Hygrophorus roseodiscoideus Bon & Chevassut

Bellanger, Jean-Michel, Moreau, Pierre-Arthur, Dima, Bálint, Albert, László, Krisai-Greilhuber, Irmgard, Campo, Emanuele, Sleiman, Sandra, Dvořák, Daniel, Zehnálek, Petr & Holec, Jan, 2022, Hygrophorus roseodiscoideus Bon & Chevassut: epitypification and updated biogeography of a poorly known but widespread thermophilous species, Cryptogamie, Mycologie 20 (4), pp. 81-90 : 83-88

Hygrophorus roseodiscoideus Bon & Chevassut

Documents mycologiques 15 (59): 42 ( Bon & Chevassut 1985).

ORIGINAL DIAGNOSIS. — Pileus 5-12 cm, convexus vel late mammosus, carnosus, margine involuta, cuticula viscosa, coloribus versus discum fulvobrunneis vel rubrocastaneis, versus marginem paulatim pallidioribus, aurantio-ochraceis vel cremeo-roseis. Lamellae arcuatae, decurrentes, distantes, pallide cremeo roseae, vel ab imo subincarnatae. Stipes 6-10(13) × 1-2.5 cm, deorsum attenuato, sursum albido-punctuato, zona viscosa subannuliformi, fugaci atque versus basim nonnulis fasciolis +/- ochraceis. Caro pallide incarnata, odore saporeque subnullo vel fungoso. Sporae 9-10 × 5.5-6.5 µm, ellipticae.Trama bilateralis; basidia 45-65 × 7-10 µm, tetraspora. Cuticula pilei hyphis × 3-5 µm, gelatinosis, pigmento mixto vel membranari interdum verrucoso. Caulocutis sursum pilis +/- refringentibus, deorsum hyphis elongatis in micaceo muco coercitis. In Querceto ilicis vel pubescentis lectus, serotinus. Holotypus no. 84 391 in herbario MB – Cotypus GC 3326.

HOLOTYPE. — France. Gard, close to Quissac, Quercus ilex and Q. pubescens on calcareous bedrock, 12.XII.1984, leg. G. Chevassut, det. M. Bon, Bon 84391 (holo-, LIP[LIP 0102284]); iso-, in herb. G. Chevassut 3326 (current location of this herbarium is unknown) ( Fig. 1 ).

EPITYPE. — France. Bouches-du-Rhône, Simiane-Collongue, calcareous bedrock, under Q. ilex and Pinus halepensis Mill. , 31.X.2000, leg. & det. P.-A. Moreau, PAM00103101 (epi-, designated here in support of the holotype cited above, LIP[LIP 0402283]), GenBank ITS: MZ576440 , MycoBank: MBT 10003653 ( Fig. 2 ).

ADDITIONAL MATERIAL EXAMINED. — Austria. Burgenland, district Oberpullendorf, community Horitschon, Ragerwald, 47°34’30”N, 16°32’30”E, 290 m a.s.l., bedrock, Inner Alpine Neogene Basin, clay, marl, marlstone, sand, gravel, limestone, in thermophilous oak forest, near Quercus cerris , Carpinus betulus L., and Acer L., c. 10 basidiomata, 29.IX.1988, leg. W. Klofac, det. A. Hausknecht (WU[WU-Myc 007470]).

Croatia. Istria Region, Novigrad, Tar, sea coast, Mediterranean area, under Quercus ilex and Arbutus unedo L., 6.XII.2003, leg. & det. E. Campo ( TUR [TUR-A 162859]); under Quercus pubescens , on calcarous soil, 6.XII.2014, leg.& det. E. Campo ( MCVE [MCVE 28439]); Kvarner Region, Krk, Malinska, in Mediterranean area, on calcareous soil under Q. pubescens and Q. cerris , 17.XI.2018, leg. & det. E. Campo (specimens not kept).

Czech Republic. Central Bohemia, near the village of Mcely, Čtvrtě National Nature Reserve, 50°17’54”N, 15°4’11.579”E, 225 m a.s.l.,under Carpinus L., Tilia L., Corylus L. and Quercus robur L. on calcareous bedrock (arenaceous marl), 10.IX.2010, leg. Jan Borovička, voucher lost; 50°17’39.96”N, 15°3’9.84”E, 250 m a.s.l., thermophilous oak forest, calcareous bedrock, under Quercus robur , 5.XI.2020, leg. & det. J. Holec, JH366/2020 ( PRM [PRM 955166]; Fig. 4A ); 50°17’52.868”N, 15°4’15.354”E, 225 m a.s.l., in warm broadleaved forest under Carpinus and Quercus , 1.XI.2020, leg. & det. J. Borovička, 3192 ( PRM [PRM 954665]) (This site is 1.4 km NEE of the previous one and very close [about 50-100 m] to the first record from Čtvrtě in September 2010 [see above].); South Moravia, near Mokrá-Horákov, Sivický les, 49°13’16.2”N, 16°45’46.439”E (accuracy several hundred meters), 350-400 m a.s.l., thermophilous oak forest, calcareous bedrock, under Quercus petraea (Matt.) Liebl. , Carpinus and Sorbus torminalis (L.) Crantz, 4.XI.2007, leg. & det. D. Dvořák, DD 501/07 ( BRNU [BRNU 677820]; Fig. 4B ).

France. Bouches-du-Rhône, Simiane-Collongue, calcareous bedrock, under Q. ilex and Pinus halepensis , 31.X.2000, leg.& det.P.-A.Moreau, PAM00103101 (epi-, LIP[LIP 0402283]; Fig. 2 ); Hérault, Montpellier, campus du CEFE-CNRS, calcareous bedrock, under Q. ilex and Pinus halepensis , 5.XII.2010, leg. & det. F. Richard, FR0512001 ( CEFE); Hérault, Puechabon, site expérimental du CEFE-CNRS, 43°44’29”N, 03°35’45”E, 270 m a.s.l., calcareous bedrock, soil under Q. ilex , 28.I.2009, leg. O. Shahin, det. F. Richard (environmental sample VAC25b-09), GenBank: JF506763 ( Richard et al. 2011); Vaucluse, Cadenet, La Royère, calcareous bedrock, under Q. ilex , Q. pubescens and P. halepensis , 7.XII.2004, leg. & det. D. Borgarino, DiBo041144; Vaucluse, Cucuron, La Capagière, calcareous bedrock, under Q. ilex , Q. pubescens and P. halepensis , 10.XII.2004, leg. & det. D. Borgarino, DiBo041202 ( Fig. 4C ).

Hungary. Budai-hegység Mts., Budapest, Mt. Széchenyi-hegy, 47°29’16.56”N, 18°58’56.279”E, 400 m a.s.l., thermophilous oak forest ( Ceraso mahaleb -Quercetum pubescentis), calcareous bedrock, under Quercus pubescens , Quercus cerris , Fraxinus ornus L., Tilia cordata Mill. , Prunus mahaleb L., Cornus mas L., 8.XI.2015, leg. & det. L. Albert, AL 280/15; 12.XI.2020, leg. & det. L. Albert & B. Dima, AL 342/20, DB 2020-11-12-2 ( ELTE) ( Fig. 4D ); Budai-hegység Mts., Budapest, Mt. János-hegy, 47°31’18”N, 18°56’59.7”E, thermophilous oak forest, calcareous bedrock, under Quercus pubescens , Quercus cerris , Fraxinus ornus , 10.X.2014, leg. & det. B. Dima, DB5586 ( ELTE); Budai-hegység Mts., Budakeszi, Wildlife Park, in deciduous forest, calcareous bedrock, under Quercus petraea , Carpinus betulus , 21.X.1976, leg. G. Bohus & M. Babos (as Hygrophorus fagi G.Becker & Bon ), det. B. Dima ( BP [BP58973]), GenBank: MK088109 ( Zajta et al. 2019); Bükk Mts., Borsod-Abaúj-Zemplén County, Miskolc, Csanyik-völgy, in deciduous forest, calcareous bedrock, under Carpinus betulus , Fagus sylvatica L., Quercus petraea , 16.X.2007, leg. & det. L. Albert & B. Dima, AL 07/90; Vértes Mts., Fejér County, Csákvár, thermophilous oak forest, calcareous bedrock, under Quercus cerris , 1.XI.2015, leg. P. Finy, det. B. Dima, FP 2015-11-01.

Italy. Friuli Venezia Giulia,Trieste, Parco di Miramare, 45°42’16.18”N, 13°42’52.37”E, 10 m a.s.l., on calcareous soil under Q. ilex , 28.XII.2012, leg. & det. P. Picciola (AMB-Muggia[AMB-Muggia 5824]); 21.XII.2014 (AMB-Muggia[AMB-Muggia 5657]); 28.XI.2015 (AMB-Muggia[AMB-Muggia 5846]); Friuli Venezia Giulia,Trieste, Muggia, Santa Barbara, 45°35’14.89”N, 13°47’4.50”E, 200 m a.s.l., on calcareous soil in mixed wood with Q. pubescens and P. nigra J.F.Arnold , 11.X.2017, leg. & det. P. Picciola (AMB-Muggia[AMB-Muggia 7196]); Friuli Venezia Giulia, Trieste, Basovizza, Bosco Igouza, 45°39’14.47”N, 13°52’24.48”E, 400 m a.s.l., on calcareous soil in mexed wood with P. nigra , Quercus sp. and other deciduous trees, 15.X.2017, leg. & det. P. Picciola (AMB-Muggia[AMB-Muggia 7175]); Toscana, Siena, Castellina in Chianti, Cipresseta S. Agnese, on calcareous soil under Quercus pubescens and Q. ilex , 28.X.2016, leg. & det. E. Campo, EC16102825 ( Fig. 4E ); Umbria, Carpegna, Passo Cantoniera, deciduous forest with Quercus cerris , 13.X.2004, leg. & det. A. Hausknecht ( WU [WU-Myc 25200]; Fig. 4F ).

Lebanon. North Lebanon, Akkar district, near the village of Tesheh, 34°29’24.048”N, 36°11’34.343”E, 1354 m a.s.l., mixed limestone, sandstone and volcanic soil in Quercus calliprinos Webb forest with understory of Styrax officinalis L. and Juniperus oxycedrus L., 15.XII.2018, leg. & det. S. Sleiman ( CEFE), GenBank: MZ088125 ( Sleiman et al. 2021).

ECOLOGY AND DISTRIBUTION. — Austria. The only known locality (Burgenland, Ragerwald) is a thermophilous oak forest with Quercus cerris on calcareous bedrock. Alltogether, some 500 species of fungi are known from this forest, among them rare in northern localities thermophilic species like Amanita caesarea (Scop.) Pers. , Neoboletus xanthopus (Klofac & A.Urb.) Klofac & A.Urb. , Rubroboletus legaliae (Pilát & Dermek) Della Maggiora & Trassinelli , R. rhodoxanthus (Krombh.) Kuan Zhao & Zhu L. Yang , R. satanas (Lenz) Kuan Zhao & Zhu L. Yang , Russula pannonica Pidlich-Aigner , as well as Omphalotus olearius (DC.) Singer , Desarmillaria tabescens (Scop.) R.A.Koch & Aime , Butyriboletus regius (Krombh.) D.Arora & J.L.Frank , and Astraeus hygrometricus (Pers.) Morgan.

Croatia. The only records known to us are from the coastal Mediterranean areas of North Croatia (Istria, Krk), on calcareous soils, under Quercus ilex , Q. pubescens or Q. cerris .

Czech Republic. Hygrophorus roseodiscoideus is known only from two localities. Both of them are thermophilous oak forests on calcareous bedrock (arenaceous marl, limestone). In Čtvrtě (Central Bohemia), the forest is mainly composed by Quercus robur but also other trees like Q. pubescens , Carpinus betulus , Cornus mas , Sorbus torminalis , or Tilia . Interestingly, H. roseodiscoideus was not found at the hottest sites typical by occurrence of Q. pubescens , but all three collections were under Quercus robur . In Sivický les (Southern Moravia), the host tree was most likely Q. petraea . Čtvrtě site is characteristic by a typical community of thermophilous ectomycorrhizal fungi ( Šebek 1990; Zíbarová 2014; Holec 2020) like Amanita solitaria (Paulet ex Vittad.) Bertill. , A. franchetii (Boud.) Fayod , Butyriboletus appendiculatus (Schaeff.) D.Arora & J.L.Frank , B. fechtneri (Velen.) D.Arora & J.L.Frank , Entoloma sinuatum (Pers.) P.Kumm. , Hemileccinum impolitum (Fr.) Šutara , Hygrophorus penarioides Jacobsson & E.Larss. , Inocybe godeyi Gillet , Lactarius acerrimus Britzelm. , L. evosmus Kühner & Romagn. , L. pterosporus Romagn. , Leccinellum crocipodium (Letellier) Della Maggiora & Trassinelli , L. pseudoscabrum (Kallenb.) Šutara , Russula decipiens (Singer) Svrček , R. luteotacta Rea and numerous Cortinarius (Pers.) Gray ( Phlegmacium (Fr.) Wünsche ) species. The locality is protected as a national nature reserve and about 500 species of fungi are recorded there. Sivický les hosts a rich community of mainly ectomycorrhizal thermophilous and calciphilous species ( Antonín et al. 2007), e.g. Amanita solitaria , Aureoboletus gentilis (Quél.) Pouzar , Butyriboletus appendiculatus , Cortinarius cotoneus Fr. , C. dibaphus Fr. , C. sodagnitus Rob.Henry and other cortinarii, Hemileccinum depilatum (Redeuilh) Šutara , H. impolitum , Hygrophorus arbustivus , H. russula (Schaeff. ex Fr.) Kauffman , Lactarius zonarius (Bull.) Fr. , Lyophyllum rhopalopodium Clémençon , Rubroboletus rhodoxanthus , R. satanas , Suillellus queletii (Schulzer) Vizzini, Simonini & Gelardi , Tricholoma filamentosum (Alessio) Alessio and many others. The site is currently declared as Special Area of Conservation (Natura 2000 site) with occurrence of Galio-Carpinetum oak-hornbeam forests (habitat 9170) and Euro-Siberian steppic woods with Quercus spp. (habitat 91I0). A small part of the area is protected as the Nature Monument Na Líchách. France. All molecularly confirmed collections of H. roseodiscoideus come from thermophilous, calciphilous Quercus ( Q. ilex , Q. pubescens ) woodlands of the Mediterranean area (cf. above). However, the species is reported from several localities in the western part of the country, under the influence of the Atlantic Ocean and always in the vicinity of Quercus trees, apparently following the geographical range of Q. ilex (cf. www.mycocharentes.fr and www.societemycologique-poitou.org). Although the identity of these collections remains to be confirmed, published photographs and descriptions are indeed compatible with H. roseodiscoideus and this species might be present there as well. Bon & Chevassut (1985) reported collections from acidic soils, but they appear to be less abundant than those from calcareous ground.

Hungary. Hygrophorus roseodiscoideus is known from five localities, of which three are situated around the forests of the capital, Budapest. Two older collections were determined as Hygrophorus fagi ( Babos 1989) and H. leporinus Fr. s. Moser ( Albert 2007). All localities are thermophilous calcareous deciduous forests dominated by Quercus species. Two of the localities (Mt. Széchenyi-hegy and Mt. Jánoshegy) are dominated by Q. pubescens with additional tree and shrub species such as Q. cerris , Fraxinus ornus , Tilia cordata , Cornus mas , etc. These habitats are hot-spots for many rare and thermophilous/ Mediterranean macrofungi such as Cortinarius atrovirens subsp. ionochlorus (Maire) Vizzini & Gasparini , C. quercilicis (Chevassut & Rob. Henry) Melot , C. violaceipes Bidaud & Consiglio , C. flavoaurantians Boccardo, Clericuzio & Vizzini , C. diffractosuavis Chevassut & Rob. Henry , C. ochrolamellatus Ballarà et al. , C. chevassutii Rob.Henry , C. prodigiosus B.Bušek et al. , Hygrophorus russula , Tricholoma basirubens (Bon) A.Riva & Bon , Boletus aereus Bull. The three other localities are not so thermophilic, they are dominated by Q. cerris or Q. petraea with admixture of Carpinus betulus .

Italy. Documented collections are from northern and central Italy (see section Additionnal material examined). In all cases, H. roseodiscoideus was collected on calcareous soil, mostly under Quercus ilex , but also under Q. pubescens or Q. cerris , sometimes in mixed tree communities with Pinus nigra . In addition, E. Campo observed the species in the regions of Veneto (commune Chioggia), Liguria (Portofino), Emilia Romagna (Bettola), Toscana (Castellina in Chianti, Lucca, Capalbio), Marche (Ancona), Lazio (Tolfa), Sardegna (Isili, Nurallao) and Abruzzo (Loreto Aprutino). In these regions the occurence was linked to Quercus ( Q. ilex , Q. pubescens , Q. cerris ) on calcareous soils. It is very curious that the species is not reported from southern Italy (G. Schirinzi, pers. comm.).

Lebanon. The first Asian record of H. roseodiscoideus is from northern Lebanon, in Quercus calliprinos forest with Styrax officinalis and Juniperus oxycedrus understory. Other species found at this site the same day were Tricholoma argyraceum (Bull.) Gillet , Cortinarius caligatus Malençon , Cortinarius subbulliardioides Rob.Henry , Cortinarius violaceipes , Cortinarius puellaris Brandrud et al. , Cortinarius luteocingulatus Bidaud & Fillion and Inocybe tenebrosa Quél. All of them are new records for Lebanon and notably, this ecosystem appears to be the richest in fungal diversity compared to Abies cilicica (Antoine & Kotschy) Carrière and Quercus cerris ecosystems in the region ( Sleiman et al. 2021).

NOTES

In the protologue, Bon & Chevassut (1985) cited a number of collections from the Montpellier area and from Roussillon, in the current Occitanie Region, as well as from Quercus woodlands near Aix-en-Provence and further east along the Côte d’Azur in the Provence-Alpes-Côte d’Azur Region. In its original concept, H. roseodiscoideus is thus a species fruiting along the whole French Mediterranean coast and in nomenclatural terms, all this cited material can be considered as paratypic. Unfortunately, the holotype could not be successfully sequenced (neither by the “classical” Sanger method nor the Illumina Miseq method), and none of the paratypes cited by Bon & Chevassut (1985: 44) could be located in Bon’s collections at LIP. Georges Chevassut’s herbarium has been lost after his death and no collection from his herbarium could be located either. To fix usage of the name, we thus epitypify it here using a sequenced collection from Simiane-Collongue, a locality 15 km south from Aix-en-Provence. This collection perfectly fits the description of H. roseodiscoideus , both macro- and micro-anatomically ( Fig. 2 ), and its ITS sequence can thus be used as a barcode for the species in future studies.

Figures

FIG. 1. — Original material of Hygrophorus roseodiscoideus Bon & Chevassut: A, hand-written description sheet and color drawing of specimens of the holotype of H. roseodiscoideus by M. Bon;B, photograph of the dried basidiomata (holo-, Bon 84391 kept in LIP).

FIG. 2. — Macro- and microcharacters of the epitype of Hygrophorus roseodiscoideus Bon & Chevassut. In situ photograph, violet hues are exaggerated as the photo has been taken with a flash. A, photo by P.-A. Moreau; B, pileipellis structure; C, lamellar trama structure; D, spore drawing; E, basidia drawing of PAM00103101 (LIP[LIP 0402283]). Scale bars: A, 1 cm; B, C, 100 µm; D, E, 10 µm.

FIG. 4. — Basidiomata of Hygrophorus roseodiscoideus Bon & Chevassut: A, Czech Republic, Čtvrtě, photo by J. Holec (PRM[PRM 955166]); B, Czech Republic, Sivický les, photo by D. Dvořák (BRNU[BRNU 677820]); C, France, Cucuron, photo by D. Borgarino (DiBo041202); D, Hungary, Mt. Széchenyi-hegy, photo by B. Dima (DB 2020-11-12-2); E, Italy, Cipresseta S. Agnese, photo by E. Campo (EC16102825); F, Italy, Passo Cantoniera, photo by A. Hausknecht (WU[WU-Myc 25200]). All collections were sequenced. For full collection data, see section Additionnal material examined.