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Habitat preferences of Hericium erinaceus in Slovakia
Fungal Ecology 27 (2017) 189e192
Contents lists available at ScienceDirect
Fungal Ecology journal homepage: www.elsevier.com/locate/funeco
Habitat preferences of Hericium erinaceus in Slovakia Vladimír Kunca*, Marek Ciliak Technical University in Zvolen, Faculty of Ecology and Environmental Sciences, Department of Applied Ecology, T.G. Masaryka 24, SK-960 53 Zvolen, Slovakia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 May 2016 Received in revised form 9 December 2016 Accepted 19 December 2016 Available online 7 January 2017
Distribution patterns, ecology and habitats of Hericium erinaceus in Slovakia are presented, together with an indication of its population size and dynamics as driven by the type of substratum the fungus feeds on. Basidiomata have been recorded both on living and dead trees, predominantly on oaks (Quercus spp.) but also on European beech (Fagus sylvatica), and at altitudes ranging from 103 to 753 m, which in Slovakia corresponds to warm hilly and upland beech-oak forests. Standing trunks were a more common substratum than fallen trunks. Although the fungus tends to occur in old-growth forests, nearly half of the observations were from managed forests. Given the observed distribution, we conclude that H. erinaceus is not a strict indicator of intact old-growth forests in Slovakia. © 2016 Elsevier Ltd and British Mycological Society. All rights reserved.
Corresponding Editor: Jacob HeilmannClausen Keywords: Old-growth forests Cultural forests Indicator species Quercus spp. Fagus sylvatica
1. Introduction Although rare in Europe and red-listed in numerous European countries (Boddy et al., 2011), Hericium erinaceus is an easily recognisable fungus (Fig. 1). A good deal of information is available ł et al., 2015) and about about its cultivation (Ko et al., 2005; Soko its distribution and ecology in Europe (Fraiture and Otto, 2015). Recently, the use of this fungus became very popular throughout the northern hemisphere due to its medicinal properties (Thongbai et al., 2015). Its distribution covers the whole of Europe, with the highest frequency of finds in Quercus spp. woodlands n, 2010), however the basidiomata may (Bernicchia and Gorjo occur on living, weakened trees and dead trunks of many broadleaved tree species. The fungus is included in the list of 21 fungal indicator species of conservation value of European beech forests (Christensen et al., 2004) and is also listed as a species of special interest (class B) (Odor et al., 2006), which denotes widespread species regarded as rare in Europe and threatened in several individual countries. Landres et al. (1988) defined an indicator species as “an organism whose characteristics (e.g. presence or absence, population density, dispersion, reproductive success) are used as an index of
* Corresponding author. E-mail address: [email protected] (V. Kunca). http://dx.doi.org/10.1016/j.funeco.2016.12.002 1754-5048/© 2016 Elsevier Ltd and British Mycological Society. All rights reserved.
attributes too difficult, inconvenient, or expensive to measure for other species or environmental conditions of interest.” Fungi can be used as indicator species (Kranabetter et al., 2009; Halme et al., 2017), in particular the forest-dwelling ones (Blasi et al., 2010), highlighting various aspects of forest ecology such as biodiversity (Parmasto, 2001) or forest continuity or nature conservation value (Christensen et al., 2004). Even though an indicator species cannot act as a surrogate for total biodiversity, all environmental conditions or habitat qualities, macrofungi have the potential to indicate conservation value and to act as easy tools to communicate complex biodiversity issues to the broader public (Halme et al., 2017). The objective of this paper was to review ecological conditions and habitat preferences of H. erinaceus in Slovakia, with special emphasis on forest conservation status and history of stand management. This contribution also evaluated the value of the species as an indicator for the classification of old-growth forests in Slovakia.
2. Materials and methods We compiled a database of records of collections of H. erinaceus in Slovakia by processing data from herbaria (public herbaria BRA, SLO, PRM, PRC e abbreviations of public herbaria adhere to Index Herbariorum (Thiers, continuously updated)), published records (Kuthan et al., 1999; Skubla, 2003), personal records (private
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4. Discussion
Fig. 1. Basidiomata of Hericium erinaceus (Javorie Mts., Slovakia) (Photo: Vladimír Kunca, 15 October, 2013).
herbarium of Vladimír Kunca (PVKU)) and communication with active amateur field mycologists (www.nahuby.sk). Records originate from the whole territory of Slovakia and include habitats considered suitable for the species. Most of the records were collected by about 20 individual collectors and originate from a range of forest types surveyed throughout the year. Altitude, tree species, living/dead, standing/lying tree and intensity of management of forest stands were evaluated in this study. All surveys were based on basidiomata occurrence and some result from targeted searches. Single-parameter data containing only one-dimensional entry (e.g. date or tree species) were also included in our database. Duplicate records referring to the same tree, stem or stump were evaluated as one database entry. Classification of forest stands in terms of management and naturalness followed Holec et al. (2015). The categorisation of forest stands according to forest management plans (commercial, protection and special purpose forests) was considered the most important parameter, followed by in-situ assessment of tree species composition, age, horizontal and vertical structure, dead wood presence and occurrence of veteran trees. We also considered the observer identity and the inclusion of the forest in the list of old-growth forests and their remnants in Slovakia (www. pralesy.sk/lokality/). Actual tree species composition was compared to that expected on the basis of forest site classification (based on soil, climate, water regime and landscape conditions) (Voloscuk, 2001). 3. Results In total, 86 records of H. erinaceus were included in this study, of which basidioma voucher specimens exist or were confirmed in 45 records. Data prior to 2000 comprise 23% of the total records, 51 records had accompanying altitude data, 76 had host tree identification (tree genus or species), 70 had vital status and standing or fallen stem indication. We were able to assign forest stand naturalness to 38 of the 86 records. Altitude of records ranged from 103 to 753 m, with the average value of 423 m a.s.l. (Fig. 2A). Fruiting basidiomata were recorded predominantly on oaks (68.4%), the next most common species was beech (25%, Fig. 2B). The species was recorded with equal frequency on dead and living trees (Fig. 2C), but was less frequent on fallen (31.4%) compared to standing trunks (60%). A majority (83%) of standing trunks were living. We found similar numbers of records of Hericium erinaceus in relatively undisturbed old-growth and intensively managed forests (Fig. 2D).
There are numerous records of H. erinaceus in Slovakia dating from the last two decades. The species occurs in varying types and categories of forests and biotopes. It was found in similar numbers in old-growth and cultural forests, and is present almost over the whole of the territory of Slovakia, from the lowlands to submontane forests. No records from forest plantations were found, however, noticeable presence of H. erinaceus in managed forests were recorded. Tree species composition in the latter category of forests largely corresponds to natural species distribution predicted for the region (Vladovi c et al., 2014) but is under permanent influence of silvicultural interventions. We recorded two occurrences in biotopes other than forest e in steppe on black locust trunk (Robinia pseudoacacia) and in an urban area on ancient specimen of beech (Fagus sylvatica) in the warmest region of Slovakia. The black locust is an introduced species in Slovakia and was planted in the area, so the species is evidently able to colonize secondary woodlands in Slovakia. Old-growth forests and their remnants (defined as min. 5 ha in area) cover 0.49% of the forest area in Slovakia (www.pralesy.sk/ lokality/). It is clear that not all locations that are potentially suitable for H. erinaceus were surveyed, some old-growth forests have no mycological description at all. The lack of data is mainly related to the strict legal protection, restricting public access to wooded areas with the highest conservation value in Slovakia. There are four old-growth forests with dominance of oaks in Slovakia, which were surveyed for this study, but the majority of old-growth forests are dominated by beech e with minor contribution from other species. It is reasonable to expect that in future we will see more confirmed finds of H. erinaceus originating from both old-growth forests and other stands, giving us an opportunity to better describe and understand its ecology and value as an indicator species. The species was found in similar numbers on living and dead trees (fallen logs) but less frequently on cut stumps, in a pattern similar to that observed in the Czech Republic (Holec and Beran, 2006). In the UK the fungus is typically found fruiting high up on wounds, or broken branch stubs of living trunks, but finds on fractured or fallen large diameter (>10 cm) pieces of wood have also been reported (Boddy et al., 2011). Although basidiomata are frequently found on living trees, a more detailed survey indicates that they tend to appear within deceased parts of living trees. The same was also observed by Boddy et al. (2011) as basidiomata on living trees occur predominantly in knotholes, fissures or wounds, often on old or senescing trees. This may suggest that H. erinaceus acts as a necrotrophic parasite (Fraiture and Otto, 2015) but perhaps more likely is that it rots dead central tissues, and wounds etc. provide an exit route for fruiting. Based on our observations, the species is predominantly found in the following two types of habitat. Firstly, sun-exposed veteran trees with wounds, especially on ridges and crests, with wounds caused by frost, lightning or branch drops. Secondly, on medium sized stems (from 30 to 50 cm in diameter) lying in wet microhabitats in more closed conditions in old-growth forests. Occasionally, basidiomata on solitary trees in very dry conditions were observed on trunks with no visible wounds. In Europe, the primary natural habitat of this species can be best described as temperate lowland forests. According to available data, no collection in Slovakia was recorded in floodplain lowland forests. Interestingly, there is no record of H. erinaceus (Sikora and Neubauer, 2015) from one of the best known lowland forest in Europe e Bialowieza Forest. The reasons for this absence could be the cool continental macroclimate prevalent in the region and the marked dominance of Quercus robur amongst the oaks in the
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Fig. 2. Altitudinal range (A, mean, ±SD and min/max boxplot), tree host species distribution (B), vital status and position of a host stem (C) and number of records with respect to the state of forest stand (D) of Hericium erinaceus in Slovakia. Numbers above the bars represent number of records.
Bialowieza forest. Although many of our collections of H. erinaceus are on Quercus sp., there were no confirmed collections on Q. robur, which in Slovakia is more typical in floodplain forests where there was a very low frequency of H. erinaceus finds. However, Fraiture and Otto (2015) reported Quercus robur as a substratum for successful growth of H. erinaceus and acidophilus Q. robur woods on sandy plains as a suitable habitat. Fraiture and Otto (2015) assigned the European distribution of the fungus primarily to the lowlands, with only rare occurrence in mountainous regions up to 1500 m. In this study, half of the basidiomata incidence ranged between 327 and 560 m in altitude (1st and 3rd quartile). In Slovakia, this altitudinal range corresponds to a range of warm hilly country and upland beech-oak forests. The geological and soil conditions do not appear to play any role in determining the occurrence of the fungus. It seems that the species has a rather broad habitat preference close to optimum altitude-driven climatic conditions as long as it can find suitable host tree. Collections from species other than oak and beech are rare. The fungus is most frequently found on beech in Poland (Pia˛ tek, 2005) and in the UK (Boddy et al., 2011), on beech and oaks in the Czech Republic (Holec and Beran, 2006) and Austria (Austrian Mycological Society, 2015), and almost exclusively on oaks in Hungary (Siller et al., 2005). However, with the exception of the Czech Republic, where it is found in more than 50 known localities (Holec and Beran, 2006), the fungus is apparently rare or very rare in all countries neighbouring Slovakia. The extent of forest coverage might explain the rarity of the fungus in Poland and Hungary (28.8% and 20.3%), when compared to Slovakia (40.8%) and the Czech Republic (34%, CBD, 2016). In addition, the higher number and area of old-growth and natural forests might favour the species in Slovakia and the Czech Republic (García Feced et al., 2015). Relatively low number of observations in Austria may perhaps be
explained by the more dominant mountainous character of the landscape, generally not suitable for the fungus. In Germany there are 188 records of H. erinaceus (German Mycological Society, 2016). Considering the facts that the area of Germany is more than seven times larger than that of Slovakia, and with incomparably higher effort of mycologists, this suggests a much lower population density in this country. Overall, our data and survey of relevant literature sources indicate that H. erinaceus has a preference for rather dry, sunexposed parts of lowland forests in warm macroclimate regions in Europe. However, most of these lowland forests have been replaced by arable land and remaining forests stands are often designated as intensively managed forests and forest parks, with a conspicuous absence of veteran trees or large decaying stems (Kaplan et al., 2009), which is probably the main reason for the rarity of the species in most European countries. Limited spore dispersal as well as low spore germination rate of the fungus could contribute further to the rarity of the species (Crockatt et al., 2007). Long distance spore dispersal may be of greater importance for rare fungi whose populations are affected by habitat fragmentation, but it is unknown to what degree long-range spore dispersal is possible in this species. Within a European context, Slovakia is relatively densely covered by old-growth forests and their remnants with a high number of veteran trees and dead-wood volume (Parviainen, 2005). Fairly rugged parts of the country covered by forests also contain a long-established network of protective forests with almost natural tree species composition all over the country. These factors may contribute to the observed high incidence of H. erinaceus in Slovakia. It is important to point out that any fungal species may remain dormant while environmental conditions are unsuitable (Crockatt et al., 2007). Recent advances in research on mycelia in dead
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wood will reveal whether the fungus is indeed as rare as its basidiomata. Given the observed distribution of the records in Slovakia, we contend that H. erinaceus prefers forests with natural tree species composition dominated by oaks and beech, but it is not a strict indicator of old-growth forests in Slovakia. As a measure aimed at increasing the area of suitable habitat in managed forests, we recommend retaining low-value and misshapen trees during harvest to let them senesce naturally. Acknowledgments The research was financially supported by the Scientific Grant Agency of the Ministry of Education, Science, Research and Sport of the Slovak Republic and of the Slovak Academy of Sciences (VEGA 1/ 0362/13) and by the Cultural and Educational Grant Agency of the Ministry of Education, Science, Research and Sport of the Slovak Republic (KEGA 007TU Z-4/2015). We are grateful to Kvetoslava , Stefan , Mgr. Ja n Hrasko, Frantisek Bal a zova Bala z, Ludmila Cillíkov a s, Pavol Kesela k, Jaroslav Hubina, Stanislav Jankech, Vladimír Juha Kuriplach, Lubica Kuriplachov a, Vladimír Macík, Ing. Ivan Nagy, Mikul as Lazor, Anton P anis, Jozef Pavlík, Ing. Maros Peiger, Dusan Sol ar, Matús Skutka and Patrik Stibraný for providing information on finds of H. erinaceus, two anonymous reviewers for detailed comments on the manuscript and Dr. Martin Luka c for the language correction. References €mon, W., Hausknecht, A., KrisaiAustrian Mycological Society, 2015. In: Da Greilhuber, I. (Eds.), Database of Fungi in Austria. http://www.austria.mykodata. net (Accessed 15 September 2016). n, S.P., 2010. Corticiaceae s.l. Edizioni Candusso, Alassio. Bernicchia, A., Gorjo Blasi, C., Marchetti, M., Chiavetta, U., Aleffi, M., Audisio, P., Azzella, M.M., Brunialti, G., Capotorti, G., Del Vico, E., Lattanzi, E., Persiani, A.M., Ravera, S., Tilia, A., Burrascano, S., 2010. Multi-taxon and forest structure sampling for identification of indicators and monitoring of old-growth forest. Plant Biosyst. 144, 160e170. Boddy, L., Crockatt, M.E., Ainsworth, A.M., 2011. Ecology of Hericium cirrhatum, H. coralloides and H. erinaceus in the UK. Fungal Ecol. 4 (2), 163e173. CBD, 2016. Convention on Biological Diversity. https://www.cbd.int/ (Accessed 14 September 2016). Christensen, M., Heilmann-Clausen, J., Walleyn, R., Adam cík, S., 2004. Woodinhabiting fungi as indicators of nature value in European beech forests. In: Marchetti, M. (Ed.), Monitoring and Indicators of Forest Biodiversity in Europe e from Ideas to Operationality. European Forestry Institute Proceedings 51, Saarijarvi, pp. 229e237. Crockatt, M.E., Ainsworth, A.M., Parfitt, D., Rogers, H.J., Boddy, L., 2007. Why are the tooth fungi Hericium cirrhatum, H. coralloides and H. erinaceus rare? In: Anonymous (Ed.), World Conference on the Conservation and Sustainable Use of Wild Fungi. Junta de Andalucia, Cordoba, Spain, pp. 116e118. Fraiture, A., Otto, P. (Eds.), 2015. Distribution, Ecology and Status of 51 Macromycetes in Europe. Results of the ECCF Mapping Programme (Scripta Botanica Belgica, Meise). García Feced, C., Berglund, H., Strnad, M., 2015. Scoping Document: Information Related to European Old Growth Forests. ETC/BD Report to the EEA. ETC/BD,
Paris. German Mycological Society, 2016. Hericium erinaceus (Bull.: Fr.) Pers. http://www. pilze-deutschland.de/organismen/hericium-erinaceus-bull-fr-pers (Accessed 19 September 2016). Halme, P., Holec, J., Heilmann-Clausen, J., 2017. The history and future of fungi as biodiversity surrogates in forests. Fungal Ecol. (this issue). Holec, J., Beran, M. (Eds.), 2006. Cervený seznam hub (makromycet u) Cesk e republiky [Red list of fungi (macromycetes) of the Czech Republic] (Príroda, Praha. [in Czech]). Holec, J., Krí z, M., Beran, M., Kolarík, M., 2015. Chromosera cyanophylla (Basidiomycota, Agaricales) e a rare fungus of Central European old-growth forests and its habitat preferences in Europe. Nova Hedwig. 100, 189e204. Kaplan, J.O., Krumhardt, K.M., Zimmermann, N., 2009. The prehistoric and preindustrial deforestation of Europe. Quat. Sci. Rev. 28, 3016e3034. Ko, H.G., Park, H.G., Park, S.H., Choi, C.W., Kim, S.H., Park, W.M., 2005. Comparative study of mycelial growth and basidiomata formation in seven different species of the edible mushroom genus Hericium. Bioresour. Technol. 96, 1439e1444. Kranabetter, J.M., Friesen, J., Gamiet, S., Kroeger, P., 2009. Epigeous fruiting bodies of ectomycorrhizal fungi as indicators of soil fertility and associated nitrogen status of boreal forests. Mycorrhiza 19, 535e548. ho parku Poloniny Kuthan, J., Adam cík, S., Antonín, V., Terray, J., 1999. Huby N arodne va n [Fungi of the Poloniny National Park]. Spra arodných parkov SR, Liptovský s (in Slovak). Mikula Landres, P.B., Verner, J., Thomas, J.W., 1988. Ecological use of vertebrate indicator species: a critique. Conserv. Biol. 2, 316e328. Odor, P., Heilmann-Clausen, J., Christensen, M., Aude, E., van Dort, K.W., Piltaver, A., Siller, I., Veerkamp, M.T., Walleyn, R., Standovar, T., van Hees, A.F.M., Kosec, J., Matocec, N., Kraigher, H., Grebenc, T., 2006. Diversity of dead wood inhabiting fungi and bryophytes in semi-natural beech forests in Europe. Biol. Conserv. 131, 58e71. Parmasto, E., 2001. Fungi as indicators of primeval and old-growth forests deserving protection. In: Moore, D., Nauta, M.M., Evans, S.E., Rotheroe, M. (Eds.), Fungal Conservation, Issues and Solutions. Cambridge University Press, Cambridge, pp. 81e88. Parviainen, J., 2005. Virgin and natural forests in the temperate zone of Europe. For. Snow Landsc. Res. 79 (1/2), 9e18. Pia˛ tek, M., 2005. Hericium erinaceum (Bull.) Pers. In: Wojewoda, W. (Ed.), Atlas of the Geographical Distribution of Fungi in Poland 3. W. Szafer Institute of Botany w, pp. 43e46. of the Polish Academy of Sciences, Krako wki jezowatej _ Sikora, A., Neubauer, G., 2015. Nowe stanowiska i wyste˛ powanie soplo Hericium erinaceus w Polsce (New sites and occurrence of the Bearded Tooth my Przyrode˛ Ojczysta˛ 71, 368e379 (in Hericium erinaceus in Poland). Chron Polish). m, F., Bratek, Z., Zagyva, I., Fodor, L., 2005. Hungarian Siller, I., Vasas, G., P al-Fa distribution of the legally protected macrofungi species. Stud. Bot. Hung. 36, 131e163. la. Skubla, P., 2003. Mycoflora Slovaca. Mycelium, Sa ł, S., Golak-Siwulska, I., Sobieralski, K., Siwulski, M., Go rka, K., 2015. Biology, Soko cultivation, and medicinal functions of the mushroom Hericium erinaceum. Acta Mycol. 50 (2), 1069. Thiers B. [continuously updated]. Index Herbariorum: a Global Directory of public Herbaria and Associated Staff. e http://sweetgum.nybg.org/ih/(Accessed 9 September 2016). Thongbai, B., Rapior, S., Hyde, K.D., Wittstein, K., Stadler, M., 2015. Hericium erinaceus, an amazing medicinal mushroom. Mycol. Prog. 14, 91. lis, F., Kri zy, K., Voda lov ^ bis, I., Vladovi c, J., Mergani c, J., Ma zov a, E., Ujha a, A., Po Bosela, M., Pavlenda, P., 2014. Reakcia diverzity na zmenu edaficko-klimatických podmienok Slovenska (The Response of Forest vegetation Diversity to Changes in edaphic-climatic Conditions in Slovakia). Technick a univerzita vo Zvolene, Zvolen (in Slovak). a prakticke proble my ekologickej stability lesných Volos cuk, I., 2001. Teoreticke mov (Theoretical and practical problems of the ecological Stability of ekosyste Forest ecosystems). Technical University in Zvolen, Zvolen (in Slovak).
Contents lists available at ScienceDirect
Fungal Ecology journal homepage: www.elsevier.com/locate/funeco
Habitat preferences of Hericium erinaceus in Slovakia Vladimír Kunca*, Marek Ciliak Technical University in Zvolen, Faculty of Ecology and Environmental Sciences, Department of Applied Ecology, T.G. Masaryka 24, SK-960 53 Zvolen, Slovakia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 3 May 2016 Received in revised form 9 December 2016 Accepted 19 December 2016 Available online 7 January 2017
Distribution patterns, ecology and habitats of Hericium erinaceus in Slovakia are presented, together with an indication of its population size and dynamics as driven by the type of substratum the fungus feeds on. Basidiomata have been recorded both on living and dead trees, predominantly on oaks (Quercus spp.) but also on European beech (Fagus sylvatica), and at altitudes ranging from 103 to 753 m, which in Slovakia corresponds to warm hilly and upland beech-oak forests. Standing trunks were a more common substratum than fallen trunks. Although the fungus tends to occur in old-growth forests, nearly half of the observations were from managed forests. Given the observed distribution, we conclude that H. erinaceus is not a strict indicator of intact old-growth forests in Slovakia. © 2016 Elsevier Ltd and British Mycological Society. All rights reserved.
Corresponding Editor: Jacob HeilmannClausen Keywords: Old-growth forests Cultural forests Indicator species Quercus spp. Fagus sylvatica
1. Introduction Although rare in Europe and red-listed in numerous European countries (Boddy et al., 2011), Hericium erinaceus is an easily recognisable fungus (Fig. 1). A good deal of information is available ł et al., 2015) and about about its cultivation (Ko et al., 2005; Soko its distribution and ecology in Europe (Fraiture and Otto, 2015). Recently, the use of this fungus became very popular throughout the northern hemisphere due to its medicinal properties (Thongbai et al., 2015). Its distribution covers the whole of Europe, with the highest frequency of finds in Quercus spp. woodlands n, 2010), however the basidiomata may (Bernicchia and Gorjo occur on living, weakened trees and dead trunks of many broadleaved tree species. The fungus is included in the list of 21 fungal indicator species of conservation value of European beech forests (Christensen et al., 2004) and is also listed as a species of special interest (class B) (Odor et al., 2006), which denotes widespread species regarded as rare in Europe and threatened in several individual countries. Landres et al. (1988) defined an indicator species as “an organism whose characteristics (e.g. presence or absence, population density, dispersion, reproductive success) are used as an index of
* Corresponding author. E-mail address: [email protected] (V. Kunca). http://dx.doi.org/10.1016/j.funeco.2016.12.002 1754-5048/© 2016 Elsevier Ltd and British Mycological Society. All rights reserved.
attributes too difficult, inconvenient, or expensive to measure for other species or environmental conditions of interest.” Fungi can be used as indicator species (Kranabetter et al., 2009; Halme et al., 2017), in particular the forest-dwelling ones (Blasi et al., 2010), highlighting various aspects of forest ecology such as biodiversity (Parmasto, 2001) or forest continuity or nature conservation value (Christensen et al., 2004). Even though an indicator species cannot act as a surrogate for total biodiversity, all environmental conditions or habitat qualities, macrofungi have the potential to indicate conservation value and to act as easy tools to communicate complex biodiversity issues to the broader public (Halme et al., 2017). The objective of this paper was to review ecological conditions and habitat preferences of H. erinaceus in Slovakia, with special emphasis on forest conservation status and history of stand management. This contribution also evaluated the value of the species as an indicator for the classification of old-growth forests in Slovakia.
2. Materials and methods We compiled a database of records of collections of H. erinaceus in Slovakia by processing data from herbaria (public herbaria BRA, SLO, PRM, PRC e abbreviations of public herbaria adhere to Index Herbariorum (Thiers, continuously updated)), published records (Kuthan et al., 1999; Skubla, 2003), personal records (private
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4. Discussion
Fig. 1. Basidiomata of Hericium erinaceus (Javorie Mts., Slovakia) (Photo: Vladimír Kunca, 15 October, 2013).
herbarium of Vladimír Kunca (PVKU)) and communication with active amateur field mycologists (www.nahuby.sk). Records originate from the whole territory of Slovakia and include habitats considered suitable for the species. Most of the records were collected by about 20 individual collectors and originate from a range of forest types surveyed throughout the year. Altitude, tree species, living/dead, standing/lying tree and intensity of management of forest stands were evaluated in this study. All surveys were based on basidiomata occurrence and some result from targeted searches. Single-parameter data containing only one-dimensional entry (e.g. date or tree species) were also included in our database. Duplicate records referring to the same tree, stem or stump were evaluated as one database entry. Classification of forest stands in terms of management and naturalness followed Holec et al. (2015). The categorisation of forest stands according to forest management plans (commercial, protection and special purpose forests) was considered the most important parameter, followed by in-situ assessment of tree species composition, age, horizontal and vertical structure, dead wood presence and occurrence of veteran trees. We also considered the observer identity and the inclusion of the forest in the list of old-growth forests and their remnants in Slovakia (www. pralesy.sk/lokality/). Actual tree species composition was compared to that expected on the basis of forest site classification (based on soil, climate, water regime and landscape conditions) (Voloscuk, 2001). 3. Results In total, 86 records of H. erinaceus were included in this study, of which basidioma voucher specimens exist or were confirmed in 45 records. Data prior to 2000 comprise 23% of the total records, 51 records had accompanying altitude data, 76 had host tree identification (tree genus or species), 70 had vital status and standing or fallen stem indication. We were able to assign forest stand naturalness to 38 of the 86 records. Altitude of records ranged from 103 to 753 m, with the average value of 423 m a.s.l. (Fig. 2A). Fruiting basidiomata were recorded predominantly on oaks (68.4%), the next most common species was beech (25%, Fig. 2B). The species was recorded with equal frequency on dead and living trees (Fig. 2C), but was less frequent on fallen (31.4%) compared to standing trunks (60%). A majority (83%) of standing trunks were living. We found similar numbers of records of Hericium erinaceus in relatively undisturbed old-growth and intensively managed forests (Fig. 2D).
There are numerous records of H. erinaceus in Slovakia dating from the last two decades. The species occurs in varying types and categories of forests and biotopes. It was found in similar numbers in old-growth and cultural forests, and is present almost over the whole of the territory of Slovakia, from the lowlands to submontane forests. No records from forest plantations were found, however, noticeable presence of H. erinaceus in managed forests were recorded. Tree species composition in the latter category of forests largely corresponds to natural species distribution predicted for the region (Vladovi c et al., 2014) but is under permanent influence of silvicultural interventions. We recorded two occurrences in biotopes other than forest e in steppe on black locust trunk (Robinia pseudoacacia) and in an urban area on ancient specimen of beech (Fagus sylvatica) in the warmest region of Slovakia. The black locust is an introduced species in Slovakia and was planted in the area, so the species is evidently able to colonize secondary woodlands in Slovakia. Old-growth forests and their remnants (defined as min. 5 ha in area) cover 0.49% of the forest area in Slovakia (www.pralesy.sk/ lokality/). It is clear that not all locations that are potentially suitable for H. erinaceus were surveyed, some old-growth forests have no mycological description at all. The lack of data is mainly related to the strict legal protection, restricting public access to wooded areas with the highest conservation value in Slovakia. There are four old-growth forests with dominance of oaks in Slovakia, which were surveyed for this study, but the majority of old-growth forests are dominated by beech e with minor contribution from other species. It is reasonable to expect that in future we will see more confirmed finds of H. erinaceus originating from both old-growth forests and other stands, giving us an opportunity to better describe and understand its ecology and value as an indicator species. The species was found in similar numbers on living and dead trees (fallen logs) but less frequently on cut stumps, in a pattern similar to that observed in the Czech Republic (Holec and Beran, 2006). In the UK the fungus is typically found fruiting high up on wounds, or broken branch stubs of living trunks, but finds on fractured or fallen large diameter (>10 cm) pieces of wood have also been reported (Boddy et al., 2011). Although basidiomata are frequently found on living trees, a more detailed survey indicates that they tend to appear within deceased parts of living trees. The same was also observed by Boddy et al. (2011) as basidiomata on living trees occur predominantly in knotholes, fissures or wounds, often on old or senescing trees. This may suggest that H. erinaceus acts as a necrotrophic parasite (Fraiture and Otto, 2015) but perhaps more likely is that it rots dead central tissues, and wounds etc. provide an exit route for fruiting. Based on our observations, the species is predominantly found in the following two types of habitat. Firstly, sun-exposed veteran trees with wounds, especially on ridges and crests, with wounds caused by frost, lightning or branch drops. Secondly, on medium sized stems (from 30 to 50 cm in diameter) lying in wet microhabitats in more closed conditions in old-growth forests. Occasionally, basidiomata on solitary trees in very dry conditions were observed on trunks with no visible wounds. In Europe, the primary natural habitat of this species can be best described as temperate lowland forests. According to available data, no collection in Slovakia was recorded in floodplain lowland forests. Interestingly, there is no record of H. erinaceus (Sikora and Neubauer, 2015) from one of the best known lowland forest in Europe e Bialowieza Forest. The reasons for this absence could be the cool continental macroclimate prevalent in the region and the marked dominance of Quercus robur amongst the oaks in the
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Fig. 2. Altitudinal range (A, mean, ±SD and min/max boxplot), tree host species distribution (B), vital status and position of a host stem (C) and number of records with respect to the state of forest stand (D) of Hericium erinaceus in Slovakia. Numbers above the bars represent number of records.
Bialowieza forest. Although many of our collections of H. erinaceus are on Quercus sp., there were no confirmed collections on Q. robur, which in Slovakia is more typical in floodplain forests where there was a very low frequency of H. erinaceus finds. However, Fraiture and Otto (2015) reported Quercus robur as a substratum for successful growth of H. erinaceus and acidophilus Q. robur woods on sandy plains as a suitable habitat. Fraiture and Otto (2015) assigned the European distribution of the fungus primarily to the lowlands, with only rare occurrence in mountainous regions up to 1500 m. In this study, half of the basidiomata incidence ranged between 327 and 560 m in altitude (1st and 3rd quartile). In Slovakia, this altitudinal range corresponds to a range of warm hilly country and upland beech-oak forests. The geological and soil conditions do not appear to play any role in determining the occurrence of the fungus. It seems that the species has a rather broad habitat preference close to optimum altitude-driven climatic conditions as long as it can find suitable host tree. Collections from species other than oak and beech are rare. The fungus is most frequently found on beech in Poland (Pia˛ tek, 2005) and in the UK (Boddy et al., 2011), on beech and oaks in the Czech Republic (Holec and Beran, 2006) and Austria (Austrian Mycological Society, 2015), and almost exclusively on oaks in Hungary (Siller et al., 2005). However, with the exception of the Czech Republic, where it is found in more than 50 known localities (Holec and Beran, 2006), the fungus is apparently rare or very rare in all countries neighbouring Slovakia. The extent of forest coverage might explain the rarity of the fungus in Poland and Hungary (28.8% and 20.3%), when compared to Slovakia (40.8%) and the Czech Republic (34%, CBD, 2016). In addition, the higher number and area of old-growth and natural forests might favour the species in Slovakia and the Czech Republic (García Feced et al., 2015). Relatively low number of observations in Austria may perhaps be
explained by the more dominant mountainous character of the landscape, generally not suitable for the fungus. In Germany there are 188 records of H. erinaceus (German Mycological Society, 2016). Considering the facts that the area of Germany is more than seven times larger than that of Slovakia, and with incomparably higher effort of mycologists, this suggests a much lower population density in this country. Overall, our data and survey of relevant literature sources indicate that H. erinaceus has a preference for rather dry, sunexposed parts of lowland forests in warm macroclimate regions in Europe. However, most of these lowland forests have been replaced by arable land and remaining forests stands are often designated as intensively managed forests and forest parks, with a conspicuous absence of veteran trees or large decaying stems (Kaplan et al., 2009), which is probably the main reason for the rarity of the species in most European countries. Limited spore dispersal as well as low spore germination rate of the fungus could contribute further to the rarity of the species (Crockatt et al., 2007). Long distance spore dispersal may be of greater importance for rare fungi whose populations are affected by habitat fragmentation, but it is unknown to what degree long-range spore dispersal is possible in this species. Within a European context, Slovakia is relatively densely covered by old-growth forests and their remnants with a high number of veteran trees and dead-wood volume (Parviainen, 2005). Fairly rugged parts of the country covered by forests also contain a long-established network of protective forests with almost natural tree species composition all over the country. These factors may contribute to the observed high incidence of H. erinaceus in Slovakia. It is important to point out that any fungal species may remain dormant while environmental conditions are unsuitable (Crockatt et al., 2007). Recent advances in research on mycelia in dead
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wood will reveal whether the fungus is indeed as rare as its basidiomata. Given the observed distribution of the records in Slovakia, we contend that H. erinaceus prefers forests with natural tree species composition dominated by oaks and beech, but it is not a strict indicator of old-growth forests in Slovakia. As a measure aimed at increasing the area of suitable habitat in managed forests, we recommend retaining low-value and misshapen trees during harvest to let them senesce naturally. Acknowledgments The research was financially supported by the Scientific Grant Agency of the Ministry of Education, Science, Research and Sport of the Slovak Republic and of the Slovak Academy of Sciences (VEGA 1/ 0362/13) and by the Cultural and Educational Grant Agency of the Ministry of Education, Science, Research and Sport of the Slovak Republic (KEGA 007TU Z-4/2015). We are grateful to Kvetoslava , Stefan , Mgr. Ja n Hrasko, Frantisek Bal a zova Bala z, Ludmila Cillíkov a s, Pavol Kesela k, Jaroslav Hubina, Stanislav Jankech, Vladimír Juha Kuriplach, Lubica Kuriplachov a, Vladimír Macík, Ing. Ivan Nagy, Mikul as Lazor, Anton P anis, Jozef Pavlík, Ing. Maros Peiger, Dusan Sol ar, Matús Skutka and Patrik Stibraný for providing information on finds of H. erinaceus, two anonymous reviewers for detailed comments on the manuscript and Dr. Martin Luka c for the language correction. References €mon, W., Hausknecht, A., KrisaiAustrian Mycological Society, 2015. In: Da Greilhuber, I. (Eds.), Database of Fungi in Austria. http://www.austria.mykodata. net (Accessed 15 September 2016). n, S.P., 2010. Corticiaceae s.l. Edizioni Candusso, Alassio. Bernicchia, A., Gorjo Blasi, C., Marchetti, M., Chiavetta, U., Aleffi, M., Audisio, P., Azzella, M.M., Brunialti, G., Capotorti, G., Del Vico, E., Lattanzi, E., Persiani, A.M., Ravera, S., Tilia, A., Burrascano, S., 2010. Multi-taxon and forest structure sampling for identification of indicators and monitoring of old-growth forest. Plant Biosyst. 144, 160e170. Boddy, L., Crockatt, M.E., Ainsworth, A.M., 2011. Ecology of Hericium cirrhatum, H. coralloides and H. erinaceus in the UK. Fungal Ecol. 4 (2), 163e173. CBD, 2016. Convention on Biological Diversity. https://www.cbd.int/ (Accessed 14 September 2016). Christensen, M., Heilmann-Clausen, J., Walleyn, R., Adam cík, S., 2004. Woodinhabiting fungi as indicators of nature value in European beech forests. In: Marchetti, M. (Ed.), Monitoring and Indicators of Forest Biodiversity in Europe e from Ideas to Operationality. European Forestry Institute Proceedings 51, Saarijarvi, pp. 229e237. Crockatt, M.E., Ainsworth, A.M., Parfitt, D., Rogers, H.J., Boddy, L., 2007. Why are the tooth fungi Hericium cirrhatum, H. coralloides and H. erinaceus rare? In: Anonymous (Ed.), World Conference on the Conservation and Sustainable Use of Wild Fungi. Junta de Andalucia, Cordoba, Spain, pp. 116e118. Fraiture, A., Otto, P. (Eds.), 2015. Distribution, Ecology and Status of 51 Macromycetes in Europe. Results of the ECCF Mapping Programme (Scripta Botanica Belgica, Meise). García Feced, C., Berglund, H., Strnad, M., 2015. Scoping Document: Information Related to European Old Growth Forests. ETC/BD Report to the EEA. ETC/BD,
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