Monograph of Coccinia (Cucurbitaceae)

Abstract

This monograph deals with all 95 names described in the Cucurbitaceae genus Coccinia and recognizes 25 species. Taxonomic novelties are Cocciniaadoensisvar.aurantiaca (C.Jeffrey) Holstein, stat. nov., Cocciniasessilifoliavar.variifolia (A.Meeuse) Holstein, stat. nov., and Cocciniaadoensisvar.jeffreyana Holstein, var. nov. For the 25 species 3157 collections were examined, of which 2024 were georeferenced to produce distribution maps. All species are distributed in sub-Saharan Africa with one species, Cocciniagrandis, extending from Senegal in West Africa east to Indonesia and being naturalized on Pacific Islands, in Australia, the Caribbean, and South America. Coccinia species are dioecious creepers or climbers with simple or bifid tendrils that occupy a range of habitats from arid scrubland, woodlands to lowland rainforest and mist forest. The corolla of Coccinia species is sympetalous, usually pale yellow to orange, and 1 to 4.5 cm long. Pollination is by bees foraging for pollen or nectar. After pollination, the developing ovary often exhibits longitudinal mottling, which usually disappears during maturation. All species produce berries with a pericarp in reddish colors (orange-red through to scarlet red), hence the generic name. The globose to cylindrical fruits contain numerous grayish-beige flat to lenticular seeds. Chromosome numbers are 2n = 20, 24, and 22 + XX/XY. Many Coccinia species are used for food, either as roasted tubers, greens as spinach, or the fruits as vegetables. Medicinal value is established in Cocciniagrandis, of which leaves and sap are used against diabetes.

Keywords: Coccinia; Cucurbitaceae; biogeography; molecular phylogeny; morphology; sex expression; taxonomy; useful plants.

Figure 1.

a Young plant of Coccinia grandis. The hypocotyl is already thickened and lignifies later-on to a tuber. The cotyledons are glabrous, have an entire margin and an obtuse apex b Adventitious root on Coccinia grandis; the beige structure to the left is a dry tendril.

Figure 2.

a Female flower bud of Coccinia microphylla (N. Holstein et al. 90); picture taken during the dry season. The stem is completely lignified, and only green short shoots are produced b Male plant of Coccinia sessilifolia. The stem is glaucous and does not lignify. Unusually, the bract is 3-lobate leaf-like.

Figure 3.

Trichomes on Coccinia species. a Node of Coccinia adoensis var. jeffreyana (J.C. Lovett 1197). The black bar equals 1 mm. b Part of a leaf Coccinia adoensis var. jeffreyana (A.F. Stolz 504). The white bar equals 1 mm. c Glandular trichome from Coccinia grandis.

Figure 4.

a Young plant of Coccinia abyssinica (N. Holstein 132). The first node is in the axilla where the glabrous cotyledons split off. The first nodes lack probracts and tendrils b Young plant of Coccinia sessilifolia (N. Holstein 131). The first leaves in this species are petiolate, sessile leaves are produced later-on. The glabrous cotyledons are already dried (plant had the same age as the one in Fig. 4a).

Figure 5.

a Cross-section of a petiole of Coccinia grandiflora, stained with astra blue and safranin (3:2). The bicollateral vascular bundles are arranged in a U-shape b Trichome on the adaxial ridge of a cross-section of a petiole of Coccinia grandiflora. Although not visible by naked-eye, the petiole is also covered with few-celled glandular trichomes c Young plant of Coccinia adoensis var. jeffreyana. The trichomes are mainly occurring on the prominent veins. The adaxial side of the petiole bears smaller trichomes on the ridges, which fade into the leaf margin.

Figure 6.

Leaf shape variability in Coccinia senensis. a H.J. Schlieben 5259 (HBG) b E.M.C. Groenendijk et al. 1031 (WAG) c A.R. Torre et al. 18788 (MO). Black bars equal 1 cm.

Figure 7.

a Male flower of Coccinia grandis (N. Holstein 37). Apices of the petals and calyx lobes, as well as major teeth on the leaf margin are colored in red. Minor margin teeth are inconspicuously colored. The calyx lobes in Coccinia grandis are spreading in flower buds and reflexed in mature flowers b Male plant of Coccinia sessilifolia. Darkish glands (extranuptial nectaries) are commonly found at the base of a lower leaf lamina. The calyx lobes are unusually large in this specimen (cp. Fig. 2b).

Figure 8.

a The probract of Coccinia grandiflora is fleshy and has a keel. The abaxial side bears many extranuptial nectaries. The structure pointing to the lower left of the picture is the tendril b The probract of Coccinia trilobata (sampled as N. Holstein & P. Sebastian 9) is spoon-shaped, papery, and without a keel.

Figure 9.

Leaky dioecy in a plant of Coccinia megarrhiza. The plant was flowering male (the bud on the left) through the season, but a single female flower developed (the second flower on this node was male). The flower was receptive and produced a normal-sized fruit and normal-shaped seeds. The probracts (left node) are spoon-shaped, the tendrils are purplish.

Figure 10.

a Male plant of Coccinia rehmannii [aff. var. littoralis] (N. Holstein 126). The plant was raised from seeds of a female plant with ovoid fruits (B. Jarret – pers. comm.) b Male flower of Coccinia adoensis var. aurantiaca (N. Holstein et al. 85). The halictid bee (H. Schaefer – pers. comm.) circled around the globose anther head harvesting pollen. The scent of the flower was strong and honey melon-like.

Figure 11.

a Longitudinal section of a female Coccinia hirtella flower (size of the small squares is 1 mm²). Perianth and style were detached. The pollen sacs on the staminodes are highly reduced. The introrse side of the staminodes bears long trichomes that in intact flowers touched the style b Female flower of Coccinia rehmannii var. rehmannii with bilobate stigma arms c Female flower of Coccinia megarrhiza with bulging stigma arms.

Figure 12.

a Cross-section through an ovary of Coccinia hirtella. The ovules are anatropous with the micropyle facing outwards b Cross- and longitudinal section of a Coccinia megarrhiza fruit. The seeds are enclosed in a hyaline hull (aril) and seemingly attached to the periphery c Cross-section through a fruit of Coccinia sessilifolia. Note that the vascular bundles in the lower left of the picture bend in the periphery, so the placentation is not parietal but involute.

Figure 13.

a Ripening fruit of Coccinia hirtella. Note the typical lobulate leaves of this species in the lower right b Ripening fruit of Coccinia sessilifolia. The fruit, like the plant, bears a waxy bloom c Ripening fruits of Coccinia megarrhiza have a dark green halo around the white longitudinal mottling. The left fruit is derived from pollination with Coccinia megarrhiza pollen, whereas the smaller fruit on the right is derived from cross-pollination with Coccinia trilobata (both pollinations were conducted on the same day).

Figure 14.

Seeds of Coccinia. The lack of fibers in e and f are preparation artifacts due to mechanical removal of the hyaline aril. Maceration (coarse crushing of the fruit and soaking of the mass in water for 2–3 weeks; R. Brüggemann – pers. comm.) retains the surface fibers. Length of white bars equals 1 mm. a Seeds of Coccinia adoensis var. jeffreyana (plant derived from seed of the same fruit: N. Holstein 130). Note the lenticular face and symmetrical shape of the seed b seeds of Coccinia abyssinica (plant derived from seed of the same fruit: N. Holstein 120 and 132) c Seeds of Coccinia trilobata d Seeds of Coccinia sessilifolia (harvested by maceration) e Seeds of Coccinia sessilifolia (harvested by mechanical extraction; taken from N. Holstein 119) f Seeds of Coccinia grandis (harvested by mechanical extraction).

Figure 15.

Chromosome preparations fixed in 3:1 EtOH – acetic acid and stained with orcein, objective lens: 100×. a Mitotic plate of a male Coccinia grandis (2n = 22 + XY) b Mitotic plate of a male plant of Coccinia hirtella (2n = 24) c Phase contrast image of a mitotic plate of a male plant of Coccinia sessilifolia (2n = 24).

Figure 16.

Hybrids of Coccinia species. a Coccinia grandis ♀ × Coccinia hirtella ♂ b Coccinia hirtella ♀ × Coccinia grandis ♂ c Coccinia grandis ♀ × Coccinia pwaniensis ♂; note that the pollen sacs are not open although the flower is in full bloom indicating sterility d Left flower: male Coccinia sessilifolia, right flower: male flower of Coccinia grandis ♀ × Coccinia sessilifolia ♂ (Coccinia grandis flowers are about equally sized as Coccinia sessilifolia).

Figure 17.

Phylogenetic relationships in Coccinia based on five plastid DNA loci (matK, ndhF–rpl32 intergenic spacer (IS), rpl20–rps12 IS, trnL intron, trnL–trnF IS, trnS–trnG IS) obtained for 75 accessions from 24 species. Shown is the topology of the 50% majority rule consensus tree obtained from Bayesian analysis including simple gap coding for ingroup InDels. Numbers above the branches are posterior probability values ≥ 0.98 with values “with InDel coding” first, followed by “without InDel coding.” Numbers below the branches are bootstrap support values from ML analysis. Topologies from the different analyses were not contradictive, although some clades were not resolved without gap coding. Roman numbers indicate clades as discussed in the text: I = Coccinia adoensis clade, II = Coccinia quinqueloba group, III = Coccinia barteri clade, and IV = Coccinia rehmannii clade.

Figure 18.

Phylogenetic relationships in Coccinia based on 505 nucleotides of the nuclear LEAFY-like 2^nd intron, obtained for 37 accessions from 23 species analyzed under maximum likelihood (ML) and the GTR + Γ model. Numbers below branches refer to ML bootstrap support > 80% from 1000 replicates. The dots at nodes and behind the two accessions refer to uniquely shared indels. Roman numbers indicate clades as discussed in the text: I = Coccinia adoensis clade, II = Coccinia quinqueloba group, III = Coccinia barteri clade, and IV = Coccinia rehmannii clade.

Figure 19.

Scenario of evolution in the Coccinia adoensis clade. The green line surrounds today’s distribution of Coccinia adoensis. Blue lines surround today’s distributions of Coccinia senensis and Coccinia pwaniensis. Blue arrows indicate peripatric speciation without shift in precipitation preference. Yellow arrows indicate speciation with shifts towards more arid habitats. Black arrows indicate speciation with shift towards more humid habitats.

Figure 20.

Distribution map of Coccinia abyssinica (pale yellow dots; based on 23 collections) and Coccinia megarrhiza (blue dots; based on 28 collections). For Ethiopia the borders of the regions are given.

Figure 21.

Male inflorescence and leaf of Coccinia adoensis; picture taken from lectotype (G.H.W. Schimper 166 (P00346261)). Note the short bent trichomes, which are a good indicator for this species (but glabrous collections or other kinds of trichomes may occur in this species, too).

Figure 22.

Distribution map of Coccinia adoensis var. adoensis (based on 311 collections).

Figure 23.

Distribution map of Coccinia adoensis var. aurantiaca (pale yellow triangles; based on 18 collections), Coccinia adoensis var. jeffreyana (pale yellow dots; based on 18 collections), Coccinia pwaniensis (blue triangles; based on 11 collections, including a natural hybrid), and Coccinia senensis (blue dots; based on 30 collections). For Tanzania the borders of the regions are given.

Figure 24.

Distribution map of Coccinia barteri (based on 99 collections).

Figure 25.

Distribution map of Coccinia grandiflora (based on 62 collections). For Tanzania the borders of the regions are given.

Figure 26.

Partial distribution map (Africa to Australia) of Coccinia grandis (based on 629 collections).

Figure 27.

Partial distribution map (Pacific Ocean and Americas) of Coccinia grandis (based on 629 collections). State borders are given for the USA.

Figure 28.

Reconstruction of the habit of a female raceme of Coccinia heterophylla based on T.-J. Klaine 414 (P). Black bar equals 0.5 cm.

Figure 29.

Distribution map of Coccinia heterophylla (based on 19 collections).

Figure 30.

Distribution map of Coccinia hirtella (pale yellow dots; based on 22 collections), Coccinia mackenii (blue triangles; based on 50 collections), and Coccinia quinqueloba (blue dots; based on 38 collections). For South Africa the borders of the provinces are given.

Figure 31.

Distribution map of Coccinia intermedia (pale yellow dots; based on 4 collections), Coccinia keayana (blue dots; based on 23 collections), and Coccinia longicarpa (blue triangles; based on 22 collections).

Figure 32.

Reconstruction of the habit of Coccinia keayana based on C.C.H. Jongkind et al. 6542 (WAG). Black bar equals 1 cm.

Figure 33.

Distribution map of Coccinia microphylla (blue dots; based on 49 collections) and Coccinia trilobata (pale yellow dots; based on 51 collections).

Figure 34.

Distribution map of Coccinia mildbraedii (based on 51 collections). The individual in Kenya is introduced. For Tanzania the borders of the regions are given.

Figure 35.

Distribution map of Coccinia ogadensis (blue dots; based on 8 collections) and Coccinia samburuensis (pale yellow dots; based on 4 collections). For Ethiopia the borders of the regions and for Kenya the borders of the provinces are displayed.

Figure 36.

Distribution map of Coccinia racemiflora (blue dots; based on 8 collections, including 1 supposed hybrid).

Figure 37.

Distribution map of Coccinia rehmannii (blue dots; based on 251 collections). For South Africa the borders of the provinces are given.

Figure 38.

Distribution map of Coccinia schliebenii (pale yellow dots; based on 27 collections). For Ethiopia and Tanzania the borders of the regions are given.

Figure 39.

Inflorescence of a male Coccinia senensis, note the long triangulate (may be narrower in other collections, then subulate) calyx lobes in contrast to the calyx lobes of Coccinia adoensis var. adoensis in Fig. 21; picture taken from the neotype (H.J.E. Schlieben 5259 (M)). Black bar equals 1 cm.

Figure 40.

Distribution map of Coccinia sessilifolia var. sessilifolia (pale yellow dots; based on 133 collections) and Coccinia sessilifolia var. variifolia (blue dots; based on 7 collections). For South Africa the borders of the provinces are given.

Figure 41.

Distribution map of Coccinia subsessiliflora (blue dots; based on 18 collections). For D.R. Congo the borders of the provinces (until 1988) are given.