Taxonomic revision of Ceropegia sect. Huernia (Asclepiadoideae, Apocynaceae) in Saudi Arabia with three new combinations

Abstract 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. khalidbinsultaniicomb. nov., C. laevis, C. lodarensis and C. macrocarpa. This study also suggested reducing two names to varietal level under C. lodarensis (var. foetidacomb. nov. and var. rubrostictacomb. nov.). A key to the species, detailed morphological descriptions, illustrations, distribution maps, ecology, etymology and preliminary conservation assessments are provided that follow IUCN criteria.


Introduction
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 (Bruyns et al. 2017). The stapeliads are widely distributed in semi-arid to arid areas of the Old World from southern Africa north-eastwards to India and Myanmar (Bruyns 2005).Their flowers are amongst the most beautiful of the dicotyledons, as well as amongst the most complex with almost all of them scented of carrion or bad fish and similar pungent odours (Pillans 1920;Court 2000). They exhibit an extraordinarily wide range of floral shapes and sizes and a wide range of complicated structures in the centre of the flower that are associated with the pollination process (Bruyns 2005). The flowers are specialised exclusively for fly pollination and this diversity appears to have arisen in response to the wide range of sizes of flies that are present in the region, combined with the wide spectrum of geological and topographical niches in the area (Bruyns 2005).
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 (Plowes and McCoy 2003). As can be expected in a section with a range this large, Huernia has a great number of species and subspecies, with over 54 species currently recognised, making it the most diverse section in the stapeliads (Bruyns et al. 2017). It is distinguished from other angled-stemmed stapeliads by the leaf-rudiments without stipular denticles; corona very rarely raised above the base of the tube on a stipe, outer series spreading at the base of the tube and often partially fused to it, tube often with an annular thickening around the mouth, but not entirely formed by an annulus (Bruyns 2014). Plants of Huernia have almost identical stems, so that the species cannot always be identified accurately without flowers. Flowers also sometimes show a variety of forms within a single species, such as H. humilis and H. thuretii from South Africa (Bruyns 2005). Consequently, the number of species approved for Huernia has varied widely over time: 45 for White and Sloane (1937), 64 for Leach (1988), 49 for Bruyns (2005) and a little over 54 currently.
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) (Collenette 2000). The famous plant collector, Mrs I. S. Collenette, was the first to collect Huernia from Saudi Arabia. Between 1972 and 1998, she collected several apparently undescribed species of Huernia with relatively large papillate flowers (Plowes 2014). These specimens have been deposited at the Royal Botanic Gardens herbaria at Kew (K) and Edinburgh (E). Only one species had previously been described by Field, in 1980, in the course of naming her collections at Kew; this was H. saudi-arabica D.V.Field (Field 1980). Somewhat later, in 1985, Collenette published her first book on Saudi Arabian plants, An Illustrated Guide to the Flowers of Saudi Arabia. She recorded two species, H. lodarensis Lavranos and H. saudi-arabica and four unnamed species (Collenette 1985). In her subsequent publications (Collenette 1998(Collenette , 1999(Collenette , 2000, three species were recognised: H. arabica N.E.Br., H. laevis J.R.I.Wood and H. saudi-arabica. Some of the five species which lacked names have an affinity to H. boleana M.G. Gilbert and H. lodarensis. Soon after, Al-Hemaid published the name H. haddaica for the specimen Collenette 5944 from Al-Hadda (Al-Hemaid 2001), but this name was not validly published (Goyder and Al-Hemaid 2009). Tom A. McCoy collected a similar plant in 1999 from Khamis Mushait, which was described in 2003 as H. khalidbinsultanii Plowes & McCoy (Plowes and McCoy 2003). Just two years later, in 2005, Bruyns reduced the number of Huernia species in north-eastern Africa and Arabia to 14 species. In his treatment, he considered H. saudi-arabica and H. khalidbinsultanii to be synonyms of H. lodarensis and H. arabica to be a synonym of H. penzigii N.E.Br. (Bruyns 2005). However, this was not accepted by Plowes who published seven new names for Collenette's other Saudi Arabian collections of Huernia that lacked names Plowes 2014). Thus, from the taxonomic perspective of Plowes, Huernia in Saudi Arabia was represented by 11 species H. anagaynensis Plowes, H. arabica, H. asirensis Plowes, H. collenetteae Plowes, H. decaloba Plowes, H. foetida Plowes, H. khalidbinsultanii, H. laevis, H. radhwana Plowes, H. rubrosticta Plowes and H. saudi-arabica. 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 closelyallied 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 (Hamam et al. 2018). Ongoing investigations on the medicinal value of Saudi Huernias have been performed (Ali et al. 1984;Mossa and Abdul Hameed 1991;Almehdar et al. 2012;Alzahrani et al. 2015;El Sayed et al. 2018, 2020Hamam et al. 2018). However, in some recent studies (e.g. Alzahrani et al. 2015;Hamam et al. 2018), the species of sect. Huernia investigated was identified as Huernia sp. nov. aff. boleana according to Collenette (1999). The precision and usefulness of medicinal investigations on sect. Huernia of Saudi Arabia will be increased by a detailed taxonomic treatment. It will also enable studies on their conservation status to be made, as it would appear that some of them are being severely threatened by overgrazing, infrastructure and housing development (Abulfatih and Nasher 1988;Collenette 2000;. 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  was justified.

Taxon sampling
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 Leach (1995). Voucher specimens were deposited in the herbarium of Umm Al-Qura University (UQU, proposed abbreviation). Pickled and dried specimens of Huernia from Saudi Arabia and the Arabian Peninsula, generally, were examined at the herbaria at Kew (K) and Edinburgh (E).

Morphological characteristics
The morphological characters were examined and recorded from the available specimens ( (Gilbert 1975;Leach 1976;Field 1980;Albers and Meve 2002;Plowes and McCoy 2003;Plowes 2014). Height of the plant, odour and colour of flowers were immediately documented in the field. Floral characters were examined using a NOVEX AP-8 binuclear microscope. Pollinia, inner corona and apices of papillae were examined using a XSZ-107BN compound optical microscope. Quantitative morphological characteristics were measured using a ruler; Suppl. material 1: Appendix 1 illustrates how the plant parts were measured. Initially, 69 characters were recorded, but 23 proved invariant leaving 46 (19 quantitative and 27 qualitative) for the analysis (Table 1, 2). The data were entered into an Excel spreadsheet and were later transformed into a format suitable for morphometric analysis. These morphological characteristics were used as the basis for our taxonomic revision for the species of sect. Huernia in Saudi Arabia. The features are richly illustrated using ibisPaint X ver.6.4.3 for Android, which allows visual comparison of the species.

Data analysis
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 Katapally and Muhajarine (2014). The standardised data were analysed with R studio package Factor Analysis of Mixed Data (FAMD) version 1.2.3; this method included principal component analysis (PCA), used here to extract relevant information from high-dimensional datasets. Cluster analysis including principle coordinates analysis (PCoA) and unweighted pairs group using mean average (UPGMA) were carried out using the statistical software Minitab ver.18.1.1.0 (Minitab, Inc., State College, PA).

IUCN Preliminary Conservation Status
To assess the conservation status of each taxon, the guidelines for the IUCN Red List Categories and Criteria version 13 (IUCN Standards and Petitions Subcommittee 2017) and the guidelines for the Application of the IUCN Red List Criteria at the regional and national levels version 4.0 (IUCN 2012) were followed. Current threats and point distribution data were gathered from field observations and from the available scientific literature. These distributional data were then input into the GeoCAT software (Bachman et al. 2011), which, in turn, calculated two main spatial metrics: the Extent of Occurrence (EOO) and Area of Occupancy (AOO). If the EOO were less than the AOO, the EOO was set equal to the AOO to ensure consistency with the definition of the AOO as an area within the EOO following the IUCN guidelines (IUCN Standards and Petitions Subcommittee 2017). Criterion B was only used for the species assessment due to data availability. Distribution maps were created using ArcGIS Online (Esri, 'Topography').

Data resources
The data underpinning the analyses reported in this paper are deposited at GBIF, the Global Biodiversity Information Facility: https://doi.org/10.15468/6n2rgz.

Results
The first two axes of PCA accounted for 74.7% of the overall variation ( Fig. 1 (Fig. 2).  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. saudiarabica were grouped in one cluster in the positive axes and weakly separated from individuals of H. rubrosticta, H. lodarensis and H. boleana (Fig. 3).
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 3.

Discussion
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 . However, the diagnostic characters that were used by Plowes are questionable. In this study, multivariate analysis of 46 quantitative and qualitative morphological characters was conducted. Analyses by PCA, PCoA and UP-GMA were used to determine the characters that were useful in the taxonomy of species of sect. Huernia in Saudi Arabia. Vegetative characters, such as habit, the number of angles into which the tubercles are arranged along the branches and leaf-rudiments are extremely variable across sec. Huernia, especially amongst the southern African species (Bruyns 2005). However, these characters were valueless in the taxonomy of Arabian members, due to their considerable similarity between species. Therefore, the species were differentiated mainly on the basis of their floral characters.
In the multivariate analysis, accessions of H. radhwana (Fig. 6D), H. asirensis (Fig. 6F), H. anagaynensis (Fig. 6G) and H. khalidbinsultanii (Fig. 6H) grouped into one   distinguished between those species by: 1) size of the corolla tube, 2) colour of the exterior of the corolla, 3) the number of flowers per inflorescence and the succession of their opening and 4) the odour of the flowers. A careful examination of the type specimens suggests that they are all samples of a single species and these characters have all proved to be unreliable in our experience. The first point is not of any value since the size of the corolla tube in H. radhwana, H. anagaynensis and H. khalidbinsultanii is easily accommodated within the known range of H. asirensis. Variation found in specimens of sect. Huernia from Wadi Thee Gazal has also demonstrated the invalidity of the second point. In the case of the third, Plowes distinguished H. radhwana from other species in the group by its solitary flowers. This is encountered often in H. asirensis, where several specimens were found to have few flowers (2-4) that opened in succession. In respect of the fourth point, we do not consider that the odour of the flower is a prominent character. We observed that the foetid odour in flowers of H. asirensis becomes faint or vanishes completely after all pollinia were removed. In addition, this character is not considered diagnostic, as it is impossible to observe in preserved specimens. Thus, our results paper suggest that Plowes' names for these species with slender papillae and tubular-campanulate flowers should all be included as synonyms under H. khalidbinsultanii, since it is the first valid name from this group. 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 (Leach 1983). Thus, this study suggests that H. khalidbinsultanii must be maintained.
Huernia collenetteae and H. saudi-arabica accessions overlapped in one cluster in both the UPGMA (Fig. 3) and PCoA (Fig. 3) analyses. Close examination of the relevant specimens shows that characters of H. saudi-arabica are accommodated within the variation range of H. collenetteae. The most noticeable character in , which can be used to distinguish them, is patterns of streaking on the inside of the corolla (see figs 1-6 in Plowes 2012). Inside, the corolla tube in H. saudiarabica (Jabal Sawdah population) is uniformly coloured with purple and with deeply coloured areas concentrated between the lobes; sometimes the inside of the corolla is entirely purple (Fig. 10 D, H, K). However, this pattern has also been seen in the population of H. collenetteae from Ash Shafa region (from 379.87 km north of Jabal Sawdah) (Fig. 10E, I; S.A. Alharbi S4B), but with concentric broken maroon lines and stripes in the corolla tube instead of a uniform maroon colour. Colours vary greatly in the flowers of widespread species of sect. Huernia, such as that recorded in H. thuretii and H. hallii from South Africa (Bruyns 2005). Thus, separating these two entities (H. collenetteae and H. saudi-arabica) into distinct species is inconsistent and this study will handle all data obtained from specimens of H. collenetteae as H. saudi-arabica in the subsequent discussion.
Huernia saudi-arabica (Fig. 10D), described from a single specimen Collenette 549, was related by its author to H. lodarensis and H. boleana (Field 1980). Distinctive features given are: 1) the corolla is slightly larger; 2) the corolla lobes have a more conspicuous papillose, frill-like margin; 3) the inner surface of the attenuate lobe-tip is covered with short, but even-sized, papillae; 4) the outer corona is distinctly 5-lobed, but, unlike H. lodarensis, each lobe is considerably wider than long and narrows towards the bifid tip rather than being somewhat parallel-sided; and 5) the inner corona-lobes are smooth and more acute towards the tips ( fig. 1 in Field 1980). The floral measurements given by Field for H. lodarensis and H. boleana are easily accommodated within the known range of H. saudi-arabica. In the case of the third point, Field stated that "in H. lodarensis, the indumentum is a mixture of a few papillae and low tubercles" (fig. 1K in Field 1980). This feature can clearly be seen in a number of samples of H. saudi-arabica. In the case of the last two points, the corona lobes turned out to be far more variable than suspected and the range, that was observed, was found in specimens collected at a single locality. Here, it was found that the outer corona lobes range from rectangular to subquadrate or rarely fused entirely to form a disc (e.g. Alharbi S5B). Likewise, the tips of the inner coronal lobes vary from smooth to minutely scabrous. Consequently, our results support Bruyns' (2005) opinion that H. saudi-arabica should treated as a synonym under H. lodarensis (Fig. 10A).
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. 12) and H. rubrosticta (Fig. 14B) type specimens reveal that they are very close to H. lodarensis. In view of the unique streaking patterns on the interior of the corolla that were not observed in any specimens of H. lodarensis, these taxa are described here as varieties under H. lodarensis. Nevertheless, many more samples and additional taxonomic work are considered necessary to either confirm or modify this treatment.
The delimitation of H. arabica (Fig. 4) is a matter of long debate. While Plowes (2014) considered the taxon as an accepted species, Albers and Meve (2002) and Bruyns (2005)  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 Plowes' ( , 2014 names. The 'folk concept' of species (Cronquist 1988), in which groups are formed intuitively by individuals 'essentially similar' and referred to as species, are found in the taxonomy of most succulent plants and largely held sway amongst the stapeliads (Bruyns 2005). This can clearly be seen in Leach's (1988) taxonomic revision of Huernia. As he saw relatively few specimens, this led him to recognise too many taxa (64) and his classifications turned out to have little predictive value (Bruyns 2005). Thus, dense sampling of sect. Huernia or of stapeliads in general is essential, especially when describing new species or assessing the status of species. Members of sect. Huernia in Saudi Arabia still need attention and, with the aid of modern molecular methods, it seems that their complexity can be mastered. Our results suggest reducing the number of names reported in Saudi Arabia from 11 to four species: H. khalidbinsultanii, H. laevis and H. lodarensis (including three proposed varieties: var. lodarensis, var. foetida and var. rubrosticta) and H. macrocarpa.
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 (Bruyns et al. 2017). However, Plowes' names of Saudi Huernias are still not transferred yet. Therefore, we propose three new combinations in Ceropegia sect. Huernia. Those are: C. khalidbinsultanii comb. nov., C. lodarensis var. foetida comb. nov. and C. lodarensis var. rubrosticta comb. nov. Diagnostic features. 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 (Bruyns 2005(Bruyns , 2014Bruyns et al. 2017).  Description. Dwarf succulent forming dense clump. Branches 60 mm long, nonrhizomatous, 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 leafrudiment. 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 wartlike 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.

Taxonomic treatment
Distribution in Saudi Arabia. Rare, known only from Asir between Abha and Jabal Sawdah, SW Saudi Arabia (Chaudhary 2001).  Habitat and ecology. Growing amongst granitic rocks and scattered shrubs on a steep hillside at 2700 m alt. (Collenette 1999).
Diagnosis. This species can be easily distinguished from other members of sect. Huernia in Saudi Arabia by the small maroon bowl-shaped flowers.
Preliminary conservation status. The species is known only from one location near Sawda Mountain; the estimated EOO and AOO of 8 km 2 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.
Additional specimens examined. Description. Dwarf succulent forming dense clump. Branches 50-100 mm long, nonrhizomatous, 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 creamywhite 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.
Distribution in Saudi Arabia. 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.
General distribution. Probably endemic to SW Arabian Peninsula, known so far from Saudi Arabia only.
Habitat and ecology. Growing on granitic outcrops often under shrubs, from 1800-2100 m alt. Flowering Dec.-May Diagnosis. 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.
Notes. The foetid odour of the flower becomes weak or completely vanishes after all pollinia have been removed from the flower.
Etymology. Khalidbinsultanii for Prince Khalid bin Sultan bin Abdulaziz M., a former Saudi Deputy Minister of Defence (Plowes and McCoy 2003).
Preliminary conservation status. Near Threatened (NT) has been assigned to Ceropegia khalidbinsultanii, based on the species' EOO of 41,490 km 2 and AOO of 2,012 km 2 and the current threats of habitat transformation (roads and housing construction), population fragmentation and tourism.

Map 3. Distribution of Ceropegia laevis in Saudi Arabia.
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, deltoidacuminate, intermediate lobes 1 mm long. Corona without basal stipe; outer lobes (discrete 5 lobes), 4 mm diam., subquadrate, emarginate to shallowly bifid, spread-  ing 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.
General distribution. Probably endemic to SW Arabian Peninsula, known so far from Saudi Arabia and Yemen (Chaudhary 2001).
Habitat and ecology. Growing amongst limestones amongst Juniperus at 1828-2000 m alt. (Collenette 1999). Flowering: mainly September-May Preliminary conservation status. 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 km 2 ) 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.
Diagnosis. 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.
Etymology. Laevis (Latin) smooth, flat; for the glabrous corolla (Eggli and Newton 2004). Description. 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 irregularshaped 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.
Key to three varieties of Ceropegia lodarensis Description. Branches 30-90 mm long; tubercles 4-10 mm long (including leafrudiment), 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.
Distribution in Saudi Arabia. Scattered over a wide area, extending from Al Habala in SW of the country to Al-Hadda in Al-Taif in the Western Region.
General distribution. Arabian Peninsula (Saudi Arabia and Yemen) and Africa (Ethiopia; Bruyns, P.V. 8432, E; http://data.rbge.org.uk/herb/E00995868) Diagnosis. 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.
Preliminary conservation status. Ceropegia lodarensis var. lodarensis should be assessed as Near Threatened (NT) in Saudi Arabia due to species' AOO of 3,900 km 2 and EOO of 12,509.959 km 2 and the current threats of tourism, overgrazing, infrastructure and housing development.
Additional specimens examined.  roon 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.
Distribution in Saudi Arabia. Rare, known so far from Jabal Fayfa, 80 km NE Jazan, SW of the country .
General distribution. Probably endemic to SW Arabian Peninsula known so far from Saudi Arabia.
Habitat and ecology. Occurs in granitic outcrops at 1550 m alt (Collenette 1999). Diagnosis. Clearly distinct by its campanulate corolla that is dotted with maroon inside and has a very foetid odour when it opens. Etymology. Foetidus (Latin) smelly, for the strong, unpleasant smell of flowers. Preliminary conservation status. Ceropegia lodarensis var. foetida is estimated to have an EOO of 80.173 km 2 (which would place the species in Critically Endangered, CR) and AOO of 88 km 2 (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). Description. 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. Distribution in Saudi Arabia. Rare, known only from Najran Region, SW Saudi Arabia .

Ceropegia lodarensis (Lavranos) Bruyns var. rubrosticta (Plowes) Alharbi
General distribution. Probably endemic to SW Arabian Peninsula, known so far only from Saudi Arabia Habitat and ecology. Concentrated amongst rounded granitic boulders at 500-1700 m alt. (Collenette 1999). Flowering: March-April.  Diagnosis. 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.
Preliminary conservation status. Ceropegia lodarensis var. rubrosticta has an estimated EOO of 97.188 km 2 (which would place the species in CR) and AOO of 20 km 2 (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).