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Taxonomic revision of the genus ( s.l.) in south Yemen

Article in Nordic Journal of Botany · August 2015 DOI: 10.1111/njb.00746

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The user has requested enhancement of the downloaded file. Nordic Journal of Botany 33: 401–413, 2015 doi: 10.1111/njb.00746, ISSN 1756-1051 © 2015 The Authors. Nordic Journal of Botany © 2015 Nordic Society Oikos Subject Editor and Editor-in-Chief: Torbjörn Tyler. Accepted 5 December 2014

Taxonomic revision of the genus Heliotropium (Boraginaceae s.l.) in south Yemen

Salah El Naggar, Azza El-Hadidy and Asmaa Olwey

S. M. El Naggar and A. O. Olwey ([email protected]), Botany and Microbiology Dept, Faculty of Science, Assiut Univ., Assiut, Egypt. – A. H. El-Hadidy, Botany Dept, Faculty of Science, Cairo Univ., Cairo, Egypt.

The flora and fauna of Arabia, particularly southern Yemen, has recently attracted the interest of many authors. In this study, the genus Heliotropium L. (Boraginaceae) is taxonomically revised in southern Yemen. Ten species are recognized. Nomenclature, typification, representative specimens and a diagnostic key to all species are provided, along with their distribution in southern Yemen. The taxonomically most valuable characters in the genus are those of flowers (calyx, corolla, androecium and gynoecium) and nutlets, and those characters are thoroughly investigated and discussed. Both light and scanning microscopy are used in the investigation. Papillate anther apices (brush-like) were recognized in some species. Connate anthers and deep or shallow ventral circular depressions on the nutlets were found to be useful in distinguishing members of H. sect. Orthostachys (viz. H. strigosum, H. rariflorum and H. ovalifolium), while winged nutlets were found only in H. pterocarpum. The length and hairiness of the style and stigma also proved to be taxonomically useful.

Boraginaceae s.l. is one of the largest families of dicoty- system of five genera was initially suggested: Nutt., ledonous angiosperms. On the account of its broadly Heliotropium L., Ixorhea Fenzl, Small and Tourne- drawn limits, it faces some debate on both the ordinal fortia L. Recently, the genus Euploca Nutt. has increasingly and the infra-familiar levels. It was placed in an uncer- accepted as a valid genus (Melo and Semir 2006, 2009, 2010, tain ordinal position by the Angiosperm Phylogeny Melo et al. 2009, Acevedo-Rodríguez and Strong 2012, Group, APG III (2009) [ – , subgroup Degen Naumann and Melo 2012), While,the validity of the Euasterids I]. The phylogenetic relationships within genus L. as a separate genus has become the family are still unclear. Currently, a concept of six questioned and some authors prefer to nest it within sub-families (Codonoideae, Wellstedioideae, Cordioideae, Heliotropium L. (Craven 2005, Luebert et al. 2011). Ehretioideae, and Boraginoideae) is Recently, biogeographers have recognized the south- still widely accepted. However, a taxon of ordinal rank western region of the Arabian Peninsula and southern (), comprising six smaller families (Boraginaceae Yemen as a part of the floristic hotspot the African Horn s.s., Hydrophyllaceae, Heliotropiaceae, Cordiaceae, Ehre- (Mittermeier et al. 1998, Myers et al. 2000). Heliotropium tiaceae, Codonaceae and Wellstediaceae) is increasingly L. in Arabia, and particularly in Yemen, has always been being used instead of Boraginaceae s.l (Böhle and Hilger problematic. Many species exhibit great polymorphism 1997, Ferguson 1999, Smith et al. 2000, Gottschling that make them hard to identify accurately. Hence, the et al. 2001, 2004, Stevens 2001, Hilger et al. 2005, Cohen number of Heliotropium species accepted as represented 2013, Refulio-Rodriguez and Olmstead 2014, Weigend in Yemen has changed through time. Forsskål (1775) et al. 2014). was the first to report 5 taxa belonging to Heliotropium The terminal style (in contrast to the gynobasic style in the area, while and Deflers (1889) recorded 7 species. of sub-family Boraginoideae), and its uniquely modified Recently, Gabali and Al-Gifri (1990) recorded 10 species, stigmatic head that consists of a basal annulus and a conical Wood (1997) reported the presence of 12 species, while infertile apex, are the best characters distinguishing the sub- Boulos (1988) accepted 9 species and two subspecies. family Heliotropioideae. Recently, a phylogenetic analysis The present study aims were to: 1) revise the different using data obtained by trnL and ITS 1 gene sequences taxa belonging to Heliotropium L. in the flora of Yemen, 2) supported the idea of raising Heliotropioideae to the familiar evaluate the taxonomic characters and attempt to find new rank as Heliotropiaceae Schrad. (Diane et al. 2002, Hilger ones that can be used in the classification of the genus in the and Diane 2003). At the same time, generic limits have also region, and 3) provide a revised synopsis and a diagnostic changed dramatically. Within Heliotropiaceae Schrad, a key for the genus in Yemen.

401 Material and methods 8. Heliotropium pterocarpum (A. DC.) Hochst. & Steud. ex Bunge material V Section Rutidotheca (A. DC.) Verdc. 9. Heliotropium longiflorum (A. DC.) Jaub. & Spach Morphological data of Yemen taxa of Heliotropium subsp. longiflorum were scored by examination of herbarium specimens i. var. longiflorum collected from different localities in southern Yemen, ii. var. stenophylum (O. Schwartz) Verdc. representing different habitats, and kept at ASTU. Some VI. Section Zeylanica Förther Saudi Arabian specimens were also investigated. High 10. Heliotropium zeylanicum (Burm. f.) Lam. quality digital photos of type specimens and authentic material were seen by the authors as indicated by (!) in the text. Key to the species

Light microscopy 1 Corolla completely yellow, or yellowish green; anthers Willd 8 and Willd 3 Zewz stereomicroscopes were bidentate …………………………… 10. H. zeylanicum used. Illustrations were made with a Camera Lucida – Corolla completely white, or tinged with yellow at the and photographs with a Canon IXUS 960 IS digital throat; anthers not bidentate ………………………… 2 camera. 2 bracteate; calyx-lobes unequal; nutlets with ventral cavities ……..……………..…………...... … 3 Scanning electron microscopy (SEM) – Inflorescence ebracteate; calyx-lobes equal or not; Material for SEM were prepared by mounting plant nutlets with or without ventral cavities .…...…………… 4 segments onto clean stubs using double-sided cellotape. 3 Subshrubs or herbs; bracts prominent; corolla 1.5– The stubs were coated with gold in a JEOL JFC 1100 E 2.0 (–2.5) mm long; anthers with erect apiculate apex; ion sputtering device, and then examined in a JEOL JSM stigma depressed ……………………… 3. H. rariflorum 5400LV scanning electron microscopy operated at an – Herbs; bracts reduced upwards; corolla 2.0–4.0 mm accelerated voltage of 15 kV at the Electron Microscopy long; anthers with curved apiculate apex, stigma not Unit (EMU), Assiut Univ., Egypt. Terminology follows depressed …..…....…………………… 2. H. strigosum Lawrence (1959), Radford et al. (1974) and Harris and 4 Corolla 3.0–5.0 mm long; nutlets 4 …....…………… 5 Harris (1994). – Corolla 5.0–7.0 mm long; nutlets 2 or 4 .…….…… 8 5 Style obsolete; stigma  sessile .…….………………… 6 – Style at least 0.2 mm long …….…………………… 7 Synopsis of the genus Heliotropium L. in 6 Greyish herb; calyx-lobes unequal with one large ; south Yemen corolla hairy inside; anthers connate when young; stigma with apical hairs; nutlets with ventral cavities The infra-generic classification proposed by Förther (1998) ……….……..…...…………………… 4. H. ovalifolium is followed here as outlined below, with the species (num- – Green herb; calyx-lobes equal; corolla glabrous inside; bered) represented in Yemen indicated within each section anthers not connate; stigma glabrous; nutlets without and subsection. cavities ………...... …………………… 1. H. europaeum 7 Flowers lax, in 1-rank, swollen at the base; anther ovate, inserted 1.00–1.25 mm from the base; style 0.2–0.5 mm Heliotropium L. (1753, p. 130) long; stigma 0.50–0.75 mm long, glabrous, longer than the style …..……….……………… 7. H. ramosissimum Taxonomic synonyms: Euploca Nutt. (1837, p. 189). – Flowers dense, in 2-ranks, swollen at the middle; anther – Piptoclaina G. Don (1837, p. 364). – Heliophytum (Cham.) oblong-lanceolate, inserted 0.5–1.0 mm from the base; A. DC. in DC. (1845, p. 551). style 0.5–0.7 mm long; stigma 0.7–1.0 mm long, gla- I. Section Heliotropium brous, or with few scattered hairs, equaling or longer than 1. L. the style …….………………………. 6. H. bacciferum II. Section Orthostachys R. Br. 8 Nutlets 2 (2-seeded), with symmetric groove at apex; A. Subsect. Bracteata I. M. Johnst. leaves 0.5–4.0  0.3–2.0 cm …………...….………… 9 2. Heliotropium strigosum Willd. – Nutlets 4 (1-seeded), without groove; leaves longer i. var. strigosum and wider, up to 10.0 cm long and 7 cm wide .… ii. var. brevifolium (Wall.) C. B. Clarke ………………………………………… 9. H. longiflorum 3. Heliotropium rariflorum Stocks 9 Greyish annual; calyx-lobes unequal; stamens inserted B. Subsect. Ebracteata I. M. Johnst. below the middle of the corolla-tube; anthers 1.0–1.5 4. Heliotropium ovalifolium Forssk. mm long; style 0.5–0.7 mm long; nutlets narrowly to III. Section Pseudocoeloma Förther broadly winged …...………………. 8. H. pterocarpum 5. Heliotropium abyssinicum Vatke – Green perennial; calyx-lobes equal; stamens inserted IV. Section Pterotropium (A. DC.) Bunge above the middle and reaching the throat; anthers 6. Heliotropium bacciferum Forssk. 0.75–1.00 mm long; style 1.5–2.0 mm long, nutlets without 7. Heliotropium ramosissimum (Lehm.) Sieb. ex A. DC. wings ………………………………… 5. H. abyssinicum

402 1. Heliotropium europaeum L. (1753, p.130) (Fig. 1a) 10–32 flowers in 2-ranks; flowers ebractaete, sessile. Calyx 5-lobed; lobes fused close to the base, equal, lanceolate to Literature: Boiss. (1875, p.130), Blatter (1922, p. 309), linear-oblong, 1.5–3.0 mm  0.5–1.0 mm, hairy outside, Schwartz (1939, p. 206), Tutin (1973, p. 85), Wood (1997, glabrous inside. Corolla white, 2.0–3.5 mm, hairy outside on p. 238). tube, glabrous inside; tube 1.5–2.5 mm long; lobes oblong- Type: Europe: Netherlands, G. Clifford s.n. (lectotype: ovate to orbicular, 0.5–0.7 mm long. Stamens inserted at BM, BM000557900!), cultivated material from the gar- 0.8–1.0 mm from the base; anthers ovate, 1.00–1.25 mm  den of George Clifford III: Hartekamp Garden, Holland long, apex acute and papillate; filament indistinct. Ovary (designed by Förther), for typification see Jarvis (1993, globose to subglobose; style absent, stigma elongate conical p. 57): Heliotropium follis ovatis integerrimis, spicis conjunctis. to conical-subulate, 0.75–1.25 mm, deeply 2-fid at apex, glabrous. Fruit of 4 nutlets; nutlets ovoid, 1.5–2.5  1.0– Taxonomic synonym: H. majus Garsault (1764, t. 299) 2.0 mm, hairy, tuberculate-rugose. [nom. inval.]. Distribution Description Mediterranean area northwards to central and southern Annual to prennial herb, 20–50 cm high. Stem  terete, Europe; Asia: south Russia, Caucasia, Iran, Turkey, Afghani- erect, much branched. Leaves ovate to elliptic, 1.0–4.0  0.5– stan, Pakistan and India; Saudi Arabia (Najran and Al 2.0 cm; apex obtuse; base cuneate; margin entire; petiole Damam) and north Africa (especially in Libya). Yemen: Taiz, 0.5–3.5 cm. Inflorescence 2.0–7.0 cm long, dense, with Lahj, Dhamar, Sanaa, Ibb and Hiddah.

Figure 1. Habit of (a) H. europaeum, (b) H. strigosum var. strigosum, (c) H. strigosum var. brevifolium, (d) H. rariflorum, (e) H. ovalifolium. Scale: 1 cm in (a), 5 cm in the rest.

403 Specimens examined Heliotropium strigosum var. brevifolium: Yemen. Hamood Yemen. Hamood s.n., Tor El-Baha, 2 Feb 2011; El Nag- s.n., Tor El-Baha, Jun 2012; El Naggar and Hamood s.n., gar s.n., Taiz,; Apr 2009; El Naggar s.n., Taiz, Mar 2005; El Top of Jisr Akan (Akan Bridge), 1 Jun 2012. Naggar s.n., El-Hoban 2008; El Naggar s.n., El-Hoban, May 2007. 3. Heliotropium rariflorum Stocks (1852, p. 174) (Fig. 1d) 2. Heliotropium strigosum Willd. (1798, p. 743) (Fig. 1b–c) Literature: Boiss. (1875, p. 144), Verdc. (1991, p. 70), Collenette (1991, p. 91), Wood (1997, p. 239), Thulin Literature: Boiss. (1875, p. 143), Blatter (1916, p. 254, (2006, p. 50). 1922, p. 311), Collenette (1991, p. 92), Verdc. (1991, Type p. 72), Wood (1997, p. 239), El-Hadidy and Boulos (2000, : Pakistan, Scinde, Jemadar Ka Landa near Kurrachi p. 276–277), Thulin (2006, p. 51). [Karachi], Stocks 492, 1851 (lectotype: K). For typification see Akhani and Förther (1994, p. 260). Based on the same type: Euploca strigosa (Willd.) Diane & Taxonomic synonym Hilger (2003, p. 49). : H. pseudostrigosum Dinter (1922, p. 250). Type: Ghana [Guinea], Isert s.n. (holotype: B, B-WILLD 3253, isotypes: C, C10003972!; P, P-JU 6571). Description Strigose subshrub or perennial herb with woody base, 40– Two varieties of H. strigosum can be recognized in Yemen: 80 cm high. Stem terete, erect, much-branched; branches 1 Bracts linear-lanceolate (1.0–2.0 mm wide); corolla lobes with white peeling epidermis. Leaves lanceolate to linear, triangular; nutlets small (1.0–1.2 mm) ……var. strigosum 0.4–2.0  0.1–0.5 cm; apex acute; base cuneate; margin – Bracts ovate (2.0–3.0 mm wide); corolla lobes rounded; revolute; sessile or shortly petioled with petiole up to 0.1 nutlets large (1.3–1.5 mm) ...... …………var. brevifolium cm long. Inflorescence lax, 1.3–9.0 cm, of 6–20 flowers in 1-rank; flowers bracteate and pedicelled; bracts linear-lan- Description ceolate, 1.5–2.5 mm; pedicel 0.5–1.0 mm. Calyx 5-lobed; Annual herb or short-lived perennial with woody base, 5– lobes fused close to the base, unequal, lanceolate to ovate, 40 cm high. Stem  terete, much-branched; branches 1.0–2.0  0.5–1.0 mm, hairy outside, glabrous inside. prostrate to erect. Leaves lanceolate to linear or narrowly Corolla white, 1.5–2.5 mm, hairy outside and inside; tube elliptic, 0.5–4.0  0.1–0.5 cm; apex acute; base cuneate; 1.5–2.0 mm; lobes ovate to oblong, 0.5–1.0 mm, curved margin revolute; petiole 0.1–0.2 cm. Inflorescence lax, inwards. Stamens inserted 1.00–1.25 mm from the base; 1.5–8.5 cm, of 5–15 flowers in 1-rank; flowers bracte- anthers connate when young, ovate, 0.5–1.0 mm long, api- ate (bract 1.0–3.0 mm), subsessile or shortly pedicelled; culate at apex, with connective tissue prolonged and erect; pedicle 0.5–1.5 mm. Calyx 5-lobed; lobes fused close to the filament ca 0.1 mm long. Ovary subglobose; style 0.5–0.1 base, unequal, ovate to narrowly elliptic, 1.5–3.0  0.50– mm, papillate, two to three times longer than stigma; stigma 0.75 mm, hairy outside, glabrous inside. Corolla white, depressed capitate/conical, 0.2–0.5 mm, entire at apex, pap- 2.5–4.0 mm, hairy outside on lobes and upper part of tube, illose and with apical tufts of hairs. Fruit of 4 nutlets; nutlets hairy inside above the anthers; tube 2.0–3.0 mm; lobes ovoid, (1.0–) 2.0–2.5  1.0–1.5 mm, hairy, with two ventral triangular or rounded to oblong, 0.5–1.0 mm. Stamens circular depressions. inserted 1.00–1.25 mm from the base; anthers connate when young, ovate, 0.75–1.00 mm, their apex apicu- Note ate and hairy, with connective tissue prolonged and According to Verdcourt (1991), H. rariflorum can be divided curved; filament ca 0.1 mm. Ovary globose to sublo- into two subspecies: subsp. rariflorum and subsp. hereoense bose; style 0.25–0.50 mm, glabrous; stigma short coni- (Schinz) Verdc. This classification is based upon nutlet hairs. cal, (0.30–) 0.50–0.75 mm, 4-lobed at apex, hairy and Our specimens are characterized by spreading bristly hairs papillose, longer than or equal to the style. Fruit of 4 on nutlets which matches subspecies rariflorum. nutlets; nutlets ovoid, 1.0–1.5(–2.0)  0.5–1.0 mm, hairy, with two deep ventral circular depressions. Distribution Northeast tropical Africa (in Dijouti, Eritrea, Ethiopia, Distribution Sudan and Somalia); tropical Africa (in Kenya, Tanzania, Egypt; tropical region of Africa; Saudi Arabia (Najran Angola and Namibia); Arabia (Saudi Arabia: Asir); Asia (Iran and Hejaz); Asia: Pakistan, Iran, India and Sri-Lanka; and Pakistan). Yemen: Lahj, Aden, Abyen and Socotra. and eastern Asia: China and Japan. Yemen: Taiz, Lahj, Tihama, Abyen, Hadhramaut and Socotra. Specimens examined Yemen. Hamood s.n., Tor El-Baha, 2012. Specimens examined 4. Heliotropium ovalifolium Forssk. (1775, p. 38) Heliotropium strigosum var. strigosum: Yemen. El Naggar (Fig. 1e) s.n., Habil Al-Salman Taiz, Nov 2008; El Naggar s.n., Habil Al-Salman Taiz, 10 Oct 2008; El Naggar s.n., Jabal Literature: Blatter (1922, p. 310), Schwartz (1939, p. 205), Sabr-Taiz, Apr 2008; El Naggar s.n., Wadi Al-Quadi, Verdc. (1991), Wood (1997, p. 238), El-Hadidy and Boulos Taiz, Apr 2008; El Naggar s.n., El-Hoban, Oct 2006. (2000, p. 277), Thulin (2006, p. 50). 404 Type: [Yemen]; Al-Hadiyah [Hadïe], 3.1763 Forsskål 299 lanceolate to lanceolate-oblong, 1.5–2.0  0.2–0.4 mm, (holotype: C, C10002362!, isotype: BM). hairy outside, glabrous inside. Corolla white with green center, 4.0–7.0 mm, hairy outside, glabrous inside; tube Taxonomic synonym: H. kunzei Lehm. (1823, p. 19), Boiss. 3.5–4.0 mm; lobes ovate, 1.5–2.0 mm. Stamens inserted (1875, p. 130). 2.25–2.50 mm from the base; anthers oblong, 0.75– Description 1.00 mm, acute at apex; filament indistinct. Ovary glo- Greyish herbaceous annual or short-lived perennial, 10– bose to subglobose; style 0.5–2.0 mm, glabrous, distinctly 90 cm high, woody at the base, covered with appressed hairs. longer than stigma; stigma elongate conical, 0.5–1.0 mm; Stem  terete, much-branched; branches procumbent or apex shortly 2-fid, glabrous. Fruit of 2 nutlets; nutlets erect to ascending. Leaves ovate or elliptic, 0.5–5.0  0.3– broadly ovoid and shallowly notched at apex and base, 2.0–  3.0 cm; apex acute; base attenuate; margin entire; petiole 2.5 1.5–2.0 mm, with a shallow groove at the middle from 0.2–2.0 cm. Inflorescence dense, 2.0–10.0 cm, of 10–30 apex to base, laterally constricted near apex, hairy, rugulose. flowers in 2-ranks; flowers ebracteate, subsessile or shortly Distribution pedicelled with pedicle 0.5–1.5 mm. Calyx 5-lobed; lobes Northeast tropical Africa: Somalia, Ethiopia and Sudan. fused close to the base, unequal with one lobe distinctly Yemen. Taiz, Lahj, Sana’a El-Hoban and Hadhramaut. larger, ovate to lanceolate-oblong, 1.0–3.0  0.2–0.8 mm, hairy outside, glabrous inside. Corolla white, 3.0–5.0 mm Specimens examined long, hairy outside and inside; tube 2.0–4.0 mm; lobes ovate Yemen. El Naggar and Hamood s.n., Taiz, 31 May 2012; to oblong or elliptic, 0.5–1.0 mm. Stamens inserted 0.75– El Naggar and Hamood s.n., Tor El-Baha, Lahj, May 2012; 1.00 mm from the base; anthers connate when young, ellip- El Naggar and Hamood s.n., Hida, 27 May 2012; Hamood tic to ovate, 0.5–1.0 mm long, apiculate and hairy at apex, s.n., Tor El-Baha, 14 Nov 2009; El Naggar s.n., Taiz, Nov with connective tissue prolonged, elongated and curved; 2009; El Naggar s.n., Habil Al-Salman Taiz, Oct 2008; El filament indistinct. Ovary subglobose; style absent; stigma Naggar s.n., El-Hoban, Jun 2007; El Naggar s.n., Taiz, Oct short conical, 0.5–1.0 mm, 2-lobed at apex, papillose and 2006. with apical hairs. Fruit of 4 nutlets; nutlets ovoid to ellip-  tic, 1.0–2.0 1.0–1.5 mm, hairy, with two ventral circular 6. Heliotropium bacciferum Forssk. (1775, p. 38) depressions. (Fig. 2b–c)

Distribution Literature: Blatter (1922, p. 308), Schwartz (1939, p. 211), North Africa: Egypt and Libya; Arabia (Oman: Dhofan); Collenette (1991, p. 89), El-Hadidy and Boulos (2000, p. southeast Asia; tropical Africa: Somalia, New Guinea, 279). Madagascar and Mascarene Islands; with slight extension to Australia and Europe (in Turkey). Yemen: Taiz, Bura’a, Lahj, Type: Arabia: Yemen; Lahaja [Al Luhayyah], 1.1763, Forsskål Tihama and Socotra. 1329 (C, C10002532, microfiche foto!; isotype: BM, KIEL). See Hepper and Friis (1994) and Förther (1998) for details. Specimens examined Taxonomic synonyms: Lithospermum hispidum Forssk. Yemen: Hamood s.n., Tor El-Baha, 27 Oct 2010; Hamood (1775, p. 38). – Heliotropium crispum Desf. (1798, p. 151, s.n., Tor El-Baha, 10 Oct 2009; El Naggar s.n., Bura’a t. 41). – H. undulatum Vahl (1790, p. 131) [nom. illeg.], Reserve, Nov 2007; El Naggar s.n., Taiz, Mar 2007; El Nag- Boiss. (1875, p. 147), Schwartz (1939, p. 206). gar s.n., Jan 2006; El Naggar s.n., Jan 2005; El Naggar s.n., Wadi Bara, Mar 2006. Description Perennial herb, 20–40 cm high, woody at the base, covered 5. Heliotropium abyssinicum Vatke (1875, p. 168) by scabrous indumentum. Stem terete, much-branched; (Fig. 2a) branches erect or ascending. Leaves lanceolate to linear, 0.5– 3.0  0.5–1.5 cm; apex acute; base cuneate or attenuate; Type: Abyssinia: Habab in locis sterilibus, Aug 1872, 7000, margin undulate-crenate and revolute; petiole 0.0–1.0 cm. Aug 1872, Hildebrandt 470/b (holotype: B, isotypes: BM, Inflorescence dense, 0.5–4.2 cm, of 5–13 flowers in 2-ranks; LE, W). flowers ebracteate, sessile. Calyx 5-lobed; lobes free almost to Taxonomic synonym: H. bottae Deflers (1889, p. 172, the base, equal, ovate-oblong or lanceolate, 1.0–3.0  0.50– t. 5), Blatter (1922, p. 308), Schwartz (1939, p. 205), Wood 0.75 mm, hairy outside and in the upper part inside. Corolla (1997, p. 238). white, 3.0–5.0 mm, hairy on tube outside, glabrous inside; tube 2.0–4.0 mm; lobes ovate to oblong or suborbicular, Description 0.5–1.5 mm. Stamens inserted 0.5–1.0 mm from the base; Perennial herb, 10–100 cm high, woody at the base. Stem anthers oblong-lanceolate, 0.75–1.00 mm, acute or shortly terete, branched; branches erect to ascending. Leaves broadly apiculate at apex; filament indistinct. Ovary ovate; style ovate, 0.5–4.0  0.3–2.0 cm; apex acute; base cuneate; 0.4–0.7 mm, glabrous; stigma elongate conical, 0.7–1.0 mm margin undulate; petiole 0.5–2.0 cm. Inflorescence lax, (with stigmatic ring 0.1–0.2 mm high), 2-/4-lobed or 2-fid 1.1–6.0 cm, of 10–27 flowers in 2-ranks; flowers ebracteate, at apex, glabrous or with few scattered hairs, equaling or lon- sessile. Calyx 5-lobed; lobes free almost to the base, equal, ger than style. Fruit of 4 nutlets; nutlets ovoid to elliptic,

405 Figure 2. Habit of (a) H. abyssinicum, (b)–(c) H. bacciferum, (d)–(e) H. ramosissimum, (f) H. pterocarpum, (g) H. longiflorum, (h) H. zeylanicum. Scale: 1 cm in (a), (e), (g), (h), 5 cm in (d), (f), 15 cm in (b).

1.5–2.0  0.75–1.00 mm, with narrow wing-like margins, 7. Heliotropium ramosissimum (Lehm.) Sieb. ex A. hairy or glabrous, often with corky tissue, rugulose. DC., in DC. (1845, p. 536) (Fig. 2d–e)

Distribution Literature: Collenette (1991, p. 91), Wood (1997, p. 239), Extending from Egypt in Meditterranean north Africa east- El-Hadidy and Boulos (2000, p. 280). wards to Pakistan, southwards in Sudan and northeast Africa Basionym H. undulatum . ramosissimum and in Saudi Arabia(Asir). Yemen: Taiz, Ibb, Sana’a, Tihama : Vahl var Lehm. and Hadhramaut (1831, p. 24, t.40). Type: Egypt, Wadi Gamuhs, Sieber s.n. (isotype: K; GH, Specimens examined GH00097757!). Yemen. El Naggar and Hamood s.n., Taiz, 31 May 2012; El Naggar and O. Hamood s.n., Sana’a Univ. ground, 25 May Taxonomic synonym: H. persicum Boiss. (1875, p. 147), 2012; El Naggar and Hamood s.n., Wadi Al-Eshsh; May non Lam. (1789). Schwartz (1939, p. 207). 2012; Hamood s.n., Tor El-Baha, 2012; Hamood s.n., Tor El-Baha, 3 Jan 2010; El Naggar s.n., Jabal Sabr, Taiz, Oct Description 2006; El Naggar s.n., Ibb, Jul 2006; El Naggar s.n., Habil Perennial herb, 20–50 cm high, woody at the base, covered by Al-Salman, Taiz, Oct 2008; El Naggar s.n., Taiz, Oct 2008; scabrous indumentum of simple hairs associated with white El Naggar s.n., Taiz, Nov 2007. sharp bristles. Stem terete, much-branched; branches erect

406 or ascending. Leaves elliptic, 0.5–3.0  0.5–1.5 cm; apex glabrous; stigma elongate conical, 0.4–0.6 mm, obscurely acute; base cuneate or attenuate; margin undulate-crenate to 4-lobed at apex, papillose, equaling or shorter than style. entire and revolute; petiole 0.0–1.0 cm. Inflorescence lax, Fruit of 2 nutlets; nutlets  oblong (excluding wings) and 0.5–1.5 cm, of 5–14 flowers in 1-rank; flowers ebracteate, with a deep sinus at apex and base, 2.0–3.0  3.0–4.0 mm sessile. Calyx 5-lobed; lobes free almost to the base, equal, (excluding wings), winged (narrow to broad, wings 1.0– lanceolate-oblong to lanceolate, 1.0–3.0  0.50–0.75 mm, 3.0 mm wide), glabrous, minutely tuberculate to rugulose. hairy outside, hairy inside. Corolla white, 3.0–5.0 mm long, hairy on tube outside, glabrous inside; tube 2.0–4.0 mm Distribution long; lobes ovate to oblong or suborbicular, 1.0–2.0 mm. North Africa: Egypt; western Arabia; northeast tropical Stamens inserted at 1.00–1.25 mm from the base; anthers Africa through Sudan and Ethiopia. Yemen: Jisr Akan, Lahj, ovate, 0.75–1.00 mm long, apex acute or shortly apiculate; Taiz, Tihama and Hadhramaut. filament indistinct. Ovary globose to ovate; style 0.2–0.5 mm, glabrous; stigma elongate-conical, 0.50–0.75 mm, Specimens examined 2-(4-)lobed at apex, glabrous, equaling or longer than style. Yemen. El Naggar and Hamood s.n., Top of Jisr Akan (Akan Fruit of 4 nutlets; nutlets ovoid, 1.0–1.5  0.75–1.00 mm, Bridge), 1 Jun 2012; El Naggar and Hamood s.n., Wadi with narrow wing-like margins, hairy or glabrous, rugulose. El-Dabab, Hifan, Taiz, May 2012; Hamood s.n., Tor El-Baha, 2012; El Naggar s.n., Habil Al-Salman, Taiz, Oct Distribution 2008; El Naggar s.n., Al-Anabi, Jan 2008; El Naggar s.n., Extending from India westwards through Iran, Afghani- Habil Al-Salman, Taiz, Oct 2006. stan and southwest Asia to Palestine, Egypt (Sinai); across north Africa to Morocco and southwards to northeast Africa, 9. Heliotropium longiflorum (A. DC.) Jaub. & Spach and in eastern and northeastern Arabia. Yemen: Jisr Akan (1852, p. 96, t. 360) subsp. longiflorum (Fig. 2g) between Taiz and Lahj, Socorta. Literature: Blatter (1922, p. 309), Schwartz (1939, p. 210), Specimens examined Collenette (1991, p. 90), Verdc. (1991, p. 67), Wood (1997, Yemen. El Naggar and Hamood s.n., Top of Jisr Akan (Akan p. 238). Bridge), 1 Jun 2012. Basionym: Heliophytum longiflorum A. DC. in DC. (1845, p. 555). 8. Heliotropium pterocarpum (A. DC.) Hochst. & Steud. ex Bunge (1869, p. 331) (Fig. 2f) Type: Arabia: Saudi Arabi; Djebel Sidr [Mt Sedder], inter rupes montis Sedder Arabiae felicism 29 Feb 1836, Schimper Literature: Blatter (1916, p. 256, 1922, p. 311), Schwartz 842 (holotype: G-DC, GH00097510!, isotype: BM). (1939, p. 205), Collenette (1991, p. 91), Wood (1997, p. Taxonomic synonym: H. gracile R. Br. (1814, p. 62) [Nom. 238), El-Hadidy and Boulos (2000, p. 279), Thulin (2006, nud.]. p. 49). Two varieties of H. longiflorum can be recognized: Basionym: Heliophytum pterocarpum A. DC. in DC. (1845, 1 Leaves ovate, 0.5–1.5 cm wide; inflorescence 10.5–23.0 p. 552). cm long, slightly lax; corolla constricted above the base Type: Arabia, in planitie deserti prope Dscheddam, 29 Feb …....………….….…….……………… var. longiflorum 1836. Schimper 835 (ed. 1, 1837, ed. 2, 1843) (holotype: – Leaves linear-lanceolate, 0.2–0.5 cm wide; inflorescence G-DC, syntype: K). 5.0–10.0 cm long; more dense, corolla not constricted … …...... var. stenophyllum Taxonomic synonym: Heliotropium deserti Vatke (1875, p. 166). Description Description Perennial herb, 50–60 cm high, woody at the base, densely Annual herb, 10–55 cm high, covered with scabrous indu- covered with 2-branched unicellular hairs (T-shaped). Stem mentum of white bristles intermixed with simple deflexed  terete, branched; branches erect to ascending. Leaves hairs. Stem terete, simple or branched; branches prostrate ovate, 1.0–6.0  0.1–3.5 cm; apex acute; base cuneate; to ascending. Leaves rhombic-ovate, 0.5–3.5  0.3–1.5 margin entire; petiole 0.1–2.0 cm. Inflorescence lax to cm; apex acute or obtuse; base attenuate; margin undulate- slightly dense, (2.0–)10.0–15.0 cm, of 22–77 flowers in crenate; petiole 0.2–0.5 cm. Inflorescence very dense and 1-rank; flowers ebracteate, sessile. Calyx 5-lobed; lobes free crowded, 0.5–1.2 cm long, of 8–14 flowers in 2-ranks; flow- almost to the base, equal, oblong to lanceolate-linear, 0.5– ers ebracteate, sessile. Calyx 5-lobed; three lobes free almost to 1.5  0.2–0.5 mm, hairy outside, glabrous inside. Corolla the base and two connate almost to the top, unequal, oblong white, 3.0–6.0 mm, hairy outside, glabrous inside; tube to linear, 3.5–4.5  0.5–1.0 mm, hairy outside and inside. 2.0–4.0 mm; lobes triangular, 1.0–1.5(–2.0) mm. Stamens Corolla white, (3.5–) 4.0–7.0 mm, hairy on tube outside, inserted 1.0–2.5 mm from the base; anthers lanceolate or glabrous inside; tube 3.5–5.0 mm; lobes ovate, 0.8–2.0 mm lanceolate-oblong, 1.0–2.5 mm, obtuse apex at; filament ca long. Stamens inserted 1.5–2.0 mm from the base; anthers 0.1 mm. Ovary subglobose, glabrous; style 0.5–1.5 mm, lanceolate, 1.0–1.5 mm, acute or apiculate at apex; filament glabrous; stigma elongate conical, 0.5–1.0 mm, apex shortly indistinct. Ovary subglobose to elliptic; style 0.5–0.7 mm, 2- or 4-fid, glabrous, shorter than style. Fruit of 4 nutlets;

407 nutlets ovoid, (1.5–) 2.0–3.0  1.5–2.0 mm, with ridge-like Distribution margin, glabrous, reticulate-rugose; margin rugose to Egypt; Arabia; Pakistan; India; tropical Africa; south Africa; aculeate. Madagascar and Mascarene Islands. Yemen: Taiz, Sana’a, Tihama, Lahj and Socotra. Distribution Northeast tropical Africa: Djibouti, Eritrea, Sudan and Specimens examined Somalia; tropical Africa: Kenya, Uganda and Tanzania; the Yemen. El Naggar and Hamood s.n., Taiz, 31 May 2012; Arabian Peninsula: Saudi Arabia (Asir and Najran). Yemen: Hamood s.n., Tor El-Baha, 9 Nov 2009; El Naggar s.n., Taiz, Lahj, Tihama, Abyen and Hadhramaout. El-Hoban, Apr 2009; El Naggar s.n., Habil Al-Salman, Taiz, Oct 2008; El Naggar s.n., El-Hoban, Apr 2008; El Naggar Specimens examined s.n., Taiz, Oct 2006; El Naggar s.n., Wadi El-Enabi, Ibb, Heliotropium longiflorum var. longiflorum: Yemen. El Oct 2005. Naggar and Hamood s.n., Taiz, 31 May 2012; El Naggar and Hamood s.n., Tor El-Baha, Lahj, May 2012; El Naggar s.n., Habil Al-Salman, Taiz, Oct 2008; El Naggar s.n., Habil Discussion Al-Salman, Taiz, Apr 2005. In spite of its distinct characters, taxonomically, Heliotropium Heliotropium longiflorum var. stenophylum: Yemen. El Nag- is considered a difficult genus in the flora of Yemen, and it gar and Hamood s.n., Hida, 27 May 2012; El Naggar and has not got proper attention. In the classical works, the Hamood s.n., Wadi Al-Eshsh; May 2012; El Naggar and of Heliotropium in Yemen was poorly investigated Hamood s.n., Sana’a University ground, 25 May 2012; under the wide-scoped floristic studies of the Arabian Hamood s.n., Tor El-Baha, 2012; El Naggar s.n., Taiz, Peninsula (Forsskål 1775, Deflers 1889). Perhaps, the most 2007. comprehensive floristic study of Yemen is the one done by Wood (1997). However, it lacks synonyms as well as type 10. Heliotropium zeylanicum (Burm. f.) Lam. (1789, citations. Many unclear matters concerning the recogni- p. 94) (Fig. 2h) tion of Heliotropium taxa in Yemen were still debateble. For example, there have been no clear delimitation of Literature: Blatter (1916, p. 255), Blatter (1922, p. 313), H. bacciferum, H. ramosissimum and H. pterocarpum; Schwartz (1939, p. 204), Collenette (1991, p. 92), Verdc. some authors such as Akhani and Förther (1994) and (1991, p. 56), Wood (1997, p. 239), El-Hadidy and Boulos Förther (1998) preferred to treat H. bacciferum and (2000, p. 272), Thulin (2006, p. 46). H. ramosissimum as a species complex under the name of Basionym: H. curassavicum L. var. zeylanicum Burm.f. H. bacciferum Forssk. s.l., here, the two taxa are distin- (1768, p. 41, t. 16/2). guished and H. ramosissimum is treated as a valid species. Heliotropium undulatum was mentioned as a synonym of Type: south India: Madras; Tutikorin, Garcin s.n. (holotype: H. ramosissimum by Wood (1997), but is treated here as G-BURM). a synonym of H. bacciferum. On the other hand, Wood Taxonomic synonyms: Tournefortia subulata Hochst. ex A. (1997) stated that the type of H. bacciferum described DC., in DC. (1845, p. 528). – Heliotropium subulatum (A. by Forsskål from Luhayyah, seemed to be H. pterocar- DC.) Vatke (1882, p. 316). pum, and consequently he excluded H. bacciferum from the flora of Yemen, here, we recognize that type to be Description H. bacciferum and is fairly distinct from H. pterocarpum. Perennial herb, 30–60 cm high, woody at the base. Stem Another case is in the taxonomy of H. bottae, which was terete, branched; branches erect. Leaves lanceolate to lin- described by Wood (1997) as having 4 nutlets; the speci- ear, 0.8–10.0  0.2–2.5 cm; apex acute; base attenuate; men seems to be misidentified, because that taxon has margin entire; petiole (0.1–)0.3–1.5 cm. Inflorescence lax, only two nutlets and here that taxon is treated under the (5.0–)10.0–23.0 cm, of 11–34 flowers in 1-rank; flowers name H. abyssinicum. There is another plant in Somalia ebracteate, sessile. Calyx 5-lobed; lobes free almost to the and tropical Africa that is morphologically very close to base, equal, ovate to narrowly elliptic, 1.0–3.0 mm  0.5– H. abyssinicum; Thulin (2006) treated these as one species 1.0 mm, hairy outside and in the upper part inside. Corolla under the name H. steudneri Vatke, however, this point yellow to yellowish green, 5.0–7.0 mm, hairy outside, gla- still need to be clarified by examination of Somali and brous inside; tube 3.0–4.0 mm; lobes ovate, 2.0–3.5 mm, African specimens. with small intercalary teeth. Stamens inserted 1.5–2.5 In recent few years, some check-lists claimed to comprise mm from the base; anthers oblong-lanceolate, 1.0–1.5 all the plant taxa in the flora of Yemen. However, these mm, apex bidentate; filament indistinct. Ovary globose, lists still need critical taxonomic revision. For example, in glabrous; style 0.7–1.5 mm, glabrous; stigma elongate- the list by Al-Khulaidi (2013), the number of species of conical, 1.0–1.7 mm, 2-lobed at apex, hairy throughout Heliotropium L. in Yemen (including Socotra) is as high and with apical tufts, longer than or equaling style. Fruit of as 44 (and only 5 of them are endemic to Socotra). That 4 nutlets; nutlets ovoid, 1.5–2.0  1.0–1.5 mm, glabrous, number is clearly exaggerated, and is caused by misuse of rugose. synonyms.

408 Nomenclature suggestions H. zeylanicum is unique by the possession of caudate corolla- lobes wich are 5.0–7.0 (–9.0) mm long, and by the presence The name H. abyssinicum is found to have priority over of intercalary teeth at the sinus. The rest of the species have H. bottae. As varietal epithets, strigosum and bervifolium seem acute or obtuse or retuse apex, and lengths up to 2.0 mm. to have priority for the two varieties of H. strigossum (instead 3) Androecium: shape, apex and connation while young of var. bicolor and var. cordofanum used by some authors). A proved to be variable characters. A bidentate apex is unique full list of synonyms for taxa of Heliotropium L. can be found to H. zeylanicum (Fig. 5). Occasionally in Heliotropium spe- in Förther (1998). cies, the connective tissue is prolonged to form an apiculate, Many authors have stressed the paramount taxonomic sterile apex. This apex is erect or curved, papillate (Fig. 6b) or importance of reproductive characters in the taxonomy of glabrous, free or connate in young stages. Connate (Fig. 6a) Heliotropium, among them Brown (1810), De Candolle and apiculate apices have been used to classify the genus into (1845), Bunge (1869), Boissier (1875), Clarke (1885), sections or subgenera (Brown 1810, Bentham and Hooker Gürke (1893), Johnston (1928), Riedl (1967) and Förther 1876, Riedl 1967, Verdcourt 1991, Förther 1998) as in (1998). The following is a list of the most important H. strigosum, H. rariflorum and H. ovalifolium of sect. morphological characters for distinguishing species of the Orthosyachys (formerly as subgenus). genus in the flora of southern Yemen: 4) Style: presence or absence, length and surface of style are of paramount taxonomic value. Heliotropium strigo- 1) Calyx: shape and size of calyx-lobes have proved to be of sum, H. bacciferum and H. ramosissimum possess glabrous taxonomic importance. H. strigosum, H. rariflorum, H. ovali- styles; while papillate styles are typical for H. rariflorum. The folium and H. pterocarpum possess unequal calyx lobes; while style is short (0.2–0.5 mm long) in H. ramosissimum, but the other species possess equal ones (Fig. 3). The shape of the relatively longer (0.5–0.7 mm) in the closely allied species calyx lobes varies from ovate to lanceolate-oblong/ -linear, or H. bacciferum. narrowly elliptic, and the lobes varies in size, 0.5–4.5  0.2– 5) Stigma: shape of the stigma, length, apex, hairiness, and its 1.5 mm. relation to the style proved to be useful for distinguishing and 2) Corolla: colour, length, distribution of hairs, shape and separating certain taxa (Fig. 7). In the large-flowered species, size of lobes, as well as the presence of intercalary teeth at the stigma is elongated-conical, 0.5–1.7 mm long. Among the sinus, proved to be valuable. Flowers of H. zeylanicum these, a stigma that is hairy throughout is diagnostic for are completely yellow, while the rest of the species possess H. zeylanicum. Among the small-flowered species, the stigma white flowers. With respect to length, two categories can be of H. rariflorum is unique by being depressed capitate or coni- recognized: 1) small-flowered species (2.0–5.0 mm long), cal with entire apex; while it is short (squat-like) or elongated- 2) large-flowered species (5.0–9.0 mm long). Heliotropium conical with 2–4-lobed or -fid apex in the other species. A europaeum, H. strigosum, H. rariflorum, H. ovalifolium, stigma that is hairy throughout distinguishes H. strigosum; H. bacciferum and H. ramosissimum belong to the first cat- while apical hairs separate H. rariflorum and H. ovalifolium. egory; while H. abyssinicum, H. pterocarpum, H. longiflorum 6) Fruit: on the basis of fruit characters (number, shape and H. zeylanicum belong to the second (Fig. 4). The inside and surface), Heliotropium has been classified into sections of the corolla is glabrous in most species, but hairy in three (Bunge 1869, Föther 1998), subgenera (Riedl 1967) or even species: H. strigosum, H. rariflorum and H. ovalifolium. How- into separate genera (Don 1837). The fruit is separated into ever, these latter species may be distinguished by the distri- 4 (1-seeded) nutlets at maturity, or into 2 (2-seeded) nutlets, bution of hairs on the outside of the corolla: corolla hairy or reduced into 1 nutlet by abortion. In this study, nutlet throughout (in H. rariflorum) vs hairy in upper part only. characters proved to be useful in recognizing certain taxa:

Figure 3. Shape of calyx in (a) H. europaeum, (b) H. strigosum, (c) H. rariflorum, (d) H. ovalifolium, (e) H. abyssinicum, (f) H. bacciferum, (g) H. ramosissimum, (h) H. pterocarpum, (i) H. longiflorum, (j) H. zeylanicum.

409 Figure 4. Corolla of (a) H. europaeum, (b) H. strigosum, (c) H. rariflorum, (d) H. ovalifolium, (e) H. abyssinicum, (f) H. bacciferum, (g) H. ramosissimum, (h) H. pterocarpum, (i) H. longiflorum, (j) H. zeylanicum.

Figure 5. Anther shape of (a) H. europaeum, (b) H. strigosum, (c) H. rariflorum, (d) H. ovalifolium, (e) H. abyssinicum, (f) H. bacciferum, (g) H. ramosissimum, (h) H. pterocarpum, (i) H. longiflorum, (j) H. zeylanicum. a) Number and shape: most species in south Yemen possess H. pterocarpum, H. longiflorum and H. zeylanicum, while hairy 4 free nutlets (Fig. 8b, d, e, n). However, H. pterocarpum in H. strigosum, H. rariflorum, H. ovalifolium and H. abyssini- and H. abyssinicum have 2 (2-seeded) nutlets (Fig. 8g). cum. In two species (H. bacciferum and H. ramosissimum), the Heliotropium pterocarpum (sect. Pterotropium) is unique by nutlets are hairy or glabrous. Nutlets with a shallow groove the presence of narrow to broad lateral wings and with a deep at the middle from apex to base are found in H. abyssinicum notch at apex and base of the nutlets (Fig. 8m); while nutlets (Fig. 8h). Heliotropium strigosum (Fig. 8c), H. rariflorum and of H. abyssinicum (sect. Pseudocoelomea) lack the lateral wings H. ovalifolium (Fig. 8f) are uniquely possessing cavities (pits) and has only a shallow notch at apex and base (Fig. 8h). on the ventral surface of the nutlets. These three species belong b) Surface: hairiness, presence or absence of ventral to the section Orthostachys as defined by this character (John- cavities and sculpture are regarded as important characters ston 1928, Frohlich 1978). Diane et al. (2003) recognized this in distinguishing certain taxa. The nutlets are glabrous in character in some other taxa belonging to the same section.

Figure 6. Androecium of H. ovalifolium. (a) LM photograph showing four anthers connate at the apex, (b) SEM micrograph of the anther apex showing clavate papillae.

410 Figure 7. Shape of gynoecium of (a) H. europaeum, (b) H. strigosum, (c) H. rariflorum, (d) H. ovalifolium, (e) H. abyssinicum, (f) H. bacciferum, (g) H. ramosissimum, (h) H. pterocarpum, (i) H. longiflorum, (j) H. zeylanicum.

Figure 8. SEM micrographs of fruit/nutlet of (a) H. europaeum, (b)–(c) H. strigosum var. strigosum, (d) H. rariflorum, (e)–(f) H. ovalifolium, (g)–(h) H. abyssinicum, (i)–(j) H. bacciferum, (k)–(l) H. ramosissimum, (m) H. pterocarpum, (n)–(o) H. longiflorum, (p)–(q) H. zeylanicum.

411 References Forsskål, P. 1775. Flora Aegyptiaco–Arabica. – Copenhagen. Förther, H. 1998. Die infragenerische Gliederung der Gattung Acevedo-Rodríguez, P. and Strong, M. T. 2012. Catalogue of seed Heliotropium L. und ihre Stellung innerhalb der subfam. of the West Indies. – SISP, Washington DC, USA. Heliotropioideae (Schrad.) Arn. (Boraginaceae). – Sendtnera Akhani, H. and Förther, H. 1994. The genus Heliotropium L. 5: 35–241. (Boraginaceae) in flora Iranica area. – Sendtnera 2: 187–276. Frohlich, M. W. 1978. Systematics of Heliotropium section Al-Khulaidi, A. A. 2013. Flora of Yemen. – The Sust. Nat. Res. Orthostachys in Mexico. – PhD thesis, Harvard Univ. Man. Pro. (SNRMP II). Gabali, S. A. and Al-Gifri, A. N. 1990. Flora of south Yemen. Angiosperm Phylogeny Group. 2009. An update of the Angiosperm Angiospermae: a provisional checklist. – Feddes Rep. 101: Phylogeny Group. Classification for the orders and families of 373–383. flowering plants: APG III. – Bot. J. Linn. Soc. 161: 105–121. Garsault, F. P. De. 1764. Les figures des plantes et animaux d’usage Bentham, G. and Hooker, J. D. 1876. Genera Plantarum. Vol. 2. en medicine, decrites dans la matiere medicale de Mr Geoffroy. – London. – Paris. Blatter, E. 1916. Flora of Aden. – Rec. Bot. Surv. Ind. 7: Gottschling, M. et al. 2001. Secondary structure of the ITS1 77–336. transcript and its application in a reconstruction of the Blatter, E. 1922. Flora Arabica. – Rec. Bot. Surv. Ind. 8: phylogeny of Boraginales. – Plant Biol. 3: 629–636. 283–365. Gottschling, M. et al. 2004. Testing hypotheses on disjunctions Böhle, U. R. and Hilger, H. H. 1997. Chloroplast DNA systemat- present in the primarily woody Boraginales: Ehretiaceae, ics of ‘‘Boraginaceae’’ and related families: a goodbye to the old Cordiaceae, and Heliotropiaceae, inferred from ITS1 sequence familiar concept of 5 subfamilies. – Scr. Bot. Belg. 15: 30. data. – Int. J. Plant Sci. 165: 123–135. Boissier, P. E. 1875. Flora Orientalis sive Enumeratio Plantarum Gürke, R. M. 1893. Boraginaceae. – In: Engler, A. and Prantl, K. in Oriente a Graecia et Aegypto ad Indiae. Vol. 4. – Basileae, (eds), Die natürlichen Pflanzenfamilien, 1st ed. W. Engelann, Geneve & Lugduni, pp. 123–280. pp. 71–131. Boulos, L. 1988. A contribution to the flora of south Yemen Harris, J. G. and Harris, M. W. 1994. Plant identification termi- (PDRY). – Candollea 43: 549–585. nology: an illustrated glossary. – Spring Lake Publ., Utah, Brown, R. 1810. Prodromus Flora Novae Hollandiae. Vol. 1. USA. London, pp. 492–498. Hepper, F. N. and Friis, I. 1994. The plants of P. Forsskål’s ‘Flora Bunge, A. Von. 1869. Über die Heliotropien der Mitteländischen Aegyptiaco-Arabica: collected on the Royal Danish Expedition Orientalischen Flora. – Bull. Soc. Imp. Nat. Moscou 42: to Egypt and the Yemen 1761–1763’. – R. Bot. Gard. Kew; 279–322. Bot. Mus., Copenhagen. Burman, N. L. 1768. Flora Indica nec non Prodromus Florae Hilger, H. H. and Diane, N. 2003. A systematic analysis of Capensis. Leiden (C Haak). – J Schreuder, Amesterdam. Heliotropiaceae (Boraginales) based on trnL and ITS1 sequence Candolle, Alph-L. P. 1845. Prodromus systematis naturalis regni data. – Bot. Jahrb. Syst. 125: 19–51. vegetabilis. Vol. 9. – Paris. Hilger, H. H. et al. 2005. The Euro Med treatment of Boragi- Clarke, C. B. 1885. Boraginaceae. Hooker’s flora of British-India. naceae in Willdenowia 34 – a response. – Willdenowia 35: Vol. 4. – London. 43–48. Cohen, J. I. 2013. A phylogenetic analysis of morphological Jarvis, C. E. 1993. A list of Linnean generic names and their types. and molecular characters of Boraginaceae: evolutionary rela- – Reg. Veg. 127: 1–100. tionships, taxonomy, and patterns of character evolution. Jaubert, H.-F. C. de and Spach, E. 1852. Illustrations plantarum – Cladistics 2013: 1–31. orientalium. Vol. 4. Paris, pp. 81–96, plates 351–360. Collenette, S. 1991. Wildflowers of Saudi Arabia (NCWCD). Johnston, I. M. 1928. Studies in the Boraginaceae. VII. 1. The – East Angraving Co. Ltd., Norwich, UK. South American species of Heliotropium. – Contrib. Gray Craven, L. A. 2005. Malesian and Australian Tournefortia Herb. Harvard Univ. 81: 3–73. transferred to Heliotropium and notes on delimitation of Lamarck, J. B. 1789. Encyclopédie Méthodique Botanique. Vol. 3. Boraginaceaea. – Blumea 50: 375–381. – Paris. Deflers, A. 1889. Voyage au Yemen. – Journal d’une excursion Lawrence, G. M. 1959. Taxonomy of vascular plants, 2nd ed. Vol. botanique faite en 1887 dans les montagnes de l’Arabie 1 (Dicotyledons). – The Macmillan Co. Heureuse. Lehmann, J. C. 1822–1840. Index Semina in Hortobotanico Degen Naumann, R. and Melo, J. I. M. 2012. Nuevas combina- Hamburgeni. – Hamburgi. ciones en el género Euploca Nutt. (Boraginaceae) del Paraguay. Lehmann, J. C. 1823. Icones et Descriptiones Novarum et Minus – Candollea 67: 368. Cognitarium Stirpium, 1st ed. – Hamburgi. Diane, N. et al. 2002. A systematic analysis of Heliotropium, Linnaeus, C. von 1753. Species Plantarum, ed. 1. Laurentius Salvi, Tournefortia and allied taxa of the Heliotropiaceae (Boragi- Holmiae. nales) based on ITS1 sequences and morphological data. Luebert, F. et al. 2011. Phylogenetic relationships and morpho- – Am. J. Bot. 9: 287–295. logical diversity in neotropical Heliotropium (Heliotropiaceae). Diane, N. et al. 2003. Leaf anatomy and foliar trichomes in – Taxon 60: 663–680. Heliotropiaceae and their systematic relevance. – Flora 198: Melo, J. I. M. and Semir, J. 2006. Euploca rodaliae J. I. M. Melo 468–485. & Semir – a new species of Euploca (Heliotropiacea) from Dinter, K. 1922. Index der aus Deutsch-Südwestafrika bis zum Brazil. – Candollea 61: 453–456. Jahre 1917 bekannt gewordenen Pflanzenarten 11. – Rep. Melo, J. I. M. and Semir, J. 2009. Two new Brazilian species and Spec. Nov. Reg. Veg.18: 248–256. new combinations in Euploca (Heliotropiaceae). – Kew Bull. Don, G. 1837. A general system of gardening, 4. – London. 64: 285–289. El-Hadidy, A. and Boulos, L. 2000. Boraginaceae. – In: Boulos, L. Melo, J. I. M. and Semir, J. 2010. Taxonomia do gênero (ed.), Flora of Egypt, 2 (Geraniaceae–Boraginaceae). Al- Euploca Nutt. (Heliotropiaceae) no Brasil. – Acta Bot. Brasil. Hadara Publ., Egypt, pp. 352. 24: 111–132. Ferguson, D. M. 1999. Phylogenetic analysis and relationships in Melo, J. I. M. et al. 2009. Padrões de distribuição geográfica das Hydrophyllaceae based on ndhf sequence data. – Syst. Bot. 23: espécies de Euploca e Heliotropium (Heliotropiaceae) no Brasil. 253–268. – Rodriguésia 60: 1025–1036.

412 Mittermeier, R. A. et al. 1998. Biodiversity hotspots and major Stocks, J. E. 1852. Notes on Beloochistan plants. – Hook. J. Bot.; tropical wilderness areas: approaches to setting conservation Kew Gard. Misc. 4: 172–181. priorities. – Conserv. Biol. 12: 516–520. Thulin, M. 2006. Flora of Somalia, 3. Angiospermae (Ericaceae– Myers, N. et al. 2000. Biodiversity hotspots for conservation Asteraceae). – R. Bot. Gard. Kew. priorities. – Nature 403: 853–858. Tutin, T. G. 1973. Heliotropium. – In: Tutin, T. G. et al. Nuttall, T. 1837. Collections towards a flora of the territory of (eds), Flora Europaea, 3 (Diapensiaceae to Myoporaceae). Arkansas. – Trans. Am. Phil. Soc. 5: 137–203. Cambridge Univ. Press, pp. 84–86. Radford, A. E. et al. 1974. systematics. – Harber Vahl, M. H. 1790. Symbolae Botanicae, 1st ed. – Hauniae. and Row Publ. Vatke, W. 1875. Plants in Itinere Africano ab J. M. Hildebrandt Refulio-Rodriguez, N. F. and Olmstead, R. G. 2014. Phylogeny of collects determinare pergit W. Vatke. – Österr. Bot. Zhurn. 25: Lamiidae. – Am. J. Bot. 101: 287–299. 166–169. Riedl, H. 1967. Heliotropium L. – In: Rechinger, K. H. (ed.), Flora Vatke, W. 1882. Plantas in itinere africano ab J. M. Hildebrandt Iranica. Vol. 48. Akad- Druck und Verlagsanstalt, pp. 9–53. collectas, Borraginaceae reliquae. – Linnaea 43. Schwartz, O. 1939. Flora des Tropischen Arabien. – Mitteil. Inst. Verdcourt, B. 1991. Boraginaceae. – In: Polhill, R. M. (ed.), Flora Allgem. Bot. Hamburg 10: 1–356. of tropical east Africa. A. A. Balkema, pp. 1–77. Smith, R. A. et al. 2000. Molecular phylogenetic evidence for the Weigend, M. et al. 2014. From capsules to nutlets. Phylogenetic origin of Lennoaceae: a case of adelphoparasitism in the relationships in the Boraginales. – Cladistics 30: 508–518. angiosperms. – Am. J. Bot., suppl. 87: 158. Willdenow, C. L. 1798. Caroli a Linne. Species Plantarum, 4th ed. Stevens, P. F. 2001. Angiosperm Phylogeny Website, ver. 12, Jul Vol. 4. Berolini, pp. 496–1968. 2012. –  www.mobot.org/MOBOT/research/APweb/ . Wood, J. R. 1997. A handbook of Yemen flora. – R. Bot. Gard. Kew.

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