Ecological and floristic characteristics of Sideritis syriaca L. populations in Bulgaria

Ina Aneva Ljuba Evstatieva Antonina Vitkova Ecological and floristic characteristics of Sideritis syriaca L. populations in Bulgaria Authors address: Institute of Biodiversity and Еcosystem Research-BAS, Sofia, Bulgaria. Correspondence: Ina Aneva Institute of Biodiversity and Еcosystem Research-BAS, 2 Gagarin Str., 1113 Sofia, Bulgaria Tel.: +359 2 8717195 e-mail: ina.aneva@abv.bg ABSTRACT Sideritis syriaca L. is included in the Red Data Book of Bulgaria (2011) in the category of Critically Endangered plants (CR). The species has a very restricted distribution in Bulgaria limited to a few localities in Strandzha Mountain. As a result of our investigation a new locality was studied in the place in addition to the already known two localities. In this field, the population is stable with a high percentage of generative individuals and in relatively great numbers. Following the conducted research study, the populations of Sideritis syriaca L. is estimated in all three localities. New data about the population structure, vegetation dynamics and the place of the species in the phytocenoses and habitats are presented. The changes in the population status that have occurred during the last 10 years are compared with the existing data in the literature. Key words: Sideritis syriaca L., populations, structure, flora Introduction This paper gives a broad framework regarding the state of populations of Sideritis syriaca L., especially in relation to the species use and gathering. Now Sideritis syriaca L. has a very restricted distribution in Bulgaria in only three localities in Strandzha Mountain. Sideritis syriaca L. is a protected species included in the Red Data Book of the People`s Republic of Bulgaria (1984) and is under the Biodiversity Law (2002). A part of its population was existed in the reserves Sredoka and protected area. Studies on the population state of the species have been performed by Evstatieva & Vassilev (1994). They provide information on the distribution and ecological characteristic of the species only in two populations. In the new edition of Red Data Book of the Republic of Bulgaria (2011), the species is given under IUCN criteria in the category Critically Endangerd [CR B1ab (ii,iii,v) + 2ab (ii,iii,iv); C2a(i)]. The purpose of this study is to investigate the population structure, vegetation dynamics and the place of the species in the phytocenoses and habitats 10 years later. Materials and Methods During spring and summer of 2012, we listed and collected plants growing in the immediate vicinity of populations of Sideritis syriaca L. The collected data on species composition in the two investigated populations ( and ) and the new one recently discovered by employees of the Strandzha Nature Park ( ) are presented on Table 1. Field observations were carried out in sample plots, 100 m 2 in size. For a description made in the areas of and and three descriptions are made in the area. The aim is to cover the entire population and to determine the status of its size as accurately as possible. During the observations in the field GPS coordinates, altitude, some biotic and abiotic factors have been described. The data from the control populations were included in special Terrain form accepted by National System for bio monitoring (Gussev et al., 2008). The following keys were used for identification of plant material: Guide to the vascular plants in Bulgaria (Kozhuharov, 1992), Flora of RP Bulgaria (Jordanov, 1963-1979; Velchev & Kozhuharov, 1982; Velchev & Kuzmanov, 1989), Flora of R Bulgaria (Kozhuharov & Kuzmanov, 1995), Flora Europaea (Tutin et al., 1964 1980, 1993). 83

The plant life-forms are determined according to the classification of Raunkiaer (1937). The geographical floristic s are described according to Walter (1974), Assyov et al. (2006). Relation of species to humidity and light follows Bondev (1991), or is determined at the authors discretion. Table 1. List of established vascular plant species in the three localities of Sideritis syriaca L. in Strandzha Mountain, South- Eastern Bulgaria MAGNOLIOPHYTA MAGNOLIOPSIDA Apiaceae 1. Daucus carota L. + Eur-As A Th 2. Eryngium campestre L. + + + Pont-Med P H 3. Orlaya grandiflora (L.) Hoffm. + + + Ap-Bal A Th 4. Torilis leptophylla (L.) Rchb. + Med-CAs A Th 5. Scandix pecten-veneris L. + + Eur-As A Th Asteraceae 6. Achillea clypeolata Sibth. & Sm. + + + Bal P H 7. Achillea coarctata Poir. + + Pont-Med P H 8. Achillea collina + Eur-subMed P H 9. Achillea millefolium L. + Boreal P H 10. Anthemis tenuiloba (DC.) R.Fernandes + + Bal P H 11. Anthemis tinctoria L. + Eur-Sib P H 12. Artemisia campestris L. + subboreal P H 13. Carduus acanthoides L. + Eur A Th 14. Carlina acanthifolia All. + + Eur P H 15. Carlina vulgaris ssp. intermedia + Eur-Med A Th (Schur) Hayek 16. Centaurea affinis ssp. affinis Friv + Bal-Dac P H 17. Centaurea salonitana Vls. + Pont-Med P H 18. Centaurea scabiosa L. + Eur-Sib P H 19. Centaurea solstitialis L. + Eur-Med P H 20. Cichorium intybus L. + Eur-Sib P H 21. Crepis biennis L. + submed A Th 22. Crepis sancta (L.) Babcock + submed A Th 23. Crupina vulgaris Cass. + + + submed A Th 24. Echinops microcephalus Sibth. & Sm. + submed P H 25. Hieracium praeltum Vill ex Goch. + Eur P H subsp. bauchinii (Bess.) Petun 26. Inula aschersoniana Janka + Bal P H 27. Inula germanica L. + submed P H 28. Leontodon crispus Vill. ssp. aspirrimus + Pont-Med P H (Willd.) Finch et P. Sell. 29. Logfia arvensis (L.) J. Holub + Eur-Med P H 30. Tragopogon dubius Scop. + Eur-Med A Th 31. Xeranthemum annuum L. + + submed A Th 84

Betulaceae 32. Carpinus orientalis Miller + submed T Ph Boraginaceae 33. Cynoglossum creticum Mill. + Med-CAs A Th 34. Myosotis ramosissima Rochel + submed A Th Brassicaceae 35. Alyssum desertorum Stapf. + + Eur-Med A Th 36. Alyssum minutum Schlecht. ex DC. + Eur-Med A Th 37. Alyssum murale Waldst. & Kit. + Eur-subMed P H 38. Arabidopsis thaliana (L.) Heynh + subboreal A Th 39. Erysimum diffusum Ehrh + subboreal A H/Th 40. Sisymbrium altissimum L. + Pont-subMed A H/Th 41. Thlaspi alliaceum L. + submed A Th 42. Thlaspi perfoliatum L. + Eur-Med A Th Campanulaceae 43. Campanula sparsa ssp. frivaldskyi + Bal A Th (Steudel) Hayek 44. Jasione heldreichii Boiss. et Orph. + Eur-Med A Th Caryophyllaceae 45. Arenaria serpyllifolia L. + Eur-As A Th 46. Cerastium brachypetalum Pers. + Eur-Med A Th 47. Cerastium glomeratum Thuill. + Kos A Th 48. Dianthus armeria ssp. armeria L. + Eur A Th 49. Gypsophila muralis L. + Eur-As A Th 50. Lychnis coronaria (L.) Desr. + Med-OT P H 51. Minuartia caespitosa (Ehrh.) Degen + Eur-Med P H/Th 52. Minuartia hybrida (Vill.) Scischkin + Med-CAs A Th 53. Paronychia cephalotes (Bieb.) Bess. + + Pont P H 54. Petrorhagia prolifera (L.) P.W. Ball & + Pont-Med A Th Heywood 55. Scleranthus polycarpos L. + submed A H/Th 56. Silene otites (L.) Wibel + Eur-Med P H/Th 57. Silene subconica Friv. + submed A Th 58. Velezia rigida L. + submed A Th Cistaceae 59. Fumana procumbens (Dunal) Gren. et Godr. + Pont-Med B Ch 60. Helianthemum numularium (L.) Mill. + + Alp-Med B Ch Convolvulaceae 61. Convolvulus cantabricus L. + Pont P H Crassulaceae 62. Sedum acre L. + + + Eur-Med P Ch 63. Sedum album L. + submed P Ch 64. Sedum hispanicum L. + Eur-Med P Ch Cuscutaceae 65. Cuscuta campestris Yunker + Adv A E 85

Euphorbiaceae 66. Euphorbia cyparissias L. + + Eur P H 67. Euphorbia myrsinithes L. + submed P H 68. Euphorbia niciciana Borbas ex Novak + Med P H 69. Euphorbia taurinensis All. + submed A Th Fabaceae 70. Coronilla scorpioides (L.) Koch. + submed A Th 71. Hymenocarpus circinatus (L.) Savi. + Med A Th 72. Medicago minima (L.) Bart. + + Eur-As A Th 73. Medicago rigidula (L.) All. var agrestis (Ten.) Burn. + Eur-Med A Th 74. Onobrychis arenaria (Kit.) DC. + + SPont A Th 75. Ononis pusilla L. + submed P H 76. Trifolium angustifolium L. + Med A Th 77. Trifolium scabrum L. + Med-As A Th Geraniaceae 78. Geranium bohemicum L. + submed A Th 79. Geranium purpureum Vill. + Med A Th Globulariaceae 80. Globularia aphyllanthes Crantz + Eur P H Hypericaceae 81. Hypericum cerastoides + submed P H 82. Hypericum perforatum L. + + Kos P H 83. Hypericum hirsutum L. + Eur-Sib P H Lamiaceae 84. Acinos arvensis (Lam.) Dandy + Eur-Med A Th 85. Acinos suaveolens Sibth. & Sm. + submed P H 86. Ajuga chamaepitys (L.) Schreber + Pont-Med A H/Th 87. Clinopodium vulgare L. + + subboreal P H 88. Marrubium peregrinum L. + submed P H 89. Melissa officinalis ssp. Altissima (Sibth. + submed P H & Sm.) Arcangeli 90. Sideritis montana L. + + + submed P H 91. Sideritis syriaca L. + + + Med P H 92. Stachys recta L. + Eur-Med P H 93. Teucrium chamaedrys L. + + submed P H 94. Teucrium montanum + + submed P H 95. Teucrium polium L. + + + Pont-Med P H 96. Thymus callieri Borbas ex Velen. + Pont P Ch Oleaceae 97. Fraxinus ornus L. + submed T Ph 98. Jasminum fruticans L. + Pont-CAs B C 99. Phillyrea latifolia L. + Med T Ph Paeoniaceae 100. Paeonia tenuifolia L. + submed P H 86

Papaveraceae 101. Hypecoum imberbe Sibth. & Sm. + submed A Th Plantaginaceae 102. Plantago lanceolata L. + + Kos P H 103. Plantago major L. + Boreal P H 104. Plantago scabra + Eur-Sib A Th 105. Plantago subulata L. + Med P H Plumbaginaceae 106. Armeria rumelica Boiss. + Bal P H 107. Plumbago europaea L. + + submed P H Primulaceae 108. Anagalis arvensis L. + Kos A Th 109. Primula veris L. + + Eur-Med P H Ranunculaceae 110. Clematis vitalba + Eur B Ph 111. Thalictrum minus L. + Eur-As P H Rosaceae 112. Crataegus monogyna Jacq. + subboreal B Ph 113. Potentilla pedata Willd. + Med P H 114. Prunus spinosa L. + Pont B Ph 115. Pyrus piraster + submed T Ph 116. Rubus canescens DC. + Eur-Med B C 117. Sanguisorba minor Scop. ssp. muricata + + subboreal P H Briq. Rubiaceae 118. Asperula arvensis L. + Eur-Med A Th 119. Asperula cynanchica L. + Eur-Med P H 120. Crucianella angustiffolia L. + Med A Th 121. Galium paschale Forssk. + Bal-Anat P H 122. Galium tenuissimum M. B. + Pont-CAs A Th Rutaceae 123. Dictamnus albus L. + Eur-As P H Scrophulariaceae 124. Linaria pelisseriana (L.) Miller + + Med A Th 125. Linaria vulgaris Miller + Eur-Sib P H 126. Odontites verna (Bellardi) Dumort. + Eur A Th ssp. serotina (Dumort.) Corb. 127. Parentucellia latifolia (L.) Caruel + Med A Th 128. Rhinanthus rumelicus ssp. rumelicus Velen. + Eur-Med A Th 129. Scrophularia canina L. + Eur-Med P H 130. Verbascum phoeniceum L. + Eur-Sib P H 131. Verbascum phlomoides L. + Eur P H 132. Veronica arvensis L. + Eur-Sib A Th 133. Veronica chamaedrys L. + Eur-As P H 134. Veronica turrilliana Stoj. et Stef. + Bal P H 87

Valerianaceae 135. Valerianella carinata Loisel. + Eur-Med A Th 136. Valerianella pumila (L.) DC. + Pont-Med A Th LILIOPSIDA Cyperaceae 137. Carex digitata L. + Eur-Sib P H Iridaceae 138. Iris reichenbachii Heuff. + Bal P H Liliaceae 139. Allium rotundum L. + + Eur-OT P Cr 140. Muscari neglectum Guss. + + Med-OT P G Poaceae 141. Aegilops neglecta Req. ex Bertol. + + submed A Th 142. Agropyron brandzae Pantu & Solac. + Pont P H 143. Agrostis canina L. + Eur-Sib P H 144. Anthoxanthum odoratum L. + + Eur-As P H 145. Avena fatua L. + Boreal A Th 146. Brachypodium pinnatum (L.) P. Beauv. + + Sib P H 147. Briza media + Eur P H 148. Bromus madritensis L. + + Med A Th 149. Bromus mollis L. + Boreal A Th 150. Chrysopogon gryllus (L.) Trin. + + + Pont-Med P H 151. Cynosurus cristatus L. + + Eur P H 152. Cynosurus echinatus L. + submed A Th 153. Dactylis glomerata L. ssp. glomerata + + Eur-As P H 154. Desmazeria rigida (L.) Tutin + + submed A Th 155. Festuca valesiaca Scheicher ex Gaudin + Pont P H 156. Koeleria simonkaii Adamovic + Eur P H 157. Lolium perenne L. + + Eur-As P H 158. Lophochloa cristata (L.) Hyl. + Med A Th 159. Melica ciliata L. + + Eur-subMed P H 160. Phleum subulatum (Savi) A. et G. + + Eur-As A Th 161. Poa bulbosa L. + + + Eur-As P H 162. Stipa capillata L. + Pont-Med P H 163. Vulpia myuros (L.) C.C. Gmelin + subboreal A Th Legend: types: A (annual herb), P (perennial herb), B (bush), T (tree). forms: Ph (phanerophyt), Ch (chamaephyt), H (hemicryptophyt), Cr (cryptophyt), T (therophyt). s: Adv (adventive), Ap-Bal (Apenino-Balkan), Bal (Balkan endemic), Bal-Anat (Balkan-Anatolian), Boreal (Boreal), Eur (European), Euro-As (Euro-Asian), Euro-Med (Euro-Mediterranean), Euro-SubMed (Euro- SubMediterranean), Euro-Sib (Euro-Siberian), Kos (Cosmopolitian), Med (Mediterranean), Med-CAs (Mediterrano-Central Asian), Pont-Med (Pontic-Mediterranean), Pont-SubMed (Pontic-Submediterranean), SubBoreal (Sub-Boreal), SubMed (Sub Mediterranean), spont (Sub-Pontic) 88

Results Locality in the area of "" is in the most volatile state (4-5 km from the town of Malko Tarnovo, the road to the village Stoilovo N 42.01603, E 27.49665). In many places there is an outlet on basic rock. The altitude is 317 m a. s. l. The population of Sideritis syriaca L. is nearly destroyed. There are only leaves at the base of 5 plants - flowering stalks were harvested before the period of full bloom. The main threat to the deposit is its proximity to trunk road and intensive pasture. 84 species from 24 families are identified in the studied region. The greatest number species are represented the following families (Figure 1): Asteraceae (17 species), Lamiaceae (10 species), Poaceae (10 species), Caryophyllaceae (6 species) and Scrophulariaceae (6 species). The total projective cover of species is around 50% for in many places there is access to the bedrock. The tree layer is represented by low trees Fraxinus ornus L., Quercus polycarpa Scur. The vast majority of the field is occupied by thermophilic shrubs Phillyrea latifolia L., Jasminum fruticans L. The coverage of herbaceous species is around 30% and that of Sideritis syriaca L. is only 1%. Perennial herbs (50 species) prevail among the biological types but the number of annual herbs is also great (27 species) Figure 2. The main geographical s are those with Mediterranean origin or close to it - 38 species are divided between the following groups: submed (17 species), Eur-Med (13 species), Med (4 species), Eur-subMed (2 species) and Med-As (2 species). The number of species with Pontic origin (15 species) also takes important role in the floristic composition. The floristic s with subboreal origin are only 4 species. Balkan endemics and subendemics have comparatively great participation 7 species (Figure 3). In relatively good condition locality of Sideritis syriaca L. is that in the area (N 42.00556, E 27.52780, 389 m a. s. l.). The population of Sideritis syriaca L. is presented of 17 developed tuffs with a diameter between 30 and 50 cm. Each tuff has a 7-17 flowering stems. The total projective cover of vegetation is about 70%. The projective cover of woody species is only 5% as the locality is open meadow surrounded by forest habitats (a species of the genus Quercus and Carpinus). The meadow occupies a smaller area. The projective cover of herbaceous species is around 60%. There have been established 75 species from 23 families. The most represented plant families are (Figure 1): Poaceae (17 species), Asteraceae (10 species), Fabaceae (5 species) and Lamiaceae (5 species). The identified species are divided according to their biological type as follows (Figure 2): 37 species of perennial herbaceous plants (49% of all), 35 annual plant species (47% of all), 1 brush species and 2 tree species. The geo characteristics of the plants growing on this field (Figure 3) reveals that the Mediterranean representatives prevail (27 species), followed by these with European origin (16 species). The locality in the " " (N 41.98790, E 27.48727, 500 m a. s. l.) is in the safe condition. The exhibition is east, the slope is 26 to 30 degrees and the basic rock is limestone. Sideritis syriaca L. population consist of 72 well developed plants with a diameter between 20 and 70 cm. 60 individuals of them are generative and have between 5 and 22 flowering stems. The total projective cover of vegetation is about 90%. There have been established 56 species from 20 families. The families Poaceae (10), Asteraceae (7), Lamiaceae (7) and Caryophyllaceae (6) are represented by the greatest number of species (Figure 1). According to the biological spectrum of the investigated field (Figure 2), the most prevalent are the perennial herbs (35 species), followed by the annual herbs (17 species). The Sub- Mediterranean chorological type dominates the flora of the study field with 11 species followed by the Euro- Mediterranean (with 6 species) and Pont-Mediterranean (with 6 species) groups (Figure 3). Figure 1. Taxonomic structure of the three localities of Sideritis syriaca L. in Strandzha Mountain, South-Eastern Bulgaria. 89

Figure 2. Distribution of biological types of the three localities of Sideritis syriaca L. in Strandzha Mountain, South-Eastern Bulgaria. Sideritis syriaca L. Of significant importance for the type of vegetation appears limestone rock base. Many of the species are basophilic. Due to very specific geographic factors, the vegetation of Strandzha Mountain is subject to different floristic influences. One can distinguish between the Mediterranean influence, the eastern (or oriental) influence, and in some cases the influence of the Middle European mountain flora. The high presence of taxa with Mediterranean and Pontic origin is mostly typical for the termophilous herbaceous communities. The population status of Sideritis syriaca L. in all three localities is unstable and threatened. The most affected is the field in the "" due to its proximity to the trunk road and respectively its easy accessibility. However the populations of Sideritis syriaca L. are in slightly better condition than 10 years ago. As was already mentioned, the species is included in the new edition of the Red Data Book of the Republic of Bulgaria (2011) under category of Critically Endangered plants (CR). Because of its conservation value it is included in the Annex 3 of the Law for the Diversity of Bulgaria (2002). In addition the localities are part of the Strandzha Nature Park and are under its protection in order to long-term conservation of the unique nature. Acknowledgement Figure 3.Geographical structure of the three localities of Sideritis syriaca L. in Strandzha Mountain, South-Eastern Bulgaria. Discussion All three localities of Sideritis syriaca L. share many environmental characteristics - the ecological factors that have the biggest impact on the floristic composition in these habitats are intensive light, air temperature and low humidity, limestone rock base, soil type, its quantity, temperature and humidity. There is also similarity in the biological type and life forms of the surrounding plant species as a result of similar environmental conditions. According to the biological spectrum of the investigated fields, the most prevalent are the perennial herbs, but the number of annual herbs is significant. Increased participation of annual plants is common for open, arid, dry and sunny places which are typical habitats of The authors are grateful to Eng. Stefan Zlatarov, Director of The Department of the Nature Park "Strandzha" for the assistance and provision of access to the localities. The financial support provided by the Bulgarian National Science Fund, Ministry of Education, Youth and Science (Project DTK 02/38) is also very much appreciated. References Assyov B, Petrova A. 2006. Conspectus of the Bulgarian Vascular Flora. Distribution Maps and Floristic Elements. Ed. 3. BBF, Sofia, p. 454. Biodiversity Act. 2002. Bulgarian Ministry of Environment and Water. Bondev I. 1991. The vegetation of Bulgaria. Map in scale 1:600 000 with explanatory text. Publ. House of Sofia University St. Kliment Ochridsky, Sofia, p. 183 (In Bulgarian). Evstatieva L, Vassilev P. 1994. Distribution, ecological peculiarities and phytocoenology of Sideritis syriaca L. in Bulgaria. Proceeding of a jubilees symposium, 2: 181 186. 90

Gussev C, Dimitrova D, Tzoneva S. 2008. Method for monitoring of higher plants. In: http://www.chm.moew.government.bg/iaos/ (accessed 2008), Expert Report on Higher Plants, Subject to National Monitoring System for Biodiversity (in Bulgarian). Jordanov D. (eds) 1963-1979. Flora na Narodna Republika Bălgarja, 1-7,. In: Aedibus Acad. Sci. Bulgaricae, Serdicae (in Bulgarian). Kožuharov S, Kuzmanov B. (eds) 1995. Flora na Republika Bălgarja, 10. Sofja. Kozhunarov S. 1992. Guidance of the vascular plants in Bulgaria. Nauka i izkustvo, Sofia (in Bulgarian). Peev D. 2011. Red Data Book of the Republic of Bulgaria, Vol.1. Plants. Digital edition. website: http://e-ecodb.bas.bg/rdb/en/vol1/ Raunkiаеr C. 1937. -form, genus area, and number of species. Botaniske Studier, 5. haefte (ed C. Raunkiær), Schultz Forlag JH, København, p. 343-356. Tutin G, Heywood H, Burges A, Valentine H, Walters M, Webb A. 1993. Flora Europea. Vol. 1, 2nd ed. Cambridge University Press, Cambridge, U.K. Velčev V. 1984. Red data book of PR Bulgaria, 1. Plants. Sofia. Velčev V, Kožuharov S. 1982. Flora na Narodna Republika Bălgarja, 8. Sofja. Velčev V, Kuzmanov B. 1989. Flora na Narodna Republika Bălgarja, 9. Sofja. Walter H. 1974. Vegetationstonen und Klima. Stutgart, p. 75 88. 91