Anabasis firouzii Akhani, 2016

Akhani, Hossein, Khoshravesh, Roxana & Malekmohammadi, Maryam, 2016, Taxonomic novelties from Irano-Turanian region and NE Iran: Oreosalsola, a new segregate from Salsola s. l., two new species in Anabasis and Salvia, and two new combinations in Caroxylon and Seseli, Phytotaxa 249 (1), pp. 159-180 : 165-170

Anabasis firouzii Akhani , spec. nov. ( Figs. 3 , 4 )

Type: — IRAN. Northern Khorassan: Ghorkhod Protected Area , on marl hills, 37°23ʹ38ʺ N, 56°27ʹ49ʺ E, 10.10.2012, H. Akhani 23260 ( IRAN, holotype; isotypes FUMH, Hb. Akhani) .

Diagnosis: —This species is unique among the Iranian species of Anabasis ; despite sharing a similar habitat and possessing similar leafy stems, it differs from A. eugeniae Iljin (1937: 215) by several characters including the caespitose habit with compact woody stems (vs. diffusely branched); stems stout, thick and 4-angled, 2–4 mm in diameter (vs. slender, thin and terete, 1–2 mm in diameter); leaves shorter (10–20 mm vs. 20–25 mm), obtuse with a spiny tip (vs. acute and non-spiny); and double-sized fruit wings.

Affinity: —Another possible relative based on molecular phylogeny or morphology is Anabasis elatior ( Meyer 1841: 341) Schischkin in Krylov (1930: 961). The new species differs from A. elatior in larger leaves 10–20 mm long (vs. reduced leaves up to 3 mm long), semi-orbicular (vs. linear) disk lobes, a smaller habit up to 15 cm (vs. to 30 cm), none or less branched inflorescence, and 7–12 (vs. 10–20) internodes. The leafy stems and habit of Anabasis firouzii are superficially similar to A. brevifolia Meyer (1829: 377) , from which it differs in longer leaves (vs. 3–8 mm long), the presence of a stout spine at the leaf apex (not ending to a deciduous bristle), and ciliate (vs. entire) disk lobes.

Description: —Subshrub, grey green or glaucous, c. 10–15 cm high and c. 10–20 cm wide, with numerous branches rising from a thick woody caudex, old stems intricate and compact, forming a semi-spherical cushion-like mass, furnished with remains of last and current year leaf sheaths; current year stems at base surrounded by sheathing reduced leaves, jointed, readily breaking at joints, in joints with tuft of woolly multicellular hairs, 4-angled, 2–4 mm in diameter; flowering plants with 7–12 internodes, mostly 3–5 internodes remain; second and third lower internodes are the largest, 3–5 cm long; remaining upper and lower nodes shorter, as short as 3 mm long in terminal nodes; epidermis minutely papillose. Lowermost leaves reduced, connate at base and sheathing; median leaves cylindrical, oblique to horizontal, semiterete, fleshy, 10–20 mm long, obtuse at apex, ending in a short (1–1.5 mm long) stout spine; leaves in floral axil as long as or longer than fruiting perianths. Inflorescence spike-like or branched, flowers occur in third internodes and upper ones, usually 3 hermaphrodite or unisexual flowers in each leaf axil, inserted on a dense tuft of white hairs, having two larger globular bracts, 3–5 mm long and two smaller bracteoles; bracteoles in fruiting time triangular, 1.7–2 mm long and wide, fleshy, rather acute; fruiting inflorescence mostly in three last terminal nodes, congested. Perianths distinct, scarious, triangular, elliptic to orbicular; flowering perianths 1.3–1.6 mm long, inequal in width, 1–2 mm wide; fruiting perianths in median part with large, erect horizontal wings, 15–20 mm in diameter; wings usually 8.2–8.5 mm long, unequal in width, larger wings fan-shaped or broadly orbicular, up to 13 mm wide, smaller wings ovate to narrowly suborbicular, up to 8 mm wide. Stamens on a disc, with five rounded lobes (staminodes), 0.6–0.7 mm × 0.6–1 mm, at top margin laciniateciliate; filaments 0.9–1 mm long, 0.33–0.35 mm wide; anthers 0.6 mm long. Seeds vertical, in fresh condition more or less globose, with fleshy testa, in dry condition lenticulate, ± 4 mm.

Additional specimens examined: — IRAN. Golestan / Northern Khorassan: Golestan National Park, near Afrali , ca. 8 km West of Soolegerd, 37º26ʹ15ʺ N, 56º3ʹ58ʺ E, 1737m, 30.6.2010 ; H. Akhani & N. Samadi 21412 ( FUMH, Hb. Akhani) ; W Bash-Kalateh , on the special road towards the new telecom station, 37˚23’55” N, 56˚27’51” E, 1660 m, 20.09.2011, Memariani & Arjmandi 44627 ( FUMH, Hb. Akhani) .

Etymology: — Anabasis firouzii is named in honour of Eskandar Firouz (b. 1926) and dedicated to his 90 th birthday in 2016. He was the founder and Director of Iranian Department of Environment and Iranian Game Council in 1967–1977. Most of the Iranian Protected Areas including GNP and GPA have been designated as protected under his authority. After the Iranian Revolution in 1979 he was jailed for six years (1979–1985). After his release, he stayed mostly in Iran and focused on writing books and memoirs ( Firouz 2005, 2012). The following species have already been named after him: Corydalis firouzii Wendelbo ( Papaveraceae ) (1976: 61) and a rodent, the Iranian Jerboa, Allactaga firouzi Womochel (1978: 65) .

Ecology: — Anabasis firouzii typically grows on marl and calcareous outcrops of Kopet Dagh Mountains. This habitat is clearly marked from the surrounding area by the white colour of lime substrate ( Fig. 3A ). In Golestan National Park, A. firouzii has been found twice: near Almeh valley (documented by a photograph; no specimen collected) and at the altitude of 1737 m in Afrali. In the latter locality, no other associated species has been observed. In the type locality, this species is associated with other species listed in Table 2. Some other species endemic to Kopet Dagh such as Caroxylon iljinii (see below) and Atraphaxis intricata Mozaffarian (2006: 107) are also associated with Anabasis firouzii . The occurrence of A. firouzii as a C 4 species in higher altitudes of Kopet Dagh could be explained by its habitat on south-facing slopes and its active growth in hot summer months.

Threats and endangered status: — Anabasis firouzii is known from three localities (two of them documented and one only observed) ( Fig. 5). Its restriction to a particular habitat suggests that the number of individuals and the range of the species is small. The known area of occupancy (EOO) is only 14 km 2 and the extent of occurrence (EOA) is 48 km 2. According to the IUCN Red List categories and criteria ( IUCN 2012), the species fits well into Endangered (EN). In spite of the established protection of the area, several fires have damaged a large part of GNP and GPA in recent years, some of them close to the habitats of A. firouzii . The type locality of the new species is behind a radar installation. The expansion of similar installations and road construction are risks that could reduce the area of occupancy.

Relationship and molecular phylogeny: —The Bayesian Inference analysis of ITS sequences ( Fig. 2 ) places both samples of the new species in a strongly supported clade and probably isolated from the other known species in Iran. Anabasis firouzii and A. aphylla Linnaeus (1753: 223) are sisters to a clade including the Central Asian and Mongolian species A. elatior and three aphyllous species endemic to Iran, A. calcarea (Charif &Aellen in Aellen 1952: 262) Bokhari & Wendelbo (1978: 292), Anabasis iranica Iljin (1960: 137) and A. haussknechtii Bunge ex Boissier (1879: 969) . The three aforementioned species of Anabasis are calcareous and halophytic, and usually grow in lowlands. They differ from A. firouzii in their reduced leaves, many-branched inflorescences, and a taller habit. Anabasis firouzii resembles the Central Asian and Mongolian species A. brevifolia but our molecular data do not support their affinity. However, the phylogenetic tree clearly shows a close affinity of A. brevifolia with A. setifera Moquin-Tandon (1840: 164) ( Fig. 2 ). Based on the tree topology and geography, we conclude that A. firouzii is a relict species still growing at higher elevations of NW Iran. The leafy stem is evidently a plesiomorphic character. Over the evolutionary process, Anabasis species with leafy stems evolved to species with reduced leaves at lower elevations. Anabasis eugeniae is another leafy Anabasis in Iran, which is sister to the remaining species in our phylogenetic tree ( Fig. 2 ). Anabasis firouzii co-occurs with Caroxylon iljinii (see below), another relict species in Chenopodiaceae . The molecular phylogeny of Salsoleae showed that Caroxylon canescens Moquin-Tandon (1849: 208) Akhani & E.H. Roalson in Akhani et al. (2007: 947) is a species closely related to C. iljinii , basally positioned in its clade. Morphological data and ITS sequence analysis indicate that additional studies are required to clarify the phylogenetic position of A. firouzii .

Kaviria aucheri (Moq.) Akhani 1

Caroxylon iljinii (Botsch.) Akhani 1

Rhamnus pallasii Fisch. & C.A. Mey. 1

Artemisia kopetdaghensis Krasch., Popov & Lincz. ex Poljakov 1

Acantholimon cf. edmondsonii Rech. f. & Schiman-Czeika 1

Pimpinella tragium Vill. 1

Lagochilus aucheri Boiss. 1

Cousinia decipiens Boiss. & Buhse 1

Crucianella gilanica subsp. transcaspica (Ehrend.) Ehrend. & Schönb. -Tem. 1

Dianthus crinitus subsp. turcomanicus (Schischk.) Rech. f. 1

Scariola orientalis (Boiss.) Soják. 1

Buffonia sintenisii Freyn 1

Piptatherum sp. 1

Echinops sp. 1

C 4 anatomy and carbon isotope value: —The leaf anatomy of A. firouzii is Kranz-Salsoloid ( Fig. 6A–C ). The Kranz-Salsoloid leaf anatomy is well known in the C 4 species of Salsoleae and Caroxyleae Akhani & Roalson in Akhani et al. (2007: 947) ( Carolin et al. 1975). There are three vein orders including: 1) midrib ( Fig. 6A ) embedded in several layers of water storage cells; 2) primary veins oriented towards the periphery with one to two WSC distance from the bundle sheath cells ( Figs. 6A and B , arrows); and 3) secondary veins in direct contact with the bundle sheath cells on their xylem side on the periphery of the water storage cells ( Fig 6B and 6C ). Epidermis contains two to three layers of thick-walled cells, and the stomata are superficial ( Fig 6C ). There is a layer of hypodermis beneath the epidermis containing numerous crystals inside ( Fig. 6C , asterisk). Crystals are present in the outer layer of WSCs as well. The relatively superficial stomata are similar to A. setifera , another leafy species in Iran, and dissimilar to species with reduced leaves such as A. calcarea as reported by Bokhari & Wendelbo (1978).

The carbon isotope value ( Table 3) of the new species (–10.08‰) well supports C 4 photosynthesis in Anabasis firouzii . This value is less negative than the average of all species (– 12.44±1.3‰). This may indicate a water stressed habitat in spite of the fact that this species grows in a much milder climate comparing to the most of other species inhabiting desert conditions.

Figures

FIGURE 2. The 50% majority rule tree from Bayesian Inference analysis of ITS sequences of 36 taxa/accessions of Salsoleae and Sympegma regelii as outgroup, showing the relationship of Oreosalsola, Kali, Salsola s.str., and the position of Anabasis firouzii and A. setifera. The numbers above branches show posterior probabilities. *The accession number EF453389 was wrongly reported in Akhani et al. (2007) under Anabasis setifera.

FIGURE 3. Habitat (A) and habit (B) of Anabasis firouzii in the type locality.

FIGURE 4. Anabasis firouzii. A. Leaves in vegetative state. B. Fruiting branch. C. Flowering perianth from side. D. Dissected flowering perianth showing staminodes. E. One stamen. F. Fruit. G–J. Mature perianth wings.

FIGURE 6. Cross section of leaves of Anabasis firouzii. A. An outline of leaf cross section representing salsoloid kranz anatomy, the arrow indicates the midvein. B. Close up of leaf Kranz anatomy, the arrow points to a primary vein. C. Close up of leaf margin showing superficial stomata and hypodermal cells, crystals are indicated by asterisk, arrow shows a secondary vein. Scale bars = 250 μm for A and B, 100 μm for C.