082 karadelev & rusevska - ecology and distribution of tulostoma

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437 Scientific Area D • Fungal diversity Ecology and distribution of species from genus Tulostoma (Gasteromycetes) in the Republic of Macedonia Mitko Karadelev & Katerina Rusevska Institute of Biology, Faculty of Natural Science and Mathematics, Arhimedova 5, P.O. Box 162, 1000 Skopje, Republic of Macedonia, e-mails: [email protected]; [email protected] Abstract. This paper contains results on the subject of the ecology and distribution of the genus Tulostoma in the Republic of Macedonia. Insufficient data about the distribution of four species (Tulostoma brumale, T. caespitosum, T. fimbriatum, T. melanocyclum) have been published so far; therefore the aim of this work is to provide a more comprehensive review on the ecology and distribution of this systematic category in the Republic of Macedonia. The species T. squamosum is new for the mycobiota of the Republic of Macedonia. A total number of five species from the genus Tulostoma have been found. Key words: distribution, ecology, reported species, R. Macedonia, Tulostoma spp. Introduction Systematic research on the genus Tulostoma Persoon 1974 : Persoon 1801 (Basidiomycota, Gasteromycetes, Tulostomataceae) has not been conducted up till now in the Republic of Macedonia, and there are rather few mycological papers concerned with individual spe- cies of this genus only, from one or two localities in the Republic of Macedonia. Publications making ref- erence to individual species of Tulostoma genus are as follows: T. brumale (Rusevska & Karadelev 2004), T. caespitosum (Wright 1987), T. fimbriatum (Lindt- ner 1939; Pilát & Lindtner 1939) and T. melanocyclum (Tortić 1988). Consequently, the objective of this pa- per is to present a more comprehensive list about the ecology and distribution of the Tulostoma species in the Republic of Macedonia. The distinctive features of this genus are the fol- lowing: a typical Tulostoma gastrocarp comprises a spore-sac or peridium and a stem. The spore-sac is usually a globose-depressed to hemispheric recepta- cle. It develops hypogeously, and upon maturation of the spores the elongation of the stem pushes it above the soil surface, and at the same time an apical open- ing appears – the stoma (mouth) – that allows spore dispersion. The peridium is composed of two distinct layers, not always easy to distinguish: the exoperidium and the endoperidium. Gleba pulverulent, yellowish brown. Capillitium simple or branched, septate, even- tually with swollen septa, where disarticulation usually takes place, showing thick walls without pores. Spores globose to ovoid, smooth or with different kind of or- namentation, such as spiny, warty, reticulate, etc. Material and methods The sources of this list are published papers, exsic- cates deposited in different collections, and research notes of the present authors. Some of the specimens, as mentioned above, have been preserved at the Natu- ral History Museum in Belgrade (BEO), Botanical De- partment, Faculty of Science in Zagreb (ZA) and in the National Collection of Fungi, FUNGI MACEDO- NICI (exs. MAK) at the Institute of Biology, Faculty of Natural Science, Ss Cyril and Methodius Universi- ty in Skopje. All species without any fungaria marks in the text have been collected and determined by the present authors. The identification of Tulostoma species has been made according to Pilát (1958), Jülich (1984), Breiten- bach & Kränzlin (1986), Wright (1987), Miller & Miller (1988), Pegler & al. (1995), Hansen & Knudsen (1997), Calonge (1998) and Krieglsteiner (2000). In a few cases, the names of the species have been modified according 57 • Proceedings of IV BBC – Sofia ' 2006

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437Scientific Area D • Fungal diversity

Ecology and distribution of species from genus Tulostoma (Gasteromycetes) in the Republic of Macedonia

Mitko Karadelev & Katerina Rusevska

Institute of Biology, Faculty of Natural Science and Mathematics, Arhimedova 5, P.O. Box 162, 1000 Skopje, Republic of Macedonia, e-mails: [email protected]; [email protected]

Abstract. This paper contains results on the subject of the ecology and distribution of the genus Tulostoma in the Republic of Macedonia. Insufficient data about the distribution of four species (Tulostoma brumale, T. caespitosum, T. fimbriatum, T. melanocyclum) have been published so far; therefore the aim of this work is to provide a more comprehensive review on the ecology and distribution of this systematic category in the Republic of Macedonia. The species T. squamosum is new for the mycobiota of the Republic of Macedonia. A total number of five species from the genus Tulostoma have been found.

Key words: distribution, ecology, reported species, R. Macedonia, Tulostoma spp.

Introduction

Systematic research on the genus Tulostoma Persoon 1974 : Persoon 1801 (Basidiomycota, Gasteromycetes, Tulostomataceae) has not been conducted up till now in the Republic of Macedonia, and there are rather few mycological papers concerned with individual spe-cies of this genus only, from one or two localities in the Republic of Macedonia. Publications making ref-erence to individual species of Tulostoma genus are as follows: T. brumale (Rusevska & Karadelev 2004), T. caespitosum (Wright 1987), T. fimbriatum (Lindt-ner 1939; Pilát & Lindtner 1939) and T. melanocyclum (Tortić 1988). Consequently, the objective of this pa-per is to present a more comprehensive list about the ecology and distribution of the Tulostoma species in the Republic of Macedonia.

The distinctive features of this genus are the fol-lowing: a typical Tulostoma gastrocarp comprises a spore-sac or peridium and a stem. The spore-sac is usually a globose-depressed to hemispheric recepta-cle. It develops hypogeously, and upon maturation of the spores the elongation of the stem pushes it above the soil surface, and at the same time an apical open-ing appears – the stoma (mouth) – that allows spore dispersion. The peridium is composed of two distinct layers, not always easy to distinguish: the exoperidium

and the endoperidium. Gleba pulverulent, yellowish brown. Capillitium simple or branched, septate, even-tually with swollen septa, where disarticulation usually takes place, showing thick walls without pores. Spores globose to ovoid, smooth or with different kind of or-namentation, such as spiny, warty, reticulate, etc.

Material and methodsThe sources of this list are published papers, exsic-cates deposited in different collections, and research notes of the present authors. Some of the specimens, as mentioned above, have been preserved at the Natu-ral History Museum in Belgrade (BEO), Botanical De-partment, Faculty of Science in Zagreb (ZA) and in the National Collection of Fungi, FUNGI MACEDO-NICI (exs. MAK) at the Institute of Biology, Faculty of Natural Science, Ss Cyril and Methodius Universi-ty in Skopje. All species without any fungaria marks in the text have been collected and determined by the present authors.

The identification of Tulostoma species has been made according to Pilát (1958), Jülich (1984), Breiten-bach & Kränzlin (1986), Wright (1987), Miller & Miller (1988), Pegler & al. (1995), Hansen & Knudsen (1997), Calonge (1998) and Krieglsteiner (2000). In a few cases, the names of the species have been modified according

57 • Proceedings of IV BBC – Sofia ' 2006

438 Plant, fungal and habitat diversity investigation and conservation • Proceedings of IV BBC – Sofia ' 2006

to Index Fungorum (2005). The species are reported al-phabetically. Under each fungal species, data on the ge-ographical distribution, altitude, forest association, data source and previous publications are provided.

ResultsOf about twenty species of Tulostoma genus identified in Europe, to date the following five species have been recorded in the Republic of Macedonia, presented in a list with the localities, altitude, association, datum, ex-siccate (exs.) and previous published data:

1. Tulostoma brumale Pers.Bogdanci: Gjavato vill., Gjurov Dol, 100 m, Querco coc-ciferae–Carpinetum orientalis, 17.12.1988, exs. MAK 88/4705; Galichica Mt: Ohrid side, near spring, 1400 m, on grass, 22.11.2002, exs. MAK 02/3042; Kichevo: Iz-vor vill., 500 m, 23.03.2004, exs. MAK 04/793; Ku-manovo: 400 m, Querco–Carpinetum orientalis mac-edonicum, 20.03.2003, exs. MAK 03/3059; between Zubovce vill. and Shuplji Kamen vill., 400 m, Querco–Carpinetum orientalis macedonicum, 15.04.2003, exs. MAK 03/1427; Zubovce vill., Bislim, 500 m, degrad-ed forest, 07.03.2004, exs. MAK 04/3976; D'lga, 400–450 m, Querco–Carpinetum orientalis macedonicum, 12.03.2003, exs. MAK 03/3837; near Skopje: Vodno, 900 m, in meadow, 04.05.2003, exs. MAK 03/3095; 500–1000 m, Querco–Carpinetum orientalis macedon-icum, 20.10.2002, exs. MAK 02/3000; 400 m, in mead-ow with Juniperus, 01.01.2003, exs. MAK 03/2928; be-tween Sredno Vodno and Matka, 900 m, 04.2004, exs. MAK 04/3975; Skopje – Veles road: St. Jovan Veter-ski monastery, 150–200 m, Juniperus excelsa forest, 23.10.2002, exs. MAK 02/2879; Skopska Crna Gora Mt: between Gornjane vill. and Blace vill., 700 m, de-graded oak forest, 25.01.2003, exs. MAK 03/3234.

2. Tulostoma caespitosum Trab. apud Sacc.Rabrovo vill., Strumica, leg. Wilson (Herb. Lloyd n° 15.425, BPI) – Wright (1987).

3. Tulostoma fimbriatum Fr.Belasica Mt: Koleshino vill., between Daravica riv-er and Baba river, 350 m, Quercus and Castanea for-est, 01.01.2003, exs. MAK 03/2893; Bogdanci: 150 m, meadow in Querco cocciferae–Carpinetum orientalis, 12.12.2005, exs. MAK 05/5516; Kuchalat, 200–300 m, Querco cocciferae–Carpinetum orientalis, 02.01.2003,

exs. MAK 03/4751; Gorni Bolovan, 200 m, Querco coc-ciferae–Carpinetum orientalis, 10.08.2002, exs. MAK 02/3741; near Krivolak: Orlovo Brdo, 150–225 m, 16.03.1939, 20.03.1939, Lindtner (1939), published as T. granulosum Lév. M.; Kumanovo: 400 m, Querco–Carpinetum orientalis macedonicum, 20.03.2003, exs. MAK 03/1403; Dobroshane vill., 350 m, mixed forest, 10.04.2005, exs. MAK 05/4866; near Skopje: Vodno, 450 m, pasture, 09.10.1937, exs. BEO, Pilát & Lindtner (1939), published as T. granulosum; Prespa: Nakolec vill., 850 m, Salicetum, 12.06.2003, exs. MAK 03/3254; Ruen Mt: Staro Nagorichane vill., 600 m, degrad-ed habitat (Paliurus spina-cristi, Quercus pubescens), 30.11.2002, exs. MAK 02/1424; Zhegljane vill., 800 m, Pinus plantings, 18.11.2002, exs. MAK 02/2913.

4. Tulostoma melanocyclum Bres.Kumanovo: 400 m, Querco–Carpinetum orientalis macedonicum, 20.03.2003, exs. MAK 03/836; between Zubovce vill. and Shuplji Kamen vill., 400 m, Quer-co–Carpinetum orientalis macedonicum, 15.04.2003, exs. MAK 03/1198; near Prilep: Pletvar, exs. ZA, SKO, Tortić 1988; Prespa: Nakolec vill., 850 m, Sali-cetum, 12.06.2003, exs. MAK 03/1395; Ruen Mt: Staro Nagorichane vill., 600 m, degraded habitat (Paliu-rus spina-cristi, Quercus pubescens), 30.11.2002, exs. MAK 02/1208.

5. Tulostoma squamosum Pers.Gradsko: Stobi, 150–200 m, meadow, 30.12.2003, exs. MAK 03/3646; Kichevo: Izvor vill., 500 m, 23.03.2004, exs. MAK 04/3955; Kumanovo: 400 m, Querco–Carpinetum orientalis macedonicum, 20.03.2003, exs. MAK 03/1220; between Zubovce vill. and Shuplji Ka-men vill., 400 m, Querco–Carpinetum orientalis mac-edonicum, 15.04.2003, exs. MAK 03/1185; D'lga vill., 650–700 m, Querco–Carpinetum orientalis macedon-icum, 12.03.2003, exs. MAK 03/1226; Ruen Mt: Staro Nagorichane vill., 600 m, degraded habitat (Paliu-rus spina-cristi, Quercus pubescens), 30.11.2002, exs. MAK 02/332; 600 m, at roadsides, near arable land, 25.10.2005, exs. MAK 05/821; beside Pchinja river, 550 m, Querco–Carpinetum orientalis macedonicum, 18.11.2003, exs. MAK 03/2939; near Skopje: Vodno, 500–1000 m, Querco–Carpinetum orientalis macedoni-cum, 20.10.2002, exs. MAK 02/1372; Markov Manastir monastery, 250 m, meadow, 06.01.2003; Skopje – Ve-les road: St. Jovan Veterski monastery, 150–200 m, Ju-niperus excelsa forest, 23.10.2002, exs. MAK 02/1203.

439Scientific Area D • Fungal diversity

DiscussionOf about twenty species of Tulostoma genus known in Europe, to date in the Republic of Macedonia the fol-lowing five species have been recorded: T. brumale, T. caespitosum, T. fimbriatum, T. melanocyclum, and T. squamosum. The localities where these fungi were found are presented on Figs 1, 2, 3 and 4.

Tulostoma brumale is psammophilous or humicolous, but does not grow in truly desert zones, but rather in ar-eas with vegetation protection, or on sandy soils among herbs, mosses, etc., generally solitary in large num-bers, frequently mixed with other species in the same population, particularly with T. melanocyclum (Wright 1987). According to Krieglsteiner (2000), this is the most common species of the Tulostoma genus in Eu-rope. In the Republic of Macedonia it grows on soil or sandy soil and is found in following associations: Quer-co–Carpinetum orientalis macedonicum, Querco coccif-erae–Carpinetum orientalis, Juniperus excelsa forest and in meadows. As regards its vertical distribution, it is found between 100 m and 1400 m altitude, registered in more than ten localities. Fruiting all the year, our ma-terial was collected in I, III–V and X–XII. According to Karadelev (2000), this species is included in the Prelim-inary Red List for the Republic of Macedonia, as a rare species, but judging by the unpublished data, a conclu-sion may be drawn that it is not a rare species (Fig. 1).

Tulostoma fimbriatum grows on sandy soil, both in open areas, forests and gardens (Calonge 1998). Accord-ing to Wright (1987), this is a typical European species, and probably the most common one. For the Republic of Macedonia, there are only few data; therefore a conclu-

sion on its frequency cannot be drawn. According to the existing data, it is not a very common species (Fig. 2). Tu-lostoma fimbriatum has been found in the following as-sociations: Querco–Carpinetum orientalis macedonicum, Querco cocciferae–Carpinetum orientalis, Quercus and Castanea forest, Pinus plantings, Salicetum and in mead-ows. The first data for this species in Republic of Macedo-nia were published by Lindtner (1939) and Pilát & Lindt-ner (1939), from Vodno and Orlovo Brdo (near Krivolak), respectively. The new data are from the following locali-ties: Kumanovo, the mountains of Ruen and Belasica, then Bogdanci and Prespa, between 150 m and 850 m altitude. This species is fruiting in autumn and winter (Calonge 1998). The data presented in this paper are from the fol-lowing months: I, III, IV, VI, VIII, XI and XII.

Tulostoma caespitosum (Fig. 3) grows on sandy soil, fruiting during autumn and winter (Calonge 1998).

Fig. 2. Distribution map of T. fimbriatum.

Fig. 3. Distribution map of T. caespitosum and T. melanocyclum:� – locality of T. caespitosum; � – localities of T. melanocyclum.Fig. 1. Distribution map of T. brumale.

440 Plant, fungal and habitat diversity investigation and conservation • Proceedings of IV BBC – Sofia ' 2006

There is only one published data for this species, by Wright (1987), Rabrovo vill., Strumica, leg. Wilson (Herb. Lloyd n° 15.425, BPI). Research conducted till now has not yet approved this species.

Tulostoma melanocyclum is a typically European species, particularly Southern, which grows on clay-ish soil with sand, amongst herbaceous vegetation (Wright 1987). This is a rather frequent species in West and South Europe (Wright 1987). In the Repub-lic of Macedonia five localities have been recorded: Prilep (Tortić 1988), Ruen Mt, Kumanovo and Pre-spa (Fig. 3); therefore a conclusion on its distribu-tion cannot be made. It is common to encounter it together with T. brumale, from which can be differ-entiated by the nature of the exoperidium, the col-our of endoperidium, the spores and the capillitial septa (Wright 1987). It is found in the following as-sociations: Querco–Carpinetum orientalis macedon-icum and Salicetum, between 400–850 m altitude. The species is fruiting from II to XII, usually IV and X (Wright 1987). The data presented here are from the following months: III, IV, VI and XI. According to Karadelev (2000), this species is incorporated as a rare species in the Preliminary Red List for the Re-public of Macedonia.

Tulostoma squamosum (Fig. 4) grows on calcar-eous soils among herbaceous vegetation, it is an in-frequent although widely distributed species in most of Europe, principally Southern and Western (Wright 1987). There are no published data about this species for the Republic of Macedonia yet. It has been record-ed in eleven localities, mostly in Querco–Carpinetum

orientalis macedonicum, but also in Juniperus excelsa forest and in meadows. Concerning its vertical distri-bution, it is found at 150–1000 m altitude. This species is fruiting all the year, in the Republic of Macedonia it is collected in the following months: I, III–IV and X-XII. This is first record of this species for the Repub-lic of Macedonia.

Acknowledgements. We are indebted to Biology Students' Re-search Society for their financial help in organizing field trips for collection of scientific material and to Stole Stojanov for his effort in material collecting activities.

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Pegler, D.N., Læssøe, T. & Spooner, B.M. 1995. British Puffballs, Earthstars and Stinkhorns. An Account of the British Gasteroid Fungi. Roy. Bot. Gard., Kew.

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Pilát, A. & Lindtner, V. 1939. Ein Beitrag zur Kenntnis der Basidiomyceten von Südserbien II. – Glasn. Skopsk. Naučn. Društva, 20: 1-11.

Rusevska, K. & Karadelev, M. 2004. Eco-taxonomic researches into macromycetes on Vodno Mountain. – Mycol. Monten., 7: 53-63.

Tortić, M. 1988. Materials for the mycoflora of Macedonia. Maced. Acad. Sci. Arts, Skopje.

Wright, J.E. 1987. The genus Tulostoma (Gasteromycetes) – A World Monograph. Geburger Borntraeger Verlagsbuchhandlung, Berlin & Stuttgart.Fig. 4. Distribution map of T. squamosum.