Research Article |
Corresponding author: Samah A. Alharbi ( sarehaily@uqu.edu.sa ) Academic editor: Peter Bruyns
© 2021 Samah A. Alharbi, Rahmah N. Al-Qthanin.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Alharbi SA, Al-Qthanin RN (2021) Taxonomic revision of Ceropegia sect. Huernia (Asclepiadoideae, Apocynaceae) in Saudi Arabia with three new combinations. PhytoKeys 174: 47-80. https://doi.org/10.3897/phytokeys.174.58867
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This study provides a taxonomic revision for Ceropegia sect. Huernia in the flora of Saudi Arabia. Forty-six quantitative and qualitative morphological characters were analysed using principal component analysis (PCA), principal coordinates analysis (PCoA) and the unweighted pairs group using mean average (UPGMA) to separate and help delimit taxa. We propose to reduce the number of species reported in Saudi Arabia from 11 to four: C. khalidbinsultanii comb. nov., C. laevis, C. lodarensis and C. macrocarpa. This study also suggested reducing two names to varietal level under C. lodarensis (var. foetida comb. nov. and var. rubrosticta comb. nov.). A key to the species, detailed morphological descriptions, illustrations, distribution maps, ecology, etymology and preliminary conservation assessments are provided that follow IUCN criteria.
Arid plants, flora of Saudi Arabia, Huernia, stapeliads, stem-succulent
The stapeliads, essentially stem-succulent leafless members of the tribe Ceropegieae (Asclepiadoideae, Apocynaceae), comprise 357 species placed in 31 genera. All of these were reduced to sections of Ceropegia after a broad circumscription of the genus, based on a recent molecular study (
Ceropegia sect. Huernia (R.Br.) Bruyns (formerly the genus Huernia R.Br.) has the widest distribution of all stapeliads, extending from west of Al-Madinah in Saudi Arabia, north of the Tropic of Cancer, to near Cape Town in South Africa, to the south of the Tropic of Capricorn (
In Saudi Arabia, sect. Huernia is restricted to the mountainous area of the western and south-western part of the country (the mountains of Sarat and Hejaz) (
Plowes’ classification of Saudi Arabian Huernia needs further investigation. His taxonomic treatment of several taxa was based on a single photo (e.g. H. decaloba) or a single specimen (e.g. H. anagaynensis, H. radhwana, H. foetida, H. khalidbinsultanii). Furthermore, morphological characters used by Plowes are not strong enough for delimiting species within sect. Huernia. For example, corolla tube size and its exterior colour, the number of flowers in the inflorescence and flower odour were used as diagnostic characters to separate H. anagaynensis, H. radhwana and H. asirensis. Observations of the first author have shown that such characters are not constant in this complex group. In addition, Plowes’ description of the species is not sufficiently detailed and is not even clearly enough illustrated for one to distinguish between these closely-related species. Moreover, it is unclear how the Saudi Huernias are distinguished from closely-allied species, such as H. boleana and H. lodarensis. There is, therefore, a need for much more sampling and detailed examination before a conclusive taxonomic statement on Saudi Arabian Huernia can be made.
Remarkably, sect. Huernia has received little taxonomic attention in Saudi Arabia, other than Plowes’ work. Taxonomic revision of this plant group in Saudi Arabia is urgently needed. Plants of sect. Huernia are commonly used for diabetes treatments in traditional medicine in the western and south-western regions of Saudi Arabia (
The objectives of the present study are: 1) to revise Ceropegia sect. Huernia in the flora of Saudi Arabia, 2) to examine morphological characters in detail and try to find new ones that can be used in the classification of the section in Saudi Arabia, 3) to investigate the relationship between Saudi Arabian Huernia and other allied species in the Arabian Peninsula and 4) to provide a diagnostic key for the species in Saudi Arabia. This will enable us to test whether the taxonomic treatment in
Twenty individuals of H. asirensis and H. collenetteae were sampled from the Ash Shafa area in Al-Taif Province, western Saudi Arabia (21°3.6583'N, 40°20.1917'E) during several expeditions to the area between September 2010 and May 2011. Specimens were preserved for each collection in a mixture of Formalin, Glycerol and Water (in the ration 2:1:20). Herbarium specimens were then made from this preserved material as described in
The morphological characters were examined and recorded from the available specimens (one H. anagaynensis, 12 H. asirensis, 10 H. collenetteae, one H. foetida, one H. laevis, one H. radhwana, one H. rubrosticta and one H. saudi-arabica). Since some characters are difficult to interpret in dry specimens, dried specimens of H. collenetteae, H. rubrosticta and H. saudi-arabica are excluded from the morphometric analysis. For species where material was unavailable, such as H. arabica and H. khalidbinsultanii and the closely-related species from Ethiopia and the Arabian Peninsula H. boleana and H. lodarensis, measurements and character-states have been extracted from the relevant literature (
Nineteen quantitative morphological characters used in morphometric analysis of Ceropegia sect. Huernia in Saudi Arabia. All measured in mm.
No. | Character | No. | Character |
---|---|---|---|
1 | length of branches | 11 | diam. of corolla tube at mouth |
2 | length of tubercles on branches | 12 | length of papillae in throat of corolla (max.) |
3 | width of base of tubercles | 13 | thickness of papillae at base |
4 | number of flowers per inflorescence | 14 | length of intermediate lobes |
5 | length of pedicel | 15 | length of corolla lobe |
6 | diam. of pedicel | 16 | width of corolla lobe at base |
7 | length of sepals | 17 | diam. of outer corona |
8 | width at base of sepals | 18 | length of inner corona |
9 | diam. of corolla | 19 | width of Inner corona at base |
10 | length of corolla tube |
Twenty-seven qualitative morphological characters and character states used in morphometric analysis of Ceropegia sect. Huernia in Saudi Arabia.
Qualitative characters were coded as multi-state, for example (1. cream, 2. shiny creamy-yellow, 3. white). Quantitative variables were standardised using the R studio version (2017) scale balance function to remove bias due to size alone, following
To assess the conservation status of each taxon, the guidelines for the IUCN Red List Categories and Criteria version 13 (
The data underpinning the analyses reported in this paper are deposited at GBIF, the Global Biodiversity Information Facility: https://doi.org/10.15468/6n2rgz.
The first two axes of PCA accounted for 74.7% of the overall variation (Fig.
Cluster analysis by UPGMA of quantitative and qualitative data indicated the presence of four clearly-distinguished groups: Group 1, with H. arabica and H. laevis is the furthest away from all other groups; Group 2, consisting of H. asirensis, H. anagaynensis, H. khalidbinsultanii, H. radhwana, H. foetida and H. rubrosticta; Group 3, with H. lodarensis and H. boleana; and Group 4, with H. collenetteae and H. saudi-arabica (Fig.
Unweighted pair-group method with arithmetic mean (UPGMA) phenogram resulting from cluster analysis. Explanations: Ar-Huernia arabica, La- H. laevis, Kh- H. khalidbinsultanii, Ra- H. radhwana, An- H. anagaynensis, As- H. asirensis, Ru- H. rubrosticta, Fo- H. foetida, Lo- H. lodarensis, Bo- H. boleana, Sa- H. saudi-arabica, Co- H. collenetteae.
PCoA separated 33 specimens into four distinct groups, corresponding largely to those obtained by UPGMA. Group 1 and 2 represent H. arabica and H. laevis, respectively, which were well-separated from the others. Accessions of H. asirensis were clustered together in one group and weakly separated from H. anagaynensis, H. radhwana, H. foetida and H. khalidbinsultanii. Accessions of Huernia collenetteae and H. saudi-arabica were grouped in one cluster in the positive axes and weakly separated from individuals of H. rubrosticta, H. lodarensis and H. boleana (Fig.
The most important characters, contributing to the separation of the groups, were corolla characteristics (corolla shape, corolla tube diam. and shape, corolla lobes spreading, corolla colour patterns and papillae shape) and corona characteristics (outer corona shape, diam. and lobe shape; inner corona length, apex and dorsal gibbosity) Table
Eigenvalues in two principal components (PC1 and PC2) of value relative to 46 morphological characters of sect. Huernia in Saudi Arabia.
Characters | PC1 | PC2 |
---|---|---|
width of base of tubercles (mm) | 0.078 | -0.038 |
length of branches (mm) | 0.003 | -0.107 |
length of tubercles on branches (mm) | 0.050 | 0.254 |
stem grooves between tubercle rows | 0.132 | -0.208 |
flower smell | -0.079 | -0.317 |
number of flowers per inflorescence | 0.014 | -0.023 |
flowers opening | -0.025 | -0.261 |
length of pedicel (mm) | 0.171 | 0.053 |
diam. of pedicel (mm) | 0.162 | 0.019 |
pedicel tapering toward the point of flower attachment | 0.139 | -0.077 |
pedicel growth direction | 0.194 | 0.268 |
length of sepals (mm) | 0.141 | -0.202 |
width at base of sepals (mm) | 0.125 | -0.043 |
corolla shape | -0.252 | 0.009 |
corolla lobe apex groove | 0.036 | 0.027 |
corolla inside surface texture | -0.085 | 0.072 |
corolla tube | 0.160 | -0.215 |
shape of papillae inside corolla | 0.241 | 0.092 |
thickness of papillae at base | 0.160 | 0.074 |
corolla inside (background colour) | 0.171 | 0.142 |
corolla inside (colour pattern) | -0.108 | 0.011 |
corolla exterior (colour pattern) | 0.076 | -0.224 |
corolla tube interior (colour pattern) | 0.158 | 0.153 |
corolla lobes colour | 0.075 | -0.158 |
corolla lobes spreading | 0.172 | 0.011 |
width of base of tubercles (mm) | 0.128 | 0.229 |
corolla lobe shape | 0.194 | 0.110 |
diam. of corolla | 0.089 | 0.022 |
length of corolla tube (mm) | 0.198 | -0.139 |
diam. of corolla tube at mouth (mm) | 0.209 | -0.045 |
length of intermediate lobe (mm) | 0.156 | 0.004 |
length of corolla lobe (mm) | 0.186 | -0.085 |
width of corolla lobe at base (mm) | 0.131 | -0.077 |
outer corona colour | 0.043 | 0.056 |
outer corona shape | -0.031 | -0.237 |
outer corona lobe shape | 0.091 | -0.259 |
outer corona lobe apex | 0.164 | 0.058 |
outer corona fleshy tubercle | -0.039 | -0.075 |
diam. of outer corona (mm) | 0.216 | 0.080 |
inner corona shape | 0.219 | -0.183 |
length of inner corona (mm) | 0.244 | 0.054 |
width of inner corona at base (mm) | 0.173 | -0.029 |
inner corona dorsal gibbosity | 0.255 | 0.071 |
inner corona base end | 0.214 | -0.210 |
inner corona apices | 0.031 | -0.265 |
inner corona apex texture | 0.100 | -0.072 |
In the experience of the present authors, sect. Huernia is a difficult group in the flora of Saudi Arabia and it has not received adequate attention. Perhaps the most comprehensive account is
In the multivariate analysis, accessions of H. radhwana (Fig.
In 2005, Bruyns reduced H. khalidbinsultanii to a synonym under H. lodarensis; here, the two taxa are differentiated according to the shape of the papillae and the corolla (see the key in the next section). In sect. Huernia, the shape of the papillae provides an important character when it is combined with other characters, such as inner corona and the shape of the corolla is the most important character indicative of the relationship between species (
Huernia collenetteae and H. saudi-arabica accessions overlapped in one cluster in both the UPGMA (Fig.
Huernia saudi-arabica (Fig.
The numerical analysis carried out in this study did not resolve the relationship between H. lodarensis, H. boleana, H. foetida and H. rubrosticta and the other species. This is probably due to the low number of specimens included in the analysis and the incomplete nature of the data obtained from literature for H. lodarensis and H. boleana. However, a thorough examination of H. foetida (Fig.
The delimitation of H. arabica (Fig.
In order to know the extent of variability within taxa, examining as many samples as possible is crucial. Our results show that the major weakness of previous taxonomic accounts of the Arabian members of sect. Huernia, particularly in Saudi Arabia, was caused by the fact that the taxa were described from single or only very small numbers of plants. This led to the recognition of many unnatural taxa, as seen in some of
Based on recent phylogenetic reconstructions in the Ceropegieae, the species of Huernia were transferred to Ceropegia, where they were placed under sect. Huernia and over 50 new combinations were made (
≡ Huernia R.Br., Mem. Wern. Nat. Hist. Soc.: 22 (1810). Lectotype
Huernia campanulata
(Masson) Haw. (designated by
= Ceropegia clavigera (Jacq.) Bruyns.
Perennial leafless dwarf succulent herb, mat-forming rarely rhizomatous, sometimes prostrate or pendulous succulent. Branches glabrous, smooth, 4- to 16-angled. Leaves reduced mainly to soft point without stipular structures. The leaf-rudiments are borne on a raised tubercle which is a much swollen leaf-base. These tubercles are arranged in rows along the branch and joined towards their bases into angles along the branch with a groove between vertical rows of tubercles. Inflorescence glabrous, usually only one per branch, arising mainly in lower half of branch between tubercles, 1–10 flowered. Corolla urceolate to campanulate to subrotate, shallowly lobed. Staminal corona in two well-separated series, inner pressed to backs of anthers mostly exceeding them and meeting in centre, often with prominent transversely-rounded dorsal projections. Outer spreading along base of tube, discrete to fused into spreading disc with fleshy tubercle beneath guide-rail obscuring entrance to small nectarial cavity. Anthers horizontal on top of style-head, margins shrinking back to expose pollinia, rectangular. Pollinium ellipsoidal, longer than broad, insertion-crest exactly along outer edge, caudicle attached with broad cupular pad to base. Follicles erect, terete-fusiform, obclavate, slender, consisting of two horns diverging at 30–60°, longitudinally mottled with narrow broken purple stripes, glabrous, smooth (
1 | Corolla inside glabrous or covered with papillae ≤ 1 mm long; inner corona lobes not or shortly exceeding anthers, not tapering to a fine point | 2 |
– | Corolla inside densely covered with papillae > 1 mm long; inner corona lobes much exceeding anthers, tapering to a fine point | 3 |
2 | Corolla bowl-shaped, papillate, uniformly purplish-maroon without annulus around mouth of tube | C. macrocarpa |
– | Corolla funnel-shaped, glabrous, shiny with irregular broad red streaks on a yellowish background with an annulus-like structure around mouth of tube | C. laevis |
3 | Tubercles on branches up to 16 mm long; corolla covered with slender (hair-like) papillae, tubular-campanulate, lobes ascending | C. khalidbinsultanii |
– | Tubercles on branches up to 12 mm long; corolla covered with conical compressed papillae, campanulate, lobes spreading or reflexed | C. lodarensis |
≡ Huernia macrocarpa Sprenger, Cat. Dammann & Co. 59: 4 (1892) Type: Eritrea • Penzig s.n. (K epitype).
= Huernia macrocarpa var. arabica (N. E. Brown) A. C. White & B. Sloane (1937)
= Huernia macrocarpa var. penzigii (N. E. Brown) A. C. White & B. Sloane (1937)
= Huernia macrocarpa var. schweinfurthii (A. Berger) A. C. White & B. Sloane (1937)
= Huernia penzigii N. E. Brown (1892)
= Huernia penzigii var. arabica (N. E. Brown) A.
= Huernia penzigii var. schimperi A.
= Huernia penzigii var. schweinfurthii A.
Dwarf succulent forming dense clump. Branches 60 mm long, non-rhizomatous, erect, decumbent, grey-green mottled with purple-red; tubercles up to 10 mm long (including leaf-rudiment), conical, spreading, laterally flattened and joined into 5 angles along branch, each tipped with a soft slender acuminate caducous leaf-rudiment. Inflorescence usually only 1 per branch, arising in lower half of branch, each bearing 2–3 flowers developing mainly successively, flowers with no unpleasant smell; pedicel spreading and holding flower facing horizontally. Corolla 15 mm diam., shallow bowl shape; outside smooth, cream-speckled with maroon, with 1 heavy (+ 2 lighter) raised longitudinal veins running from lobes to base of tube; inside uniformly coloured with purplish-red, covered except in lower third of tube with very small wart-like papillae; tube cupular; lobes ascending, deltoid, acuminate. Corona without basal stipe; outer lobes spreading on base of tube and fused partially to it, discrete to 5-lobed with each lobe subquadrate emarginate or slightly crenate, blackish-maroon; inner lobes maroon, adpressed to backs of anthers exceeding them and meeting in centre, dorsiventrally flattened around laterally broadened base becoming terete above and tapering gradually to obtuse bristly apex, a transversely conspicuously gibbous, broadened at the base with an acute end.
Rare, known only from Asir between Abha and Jabal Sawdah, SW Saudi Arabia (
Somaliland, Sudan, Eritrea, Ethiopia, South west Arabian Peninsula (Saudi Arabia, Yemen) (
Growing amongst granitic rocks and scattered shrubs on a steep hillside at 2700 m alt. (
This species can be easily distinguished from other members of sect. Huernia in Saudi Arabia by the small maroon bowl-shaped flowers.
Macrocarpus (Greek) 'makros', large; and 'karpos', fruit (
The species is known only from one location near Sawda Mountain; the estimated EOO and AOO of 8 km2 would place the species in the Critically Endangered (CR) status. However, little is known about the size of the population and possible threats. Therefore, Data Deficient (DD) is assigned to this species.
Ethiopia, Gilbert 2945 (E [fl in spirit])
≡ Huernia khalidbinsultanii Plowes & McCoy, Cact. Succ. J. (Los Angeles) 75(1): 19 (2003). Type: Saudi Arabia – Asir • T.A. McCoy 2446 (holotype: MO; isotypes P & SRGH); 25 km SW of Khamis Mushayt; 18°4.0906'N, 42°43.8908'E; alt. 2100 m; 15 Jan 1999.
= Huernia asirensis Plowes, Asklepios 114: 7 (2012), syn. nov. Type: Saudi Arabia – Tanumah • I.S. Collenette 2655 (Holotype: K!, [fl in spirit: 44279.000]); 12 km S. of An Numas on Taif to Abha Road;18°56.1481'N, 42°11.2139'E; alt.1800 m; 10 May 1981.
= Huernia radhwana Plowes, Asklepios 114: 10 (2012), syn. nov. Type: Saudi Arabia – Jabal Radhwa • I.S. Collenette 5944 (Holotype: K!, [fl in spirit: 51187.000]); 75 km NE Yanbu; 24°32.3717'N, 38°20.4741'E; alt. 1750 m; 01 Feb 1987.
= Huernia anagaynensis Plowes, Asklepios 114: 7 (2012), syn. nov. Type: Saudi Arabia – Jabal Anagayn • I.S. Collenette 5970 (Holotype: K!, [fl in spirit: 50937.000]); 95 km south of Madinah; 23°21.5747'N, 39°34.9766'E; alt. 1371 m; 06 Dec1986.
Huernia haddaica Al-Hemaid (nom. inval. Art 37.2), Saudi J. Biol. Sci. 8: 168 (2001).
Dwarf succulent forming dense clump. Branches 50–100 mm long, non-rhizomatous, decumbent, grey-green mottled with purple-red; tubercles 7–16 mm long (including leaf-rudiment), 1.5–5 mm broad at base, conical, spreading, laterally flattened and joined into 5 angles along stem, each tipped with a soft slender acuminate caducous leaf- rudiment. Inflorescence usually only 1 per branch, arising in lower half of branch, each bearing 1–7 flowers developing mainly simultaneously or in gradual succession from short peduncle, with several filiform bracts without lateral teeth, flowers with mainly very foetid odour, rarely faint or no unpleasant smell; pedicel 5–21.5 mm long, 1–2 mm thick, spreading and holding flower facing horizontally, tapering sometimes toward the point of flower attachment; sepals 10–18 mm long, 1–2 mm broad at base, attenuate. Corolla 27–47 mm diam., tubular-campanulate to campanulate; outside smooth, white to creamy-white or cream speckled with pale maroon spots uniformly scattered, sometimes spots become darker especially on the lower or upper half of corolla tube, with 1 heavy (+ 2 lighter) raised longitudinal veins running from lobes to base of tube; inside creamy-white to cream with irregular-shaped narrow short maroon lines and dashes changing to narrow concentric broken lines in lower half of tube, covered except in lower third of tube with slender (hair-like) papillae densely crowded around mouth of tube (up to 3 mm long and 0.75 mm an base in tube mouth), each tipped by minute apical acuminata bristle; tube 7–13 mm long, 9–14 mm broad at mouth, pentagonal; lobes 13–18 mm long, 8–12 mm broad at base, ascending to slightly spreading, narrowly deltoid and usually longer than wide, attenuate usually concave or form channel above, intermediate lobes 1–2.5 mm long. Corona without basal stipe; outer lobes (4.5–8 mm diam.) spreading on base of tube and fused partially to it; fused together into disc with crenate margin to a slightly disc-like with rounded to subquadrate short and broad lobes, rarely discrete to 5-lobed with each lobe subquadrate mucronate, blackish maroon; inner lobes 3–5.5 mm long, 0.5–1.5 mm at base, ivory white sometimes mottled with a few maroon spots at the tips, adpressed to anthers in their lower half then rising up connivent and then diverging towards apices, dorsiventrally flattened around laterally-broadened base becoming terete above and tapering gradually to a slender fine minutely-scabrous apex, at base with inflated transversal dorsal gibbosity with rounded to acute end. Pollinia 0.1–0.7 mm long.
Scattered over a wide area, extending from Khamis Mushait in SW of the country to Jabal Radhwa, 75 km north of Yanbu in the Western Region.
Probably endemic to SW Arabian Peninsula, known so far from Saudi Arabia only.
Growing on granitic outcrops often under shrubs, from 1800–2100 m alt. Flowering Dec.-May
Ceropegia khalidbinsultanii is best distinguished from the closely-related C. lodarensis by longer tubercles (up to 16 mm) on the branches and the smaller, white to creamy-white tubular-campanulate corolla streaked with narrow maroon lines, slender (hairy) papillae and a very foetid odour.
The foetid odour of the flower becomes weak or completely vanishes after all pollinia have been removed from the flower.
Khalidbinsultanii for Prince Khalid bin Sultan bin Abdulaziz M., a former Saudi Deputy Minister of Defence (
Near Threatened (NT) has been assigned to Ceropegia khalidbinsultanii, based on the species’ EOO of 41,490 km2 and AOO of 2,012 km2 and the current threats of habitat transformation (roads and housing construction), population fragmentation and tourism.
Ceropegia khalidbinsultanii A Alharbi S00 (H. asirensis) B Alharbi S10b (H. asirensis) C Alharbi S4a (H. asirensis) D Collenette 5944, Jabal Radhwa, (H. radhwana, Type) E Alharbi S16a (H. asirensis) F Collenette 1309, Al-Baha, (H. asirensis, Type) G Collenette 5970, Jabal Anagyan (H. anagaynensis, Type) H ex Tom McCoy KSA129 sub DP8384, 25 km SW of Khamis Mushayt, (H. khalidbinsultanii, Type) I follicles, Alharbi S14a. (A–C, E, I) photo by the first author from Wadi Thee Gazal, Ash Shafa; (D, F, G) reproduced from
Saudi Arabia – Al-Taif • S.A. Alharbi S3a (UQU); Wadi Thee Gazal, Ash Shafa; 21°5.5702'N, 40°21.785'E; alt. 2057 m; 23 Jan 2011; S.A. Alharbi S4a (UQU); same data as for preceding; 1 Jan 2011; S.A. Alharbi S6a (UQU); same data as for preceding;10 Jan 2011; S.A. Alharbi S7a (UQU); same data as for preceding; 9 Dec 2010; S.A. Alharbi S8a (UQU); same data as for preceding; 19 Jan 2011; S.A. Alharbi S16a (UQU); same data as for preceding; 8 Jan 2011; S.A. Alharbi S16A (UQU); same data as for preceding; 30 Dec 2010; S.A. Alharbi S13a (UQU); same data as for preceding; 9 Dec 2010; S.A. Alharbi S14a (UQU); same data as for preceding; 17 Dec 2010; S.A. Alharbi S00 (UQU); 9 Dec 2010; S.A. Alharbi S10b (UQU); same data as for preceding; 21°5.4656'N, 40°21.7937'E; 9 Dec 2010.
≡ Huernia laevis J.R.I. Wood, Kew Bull. 39:128 (1984).
Yemen • J.R.I. Wood 3037 (holotype: K [46740.000]); Jebel Marran, Khawlan As Sham; 16°49.2672'N, 43°24.7619'E; alt. 1400 m; 31 Oct 1979.
Dwarf succulent forming dense clump. Branches non-rhizomatous, up to 80 mm long, erect, decumbent, grey-green mottled with purple or red; tubercles 3–5 mm long, 1 mm broad at base, conical, spreading, laterally flattened and joined towards base into 5 angles along branch, abruptly narrowing into fine spreading slender acuminate tooth. Inflorescences 1–2 per branch, each of 2–5 flowers developing in gradual succession on short peduncle with few narrow filiform bracts; pedicel 15 mm long, spreading and holding flower facing horizontally; flowers with no scent; sepals 15 mm long, 3 mm broad at base, narrowly ovate attenuate. Corolla 32 mm diam., broadly funnel-shaped, margin weakly bulging like an annulus; outside smooth, pale cream with 1 heavy (+ 2–4 lighter) raised longitudinal veins running down each lobe; inside shiny creamy-yellow, marked with shiny irregular broad maroon streaks and scrolls, smooth with few low conical papillae (wart-like) at corolla lobes apices each with minute apical bristle; tube 6 mm long, 10 mm broad at mouth, cupular; lobes 10 mm long, 14 mm broad at base, reflexed, deltoid-acuminate, intermediate lobes 1 mm long. Corona without basal stipe; outer lobes (discrete 5 lobes), 4 mm diam., subquadrate, emarginate to shallowly bifid, spreading on base of tube and fused to it towards base, blackish-maroon; inner lobes 1 mm long, purple with cream at base, adpressed to backs of anthers and shorter than them, dorsiventrally flattened with ascending obtuse conspicuous gibbous at base, tapering to small smooth acute apex.
Jabal Al Qahar, 90 km NE of Baysh, Jazan, SW Saudi Arabia (
Probably endemic to SW Arabian Peninsula, known so far from Saudi Arabia and Yemen (
Growing amongst limestones amongst Juniperus at 1828–2000 m alt. (
Ceropegia laevis should be considered as Nationally Endangered (EN), according to the IUCN Red List criteria. The species is known from only one location, its EOO and AOO (104.00 km2) would both qualify as Endangered. Its habitat is not part of any protected area and its continuing decline is projected because of anthropogenic activities in the area.
Ceropegia laevis can easily be distinguished from most other species of sect. Huernia in Saudi Arabia by the glabrous shiny yellow background colour of the inside of the corolla, which has an annulus-like area around the mouth of the tube.
Laevis (Latin) smooth, flat; for the glabrous corolla (
Saudi Arabia – Jazan • I.S. Collenette 8180 (K [fl in spirit: 57656.000]); Jabal Qahar; 17°42.0367'N, 42°51.1983'E; alt. 2000 m; 20 Apr 1992.
Dwarf succulent forming dense clump. Branches 30–100 mm long, non-rhizomatous, erect to decumbent, grey-green mottled with purple-red; tubercles 4–10 mm long (including leaf-rudiment), 1.5–5 mm broad at base, conical, spreading, laterally flattened and joined into 5 angles along branch, each tipped with a soft slender acuminate caducous leaf-rudiment. Inflorescence arising in lower half of branch, usually 1 per branch, each bearing 2–10 flowers developing in gradual succession from short peduncle sometimes 3 flowers developing simultaneously, bracts filiform without lateral teeth, flowers with no foetid odour, rarely with faint unpleasant smell; pedicel 8–20 mm long, 1–2.5 mm thick, ascending holding flower facing upwards, tapering sometimes toward the point of flower attachment; sepals 8–18 mm long, 1–2.5 mm broad at base, attenuate. Corolla 30–50 mm diam., campanulate; outside smooth, cream-speckled with pale maroon spots uniformly scattered or concentrated on the upper half of corolla tube sometimes spots become darker especially on the upper half, with 1 heavy (+ 2–4 lighter) raised longitudinal veins running from lobes to base of tube; inside cream with irregular-shaped short maroon lines and dashes changing to concentric broken lines in lower half of tube or uniformly coloured with purplish-red, sometimes deep coloured areas concentrated between the lobes or corolla entirely uniformly coloured with purplish-red; corolla covered, except in lower third of tube with compressed conical papillae densely crowded and reaching maximum size around mouth of tube (up to 3 mm long and 1.2 mm base width), each tipped by minute apical acuminata bristle; tube 7.5–15.5 mm long, 11–22 mm broad at mouth, pentagonal; lobes 9–22.8 mm long, 9–14.25 mm broad at base, spreading with recurved apex or sometimes reflexed, deltoid, caudate to acute or acuminate rarely attenuate usually concave or form channel at tip, intermediate lobes 1.5–4 mm long. Corona without basal stipe; outer lobes (5–10 mm diam.) spreading on base of tube and fused partially to it, discrete to 5 lobes with each lobe rectangular rarely subquadrate crenate, dentate, mucronate, emerginate or bifid blackish-maroon; inner lobes 3–6 mm long, 1–1.5 mm at base, ivory white sometimes mottled with a few maroon spots at the tips or marked entirely with small purple spots adpressed to anthers in their lower half, then rising up connivent and then diverging towards apices, dorsiventrally flattened around laterally-broadened base becoming terete above and tapering gradually to a slender fine minutely-scabrous or smooth apex, at base with slightly inflated transversal dorsal gibbosity with rounded to truncate end, sometimes a conspicuous acute humb appearing in the staminal tube under corona base, rarely hook-like appendages grow from both sides of the base meeting above the guardrails. Pollinia 0.7–0.8 mm long.
1 | Branches not stout, up to 100 mm long; corolla up to 50 mm diam., marked inside with irregular short maroon lines and dashes or rarely dotted; outer corona mostly consisting of five distinct rectangular lobes | 2 |
– | Branches stout, up to 60 mm long; corolla up to 30 mm diam., marked inside with maroon rounded spots or dashes; outer corona disc or disc-like | C. lodarensis var. rubrosticta |
2 | Corolla tube inside with concentric broken lines or uniformly coloured with purplish-red, lobes marked with irregular-shaped short maroon lines and dashes sometimes deep coloured areas concentrated between the lobes or corolla entirely uniformly coloured with purplish-red | C. lodarensis var. lodarensis |
– | Corolla tube inside with concentric short dashes, corolla lobes marked with small maroon dots | C. lodarensis var. foetida |
≡ Huernia lodarensis Lavranos, J. S. African Bot. 30: 87 (1964). Type: Yemen – Lodar (Lawdar) • J.J.Lavranos 1900 (holotype: K [fl in spirit: 24982.000]); 13°52.6751'N, 45°51.7598'E; alt. 900 m; 19 Aug 1962.
= Huernia collenetteae Plowes, Asklepios 114: 8 (2012). syn. nov. Type: Saudi Arabia – Asir • I.S. Collenette 1176 (clonotype: SRGH [DP6868]); between Abha and Jabal Sawdah; 18°14.425'N, 42°25.2244'E; alt. 2650 m.
= Huernia saudi-arabica D.V.Field, Kew Bull. 35(4): 754 (1981). Type: Saudi Arabia – Asir • I.S. Collenette 549 (holotype: k! [K000911103]); between Abha and Jabal Sawdah, 12 km NW Abha; 18°15.7389'N, 42°23.1535'E; alt. 2650 m.; 31 Mar 1978.
Branches 30–90 mm long; tubercles 4–10 mm long (including leaf-rudiment), 1.5–5 mm broad at base. Inflorescence bearing 2–10 flowers developing in gradual succession from short peduncle, sometimes 3 flowers developing simultaneously, flowers with no foetid odour, rarely with faint unpleasant smell; pedicel 8–20 mm long, 1–2.5 mm thick, ascending holding flower facing upwards, tapering sometimes towards the point of flower attachment; sepals 8–18 mm long, 1–2.5 mm broad at base, attenuate. Corolla 30–50 mm diam., campanulate; outside smooth, cream-speckled with pale maroon spots uniformly scattered or concentrated on the upper half of corolla tube, sometimes spots become darker especially on the upper half; inside cream with irregular-shaped short maroon lines and dashes changing to concentric broken lines in lower half of tube or uniformly coloured with purplish-red, sometimes deep coloured areas concentrated between the lobes or corolla entirely uniformly coloured with purplish-red; papillae up to 3 mm long and 1.2 mm base width; tube 7.5–15.5 mm long, 11–22 mm broad at mouth, pentagonal; lobes 9–22.8 mm long, 9–14.25 mm broad at base, spreading to spreading with recurved apex or sometimes reflexed, deltoid, caudate to acute or acuminate, concave at tip, intermediate lobes 1.5–4 mm long. Outer corona lobes (5–10 mm diam.) discrete to 5 rectangular lobes; inner lobes 3–6 mm long, 1–1.5 mm at base.
Ceropegia lodarensis var. lodarensis A ex J Lavranos 1789, sub DP3604, Yemen, (H. lodarensis, Type) B Alharbi S6B (H. collenetteae) C Alharbi S9B (H. collenetteae) D ex Collenette 549 sub DP6865, Jabal Al Sawdah, (H. saudi-arabica, Type) E Alharbi S2B (H. collenetteae) F Alharbi S18a (H. collenetteae) G Collenette 2227, Al-Hadda, (H. collenetteae) H ex Collenette 8232 sub DP8126, (H. saudi-arabica) I Alharbi S4B (H. collenetteae) J ex Collenette 1176 sub DP6868, Jabal Al Sawdah, (H. collenetteae, Type) K maroon uniform colour of corolla tube in ex Collenette sub DP6594, Abha, (H. saudi-arabica) L concentric broken maroon lines of corolla tube in Alharbi S6B (H. collenetteae). (A) reproduced from
Scattered over a wide area, extending from Al Habala in SW of the country to Al-Hadda in Al-Taif in the Western Region.
Arabian Peninsula (Saudi Arabia and Yemen) and Africa (Ethiopia; Bruyns, P.V. 8432, E; http://data.rbge.org.uk/herb/E00995868)
It occurs at 900–2650 m alt. in granitic outcrops mainly under shrubs. Flowering: mostly Aug-May
Ceropegia lodarensis var. lodarensis is most similar to C. khalidbinsultanii, but differs in having a larger campanulate corolla with compressed conical papillae (up to 1.2 mm broad at base), sometimes uniformly coloured with purplish-red, flower with no or only faint bad smell and has shorter tubercles on the branches.
Lodarensis for the occurrence at Lodar (Lawdar) in Yemen (
Ceropegia lodarensis var. lodarensis should be assessed as Near Threatened (NT) in Saudi Arabia due to species’ AOO of 3,900 km2 and EOO of 12,509.959 km2 and the current threats of tourism, overgrazing, infrastructure and housing development.
Saudi Arabia – Asir • I.S. Collenette 1280 (k [fl in spirit: 44272.000] & E); Al Habala, 50 km SE of Abha; 18°1.6787'N, 42°51.3655'E; alt. 2384 m; 06 Apr1979.
Saudi Arabia – Al-Baha • I.S. Collenette 7785 (k [fl in spirit: 57339.000]); Jabal Shada, SW of Al Baha; 19°50.9947'N, 41°19.0693'E; alt.1933 m; 07 Apr1991; I.S. Collenette 8267 (K [fl in spirit: 59350.000]); same data as for preceding; 15 Sep1992.
Saudi Arabia – Al-Taif • I.S. Collenette 815 (K!, herbarium specimen); Wadi Ammak near Al Hadda; 21°20.9808'N, 40°17.7485'E; alt. 2100 m; I.S. Collenette 2227 (K [fl in spirit: 44371.000, 53692.000]); Al-Hada; 21°20.8387'N, 40°17.152'E; alt. 2000 m; 1981; I.S. Collenette 2633 (K [fl in spirit:45473.000, 45894.000, herb. material sub DP6599 & sub Leach 17652]); SW of Al Hadda, off Taif to Abha Road; 21°18.4696'N, 40°22.1371'E; alt. 2100 m; 07 May 1981; I.S. Collenette 5780 (K [fl in spirit: 35856.000]); Between Al Hadda and Harithi; 21°5.7571'N, 40°55.0155'E; alt. 1620 m; 23 Mar1986; S.A. Alharbi S1b (UQU); Wadi Thee Gazal, Ash Shafa; 21°5.4656'N, 40°21.7937'E; alt. 2057 m; 29 Dec 2010; S.A. Alharbi S2b (UQU); same data as for preceding; 09 Dec 2010; S.A. Alharbi S3b (UQU); same data as for preceding; 23 Jan 2011; S.A. Alharbi S4b (UQU); same data as for preceding; 29 Dec 2010; S.A. Alharbi S5b (UQU); same data as for preceding; 23 Nov 2010; S.A. Alharbi S6b (UQU); same data as for preceding; 02 Oct 2011; S.A. Alharbi S9b (UQU); same data as for preceding; 23 Nov 2010; S.A. Alharbi S9a (UQU); same data as for preceding; 05 Jan 2011; S.A. Alharbi S18a (UQU); same data as for preceding; 21°5.5702'N, 40°21.785'E; 17 Dec 2010.
I.S. Collenette 1523 (E [fl in spirit]); A.J. Bntler AJB 13 (E [fl in spirit]).
≡ Huernia foetida Plowes, Asklepios 114: 9 (2012).
Saudi Arabia – Jazan • I.S. Collenette 3743 (holotype: K! [fl in spirit: 38892.000]); Jabal Fayfa, 80 km NE Jazan; 17°14.5296'N, 43°4.9368'E; alt. 1550 m; 31 Jul 1982.
Branches up to 100 mm long; tubercles 7 mm long (including leaf-rudiment), 1.5 mm broad at base. Inflorescence bearing up to 4 flowers developing in gradual succession, flowers with very foetid odour; pedicel spreading and holding flower facing horizontally, tapering towards the point of flower attachment. Corolla 40 mm diam., campanulate; outside smooth, cream; inside cream with maroon dots changing to concentric short dashes in lower half of tube covered, except in lower third of tube with compressed conical papillae densely crowded and reach maximum size around mouth of tube (up to 1 mm long and 0.5 mm broad at base); tube 11 mm long, 10 mm broad at mouth, pentagonal; lobes spreading, deltoid, attenuate with deep groove at tip, intermediate lobes 1 mm long. Outer corona lobes 8 mm diam., five discrete rectangular lobes; inner lobes 3 mm long, 1 mm at base.
Rare, known so far from Jabal Fayfa, 80 km NE Jazan, SW of the country (
Probably endemic to SW Arabian Peninsula known so far from Saudi Arabia.
Occurs in granitic outcrops at 1550 m alt (
Foetidus (Latin) smelly, for the strong, unpleasant smell of flowers.
Ceropegia lodarensis var. foetida is estimated to have an EOO of 80.173 km2 (which would place the species in Critically Endangered, CR) and AOO of 88 km2 (which would place it in EN). The size of its populations and current threats are not well-known, but populations in mountainous areas in Saudi Arabia are likely impacted by agriculture, overgrazing, development and tourism. Therefore, var. foetida should be considered Data Deficient (DD).
≡ Huernia rubrosticta Plowes, Asklepios 114: 11 (2012).
Saudi Arabia – Najran • I.S. Collenette 1482 (holotype: k! herb. material); Jabal Manfah, 24 km NE Najran; 17°36.9386'N, 44°12.3742'E; alt. 1700 m; 30 Apr 1979.
Branches 30–60 mm long, stout; tubercles 5.5–6 mm long (including leaf-rudiment), 2–3 mm broad at base. Inflorescence bearing 6 flowers developing in gradual succession from short peduncle, flowers with faint unpleasant smell; pedicel 11 mm long, 2 mm thick, ascending holding flower facing upwards, tapering sometimes towards the point of flower attachment; sepals 9.5 mm long, 2 mm broad at base, attenuate. Corolla 32 mm diam., campanulate; outside smooth, cream-speckled with pale maroon spots on the upper half of corolla tube; inside cream with rounded maroon spots or dashes changing to concentric broken lines in lower half of tube; papillae up to 1.5 mm long and 0.75 mm broad at base; tube 10 mm long, 12 mm broad at mouth, pentagonal; lobes 8 mm long, 7.5 mm broad at base, spreading with recurved apex, deltoid, acute concave at tip, intermediate lobes 1.5 mm long. Outer corona lobes 5 mm diam. fused into disc or a slightly disc-like with short subquadrate crenate; inner lobes 3 mm long, 1 mm at base.
Rare, known only from Najran Region, SW Saudi Arabia (
Probably endemic to SW Arabian Peninsula, known so far only from Saudi Arabia
Concentrated amongst rounded granitic boulders at 500–1700 m alt. (
The variety is most similar to the Ethiopian endemic Huernia boleana, from which it can be separated with flowers by the much more campanulate corolla that is wider than the long, pentagonal tube, the more conical papillae and the shorter inner coronal lobes (ca. 3 mm compared to ca. 6 mm in H. boleana) and with habit and habitat that is erect to decumbent amongst granitic rocks compared to H. boleana that is erect, pendulous or prostrate in basalt or sandstone.
It can be easily distinguished from the other varieties of C. lodarensis proposed here by the stout branches, flowers with more evenly-rounded spots inside that are more red in colour and by the more slender papillae.
Ceropegia lodarensis var. rubrosticta has an estimated EOO of 97.188 km2 (which would place the species in CR) and AOO of 20 km2 (which would place it in EN). The size of populations and current threats are little known. Therefore, C. lodarensis var. rubrosticta should be considered Data Deficient (DD).
Saudi Arabia – Najran • I.S. Collenette 6059 (K [fl in spirit: 51184.000]); Al Jawshan, 70 km NW Najran; 18°8.4287'N, 43°51.2486'E; alt. 1520 m.; 07 Mar 1987.
We would like to thank the directors and members of staff of the herbaria at Kew (K) and Edinburgh (E) for providing specimens of sect. Huernia for this study and we would like to express our gratitude to the International Asclepiad Society and the Cactus and Succulent Society of America for their kind permission to reproduce photographs from Asklepios 114 and Haseltonia 19, respectively.
Appendices 1–3
Data type: statistical data
Explanation note: Illustration shows how the plant parts were measured, Screen plot eigenvalues for identification of principal components and boxplot showing differences in morphological characters of Huernia species.