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Taxonomic Revision of the Genus Ononis (Trifolieae, Fabaceae) in Egypt, with the First Record of Ononis Viscosa Subsp

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Taxonomic Revision of the Genus Ononis (Trifolieae, Fabaceae) in Egypt, with the First Record of Ononis Viscosa Subsp Phytotaxa 408 (1): 001–029 ISSN 1179-3155 (print edition) https://www.mapress.com/j/pt/ PHYTOTAXA Copyright © 2019 Magnolia Press Article ISSN 1179-3163 (online edition) https://doi.org/10.11646/phytotaxa.408.1.1 Taxonomic revision of the genus Ononis (Trifolieae, Fabaceae) in Egypt, with the first record of Ononis viscosa subsp. breviflora ABDEL AZIZ A. FAYED1, AZZA H. EL-HADIDY2, AHMED M. FARIED1 & ASMAA O. OLWEY1* 1Botany and Microbiology Department, Faculty of Science, Assiut University, Assiut, Egypt. 2Botany and Microbiology Department, Faculty of Science, Cairo University, Giza, Egypt. *E-mail: [email protected] Abstract The genus Ononis comprises 86 species worldwide distributed in temperate regions. It is represented in Egypt by ten species. During recent excursions to the mountains of southern Sinai Peninsula, a newly recorded species, namely O. viscosa subsp. breviflora, was collected. This new record was previously confused with O. sicula. These two species can be differentiated by corolla length and shape. This study provides a full taxonomic revision of the genus for the flora of Egypt, updated no- menclature for all taxa, amended descriptions, detailed hand drawings, and a diagnostic key to the species. The most valuable diagnositic characters in the taxonomy of the genus in Egypt are discussed. After critical examination and literature study, we found that two names (O. serrata and O. vaginalis) needed to be lectotypified. Key Words: Ononis, Fabaceae, Flora of Egypt, Lectotypification, Trifolieae Introduction Fabaceae Lindley (1836: 544) or Leguminosae Jussieu (1789: 345) is the third largest family of flowering plants, with approximately 19,500 species classified into approximately 770 genera (Polhill & Raven 1981, Christenhusz & Byng 2016, LPWG 2017). Recent molecular and morphological evidence supports Fabaceae as a single monophyletic family (Wojciechowski et al. 2000, Lock 2005, Bello et al. 2009, 2012, Lewis et al. 2013, LPWG 2017, Soltis et al. 2018). The genus Ononis Linnaeus (1753: 716, 1754: 321) is nested within the tribe Trifolieae Fries (1835: 100) and comprises 86 species worldwide that are distributed in temperate regions (Turini et al. 2010). Linnaeus (1753, 1754) recognized only 17 species. De Candolle (1825) classified the genus into two sections: Euononis De Candolle (1825: 158) and Lotononis De Candolle (1825: 166), based on leaf stipules (whether or not stipules adhere to the petiole). Later, Willkomm (1877) subdivided Ononis into four sections and six subsections based on habit, leaf composition, presence or absence of spines, pedicel elongation (to produce arista) and flower colour. The most comprehensive taxonomic monograph of the genus was presented by Širjaev (1932), who accepted 68 species distributed in two sections: sect. Ononis, which is characterized by reduced peduncles and few-seeded pods (2– 4); and sect. Natrix Grisebach (1843: 12), which is characterized by distinct peduncles and multi-seeded pods. More recently, Turini et al. (2010) studied the phylogeny of the genus Ononis using the plastid region trnL-F and nuclear ITS sequences and found that Ononis is a monophyletic group. However, the morphological and molecular evidence contradicted the traditional infrageneric classification; five new major lineages within the genus were suggested that are morphologically supported by peduncle length, flower colour and habit. In Egypt, Ononis has been treated only in broad floristic studies (e.g., Täckholm 1956, 1974, El Hadidy 1989, El Hadidi & Fayed 1995, Boulos 1999), which lack proper synonymy lists, full type citations, and detailed illustrations. In addition, Ononis has also been treated in studies concerning the tribe Trifolieae (e.g., Ayyad & Moore 1994, Taia 2004a, b, Lashin 2006). Accepted by James Boatwright: 19 Mar. 2019; published: 27 Jun. 2019 1 2 • TABLE 1. Historical review for Ononis taxa recordedin Egypt (+ = present, - = absent, x = a synonym was recorded). Phytotaxa Forsskål Ascherson Muschler (1912: Täckholm (1956: Täckholm (1974: El Hadidi & Fayed Boulos (1999: The present (1775:130) &Schweinfurth 468-475) 278-279) 229-230 ) (1994/1995: 59) 261-262) study (1889:61) 408(1)©2019 MagnoliaPress Ononis diffusa Tenore -- - - - + + + Syn. Ononis serrata -- - x x + + + Forssk.var. major Lange Ononis serrata ++ + + + + + + Forsskål Ononis mitissima - + + + + + + + Linnaeus Ononis variegata -- - + + + + + Linnaeus Ononis natrix -- - - + + + + Linnaeus subsp. natrix O. natrix L. subsp. -- + - + + + + stenophylla(Boiss.) Širjaev Syn. O. natrixL. var. -- + x + + + + stenophylla Boissier Ononis vaginalis Vahl -+ + + + + + + Syn. Ononis cherleri x + - + + + + + Forsskål Ononis reclinataL. -- - - - - - + subsp. mollis(Savi) Béuinot Syn. Ononis -+ x + + + + + mollisSavi Syn. Ononis -+ + + + + + + reclinataL. var. minor Moris Ononis -+ + + + + + + pubescensLinnaeus Syn. Ononis calycina -+ x + + + + + Lamarck FAYED FAYED Ononis siculaGussone -+ + + + + + + Ononis viscosa -- - - - - - + ET AL. ET L.subsp. breviflora (DC.) Nyman The number of species of Ononis recorded in Egypt has increased over time (Table 1); Forsskål (1775) recognized four species in Egypt, two of which were validated by subsequent authors such as Greuter & Raus (1989): Ononis cherleri Forsskål (1775: 130) [= O.vaginalis Vahl (1790: 53)] and O. serrata Forsskål (1775: 130). Then, Raffeneau- Delile (1812) recorded four species in Egypt (adding two more to Forsskål’s list), namely, O. pubescens Linnaeus (1771: 267–268) and O. cherleri Linnaeus (1763: 1007). Ascherson & Schweinfurth (1889) added O. mitissima Linnaeus (1763: 1007) and O. sicula Gussone (1821: 78). Then, Muschler (1912) added one more taxon: O. natrix Linnaeus (1753: 717) subsp. stenophylla (Boissier) Širjaev (1932: 470). Täckholm (1974) listed eight species of Ononis in Egypt, while Boulos (1999, 2009) added one more species to the list for a total of nine species. Despite the fact that its natural geographic distribution is along the Mediterranean coast, Ononis viscosa Linnaeus subsp. breviflora (DC.) Nyman (1878: 161) has never been recorded in the Flora of Egypt, although Širjaev (1932: 530) suspected the presence of this taxon in Egypt. Recent excursions to the mountains of the southern Sinai Peninsula uncovered many floristic treasures (Fayed et al. 2004), one of which was the first record of O. viscosa subsp. breviflora. The aims of this study were as follows: first, to provide an updated taxonomic revision of all taxa belonging to the genus Ononis in Egypt; second, to critically evaluate previously used taxonomic characters and discuss their taxonomic validity; and third, to provide an improved diagnostic key for the taxa of Ononis in Egypt. Materials and methods This study was based on herbarium specimens kept in the following Egyptian herbaria: ASTU, CAI, CAIM and MAZHAR, in addition to fresh material collected from different localities representing the different habitats of Ononis in Egypt. Acronyms of herbaria are according to Thiers (continuously updated). High-quality digital photos of Egyptian material as well as the authentic type specimens kept in different herbaria worldwide were examined by the authors. The specimens examined for each species are listed according to the phytogeographical regions of Egypt, from north to south and from west to east. Within each phytogeographical region, specimens are arranged according to the date of collection. Abbreviations of Egyptian phytogeographical areas were adopted from Boulos (1999): Sinai (S), Mediterranean coastal belt (M), and Nile valley (N). Conservation assessments for each species were checked through the different Red List categories (IUCN 2018). The line drawings were made (by Olwey A.) with the help of a camera lucida attached to a Wild M8 Zewz stereomicroscope, and photographs were taken using an Olympus SC100 digital camera. Results and discussion The diagnositic characters for the genus Ononis in Egypt:— Habit:—Based on habit, the genus Ononis was subdivided into sections by Wilkomm (1877), Ascherson & Graebner (1907) and Širjaev (1932). Regarding the Egyptian species of Ononis, only two species are subshrubs: O. natrix and O. vaginalis; all remaining taxa are annual herbs. Leaf composition:—All studied taxa bear two types of leaves: simple and trifoliate leaves; only Ononis variegata Linnaeus (1753: 717) is unique in having simple leaves as the dominant type, and it rarely bears trifoliate leaves. Leaf stipules:—The shape of the stipules proved to be a critical character in the discrimination of different species of Ononis in Egypt. Ononis mitissima can easily be distinguished by its large membranous stipules, while the remaining taxa have green stipules. Stipule outline is a taxonomically informative character for distinguishing Egyptian Ononis. The stipule outline is either ovate (in O. diffusa Tenore (1811: XLI), and in O. serrata), oblong (in O. mitissima and O. natrix), obovate-rhombic (in O. variegata), linear to linear-lanceolate (in O. sicula) or deltoid (in O. viscosa subsp. breviflora). The vestiture of the stipules was neglected by many previous authors; however, it appears to have merit as a diagnostic character. Two species (O. variegata and O. mitissima) can be diagnosed as having glabrous stipules instead of the glandular stipules found in all the remaining taxa under investigation. Based on the length of the stipules, Egyptian Ononis can be classified into two groups: taxa with small stipules ranging from 2.5–5.0 mm, including O. diffusa,
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