ON VIRIDIATRUM (WULFEN) KÖRB. IN NORTH-EASTERN IRAN

M. Haji Moniri & S. Kamyabi Received 27. 07. 2011. Accepted for publication 08.11.2011.

Haji Moniri, M. & Kamyabi, S. 2011 12 31: On Rhizocarpon viridiatrum (Wulfen) Körb. in north-eastern Iran. - Iran. J. Bot. 17 (2): 276-281. Tehran.

Morphology, anatomy, chemistry and distribution of the species Rhizocarpon viridiatrum (, Lichenized Fungi) in NE Iran are presented based on observations from 357 samples collected in Razavi Khorasan province during 2006-2007, an analysis of substances and a literature survey.

Mahroo Haji Moniri (correspondence ) & Saleh Kamyabi, Department of Biology, Faculty of Science, Mashhad Branch, Islamic Azad University, Mashhad, Iran, Rahnamaie St., Mashhad.

Keywords. Lichenized Fungi, Rhizocarpon viridiatrum, Razavi Khorasan.

   Rhizocarpon viridiatrum (Wulfen) Körb.  .                .      # $         ! "   #  +  , (Rhizocarpaceae, Lichenized Fungi) Rhizocarpon viridiatrum ! (!'  &$ !'   %  ,  !& 8 9 : ;$' <$9=' &# , 2007  2006 2 #3  2!4 1  1    2 ( &0 !& 357 . ! >  (, 

Introduction Khorasan province, have been reported (Seaward et al. The lichen genus Rhizocarpon introduced by Ramond 2008; Moniri et al. 2009). Razavi Khorasan province in 2 in Flore Francaise ed. III (Lamarck and Candolle, the northeast of Iran with an area of c. 127,432 km 1805) has been subject to taxonomic debate. Originally biogeographically belongs to Irano-Touranian region its species were included in Lecidea, Buellia and (Takhtajan, 1977). Razavi and Northern Khorasan Diplotomma. Since 1871 new attempts have been made provinces have more mountain ranges than any other to delimit a separate genus Rhizocarpon Lam. ex DC. parts in the country, including Ala Dagh, Binaloud, as a cosmopolitan with ca. 200 species (Feuerer, 1978). Hazar Masjid and Kopet Dagh (Zomorodian, 2002), Traditionally the genus is divided in a group of species and certainly they must have a greater saxicolous lichen with yellow-green thallus and a group with non-yellow- diversity than the little attention to the area has green, generally grayish or brownish thallus (Thomson, revealed so far. 1967). The yellow group is distributed in the Arctic and The present study is a continuation of our analyses the Antarctic and the temperate zones of the world, as of Rhizocarpon in Razavi Khorasan province (Haji well as at high elevations in the mountains of warmer Moniri et al., 2010; Haji Moniri & Kamyabi, 2010), zones (Runemark, 1956). and deals with morphology, anatomy, chemistry and The presence of the genus in Iran is very poorly distribution of R. viridiatrum (Wulfen) Körb. The known, as is knowledge generally for , while ecology is not yet included because more extensive recent investigations are beginning to change that sampling of other regions of the province, especially situation. The lichenological knowledge in Iran mountainous zones, as well as microhabitat studies are experienced a considerable improvement in the last needed to improve our knowledge of the species. decade (Seaward et al., 2004; 2008). As a result, the presence of ten species and one subspecies of Rhizocarpon in Iran, including six species for Razavi 277 Haji Moniri & Kamyabi IRAN. J. BOT. 17 (2), 2011

Material and Methods is restricted to the slightly and markedly wet zones with 357 samples of R. viridiatrum were collected on shaded annual precipitation 100-300 mm. Among the known siliceous and calcareous-siliceous rocks in 19 sampling species of the genus Rhizocarpon, R. viridiatrum is the sites (Fig. 1) during the period from the spring of 2006 most frequent below 1000 m in the province (Kamyabi, to the fall of 2007 by the second author. For more 2009; Moniri et al., 2009). information about the sampling sites see Moniri et al., The Iranian record of R. viridiatrum (Szatala, 1940) 2009. The study area is covered by permanent is also from the northeast of Iran. Evidently, the species grasslands and permanent pastures in irregular is much more common in Razavi Khorasan province arranges, and is mostly situated in highlands with cold than elsewhere in Iran, as it has not been reported from climate ranging from 960 to 2360 m. Identification and other provinces yet (Seaward et al., 2008). measurements were made using a stereomicroscope and At the world level, the species is widespread, being a compound microscope. For the applied spot tests see reported from Africa, Asia, the Arctic, Australia, Orange et al. (2001). TLC of a sample of R. viridiatrum Europe, and North and South America (Anonymous, was kindly done by Dr. Kukwa in Gdansk, Poland. 2011; Thomson 1997; Nash et al., 2004). As to Original material is deposited in the first author's lichen neighboring countries, the species is reported from collection, with a duplicate in MSC. Tajikistan, Kazakhstan and Turkey (Wagner & Spribille 2005; Anonymous 2011). Results and discussion Notes. Rhizocarpon viridiatrum is readily recognized Rhizocarpon viridiatrum (Wulfen) Körb. by being lichenicolous, by its convex and immarginate apothecia and its pale greenish yellow thallus. The dark Description. Thallus to 3 cm in diam., initial areola olivaceous to brown ascospores are suggestive of R. on Aspicilia sp. (Fig. 2), with limited number of saurinum, but that species has less septate smaller secondary areoles, without hypothallus and areoles ascospores (Moniri et al. 2009) and lacks black separated by substrate, marginal areoles flattened with granules in the epihymenium. indistinct prothallus or without prothallus; not Rhizocarpon viridiatrum belongs to the sorediate. “Viridiatrum group” of species. These have Areoles 0.2-0.6 mm in diam., yellow-green, plane multiseptate ascospores, an epihymenium with dark and/or slightly convex, surface pruinose, matt (Fig. 3), granules, and a medulla reacting negatively with secondary areoles angular; cortex ca. 10-25 µm thick, Lugol’s iodine (Runemark, 1956). R. viridiatrum in this necrotic top layer ca.10-20 µm thick, medulla white, group is distinguished by its very dark ascospores, so over 200 µm thick, I –, seldom I + light blue, algal that the septa are not recognized easily, at least in layer ca. 40-90 µm thick (Fig. 4). Iranian collections (Kamyabi, 2009). In addition, its Apothecia 0.5-1 mm in diam., 0.8 mm thick, round or prothallus is thin and not always distinguishable while angular, disk initially flat but soon strongly convex, it is always lichenicolous (Runemark, 1956). without margin, epruinose, matt. Exipulum very thin Most of the investigated Khorasan samples are with a black margin, 10 µm thick; hymenium 80-120 lichenicolous on thalli of Aspicilia spp. (259) while a µm thick, hyaline, uppermost part dark red; paraphyses good number grows associated with the areoles of colourless, slightly branched, apical cells clavate; Acarospora spp. (46) (Kamyabi, 2009). epihymenium dark reddish-brown with black granules,

K + red, usually 15-30 µm thick; asci clavate, ca. 80- 115×28-33 µm, containing 8 spores; ascospores Acknowledgement submuriform to muriform, black or dark brown, 12-25 We are grateful to Dr. M. Kukwa, Gdansk University × 7-13 µm (Fig. 5). Pycnidia not studied. (Poland), for his help in TLC. Lichen substances. Rhizocarpic acid and an unknown fatty acid, identified by TLC on the specimen References no. 2354, collected from Torbat-e Jam, Bezd, UTM Anonymous, 2011: checklists/lichens URL: 41S, 261304 3899185, 1562 m elev., 19. Jul. 2007 (hb. http://www.biologie.uni-hamburg.de Haji Moniri, hb. Kukwa). Arnold, F., 1871: Lichenologische fragmente, XII. – Ecology. R. viridiatrum has been found in quite Flora, 53. Regensburg. concave depressions of siliceous and calcareous rocks, Feuerer, T. 1978: Zur Kenntnis der Flechtengattung in which rainwater accumulates. Rhizocarpon in Bayern. -Berichte der Bayerischen Distribution. R. viridiatrum is mainly found in the Botanischen Gesellschaft 49: 59–135. northern areas of the province and has few localities in Fries, Th. M., 1874: Lichenographia Scandinavica II. – the central and south-eastern parts (Fig. 1), (Table 1). It Upsaliae. IRAN. J. BOT. 17 (2), 2011 Rhizocarpon viridiatrum in Iran 278

Table 1. Distribution and abundance of Rhizocarpon viridiatrum (Wullfen) Körb. in Razavi Khorasan province. Total Thallus of Frequency % Locality/ Elevation (m) Thallus of R. viridiatrum Rhizocarpon R. viridiatrum Mashhad-Kordineh/ 1763- 78 25 32.06 1873 Mashhad-Taraghdar- 93 24 25.81 Dehbar/ 1600-1710 Mashhad-Zoshk/ 1700 41 10 24.36 Mashhad-Kang/ 1750- 83 18 21.68 1850 Torbatjam-Bezd/ 1540 117 20 17.09 Torbatjam-Palangavar/ 31 23 76.19 1560 Khaf-Arzaneh/ 1070-1340 64 32 50 Neyshabour-Darroud/ 27 10 37.04 1700 Neyshabour-Boujan/ 1750 53 10 18.86 Kallat-Ghalenow/ 1350 63 12 19.04 Kallat-Zavin/ 1500 18 11 61.12 Kashmar-Kariz/ 1560 32 26 81.25 Kashmar/Chehelpou/ 1820 68 68 100 Chenaran- Baroo/ 1260 25 25 100 Torbatheidarie- 12 12 100 Roudmaajan/ 1630 Sabzevar-Shareh/ 1300- 17 17 100 1530 Quchan-Dorbadam/ 2300 9 9 100 Daregaz-Chehelmir/ 1300 5 5 100

Haji Moniri, M., Kamyabi, S. & Clayden, S. R. 2010: Region. -Arizona State University, Tempe, Arizona. A preliminary study of Rhizocarpon macrosporum USA. VII: 742 p. in Razavi Khorasan province (NE Iran). -The Orange, A., James, P. W. & White, F. J. 2001: Iranian Journal of Botany 16 (1): 185-189. Microchemical methods for the identification of Haji Moniri, M. & Kamyabi, S. 2010: Morphological lichens. -British Lichen Society, London, 101 pp. and anatomical investigation of Rhizocarpon Runemark, H. 1956: Studies in Rhizocarpon, 1. disporum and its distribution in Razavi Khorasan of the yellow species in Europe. -Opera province. -Journal of Plant Science Researches 17 Botanica. A Societate Botanica Lundensi in (1): 36-43. Supplementum Seriei "Botanica Notiser" edita 2: 1, Kamyabi, S. 2009: Investigation of biodiversity of 152 pp. Rhizocarpon Lam. ex DC. in Razavi Khorasan Seaward, M. R. D., Sipman, H., Schultz, M., province. -MSc thesis, Islamic Azad University, Maassoumi, A., Haji Moniri, M. & Sohrabi, M. Mashad. 2004: A preliminary lichen checklist for Iran. - Lamarck, J. B. & De Candolle, A. P., 1805: Flore Willdenowia 34: 543–576. Francaise, ed. III. - Paris. Seaward, M. R. D., Sipman, H. J. M. & Sohrabi, M. Moniri, M. H., Kamyabi, S. & Fryday, A. M. 2009: 2008: A revised checklist of lichenized, Rhizocarpon saurinum new to Asia, and other lichenicolous and allied fungi for Iran. -Sauteria 15: reports of Rhizocarpon species from Razavi 459–520. Khorasan Province. -Iran. Mycologia balcanica 6: Szatala, S. 1940: Lichenes. In: K. H. Rechinger, J. 89-92. Baumgartner, F. Petrak & S. Szatala, Ergebnisse Nash, T. H., Ryan, B. D., Diedrich, P., & Gries C. einer botanischen Reise nach dem Iran, 1937. - 2004: Lichen Flora of the Greater Sonoran Desert Annales des Naturhistorischen Museums in Wien 50: 521-533. 279 Haji Moniri & Kamyabi IRAN. J. BOT. 17 (2), 2011

Fig. 1. Distribution map of Rhizocarpon viridiatrum in Razavi Khorasan Province (Kamyabi, 2009).

Fig. 2. Primary areoles of Rhizocarpon viridiatrum on Aspicilia sp. (Kamyabi, 2009).

Fig. 3. Areolate thallus of Rhizocarpon viridiatrum, the absence of a prothallus (Kamyabi, 2009).

IRAN. J. BOT. 17 (2), 2011 Rhizocarpon viridiatrum in Iran 280

Fig. 4. Longitudinal section of an areole of Rhizocarpon viridiatrum, Co: cortex, Gl: algal layer, Me: medulla (Kamyabi, 2009).

Fig. 5. Rhizocarpon viridiatrum (Kamyabi, 2009) (a): Hymenium; (b): Clavate ascus containing 8 dark ascospores; (c): Muriforme ascospores (d): Submuriforme ascospores. 281 Haji Moniri & Kamyabi IRAN. J. BOT. 17 (2), 2011

Fig. 6. Schematic pictures of thallus and reproductive organ in Rhizocarpon viridiatrum: (a). Thallus with flattened marginal areoles, (b). Longitudinal section of apothecium, (c). Ascus containing 8 muriforme ascospores and (d). Different shapes of ascospores (Kamyabi, 2009).

Takhtajan, A. 1977: Floristic Regions of the World Wagner, V. & Spribille, T. 2005: Preliminary checklist translated to English by Theodor J. Crovello in of lichens of Kazakhstan URL: 1986. - University of California Press, California, http://www.geobotanik.uni-geottingen.de. 552 pp. Zomorodian M. J., 2002: Geomorphology of Iran, Thomson, J. W. 1967: Notes on Rhizocarpon in the Structural Processes and Internal Dynamics 1. – Arctic. -Nova Hedwigia 14: 421–481. Mashhad, 257 pp. Thomson, J. W. 1997: American Arctic Lichens 2. Microlichens. -University of Wiscosin Press, Madison, 675 pp. IRAN. J. BOT. 17 (2), 2011 Rhizocarpon viridiatrum in Iran 282