Bituminaria antiatlantica (Psoraleeae, Fabaceae), a new species from Morocco

Abstract A new species of Bituminaria is described and illustrated: Bituminaria antiatlantica Brullo, C. Brullo, Cambria, Cristaudo & Giusso, sp. nov., which is endemic to Anti-Atlas Mountains (Morocco). It is a true chasmophyte, characterized by a suffruticose habit, several woody branches, leaflets coriaceous, rounded to ovate, small, few-flowered inflorescences and corolla pale coloured.


Introduction
The genus Bituminaria Heist. ex Fabricius (Psoraleeae, Fabaceae), is widespread across the Mediterranean region and Macaronesian Islands, where, according to Egan and Crandall (2008), it is estimated to have diverged from other Psoraleoid genera approximately 6.78 million years ago. The first significant diversification of populations in the Psoraleeae occurred about 6.3 mya after the transcontinental split between North America and the Old World (Lavin et al. 2005). Molecular studies have revealed that et al. 2016) highlighted that more studies were needed to discriminate clearly the taxa belonging to the B. bituminosa complex, which is widely distributed in the Mediterranean territories. As part of these investigations we examined an isolated population of plants occurring in Morocco, which had been described by Maire (1936) as Psoralea bituminosa var. rotundata. To clarify the taxonomic position of this plant, we visited the Anti Atlas Mountains (southern Morocco), during which it was possible to collect specimens used as exsiccata and pods for its cultivation.
Plants referable to Psoralea bituminosa var. rotundata (previously recorded by Maire (1936) and Benabid and Cuzin (1997)) were found in two locations of the subdesertic area. They are represented by Mount Tachilla (locus classicus) and Djebel Imzi respectively, where the plant grows in the crevices of cliffs and steep rocky north-facing surfaces. In-depth taxonomic investigations of herbarium specimens and living plants cultivated from wild pods allowed us to observe significant morphological differences between these Moroccan populations and those of other Bituminaria species, occurring in various Mediterranean territories. These Moroccan plants (Psoralea bituminosa var. rotundata) are recognised as a distinct species and raised to specific rank as B. antiatlantica. The plants are characterized by: a suffruticose habit and very branched, woody stems; coriaceous semi-round to ovate leaves; small, few-flowered inflorescences and pale coloured corollas. It is a rare chasmophyte linked to very dry climatic conditions, and grows together with several other relic endemic species. Description. Perennial, suffruticose, dark green, erect to ascending, up to 60 cm tall. Stems dark green-brown, sparsely hairy, with hairs short and appressed, very branched; branches woody, leafy along entire length. Stipules 5-6 mm long, rigid, linear-triangular, adnate to the petiole. Leaves pinnately 3-foliolate, green, with petiole 1.8-6(7) cm long, sparsely hairy; leaflets semi-round to ovate, subglabrous  above and sparsely hairy below, 10-35 × 8-21 mm, with apex obtuse to acute, ending in a straight mucro 0.3-0.5 mm long. Inflorescence definite, subspicate, lax, 1.5-2 cm long, with 3-10 flowers. Peduncle 3.5-14 cm long, overtopping the leaves. Bracts 1-3 toothed, 5-8 mm long, subtending 2 or more flowers. Flowers 16-17 mm long. Calyx 12-13.5 mm long, green, densely hairy, with hairs white mixed to short black hairs; lower teeth 7-8 mm long, laterals shorter, 5.5-7 mm long. Corolla whitish-pink to whitish lilac; standard 16-16.5 × 7-7.5 mm, elliptic, striate with lilac in the middle, apex obtuse; wings 14-15 × 3-4 mm; keel 10.5-11 × 2-2.3 mm, having a macula dark violet in the upper part. Staminal tube 11-11.5 mm long, with anthers yellow, 0.7-0.8 × 0.3-0.35 mm; vexillary w with filament fused below with the other ones. Pistil 10-10.5 long, ovary hairy, style curved towards the apex, t h i c k e n e d a t p o i nt o f flexure, stigma capitate, penicillate. and ovary hairy. Pod 11-23 mm long (beak included), with beak pubescent, 14-16 mm long. Seed reniform, 6-7 × 3.4-4 mm.

Bituminaria antiatlantica
Distribution and ecology. Bituminaria antiatlantica is a rare and localized species, currently known only from Mount Tachilla and Djebel Imzi in the Anti-Atlas Mountains in southern Morocco, (Fig. 3). It grows between 300 and 1500 m of altitude, on steep, north-facing slopes, chiefly constituted of Precambrian quartzite. From the bioclimatic viewpoint, this area falls within the infra-and the thermo-mediterranean type, with semiarid to subhumid ombrotype (Benabid and Cuzin, 1997). This species is an element of a chasmophytic vegetation type characterized by Celsia longirostris Etymology. The specific epithet refers to the Anti-Atlas range, where the species occurs. Conservation status. Based on current knowledge, Bituminaria antiatlantica seems to have a scattered distribution over an area smaller than 2,000 km 2 . Therefore, following the IUCN criteria (2014), this species should be classified as "Vulnerable" (VU B2). As regards the conservation policy of the growing site, it has been proposed its inclusion in the list of the UNESCO World Heritage Sites for its richness in endemic, rare or important plants, as well as for its breath-taking landscape (see http:// whc.unesco.org/en/tentativelists/1180/). Seed and pod micro-morphology. As emphasized by several authors (Barthlott 1981, Koul et al. 2000, Kirkbride et al. 2003, Celep et al. 2012, Gandhi et al. 2011 Brullo et al. 2011Brullo et al. , 2013 seed coat micro-morphology plays an important role in the taxonomic survey at generic and specific level, especially in those rather critical groups. The seed testa sculptures o f Bituminaria were investigated by Minissale et al. (2013), Giusso et al. (2015), Brullo et al. (2016) and Bogdanović et al. (2016), who highlighted the systematic relevance of these features providing additional information in order to discriminate among the allied species. In particular, the species hitherto examined are B. bituminosa, B. palaestina, B. kyreniae, B. basaltica and B. plumosa, which are characterized by different patterns of seed testa. In this study SEM investigations were carried out on the seed of B. antiatlantica, according to the protocol of Stork et al. (1980) using the terminology followed Bartholot (1981) and Gontcharova et al. (2009). The results revealed that seed coat sculptures of B. antiatlantica differ markedly from the species mentioned above. The seed testa of B. antiatlantica is characterized by a fine and inconspicuous reticulum, bordering the cells, which appears irregularly polygonal and 3.5-9(10) µm wide. The anticlinal walls are irregularly curved to straight, slightly grooved and smooth, while the periclinal walls are flat with the epidermis smooth to finely rugose ( Fig. 5B-C). The pod corpus is characterized by minutely rugose surfaces, and the indumentum hairs are minutely papillose, with the longitudinal furrow broadly widened at the base (Fig. 5E-F).  In this study pollen grains of B. antiatlantica were excised from flower buds in ahydrated state and were examined according to Walker and Doyle (1975), Punt et al. (1994Punt et al. ( , 2007 and Hesse et al. (2009). The pollen grains are very similar to that of B. bituminosa sensu stricto from Sicily, which has been examined in detail by Brullo et al. (2016), although there are differences in size and ornamentations which distinguishes clearly the pollens of the two species. Actually, The pollen grain of B. bituminosa   Fig. 6A) is smaller with a size of 25-30(34) µm, with larger brochi (4-17 µm) and fewer in number, showing a laxly papillose lumen and less deep (0.5-1 µm) and narrower (1-1.2 µm) muri. In B. antiatltantica, the pollen grain ( Fig. 6) is slightly larger (37-38 µm) with smaller brochi (4.3-11 µm) and more numerous, with a lumen minutely papillose and muri deeper (1.4-1.8 µm) and larger (1.4-1.7 µm).
Discussion. Bituminaria antiatlantica shares some ecological and morphological characteristics with B. flaccida, a very rare species occurring in the semidesert countries of Jordan and Sinai in the Middle East; e.g., reduced leaflets, the size and few-flowered inflorescences, and flower colour. However, the latter differs from B. antiatlantica in several significant features (Table 1), such as its herbaceous habit, greyishglaucous stems and leaves, obovate to linear-lanceolate and densely pubescent cauline leaflets, shorter calyx, longer and slightly retuse standard, shorter staminal tube, and feature of pod and seed.
Other specimens examined (