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25 May 2022

The Checklist of Sicilian Macrofungi: Second Edition

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1
Department of Agricultural, Food and Forest Sciences, University of Palermo, Viale delle Scienze, Bldg. 5, 90128 Palermo, Italy
2
Department of Agricultural and Environmental Science, University of Bari Aldo Moro, Via Amendola 165/A, 70126 Bari, Italy
*
Authors to whom correspondence should be addressed.
J. Fungi2022, 8(6), 566;https://doi.org/10.3390/jof8060566
This article belongs to the Special Issue Fungal Diversity in Europe
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Abstract

Approximately 30 years after the publication of the first Sicilian checklist of macrofungi, a new updated version is presented here. The census of macromycetes was carried out through periodic observations in different agricultural and forest ecosystems, in urban areas, in public and private gardens, and in botanical gardens. The 1919 infraspecific taxa included in 508 genera belonging to 152 families were collected in the Sicilian territory. Ectomycorrhizal fungi are the most represented ecological category, followed by saprotrophs on wood, saprotrophs on litter, and terricolous saprotrophs. The interest in this rich group of organisms is evidenced by the nutritional and therapeutic value of a high percentage of species. The actions linked to the National Recovery and Resilience Plan and The Network for the Study of Mycological Diversity will further increase the number of macrofungi for Sicily in the future.

1. Introduction

The checklists are modern tools for evaluation of fungal diversity and valuable papers to highlight ecological data, and tips for management and exploitation of protected areas, agro- and forest ecosystems. Relevant studies were published around the world—in Europe and in Italy [1,2,3,4,5,6,7,8].
The assessment of fungal diversity in the Italian regions is still incomplete and needs further investigation. In most Italian regions, it is difficult to document the exact number of mushrooms due to lack of mycologists. Even greater difficulty is faced in the evaluation of the presence of hypogeous macrofungi as few research groups have dogs trained to harvest.
The territories included in the Med-Checklist consider the Italian peninsula as a separate region from a floristic point of view, and its two major islands, Sicily and Sardinia, are separately coded [9]. The environmental peculiarities of Sicily in close relation to different habitats and ecosystems [10] determine high levels of biodiversity in all groups of organisms (plants, lichens, fungi, bryophytes, algae, and insects).
On the basis of literature data reported from 1814 to 1991, a preliminary survey on fungal diversity in Sicily was carried out by Venturella [11], with an estimate of approximately 750 macromycetes. Subsequently, Venturella et al. [12] published a report on the state of fungal diversity in Italy and analyzed the number of macrofungi for each region. This study showed that Sicily boasts a high number of macrofungi compared to other Italian regions.
From 1991 to present, the study of macromycete diversity has continued unabated through an intensive exploration of forest ecosystems, natural parks, nature reserves, public and private gardens, botanical gardens, cultivated and uncultivated lands.
Based on data collected during 30 years of long-term observation, an up-to-date assessment of fungal diversity of Sicily is reported in this paper.

2. An Outline of Vegetation Types of Sicily

The physiographic uniqueness of Sicily (southern Italy) coupled with the paleogeographic vicissitudes, over time have determined the progressive evolution of a rich vascular flora (ca. 3000 species) and the presence of a number of rare species or in any case of considerable taxonomic significance [13]. In agreement with Fenaroli and Giacomini [14] and Di Martino and Raimondo [15], Sicily is considered as a floristic area in itself, well characterized by a considerable endemic contingent (approximately l% of the entire flora), which can be defined as a Sicilian domain according to phyto-corological criteria.
The forest area of Sicily corresponds to 512,121 hectares and includes 58 types of forest vegetation [16]. The coastal and hilly belt is characterized by evergreen oak forests with Quercus ilex L. subsp. ilex, Q. coccifera L., and Q. suber L. as well as semi-evergreen oaks Quercus pubescens Willd. s.l. and Q. virgiliana (Ten.) Ten. In the warmer areas near the sea, forests can be replaced by aspects of Mediterranean maquis such as those characterized by Juniperus turbinata Guss., J. oxycedrus L. subsp. oxycedrus, J. macrocarpa Sm., Pistacia lentiscus L. and other sclerophyllous shrubs such as Cistus creticus L., C. salvifolius L. and C. monspeliensis L.
In the areas most subject to disturbance, the vegetation is currently represented by Ampelodesmos mauritanicus (Poir.) T. Durand & Schinz and other types of grassland and shrub communities. Even rarer are the natural forests of Mediterranean conifers such as Pinus halepensis Mill., P. pinea L. and P. pinaster Aiton, which are considered pioneer plants. In the hills, the natural forest vegetation, in the hottest and driest conditions, consists of mixed forests of deciduous oaks with dominance of Q. pubescens, while in cooler climatic conditions, with a marked oceanic climate, are more diffused Q. cerris L., Q. petraea (Matt.) Liebl and the endemic Q. gussonei (Borzí) Brullo. These species have in some cases been replaced for agricultural purposes or for the use of wood by Corylus avellana L., Fraxinus ornus L., and Castanea sativa Mill. The degradation aspects are represented by mesophilic shrubs dominated by different taxa belonging to the family of Rosaceae such as Pyrus pyraster. (L.) Burgsd. and P. amygdaliformis Vill. The forest vegetation of the mountain area is characterized by forests of Fagus sylvatica L. sometimes mixed with Acer pseudoplatanus L., Quercus petraea (Mattuschka) Liebl., Taxus baccata L. and llex aquifolium L. An exclusive characteristic of Sicily is the presence of forests of Q. ilex that reach an altitude of 1500 m well above the maximum elevation found in other parts of Italy. Of considerable interest is also the presence of different endemic trees and shrubs and evidence of relict forest vegetation such as Abies nebrodensis (Lojac.) Mattei, Betula aetnensis Raf., Celtis aetnensis (Tornab.) Strobl, Populus tremula L., Pinus laricio Poir., Quercus gussonei (Borzì) Brullo, Zelkova sicula Di Pasquale, Garfi & Quézel, and Genista aetnensis (Raf. ex Biv.) DC. Upland shrubs such as Sorbus graeca (Spach) Schauer and Berberis aetnensis C. Presl. are found in some areas lacking tree forest vegetation. Woody species that vegetate above the edge of the forest are found only on Mount Etna, but also in the Madonie. This vegetation is dominated by the shrubs of Astragalus nebrodensis on the Madonie and by A. siculum on Mount Etna.
The presence of Fagus sylvatica L. in Sicily can therefore be considered a remnant of the glaciations, when conditions had to be favorable even at lower altitudes.
The vegetation of the watercourses is characterized by typical riparian species such as Salix pedicellata Desf., S. alba L. and S. purpurea L., associated with Populus nigra L., P. alba L., Laurus nobilis L., Sambucus ebulus L., Cornus sanguinea L., Prunus mahaleb L. and Alnus cordata (Loisel.) Desf. [17].
In the sandy dunes, some plant associations such as Salsolo kali–Cakiletum maritimae Costa & Mansanet 1981, corr. Rivas-Martínez et al. 1992 and Salsolo kali–Euphorbietum peplis Géhu et al. 1984 are distributed.

3. Materials and Methods

The census of macromycetes was carried out through periodic observations, weekly or fortnightly (monthly during summer), in different agricultural and forest ecosystems, in urban areas, in public and private gardens, and in botanical gardens. For each species, the fresh basidiomata and ascomata were collected and subsequently identified on the basis of macroscopic (pileus, flesh, lamellae, stipe, and type of occurrence: solitary, grouped, clustered, cespitose, color of spore prints, etc.) and microscopic characters (spores, basidia, asci, cystidia, pileipellis, element of the stipe surface, etc.), also with the help of distilled water, immersion oil, chemical reagents (Melzer’s reagent, KOH, Ammoniated Congo Red, Cotton blue-lactic acid), and analytical keys related to the different genera. Most specimens were identified solely on the basis of morphological characteristics; for some critical groups (e.g., Daldinia and Pleurotus), reference was made to previous studies using molecular analysis [18,19,20]. The dried specimens, prepared in a universal dryer 475 Watt stainless steel structure with 5 baskets, are kept in the Herbarium SAF of the Department of Agricultural, Food and Forest Sciences (SAAF) of the University of Palermo. The nomenclature of fungi follows Index Fungorum while that of plants refers to Euro + Med PlantBase.

4. Results

The 1919 infraspecific taxa included in 508 genera belonging to 152 families were collected in the Sicilian territory (Table 1).
Table 1. List of recorded taxa with indications on family, province and ecological category. Provinces: AG = Agrigento, CL = Caltanissetta, CT = Catania, EN = Enna, ME = Messina, PA = Palermo, RG = Ragusa, SR = Siracusa, and TP = Trapani. Ecological categories: Em = Ectomycorrhizal, Pm = Parasite on mushrooms, Pn = Necrotroph parasites, Sbg = Saprotrophs on burnt ground, Sd = Saprotrophs on dung, Sc = Saprotrophs on cones, Scl = Saprotrophs on cladodes, Scu = Saprotrophs on cupules, Se = Saprotrophs on esuviae, Sh = Saprotrophs on humus, Sl = Saprotrophs on litter, Sle = Saprotrophs on leaves, Sm = Saprotrophs on mosses, St = Terricolous saprotrophs, Sw = Saprotrophs on wood, and UNK = Unknown.
Families with the highest number of species are Russulaceae (164 taxa) and Agaricaceae (125 taxa).
According to Index Fungorum, 131 taxa of uncertain taxonomic classification are reported in Table 1 as Incertae sedis. Other families, with number of infraspecific taxa greater than 50 (Figure 1), are Boletaceae (78), Cortinariaceae (72), Hygrophoraceae (63), Inocybaceae (58), Hymenogastraceae (56), Tricholomataceae (54), Amanitaceae (51), Pyronemataceae (51), and Psathyrellaceae (51).
Figure 1. Most representative families with number of taxa greater than 50.
The highest number of infraspecific taxa (Figure 2) is found in the province of Palermo (1610) followed by in Messina (1546) and Catania (1517). The province with the lowest number of infraspecific taxa is Caltanissetta (330).
Figure 2. Number of taxa per provinces.
The taxa listed in Table 1 belong to 15 ecological categories. For ten taxa, the ecological category to be assigned is unclear and is therefore listed as Unknown (UNK).
Ectomycorrhizal fungi (637 taxa) are the most represented ecological category (Figure 3), followed by saprotrophs on wood (484 taxa), saprotrophs on litter (386 taxa), terricolous saprotrophs (279 taxa), saprotrophs on mosses (39 taxa) saprotrophs on dung (39 taxa), saprotroph on burnt ground (19 taxa), necrotroph parasites (8 taxa), saprotrophs on leavers (5 taxa), and saprotrophs on humus (2 taxa). Three saprotrophic species characterized by particular substrates such as exuviae of different insects [Cordyceps militaris (L.) Fr.], cupules of Castanea sativa Miller [Lanzia echinophila (Bull.) Korf], and cladodes of Opuntia ficus-indica [Pleurotus opuntiae (Durieu & Lév.) Sacc.] complete the list.
Figure 3. Number of taxa per ecological categories.

5. Discussion

Fungi are recognized worldwide as fundamental components in every type of ecosystem [21]. After a long period in which fungi have received insufficient consideration in biodiversity studies [22], in the last twenty-five years, there has been a growing interest in this group of living organisms, which are of great importance as a food source for future generations [23], potential remedies for human and animal diseases [24], and for the protection of the environment [25].
The climatic features of Sicily are favorable to the development of basidiomata and ascomata of different fungal species. The observations carried out during the present study showed a constant presence throughout the year of macrofungi in ecosystems. Most species are collected in fall, although the presence of macrofungi appears to be strongly affected in some years by prolonged periods of drought. In the woods of the hinterland, it is possible to have optimal conditions of temperature and humidity able to favor the appearance of macrofungi even in the summer. In Sicily, spring is not a season of abundance for fungal fruiting and ascomycetes predominate among species. In winter and summer, pathogenic basidiomycetes and wood saprotrophs can be predominantly observed.
Due to the presence of the three major regional parks (Madonie Park, Nebrodi Park, and Etna Park) in these territories, the largest number of infraspecific taxa is found in the provinces of Palermo, Messina and Catania. In the other provinces, reafforestations are prevalent and thus the composition of fungal coenoses is reduced in quality and quantity.
The greatest number of species is found within beech forests. The low night temperatures, the summer storms and the presence of occult precipitations determine, starting from the second decade of August, the early appearance of macrofungi that are generally found, at lower altitudes, in autumn within the forest ecosystems. A rich number of lignicolous species, mostly pathogenic and to a lesser extent saprotrophic, has also been surveyed within beech forests, growing on trees, branches of different sizes that have fallen to the ground and stumps. A similar condition of prevalence of mycorrhizal species is found in oak and holly forests and in chestnut groves. In the latter type of forest, an important role in the decomposition of the abundant litter layer is provided by Marasmius bulliardii while it is very common to observe Fistulina hepatica at the base of chestnut trees. In Quercus ilex forests, fungi responsible for wood decay (Armillaria mellea, Fuscoporia torulosa, Cyclocybe cylindracea, Laetiporus sulphureus, and Daldinia raimundi) are observed on stumps and trunks. Compared with other oak forests, fewer macrofungi are reported Quercus suber forests and in the maquis. This is due to the greater state of degradation of the forest coenosis due to frequent fires that cause a significant reduction in the number of mycorrhizal species and saprotrophs, the latter negatively affected by the drastic reduction in plant residues. In pastures, grasslands, and garrigues, the number of mycorrhizal species is limited to those of shrubs of the genus Cistus (Lactarius cistophilus and Leccinellum corsicum). Saprotrophs on litter and lignicolous species are widespread in riparian vegetation.
The high percentage of mycorrhizal species within the natural forests and reforestations of Sicily allows to exclude at the moment a decline in forest ecosystems. In some forested areas, frequent fires cause a reduction in mycorrhizal species and saprotrophs on litter due to the drastic reduction in plant residues. Conversely, silvicultural practices and the resulting failure to remove woody debris of different sizes promote the appearance of crusty, shelf-like, or gelatinous lignicolous macrofungi.
The presence of prized and edible truffles, especially within the holm oak and pine woods, is of relevant interest especially for the areas of the Sicilian hinterland characterized by a depressed economy [26]. These prized truffles and other mushrooms of excellent edibility and high organoleptic qualities (e.g., Pleurotus ssp.) represent a valuable example for the economic enhancement of fungal diversity in Sicily. Of great interest is the presence on the Sicilian territory of rare species classified according to IUCN criteria as Vulnerable (Alessioporus ichnusanus) [27], Least Concern (Poronia punctata) [28], and Endangered (Pleurotus nebrodensis) [29]. Mushrooms are considered healthy food components to be preserved for future generations in terms of nutritional, bioactive and therapeutic value. Among the species surveyed in Sicily, there are medicinal mushrooms, such as Grifola frondosa, Ganoderma lucidum, and Ericium erinaceus, with proven pharmacological activities including antibacterial, antifungal, antiviral, cytotoxic, immunomodulating, anti-inflammatory, antioxidative, antiallergic, antidepressive, antihyperlipidemic, antidiabetic, digestive, hepatoprotective, neuroprotective, nephroprotective, osteoprotective, and hypotensive activities.

6. Conclusions

Although the number of fungal species is still in constant flux, Sicily is among the Italian regions with the highest diversity of fungal species, many of which are of potential applicative interest and economic interest. Therefore, it is necessary to raise the level of knowledge and attention on the part of local communities towards this group of organisms. The data reported in this survey strongly increase the knowledge on distribution and ecology of macromycetes in Sicily and may help better valorize such non-timber products. The outcome of the checklist carried out in Sicily could provide the Regional Administration with useful information for the conservation and exploitation of fungi in natural habitats, with particular reference to forest ecosystems. Legislation should limit the level of danger existing for the conservation of fungal diversity and support such strategies with more rigorous limits against wild edible mushroom overharvesting. The cultivation of some prized edible mushrooms, i.e., Pleurotus and Tuber species, can provide an important income in agroecosystems, especially in rural or marginal areas.
The National Recovery and Resilience Plan (NRRP) and The Network for the Study of Mycological Diversity (NSMD), recently launched, will contribute to implement the monitoring of mycological biodiversity within national terrestrial habitats.
These actions will be carried out with the contribution of institutions such as the Higher Institute for Environmental Protection and Research (ISPRA) of the Italian Ministry of Ecological Transition and the Working Group for Mycology of the Italian Botanical Society through an Open Science initiative.

Author Contributions

Conceptualization, G.V. and M.L.G.; data curation, V.F. and G.M.; investigation, V.F., G.V., F.C., G.M., M.L.G. and P.C.; methodology, G.V.; supervision, G.V.; validation, G.V.; visualization, F.C.; writing—original draft, G.V., M.L.G. and P.C.; writing—review and editing, G.V., F.C. and M.L.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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