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Basidiomycetes Associated with Alnus Glutinosa Habitats in Andros Island (Cyclades, Greece)

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Basidiomycetes Associated with Alnus Glutinosa Habitats in Andros Island (Cyclades, Greece) diversity Article Basidiomycetes Associated with Alnus glutinosa Habitats in Andros Island (Cyclades, Greece) Elias Polemis, Vassiliki Fryssouli, Vassileios Daskalopoulos and Georgios I. Zervakis * Laboratory of General and Agricultural Microbiology, Agricultural University of Athens, 11855 Athens, Greece; [email protected] (E.P.); [email protected] (V.F.); [email protected] (V.D.) * Correspondence: [email protected]; Tel.: +30-210-5294341 Received: 15 May 2020; Accepted: 7 June 2020; Published: 9 June 2020 Abstract: Alluvial forests dominated by black alder (Alnus glutinosa) are widespread in Europe along river banks and watercourses forming a habitat of renowned ecological/conservation importance. Despite the considerable interest this habitat has attracted in terms of the associated fungal diversity, very few pertinent data are available from the eastern Mediterranean. Andros island (Aegean Sea, Greece) hosts the southernmost population of A. glutinosa in the Balkan Peninsula; such stands have been systematically inventoried for several years in respect to macrofungi. In total, 187 specimens were collected and studied by examining morphoanatomic features and by evaluating (when necessary) the outcome of sequencing the internal transcribed spacer (ITS) region of nuclear ribosomal DNA (nrDNA) to elucidate their identity and obtain an insight into phylogenetic relationships. As a result, 106 species were recorded, 92 are saprotrophic and 14 form ectomycorrhizae (ECM) with alders. Twenty-one species are first national records, while 68 other species are reported for the first time from this habitat in Greece. Several findings of particular interest due to their rarity, ecological preferences and/or taxonomic status are presented in detail and discussed, e.g., six Alnicola taxa, Cortinarius americanus, Lactarius obscuratus, Paxillus olivellus and Russula pumila (among the ECMs), and the saprotrophs Entoloma uranochroum, Gymnopilus arenophilus, Hyphoderma nemorale, Lepiota ochraceofulva, Phanerochaete livescens and Psathyrella hellebosensis. Keywords: macrofungi; Basidiomycota; mushroom diversity; ectomycorrhiza; saprotroph; alder; Aegean Sea; Mediterranean; Alnicola 1. Introduction Alluvial forests with Alnus glutinosa Gaertn. and Fraxinus excelsior L. (priority habitat 91E0*; Annex I, Directive 92/43/EEC) are distributed throughout Europe, but they are generally rare and threatened since only remnants exist, mainly in central and northern Europe [1]. Alder stands are considerably less frequent in the Mediterranean region, where the repercussions of changes in the hydrological cycle caused by global warming and climate destabilization are much more evident [2]. The southernmost limit of the priority habitat 91E0* in the Balkan Peninsula is located in Andros island (Figure1), i.e., the northernmost in the Cyclades and situated at a transition zone between continental Greece and other islands of the Aegean Archipelago. From the geomorphological point of view, it is characterized by a remarkably intense relief and by many rivulets and streams of constant flow, which are unique among most of Central and South Aegean islands. A. glutinosa trees demonstrate a patchy distribution in Andros, predominantly occurring along the main streams within the Site of Community Importance (SCI) GR4220001 and in altitudes ranging from sea level to as high as 850 m above sea level (a.s.l.), very close to the highest peaks of the island. In many cases black alders are mixed with Platanus orientalis L., Fraxinus ornus L. and/or Nerium oleander L. (in lower altitudes), while they also form pure stands, as it is the case at the estuaries of the Vori stream in NE Andros. Diversity 2020, 12, 232; doi:10.3390/d12060232 www.mdpi.com/journal/diversity Diversity 2019, 11, x FOR PEER REVIEW 2 of 21 Diversityaltitudes)2020, ,while12, 232 they also form pure stands, as it is the case at the estuaries of the Vori stream in2 of NE 22 Andros. FigureFigure 1.1. MapMap presentingpresenting NaturaNatura 20002000 sites,sites, whichwhich includeinclude thethe prioritypriority habitathabitat 91E0*91E0* inin continentalcontinental EuropeEurope (in(in green)green) andand inin islandsislands (in(in blue);blue); AndrosAndros islandisland isis indicatedindicated byby thethe redred arrow.arrow. DataData fromfrom https:https://www.eea.europa.eu/data//www.eea.europa.eu/data-and-maps-and-maps/data/natura-6./data/natura-6. AlderAlder treestrees areare knownknown toto formform symbiotic relationshipsrelationships withwith nitrogen-fixingnitrogen-fixing actinomycetesactinomycetes ofof thethe genusgenus FrankiaFrankia BrunchorstBrunchorst [[3,4],3,4], withwith arbusculararbuscular mycorrhizalmycorrhizal fungifungi (AM)(AM) ofof GlomeromycotaGlomeromycota [[5,6]5,6] andand withwith variousvarious ectomycorrhizalectomycorrhizal (ECM)(ECM) fungifungi ofof AscomycotaAscomycota andand BasidiomycotaBasidiomycota [[7–9].7–9]. EuropeanEuropean alderalder standsstands have been been relatively relatively well well-studied-studied in in terms terms of ofboth both macro- macro- and and microfungal microfungal communities, communities, and andapprox. approx. 1000 1000 species species of saprotrophic of saprotrophic and and ECM ECM macrofungi macrofungi were were reported reported [10–15]. [10–15]. In In addition, mycocoenologicalmycocoenological studies from Europe and North America suggested that ECM fungi of Alnus spp. exhibitexhibit aa remarkablyremarkably highhigh degreedegree ofof hosthost specificityspecificity comparedcompared toto otherother treetree speciesspecies [[8,16],8,16], whilewhile thethe analysisanalysis ofof bothboth sporophoressporophores andand ectomycorrhizaeectomycorrhizae evidencedevidenced thatthat aldersalders havehave aa lowlow numbernumber ((<50)<50) ofof ECMECM symbiontssymbionts worldwideworldwide [[17–19].17–19]. LimitedLimited knowledgeknowledge is is available available on on the the diversity diversity of fungiof fungi associated associated with with alders alders in Greece, in Greece, andonly and preliminaryonly preliminary data are data reported are reported in the few in the pertinent few pertinent publications publications [20,21]. On [20,21]. the other On hand,the other Andros hand, is theAndros only is island the only of the island Aegean of the Archipelago Aegean Archipelago where a systematic where a inventorysystematic of inventory macrofungi of macrofungi is in progress is forin progress more than for 20more years. than Biotopes 20 years. characterized Biotopes characterized by river banks,by river springs banks, andsprings alluvial and alluvial forests, forests, where A.where glutinosa A. glutinosais often is the often dominant the dominant tree species, tree species, were forayed were forayed in the past in the and past 37 mushroomand 37 mushroom species werespecies reported were reported from this from particular this particular habitat in Andros,habitat in including Andros, ECMincluding symbionts ECM assymbionts well as xylotrophic, as well as litterxylotrophic, and/or humuslitter and/or saprotrophs humus [sa22protrophs–24]. Among [22–24]. the latter, AmongEntoloma the latter, alnicola EntolomaNoordel. alnicola & Polemis Noordel. was & describedPolemis was asnew described species asnew for science species and for it science is still knownand it is from still theknown type from locality the onlytype [locality25]. only [25]. SinceSince 2017, mycodiversity studies in in alder alder stands stands of of Andros Andros were were intensified intensified in in the the frame frame of of a aLIFE LIFE Nature Nature project project (LIFE16-NAT_GR_000606), (LIFE16-NAT_GR_000606), which which -among -among others- others- aims aims at the at theconservation conservation and and restoration of the priority habitat 91E0* in the island. Hence, during the last few years, new Diversity 2019, 11, x FOR PEER REVIEW 3 of 21 Diversity 2020, 12, 232 3 of 22 restoration of the priority habitat 91E0* in the island. Hence, during the last few years, new sites with sitesalder with stands alder were stands repeatedly were repeatedly forayed forayed(in addition (in addition to those to previously those previously investigated), investigated), and a andlarge a largenumber number of new of new collections collections were were made. made. These, These, together together with with previously previously sampled—butsampled—but stillstill unidentified—specimens,unidentified—specimens, werewere subjectedsubjected toto detaileddetailed morphoanatomicalmorphoanatomical examinationexamination inin conjunctionconjunction withwith sequencingsequencing andand phylogeneticphylogenetic analysesanalyses (where(where judgedjudged necessary)necessary) inin order to assess their identity. Moreover,Moreover, inin severalseveral occasions,occasions, pastpast relevantrelevant reportsreports onon recordedrecorded taxataxa werewere revisedrevised/re-evaluated/re-evaluated accordingaccording toto thethe latestlatest respectiverespective taxonomictaxonomic andand phylogeneticphylogenetic concepts. concepts. Hence,Hence, thisthis workwork presentspresents anan updatedupdated compilation compilation of of available available data data on theon diversitythe diversity of macrofungi of macrofungi in a habitat in a habitat of significant of significant interest occurringinterest occurring at the limits at the of limits its distribution of its distribution in Europe. in Europe. 2.2. MaterialsMaterials andand MethodsMethods 2.1.2.1. SamplingSampling ofof BiologicalBiological MaterialMaterial DataData
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