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A REVISION OF CUSCUTACEAE FAMILY IN IRAN

E. Jafari, M. Assadi, G. A. Ghanbarian

Received 2016. 01. 25; accepted for publication 2016. 04. 27

Jafari, E., Assadi, M., Ghanbarian , G. A. 2016. 06. 30: A revision of Cuscutaceae family in Iran. - Iran. J. Botany 22(1): 23-29. Tehran.

Cuscutaceae family is reviewed based on the literature and available herbarium materials. This is a monotypic family and includes a single , three subgenera and eighteen in Iran, among them haussknechtii Engelm, is the only endemic species in Iran. This genus has been studied for the ongoing project of the Flora of Iran. The study was based on fresh materials from field as well as herbarium specimens. All specimens existed in the herbaria of Research Institute of Forests and Rangelands (TARI), herbarium of Iranian Research Institute of Protection (IRAN), Ferdowsi University of Mashad (FUMH), Research Center of Agricultural and Natural Resources of Fars Province were revised. A synopsis and identification key is provided to the eighteen species. Diversity centers and distribution of taxa in Iran are presented. Also the checklist of accepted species, synonyms, typical characters of the taxa are given. In this research new localities and new host are added to species and a new variety C. lehmanniana var. lehmanniana is introduced as a new record to Iran.

Efat Jafari (correspondence) Research Center for Agriculture and Natural Resources of Fars Province P. O. Box 71555-617, Shiraz, Iran. -Mostafa Assadi, Research Institute of Forest and Regelands, , Agricultural Research, Education and Extension Organization (AREEO), P. O. Box 13185-116, Tehran, Iran- Gholam Abbas Ghanbarian, Dept. of Natural Resources and Environment, Faculty of Agriculture, Shiraz University, Shiraz, Iran.

Key words: Cuscuta; ; species; hosts; Iran

بازنگري تیره Cuscutaceae در ايران عفت جعفري، مربي پژوهش، عضو هيئت علمي مرکز تحقيقات کشاورزي و منابع طبيعي فارس مصطفي اسدي، استاد پژوهش، موسسه تحقيقات جنگلها و مراتع کشور غالم عباس قنبريان، استاديار، دانشگده کشاورزي دانشگاه شيراز Cuscutaceae تيره سس ) ( بر اساس منابع و نمونههاي هرباريومي مورد بازنگري قرار گرفتهاست. اين خانواده. شامل يک جنس، سه زيرجنس و هجده گونه در سطح ايران است. به طورکلي اهداف اين پژوهش شامل: شناسايي گونهها، ارائه کليدهاي مربوطه بر اساس ويژگيها و صفات مهم، " تهيه نقشه پراکنش و نهايتا نگارش فلورفارسي براي اين خانواده است. به اين منظور پس از بررسي منابع و مطالعات کتابخانهاي و تعيين محل پراکنش گونههاي مختلف، مطالعات بر اساس جمعآوري نمونههاي کمبود از مناطق رويشي و بررسي نمونههاي هرباريومي موجود درهرباريوم IRAN TARI مؤسسه تحقيقات جنگلها و مراتع کشور ) (، مؤسسه تحقيقات گياهپزشكي کشور ) (، هرباريوم پژوهشكده علوم گياهي دانشگاه FUMH فردوسي ) ( و هرباريومهاي مختلف ساير مراکز آموزشي و پژوهشي صورت گرفت. نتايج حاصل از اين بررسي به صورت کليدهاي شناسايي و شرح هجده تاکسون پذيرفته شده و مشخص شدن دقيق مراکز تنوع و پراکنش گونههاي اين جنس در ايران و ترتيب گونهها به همراه اسامي مترادف و نمونههاي ديده شده ارايه ميگردد. در اين تحقيق نويسندگان رويشگاهها و ميزبانهاي جديدي براي اين جنس از ايران معرفي کردهاند.

INTRODUCTION species in both hemispheres. According to Flora Iranica The genus Cuscuta L. belongs to Cuscutaceae (Yunker & Rechinger 1964) there are 17 species in family is a cosmopolitan. The taxon includes about 170 different regions of Iran. It is an annual plant known by

24 A revision of Cuscutaceae in Iran IRAN. J. BOT. 22 (1), 2016 several common names, such as dodder; strangle weed, eighteen species includes three subgenera and five angel’s hair, and golden thread (Yuncker, 1965). Sections. The specific differences between them are Seedlings consist only of stem tissue and have no based on the stems, and . or . Stems filiform to moderately robust, twining, white, yellow or red, adhering to hosts by Checklist of Cuscuta L. species in Iran haustoria. It is incapable of producing its own food and Subgen . 1. Grammica (Loureiro) Engelm. hence is completely dependent upon its host plants for Sec. Cleistogrammica Engelm. survival (Agrios, 1988, Tanase et al. 2012). Flowers 1. C. australis R. Br., Prodr. FL. Nov, Holl. small, 4-5-merous, sessile or shortly pedicellate. Calyx 1:491(1810). and corolla tubular to campanulate, whitish or variously Typical characters: Corolla lobes ovate, obtuse or sub- coloured. inserted in throat or very shortly acute, erect to patent. produced beyond it; scales mostly present, equaling This species with 2 varieties was reported from Gilan stamens in number, attached to corolla below filament and Khorasan Provinces by Yunker & Rechinger attachment, simple or bifid, usually fimbriate, dentate (1964). However, despite the visited sites, any plant or fimbriate-ciliate. Styles 2 or united into 1, distinct to with these characteristics was not found. obsolete; (s) capitate or linear-elongate. Capsule 2. C. campestris Yunck., Mem. Torrey Club 18: 138 membranous, irregularly or regularly circumscissile (1932). near base or indehiscent. small. 4 or fewer. Typical characters: Corolla lobes triangular, acute, Embryo filiform, coiled, lacking (Plttmann often inflexed. Stigma capitate. Capsule indehiscent. 1978) Distribution in Iran: N, NW, W, C, NE. Cuscuta is one of the commonly used herbal New hosts: Cichorium intybus L., Cousinia Cass., constituents in functional foods and medicinal tonics to Scariola orientalis (Boiss.) Sojak., Polygonum nourish the different body parts. It is often added as dumosum Boiss., Reseda lutea L., Solanum nigra L., nutrient in porridge and alcoholic beverages to improve Tamarix L., Dendrostellera lessertii (Wikstr. )Van quality of food (Anjum et al. 2013). It is also used to Tigeh). prevent abortion as well as aging in clinical treatment. Previous studies have indicated that it possesses Sect. Eugrammica Yuncker anticancer and immune stimulatory activities (Ozenda 3. C. chinensis Lam., Encycl. Meth. Bot. 2: 229(1786) 1965). It has been often utilized in folk medicine; and Typical characters: Corolla lobes triangular, acute, several components of medicinal value have been often inflexed. Stigma capitate. Capsule dehiscent. found within it (Nemli 1987, Nisa et al. 1985, Watt Distribution in Iran: N, NW, C, SE. 1972). New hosts: Artemisia annua L., Lactuca serriola L., The aim of this study is to give an identification key Beta vulgaris L., Alhagi mannifera Desf., Medicago to the species of Iran, new hosts of the species, list of sativa L., Trigonella L., Plantago lanceolata L., Phyla accepted species and synonymies and distribution of nodiflora (L. ) Greene. the species in Iran. Subgen II . Monogyna (Engelm.) Yunck. MATERIALS AND METHODS Sect. Monogyna Engelm All specimens existed in different herbaria of Iran: 4. C. monogyna Vahl., Symb. Bot. 2: 32 (1791). TARI, IRAN, FUMH and Herbarium of Research Typical characters: Stem thick. Mainly on trees and Center of Agricultural and Natural Resources of Fars rarely on herbaceous hosts. Scale inside the province, were revised. Stereomicroscopy was used for petal almost reaching anther. Style 1 (united). observation of morphological and micro morphological Distribution in Iran: N, NW, W, C, NE. characters. Different Floras and references were used New hosts: Echinophora cinerea (Boiss.) Hedge & for the identification of the taxa (Boisser 1875, Yunker Lamond., Ferulago angulata (Schlecht.) Boiss., 1932, Koroleva 1934, Parsa 1949, Meshcheriakov Convolvulus L., Amygdalus scoparia Spach., Malus 1954, Terekhova 1964, Yuncker 1965, Kutateladze domestica Borkh., Citrus L., Ulmus L. 1967, Feinbrun 1972, Feinbrun 1978, Jafri 1978, 5. C. lehmanniana Bunge in A. Lehm., Mem. Sav. Plttmann 1978, Iranshahr 1983, Rajput 1988, Iranshahr Etrang. Petersh. 7: 396 (1851). 1999). - var. lehmanniana Typical characters: Stem thick. Mainly on trees and RESULTS shrubs rarely on herbaceous hosts. Style1 (united). The genus Cuscuta is represented in Iran by Scale inside the petal not reaching anthers (fig. 1.).

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Fig. 1. Cuscuta lehmanniana Bunge var. lehmanniana.

26 A revision of Cuscutaceae in Iran IRAN. J. BOT. 22 (1), 2016

Distribution in Iran: NE. Distribution in Iran: W. New hosts: Alhagi mannifera Desf. ), Agrimonia New hosts: Lycopersicum esculentum Mill., Peganum eupatoria L. harmala L.

Subgenus III Cuscuta 10. C. europaea L., Sp. Pl. 124 (1753). Sect. Epistigma Engelm ., Typical characters: Flowers usually 4- merous, 6. C. haussknechtii Yunck. Mem. Torrey Club. infrequently 5- merous, calyx tubes obtuse. 18:269(1932). Distribution in Iran: N, C, SE. Typical characters: Calyx truncate at margin of tube, New host: Polygonum L. calyx lobes very short, stigmas elongate. 11. C. epilinum Weihe., Arch. d. Apothekerver. in Distribution in Iran: W, C. nördll. Deutschland 8: 50, 51(1824). New hosts: Salvia multicaulis Vahl., Stachys L., Alhagi Typical characters: Usually parasite of Linum, calyx mannifera Desf., Onobrychis cornuta (L. ) Desv. lobes membranous, shorter than corolla tube. Distribution in Iran: NW, W. 7. C. kotschyana Boiss. Diagn. Pl. Or. Nov. 1, 7: 12. C. kurdica Engelm., Trans. Acad. Sci. St. Louis 29(1846) 1:470 (1859) Typical characters: Corolla lobes triangular, acute and Typical characters: 2-3 mm long, calyx lobes elongate. Ovary spherical. smooth, corolla lobes often erect. - var. kotschyana Distribution in Iran: NW, W, C. Typical characters: Corolla lobes more elongate and New hosts: Nepeta L., Thymus daenensis Celak., sharper than above. Ovary conical. Astragalus L., Acantholimon Boiss., Galium L. Distribution in Iran: NW, W, C, NE, E, SE. 13. C. palaestina Boiss., Diagn. Pl. Or. Nov. Ser. 2: 86 New hosts: Scandix aucheri Boiss., Achillea L., (1849). Jurinella Jaub & Spach., Arenaria persica Boiss., Typical characters: Flower 1. 5 – 2 mm long, calyx Juniperus excelsa M. B. ), Andrachne telephoides L., lobes smooth, rarely papillate, corolla lobes often Euphorbia L., Oxytropis DC. ), Atraphaxis L. inflexed. - var. caudata Bornm. & Schwarz. Distribution in Iran: N, NW, W, C, S. Typical characters: Calyx with distinct lobes, Calyx New hosts: Ferulago angulata (Schlecht. ) Boiss., lobes triangular. Scorzonera L., Scrophularia L. Distribution in Iran: N, NW, W, C, NE. 14. C. epithymum Murr. in L., Syst. Veget., ed 13, 140 (1774). 8. C. pedicellata Ledeb., Fl. Alt. 1: 293(1824). -var. epithymum Typical characters: Flowers small, 2-3 mm long, not Typical characters: Flowers elongated 2- 3 mm long, papillate, usually 4- merous, clustered in umbelliform apex of calyx and corolla very long and acute, calyx cymes. lobes smooth, rarely papillate. Distribution in Iran: N, NW, W, C, NE, S, SE. Distribution in Iran: N, NW, W, C, NE, E, S. New hosts: Pycnocycla Lindl., ebulus L., New hosts: Centaurea gaubae (Bornm) Wagenitz., Convolvulus L., Vicia erivilia (L.) Willd., Galium L., Cousinia Cass., Lacuca L., Nikitinia leptoclada Scrophularia L. (Bornm. & Sint. IIjin)., Euphorbia L., Ajuga L., Perovskia abrotanoids Karel., Phlomis aucheri Boiss., Sect. cuscuta Ziziphora clinopodioides Lam., Astragalus L., 9. C. babylonica Auch. ex Choisy, Mem. Soc. Phys. Acantholimon Boiss. Geneve 9:270 (1841). -var. kotschyi (Des Moulins) Engelm. - var. babylonica Typical characters: Flowers shorter than above, apex of Typical characters: Corolla lobes ovate- triangular, calyx and corolla shorter than above, calyx lobes equaling or shorter than tube, flowers smooth or papillate. sparsely papillate. Distribution in Iran: N, NW, W, C, NE, E, S. Distribution in Iran: NW, W, C, NE. New hosts: Pistacia atlantica Desf., Amygdalus New hosts: Satureja bachtiarica Bunge., Prosopis scoparia Spach. juliflora (Swartz) DC. ), Meristotropis xanthioides 15. C. brevistyla A. C. H. Braun ex A. Rich., Tent. Vassilez. Abyss. 2: 79 (1851). - var. elegans Engelm. Typical characters: Stigma and style together smaller Typical characters: Corolla lobes ovate- oblong, longer than ovary, calyx lobes thickened and fleshy, as long as than tube, flowers densely granular- papillate. corolla tube.

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Distribution in Iran: N, NW, W, C, NE, S. 18. C. approximata Babingt., Ann. et Mag. Nat. Hist. New hosts: Artemisia sieberi Besser., Centaurea L., 13: 253 (1844). Cousinia multiloba DC., Rhabdosciadium aucheri - var. approximate Boiss., Tanacetum polycephalum Schultz- Bip., Typical characters: Calyx and corolla lobes triangular Arenaria persica Boiss., Nepeta L., Phlomis cancellata to ovate, acute pointed apex, calyx shining and finely Bunge., Stachys trinerris Aitch. & Hemsl., Thymus L., netted with prominent veins when dry. Flowers and Ziziphora clinopodioides Lam., Asphodelus tenuifolius inflorescences large. Cav., Acantholimon Boiss., Pteropyrum aucheri Jaub. Distribution in Iran: N, NW, W, C, NE, E, S, SE. & Spach. New hosts: Buplerum L., Centaurea L., Helichrysum Mill., Capparis L., L., Hypericum 16. C. balansae Boiss. & Reut. ex Yunek., Gen. scabrum L., Ziziphora clinopodioides Lam., Cuscuta, Mem. Bot. Club. 18, 2: 290 (1932) Torr. Asphodelus tenuifolius Cav., Daphne mucronata Typical characters: Flowers 4- merous, calyx lobes Royle., Peganum harmala L. papillate, acute. Distribution in Iran: NW, W, C, NE, S. -var. urceolata (Kuntze) Yunck. New hosts: Cleome brachycarpa Vahl ex DC., Typical characters: Calyx lobes very turgid at apex, Taverniera glabra Boiss., L., Scrophularia wide of calyx lobes longer than its length, shining and L. finely netted with prominent veins when dry 17. C. planiflora Ten., Fl. Napolit. 3: 250 (1824. 1829). Distribution in Iran: N, NW, W, C, NE, E. - var. planiflora New hosts: Achillea L., Artemisia L., Scariola Typical characters: Flowers small, 1. 5 – 2 mm long, orientalis (Boiss. ) Sojak., Hypericum L., Perovskia corolla and calyx lobes longer than tubes, outer surface atriplicifolia Benth., Phlomis olivieri Benth. of calyx smooth. Distribution in Iran: C, S, SE. -var. shiraziana (Boiss. ) Yunck. New hosts: Bupleurum L., Artemisia scoparia Waldst. Typical characters: Flowers and inflorescences small. & Kit., Centaurea intricata Boiss., Platycheate Calyx and corolla lobes ovate, acute, calyx lobes glaucescens (Boiss. ) Boiss., Platycheate mucronifolia slightly turgid at apex, shining and finely netted with (Boiss. ) Boiss., Senecio vernalis Waldest. & Kit., prominent veins when dry. Erysimum oleifolium J. Gay., Gymnocarpus decander Distribution in Iran: W, C. Forssk., Helianthemum lipii (L. ) Pers., Convolvulus L., Andrachne telephoides L., Salvia L., Ziziphora L., -var. leucosphaera Boiss & Heldr. ex Yunk. Asphodelus tenuifolius Cav., Boerhavia elegans Typical characters: Calyx lobes very turgid at apex, Choisy., Papaver L., Astragalus L., Lotononis apex of calyx and corolla lobes very long, calyx lobes platycarpos (DC. ) Ecki. & Zeyh., Medicago longer than the broad, shining and finely netted with polymorpha L., Scorpiurus muricatus L., Taverniera prominent veins when dry. glabra Boiss., Acanthophyllum Boiss., Ziziphus spina- This species by Yunker& Rechinger (1964) reported christii (L. ) Willd. from Fars Province. But it was not found in the area.

-var. sicula (Tin. ex Engelm. ) Trab. KEY TO THE SPECIES Typical characters: Flowers large. Calyx lobes ovate- 1. Style 1 (united), stem thick, parasites of trees and abuts, rounded at apex, corolla and calyx lobes as long shrubs 2 as tubes, Outer surface of calyx smooth. - Style 2, stem thin to medium, parasites of dwarf Distribution in Iran: N, NW, W, C. shrubs and herbs 3 New hosts: Rhabdosciadium aucheri Boiss., Artemisia 2- Scale inside the petal not reaching anthers L., Marrubium L., Stachys L., Thymus L., Ziziphora 5. C. lehmanniana clinopodioides Lam. - Scale inside the petal almost reaching anthers 4. C. monogyna -var. papillosa Engelm. 3- Stigma capitate 4 Typical characters: Flowers large. Calyx lobes as long - Stigma elongate 6 as tube, elongate, acute, acuminate, very turgid at apex, 4- Capsule indehiscent 5 outer surface of calyx papillate. - Capsule dehiscent 3. C. chinensis Distribution in Iran: W. 5- Corolla lobes ovate or orbicular, obtuse or sub-acute, New hosts: Helianthemum lippii (L.) Pers. often erect to patent 1. C. australis

28 A revision of Cuscutaceae in Iran IRAN. J. BOT. 22 (1), 2016

- Corolla lobes triangular, acute, often inflexed (Iranshahr, 1983). 2. C. campestris In this work 17 species of Cuscuta were studied. C. 6- Capsule dehiscing irregularly, styles reduced or short australis R. Br., reported by Yunker & Rechinger and thick 7 (1964) from Gilan and Khorasan Provinces was not - Capsule dehiscing regularly, styles long and thin 9 found in neither of localities. Nevertheles we included 7- Flowers 4 mm long, 5 merous, papillate, sessile or it in the list of species of Iran. shortly pedicellate 8 Phytogeographically, the majority of the species of - Flower 2- 3 mm long, not papillate, usually 4 merous, Cuscuta are found in Irano-Turanian region, a few pedicellate, clustered in umbelliform cymes species are found in Saharo- Sindian and Euro- 8. C. pedicellata Siberian regions. Some species of this genus have a 8- Calyx truncate at margin of tube, calyx lobes very limited distribution in Iran and grow individually or in short, stigmas elongate 6. C. haussknechtii the small isolated patches. These species are usually - Calyx not truncate, with distinct and triangular lobes, very rare or can be endangered, but some species, have stigmas shorter than above 7. C. kotschyana widespread distribution in the country. 9- Flowers 5 merous, pedicellate in umbellate cymes, In this study about 266 plants which serve as hosts calyx truncate at margin of tube, with reduced lobes for Cuscuta were identified, among them 134 new 9. C. babylonica hosts are reported. The results showed that C. - Flowers 4- 5 merous, mostly sessile or shortly campestris with 43 hosts, C. planiflora with 32 hosts, pedicellate, cymes not as above, calyx with distinct C. epithymum with 28 hosts, C. approximata with 27 lobes 10 hosts, C. brevistyla with 26 hosts and C. monogyna 10- Flowers usually 4 merous, infrequently 5 merous11 with 23 hosts have the greatest number. - Flowers 5 merous, infrequently 4 merous 14 11- Calyx lobes obtuse 10. C. europaea ACKNOWLEDGEMENT - Calyx lobes acute 12 The authors are grateful to Mr. M. R. Joharchi for 12- Calyx lobes papillate, acuminate 16. C. balansae his guiding and Mr A. Hatami for identification of -Calyx lobes smooth, rarely papillate 13 many host plants. 13- Corolla lobes often erect, flowers 2-3 mm long 12. C. kurdica REFERENCES - Corolla lobes often inflexed, flowers 1. 5- 2 mm long Agrios, G. N. 1988. . Third ed. 13. C. palaestina Academic Press, Inc. San Diego. 803 p. 14- Stigma and style together smaller than ovary 15 Ainsworth, A. E & Gillespie. K. M. 2007. Estimation - Stigma and style together longer than ovary 16 of total phenolic content and other oxidation 15- Calyx lobes membranous, shorter than corolla tube, substrates in plant tissues using folin-ciocalteu usually parasite of Linum 11. C. epilinum reagent, Protocol. 24: 875-877. - Calyx lobes thickened and fleshy, as long as corolla Anjum, F, Bukhari, S. A, Shahid, M., Anwar, S. & tube 15. C. brevistyla Afzal, M. 2013. Comparative evaluation of 16- Calyx golden- yellow, shiny and finely reticulate, antioxidant potential of collected calyx lobes turgid at apex 18. C. approximata from different hosts. J Food Process Technol 4: - Calyx golden- yellow, shiny, not reticulate, calyx 228. doi:10. 4172/2157-7110. 1000228 lobes not as above 17 Boisser, E. 1875. Cuscuta in Flora Oricntalis. vol. 4: 17- Calyx lobes obtuse, fleshy, longer than calyx tube 115-123. Genevae & Basileae 17. C. planiflora Feinbrun, N. 1972: Cuscuta in Tutin, T. G. et al. Flora - Calyx lobes triangular, acute, membranous, as long as Europaea vol. 3: 74-77. Cambridge University calyx tube 14. C. epithymum Press. Feinbrun, N. 1978. Cuscuta in M. Zohary & N. DISCUSSION Feinburn- Dothan (eds. ) Flora Palaestina. vol. 3: Based on Flora Iranica, there are 17 species of 44-50. The Israel Academy of Sciences and Cuscuta in Iran ((Yunker & Rechinger 1964). After the Humanities. Jerusalem. draft of Flora Iranica, Cuscuta has been studied by Iranshahr, M. 1983. New records of Cuscuta from Iran. Iranshahr. In his study number of Cuscuta taxa Iran. Journal. Bot. 2 (1): 9-12. increasing to 18, among them C. campestris Yunck Iranshahr, M. 1999. Parasitic and semiparasitic reported as a new record to the flora of Iran. Also a flowering plants of Iran. vol. 1: 15- 56. Agricultural new gathering of C. haussknechtii Yunck., previously Research, Education and Extention Organization. only known from the type locality, was reported. Jafri, S. M. H & A, El-Gadi, 1978. Cuscutaceae, in

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