29 June 1931, Decary 9065 (P). REGION
ANOSY: DISTRICT AMBOASARY ATSIMO: Near
Amboasary, due east of Ambovombe, seasonally dry,
spiny forest, orange–brown sand, 150 m, 19 February
2001, Davis and Rakotonasolo 2730 (BR, K, MO, P,
TAN, TEF); Fort Dauphin, hill past Amboasary, dry
forest, limestone, 28 March 2010, De Block, Groeninckx and Rakotonasolo 2386 (BR, K, MO, P, TAN).
MOLECULAR
STUDY
Sequence data from the aligned atpB-rbcL, petD,
rps16 and trnL-trnF regions were first analysed separately (results not presented). Characteristics of each
data matrix and the corresponding tree statistics are
presented in Table 2. Individual analyses were topologically congruent. Therefore, only the strict consensus from the combined analysis is presented (Fig. 9).
The resulting topology is congruent with the ones
from previously published studies within Spermacoceae (Kårehed et al., 2008; Groeninckx et al., 2009a,
b). The genus Amphistemon is monophyletic (BS = 99,
JS = 99) and is sister to Thamnoldenlandia (BS = 100,
JS = 100). This strongly supported clade shares a
common ancestor with Astiella delicatula (BS = 89,
JS = 93). This Madagascan clade is sister to an American clade including Arcytophyllum Willd. ex Schult. &
Schult.f., Oldenlandia microtheca (Cham. & Schltdl.)
DC., Houstonia L. and Stenaria (Raf.) Terrell
(BS = 78, JS = 78). The remaining Madagascan
endemics in our sampling, Lathraeocarpa and Gomphocalyx, form a strongly supported clade with the
Afro-Madagascan genus Phylohydrax (BS = 100,
JS = 100). This Madagascan clade shares a common
ancestor with the African mainland taxa Manostachya ternifolia E.S.Martins and Oldenlandia rosulata K.Schum. (BS = 87, JS = 91). Widespread taxa
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
462
I. GROENINCKX ET AL.
Table 2. Characteristics of each data matrix and the corresponding tree statistics
atpB-rbcL
petD
rps16
trnL-trnF
combined
No. of
taxa
No. of
characters
No. of PI
characters
No. of
PI indels
No. of
MPT
MPT
length
CI
RI
104
103
99
101
115
1357
1870
699
1074
5000
152
296
153
150
751
34
65
23
36
158
5470
6321
6
280
2250
449
963
482
432
2426
0.54
0.51
0.55
0.61
0.52
0.82
0.80
0.81
0.87
0.80
CI, Consistency Index (Kluge & Farris, 1969); MPT, most parsimonious tree(s); PI, potentially informative; RI, Retention
Index (Farris, 1989).
occurring in Madagascar and other tropical regions
are scattered over the tree (indicated in bold type).
DISCUSSION
GENERIC
DELIMITATION PROBLEMS
WITHIN
SPERMACOCEAE
Within Spermacoceae, and especially within the
Hedyotis–Oldenlandia complex, subdivision into
genera is problematic. The Hedyotis–Oldenlandia
complex, including most species of the former tribe
Hedyotideae, is one of the most troublesome groups
of the family Rubiaceae. The interrelationships and
taxonomic status of Hedyotis L., Oldenlandia L. and
their satellite genera (e.g. Amphiasma Bremek.,
Arcytophyllum, Houstonia, Kohautia Cham. &
Schltdl. and Kadua Cham. & Schltdl.) have been
controversial for decades. The central question has
been whether most species of the complex should be
lumped into Hedyotis (advocated by Merrill &
Metcalf, 1946; Wagner, Herbst & Sohmer, 1989;
Fosberg & Sachet, 1991; Dutta & Deb, 2004) or if
many small genera should be recognized in addition
to a narrow circumscription of Hedyotis (supported
for the African taxa by Bremekamp, 1952, for the
neotropical taxa by Terrell et al., 1986 and Terrell,
1991, 2001a, b, c and for the Asian taxa by Terrell &
Robinson, 2003).
Generic delimitations within the Hedyotis–
Oldenlandia complex are complicated by the strong
habitual similarity between the representatives,
which makes it difficult to find morphological characters to define genera. Several attempts have been
made to split the complex in distinct genera. Terrell
initiated the generic dissection for the North and
Central American species of the complex by revising
Hedyotis, Oldenlandia and Houstonia for this area and
by establishing Oldenlandiopsis Terrell & W.H.Lewis
(Terrell & Lewis, 1990), Stenaria (Terrell, 2001a),
Stenotis Terrell (Terrell, 2001b) and Carterella Terrell
(Terrell, 1987). Studies of Terrell indicated that seed
characters provide the most important clues to understanding the phylogenetic relationships among species
of the Hedyotis–Oldenlandia complex. Seed morphology seems to be useful for the delimitation of genera,
especially when combined with pollen morphology,
chromosome number and geographical distribution.
Bremekamp (1952), however, revised the African
species of the complex and recognized many segregate
genera (Agathisanthemum Klotzsch, Amphiasma,
Conostomium (Stapf) Cufod., Dibrachionostylus
Bremek., Diotocranus Bremek., Eionitis Bremek.,
Exallage Bremek., Hedythyrsus Bremek., Kohautia,
Lelya Bremek., Manostachya Bremek., Metabolos
Blume, Nesohedyotis (Hook.f.) Bremek., Oldenlandia s.s., Pentanopsis Rendle, Pentodon Hochst.,
Sacosperma G.Taylor, Stephanococcus Bremek. and
Thecorchus Bremek.) based mainly on fruit characters
(in particular fruit dehiscence), the position of the
inflorescence and the form of the stipules.
In the absence of molecular data, the delimitation
of genera is inevitably the result of a somewhat
subjective decision of the taxonomic rank that should
be attributed to groups based on morphological or
anatomical differences observed between species.
When revising the representatives of the complex for
Madagascar, we arrived at a similar pattern of difficult to delimit groups, comprising a large number of
morphologically ill-defined species and highly characteristic taxa. Contrary to authors of the previous
century, we could use molecular evidence to find phylogenetic patterns. Our molecular study reveals surprising relationships that had not been suggested
before based on morphology alone. By placing our
morphological observations into this molecular phylogenetic framework, we are able to recognize the two
new genera, Amphistemon and Thamnoldenlandia,
with more certainty. In the following paragraphs, we
discuss the results of our integrated study in more
detail.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
TWO NEW RUBIACEAE GENERA ENDEMIC TO MADAGASCAR
463
Figure 9. Strict consensus tree based on atpB-rbcL, petD, rps16 and trnL-trnF sequences with bootstrap (left) and
jackknife (right) support values (> 65%) indicated above branches. Madagascan clades 1 and 2 are highlighted in grey.
Widespread taxa also occurring in Madagascar are in bold. Taxa characterized by both a woody habit and winged seeds
are indicated with an asterisk. Outgroup = Batopedina pulvinellata Robbr., Carphalea madagascariensis Lam. and
Pentanisia parviflora Stapf ex Verdc.
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
464
I. GROENINCKX ET AL.
AMPHISTEMON
AND
THAMNOLDENLANDIA,
SPERMACOCEAE
TWO NEW
GENERA OF
Our molecular study demonstrates that Amphistemon
and Thamnoldenlandia belong to the Hedyotis–
Oldenlandia complex of tribe Spermacoceae. Molecular and morphological data support Amphistemon as
monophyletic. The insertion of the stamens at two
levels in the corolla tube is a synapomorphy for the
genus absent from other taxa in Spermacoceae. Within
Rubiaceae, dimorphism in anther position has only
been reported in two genera of tribe Paederieae DC.,
Aitchisonia Hemsl. ex Aitch. (Robbrecht, 1988) and
Paederia L. (Puff & Igersheim, 1991), and in Didymochlamys Hook.f., a genus of uncertain position (cf. plate
in Brown, 1901). The two species described within the
genus Amphistemon can easily be distinguished from
one another. Amphistemon humbertii is a subshrub
with winged seeds, whereas Amphistemon rakotonasolianus is a geoxylic plant with woody underground
organs, a woody base and wingless seeds.
The monospecific genus Thamnoldenlandia is a
medium-sized shrub with winged seeds. Species of the
Hedyotis–Oldenlandia complex are generally annual
or perennial herbs, occasionally plants with a woody
base or subshrubs. In Spermacoceae, the combination
of a woody habit and winged seeds is only found in
two distantly related genera, i.e. Hedythyrsus and
Bouvardia Salisb. (both taxa are indicated with an
asterisk on the molecular tree, Fig. 9) and in Amphistemon humbertii.
Thamnoldenlandia and Amphistemon were found
to be sister in the molecular study. An alternative
would therefore have been to recognize one genus for
the clade containing the three new Madagascan
species. However, the following section, discussing the
taxonomic position of Astiella, will provide arguments
for the recognition of two genera.
CLARIFICATION
OF THE TAXONOMIC POSITION OF
THE ENIGMATIC GENUS
ASTIELLA
Amphistemon and Thamnoldenlandia share a
common ancestor with the enigmatic genus Astiella.
Astiella was described by Jovet (1941) as a monospecific, herbaceous genus, endemic to Madagascar. The
only species, Astiella delicatula, has several peculiar
characters, which until now made it difficult to
discuss its relationships with other representatives of
Spermacoceae. Astiella delicatula is characterized by
having only two calyx lobes, uni-ovulate locules, distinctly beaked fruits with a conspicuous boat-shape
and pluri-aperturate pollen. Because of its peculiar
morphology and the fact that until now no molecular
data have been available for Astiella, the taxonomic
position of the genus has remained controversial.
Based on the fruit shape, Jovet (1941) suggested a
close relationship between Astiella and the AfroMadagascan genus Mitrasacmopsis Jovet. Both
genera are characterized by the presence of a prominent beak in the fruiting stage, which gives the whole
ovary a semi-inferior appearance (Groeninckx et al.,
2007). Jovet (1941) also proposed a close relationship
between Astiella and the Asian Anotis DC., now classified in the genus Neanotis W.H.Lewis (Lewis, 1966).
Besides a reduction in seed number and the presence
of seeds with a ventral groove, species of Neanotis
also have pluri-colporate pollen grains, as observed in
Astiella (Lewis, 1966).
Our molecular study does not support the suggested close relationship between Mitrasacmopsis and
Astiella. With no molecular sequence data available
for the genus Neanotis, it also remains premature to
hypothesize a close relationship with Astiella.
Molecular data are conclusive in placing Astiella delicatula as sister to Amphistemon and Thamnoldenlandia. The idea to merge the two new genera into
Astiella can be rejected when listing all morphological
differences. Table 3 summarizes the main similarities
and dissimilarities between the two novelties and
Astiella. No synapomorphy can be found to characterize the Madagascan clade 2. Furthermore, no
synapomorphy seems to exist for the clade of Amphistemon plus Thamnoldenlandia. Each taxon is characterized by a unique set of characters and is for this
reason best treated as a distinct genus. Amphistemon
differs from Astiella and Thamnoldenlandia in having
its anthers positioned at two levels in the corolla tube.
The dimorphic anther position is a synapomorphy for
the genus. Astiella, however, differs from its sister
taxa Amphistemon and Thamnoldenlandia in floral
organization (isostylous vs. heterostylous), number of
calyx lobes (two vs. four), number of ovules (one vs.
many), fruit shape (broadly triangular and distinctly
beaked vs. broadly ovate), seed morphology (presence
of a ventral groove vs. absence of a ventral groove)
and number of pollen apertures (five to six vs. three).
The character combination found in Astiella delicatula is unique within Spermacoceae. Thamnoldenlandia differs from Amphistemon and Astiella in being a
medium-sized shrub with distinctly winged seeds.
The genus shows a clear resemblance to its sister
Amphistemon, but lacks the dimorphic anther position. Merging Thamnoldenlandia into Amphistemon
would create a taxon for which no synapomorphy
exists. Therefore, we believe it is better to treat
Thamnoldenlandia as a separate genus.
ORIGIN
OF THE
MADAGASCAN
ENDEMICS
The present-day biota of Madagascar is largely comprised of the descendents of Cenozoic dispersers, pre-
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
TWO NEW RUBIACEAE GENERA ENDEMIC TO MADAGASCAR
465
Table 3. Morphological differences between Amphistemon humbertii, A. rakotonasolianus, Thamnoldenlandia ambovombensis and Astiella delicatula
A. humbertii
A. rakotonasolianus
T. ambovombensis
A. delicatula
Habit
Floral
organization
Subshrub
Heterostylous, anthers
inserted at two
levels; anthers and
style included/
excluded
Herb
Heterostylous, anthers
inserted at two
levels; anthers and
style included/
excluded
Shrub
Heterostylous, anthers
inserted at the same
level; anthers and
style included/
excluded
Calyx lobes
Ovary
Pollen apertures
Pollen exine
Four
Multi-ovulate
3-aperturate
Different in LF and
BF. Bireticulate
in LF; SR
microreticulate; IR
reduced, present as
granules in the
lumina of the SR.
Micro-ornate with
granules on the muri
in BF
Broadly obovate
Four
Multi-ovulate
3-aperturate
Identical in LF and
BF. Bireticulate; SR
microreticulate to
reticulate, smooth;
IR microreticulate,
granulate to
spinulate
Four
Multi-ovulate
3-aperturate
Identical in LF and BF.
Bireticulate; SR
microreticulate to
reticulate, smooth;
IR reduced, present
as an extension of
the muri of the SR,
with granules
Herb
Isostylous, anthers
inserted at the
same level;
anthers and style
included in the
lower half of the
corolla tube
Two
Uni-ovulate
5- to 6-aperturate
Bireticulate; SR
microreticulate to
reticulate, smooth;
IR perforate with
granules on the
muri
Broadly obovate to
transversely broadly
obovate
Absent
Absent
Broadly obovate to
transversely broadly
obovate
Clearly present
Absent
Fruit shape
Seed wing
Seed ventral
groove
Present but reduced
Absent
Transversely
broadly obovate
Absent
Present
BF, brevistylous flowers; IR, infrareticulum; LF, longistylous flowers; SR, suprareticulum.
dominantly of African origin (Yoder & Nowak, 2006).
For Begonia L. (Begoniaceae) (Plana et al., 2004), and
the genera of Rubiaceae Coffea (Maurin et al., 2007),
Gaertnera Lam. (Malcomber, 2002) and Tricalysia
(Tosh et al., 2009), a single dispersal event from
Africa, followed by island speciation, has been
inferred. Lavin et al. (2000) inferred that the Madagascan species of the genus Ormocarpum P.Beauv.
(Fabaceae) are the result of two dispersal events from
Africa and an investigation of Streptocarpus Lindl.
(Gesneriaceae) has shown multiple out-of-Africa colonization events for the Madagascan representatives of
that genus (Möller & Cronk, 2001).
Given that the first fossil record of Rubiaceae is
from the early Eocene (Roth & Dilcher, 1979;
Graham, 2009), long-distance dispersal is also the
most likely explanation for the origin of the family
on the island. The present study indicates that Spermacoceae has invaded Madagascar at least 12 times
since the Eocene (Fig. 9). The endemic Madagascan
species are the product of at least two colonization
events. One event corresponds to a clade containing
the endemic genera Lathraeocarpa and Gomphocalyx
and the Afro-Madagascan genus Phylohydrax (clade
1). A second Madagascan clade, including the
remaining endemics in our sampling, Thamnoldenlandia, Amphistemon and Astiella, corresponds to a
second colonization (clade 2). The Madagascan clade
1 is part of a clade of African mainland taxa, suggesting an African origin for the Madagascan endemics Lathraeocarpa and Gomphocalyx. The AfroMadagascan genus Phylohydrax, which also belongs
to clade 1, consists of two species that are both
included in our analyses. Phylohydrax madagascariensis (Willd. ex Roem. & Schult.) Puff is restricted
to the coast of Madagascar, whereas P. carnosa
(Hochst.) Puff is restricted to the east coast of continental Africa (Puff, 1986). The presence of the AfroMadagascan Phylohydrax in clade 1 suggests a
recolonization of the African mainland from Madagascar. The Madagascan clade 2 shares a common
ancestor with a clade including the neotropical genus
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
466
I. GROENINCKX ET AL.
Arcytophyllum, the Mexican Oldenlandia microtheca
(Cham. & Schltdl.) DC. and the North and Central
American
Houstonia
and
Stenaria.
This
Madagascan–American clade is sister to a clade
including both palaeotropical (mainly African mainland taxa) and neotropical taxa. The origin of the
Madagascan clade 2 needs clarification by a much
broader species sampling.
MORPHOLOGICAL DIVERSITY OF ENDEMIC
MADAGASCAN SPERMACOCEAE
In our study of the endemic Madagascan Spermacoceae, we observed a striking diversity in habitat. The
tribe is present in dry spiny forests (e.g. Thamnoldenlandia), xerophyllous scrublands (e.g. Amphistemon
humbertii), seasonally dry semi-deciduous forests
(e.g. Astiella), on sand dunes (e.g. Amphistemon rakotonasolianus and Lathraeocarpa) and on beaches
close to the sea (Phylohydrax madagascariensis).
Beside variation in habitat, we also observed considerable variation in morphology. In the following
paragraphs, we discuss some aspects of this morphological diversity of Spermacoceae on Madagascar.
First, we discuss the variety of growth forms
present on the island, with special focus on the
occurrence of island woodiness. Then, we discuss the
different forms of floral organization in relation to
outcrossing.
HABIT
DIVERSITY AND ISLAND WOODINESS
Species of Spermacoceae present on Madagascar
exhibit different growth forms. Some are prostrate or
upright, annual or perennial herbs (e.g. Astiella delicatula). Others are ‘woody’ herbs (i.e. geoxylic herbs)
with a woody base and/or woody underground parts
(e.g. Amphistemon rakotonasolianus and Gomphocalyx herniarioides Baker). The most striking examples
of island woodiness in Madagascan Rubiaceae are
Thamnoldenlandia ambovombensis (medium-sized
shrub), Amphistemon humbertii (subshrub) and Lathraeocarpa (subshrub). A wood anatomical study has
demonstrated that these woody species of Spermacoceae are secondarily woody, i.e. they are derived from
a herbaceous ancestor (Lens et al., 2009). Wood anatomical sections illustrate that Lathraeocarpa acicularis Bremek., Thamnoldenlandia ambovombensis
and Amphistemon humbertii have dense wood
because of thick-walled tracheids in the ground
tissue. Dense wood is hypothesized to withstand
stronger drought-induced negative pressures better
than low-density wood (Hacke et al., 2001). Not surprisingly, these three species are found in south-west
Madagascar, characterized by little rainfall and a long
dry season.
Woodiness is a prominent trait among island
endemics. Numerous island-inhabiting species of predominantly herbaceous plant groups are woody
shrubs or trees (Carlquist, 1974, 2009a, b; Böhle,
Hilger & Martin, 1996; Kim et al., 1996; Baldwin,
1997). Hypotheses as to why woodiness has evolved
frequently on islands (or in island-like conditions as
on mountain peaks) are numerous but as yet
untested.
FLORAL
ORGANIZATION AND OUTCROSSING
Madagascan species of Spermacoceae are either heterostylous or isostylous. Astiella delicatula has isostylous flowers with anthers and style both included in
the lower half of the corolla tube, with the stigma
lobes close to the anthers allowing self-pollination. In
contrast, Amphistemon, Thamnoldenlandia, Lathraeocarpa, Gomphocalyx and Phylohydrax are heterostylous. Heterostyly is a common feature in
Spermacoceae and Rubiaceae in general (Robbrecht,
1988). However, surveys of oceanic island floras have
shown that heterostyly is often absent in taxonomic
groups where it is otherwise common, e.g. in Hawaii
(Carlquist, 1974), New Zealand (Godley, 1979) and
the Galapagos Islands (McMullen, 1987). This
absence of heterostyly is attributable to the fact that
heterostylous species are self-incompatible and that
self-compatible species are more likely to establish
populations after long-distance dispersal as a result of
their ability to reproduce in the absence of pollinators
(Baker, 1955, 1967). The occurrence of heterostylous
Spermacoceae on Madagascar may thus be an
exception to Baker’s law for the importance of
self-compatibility for island colonization. Selfincompatibility may have either been maintained
during colonization (in this case, population foundation must have involved more than one selfincompatible colonist arriving on Madagascar) or
evolved subsequent to initial colonization.
Due to the insertion of its anthers at two levels in
the corolla tube, Amphistemon represents a different
kind of heterostyly than that present in the other
Madagascan endemic members of Spermacoceae. In
long-styled plants, stigmas are placed above two
whorls of stamens, whereas, in short-styled plants,
stigmas are placed below two whorls of stamens. This
modified heterostylous floral organization may represent one step in the evolutionary breakdown of
heterostyly to self-fertilization. Further reduction
of stigma–anther separation may eventually result
in self-fertilization. A breakdown of the selfincompatibility system permitting self-pollination has
been reported in several distylous species, e.g. in
Gaertnera vaginata Poir. (Rubiaceae) on La Réunion
(Pailler & Thompson, 1997).
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
TWO NEW RUBIACEAE GENERA ENDEMIC TO MADAGASCAR
ACKNOWLEDGEMENTS
We thank Marijke Meersman for the beautiful line
drawings. Research in Madagascar was facilitated by
the following Madagascan governmental institutions,
which provided permission to collect specimens in
protected areas: Association Nationale pour la Gestion
des Aires Protégées (ANGAP), Ministère des Eaux et
Forêts (MEF) and Parc Botanique et Zoologique de
Tsimbazaza (PBZT). We thank Dr P. Lowry, Head of
the Africa and Madagascar Department of Missouri
Botanical Garden, for the opportunity to perform fieldwork within the framework of MBG’s Madagascar
Research and Conservation Program. We also thank
the members of the MBG staff in Madagascar for their
hospitality and help. In particular, we are grateful to
Dr Franck Rakotonasolo (PBZT), who accompanied us
in the field. We also appreciate the comments of the
two anonymous reviewers, which highly improved
the text. This research was supported by grants from
the Fund for Scientific Research, Flanders (F.W.O.,
G.0205.05 and G.0268.04).
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APPENDIX
List of taxa used in the molecular phylogenetic analysis with voucher information (geographical origin,
collector, collector number, herbarium) and GenBank
accession numbers. Previously published sequences of
atpB-rbcL, rps16, trnL-trnF and petD are provided
with literature citations. New sequences are marked
in bold and underlined. Key to literature citations:
(1)
Andersson & Rova 1999; (2)Andersson et al. 2002;
(3)
Dessein et al. 2005; (4)Groeninckx et al. 2009a;
(5)
Kårehed et al. 2008; (6)Groeninckx et al. 2009b.
Agathisanthemum Klotzsch: A. bojeri Klotzsch,
Zambia, Dessein et al. 671 (BR), EU542917(4),
EU543018(4), EU543077(4), EU557678(5); A. globosum
(Hochst. ex A. Rich.) Klotzsch, Zambia, Dessein et al.
201 (BR), EU542918(4), EU543019(4), EU543078(4),
EU557679(5). Amphiasma Bremek. A. benguellense
(Hiern) Bremek., Angola, Kers 3350 (S), EU542919(4),
AF002753(1), EU543079(4), EU557680(5); A. luzuloides
(K. Schum.) Bremek., Zambia, Dessein et al. 1167
(BR),
EU542920(4),
EU543020(4),
EU543080(4),
(5)
EU557681 . Amphistemon Groeninckx ined. A.
humbertii Groeninckx ined., Madagascar, De Block
et al. 2294 (BR), GU475969, GU475977, GU47598,
GU475973; A. rakotonasolianus Groeninckx ined.,
Madagascar, Groeninckx et al. 147 (BR), GU475970,
GU475978, GU475982, GU475974. Arcytophyllum
Willd. ex Schult. & Schult.f. A. ciliolatum Standl.,
Ecuador, Ollgaard et al. 58395 (NY), AF333350(2),
AF333351(2); A. ericoides (Willd. ex Roem. & Schult.)
Standl., unknown, Edwin et al. 3624 (S), AF333352(2),
AF333353(2); A. muticum (Wedd.) Standl., Colombia,
Andersson et al. 2195 (GB), EU542921(4), AF002754(1),
EU543081(4), EU557682(5); A. rivetii Danguy &
Cherm., Ecuador, Harling & Andersson 22232 (GB),
EU542922(4), AF333362(2), AF333363(2); A. thymifolium (Ruiz & Pav.) Standl., Ecuador, Ståhl 4481 (GB),
EU542923(4), AF333366(2), EU543082(4), EU557683(5).
Astiella Jovet: A. delicatula Jovet, Madagascar, De
Block et al. 2173 (BR), GU475971, GU475979,
GU475983, GU475975. Bouvardia Salisb. B. glaberrima Engelm., cult., Forbes s.n. (S), EU542925(4),
EU543022(4), EU543084(4), EU557685(5); B. ternifolia
(Cav.) Schltdl., unknown, cult. at N.B.G.Belgium, Van
Caekenberghe 264 (BR), AF002758(1); Mexico, Spencer
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
470
I. GROENINCKX ET AL.
et al. 363 (NY), EU642537(4). Conostomium (Stapf)
Cufod. C. natalense (Hochst.) Bremek., South Africa,
Dahlstrand 1346 (GB), AF002760(1), EU543085(4),
EU557687(5); South Africa, Bremer et al. 4341 (UPS),
EU542927(4); C. quadrangulare (Rendle) Cufod.,
Ethiopia, Puff & Kelbessa 821222 (UPS), EU542928(4),
EU543024(4), EU543086(4), EU557688(5); C. zoutpansbergense (Bremek.) Bremek., South Africa, Bremer
et al. 4331 (UPS), EU542929(4), EU543087(4),
EU557689(5). Crusea Cham. & Schltdl. C. calocephala DC., Guatemala, Gustafsson et al. 215 (GB),
EU542930(4), EU543088(4), EU557690(5); C. megalocarpa (A. Gray) S. Watson, Mexico, Pringle 3852 (S),
EU542931(4), EU543025(4), EU543089(4), EU557691(5).
Dentella J.R. Forst & G. Forst. D. repens (L.) J.R.
Forst. & G. Forst., Australia, Andersson 2262 (GB),
EU542932(4), AF333370(2), EU543091(4), EU557693(5).
Dibrachionostylus Bremek. D. kaessneri (S.
Moore) Bremek., Kenya, Strid 2598 (GB),
EU542933(4), AF002761(1), EU557694(5). Diodia L. D.
aulacosperma K. Schum., Kenya, Luke 9029 (UPS),
EU542934(4), EU543026(4), EU543092(4), EU557695(5);
D. spicata Miq., French Guiana, Anderson et al.
1961 (GB), EU542935(4), EU543027(4), EU543093(4),
EU557696(5). Emmeorhiza Pohl ex Endl. E. umbellata (Spreng.) K. Schum., Trinidad, Hummel s.n.
(GB),
EU542936(4),
AY764289(3),
EU543094(4),
(5)
EU557697 . Ernodea Sw. E. littoralis Sw., Cuba,
Rova et al. 2286 (GB), EU542937(4), AF002763(1),
EU543095(4), EU557698(5). Galianthe Griseb. G. brasiliensis (Spreng.) E.L. Cabral & Bacigalupo, Argentina, Vanni & Radovancick 996 (GB), EU542938(4),
AY764290(3), EU543096(4), EU557699(5); G. eupatorioides (Cham. & Schltdl.) E.L. Cabral, Argentina, Schinini & Cristobal 9811 (GB), EU542939(4), EU543028(4),
EU543097(4), EU557700(5). Gomphocalyx Baker: G.
herniarioides Baker, Madagascar, De Block et al.
569 (BR), AY764291(3); Madagascar, Groeninckx et al.
125 (BR), EU542940(4), EU567466(4), EU567461(5).
Hedyotis L. H. fruticosa L., Sri Lanka, Larsson &
Pyddoke
22
(S),
EU542942(4),
EU543098(4),
(5)
EU557702 ; H. korrorensis (Valeton) Hosok., The
Caroline Islands, Fosberg 47697 (S), EU542943(4),
EU543099(4), EU557703(5); H. lawsoniae Wight, Sri
Lanka, Wambeek & Wanntorp 2996 (S), EU542944(4),
EU557704(5); H. lessertiana Thwaites var. lassertiana, Sri Lanka, Klackenberg 413 (S), EU542945(4),
EU543029(4), EU543100(4), EU557705(5); H. lessertiana Thwaites var. marginata Thwaites & Trimen,
Sri Lanka, Fagerlind 3668 (S), EU542946(4),
EU543030(4), EU543101(4), EU557706(5); H. macrostegia Stapf, Malaysia, Sabah, Wallander 6 (GB),
EU542947(4), AF002767(1), EU543102(4); H. quinquenervis Thwaites, Sri Lanka, Bremer et al. 163 (S),
EU542948(4), EU543103(4), EU557707(5); H. rhinophylla Thwaires ex Trimen, Sri Lanka, Fagerlind
5082 (S), EU542949(4), EU543104(4), EU557708(5); H.
swertioides Hook.f., South India, Klackenberg &
Lundin 3 (S), EU542950(4), EU543031(4), EU543105(4),
EU557709(5). Hedythyrsus Bremek. H. spermacocinus (K. Schum.) Bremek., Zambia, Dessein et al. 1017
(BR),
EU542951(4),
EU543032(4),
EU543107(4),
(5)
EU557711 . Hemidiodia K. Schum. H. ocymifolia
(Willd. ex Roem. & Schult.) K. Schum., French
Guiana, Andersson et al. 2040 (GB), EU542952(4),
EU543108(4), EU557712(5). Houstonia L. H. caerulea L., USA, Vincent & Lammers s.n. (GB),
EU542953(4), AF333379(2), EU543109(4), EU557713(5);
H. longifolia Gaertn., USA, Yatskievych 96-49 (MO),
EU542954(4), AF002766(1), EU567462(5); USA, Weigend
9963 (NY), EU642536(4). Kadua Cham. & Schltdl. K.
acuminata Cham. & Schltdl., USA, Hawaii, cult. at
N.B.G.Belgium (BR), EU542955(4), EU543110(4),
EU557714(5); K. affinis Cham. & Schltdl., USA,
Hawaii, Motley 1733 (NY), EU642523(4), EU642538(4);
K. axillaris (Wawra) W.L. Wagner & Lorence, USA,
Hawaii, Harrison-Gagne s.n. (GB), AF002765(1); USA,
Hawaii, Maul, Motley 1724 (NY), EU642524(4),
EU642535(4); K. centranthoides Hook. & Arn., USA,
Hawaii,
Skottsberg
6788
(S),
EU542956(4),
EU543033(4), EU543111(4), EU557715(5); K. cordata
Cham. & Schltdl., cult., Lorence 8021 (PTBG),
EU542957(4), AF333376(2), EU543112(4), EU557716(5);
K. degeneri (Fosberg) W.L. Wagner & Lorence, cult.,
Wood 5062 (PTGB), EU542958(4), AF333371(2),
EU543113(4), EU557717(5); K. fosbergii (W.L. Wagner
& D.R. Herbst) W.L. Wagner & Lorence, USA,
Hawaii, Oahu, Motley 1677 (NY), EU642529(4),
EU642543(4); K. littoralis Hillebr., USA, Hawaii,
Molokai, Kiehn & Luegmayr 920823 (WU),
EU542960(4), EU543034(4), EU543115(4), EU557719(5);
K. parvula A. Gray, cult., Perlman 12783 (GB),
EU542961(4), AF333375(2), EU543116(4), EU557720(5).
Kohautia Cham. & Schltdl. K. amatymbica Eckl. &
Zeyh., South Africa, Bremer et al. 4307 (UPS),
EU542962(4), EU543035(4), EU543117(4), EU557721(5);
K. caespitosa Schnizl., Zambia, Dessein et al. 432
(BR),
EU542963(4),
EU543036(4),
EU543118(4),
(5)
EU557722 ; K. coccinea Royle, Zambia, Dessein
et al.
751
(BR),
EU542964(4),
EU543037(4),
(4)
(5)
EU543119 , EU557723 ; K. cynanchica DC., South
Africa, Dessein et al. 469 (BR), EU542965(4),
EU543038(4), EU543120(4), EU557724(5); K. microcala Bremek., Zambia, Dessein et al. 1149 (BR),
EU542966(4), EU543039(4), EU543121(4), EU557725(5);
K. obtusiloba (Hiern) Bremek., Kenya, Luke 9035
(UPS), EU542967(4), EU543040(4), EU543122(4),
EU557726(5); K. subverticillata (K. Schum.) D.
Mantell, Zambia, Dessein et al. 462 (BR), EU557727(5);
Zambia, Dessein et al. 470 (BR), EU542968(4),
EU543041(4), EU543123(4); K. virgata (Willd.)
Bremek., Madagascar, De Block et al. 539 (BR),
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
TWO NEW RUBIACEAE GENERA ENDEMIC TO MADAGASCAR
EU542969(4), EU543124(4), EU557728(5). Lathraeocarpa Bremek. L. acicularis Bremek., Madagascar,
De Block et al. 2316, EU642516(6), EU642521(6),
EU642532(6), EU642519(6). Lelya Bremek. L. osteocarpa Bremek., Tanzania, Gereau 2513 (BR),
EU542970(4), EU543125(4), EU557729(5). Manettia
Mutis ex L. M. alba (Aubl.) Wernh., French Guiana,
Andersson et al. 1917 (GB), EU542971(4), AF002768(1);
M. lygistum (L.) Sw., Colombia, Andersson et al. 2128
(GB),
EU542972(4),
AF002769(1),
EU543126(4),
EU557730(5). Manostachya Bremek. M. ternifolia
E.S. Martins, Zambia, Dessein et al. 265 (BR),
EU542973(4), EU543042(4), EU543127(4), EU557731(5).
Mitracarpus Zucc. ex Schult. & Schult.f. M. frigidus (Willd. ex Roem. & Schult.) K. Schum., French
Guiana, Andersson et al. 1995 (GB), EU542974(4),
AF002770(1),
EU543128(4),
EU557464(5);
M.
microspermus K. Schum., Guiana, Jansen-Jacobs
et al. 4785 (GB), EU542975(4), EU543044(4),
EU557732(5). Mitrasacmopsis Jovet: M. quadrivalvis Jovet, Zambia, Dessein et al. 1273 (BR),
EU542976(4), EU543045(4), EU543129(4), EU557733(5).
Oldenlandia L. O. affinis (Roem. & Schult.) DC.,
Zambia, Dessein et al. 627 (BR), EU542977(4),
EU543046(4), EU543130(4), EU557734(5); O. angolensis K. Schum., Zambia, Dessein et al. 932 (BR),
EU542978(4), EU543047(4), EU543131(4), EU557735(5);
O. biflora L., Japan, cult. at N.B.G.Belgium, Van
Caekenberghe 63 (BR), EU542979(4), EU543132(4),
EU567459(5), EU557736(5); O. capensis L.f. var. capensis, Zambia, Dessein et al. 843 (BR), EU542980(4),
EU543048(4), EU543133(4), EU557737(5); O. capensis
L.f. var. pleiosepala Bremek., Tanzania, Kayombe
et al.
s.n.
(BR),
EU542981(4),
EU543049(4),
(4)
(5)
EU543134 , EU557738 ; O. corymbosa L., Zambia,
Dessein et al. 487 (BR), EU542982(4), EU543050(4),
EU543135(4), EU557739(5); O. echinulosa K. Schum.,
Zambia, Dessein et al. 928 (BR), EU542983(4),
EU543051(4), EU543136(4), EU557740(5); O. echinulosa K. Schum. var. pellicida (Hiern) Verdc., Tanzania, Kayombo & Kahemela 1993 (BR), EU542984(4),
EU543137(4), EU557741(5); O. fastigiata Bremek.,
Zambia, Dessein et al. 1019 (BR), EU542985(4),
EU543052(4), EU543138(4), EU557742(5); O. galioides
(F. Muell.) F. Muell., Australia, Harwood 1511 (BR),
EU542986(4), EU543053(4), EU543139(4), EU557743(5);
O. geophila Bremek., Zambia, Dessein et al. 935
(BR),
EU542987(4),
EU543054(4),
EU543140(4),
EU557744(5); O. goreensis (DC.) Summerh., Zambia,
Dessein et al. 1286 (BR), EU542988(4), EU543055(4),
EU543141(4), EU557745(5); O. herbacea (L.) Roxb.
var. goetzei (DC.) Summerh., Zambia, Dessein et al.
442 (BR), EU542989(4), EU543056(4), EU543142(4),
EU557746(5); O. herbacea (L.) Roxb. var. herbacea,
Zambia, Dessein et al. 463 (BR), EU542990(4),
EU543057(4), EU543143(4), EU557747(5); O. lancifolia
471
(Schumach.) DC., Zambia, Dessein et al. 1356 (BR),
EU542991(4), EU543058(4), EU543144(4), EU557748(5);
O. microtheca (Cham. & Schltdl.) DC., Mexico,
Frödeström & Hultén 681 (S), EU542992(4),
EU543059(4), EU543145(4), EU557749(5); O. mitrasacmoides F. Muell., Australia, Harwood 1516 (BR),
EU542993(4), EU543146(4), EU557750(5); O. nematocaulis Bremek., Zambia, Dessein et al. 924 (BR),
EU542994(4), EU543060(4); O. nervosa Hiern, Gabon,
Andersson & Nilsson 2326 (GB), AF333382(2); O. robinsonii Pit., Zambia, Dessein et al. 346 (BR),
EU543061(4), EU543147(4), EU557751(5); O. rosulata
K. Schum., Zambia, Dessein et al. 1197 (BR),
EU543043(4), EU567467(5), EU567465(5); O. salzmannii (DC.) Benth. & Hook.f. ex B.D. Jacks., Brazil,
Harley 15514 (UPS), EU542995(4), AY764294(3),
EU543148(4), EU557752(5); O. taborensis Bremek.,
Tanzania, Bidgood et al. 4015 (BR), EU542996(4),
EU543149(4), EU557753(5); O. tenelliflora (Blume)
Kuntze, Japan, cult. at N.B.G.Belgium, Van Caekenberghe
70
(BR),
EU542997(4),
EU543062(4),
(4)
(5)
EU543106 , EU557710 ; O. tenuis K. Schum.,
Guyana, Jansen-Jacobs et al. 41 (UPS), EU542998(4),
AY764293(3), EU557754(5); O. uniflora L., USA,
Godfrey 57268 (GB), EU542999(4), AY764295(3),
EU543150(4), EU557755(5); O. wauensis Schweinf. ex
Hiern, Ethiopia, Friis et al. 2560 (UPS), EU543017(4),
EU543076(4), EU543168(4), EU557774(5); O. wiedemannii K. Schum., Kenya, Luke & Luke 8362 (UPS),
EU543000(4), EU543063(4), EU543151(4), EU557756(5).
Pentanopsis Rendle: P. fragrans Rendle, Ethiopia,
Gilbert et al. 7458 (UPS), EU543065(4), EU543153(4),
EU557758(5); P. gracilicaulis (Verdc.) Thulin &
Bremer, Somalia, Thulin et al. 10512 (UPS),
EU567458(5), EU567460(5), EU567468(5). Pentodon
Hochst. P. pentandrus (K. Schum. & Thonn.) Vatke,
Zambia, Dessein et al. 598 (BR), EU543002(4),
EU543066(4), EU543154(4), EU557759(5). Phylohydrax
Puff: P. carnosa (Hochst.) Puff, South Africa, Bremer
3783 (UPS), EU543003(4), EU543067(4), EU642534(5),
EU557760(5); P. madagascariensis (Willd. ex Roem.
& Schult.) Puff, Madagascar, De Block et al. 640 (BR),
EU543004(4), AY64292(3), EU543155(4), EU557761(5).
Richardia L. R. scabra L., Colombia, Andersson
et al.
2073
(GB),
EU543005(4),
AF003614(1),
(4)
(5)
EU543156 , EU557762 ; R. stellaris (Cham. &
Schltdl.) Steud., Australia, Egerod 85343 (GB),
EU543006(4), EU543068(4), EU543157(4), EU557763(5).
Spermacoce L. S. capitata Ruiz & Pav., French
Guiana, Andersson 1908 (GB), EU543007(4),
EU543069(4), EU543158(4), EU557764(5); S. erosa
Harwood,
Australia,
Harwood
1148
(BR),
EU543008(4), EU543070(4), EU543159(4), EU557765(5);
S. filituba (K. Schum.) Verdc., Kenya, Luke 9022
(UPS), EU543009(4), EU543071(4), EU543160(4),
EU557766(5); S. flagelliformis Poir., Madagascar, De
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
472
I. GROENINCKX ET AL.
Block et al. 794 (BR), EU543010(4), EU543072(4),
EU543161(4), EU557767(5); S. hispida L., Sri Lanka,
Wanntorp et al. 2667 (S), EU543011(4), EU543073(4),
EU543162(4), EU557768(5); S. prostrata Aubl., Colombia, Andersson et al. 2078 (GB), EU543012(4),
EU543163(4), EU557769(5); S. remota Lam., French
Guiana, Andersson et al. 2016 (GB), EU543013(4),
EU543164(4), EU557770(5); S. ruelliae DC., Gabon,
Andersson & Nilsson 2296 (GB), EU543014(4),
EU543074(4), EU543165(4), EU557771(5). Stenaria
(Raf.) Terrell: S. nigricans (Lam.) Terrell, USA,
Yatskievych 96-92 (MO), EU543015(4), AF333373(2),
EU543166(4), EU557772(5). Synaptantha Hook.f. S.
tillaeacea (F. Muell.) Hook.f., Australia, Lazarides
& Palmer 272 (K), EU543016(4), EU543075(4),
EU543167(4),
EU557773(5).
Thamnoldenlandia
Groeninckx ined. T. ambovombensis Groeninckx
ined., Madagascar, De Block et al. 2328 (BR),
GU475972, GU475980, GU475984, GU475976.
Outgroup: Batopedina Verdc. B. pulvinellata E.
Robbr., Zambia, Dessein et al. 264 (BR), EU542924(4),
EU543021(4), EU543083(4), EU557684(5). Carphalea
Juss. C. madagascariensis Lam., Madagascar, De
Block et al. 578 (BR), EU542926(4), EU543023(4),
EU557686(5). Pentanisia Harv. P. parviflora Stapf
ex Verdc., Zambia, Dessein et al. 678 (BR),
EU543001(4), EU543064(4), EU543152(4), EU557757(5).
© 2010 The Linnean Society of London, Botanical Journal of the Linnean Society, 2010, 163, 447–472
Petra de Block