Larger Fungi – Indicator Species for Xerothermic Grasslands of Protected Area “Sheep Hills” Thracian Lowland (Bulgaria)

Original Contribution LARGER FUNGI – INDICATOR SPECIES FOR XEROTHERMIC GRASSLANDS OF PROTECTED AREA “SHEEP HILLS” THRACIAN LOWLAND (BULGARIA)

M. Lacheva*

Department of Botany and Agrometeorology, Agricultural University, Plovdiv, Bulgaria

ABSTRACT In the Protected Area “Sheep Hills”, xerothermic grasslands are semi-natural habitats developed on old volcanic and limestone hills. Xerothermic grassland belongs to the class Thero-Brachypodietea, and the alliances Thero-Brachypodion and Astragalo-Poion bulbosae. The xerothermic grasslands have their own characteristic mycota, as following steppe, xerothermic, and thermophilous fungi deserve special attention: Agaricus bernardii, A. comtulus, A. maleolens, Crinipellis mauretanica, Entoloma incanum, Hygrocybe virginea, H. persistens, Lepiota erminea, Leucopaxillus lepistoides, Tulostoma fimbriatum, and T. volvulatum. The studyfound the occurrence of 6 fungi included in the Bulgarian Red List of fungi and the Red Data Book in the Republic of Bulgaria – Amanita vittadinii, Crinipellis mauretanica, Geastrum melanocephalum, Myriostoma coliforme, Tulostoma fimbriatum, and T. volvulatum. The main factors threatening xerothermic grasslands of the Sheep Hills area, among others, the devastation and disappearance of natural habitats, often as a result of in appropriate land management as well as the pollution of air, water, and soil. The aim of the paper is to enrich the information about larger fungi indicator species for xerothermic grasslands in this protected area and the country.

Key words: Protected Area “Sheep Hills”, xerothermic grasslands, larger fungi, semi-natural habitats, Thero-Brachypodietea, steppe fungi, xerothermic fungi

INTRODUCTION podzolized cinnamon-forest soils. The The Protected Area “Sheep Hills” is situated in predominant soil types are cinnamon-podzolic the Тhracian Lowland region, in the land of soils (4). village of Ovchepoltsi, Pazardzhik municipality, Plovdiv distr., close to the Pazardzhik town. The The protected area is included in the national climate is transitional continental (1). Summers Natura 2000 Network, with the sole purpose of are warm and winters are mild and moderately protecting the natural habitat and maintain cold, without lasting snow cover and withsmall representative ecosystem for eastern sub- temperature amplitudes. Mediterranean dry grasslands, eastern forests of Quercus pubescens and pseudo-steppe with According to the physical and geographical grasses and annuals of the Thero- regionalisation, the mountain is situated within Brachypodietea; (BG0000365, Protected area the Thrace region (2, 3). The highest peak in the according to Directive 92/43/ЕЕСfor Sheep Hills is mainly constitutes of old and e conservation of natural habitats and of wild site and volcanic rocks, with some limestone out fauna and flora). This is the first mycological crops. Soil cover in the Protected Area is study conducted on the territory of this represented by shallow leached and interesting area. Data from this study in the ______Sheep Hills provide information on the fungi – *Correspondence to: Maria Lacheva, Department of indicator species in the xerothermic grasslands in Botany and Agrometeorology, Agricultural, Bulgaria. University-Plovdiv, 12, Mendeleev Str., 4000 Plovdiv, Bulgaria, e-mail: [email protected]

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LACHEVA M. The Protected Area “Sheep Hills” can be distributedin the communities belonging to the characterized by the presence of volcanic and class Thero-Brachypodietea. Collection of fruit limestone hills. Xerothermic grasslands bodies was carried out each year from April- developed on slopes of these hills are semi- October. Furthermore, fungi were also collected natural habitats. The development of outside the permanent study plots, using so- xerothermic grasslands was strictly connected called the itinerary method, which allowed us to with agricultural and pastoral farming of man. enrich observations and to gather data Typical representatives of the herbaceous plants concerning the composition of larger fungi are Aegilops neglecta, A. geniculata, Bromus species growing in the xerothermic grasslands. fasciculatus, B. madritensis, B. intermedius, Bothriochloa ischaemum, Brachypodium To illustrate the floristic composition and distachyon, Chrysopogon gryllus, Cynodon existing phytosociological relationships in the dactylon, Cynosurus echinatus, Dactylis investigated phytocoenoses, phytosociological glomerata, Dichanthium ischaemum, Eryngium study were performe dusing the (23) method. campestre, Knautia orientalis, Medicago The nomenclature for fungi is according to (24), minima, M. rigidula, Poa bulbosa, Salvia viridis, vascular plants according to (25), and plant Trifolium echinatum, T. purpureum, T. communities according to (26) and (27). The subterraneum, Xeranthemum annuum, etc.). author’s names of the fungal taxa are abbreviated These grasses belong to the class Thero- according to (28). Identification and Brachypodietea and the alliances Thero nomenclature of the specimens was performed Brachypodion, Astragalo-Poion bulbosae, according to (29-45). The conservation status is Trachynion distachya and Xerаnthemion annui. indicated according to the Red List of fungi in Bulgaria (46). Тhe larger fungi in xerothermic grasslands in Bulgaria are poorly known. A summary over Studied specimens are kept in the Agricultural view of macromycetes in Mediterranean and University (SOA) in Plovdiv; their accession sub-Mediterranean plant communities in the numbers are given in brackets atthe end of each country provides (5). The importance of this record. Specimens were collected by the author, problem stems from the fact that knowledge and unless other wise stated. literature on fungi associated with thermophilous The identification of the collected material was and xerothermic grasslands in Europe and done in two stages. In the first stage, if it was Bulgaria are still very inadequate (5-22). possible, fruit bodies were identified in fresh In recent years, many changes in the xerothermic samples, while during the second stage grassland communities of the Protected Area identification was performed after fruit bodies “Sheep Hills” have been observed. These had been dried. Microscopic features are changes may lead to the disappearance of rare observed and measured in lactophenol under an plants as well as whole phytocoenoses of an Amplival ML light microscope, with extreme interest. magnification ×1000.

The xerothermic grasslands have their own RESULTS AND DISCUSSION mycota characteristic for them. The aim of the Changes taking place in the plant communities investigations was to identify resources of larger have a strong influence on the species fungi growing in the xerothermic grasslands composition of fungi (11, 22). ofthe study area and to distinguish indicator During the course of the investigations on the species for them. The collected scientific mycobiota of the Sheep Hills xerothermic information will be used for analysis and grasslands, the occurrence of more than 46 planning activities on the conservation and species of larger fungi belonging to the classes management of the biodiversity in the protected Agaricomycetes was established. From among territory in the future. this group, 36 species were selected which were MATERIALS AND METHODS identified, based on their general distribution and The current research is based on observationsand habitat requirements, to be distinctly connected collection of larger fungi in the xerothermic with the xerothermic grasslands. These species grasslands of the Protected Area “Sheep Hills” can be considered to be indicative of this type of between 2010-2012. The study was carried out habitats (Table 1). in 12 permanent plots with size 1000 m2 each

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LACHEVA M. Table 1. List of larger fungi species from xerothermic grasslands in the Protection Area “Sheep Hills” Species of larger fungi Plant alliances in which the occurrence of larger fungi was confirmed Agaricus arvensis Schaeff. Astragalo-Poion bulbosae, Trachynion distachya A. bernardii Quél. Astragalo-Poion bulbosae A. comtulus Fr. Astragalo-Poion bulbosae, Trachynion distachya A. cupreobrunneus (F.H. Møller) Pilát Astragalo-Poion bulbosae A. campestris L. : Fr. Thero-Brachypodion, Trachynion distachya A. maleolens F.H. Møller Astragalo-Poion bulbosae A. xanthodermus Genev. Thero-Brachypodion, Trachynion distachya Agrocybe molesta (Lasch) Singer Astragalo-Poion bulbosae Amanita vittadinii (Moretti) Vittad. Astragalo-Poion bulbosae, Trachynion distachya Bovista plumbea Pers. : Pers. Thero-Brachypodion, Trachynion distachya Conocybe apala (Fr. : Fr.) Arnolds Astragalo-Poion bulbosae Coprinus comatus (O.F. Müll. : Fr.) Pers. Thero-Brachypodion, Trachynion distachya Crinipellis mauretanicaMaire Thero-Brachypodion C. scabella (Alb. & Schwein. : Fr.) Murrill Thero-Brachypodion Cyathus olla (Batsch. : Pers) Pers Astragalo-Poion bulbosae, Trachynion distachya Entholoma incanum (Fr. : Fr.) Hesler Thero-Brachypodion Geastrum fornicatum (Huds.) Hook. Thero-Brachypodion, Trachynion distachya G. melanocephalum (Czern.) V.J. Stanĕk Thero-Brachypodion G. rufescens Pers. : Pers. Thero-Brachypodion Hygrocybe miniata (Fr. : Fr.) P. Kumm. Astragalo-Poion bulbosae H. persistens (Britzelm.) Singer Thero-Brachypodion H. virginea (Wulfen : Fr.) P.D. Orton & Watling Astragalo-Poion bulbosae, Trachynion distachya Leucopaxillus lepistoides (Maire) Singer Thero-Brachypodion Lepiota erminea (Fr. : Fr.) P. Kumm. Thero-Brachypodion, Trachynion distachya Marasmius oreades (Bolton : Fr.) Fr. Thero-Brachypodion, Trachynion distachya Macrolepiota excoriata (Schaeff. : Fr.) Wasser Astragalo-Poion bulbosae,Trachynion distachya M. procera (Scop. : Fr.) Singer Thero-Brachypodion Panaeolus sphinctrinus (Fr.) Quél. Thero-Brachypodion, Trachynion distachya Pleurotus eryngii (DC. : Fr.) Quél. Thero-Brachypodion, Trachynion distachya Stropharia coronilla (Bull. : Fr.) Fr. Thero-Brachypodion, Trachynion distachya S. semiglobata (Batsch. : Fr.) Qéll. Astragalo-Poion bulbosae Tulostoma brumale Pers. : Pers. Thero-Brachypodion, Trachynion distachya T. fimbriatum Fr. Thero-Brachypodion T. volvulatum I.G. Borshch. Thero-Brachypodion Vascellum pratense (Pers. : Pers.) Kreisel Thero-Brachypodion, Trachynion distachya

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LACHEVA M. The analysis of the macromycetes species The habitats of the Sheep Hills xerothermic composition of the studied grasslands belonging grasslands are the place of occurrence of many to the class Thero-Brachypodietea reveals its interesting macromycetes species, some of uniqueness. Of particular importance are the which are consideredas rare and threatened both steppe, xerothermic, and thermophilous fungi in Bulgaria and Europe. The study found the whose presence underline the mycological occurrence of 6 fungi being on the Bulgarian relationship with the plant communities Red List of fungi (46) and Red Data Book in the belongingto the alliance Thero-Brachypodion, Republic of Bulgaria (51) which are as follows: and these are as follows: Entoloma incanum, Amanita vittadinii, Crinipellis mauretanica, Hygrocybe persistens, Lepiota alba, and Geastrum melanocephalum, Myriostoma Leucopaxillus lepistoides, although latter has the coliforme, Tulostoma fimbriatum, and T. most out standing features considered to be a volvulatum. typical steppe species (10, 11, 19, 22). The occurrence of typical steppic species of CONCLUSION macromycetes is very rare in Bulgaria. The effective protection of many plant species Additionally, other interesting fungi connected and macromycetes is only possible by protecting with the Astragalo-Poion bulbosae grasslands their entire semi-natural habitats, and not only are Agaricus bernardii, A. cupreobrunneus, and their single components. Hygrocybe virginea (22, 47). A characteristic The achieved results have a significant feature of the grassland mycobiota in this area is importance for the identification of the occurrence of calciphilous fungi that include, macromycetes biota growing in rare ecosystems among others Bovista plumbea, Entoloma in the communities belonging to the class Thero- incanum, Lepiota alba, Leucopaxillus Brachypodietea withinthe investigated area. The lepistoides, Geastrum minimum, and Tulostoma knowledge of selected fungi, which can be fimbriatum, which can beconsidered to be a considered to have diagnostic features, allows us characteristic species for the xerothermic to use these organisms for bioindication of their grasslands (11, 30). habitats. This is of particularly great significance Equally interesting and rare is Agaricus during the preparation of conservations plans for maleolens, a species that is associated with nature reserves and protected areas as well as xerothermic grasslands (30). Basidiomata of during the evaluation of negative impacts on the Crinipellis mauretanica develop on rotten sticks environment. in grassy placesand of Crinipellis scabella Hope that this study will enrich information occuron a largely degree on dry grass blades (21, about fungal diversity of the Protected Area 48-50). Fruit bodies of Stropharia coronilla, “Sheep Hills” as well as for the fungal diversity Marasmius oreades, Pleurotus eryngii and to xerothermic grasslands in Bulgaria, on the Vascellum pratense also occur in vast numbers. whole. These are fungi with a wide range of occurrence, mostly in the grasslandsin question, but also in REFERENCES psammophilous grassland, and in dry pine 1. Velev, S. Climatic regionalization. In: forests (11, 22). Geography of Bulgaria. Physical geography. Socio-economic geography. For The fungi associated with dry and warm habitats Com Publ. House, pp. 155-157, 2002. are the most interesting. These fungi belong to 2. Georgiev, M., Physical Geography of extremely specialised thermophilous and Bulgaria. Science and Art Publishing calciphilous organisms whose development is House, Sofia, p. 406, 1985 (Bg). possibleonly in deforested and open xerothermic 3. Yordanova, M., Velev, S., Drenovski, I., communities (22). A separate group comprises Characteristic features of the physical of fungi more often growing in the meadows and geographical regions. In: Geography of pastures, including among others Agaricus Bulgaria. Physical geography. Socio- arvensis, A. campestris,A. xanthodermus, economic geography., For Com Publ. Cyathus olla, Hygrocybe virginea, Macrolepiota House, pp. 409-411, 2002. excoriata and M. procera which are also present 4. Ninov, N., Soil-geographic Regions. In: intoxerothermic grasslands. Were observed and Geography of Bulgaria. I. Sofia, 397-405, some mushrooms developing on excrement, 1982 (Bg). namely Coprinus comatus, Panaeolus 5. Gjoševa, M., Macromycetes in sphinctrinus, and Stropharia semiglobata. Mediterranean and submediterranean plant Trakia Journal of Sciences, Vol. 13, № 1,2015 15

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