Blackwell Science, LtdOxford, UKBOJBotanical Journal of the Linnean Society0024-4074The Linnean Society of London, 2005? 2005 149? 419432 Original Article THE APTERANTHES EUROPAEA COMPLEX U. MEVE and S. HENEIDAK Botanical Journal of the Linnean Society, 2005, 149, 419–432. With 12 figures A morphological, karyological and chemical study of the Apteranthes (Caralluma) europaea complex ULRICH MEVE1* and SAMIA HENEIDAK2† 1 Received November 2004; accepted for publication May 2005 The Apteranthes europaea complex (Apocynaceae–Asclepiadoideae–Ceropegieae–Stapeliinae) distributed from Morocco/southern Spain along the North African coast of the Mediterranean Sea up to Sinai, Negev and southern Jordan is studied with emphasis on stem and flower morphology by SEM, chromosome sizes and flavonoid compounds. Apteranthes europaea was found to be rich in rather uncommon flavone glycosides. Of these, luteolin 4′-neohesperidoside represents the major flavonoid of all samples; luteolin-3′-O-(6′-O-sinapoylglucoside)-4′-Oneohesperidoside and luteolin-3′-O-(6′-O-feruloylglucoside)-4′-O-neohesperidoside are reported here for the first time. Flavonol glycosides also occur, but in much smaller quantities. The different flower morphs, variation in stem and corolla epidermal structures, slight variations in the length of the 2n = 22 chromosomes and in quantitative flavonoid composition are taxonomically best reflected by subdividing the complex into a western var. europaea (Europe and Africa) and an eastern var. judaica (Sinai, Arabia). © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432. ADDITIONAL KEYWORDS: Africa – Arabia – chromosomes – flavonoids – Spain. INTRODUCTION Apteranthes europaea (Guss.) Plowes, the former Caralluma europaea, has been transferred to Apteranthes Mikan with the reinstatement of the genus by Plowes (1995). The molecular study of Meve & Liede (2002) revealed this taxonomic placement as the currently most suitable interpretation of relationship. Apteranthes europaea originally was described from the small island of Lampedusa in the Mediterranean Sea (Gussone, 1839). Since then, it has been reported from southernmost Iberian Peninsula, Morocco and, with some interruptions, along the southern coast of the Mediterranean Sea up to the Sinai, Israel and Jordan (Fig. 12). In its easternmost habitats in Israel and south-eastern Jordan it inhabits more or less desert and montaneous habitats (e.g. Judean Mts.) more distant from the coast. With this large area of occurrence it constitutes one of the most widely distributed stape- *Corresponding author. E-mail: ulrich.meve@uni-bayreuth.de †Current address. Biological Sciences Department, Faculty of Education at Suez, Suez Canal University, Egypt. liad species. Together with Apteranthes munbyana (Decne.) Meve & Liede, it moreover is the only stapeliad species extending to Europe. The c. 400 species (34 genera) of stem-succulent Ceropegieae-Stapeliinae (Apocynaceae-Asclepiadoideae) are predominantly found in semiarid, mostly subtropical areas with centres of distribution in East Africa and southern Africa (Albers & Meve, 2002). Apteranthes (sensu Meve & Liede, 2002) is a small genus of six species showing a strikingly northern and wide distribution ranging from the Canary Islands to Nepal. There is considerable floral (but also vegetative) variability in A. europaea, quite often even between plants of single populations, but almost always between different populations. These circumstances have stimulated many taxonomists and regional florists to describe morphotypes, ecotypes or geographical races as new species, subspecies, varieties or forms. Starting with Hooker (1874), this trend culminated with Maire’s preparations for the ‘Flore du Maroc’, published in many subsections between 1924 and 1943 in the Bulletin de la Societé d’Histoire Naturelle d’Afrique du Nord (see Taxonomy). In the © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 419 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 Department of Plant Systematics, University of Bayreuth, D-95440 Bayreuth, Germany Botany Department, Faculty of Science, Suez Canal University, Ismailia, Egypt 2 420 U. MEVE and S. HENEIDAK sible differences in the structure of the interstaminal corona. In the last complete review of the genus Caralluma (which included all Apteranthus species), Gilbert (1990) lumped all taxa of the A. europaea complex into one variable species without discussion. With special reference to micromorphological, karyological and chemical data, this paper is the first attempt to present a detailed picture of the infraspecific differentiation within the complex. Apteranthes joannis Maire from Morocco is closely related to A. europaea, but was not included in this study because of its undisputed status as a good species (cf. also Gilbert, 1990; Raynaud, 1991). Vegetatively and florally similar to A. europaea, the stout, papillose and rugose corolla of A. joannis characterizes this invariable species sufficiently (cf. figs in Jonkers & Walker, 1993). In addition, it represents one of the very few hexaploid species in Asclepiadoideae (cf. Reese & Kressel, 1967; Raynaud, 1991; Albers & Meve, 2001), in contrast to the always diploid A. europaea (as demonstrated below). MATERIAL AND METHODS TAXA The material used for morphological, chemical and karyological investigations is summarized in Table 1. Morphology Stems and flowers have been investigated under the stereo microscope and in the Scanning Electron Micro- Table 1. Apteranthes europaea material used for SEM (M), chromosome (©) and chemical (§) investigations Subspecies Origin Voucher europaea M © § europaea © europaea © europaea © europaea M © § europaea M © § europaea © europaea © § europaea M © § europaea M © europaea M judaica M © § judaica M © judaica © judaica M © judaica M © judaica M © judaica M © § judaica © Egypt: north Matrûh Italy: Lampedusa Spain: Almeria Spain: Mazarron Spain: Capo da Gata Spain: Capo da Gata Morocco: Tafraroute Morocco: Aoulez Morocco: Nador to Guercif Morocco: Tafraroute Libya: Al Beida Egypt: north Sinai, Gidda Pass Israel: Jerusalem, Campus Israel: Har Hanagev Israel: Arad Israel: Dimona Israel: Jerusalem, Givat Ram Israel: north Bethlehem Israel: Jerusalem Morsy et al. s.n. (CAIH) Bruyns 2396 (MSUN) Jury et al. s.n. (ex hort. MSUN) Bosma 3 (ex hort. UBT) Albers 87-23-001 (MSUN) Albers 87-23-004 (MSUN) Jury et al. 14360 (MSUN) Jonkers 217 (MSUN, UBT) t’Hart 33b (MSUN) Jonkers 221 (MSUN) Anderberg 808 (S) Heneidak s.n. (Suez C. Uni. Herb.) Veste s.n. (ex hort. MSUN) Chaout s.n. (HUJ, MSUN) Bruyns 2482 (MSUN) Bruyns 2483 (MSUN) Bruyns 2475 (MSUN) sub Plowes 7567 (MSUN, UBT) Avishai s.n. (MSUN) © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 end, Maire tried to distinguish between ten different taxa in Morocco alone. The diversity of Apteranthes europaea in Morocco is indeed higher than anywhere else. However, Morocco also represents the best investigated area, and therefore the impression of an exceptional high variety there might be influenced by this fact also. Along the Mediterranean coast collections are particularly sporadic, pointing to a partly fractioned distribution area in Africa (Fig. 12). In the east, in Israel, A. europaea is again more abundant and morphologically diverse, which is also expressed by the number of synonymous taxa described. With Bruyns’ revision of ‘Caralluma’ europaea in Israel (Bruyns, 1987a), only C. europaea var. judaica, including also C. negevensis Zohary, has been accepted to accommodate the eastern populations. Danin, Shmida & Liston (1985) assumed that the dubious Caralluma aaronis (Hart) N.E. Br., a species additionally cited for the Sinai by Taeckholm (1974), refers to C. negevensis Zohary, a view supported by Bruyns (1987a), who then subsumed it under var. judaica. Bruyns (1987a, b) left all African, especially the variable Moroccan, material unconsidered, and therefore the question of how to treat the complete complex taxonomically still needs to be answered because this complex has never been revised as a whole. It has been partially treated in regional floras [e.g. Morocco (Raynaud, 1986), Algeria (Quezel & Santa, 1962–63), Libya (Ali, 1977), Egypt (Taeckholm, 1974)]. Raynaud (1986) recognized the subspecies maroccana against the typical subspecies in Morocco on the basis of osten- THE APTERANTHES EUROPAEA COMPLEX scope (SEM) using critical point dried and goldsputtered samples which were scanned with a Hitachi S 53 at 20 KV. Chromosome counts Chromosome numbers were established from adventitious root tip squash preparations. The root tips were pretreated in 0.002 M hydroxyquinoline for 4 h at 20 °C (Tjio & Levan, 1950), fixed in Carnoy’s solution for 24 h at 20° and stained with carmine for 24 h at 60 °C (Snow, 1963). RESULTS HABITAT AND HABIT As is typical for most stapeliads, Apteranthes europea prefers shaded stands such as the base of bushes wherein the plants are often scrambling (e.g. Jonkers & Walker, 1993). The individuals nevertheless vary considerably in their general habit depending on the edaphic situation. In deep, sandy soil there is a strong tendency to form rhizomes. On rocks the plants usually form compact clumps of rather thick stems (up to 30 mm in diameter). On calcareous rocks in the Negev they tend to be extraordinarily short and stout (e.g. ‘Caralluma negevensis’; Feinbrun-Dothan, 1977: fig. 44), while on the granites of the Anti-Atlas in Morocco the thick stems elongate to 25 cm (Jonkers & Walker, 1993). In Egypt, the dwarf thick branches are 20 cm long at the most. Typically, the species grows on rocky slopes among rocks (often partly under rocks), or in fissures of smooth rocks (Boulos, 2000; Heneidak, 2001). In the Judean Mountains, the thinnest stems are found, measuring just around 13 mm in diameter (e.g. Feinbrun-Dothan, 1977: fig. 43). VEGETATIVE MORPHOLOGY While the shape of leaf rudiments is a character of high taxon-specificity in many stapeliad taxa, it is highly variable in A. europaea. The general trend is from small, slightly thickish and rather acute leaf rudiments in European/African material (Fig. 1) to larger, broader and increasingly membraneous ones in Israel (Fig. 2). The degree of ciliation is variable throughout, although the leaf rudiments are usually glabrous west of Suez, but ciliate east of it (Fig. 2). Stipules (stipular glands) are absent (Fig. 1) or present (Fig. 2) throughout the whole complex. Therefore, stipular structures are without taxonomic value here. Stem surfaces are variable. The colour varies from uniform bright green to dark green or dark blue-green. In Europe, the stems are dark green, in west Morocco they are green or blue-green, and often speckled with dark green or purple. Along the Mediterranean Sea coast up to Egypt only greenish, but speckled, stems are found. In Israel the stems are a fresher green, sometimes even bright green, but never speckled. SEM studies of the stem epidermis revealed no fundamental variation. All eight specimens investigated possess a stem epidermis typical for Caralluma s.l. with a rather homogeneous pattern of isodiametric cells with slightly convex periclinal walls (Figs 3, 4). There is nevertheless a trend to more prominent stem epidermal sculptures in the western parts of the distribution area, as in bluish-stemmed individuals from Morocco (with brownish flowers, also, Jonkers 221). Here, a number of interspersed cells are enlarged and more convex, and these cells possess a raised central papilla (Fig. 3). However, the almost unsculptured, smooth surfaces of the Israeli plants (Fig. 4) occur also frequently in green-stemmed/red-flowered European and north-west African representatives. FLORAL MORPHOLOGY Variability in flower morphology of Apteranthes europaea is higher than typically found in widespread stapeliads, and has therefore hampered a sound taxonomic treatment. The increasing availability of plant material has demonstrated an infraspecific variability, where almost every population shows its own features [cf. the many illustrations published by Bruyns (1987a, b, 1988), Jonkers & Walker (1993), Shaw (1980), White & Sloane (1937)]. Especially with regard to frequently occurring differences in corolla structure, size and ciliation, a wealth of taxa has been © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 Flavonoid analysis For extraction of flavonoids 1 g of crushed fresh stem material was extracted in 3 mL absolute EtOH, boiled for about 2 min, cooled and left for 24 h. Samples were filtered, dried and rehydrated in 3 mL of 70% EtOH. About 40 µL of this solution was analysed using 2-D Paper Chromatography (2-D PC), and 20 µL were used for analytical High Performance Liquid Chromatography (HPLC with photodiode array detection) analysis. For the isolation of flavonoids, 50–100 g stem material were extracted by the same procedure as for extraction. Flavonoids were then purified by Preparative Paper Chromatography (PPC) and semipreparative HPLC. They were identified by means of UV spectroscopy using shift reagents (Mabry, Markham & Thomas, 1970; Markham, 1982), acid hydrolysis and analysis of aglycone and sugar moieties (Harborne, 1998), cochromatography with authentic standards, coelution using HPLC, Liquid Chromatography coupled to Atmospheric Pressure Chemical Ionization Mass Spectrometry (APCI-LC-MS) (Grayer et al., 2000), and Nuclear Magnetic Resonance Spectroscopy (NMR). 421 422 U. MEVE and S. HENEIDAK 500 mm 3 5 200 mm 2 4 6 100 mm 50 mm 1 mm 200 mm 50 mm Figures 1–6. Scanning electron micrographs of Apteranthes europaea. Figs 1−2. Leaf rudiments in adaxial view. Fig. 1. A. europaea var. europaea (Albers 04). Fig. 2. A. europaea var. judaica (Veste s.n.). Figs 3–4. Stem epidermis. Fig. 3. A. europaea var. europaea (Jonkers 221). Fig. 4. A. europaea var. judaica (Veste s.n.). Figs 5–6. Adaxial corolla epidermis. Fig. 5. A. europaea var. europaea (left, t’Hart 33; right, Jonkers 221). Fig. 6. A. europaea var. judaica (Bruyns 2475). © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 1 THE APTERANTHES EUROPAEA COMPLEX CHROMOSOMES All 18 plants investigated (Table 1) possess somatic 2n = 22 chromosomes (Figs 9, 10; cf. also Albers, 1976; Albers & Austmann, 1987; Albers, Austmann & Meve, 1988, 1990; De Loewenstern & Garbari, 2004). This is the standard situation in Asclepiadoideae, where c. 96% of the investigated taxa have a basic chromosome number of x = 11, and over 90% are euploid diploids (Albers & Meve, 2001). Karyotype analysis revealed a homogeneous genome of predominantly meta- to submetacentric chromosomes for A. europaea. One pair of chromosomes shows secondary constrictions with satellites. Satellites, however, do not represent specific Table 2. Average karyotype and chromosome lengths in Apteranthes europaea Length (µm) Variety Voucher europaea europaea europaea europaea europaea europaea europaea judaica judaica judaica Jury et al. s.n. Bosma 3 Albers 87-23-001 Albers 87-23-004 Jury et al. 14360 Jonkers 221 t’Hart 33b Bruyns 2482 sub Plowes 7567 Avishai s.n. Karyotype Chromosome 23.43 27.31 28.89 27.13 25.90 28.85 30.34 26.12 23.24 23.80 1.07 1.23 1.31 1.23 1.18 1.17 1.38 1.19 1.06 1.08 structures in the stapeliads. Usually they have been observed in the karyotypes of Caralluma s.l. and other stapeliads, as well as further asclepiads or periplocs (e.g. Albers, 1983; Albers & Meve, 2001). Most probably, satellites are a typical element of all stapeliad genomes. The chromosome lengths of ten different samples were determined, seven belonging to the western and three to the eastern form (cf. Tables 1, 2). In Africa and Europe the average chromosome length is 1.22 µm (1.07–1.38 µm), while east of the African continent, the average chromosome length is 1.11 µm (1.06–1.19 µm) (Figs 9, 10). This difference in chromosome length is not significant, but a slight trend of chromosomes diminishing in size from west to east is apparent. CHEMISTRY The flavonoid profiles of seven plants of the complex were investigated (Tables 1, 3, 4). The HPLC retention times, UV spectral maxima and positive ion APCI mass spectral data of the ten flavonoid compounds traced are given in Table 3. The composition percentages of each flavonoid compound in relation to the total amount of flavonoids present in each plant are shown in Table 4. Independent from the place of origin, whether Egypt, Spain, Morocco or Israel, all investigated samples show nearly identical patterns (Table 4). They appear to be very rich in rather uncommon flavone glycosides (substances 1–7; Table 3). Five compounds of luteolin O-glycosides glycosylated in the B-ring; two of these luteolin glycosides are additionally acylated with hydroxycinnamic acid, ferulic acid and sinapic acid (3, 4). Luteolin 4′-neohesperidoside (5) is the major flavonoid in the seven samples, while © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 described in the past (see taxonomic treatment). However, several distinct tendencies that support infraspecific differentiation have to be considered. Basal coloration of the corolla surface is predominantly white in the west, but cream in the east. Dense brickred to purple-red transversal stripes or streaks are found in Europe and Africa, whereas in the Sinai and the Orient brownish coloration on creamy background with rather few and thin brownish stripes and uniformly brownish tips of corolla lobes dominates. In addition, an unusual form exists in the Moroccan AntiAtlas with coarse brownish bands on greenish background (see sub Jonkers 221; Jonkers & Walker, 1993: fig. 2); the corolla indumentum consists of simple hairs, either on the surface and/or as cilia. Large clavate, purplish cilia frequently occur east of Suez but are lacking anywhere else. SEM studies of the corolla epidermis of four samples of each variety were conducted that revealed a characteristic separation between the populations west and east of Suez. In the western samples, the epidermis cells are homogeneously isodiametric with slightly convex to dome-shaped periclinals (Fig. 5, left & right). Each periclinal wall is crowned with a small, verruculose papilla (Fig. 5). The cuticle is considerably more pleated than usual only in the brown-flowered Moroccan form (Fig. 5, right). In the eastern samples the epidermal cells are less isodiametric, showing a nearly rounded outline (Fig. 6). The periclinals are elongatedly dome-shaped, leading to a rather bottle-shaped appearance of the cells. The very smooth and tiny periclinals lack a pleated cuticle but they are topped by mighty papillae-like structures showing a verrucose to prickly surface (Fig. 6). Corona structures and their coloration are rather similar over the whole area of distribution. The corona is normally purplish; however, east of the Suez it is occasionally yellow to yellowish-brownish. On average, gynostegial characters such as anther wings (guide rails) or pollinaria (Figs 7, 8) are broader in var. europaea (Fig. 7). 423 424 500 mm 9 10 mm 10 10 mm 8 500 mm 11 Figures 7–11. Pollinarium and guide rail, SEM. Fig. 7. Apteranthes europaea var. europaea (Jonkers 221). Fig. 8. A. europaea var. judaica (Bruyns 2475). Figs 9–10. Squash preparations of mitotic metaphase chromosomes, 2n = 22. Fig. 9. 2n = 22, Apteranthes europaeae var. europaea (Morsy et al. s.n.). Fig. 10. A. europaea var. judaica (Heneidak s.n.). Fig. 11. Illustration of the type plant [published as unnumbered, uncoloured copper engraving in Gussone (1839)]. chrysoeriol 4′-O-neohesperidoside (6) and apigenin 4′O-neohesperidoside (7) are distributed in very small amounts, only. Flavonol glycosides also occur, but in much smaller quantities than flavone glycosides, and only glycosides of quercetin were detected. An unidentified quercetin O-rhamnosyl-pentosyl-hexoside (8), a pentosyl-hexoside (9) and quercetin 3-O-rutinoside (rutin, 10) were found. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 7 U. MEVE and S. HENEIDAK THE APTERANTHES EUROPAEA COMPLEX 425 Table 3. HPLC retention times, UV spectral maxima and positive ion APCI mass spectral data of flavonoid compounds found in the seven studied plants APCI LC-MS in pos. mode HPLC 4 5 6 7 8 9 10 Aglycone [A + H]+m/z (relative abundance) Luteolin-3′-O-glucoside-4′-O-12.48 neohesperidoside Luteolin-3′-4′-O-diglucoside Luteolin-3′-O-(6′-O-sinapoylglucoside)4′-O-neohesperidoside Luteolin-3′-O-(6′-O-feruloylglucoside)4′-O-neohesperidoside Luteolin-4′-O-neohesperidoside Chrysoeriol-4′-O-neohesperidoside Apigenin-4′-O-neohesperidoside Quercetin – hexose – rhamnose – pentose Quercetin – hexose – pentose Quercetin-3-O-rutinoside 270, 331 757 (30) 595 (100) 287 (7) 12.58 13.55 270, 329 274, 329 611 (100) 963 449 (63) 817 287 (6) 287 14.07 274, 329 933 787 287 14.42 14.90 15.05 11.60 268, 271, 271, 257, 595 (100) 609 579 743 (90) 449 (2.5) 463 433 611 (13) 287 (8) 301 271 465 (12) 11.92 13.45 257, 356 256, 353 597 (45) 611 (19) 465 (16) 465 (68) 303 (64) 303 (38) 339 338 328 356 Table 4. Composition percentages of each flavonoid in relation to the total amount of flavonoids Taxon 1 2 3 4 5 6 7 8 9 10 europaea (Egypt) europaea (Spain 1) europaea (Spain 4) europaea (Morocco J) europaea (Morocco H) judaica (Egypt) judaica (Israel) 11.68 8.88 9.52 6.64 12.49 7.69 15.91 10.22 11.83 7.48 13.28 3.29 6.15 9.10 10.22 5.92 6.80 4.09 6.57 7.69 5.68 6.57 3.95 5.44 6.13 8.76 6.92 4.55 40.88 46.35 55.78 45.97 33.95 50.77 55.68 5.84 6.90 6.80 18.80 14.79 6.92 3.41 2.92 2.96 1.36 2.04 7.67 4.62 1.14 5.84 8.88 4.08 1.02 3.29 6.15 2.27 2.92 2.17 1.36 1.02 5.92 1.54 1.14 2.92 2.17 1.36 1.02 3.29 1.54 1.14 DISCUSSION All seven plants of A. europaea investigated and collected in different countries differ only in the amount of their limited flavonoid compounds. Flavonoids, so far known, generally are of limited occurrence and diversity in Apocynaceae-Asclepiadoideae. Mostly, aglycone and glycosides occur in limited diversity and quantity in comparison to many angiosperm families (Hegnauer, 1964, 1986, 1989). Especially from the former Caralluma s.l. (now subdivided in Apteranthes, Boucerosia, Caralluma, Caudanthera, Desmidorchis and Monolluma; cf. Meve & Liede, 2002) glycosides are mostly known as pregnane glycosides (e.g. Halim & Khalil, 1996). In the stapeliads, however, studies were often restricted to the easily investigated aglycone parts the flavonoid glycosides. Rather widespread are quercetin and kaempferol (e.g. Kozjek, Jay & Nétien, 1973; Rahman & Wilcock, 1991; Meve, 1997). Analyses of the complete, glucosylated molecules are fairly rare. In Glossonema edule N.E. Br. of the tribe Asclepiadeae, Rizk et al. (1990) detected luteolin-7-O-glucoside and apigenin-6,8-di-C-glucoside. A detailed compilation of the substances known for Apteranthes and related taxa are given in Table 5. Luteolin-4′-O-neohesperidoside is fairly ubiquitous, although this molecule is lacking in Caudanthera. The two species of Caudanthera investigated [the third species, C. mireillae (Lavranos) Meve & Liede, is closely related to C. sinaica (Albers & Meve, 2002)] are very different with regard to flower morphology. However, they are characterized by nearly identical patterns (Table 5) supporting the congeneric treatment proposed by © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 2 3 Intermediate (s) [I + H]+m/z (relative abundance) Rt (min.) Identity 1 UV λmax (nm) Molecular Ion [M + H]+m/z (relative abundance) 426 U. MEVE and S. HENEIDAK Table 5. Summary of the isolated flavonoid compounds from the species of Ceropegieae studied by previous authors Isolated flavonoid compounds Country Reference Apteranthes europaea var. europaea (Caralluma europaea var. europaea) Luteolin-3′-O-glucoside-4′-O-neohesperidoside, Luteolin-3′-4′-O-diglucoside, Luteolin-3′-O-(6″-Osinapoylglucoside)-4′-O-neohesperidoside, Luteolin-3′O-(6″-O-feruloylglucoside)-4′-O- neohesperidoside, Luteolin-4′-O-neohesperidoside, Chrysoeriol-4′O-neohesperidoside, Apigenin-4′-O-neohesperidoside, Quercetin-O-rhamnosyl-pentosyl-hexoside, QuercetinO-pentosyl-hexoside, Quercetin-3-O-rutinoside Luteolin-3′-O-glucoside-4′-O-neohesperidoside, Luteolin-3′-4′-O-diglucoside, Luteolin-3′-O-(6″-Osinapoylglucoside)-4′-O-neohesperidoside, Luteolin-3′-O(6″-O-feruloylglucoside)-4′-O- neohesperidoside, Luteolin-4′-O-neohesperidoside, Chrysoeriol-4′O-neohesperidoside, Apigenin-4′-O-neohesperidoside, Quercetin-O-rhamnosyl-pentosyl-hexoside, QuercetinO-pentosyl-hexoside, Quercetin-3-O-rutinoside Luteolin 3′,4′-di-O-β-d-glucopyranoside, Luteolin 3′-O-β-dglucopyranoside-4′-O-α-l-rhamnopyranosyl-(1→2)-β-dglucopyranoside Egypt Heneidak (2001) Egypt Heneidak (2001) Jordan Bader et al. (2003) Luteolin-4′-O-neohesperidoside, Kaempferol-7-Oneohesperidoside, Kaempferol-3-O-rutinoside Pakistan Rizwani et al. (1990) Luteolin-4′-O-neohesperidoside India Ramesh et al. (1999) Luteolin-4′-O-neohesperidoside India Ramesh et al. (1999) Luteolin-3′-4′-O-diglucoside, Luteolin-3′-O-(6″-Osinapoylglucoside)-4′-O-glucoside, Luteolin-3′-O(6″-O-feruloylglucoside)- 4′-O-glucoside, Vicenin-2, Quercetin-O-rhamnosyl-pentosyl-hexoside Luteolin-3′-4′-O-diglucoside, Luteolin-3′-O-(6′-Osinapoylglucoside)-4′-O-glucoside, Luteolin-3′-O-(6″-Oferuloylglucoside)- 4′-O-glucoside, Vicenin-2, Quercetin 3-O-rutinoside Luteolin-4′-O-neohesperidoside, Apigenin-4′-Oneohesperidoside, Vicenin-2, Vitexin, Vitexin-2′-Orhamnoside, Isovitexin-2′-O-rhamnoside, Quercetin-Orhamnosyl-dihexoside Egypt Heneidak (2001) Egypt Heneidak (2001) Egypt Heneidak (2001) Apteranthes europaea var. judaica (Caralluma europaea var. judaica) Apteranthes europaea var. judaica (Caralluma negevensis) Apteranthes tuberculata (Caralluma tuberculata) Boucerosia umbellata (Caralluma umbellata and C. lasiantha) Caralluma adscendens var. attenuata (C. attenuata) Caudanthera edulis (Caralluma edulis) Caudanthera sinaica (Caralluma sinaica) Desmidorchis acutangula (Caralluma acutangula) Meve & Liede (2002). Apteranthes europaea var. europaea and var. judaica do not differ in a single position in their unusually highly diverse glucoside pattern. This might underline their shared gene pool. In consequence, glucoside patterns do not support any further infraspecific division of the complex. This is the first report at all of compounds 3 [luteolin-3′-O-(6′-O-sinapoylglucoside)-4′-O-neohesperi- doside] and 4 [luteolin-3′-O-(6′-O-feruloylglucoside)4′-O-neohesperidoside] (Table 3; Heneidak, 2001). Compound 1 (luteolin-3′-O-glucoside-4′-O-neohesperidoside) has been detected in Apteranthes europaea var. judaica (‘Caralluma negevensis’) by Heneidak, 2001) as well as by Bader et al. (2003). In addition, Heneidak (2001) recorded the same compound in A. europaea var. europaea (Tables 4 and 5). Luteolin-3′-4′-O- © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 Taxon THE APTERANTHES EUROPAEA COMPLEX Shaw (1980) suggested that the A. europaea complex in Israel may consist of just one species. This has not been questioned by succeeding Apteranthes (Caralluma) investigators except for Chaout (in Plowes, 1995) with regard to C. negevensis. Considering the high vegetative, floral and chemical similarity, the diploidy and the wide and nearly continuously distribution, the treatment of the complex as one single species is indisputable for the present authors. Probably, A. europaea is nowadays best expressed as a polytopic–bitypic species, which can be separated nevertheless into at least two entities (morphotypes). These entities can be differentiated by deviations in stem and leaf morphology, corolla shape, indumentum and coloration, and in average chromosome length. The two entities could be treated as subspecies but there are fairly many transitions, and it finally remains unclear whether or not there is complete allopatry (regarding an Afro-European vs. an Arabian distribution area), which is a widely accepted presupposition for recognizing subspecies (cf. Stuessey, 1990). The brown-flowered form in Morocco, which superficially resembles var. judaica because of the similar flower colour, might represent a simple parallelism (homoiology), pointing to independent evolution within the Moroccan populations. Jonkers & Walker (1993) also observed different ecological preferences, with the typical form found usually on limestone and the brown-flowered, mostly slightly campanulate form, which is often missing sharp stem angles in addition, on granite. The latter has sometimes been called (erroneously) ‘Caralluma maroccana’, although the type of Boucerosia maroccana J.D. Hooker is clearly a red-flowered specimen (cf. Hooker, 1874). Thus, these two forms might be considered as two different Moroccan ecotypes. Spain Km 400 35° n Tu co Algeria Egypt Libya OMC 0° 20° Jord a n a isi roc Mo 30° 25° 40° Figure 12. Distribution map of Apteranthes europaea var. europaea (broken lines) and A. europaea var. judaica (dotted line). The type locality of A. europaea (Italy, Lampedusa) is marked by a triangle. © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 diglucoside (compound 2) occurs in considerable amounts in Apteranthes, which has been corroborated for A. europaea var. judaica (‘Caralluma negevensis’) by Bader et al. (2003). This flavonoid, outside of the Apocynaceae detected only in leaves of Listera ovata (Orchidaceae; Williams, 1979), serves as the major and most characteristic flavonoid for the small stapeliad genus Caudanthera (Table 5). Luteolin 4′-Oneohesperidoside, in contrast, seems to have a more ubiquitous distribution within the tribe Ceropegieae because it is the major flavonoid for genera such as Apteranthes, Boucerosia, Caralluma, and Desmidorchis as shown by Rizwani et al. (1990), Ramesh et al. (1999) and Heneidak (2001; Table 5). Possibly this flavonoid is characteristic for this group of more basal stapeliad genera (cf. Meve & Liede, 2002), for the stapeliads at all, or for the whole tribe. Morphologically, there are quantitative differences between the varieties. Typically, the stem epidermis of those samples of western origin (var. europaea) is more prominently sculptured. Vice versa, the corolla epidermis is more strongly sculptured in the plants from the east (var. judaica) with markedly convex outer epidermal wall. The Suez Canal serves as demarcation line between the two varieties (Fig. 12). Taxonomically significant variation in chromosome sizes in stapeliads have been reported by Albers & Meve (2001) at the tribe level and by Meve & Liede (2001a, b) at genus and species levels. Even within species, however, chromosome length might vary around 0–20%. Included is an undetermined rate of error owing to the preparation method, which is difficult to reproduce exactly in each case (Meve, unpubl. data). The c. 10% deviation found between the two varieties of A. europaea is then not significant at all, and falls within the variation range which can be expected on species level. 427 428 U. MEVE and S. HENEIDAK KEY TO THE VARIETIES a. Surface of corolla tube and corolla lobe bases with dense, purplish (rarely coarse and brownish) transverse stripes on whitish (rarely greenish) background, corolla lobes or tips uniform purple (rarely brown-striped in total), without clavate hairs.............................................................................................................................. A. europaea var. europaea b. Surface of corolla tube and lower half of corolla lobes with thin transversely brownish (–purple) stripes on greenish to yellowish-cream background, tips of corolla lobes uniformly brownish (–purple), often with clavate hairs.............................................................................................................................................. A. europaea var. judaica TAXONOMY Apteranthes europaea (Guss.) Plowes, Haseltonia 3: 59 (1995). Basionym: Stapelia europaea Guss., Flor. Sic. Prod., Suppl.1: 65 (1832) = Boucerosia europaea (Guss.) Caruel, Parl., Fl. Ital. 6: 725 (1886) = Desmidorchis europaea Kuntze, Rev. General: 418 (1891) = Caralluma europaea (Guss.) N.E. Br., Gard. Chron. 12: 369 (1892). Holotype: Italy, Sicily (Lampedusa), on calcareous rocks close to sea, Gussone s.n. [NAP]. Together with a more detailed description, Gussone (1839) additionally depicted the type plant by a copper engraving plate (Fig. 11). VAR. EUROPAEA = Apteranthes gussoneana J.C. Mikan, Nov. Act. Nat. Cur. 17: 594 (1835) (Stapelia gussoneana (J.C. Mikan) Jacq. ex Lindl. Bot. Reg. t. 1731 (1835) (Boucerosia gussoneana (J.C. Mikan) Hook. f., Bot. Mag. 100. t. 6137 (1874) (Caralluma europaea ssp. gussoneana (J.C. Mikan) Maire, in Jahandiez & Maire, Cat. Pl. Maroc 3: 582 (1924) (Apteranthes europaea ssp. gussoneana (J.C. Mikan) Plowes, Haseltonia 3: 59 (1995). Holotype: (?W?; cf. Gilbert, 1990). = Boucerosia maroccana Hook. f., Bot. Mag. 100, t. 6137 (1874) (Caralluma maroccana (Hook. f.) N. E. Br., Gard. Chron. 12: 370 (1892) (Caralluma europaea var. maroccana (Hook. f.) Berger, Stap. Klein. 96 (1910) (Caralluma europaea ssp. maroccana (Hook. f.) Maire, in Jahandiez & Maire, Cat. Pl. Maroc 3: 582 (1924) (Apteranthes europaea ssp. maroccana (Hook. f.) Plowes, Haseltonia 3: 60 (1995). Holotype: Morocco, Magador (K!). = Caralluma affinis de Wild., Icon. Select. Hort. Then. 5: 29 (1904) (Caralluma europaea var. affinis (de Wild.) Berger, Stap. Klein: 97 (1910) (Apteranthes europaea var. affinis (de Wild.) Plowes, Haseltonia 3: 59 (1995). Type: pl. 167 of protologue (lecto, designated by Gilbert, 1990). = Caralluma simonis hort. ex Berger, Monatsschr. Kakt. 14: 6 (1904) (Caralluma europaea var. simonis (hort. ex Berger) Berger, Stap. Klein. 95 (1910) (Boucerosia simonis (hort. ex Berger) A.C. White & B. Sloane, Stap. 191 (1933) (Apteranthes europaea var. simonis (hort. ex Berger) Plowes, Haseltonia 3: 61 (1995). Neotype: Libya, Derna, Taubert 341 (K!, P!). = Caralluma europaea var. marmaricensis Berger, Stap. Klein. 95 (1910) (Apteranthes europaea var. marmaricensis (Berger) Plowes, Haseltonia 3: 61 (1995). Iconotype: fig. 21 in Berger, Stap. Klein. (lecto, designated here). = Caralluma confusa Font Quer, Bull. Institute Cat. Hist. Nat. 1922: 31 (1922) (Caralluma europaea var. confusa (Font Quer) Font Quer, Mem. Mus. Cienc. Nat. Barcel. 2: 10 (1924) (Apteranthes europaea var. confusa (Font Quer) Plowes, Haseltonia 3: 61 (1995). Type: Spain, Capo da Gata (no type material traced). = Caralluma europaea ssp. maroccana var. barrueliana Maire, Bull. Soc. Hist. Nat. Afr. Nord. 26: 218 (1935) (Apteranthes europaea ssp. maroccana var. barrueliana (Maire) Plowes, Haseltonia 3: 60 (1995). Syntypes: Morocco, Sous, Adimine and Anti-Atlas, Ait-Mzal, Gattefossé & Barruel s.n. (water-colour at MPU only). = Caralluma europaea ssp. maroccana var. albotigrina Maire, Bull. Soc. Hist. Nat. Afr. Nord. 27: 79 (1936) (Apteranthes europaea ssp. maroccana var. albotigrina (Maire) Plowes, Haseltonia 3: 61 (1995). Type: Morocco, Qued Mellah near Casablanca, Gattefossé s.n. (no type material traced). = Caralluma europaea ssp. maroccana var. gattefossei Maire, Bull. Soc. Hist. Nat. Afr. Nord. 27: 79 (1936) (Apteranthes europaea ssp. maroccana var. gattefossei (Maire) Plowes, Haseltonia 3: 61 (1995). Holotype: Morocco, Qued Mellah near Casablanca, Gattefossé s.n. (G!; MPU!) = Caralluma europaea ssp. maroccana var. decipiens Maire, Bull. Soc. Hist. Nat. Afr. Nord. 29: 436 (1938) (Caralluma europaea ssp. gussoneana var. decipiens (Maire) Maire, Bull. Soc. Hist. Nat. Afr. Nord. 32: 214 (1943) (Apteranthes europaea ssp. maroccana var. decipiens (Maire) Plowes, Haseltonia 3: 61 (1995). © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 In conclusion, subdivision of A. europaea into two varieties seems to be the most appropriate treatment. The differences between the two varieties are not really pronounced, however: the fairly high number of characters concerned point to a considerable degree of separation. THE APTERANTHES EUROPAEA COMPLEX Description: Mat-forming succulent stems, 5–25 cm high, procumbent to ascending, mostly soboliferous; STEMS 4-angled, sometimes irregularly angled when inflorescences have destroyed symmetry, 13–30 mm thick, green to blue-green, often speckled with dark green or reddish dots, glabrous, glaucous. LEAF rudiments on broad tubercles along sharp angles, mostly slightly deflexed, without stipules, broadly deltoid, 1.5–2.5 mm × 2 mm, sessile, mostly shortly acuminate, caducous. INFLORESCENCES 2–15-flowered, in terminal or subterminal pseudo-umbels. Bracts c. 3 × 1 mm. Pedicels 1–4 mm long. FLOWERS with odour of excrement, rarely without. Calyx lobes deltoid, c. 1.5–3 × 1–1.5 mm, acute, fleshy. Corolla rotate, 13–20 mm in diameter; surface of corolla tube and corolla lobe bases with dense, purplish (rarely coarse and brownish) transverse stripes on whitish (rarely greenish) background, corolla lobes or tips only uniform purple (rarely brown-striped in total), corolla tube shallowly bowl-shaped, 1–3 mm long; corolla lobes 5–8 mm × c.5 mm, broadly ovate-deltoid, slightly to considerably recurved, acute, adaxially white-hairy all over, on the central portion only or glabrous, margins ciliate or glabrous, cilia c. 1 mm long, fusiform, rarely vibratile, unicellular. Gynostegium with corona shortly stalked, reddish-purple. Interstaminal corona lobes 1–2 × 1–1.2 mm, bifid, tips of deltoid to subulate segments rounded, often knobby, shiny-yellow. Staminal corona lobes 1.0 × 0.5 mm, linear-ovate to spathulate, rounded, incumbent on the anthers. Filament tube c. 1–1.2 mm long. ANTHERS rectangular, c. 1 × 1 mm, guide rails c. 0.3 mm long, spreading at mouth. STYLE-HEAD c. 0.5 × 2 mm, shiny white. POLpollinia ovate-rectangular, 0.25–0.3 in diam. Follicles in pairs, erect and spreading in an acute angle, 8–13 × 0.5–0.8 cm, narrowly fusiform, beaked, smooth and glabrous, grey-green with redbrown stripes. Seeds 7–9 × 4.5–6 mm, ovate, plano-convex (dark) brown with pale (red) brown margin (wings), apically slightly emarginate, coma 1.8–3 cm long, snowy white to slightly yellowish. LINARIA: Chromosome number: 2n = 22 Table 1). (for vouchers see Flowering time: October–January. Habitat: On rocky sandy soil growing under bushes of Suaeda, on sandstone rocks, on calcareous seashore rocks. Distribution: Egypt (Matrûh and Salûm), Spain, Italy (Sicily: Lampedusa), Libya, Tunisia, Algeria and Morocco (Fig. 12). Remarks: The many types relevant here are spread over a number of different herbaria. Considerable efforts were made to trace the types of R. Maire’s Moroccan taxa. The herbarium in Algier (AL) responded on our request that no types could be traced there. A personal search in the ‘Herbier de l’Afrique Nord’ in Montpellier (MPU) brought only little material to light, and no material at all was traced at the University of Marseille (MARS), where Maire taught. The holotype of Stapelia europaea Guss., however, is still preserved in Naples (NAP) (Santangelo, pers. comm.). Selected specimens: EGYPT: Mediterranean Coast. Wadi El Nassara, Salûm, 14.iv.1934, Shabetai Z 3409 (CAIM); Bir Ramla, Salûm, 07.iv.1970, Abbas 54 (CAIM); Plateau of Salûm, 22.iv.1973, Amal Amin et al. s.n. (CAI); Cliffs north of Salûm, 23/24.x.1995, Osborn & Helmy s.n. (CAI); between Matrûh & Barrani, 11.iv.1932, Shabetai Z 1699 (CAIM); Alam Abed, between Matrûh & Barrani, 17.iv.1934, Shabetai Z 3410 (CAIM); between Matrûh & Barrani, 17.iv.1984, Atta s.n. (CAIM); 15 km west of Matrûh, 27.v.1935, Drar s.n. (CAIM); Wadi Habis, Matrûh, iii.1990, Fahmy s.n. (CAI); 10 km north of Matrûh, Wadi ElHash El-Gharby, 10.vi.1998, Morsy et al. s.n. (CAIH, Suez Canal University Herb.). LIBYA: Cyrenaica, Wadi al Harib, deep gorge 16 km west of Al Beida, on limestone cliffs, 4.ii.1987, Anderberg 808 (S); Wadi ElKouf, Gebel Akhdar, 25.i.1967, Lofty Boulos 1468 (S); west Derna, near Ain-al-Sib, l. iv.1939, Sandwith 2512 (K); Benghazi, Grotto di Lette, on limestone rocks, iv.1939, Sandwith 2229 (K); Derna, iter cyrenaicum, © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 Type: Morocco, Middle Atlas, below Ksiba, Maire s.n. (MPU!, drawing only). = Caralluma europaea var. affinis f. parviflora Maire, Bull. Soc. Hist. Nat. Afr. Nord. 30: 357 (1941). Type: Anti Atlas, Tafraout, Maire, Weiller & Wilczek s.n. (no type material traced). = Caralluma europaea ssp. gussoneana var. tristis (Maire), Bull. Soc. Hist. Nat. Afr. Nord. 32: 213 (1941) (Aperanthes europaea ssp. gussoneana var. tristis (Maire) Plowes, Haseltonia 3: 59–60 (1995). Type: Algeria, near Ain-el-Hadjel, Maire s.n. (no type material traced). = Caralluma europaea ssp. maroccana var. micrantha Maire, Bull. Soc. Hist. Nat. Afr. Nord. 32: 213 (1941) (Apteranthes europaea ssp. maroccana var. micrantha (Maire) Plowes, Haseltonia 3: 61 (1995). Type: Morocco, Saffi, Maire s.n. (water-colour at MPU only). = Caralluma europaea var. schmuckiana Gattefossé & Maire Bull. Soc. Hist. Nat. Afr. Nord. 34: 183 (1943) (Apteranthes europaea var. schmuckiana (Gattefossé & Maire) Plowes, Haseltonia 3: 59 (1995). Type: Morocco, Marakech, Guéliz, Hintermann s.n. (no type material traced). 429 430 U. MEVE and S. HENEIDAK VAR. JUDAICA Apteranthes europaea var. judaica (Zohary) Plowes, Haseltonia 3: 61 (1995). Basionym: Caralluma europaea var. judaica Zohary (Pal. J. Bot. ser. 2: 173, 1941) Holotype: Israel, Jerusalem, between Beth Hakerem and Bayith Vegan, D. Zohary 2189 (HUJ). = Boucerosia aaronis Hart, Trans. Roy. Irish Acad. 28: 436, t. 17 (1885). Holotype: Jordan, Mt. Hor, Hart s.n. (K!); = Caralluma negevensis Zohary, in Feinbrun-Dothan, Fl. Palest. 3, Appendix, t. 44 (1978) (Apteranthes negevensis (Zohary) Plowes, Haseltonia 3: 61 (1995). Holotype: Egypt, Central Negev, Wadi Khoreiza, D. Zohary 11991 (HUJ). = Caralluma israelitica M. Zohary & Chaouat, nomen nudum, New Analyt. Fl. Isr. 289 (1979). Description: STEMS 3–20 cm × 1.2–2.0 cm, green. LEAF rudiments c. 4 mm × 3 mm, spreading rather horizontally, sessile to shortly stalked, broadly deltoid, broadly lanceolate or nearly round, usually acuminate. INFLORESCENCES subterminal near tips of stems, in dense pseudo-umbellate clusters of 3–12 flowers. Bracts c. 3 × 1 mm. Pedicels 1–1.5 mm long. FLOWERS with odour of excrement. Calyx lobes deltoid, c. 3–4 × 1–2 mm. Corolla rotate to campanulate, nearly 10–20 mm in diameter, adaxially with thin transversely brownish (–purple) stripes on greenish to yellowish-cream background, tips of corolla lobes uniformly brownish (–purple); corolla tube bowl-shaped to campanulate, 1–5 mm long; corolla lobes deltoid, 4–8 × 3–4 mm, ovate-deltoid, acute, spreading, fleshy, tips more or less recurved, usually solid brownishpurple, margins of corolla lobes with 1.5 mm long, purple, fusiform, vibratile unicellular hairs. Gynostegium with corona shortly stalked, rarely hairy outside, yellow to yellow-brownish purple with yellow tips. Interstaminal corona lobes c. 2 × 1 mm, ±bifid, segments flattened and rounded, tips mostly yellow; staminal corona lobes 1–1.5 × c. 0.5 mm, linear-ovate to spathulate, incumbent on the anthers, rounded or irregularly toothed. Filament tube c. 1.5 mm long. ANTHERS rectangular, 0.5 mm × 0.3 mm, guide rails c. 0.25 mm long, spreading at mouth. Stylar head 0.4 mm × 1.5 mm – Otherwise as in the type. Chromosome number: 2n = 22 Table 1). (for vouchers see Flowering time: April–June. Habitat: On rocky outcrops, respectively, chasmophytic in rock fissure plant communities on different sort of substrates. Distribution: Egypt (Northern Israel, Jordan (Fig. 12). Sinai), Palestine, Remarks: There is no evidence to uphold C. negevensis as species of its own as Plowes (1995) proposed in contrast to Bruyns (1987a), who already subsumed this taxon under var. judaica. Selected specimens: EGYPT: Di, North Sinai. Wadi Ain El-Gedeirat, on the slopes of hills, 06.iv.1939, Drar s.n. (CAIM, CAI); 2 km north-west of Gidda Pass, Gebel Sahaba, 05.v.1991, 07.iv.1995 & 10.v.1997, Heneidak s.n. (Suez Canal University Herb.); 2 km north-west of Gidda Pass, 5.v.1991, Förther 4369 (M); Ain El-Gedeirat, 12.iv.1929, Shabetai 6608 (CAIM, K); © 2005 The Linnean Society of London, Botanical Journal of the Linnean Society, 2005, 149, 419–432 Downloaded from https://academic.oup.com/botlinnean/article/149/4/419/2420197 by guest on 25 May 2022 1887, P. Taubert 341 (K, P); Wadi Kuf (Cyrinaique), 350 m, 21.iv.1938, Maire & Weiller 1049 (MPU). TUNISIA: An Charichira (An-Chezichra), M. Cosson et al. T/1885, 19.vi.1883 (G, K, P); Qued Guermessa (Djebel Eabior, S Tunisia), 16.ii.1907, Joly s.n. (MPU); east Ouled Mikamed, Kalkfelsritzen, c. 500 m, 21.i.1971, Röthlisberg s.n. (G); Gafsa (Djebel Gafsa, 34°23′N, 08°55′E) in aridis deserti, iv.1909 and 1919, Pitard s.n. (G). ALGERIA: O Garh. Rouban, Djorf el Aach, v.1856, Pomel s.n. (MPU); Oran, rochers dolomitique du Mons. Djado, xii.1923, Pomel s.n. (MPU); Oran, Santa Cruz, 1944, Aleizette s.n. (MPU); Oran, Santa Cruz, Aleizette s.n., v.1917 (G); Oran, Santa Cruz, 1885, Battandier s.n. (MPU); Oran, Rochers de la crete de Murdjudjo, Aleizette s.n., xi.1912 (MPU); Oran, above Mert el Kibir, iv.1849, Boissier & Reuter s.n. (G); Oran, Debeau 22.iv.1881 (G); S Oran, iv.1923, Humbert s.n. (P); Biskio, Djebel Senà, touffs, i.1899, Chevalier s.n. (P). MOROCCO: Vallée Qued Mellah, près Sidi Larbi, 20.xii.1935 Gattefossé 818 (K, MPU, P); Greater Atlas, Imintouga, v.1871, Hooker s.n. (K, P); neae Mogaor, Ain el Hadjah, iv–v.1871, Hooker s.n. (K); above Milhain, 1100–1200 m a.s.l., 28/29.v.1871, J. Ball s.n. (P); environs de Mogador, v.1867, Balansa (P); beneath Ksiba (Moyen Atlas), 900 m a.s.l., 09. iv.1937, Maire s.n. (MPU); Djebel el Maij, 30.v.1918, Maire s.n. (MPU); north Bon Denib (on the mountains), iv.1923, Humbert s.n. (MPU); Ait. Issehaq., 1941, Olivier s.n. (MPU); Oasis near Tarda, 1100 m a.s.l., 19.iv.1933, Maire & Wilczek s.n. (MPU); HassiBerkhan (Beni-bu-Yahi), 10.vi.1931, Sennen & Mauricio 7931 (G, MPU); Zaians, near Kenifra, 900 m, v.1927, Weiller 549.27 (MPU); Djebrlets, near Marakesh, on silicate rocks, iv.1923, Braun-Blanquet s.n. (MPU). SPAIN: Almeria, 20.xii.1982, Bruyns 2399 (K); Cabo da Gata, 20.xii.1982, Bruyns 2402 (K); north Totona, 23.xii.1982, Bruyns 2403 (K). ITALY: Sicily: Lampedusa, in rupibus calcareis reg. inferioris, vi.1900, Ross 263 (G, HBG, WAG); Lampedusa, 09.ix.1982, Bruyns 2396 (K). THE APTERANTHES EUROPAEA COMPLEX ACKNOWLEDGEMENTS Annalisa Santangelo, Curator at NAP (Naples, Italy), kindly provided us with scans of the type specimen of Stapelia europaea. We thank Dr Renée Grayer (Jodrell Laboratory, Kew) for helping in the identification of flavonoid compounds. REFERENCES Albers F. 1976. Asclepiadaceae. In: Löve A, ed. IOPB Chromosome number reports LI. Taxon 25 (1): 155–164. Albers F. 1983. Cytotaxonomic studies in African Asclepiadaceae. Bothalia 14: 795–798. 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