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26 February 2024 Diversity of epiphytic lichens and allied fungi on Pinus heldreichii and P. peuce in Bulgaria
Veselin V. Shivarov
Author Affiliations +
Abstract

The study presents all available information for epiphytic lichens and allied fungi on Pinus heldreichii and P. peuce in Bulgaria. The trees are respectively, subendemic and endemic for the Balkan Peninsula. Comments on distribution and diversity of species are provided. A total of 78 species are reported. Two lichen species are reported for the first time from Bulgaria, Blastenia monticola and Hypogymnia laminisorediata. Lecanora cadubriae is confirmed from Bulgaria. The following species are reported for the first time for the Pirin Mountains: Cladonia glauca, Lepraria elobata, Melanelixia glabratula, Micarea prasina, Nephromopsis chlorophylla, Strangospora moriformis, while Lichenoconium erodens is new for the Vitosha region and L. lecanorae for the Rila Mountains.

Introduction

Pinus peuce Griseb. and P. heldreichii Christ are respectively, Balkan endemic and subendemic coniferous trees, distributed in most Balkan countries, while P. heldreichii is known also from Calabria, south Italy (Panayotov et al. 2016).

In Bulgaria, both species form the upper forest boundaries in the highest Bulgarian mountains. Natural stands of P. heldreichii are known only from the Pirin and Slavianka Mountains on marble, while P. peuce is more widely distributed on different siliceous substrates in the Pirin, Rila, the Balkan range and the Rhodopes floristic regions. The communities of P. heldreichii and P. peuce are included as vulnerable (VU) and endangered (EN) in the Red Data Book of the Republic of Bulgaria (Biserkov et al. 2015). The epiphytic lichen communities on both trees were not studied and included in the Red Data Book of the Republic of Bulgaria. However, many lichenological studies in Bulgaria report lichen species from P. heldreichii and P. peuce, as a result of fieldtrips in the Pirin and Rila Mountains (Suza 1929, Szatala 1930, Zhelezova 1956b, Mayrhofer et al. 2020). In this study we present all available information about lichen diversity on both species. The information is gathered from literature, specimens deposited in SOMF, and fieldwork during the period from 2019 to 2022.

The role of P. heldreichii and P. peuce in forming the highest-elevation forest belts makes them important for studies of the effects of global warming on epiphytic lichens. Within the frame of the project ‘Structural and functional characteristics and perspectives for diverse use of endemic relict coniferous forest communities in Bulgaria in state of climate change′ we studied six sites (Fig. 1) in forests of P. heldreichii and P. peuce, where the total diversity of epiphytic lichens was recorded and permanent plots were established for future analyses of changes in lichen communities and cover due to climate change.

Two species are reported for the first time from Bulgaria, namely Blastenia monticola Arup & Vondrák and Hypogymnia laminisorediata D.Hawksw. & Poelt. Comments on lichen diversity and distribution are presented.

Figure 1.

Map of Bulgaria with six sites where a complete inventory of species was made and permanent plots were established. Red dots indicate sites with Pinus peuce, while blue ones indicate Pinus heldreichii.

img-z2-7_01.jpg

Material and methods

The sampling sites are in the Balkan range, Vitosha region, Pirin and Rila Mountains. Permanent plots were established in six sites, where a total diversity of epiphytic lichens was recorded (Fig. 1). Each site has dimensions of 100 × 100 m with homogeneous forest.

Studied specimens were deposited in the Mycological Collection of the Institute of Biodiversity and Ecosystem Research, Sofia (SOMF). Specimens collected by B. Zhelezova, A. Vězda, J. Motyka, A. Atanassova, H. Mayrhofer and S. Nikolova from P. heldreichii and P. peuce were revised. All information about species distribution is presented, following the floristic regions of Bulgaria and their numeration (Denchev et al. 2022). Localities from old sources are given separately if there was an indication of altitude or other important information for the distribution. Several localities are from the area of the Banderitsa Chalet, and if there is no other information, the Banderitsa Chalet is considered as one locality.

The main sources for identification of lichen specimens were Wirth (1995), Randlane et al. (2009), Smith et al. (2009), Arcadia (2022) and Nimis (2023). Chemical reactions were made following Orange et al. (2010). The taxonomic concept follows Denchev et al. (2022), whereas the new records for Bulgaria follows the protologues (Hawksworth 1973, Vondrák et al. 2020).

List of localities and sampling sites

Balkan range

  • 5-1. Site Petrohan Pass, 43.11428°N, 23.13345°E, 1472 m.

Vitosha region

  • 8-1. Site Goli Vrah, 42.59197°N, 23.29262° E, 1814 m.

Pirin Mountains

  • 14-1. Blagoevgard Province, 41.76333°N, 23.42028°E, 1875 m (Mayrhofer et al. 2020).

  • 14-2. Near Banderitsa Chalet, 29.VII.1954, B. Zhelezova (SOMF).

  • 14-3. Banderitsa Chalet, B. Zhelezova (SOMF) (Motyka and Zhelezova 1962, Zhelezova 1963, Atanassova and Mayrhofer 2012).

  • 14-4. Banderitsa Chalet, 1850 m (Zhelezova 1956b).

  • 14-5. Site Vihren Chalet, 41.76192°N, 23.41695°E, 1969 m.

  • 14-6. Near Demyanitsa Chalet, 1900–2200 m (Zhelezova 1956b).

  • 14-7. The path to Malak Kazan circus, 2100 m, 2.X.1962, B. Zhelezova (SOMF) (Zhelezova 1963).

  • 14-8. Near Banderitsa Chalet, 1900 m (Zhelezova 1963).

  • 14-9. Banderitsa River, 900 m (Zhelezova 1956b).

  • 14-10. Demyanitsa Chalet, B. Zhelezova (SOMF) (Motyka and Zhelezova 1962).

  • 14-11. Along the road from Banderitsa Chalet to Bansko, 41.77632°N, 23.43917°E, 11.VII.2007, H. Mayrhofer & S. Nikolova (SOMF).

  • 14-12. Pirin Chalet, B. Zhelezova (SOMF).

  • 14-13. Banderitsa Chalet, 29.VII.1954, Zhelezova (SOMF).

  • 14-14. The region of Kazan circuses, 2.X.1962, B. Zhelezova (SOMF).

  • 14-15. The region of Banderitsa Chalet, 14.VII.1967, A. Vězda (SOMF).

  • 14-16. The valley of Banderitsa River, 1850 m (SOMF) (Zhelezova 1956b).

  • 14-17. Along the road to Vihren Chalet near Baykusheva Mura, 41.76330°N, 23.42020°E, 10.VII.2007, H. Mayrhofer & S. Nikolova (SOMF).

  • 14-18. Demyanitsa Chalet, 2000–2200 m (Zhelezova 1956b).

  • 14-19. Below Bezbog Chalet (Zhelezova 1960, Pišút 1969, 1986, Shivarov et al. 2023).

  • 14-20. Between Gotse Delchev Chalet and Bezbog Lake, 01.X.1957, B. Zhelezova (SOMF).

  • 14-21. The valley of Banderitsa River, 1700 m (Zhelezova 1956b).

  • 14-22. Demyanitsa Chalet, B. Zhelezova (SOMF).

  • 14-23. Bayuvi Dupki–Dzhindzhiritsa Reserve, B. Zhelezova (SOMF).

  • 14-24. Bezbog Lake, B. Zhelezova (SOMF) (Motyka and Zhelezova 1962).

  • 14-25. Above Gotse Delchev Chalet (Motyka and Zhelezova 1962).

  • 14-26. Vihren Chalet (Motyka and Zhelezova 1962).

  • 14-27. Between Banderitsa Chalet and Vihren Chalet, 41.76333°N, 23.42028°E, 1875 m, 10.VII.2007, H. Mayrhofer & S. Nikolova (Mayrhofer et al. 2020).

  • 14-28. Site Yavorov Chalet, 41.82300°N, 23.37727°E, 1716 m.

  • 14-29. Site Banderitsa Chalet, 41.76805°N, 23.42392°E, 1876 m.

  • 14-30. Yavorov Chalet (SOMF) (Zhelezova 1963).

  • 14-31. The valley of Treta Reka River, above Pirin Chalet, 1750 m (Pišút 2001).

  • 14-32. The trail to Vihren, 41.77278°N, 23.42639°E, 2011 m, 11.VII.2007, H. Mayrhofer & S. Nikolova (Mayrhofer et al. 2020).

  • 14-33. Pirin Mts (Zhelezova 1956b, Motyka and Zhelezova 1962).

  • 14-34. The trail towards Vihren Chalet, 1850 m (Pišút 1969, 1986).

  • 14-35. Above Banderitsa Chalet near Kazanite, 2.X.1962, B. Zhelezova (SOMF).

  • 14-36. Above Banderitsa Chalet towards Kutelo Peak (Pišút 1986, 2001).

  • 14-37. Along the tourist road from Banderitsa Chalet to Kazanite circus; 41.77278°N, 23.42642°E, 1867 m, H. Mayrhofer & S. Nikolova (SOMF).

  • 14-38. Razloshki Suhodol Circus, 2200 m (Zhelezova 1960).

  • 14-39. Near Banderitsa Chalet, 41.76750°N, 23.42333°E, 1883 m, 10.VII.2007, H. Mayrhofer & S. Nikolova (SOMF).

  • 14-40. Below Banski Suhodol circus (Cretzoiu 1937).

Rila Mountains

  • 15-1. The valley of Skakavitsa River, 1800 m (Suza 1929).

  • 15-2. The valley of Levi Iskar River, 1500–1700 m (Szatala 1930).

  • 15-3. The valley of Levi Iskar River, 1500 m (Szatala 1930).

  • 15-4. Site Treshtenik Chalet, 42.082167°N, 23.61803°E, 1915 m.

  • 15-5. Site Malyovitsa River, 42.20897°N, 23.39003°E, 1760 m.

  • 15-6. Near Skakvitsa Chalet (Zhelezova 1963).

  • 15-7. Ribni ezera Chalet, 2200 m (Zhelezova 1956b).

  • 15-8. Above Kirilova polyana towards Tiha Rila, 27.VI.2001, M. Gyosheva (SOMF).

  • 15-9. Above Kirilova polyana towards Ribni ezera Lakes, IX.1961, B. Zhelezova (SOMF).

  • 15-10. Semkovo, 30.VII.1972, B. Zhelezova (SOMF).

  • 15-11. Above Kirilova polyana (Zhelezova 1956b).

  • 15-12. Belmeken Chalet, route for Kostenets, II.1962, B. Zhelezova (SOMF).

  • 15-13. Near Ribni ezera Chalet, 1900 m (Motyka and Zhelezova 1962).

  • 15-14. Suhoto Lake, 20.V.1950, B. Zhelezova (SOMF).

Table 1.

Species diversity and distribution on Pinus heldreichii and Pinus peuce in Bulgaria.

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Continued.

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Results and discussion

A total of 46 lichen species were recorded on P. heldreichii and 51 lichens, two non-lichenized, and two lichenicolous fungi on P. peuce (Table 1). Three species have conservation status in Bulgaria: Anaptychia ciliaris Flot. (NT), Cetraria sepincola (Ehrh.) Ach. (EN), and Letharia vulpina Hue (NT) (Shivarov et al. 2023). During the fieldwork, single thalli were found of A. ciliaris and L. vulpina, whereas C. sepincola was not found. The wolf lichen L. vulpina was known as common on P. peuce in the past (Zhelezova 1956a). Nowadays it is common only in the region of Bezbog Chalet, Pirin Mountains (14-19).

The most common epiphytic lichens are Lecanora pulicaris (Pers.) Ach., Parmeliopsis ambigua (Hoffm.) Nyl., and P. hyperopta (Ach.) Arnold. In some sites the dominant species on trunks can be H. laminisorediata (Fig. 2A–B) and H. physodes Nyl. The base of the observed trunks is usually covered with Lepraria elobata Tønsberg.

Physconia distorta (With.) J.R.Laundon, a species, that is widespread in lowlands in Bulgaria was found near Banderitsa Chalet at 1848 m. The occurrence of species with Mediterranean distribution at high altitudes indicate change in vertical distribution due to climate change. Moreover, the region of Banderitsa Chalet is well studied in the past by many lichenologists and this species has not been reported previously.

Two lichen species are reported for the first time from Bulgaria, B. monticola and H. laminisorediata. The specimens collected near Banderitsa Chalet by B. Zhelezova on P. heldreichii and P. peuce published as Caloplaca ferruginea (Huds.) Th. Fr. (Zhelezova 1956b, 1963) belong to B. monticola. The latter is characterized by the presence of blastidia and isidia, which usually exceed 150 µm diam. in the studied Bulgarian specimens (Fig. 2C), whereas in Blastenia ferruginea (Huds.) A.Massal. vegetative diaspora absent and the species is with different ecology. Blastenia monticola occurs on bark and wood of subalpine/subarctic trees and is known from bark of P. heldreichii in the mountains of the Balkans (Vondrák et al. 2020). Here it is reported also on bark of P. peuce.

Hypogymnia laminisorediata was found at Yavorov Chalet (14-28) as a dominant species covering the trunks of P. heldreichii. The thalli were well developed and exceeded 10 cm in diam., with wide marginal lobes, and with rugose soralia in the central parts (Fig. 2A–B). The observed specimens deposited in SOMF from bark of P. heldreichii and P. peuce as Parmelia bitteriana Zahlbr. well agree with the description of H. laminisorediata in Hawksworth (1973). The species is known from Morocco, Italy, Serbia, Greece and Turkey (Arcadia 2022), and the occurrence in Bulgaria is expected. However, H. laminisorediata differs from Hypogymnia farinacea Zopf only by the wider lobes and thallus size (Hawksworth 1973). Further studies with molecular support are needed to confirm that the species is distinct from H. farinacea, as there are no DNA sequences available from H. laminisorediata.

Lecanora cadubriae (A.Massal.) Hedl. was excluded earlier from lichens occurring in Bulgaria (Denchev et al. 2022). However, a specimen of L. cadubriae collected by A. Vězda (14-15) was found, and the species was also collected during the fieldwork at the site Treshtenik Chalet (15-4).

Figure 2.

Blastenia monticola and Hypogymnia laminisorediata, general habit. A: H. laminisorediata on P. heldreichii in site Yavorov Chalet. B: H. laminisorediata SOMF 24313, locality 14-12, on P. peuce. C: B. monticola SOMF 31122, locality 14-3, on P. heldreichii. Scale bars: A and B = 1 cm, C = 2 mm.

img-z6-1_01.jpg

The following species are reported for the first time for the Pirin Mountains: Cladonia glauca Flörke, L. elobata Tønsberg, Melanelixia glabratula (Lamy) Sandler & Arup, Micarea prasina Fr., Nephromopsis chlorophylla (Willd.) Divakar, A.Crespo & Lumbsch, Strangospora moriformis (Ach.) Stein, while Lichenoconium erodens M.S.Christ. & D.Hawksw. is new for the Vitosha region and Lichenoconium lecanorae (Jaap) D.Hawksw. for the Rila Mountains.

Although the lichen diversity is well-studied, especially in the Pirin and Rila Mountains, we can expect a considerably higher number of species to be found in remote and conserved forest. Studies with focus on P. heldreichii stands in Mt Slavyanka will reveal further species as this mountain is well conserved and not affected by the intensive tourism. High biodiversity can be expected on logs and snags of P. heldreichii and P. peuce, and more studies will be needed in such habitats.

Conclusion

The study presents all available data for epiphytic lichens and allied fungi on P. heldreichii and P. peuce in Bulgaria. Information on all 78 currently known epiphytic species of both trees is included. Blastenia monticola and H. laminisorediata are reported for the first time for the Bulgarian lichenized mycota. To our knowledge this is the first work with a focus on epiphytic species on P. heldreichii and P. peuce. The data for diversity and distribution will be useful in future analyses of changes in lichen communities in response to climate changes.

Acknowledgements

This study was supported by the Bulgarian National Science Fund (Grant no. KP-06-N36/13/17.12.2019).

© 2024 The Authors. This is an Open Access article

Data availability statement

There are no additional data for this paper

References

1.

Arcadia, L. 2022. Lichen flora of Greece, including lichenicolous fungi, ver. 10. –  http://www.lichensofgreece.com/flora.pdfGoogle Scholar

2.

Atanassova, A. and Mayrhofer, H. 2012. Physciaceae. Part 1. Foliose genera. – In: Denchev, C. M., (ed.), Fungi of Bulgaria, vol. 9. Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences. Google Scholar

3.

Biserkov, V. et al. (eds) 2015. Red data book of the Republic of Bulgaria, volume 3: natural habitats. – BAS & MoEW. Google Scholar

4.

Cretzoiu, P. 1937. Zur Flechtenflora von Bulgarien. – Rev. Bryol. Lichenol. 9: 176–193. Google Scholar

5.

Denchev, C. M., Shivarov, V. V., Denchev, T. T. and Mayrhofer, H. 2022. Checklist of the lichenized and lichenicolous fungi in Bulgaria. – Mycobiota 12: 1–116.. Google Scholar

6.

Hawksworth, D. L. 1973. Two new species of Hypogymnia (nyl.) nyl. – Lichenologist 5: 452–456. Google Scholar

7.

Mayrhofer, H., Atanassova, A., Nikolova, S. O. and Denchev, C. M. 2020. Additions to the lichenized and lichenicolous fungi in Bulgaria. – Mycobiota 10: 39–62. Google Scholar

8.

Motyka, J. and Zhelezova, B. 1962. A monographic study of Usnea in Bulgaria, vol. 10. – Izvestiya na Botanicheskiya Institut, pp. 67–120, inBulgarian. Google Scholar

9.

Nimis, P. L. 2023. ITALIC – the information system on Italian lichens, ver. 7.0. – Dept of Biology, Univ. of Trieste. Google Scholar

10.

Orange, A., James, P. W. and White, F. J. 2010. Microchemical methods for identification of lichens, 2nd edn. – British Lichen Society. Google Scholar

11.

Panayotov, M., Tsvetanov, N., Gogushev, G., Tsavkov, E., Zlatanov, T., Anev, S., Ivanova, A., Nedelin, T., Zafirov, N., Aleksandrov, N., Dountchev, A., Vasileva, P., Shishkova, V., Stoyanov, B., Sotirova, N., Vatov, A., Bebi, P. and Yurukov, S. 2016. Mountain coniferous forests in Bulgaria – structure and natural dynamics. – Univ. of Forestry. Google Scholar

12.

Pišút, I. 1969. Beitrag zur Kenntnis der Flechten Bulgariens. II. – Acta Rerum Nat. Musei Natl Slov. 15: 27–37. Google Scholar

13.

Pišút, I. 1986. Lichenologische Bemerkungen 4. – Annot. Zool. Bot. 172: 1–6. Google Scholar

14.

Pišút, I. 2001. Beitrag zur Kenntnis der Flechten Bulgariens. III. – Acta Rerum Nat. Musei Natl Slov. 47: 21–26. Google Scholar

15.

Randlane, T., Törra, T., Saag, A. and Saag, L. 2009. Key to European Usnea species. – Bibliotheck 100: 419–462. Google Scholar

16.

Shivarov, V. V., Denchev, C. M. and Denchev, T. T. 2023. Red List of lichenized fungi in Bulgaria. – Mycobiota 13: 1–30. Google Scholar

17.

Smith, C. W., Aptroot, A., Coppins, B. J., Fletcher, A., Gilbert, O. L., James, P. W. and Wolseley, P. A. (eds). 2009. The lichens of Great Britain and Ireland, 2nd edn. – The British Lichen Society. Google Scholar

18.

Suza, J. 1929. Lichenes Bulgariae, I. – Acta Bot. Bohem. 8: 7–25. Google Scholar

19.

Szatala, Ö. 1930. Beiträge zur Flechtenflora von Bulgarien II. – Magy. Bot. Lapok 29: 58–104. Google Scholar

20.

Vondrák, J., Frolov, I., Košnar, J., Arup, U., Veselská, T., Halıcı, G., Malíček, J. and Søchting, U. 2020. Substrate switches, phenotypic innovations and allopatricspeciation formed taxonomic diversity within the lichen genus Blastenia . – J. Syst. Evol. 58: 295–330. Google Scholar

21.

Wirth, V. 1995. Die Flechten baden-Württemmbergs. Teil 1 & 2. – E. Ulmer GMBH Co. Google Scholar

22.

Zhelezova, B. 1956a. The wolf lichen – Letharia vulpina (L.) Vain. – Priroda 5: 66–68, inBulgarian. Google Scholar

23.

Zhelezova, B. 1956b. Contribution to the lichen flora of Bulgaria, vol. 5. – Izvestiya na Botanicheskiya Institut, pp. 387–403, inBulgarian. Google Scholar

24.

Zhelezova, B. 1960. Contribution to the lichen flora of Bulgaria, vol. 7. – Izvestiya na Botanicheskiya Institut, pp. 351–357, inBulgarian. Google Scholar

25.

Zhelezova, B. 1963. Materials on the lichen flora of Bulgaria, vol. 12. – Izvestiya na Botanicheskiya Institut, pp. 245–265, inBulgarian. Google Scholar
Veselin V. Shivarov "Diversity of epiphytic lichens and allied fungi on Pinus heldreichii and P. peuce in Bulgaria," Lindbergia 2024(1), (26 February 2024). https://doi.org/10.25227/linbg.025278
Accepted: 12 December 2023; Published: 26 February 2024
KEYWORDS
Balkan endemic
Bulgarian lichen mycota
climate change
coniferous forests
new records
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