KEW BULLETIN
(2019) 74:52
DOI 10.1007/S12225-019-9840-3
ISSN: 0075-5974 (print)
ISSN: 1874-933X (electronic)
Cola species of the limestone forests of Africa, with a new,
endangered species, Cola cheringoma (Sterculiaceae),
from Cheringoma, Mozambique
Martin Cheek1 , Quentin Luke2, Hermenegildo Matimele1,3, Aurélio Banze3 & Poppy Lawrence4
Summary. Cola cheringoma is described from the limestone gorge forest of the Cheringoma Plateau in Sofala
Province of Central Mozambique. Tentatively treated previously as C. clavata Mast., it differs in being restricted to limestone substrate, the leaves drying white-green below (not on sandy soils, drying dark greybrown). The tepal number of female flowers is 5 (not (5 –) 6), staminode number 5 (not 8), and the
indumentum of the outer perianth covers only 50 – 60% of the surface with two distinct hair classes (not
100% coverage with a single hair type). The species is assessed as EN B2ab(iii) using the IUCN 2012
standard due to threats from the low number of locations, quarrying, and habitat modification. The Cola
species growing in forest on limestone in tropical Africa are mapped and reviewed with respect to their
status as obligate or facultative calcicoles, and with respect to their probable evolutionary origin. Based on
morphological characters, adaptation to limestone habitats has probably occurred at least four times in the
genus. Forests on limestone are rare and threatened in tropical Africa: only thirteen locations are known
with certainty: these occur in Kenya (10 locations), Tanzania (2 locations) and Mozambique (1 location).
Key Words. Calicole, conservation, mining, monograph, quarrying, taxonomy, threatened.
Introduction
For most of the twentieth century Cola Schott. & Endl.
was included in tribe Sterculieae of Sterculiaceae sensu
lato of the core Malvales. Phylogenetic investigation of
Malvales showed that in place of the traditional four
families recognised (Malvaceae, Bombacaceae,
Sterculiaceae, Tiliaceae) there is a choice of either
recognising nine subfamilies in a super-Malvaceae
(Bayer et al. 1999; Bayer & Kubitzki 2003) or
recognising the same units as the families,
Bombacaceae, Brownlowiaceae, Byttneriaceae,
Dombeyaceae, Durionaceae, Helicteraceae, Malvaceae
sensu stricto, Sparrmanniaceae, Sterculiaceae and
Tiliaceae (Baum et al. 1998; Cheek & Dorr 2007;
Cheek in Heywood et al. 2007; Skema 2012; Wilkins &
Whitlock 2012). Cola can therefore now be placed
either in Malvaceae-Sterculioideae or Sterculiaceae s.s.
The second approach is preferred since it is less
cumbersome and creates less taxonomic instability
(Cheek & Dorr 2007).
The Sterculiaceae sensu stricto are characterised
within Malvales by unisexual flowers with a single
perianth whorl that lack an epicalyx. The male flowers
have an androgynophore bearing the anthers in a
terminal capitulum or ring, the gynoecium vestigial
and inconspicuous. Female flowers usually have a
sessile or subsessile gynoecium developing into an
apocarpous fruit of (1 –) 4 – 5 (– 15) fruitlets or
mericarps, the base surrounded by indehiscent anthers. The family is pantropical, with c. 415 species
arranged in 13 genera (Cheek in Heywood et al. 2007).
Pterygota Schott & Endl., pantropical, with dehiscent, woody mericarps containing dry, winged seeds,
is in a sister relationship with Cola, while Octolobus
Welw., confined to tropical Africa, with numerous
spirally inserted indehiscent mericarps, is sister to
Pterygota-Cola combined (Wilkie et al. 2006). The
remaining genera of the Cola clade, Hildegardia
Schott & Endl., Firmiana Marsili, Pterocymbium R.Br.,
and Scaphium Schott & Endl. all have winged
fruitlets and are wind-dispersed, and all but the first
are confined to SE Asia and adjoining areas. In
comparison, the pantropical genus Sterculia L.,
sometimes confused with Cola, is in an entirely
different subclade, and always has dehiscent fruit
with the seeds with radicle directed away from the
Accepted for publication 8 August 2019.
1
Science, Herbarium, Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AE, U.K. e-mail: m.cheek@kew.org
2
East African Herbarium, National Museums of Kenya, Museum Hill Road, P.O. Box 45166, Nairobi 00100, Kenya.
3
National Herbarium of Mozambique, Institute for Agricultural Research of Mozambique, P.O. Box 3658, Mavalane, Maputo 8, Mozambique.
4
College of Life and Environmental Sciences, University of Exeter, Exeter EX4 4QD, U.K.
© The Author(s), 2019
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hilum and hard-coated, borne on a placenta with
irritant hairs.
The genus Cola is mostly confined to evergreen
lowland and submontane forest in continental
subsaharan Africa with only two species, C. cordifolia
(Cav.) R.Br. and C. gigantea A.Chev., in deciduous
forest or woodland. With 100 – 125 species of trees
and shrubs, Cola is the most species-diverse genus in
the Sterculiaceae. The genus is characterised by
indehiscent (rarely at length dehiscent) fleshy orange or red mericarps containing seeds with a soft,
fleshy, edible seedcoat, the radicle directed towards
the hilum. The endocarp is glabrous. Seed is thought
to be dispersed mainly by monkeys and apes, which
may explain the absence of Cola from oceanic islands
near Africa such as Madagascar. While some Cola
species are widespread, many are extremely local,
and some are known from few or single forest
patches and so are vulnerable to extinction. Eight
species of Cola in Cameroon, the most species diverse
country for the genus, have been assessed as
threatened (Onana & Cheek 2011). Cola nitida
(Vent.) Schott. & Endl. and C. acuminata (P.Beauv.)
Schott. & Endl. are planted throughout the tropics
for their seeds, which act as stimulants when chewed
and are an ingredient of the eponymous and
ubiquitous ‘Cola’ soft drinks. Two other species also
have stimulant seeds, but are only locally cultivated
(Cheek 2002a; Cheek & Dorr 2007).
Most species of Cola occur in Tropical Africa, with
only three species, C. natalensis Oliv., C. dorrii Cheek
and C. greenwayi Brenan in South Africa (Cheek et al.
2018a). In East Africa (Uganda, Kenya and Tanzania),
21 species are native (Cheek & Dorr 2007). However,
West and Central Africa are the heartland of Cola. The
largest number of species for any flora region is that in
the Flora of West Tropical Africa (FWTA), with 42
species, and with an additional nine imperfectlyknown species (Keay & Brenan 1958). Thirty-three
species are recorded from Gabon (Hallé 1961) and 32
from Congo-Kinshasa (Germain 1963). The Flore du
Cameroun account awaits completion. However,
Kenfack et al. (2018) report 43 species from Cameroon, most of which are confined to the Cross-Sanaga
interval (Cheek et al. 2001). The genus was last
monographed by Schumann (1900) when 33 species
were recognised. Although Brenan did much research
on the genus throughout its range, he confined
himself, largely, to publishing accounts of new species
(e.g. Brenan & Keay 1955).
During preparation for a monograph (Cheek
2002a, b; Cheek & Dorr 2007; Cheek et al. 2018a)
and for conservation assessments of all known
species of Cola, 10 specimens from the limestone
area of Cheringoma, Mozambique were observed.
These had been collected in a series of five visits
from Nov. 1957 – Oct 1962 by António de
© The Author(s), 2019
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Figueiredo Gomes e Souza (1896 – 1973) of the
Mozambique Agricultural Service who produced the
Dendrologia de Moçambique (Gomes e Sousa 1967;
Burrows et al. 2018). This intensive targetting of the
Cheringoma limestone Cola by Gomes e Sousa,
which extended over several years, suggests that
he had identified that it was an interesting taxon,
and that he repeatedly but unsuccessfully sought
material of stages additional to the male flowering
collection he had made at his first gathering.
Finally, he identified his specimens as “Cola
?clavata” indicating that he considered that they
might represent a different species. The LMA
duplicate shows that the material puzzled other
botanists. It is annotated “Cola clavata Mast.?, Kew”,
but also “Cola cf natalensis Oliv. Pretoria”, and
finally it was identified as C. greenwayi in 1971, by
Graca Silva at LMA where it was filed as such (C.
Langa pers. comm. 2018). In the last ten years
there have been two botanical surveys to the
Cheringoma limestone gorges (Wursten 2014). In
one of these, gathering material for the excellent
“Trees & Shrubs Mozambique” (Burrows et al.
2018), sight records were made in three different
gorges of a Cola ascribed to C. mossambicensis Wild
(Burrows et al. 2012). It is most likely that this was
also misidentification for the species described here
as new to science.
Limestone substrates around the world are renowned for harbouring narrowly endemic species,
and new species narrowly endemic to limestone are
still being discovered frequently, such as species of
Polyalthia Blume (Annonaceae) in Peninsular Malaysia
(Turner et al. 2018), Pilea (Urticaceae) from China
(Monro et al. 2012), Begonia (Begoniaceae) from karst
at the Sino-vietnamese border (Chung et al. 2014) or
in Borneo (Sang et al. 2013, describing 13 new species
from Sarawak), Nepenthes (Nepenthaceae) in Indonesian New Guinea (Cheek et al. 2018b) and sometimes
even genera, e.g. Khaosokia caricoides D.A.Simpson,
Chayam & J.Parn., a monotypic genus of the
Cyperaceae in Thailand (Simpson et al. 2005). In the
Americas, Ficus bonijesulapensis R.M.Castro in
Moraceae (Castro & Rapini 2006), Ceiba rubriflora
Carv.-Sobr. & L.P.Queiroz in Bombacaceae
(Carvalho-Sobrinho & Queiroz 2008), Oxalis calcicola
Fiaschi in Oxalidaceae (Fiaschi 2014) and the new
Gesneriaceae genus Chautemsia calcicola A.O.Araujo &
V.C.Souza (Araújo et al. 2010) are all examples from
Brazil. However far fewer botanical studies have
focussed on species of limestone habitats in tropical
Africa.
Materials and Methods
Names of species and authors follow IPNI
(continuously updated). Nomenclatural practice fol-
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lows Turland et al. (2018). Herbarium material was
examined with a Leica Wild M8 dissecting binocular
microscope fitted with an eyepiece graticule measuring in units of 0.025 mm at maximum magnification. The drawing was made with the same
equipment with a Leica 308700 camera lucida
attachment. Specimens were inspected from the
following herbaria: BM, BNRH, EA, FHO, K, LMA,
PRE. The format of the description follows those in
other papers describing new species in Cola, e.g.
Cheek (2002a, b). All specimens indicated “!” have
been seen by the first author. Points were
georeferenced using locality information from herbarium specimens. The map was made using
ArcMap version 10.5, with additional layers showing
protected areas (UNEP-WCMC 2017) and lakes
(ESRI 1992).
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52
The conservation assessment follows the IUCN
(2012) standard. Herbarium codes follow Index
Herbariorum (Thiers, continuously updated).
Results
The Gomes e Sousa specimens collected at Cheringoma
resemble those of Cola clavata but can be separated by the
characters shown in Table 1. Even in the vegetative state,
the two species can be distinguished by the differences in
colour of the dried leaf-blades, and of the differences in the
bud-scales and stem indumentum. No other Cola species
have been recorded from limestone in Mozambique, nor
in fact for the entire Flora Zambesiaca area (Wild 1961),
although many species of Cola do occur on limestone in
Tanzania & Kenya (see discussion below). A key to the
species of Cola in Mozambique is provided below.
Key to the species of Cola in the Flora Zambesiaca area (Mozambique, Zimbabwe, Zambia, Malawi &
Botswana)
1. Petioles on a single stem, consistently short, 2 – 7 mm long . . . . . . . . . . . . . . . . . . . . . . . . . . C. chlorantha
Petioles on a single stem varying from 4 – 5 mm to at least 30 mm long, in most species to 60 – 100 (– 270) mm
long . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Young stems densely covered in orange or reddish-brown indumentum . . . . . . . . . . . . . . . . . . . . . . . . . . 3
Young stems glabrous to very sparsely and inconspicuously hairy . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3. Occurring in forest <900 m altitude; longest petiole to 10 cm long; leaf-blade 14 – 21 × 7 – 11 cm;
young stems and petioles with a thick scurfy felt-like layer of red-brown hairs that is shed to reveal white
stems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. mossambicensis
Occurring at >1100 m altitude; petioles 0.3 – 4 (– 5.6) cm long; leaf-blade 3 – 16 × 1 – 6 cm; stems with
subscabrid, persistent, red or black indumentum, stems greyish-brown . . . . . . . . . . . . . . . . . . C. greenwayi
4. Inflorescences multiple-flowered; pedicels 4 – 6 mm long; perianth lobes (3 –) 3.5 – 4.5 × 1.5 – 2 (– 2.5) mm;
stipules 3 mm long . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. discoglypremnophylla
Inflorescences single-flowered; pedicels 7 – 10 mm long; perianth lobes 4 – 5.5 × 2 – 3.1 mm; stipules >8.5 mm
long . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
5. Leaf-blades discolorous, light green above, white-green below; indumentum of young stems sparsely white
peltate-stellate hairy, hairs persistent for a season; abaxial surface of tepals with 50 – 60% indumentum
coverage, hairs strongly dimorphic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. cheringoma
Leaf-blades concolorous, dark grey-brown on both surfaces; indumentum of young stems moderately densely
red stellate hairy, hairs early caducous; abaxial surface of tepals with 100% indumentum coverage, hairs
monomorphic . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . C. clavata
Cola cheringoma Cheek sp. nov. Type: Mozambique,
Sofala Province, Cheringoma Distr., Condué R., calcareous soils, fl. 6 Nov. 1957, Gomes e Sousa 4441
(holotype K!; isotypes K!; LMA!).
http://www.ipni.org/urn:lsid:ipni.org:names:60479325-2
Dioecious (probably), evergreen, small tree (3 –) 4 – 7 m
tall; trunk characters not reported. Leafy stems terete, c.
3 mm diam., main shoots c. 12 cm long each season,
spur-shoots c. 2 cm long, epidermis white, smooth,
lenticels not conspicuous, current season’s growth
sparsely covered with white, appressed peltate-stellate
7 – 10-armed hairs 0.2 – 0.25 mm diam., the arms
tapering to a point from the peltate base; previous
season’s stems longitudinally ridged, discoloured by
black epiphytic patches, cicatrices raised, glabrescent.
Bud scales c. 5, ovate, 2.25 × 1.5 mm, slightly concave,
api cul ate, midrib raised on outer surface;
indumentum white, stellate, 8 – 9-armed, 0.3 –
0.4 mm diam., dense. Leaves 3 – 14 over the length
of a season’s growth, alternate, spirally arranged
leaves; at anthesis the distalmost leaves subsessile, with
the smallest blades, the leaves produced at the
beginning of the season with the longest blades and
longest petioles. Leaf blades discolorous, green to
yellowish-green on upper surface, lower surface
white-green, largest leaves (produced at beginning of
© The Author(s), 2019
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Table 1. Characters distinguishing Cola cheringoma from Cola clavata (data for C. clavata from Simão 1202 (K, LMA) and Kirk 235
(holotype K).
Character
Cola cheringoma
Cola clavata
Substrate
Leaf blade colour on drying
calcareous-clay
discolorous light green above;
white-green below
ovate with raised midrib, apex
rounded but with short apiculus
orbicular, concave, coriaceous;
length:breadth ratio 1:1
sparsely white peltate-stellate hairy,
hairs persistent for a season
black/black
sandy soils
concolorous, dark grey-brown on both
surfaces
subulate, apex narrowly acute
Bud-scales
Innermost bracts (shape, texture
and length: breadth ratio)
Indumentum of young stems
Predominant colour on drying of
inner/outer surface of tepals
Indumentum coverage
50 – 60%
Indumentum of outer surface of tepal lobes
Number of hair types
2 distinct hair types
Orientation of hair arms
along long axis of tepal lobe
Tepal number (female flowers)
5
Staminode number (fema le
5
flowers)
season), oblanceolate or elliptic (8.7 –) 11.7 – 17.4 (–
20.3) × (3.9 –) 4.8 – 7.8 (– 9.7) cm, apex shortly
acuminate, acumen 0.5 – 0.8 mm long, base acute,
obtuse or rounded; smallest leaves (produced at end
of season) ovate, (0.7 –) 1 – 2.5 ( – 4.7) × (0.3 –) 0.4 –
1.1 (– 1.5) cm, apex acuminate, base cordate. Secondary nerves 4 – 6 (– 7) on each side of the midrib,
arising at c. 45° from the midrib, arching very
gradually towards the margin, in the distal half of the
blade the nerves often connecting with the secondary
nerve above, forming an incomplete looping marginal
nerve 2 mm from the margin, domatia absent; tertiary
and quaternary nerves forming a prominent reticulum, glabrous. Petioles terete, (2.3 –) 3 – 8.4 cm long
(longest leaves) and 0.1 – 0.4 cm long (shortest leaves),
c. 1 mm wide, pulvini 2.5 – 3 mm long at apex and
base of petiole of the longer leaves, indumentum of
sparse simple, white ascending hairs 0.1 mm long, c.
5% cover, at length glabrescent; pulvini densely
covered in 8 – 9-armed translucent stellate hairs
0.075 – 0.1 mm diam., 90 – 100% cover. Stipules
caducous, lanceolate, 8.75 × 2 mm, proximal third
widest, concave, distal part linear. Inflorescences 1flowered, flower buds developing in dormant season
on previous (mainly) and current season’s growth, 1 –
4 per leaf axil, from several nodes in succession; buds
globose, c. 4 mm diam. pre-anthesis, protected by 6 – 8
concave, suborbicular bracts (Fig. 1N). Bracts slightly
broader than long, suborbicular 2 mm long, 2.3 mm
wide, apex rounded with margin slightly hooded,
margin densely hairy, inner surface with 10 – 12 equal,
parallel, equally-spread nerves; outer surface densely
appressed hairy, hairs simple 0.2 – 0.6 mm long,
intermixed with inconspicuous sparse 4 – 8-armed
stellate hairs 0.5 – 0.75 mm long, the arms directed to
either base or apex of the bract. Flowers opening while
© The Author(s), 2019
narrowly rhombic-rectangular,
membranous; length:breadth ratio10:1
moderately densely red stellate hairy, hairs
early caducous
red-brown/golden-brown
100%
one hair type
radial
(5 –) 6
8
stem apex is dormant, from stems of current and
previous season’s growth; flower buds 1-flowered, 1 –
several per axil, opening synchronously. Pedicels 7 –
7.5 mm long (male flowers), 0.5 – 0.6 mm diam., not
articulated, proximal 1.5 mm swollen, 1 mm diam.,
bearing the scars of four bracts, indumentum of sparse
stellate hairs, 3 – 6-armed, 0.2 – 0.3 mm diam., arms
mainly directed towards base or apex of pedicel (Fig.
1M). Female pedicels (Fig. 1L) with hairs denser,
larger, 0.3
– 0.5 mm diam., 5 – 7-armed. Perianth
divided by 4 5 into 5 ± patent lobes, each 4.5 – 5 mm
long, 2.5 – 3.5 mm wide, the slender margins inflexed,
forming a raised rim c. 0.2 mm high, outer surface 50
– 60% covered in dimorphic stellate hairs (Fig. 1K):
type 1 hairs cover 40 – 50% of the surface, so that the
hairs nearly touch each other, 0.1 – 0.13 mm diam., 3
– 6-armed, white, type 2 hairs sparse, larger, 0.25 –
0.5 mm diam., 7 – 10-armed, the arms directed along
axis of lobe golden-brown. Inner surface with minute
translucent vesicles densely covering the surface of the
lobes, the inner, unlobed part of the perianth slightly
domed, glabrous, stellate hairs absent from inner
surface apart from a few white filiform stellate hairs
towards the tips of the lobes. Male flowers 16 – 21 mm
wide, with an androphore 3 – 3.3 mm long, cylindrical,
0.2 mm diam. at base, 0.15 mm wide near apex,
glabrous, apart from densely pubescent ring at the
junction with the perianth, the hairs yellow, erect,
simple 0.05 mm long; anthers uniseriate, 10, glabrous,
in a disc 1 – 1.3 mm long, 2.5 – 2.7 mm diam.; ovary
vestigial, concealed within anther head (Fig. 1G & H).
Female flowers 14 mm wide, with androphore absent;
anthers at base of ovary, not reduced in size; ovary
depressed globose, 1.8 mm long, 2.2 mm diam.,
inconspicuously 5-lobed, densely stellate hairy, hairs 8
– 10-armed, 0.4 – 0.5 mm diam., arms stiff, ascending.
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Style 1.4 mm long, 0.9 mm diam., indumentum as
ovary; stigmas 5, patent, obovate, 1 mm long, 0.6 mm
wide, apex pleated, reflexed, upper surface glabrous,
but with long papillae 0.6 – 0.8 mm long. Female
flowers with tepals longer and broader than in the
males. Fruits and seeds unknown. Fig. 1.
RECOGNITION. Differing from Cola clavata Mast. in that
leaf-blades discolorous, light green above; white-green
below (not ± concolorous, dark grey-brown); outer
perianth indumentum covering 50 – 60% surface, with
two distinct hair classes, largest stellate hairs with arms
directed along longitudinal axis of tepal (not 100%
coverage, a single hair type, stellate hair arms radiating), tepal number 5 (not (5 –) 6); staminode number
5 (not (5 –) 6). See Table 1 for additional characters.
DISTRIBUTION . Mozambique: Sofala Province,
Cheringoma Plateau (Map 1).
SPECIMENS EXAMINED. MOZAMBIQUE. Sofala Province,
Cheringoma. Condué Distr., near the sawmills of Mr
M. Sol, fl. 6 Nov. 1957, Gomes e Sousa 4441 (holotype
K!; isotypes K!, LMA!); ibid. st. 3 Dec. 1960, Gomes e
Sousa 4441A (K!); ibid. gallery forest of Condué R.
18°25'S, 35°02'E st. 11 Oct. 1961, Gomes e Sousa 4712
(K!); ibid. 18°40'S, 34°50'E, st. 13 June 1962, Gomes e
Sousa 4773 (K!); ibid. 18°45'S, 34°40'E, st. 25
Aug. 1962, Gomes e Sousa 4786 (K!); ibid. st. 25
July 1962, Gomes e Sousa 4787 (K!); ibid. st. 12
Oct. 1962, Gomes e Sousa 4793 (K!); “near n. 4793,
not opened flowers” 12 Oct. 1962, Gomes e Sousa 4793A
(K!); ibid. Gomes e Sousa 4793B (K!); ibid. Gomes e Sousa
4793C (K!).
CONSERVATION STATUS. The ten specimens of Cola
cheringoma derive from four points (Map 1), all of
which are indicated by the collector as being
gallery forest on limestone substrate. These points
appear to correspond to the limestone gorge area
of the Cheringoma Plateau, apparently the only
limestone forest area currently confirmed in Mozambique (but see note below). The Cheringoma
Formation of limestone forms a continuous belt
along the northeastern boundary of the ZânguèUrema depression and covers wide areas north of
the Búzi River (GTK Consortium 2006). The total
area of the limestone is not known. The
Cheringoma Plateau is aligned SSW to NNE,
forming the eastern side of the southern end of
the African Rift valley. Most of the northern half of
the plateau is calcareous sandstone that hosts
woodland. Underneath the sandstone is Eocene
limestone, exposed by river cutting and at cliffs,
the forest on it being restricted to the sides and
floors of the gorges.
Across Mozambique, most of the surviving patches
of lowland forest are threatened by clearance for
agriculture, uncontrolled logging, and uncontrolled
wildfires, so those that survive now exist as isolated
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patches (I. Darbyshire pers. comm. 2018). Around
Inhaminga and Inhamitanga, whence two of the
points occur, including the type specimen, the forest
is being cleared for farmland and timber, so it is
possible that the location for Cola cheringoma at this
location has been lost completely (observations
made on Google Earth, accessed 15 Sept. 2018). At
Catapú near to Imhamitanga, a major international
limestone mining extraction programme is intended
to supply material for cement, aggregate and agrilimestone markets, facilitated by the proximity of the
Beira-Tete railway (Premier African Minerals 2016).
There is also evidence of limestone exploitation near
Condué, where the natural vegetation is being
cleared for ‘borrow pits’ and associated infrastructure. This includes the construction of access roads,
which further fragment the surviving forest patches
(Google Earth imagery 2018). This location is at the
edge of the Gorongosa National Park, which offers
some levels of protection. It is also probably
protected within Coutada 12, a former hunting
concession which is now under the control of
Gorongosa, and which will likely eventually be
included within the park (B. Wursten pers. comm.
2018).
The four points for Cola cheringoma equate to three
threat-based locations as defined by IUCN. Using the
georeferenced specimens cited in this paper, the area
of occupancy (AOO) and extent of occurrence (EOO)
have been calculated using GeoCat (Bachman et al.
2011). Both AOO and EOO are below the threshold
for Endangered according to the IUCN categories and
criteria (AOO = 16 km2, EOO = 292 km2). Therefore,
given the threats and the decline in both quality and
extent of the habitat across this species range, Cola
cheringoma is here assessed as Endangered
B1ab(iii)+B2ab(iii).
ETYMOLOGY. Named for the Cheringoma Plateau, to
which this species seems restricted.
LOCAL NAMES. Sangala (in the local language according to Gomes e Sousa 4712 (K)).
ECOLOGY. All ten specimens known for Cola cheringoma
indicate that it grows in gallery forest of the river
Condué on alluvial lime soil (“alluvionar lime-argillous
soil”). The range of altitudes given is 180 – 200 m alt.
The forest is characterised as ‘dense subhygrophile’
(Gomes e Sousa 4793 B). Although the river Condué has
not yet been located by us with certainty, the reference
to Cheringoma (Gomes e Sousa 4712) and the three
grid references given (see specimens examined) allow
us to conclude that this species occurs in the poorly
explored limestone gorge area of the Cheringoma
Plateau.
The Cheringoma limestone gorge forest appears to
have been reported for the first time as a distinct
vegetation type in Stalmans & Beilfuss (2008). Those
authors map the vegetation as “Limestone Gorge”
© The Author(s), 2019
52
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Fig. 1. Cola cheringoma. A habit, male flowering branch; B female flower; C female flower from B, without perianth; D detail of
hairs from C; E male flower; F androecium from E; G longitudinal section of anther head from F, showing the vestigial gynoecium
within; H plan view of the style-stigmas from G; J detail of the inner surface of the female perianth at the sinus between lobes; K
indumentum from outer surface of perianth, female flower; L indumentum from pedicel, female flower; M indumentum from
pedicel, male flower; N inner surface of outermost bract; P detail of indumentum of the outer surface of bract, from N. All from
Gomes e Sousa 4441 (K). DRAWN BY ANDREW BROWN.
© The Author(s), 2019
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Page 7 of 14
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Map 1. Cola cheringoma sp. nov. of Mozambique, global distribution, showing protected areas.
within the Gorongosa National Park (GNP), depicting
it as a slender irregular band about 0.5 – 1 km wide,
consisting of c. 15 000 Ha extending along the length
of the plateau where it is surrounded by calcareous
sandstone. From this map and our data points we are
aware that it extends outside the GNP and in total is
perhaps 60 km long SSW to NNE. A succinct
description of this vegetation is that of Burrows et al.
(2018: 9 – 10): “A tall sheltered forest protected within
the deep limestone gorges on the western edge of the
Cheringoma Plateau, Sofala Province. Climate is very
humid and hot (annual mean temperature 34°C) with
a mean annual rainfall of just over 1100 mm,
occurring at altitudes of 100 to 280 m. The surrounding limestone shelf is dominated by Androstachys
johnsonii. The sheltered and protected gorges harbour
several very interesting and special species.” The
limestone was deposited in the Eocene (Anon.,
downloaded 17 Sept. 2018) and is nummulitic
(Mercader & Sillé 2013), including caves with stoneage remains. This vegetation type is not mapped in the
Vegetation map of the Flora Zambesiaca area (Wild &
Barbosa 1967), probably because the scale used there
is too coarse. In fact, the only limestone-based
vegetation type included in that work is a savanna
(woodland) type that occurs in central Zimbabwe.
52
DESIGNED BY POPPY LAWRENCE.
Additional locations in Mozambique with limestone
are documented in GTK Consortium (2006): “Limestones of the Tertiary Salamanga Formation, south of
Maputo, of the Cheringoma Formation west of Beira
along the Buzi River and in the type locality north of
Beira on the Cheringoma Plateau, have high calcium
carbonate contents. The Miocene Jofane Formation is
a second important accumulation of limestone. A
large area with limestone outcrops extends from the
Save River southwards to Inhambane. Limestone
occurrences are also known at Urrongas”. Thus, there
may be as many as five other limestone locations in
Mozambique, although some of these may be
subsurface and so may not support calcicole plants,
and if that is not the case may not support forest.
Several of these sites are already active limestone
quarries and any narrow endemics present may have
become extinct.
No detailed documentation of the limestone
gorge vegetation was available until recently when
an unpublished checklist of about c. 320 species by
Burrows et al. (2012) was made. Coates-Palgrave
et al. (2007) published a survey of the woody flora
and vegetation at Catapú, near Inhamitanga, which
is in the vicinity of the limestone, but that study
does not refer to any vegetation on limestone, even
© The Author(s), 2019
52
Page 8 of 14
though a prospective limestone mine occurs at the
northern boundary of Catapú (see conservation
section).
PHENOLOGY. Flowering occurs in early November
after the southern rains begin (Gomes e Sousa 4441)
in September. New shoots are extended in October
(Gomes e Sousa 4712). By early December only the
presence of numerous old floral bracts shows that
flowering has occurred, and the apical stem buds
are already dormant (Gomes e Sousa 4441A).
Through June, July, August to October, new axillary
floral buds develop while the stem apex remains
dormant (Gomes e Sousa 4773, 4786, 4787, 4793,
4793A, 4793B). It is clear that the flowering period
is brief, since, of ten specimens made throughout
the year, only one is in flower.
DIOECY. There is not enough evidence available to
determine whether Cola cheringoma is dioecious or
monoecious. The single flowering sheet had all
male flowers on the branch, and a pocket with
further male flowers, and a single female flower. It
is not possible to be certain whether the female was
from the same tree as the male, although this seems
most likely, in which case the species is monoecious.
POPULATION. On his specimen labels, Gomes e
Sousa often gives an indication of the number of
individuals that he observed. This varies from a
single individual (Gomes e Sousa 4441), to two
individuals (Gomes e Sousa 4712), to three (Gomes e
Sousa 4773), to ‘frequent in that place’ (Gomes e
Sousa 4786, 4787) to ‘common’ (Gomes e Sousa 4793
A-C).
Discussion
New species
Approximately 2000 new flowering plant species are
described each year (Willis 2017), adding to the
estimated 369,000 already known to science (Nic
Lughadha et al. 2016) although this total is disputed
(Nic Lughadha et al. 2017). Widespread species tend
to have already been discovered, so that many newly
discovered species are those that are range-restricted
and so are much more likely to be threatened, such as
Cola cheringoma. Evidence-based conservation assessments exist for about 21 – 26% of known species, and
30 – 44% of these assessments rate the species
concerned as threatened (Bachman et al. 2018). This
makes it imperative to discover and publish such
species so that they can assessed, and, if merited,
conservation actions taken to reduce their extinction
risks, such as through designating and implementing
Important Plant Areas (Darbyshire et al. 2017).
Cola cheringoma is one of numerous rangerestricted species new to science discovered in
Mozambique in recent years, mainly in connection
© The Author(s), 2019
KEW BULLETIN
(2019) 74:52
with the Trees & Shrubs of Mozambique project
(Burrows et al. 2018) and the Tropical Important
Plant Areas Project (Darbyshire et al. 2017). Due to
the unrest associated with the war of independence
(1964 – 1975) and subsequent civil war (1977 –
1992), Mozambique had experienced a long period
of relative neglect in terms of biodiversity research.
In the last 15 years this has changed to an upsurge in
botanical exploration and discovery as reported in
Cheek et al. (2018c). Since that date Olinia
chimanimani T.Shah (Shah et al. 2018) from
Chimanimani and Eriolaena rulkensii Dorr in the
Dombeyaceae (Dorr & Wurdack 2018) from near
Pemba in NE Mozambique have been published. The
latter is the first time that a member of this genus,
previously thought restricted to Asia, has been
recognised in continental Africa. Similarly, Erythrina
madagascariensis Du Puy & Labat, previously thought
restricted to Madagascar and the Comoro Islands,
has also been recently discovered in NE Mozambique
(see Burrows et al. 2018). More exciting species
discoveries in Mozambique are expected as botanical
exploration continues. The species richness is likely
to be the highest of the Flora Zambesiaca region
although due to under-exploration, the total species
number is unknown. New surveys at botanically
interesting sites in Mozambique are constantly producing new country records and new species.
African Limestone forest with Cola species
Although Cola species are almost ubiquitous in good
quality forest in tropical Africa, limestone (calcium
carbonate) surface outcrops are very rare in those
areas with sufficient precipitation to support forest, as
opposed to woodland or thicket. Surprisingly, there
seems to be no overview of limestone forest areas in
Africa, but much useful data for Kenyan and Tanzanian forest on limestone is contained in Hawthorne
(1984). Hawthorne (1984) mapped three types of
limestone. The most recently formed is that on the
coast: Neogene or quaternary coral rag, formed from
recently uplifted coral platforms and breccia. Further
inland is Jurassic oolitic limestone, weathered into
pinnacles and ridges (often known as karst). This
occurs mainly in southern Kenya (Kambe limestone)
and outcrops also near Tanga in northern Tanzania
(Tanga limestone). Finally, still further inland, and
further to the south, forming foothills to the crystalline Uluguru Mts, are the palaeozoic marble limestones of the Kimboza and Mandambala Hills in
Tanzania (Hawthorne 1984).
Table 2 documents all the known forested limestone outcrop locations in tropical Africa on which
Cola species occur. These are confined to only three
countries: Kenya, Tanzania and Mozambique. Of the
currently known 13 locations, 10 occur in Kenya
Longitude
(decimal degrees)
Altitude
(m)
Limestone type
Country
1. Dzitsoni to Jaribuni
2. Cha Simba
2. Cha Simba
3. Mwarakaya
4. Vipingo Buxton
5. Pangani
5. Pangani
5. Pangani
5. Pangani
6. Kambe Rocks
7. Kaya Kambe
7. Kaya Kambe
6. Kaya Kambe
8. Kaya Waa
8. Kaya Waa
9. Kaya Diani
10. Kaya Kinondo
11. Kimboza FR
11. Kimboza FR
11. Kimboza FR
11. Kimboza FR
3.666667
3.683333
3.716667
3.783333
3.8
3.85
3.85
3.85
3.85
3.866667
3.866667
3.866667
3.866667
4.2
4.2
4.266667
4.383333
7.016667
7.016667
7.016667
7.016667
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
S
39.73333
39.73333
39.7
39.68333
39.81667
39.66667
39.66667
39.66667
39.66667
39.65
39.65
39.65
39.65
39.6
36.6
39.58333
39.53333
37.8
37.8
37.8
37.8
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
150
200
200
140
10
80
80
80
80
80
150
100
150
10
15
7
5
450
0
450
220
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Coral Rag
Coral Rag
Coral Rag
Coral Rag
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Jurassic Limestone
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Kenya
Tanzania
Tanzania
Tanzania
Tanzania
11. Kimboza FR
12. Ruawa Forest
7.016667
9.970236
S
S
37.8
39.49222
E
E
225
427
13. Cheringoma
Gorges
18.750000
S
34.66667
E
180-200
Jurassic Limestone
Coral Rag (to be
confirmed)
Eocene Limestone
Cola Species recorded
Collector or
observer
Voucher
number
Luke
Luke
Luke
Luke
Luke
Luke
Luke
Luke
Luke
Luke
Robertson
Luke
Robertson
Pakia
Luke
Robertson
Robertson
Luke
Luke
Luke
Luke
6287
sr
1867
sr
4269
sr
1835
486
494
sr
4798
2893
4787
102
50
sr
4881
771
sr
772
7657
Tanzania
Tanzania
Cola sp.
Cola minor Brenan
Cola pseudoclavata Cheek
Cola pseudoclavata Cheek
Cola octoloboides Brenan
Cola minor Brenan
Cola porphyrantha Brenan
Cola pseudoclavata Cheek
Cola uloloma Brenan
Cola minor Brenan
Cola octoloboides Brenan
Cola pseudoclavata Cheek
Cola uloloma Brenan
Cola minor Brenan
Cola sp.
Cola minor Brenan
Cola pseudoclavata Cheek
Cola kimbozensis Cheek
Cola pseudoclavata Cheek
Cola quentinii Cheek
Cola greenwayi Brenan
var. greenwayi?
Cola uloloma Brenan?
Cola ruawaensis Cheek
Luke
Mbago
8814
2279
Mozambique
Cola cheringoma Cheek
Gomes e
Sousa
4441
(2019) 74:52
Site name
Latitude
(decimal
degrees)
KEW BULLETIN
Table 2. Limestone forest locations in Tropical Africa with Cola species. Sr = sight record. Incomplete, or, marked “?”, tentative identifications, are due to sterile material. Data from
Luke, with additions by Cheek.
Page 9 of 14
52
© The Author(s), 2019
52
Page 10 of 14
(Map 2). Forest on limestone outcrops appears to be
unknown in West and Congolian Africa. While continental Africa may have as much as 20% of its surface
with carbonate present according to remote sensing
studies (Williams & Fong 2016), most of this occurs
outside the tropical forest belt, particularly in North
and Saharan Africa, and in the arid NE. Those
carbonate areas which have been mapped in forest
areas e.g. in southern Nigeria, Cameroon or DRC
(Williams & Fong 2016), appear to be either so low in
concentration of carbonate, or so deeply buried under
soil, that they are not detectable to botanists and have
no impact on the vegetation above them (Cheek,
Luke, pers. obs. 1984 – 2018).
Additional forests on limestone, from which Cola have
not been reported, are few. The Kingupira forest in the
eastern Selous occurs on Jurassic limestone and extends for
c. 5 km2. However, this is a Groundwater Forest, where
moving water occurs close to the surface. In addition, a thin
layer of soil intervenes over the limestone (Vollesen 1980:
10 – 11). Therefore, this site may not equate to other forests
KEW BULLETIN
on limestone which are free-draining, and lack such soil
coverage. At least parts of Matumbi-Kichi-Tendaguru, near
Kilwa in coastal Tanzania had dry coastal forest in the
1980's and 90's (Vollesen pers. comm. to Cheek,
Sept. 2018), but these are not known to either survive, or
to have been well surveyed.
Numerous plant species have evolved to adapt to
the physiological challenges of growing on a limestone
substrate. Some can only grow on limestone (obligate
calcicole species) while others can grow both on and
off the substrate (facultative calcicoles). Obligate
calcicoles are often restricted to single or very few
limestone patches and so are narrowly endemic, such
as, in Gesneriaceae, Streptocarpus kimbozensis
B.L.Burtt.and Saintpaulia ionantha Wendl. subsp.
rupicola (B.L.Burtt) I.Darbysh. (Darbyshire 2006), or
in Meliaceae, Turraea kimbozensis Cheek (Cheek 1989)
and in Acanthaceae Isoglossa asystasioides I.Darbysh. &
Ensermu (Darbyshire & Ensermu Kelbessa 2007) and
Justicia lukei Vollesen (Darbyshire et al. 2010). The
highly restricted distribution of these species and the
Map 2. Distribution of the ten limestone forest locations with Cola in Kenya.
© The Author(s), 2019
(2019) 74:52
DESIGNED BY POPPY LAWRENCE.
KEW BULLETIN
Page 11 of 14
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Map 3. Distribution of all obligate and of key facultative forest calcicole Cola species in Africa.
threats that their habitat faces from tree-cutting for
timber or charcoal, quarrying of the limestone substrate for cement, building stone or marble, makes
them especially threatened. It is the geologically oldest
limestone area that has the greatest number of point
endemics: the 385 ha of the Kimboza forest have
eleven strictly endemic species (Cheek & Dorr 2007,
citing data mainly from Luke).
Cola cheringoma is only known from the Cheringoma
limestone area and is likely to be specific to the substrate
at this location. To the north, in Tanzania, just over the
border near Lindi, C. ruwaensis Cheek is also restricted,
52
DESIGNED BY POPPY LAWRENCE.
to an area of coastal limestone, while further north still,
C. kimbozensis Cheek, and C. quentinii Cheek are also both
obligate calcicoles, restricted to the palaeozoic marble
limestone of the Kimboza Forest in Tanzania which is
probably the richest site for forest limestone point
endemic plant species in tropical Africa (Cheek &
Dorr 2007: 31 – 32).
Cola uloloma Brenan, C. porphyrantha, Brenan,
C. octoloboides Brenan, C. pseudoclavata Cheek, and C. minor
Brenan of coastal Kenya and Tanzania are all facultative
calcicoles, occurring in forest both on limestone, usually but
not always coral rag, and off limestone, e.g. on volcanic
© The Author(s), 2019
52
Page 12 of 14
substrate (e.g. Cola octoloboides at Zombo in Kenya – Luke
pers. obs.). Fourteen other species of Cola in East Africa
(Uganda, Kenya and Tanzania) are not known to occur on
limestone (Cheek & Dorr 2007). The limestone Cola species
appear from their morphology to comprise four different
clades. Each putative clade, still to be supported by
molecular phylogenetic analysis, has one or more facultative
calcicole species and a single obligate calcicole species.
While Cola quentinii and C. porphyrantha are part of
the ‘Cola stelechantha’ group, C. ruwaensis and Cola
octoloboides form a distinctive and entirely morphologically separate, species-pair (Cheek & Dorr 2007). Cola
kimbozensis has no obvious connection to the foregoing
groups. Cola cheringoma appears to be a fourth
radiation onto limestone from a probable nonlimestone specific ancestor, possibly shared with the
geographically and morphologically close C. clavata
which is not known from limestone substrates, although the equally closely similar C. pseudoclavata
Cheek, and C. minor Brenan, are both facultative
calcicoles, from further north, in southern Kenya
and northern Tanzania (see Table 2 and Map 3).
At the moment, Cola cheringoma is the only endemic
plant species known from the Cheringoma limestone.
This is likely to be an artefact of under-collection.
With further targeted surveys to this habitat, additional
new calcicole species are likely to be discovered.
Acknowledgements
The impetus to resuscitate the revision of Cola was
provided by sponsorship via IUCN from the Toyota
Motor Corporation to the R.B.G., Kew Plant Assessment
Unit (PAU) to increase assessment output of plant
species. This resulted in support by Eimear Nic
Lughadha and Serene Hargreaves for an internship
specifically to assess the conservation status of Cola
species (Poppy Lawrence), necessitating renewed work
on species delimitation of that genus by the first author
to support these. Hermenegildo Matimele and Aurélio
Banze thank Camilla Sousa at LMA for her support, and
the Bentham Moxon Trust for funding their visit to Kew
in which they collected data contributing to this paper.
Thanks to Clayton Langa at LMA for finding the type
specimen and relating to us its annotations. Marc
Stalmans at Gorongosa National Park, David Goyder
and Bart Wursten are thanked for information on the
Cheringoma area. Barbara Turpin at BNRH kindly
provided scans of all specimens of Cola at her herbarium.
Peris Kamau at EA also kindly checked for duplicates of
the type. Alexandre Monro is thanked for discussions on
global limestone literature, Pablo Hendrigo for information on newly discovered Brazilian calcicoles, Iain
Darbyshire and Kaj Vollesen for data and discussions on
limestone and plants in Tanzania. Anne Marshall
expertly detected and retrieved relevant literature. Janis
© The Author(s), 2019
KEW BULLETIN
(2019) 74:52
Shillito is thanked for typing the manuscript, Isabel
Baldwin for software expertise, Marc Stalmans and
Laurence J. Dorr and an anonymous reviewer for
valuable comments on an earlier version of this paper.
Open Access This article is distributed under the
terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/
licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give appropriate credit to the original
author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes
were made.
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