Known Localities in Poland (Figure 1A)

Fd-38 KRAKÓW-CZĘSTOCHOWA UPLAND, Olkusz Upland: Trzyciąż planned reserve, in mixed forest (Abies, Picea, Acer pseudoplatanus), 400 m a.s.l., September 2013 (Chachuła, 2018).

New Localities (Figure 1A)

Bf-47 EASTERN SUDETES, Śnieżnik Mt: Kletno, in mixed forest (Picea, Fagus), 710 m a.s.l., 2013-07-20, leg. & det. M. Kozak & K. Kozłowska-Kozak, KRA F-2013-35.

Gd-17 OUTER WESTERN CARPATHIANS, Beskid Żywiecki Mts, Babia Góra Range, Skawica, in the middle part of the Skawiczanka Stream Valley, in mixed forest (Abies, Fagus, Picea), 550 m a.s.l., 2012-06-28, leg. & det. M. Kozak, KRA F-2012-38.

Gd-59 CENTRAL WESTERN CARPATHIANS, Western Tatra Mts: Tatra National Park:

Ge-11 OUTER WESTERN CARPATHIANS, Gorce Mts: mouth of Za Palacem Stream, in garden near buildings, close to the forest edge (Abies, Picea, Fagus), 650 m a.s.l., 2015-11-09, leg. E. Zając, det. P. Mleczko, KRA F-2015-3.

Ge-21 OUTER WESTERN CARPATHIANS, Gorce Mts:

Notes

The features of the Polish specimens correspond to those published in other studies, for example, Montecchi and Sarasini (2000) and Van Vooren (2017). Tuber-like sporocarps, which can reach over 5 cm in diameter, vinaceous-black-to-black peridium with a granular-to-warty surface, and cream-colored, solid gleba that turns gray with age in fertile chambers, are macroscopic characters of the species (Figure 2A). However, the most distinguishing features are lemon-shaped, deeply yellow-to-yellow-brown, guttulate spores with dimensions of approximately 65–70 × 20–35 μm (Figure 2E,F).

Originally described as a new species of Picoa by Tulasne & Tulasne (1862), the species was then classified within the genus Leucangium by Paoletti (Saccardo, 1889). Recent phylogenetic studies based on multilocus sequence analysis have confirmed its position within the Morchellaceae-Discinaceae lineage in the Morchellaceae family, whereas species of Picoa, such as P. lefebvrei and P. juniperina, have been placed in Pyronemataceae (O’Donnel et al., 1997; Sbissi et al., 2010; Trappe et al., 2010).

The first record of this species in Poland comes from the Olkusz Upland, a calcareous region in the central part of the country (Chachuła, 2018). Several other localities were discovered in southern Poland, mostly in the Carpathians but also in the Sudetes (see the list above). The species is associated in Europe with the coniferous trees A. alba and P. abies (e.g., Montecchi & Sarasini, 2000). However, in North America, it is a mycorrhizal partner of Pseudotsuga menziesii (Palfner & Agerer, 1998; Trappe, 1971; Trappe et al., 2010). In North Africa, L. carthusianum grows near Rhanterium suaveolens and Helianthemum lipii in calcareous alkaline soils, but it could still be a separate taxon (Thomas et al., 2019).

The species is widespread but rare in Europe (Montecchi & Sarasini, 2000; Van Vooren, 2017). Most reports regarding its taxonomy and distribution are provided by MycoDB [“Base de Jacques Trimbach (Picoa carthusiana),”2020], Oertel (2011), and Van Vooren (2017). Other than Southern and Western European countries, such as France (Van Vooren, 2017), Italy (Montecchi & Sarasini, 2000), Spain, and Switzerland (Flammer, 2011; Senn-Irlet, 1985), it has also been found in all Central European countries, including Austria (“5976. Picoa carthusiana Tul.,” 2020), the Czech Republic (Valda, 2018; Veselý, 1928), Germany (“Picoa carthusiana Tul. & C. Tul. 1862,” 2020), Hungary (Bratek et al., 2013), Slovakia (Glejdura, 2013; nahuby.sk, 2020; Pejger, 2019), northern Romania (Béres, 1999), and Poland. Most localities are present in mountain ranges, for example, the Alps in southern Germany and Austria, the Sudetes in southeastern Germany and Poland, and the Carpathians in Hungary, Romania, Slovakia, and southern Poland. However, it has also been found in low elevation areas, such as the Moravia and Prague regions in the Czech Republic and the Olkusz upland in Poland. It has been recorded in both calcareous regions, such as the Olkusz upland, Tatras, and Alps, and on acid, volcanic bedrocks, for example, the Stolicke vrchy in Slovakia (Glejdura, 2013) and the Sudetes.

New Localities (Figure 1B)

Gd-59 CENTRAL WESTERN CARPATHIANS, Western Tatra Mts: Tatra National Park: left slope of Strążyska Valley, on a limestone rock, under Pinus mugo, 1,130 m a.s.l., 2019-10-14, leg. M. Kozak & J. Brańka, det. P. Mleczko, KRA F-TPN/19/0056.

Notes

The species was described by Lange in 1957, who based its description on the specimen collected by Franz Petrak in Moravia. Because of the peculiar bullet-shaped thick-walled pigmented spores, it was believed to occupy a transitional position between the genera Rhizopogon and Melanogaster (Lange, 1957; Martín, 1996; Trappe, 1975). In the monograph of the European species of Rhizopogon, Martín (1996) included R. melanogastroides in this genus; however, phylogenetic analysis based on the ITS nrDNA region suggested that the taxon should be placed outside Rhizopogon (Martín & Raidl, 2002). The results of molecular studies as well as the features of the ectomycorrhizas were arguments against including this species in the genus Melanogaster. Indeed, although peculiar due to the presence of globular cells in the outer mantle, the ectomycorrhizas of R. melanogastroides share some important features with other Rhizopogon species, that is, a lack of sclerotia, clamps, and globular to capitate cystidia (typical for Melanogaster ectomycorrhizas) and the presence of a gelatinous matrix in the outer mantle (Agerer, 2006). In the phylogenetic analyses based on the LSU nrDNA region, performed by Binder and Hibbett (2006), it was found to be nested within the genus Rhizopogon.

This species is extremely rare in Europe. Long known only from the historical type locality in Moravia, in the municipality of Hranice (German: Mährisch Weißkirchen), and in the Moravian Gate between the Carpathians and the Sudetes (Lange, 1957; Martín, 2001), it was then discovered in 1997 in the Bad Tölz-Wolfratshausen District, Bavaria, Germany, in the Northern Limestone Alps (Martín & Raidl, 2002; Raidl et al., 1998) and 10 years later, in 2007, in Cancano, the province of Sondrino, Lombardy, Italy, in the Southern Limestone Alps (Bincoletto, 2014). In all three localities, sporocarps were found in limestone areas under Pinus: in the Czech Republic – in open slopes, under undetermined Pinus species, in a mixed wood dominated by Quercus sp. (Lange, 1957); in Germany, in a loose stand of Picea abies, Pinus sylvestris, P. mugo, and some shrubs (Erico-Pinetum plant association), close to the bank of the river Isar, at 795 m a.s.l. (Martín & Raidl, 2002); in Italy, in an alpine grassland with Dryas octopetala, Salix serpyllifolia, Gentianella ciliata, G. campestris, Leontopodium alpinum, and Chamorchis alpina, at ca. 2,000 m a.s.l. (Bincoletto, 2014). The Polish locality is also placed in an exposed limestone rock with scattered P. mugho at 1,130 m a.s.l. in the mountain valley.

Lange based his description of the new species on exsiccatum, which consisted of one well-preserved sporocarp, deposited in the Botanical Museum of the University of Copenhagen (Museum Botanicum Hauniense). Macromorphological characters were then completed by the description of fresh sporocarps from Germany and Italy (Bincoletto, 2014; Martín & Raidl, 2002; see Table 1). The study of Italian sporocarps revealed a strong dextrinoid reaction of young, hyaline spores that cannot be observed in mature, pigmented ones. Analysis of sporocarps from the Tatra Mts confirms this statement (Table 1, Figure 3D). We also found no bluing reaction of mature sporocarps after touching, reported for the material collected in Germany (Martín & Raidl, 2002), However, we found a reddish peridium reaction after the application of 10% KOH, as reported by Bincoletto (2014), which can also be tested in dry specimens. Macro- and microcharacters of specimens from Tatra Mts are generally in agreement with those presented in previous studies (Table 1, Figure 2C,D, Figure 3C–H).

New Localities (Figure 1C)

Ge-50 CENTRAL WESTERN CARPATHIANS, Western Tatra Mts: Tatra National Park: S slope of Kopieniec Wielki Mt, artificial stand (Alnus incana, Larix sp.) in a calcareous sward representing Seslerion tatrae alliance, 1,300 m a.s.l., 2019-08-26, leg. F. Karpowicz & K. Kozłowska-Kozak, det. P. Mleczko, Filip Karpowicz, KRA F-TPN/19/0006.

Ge-51 CENTRAL WESTERN CARPATHIANS, High Tatra Mts: Tatra National Park: mouth of Waksmundzki Stream, Alnetum incanae association (Alnus incana, Picea), 1,000 m a.s.l., 2019-09-21 (found in two localities), leg. & det. M. Kozak, KRA F-TPN/19/0291, KRA F-TPN/19/0292.

Gf-46 OUTER EASTERN CARPATHIANS, Western Bieszczady Mts: Łubne, mouth of the Kotanica Stream, in Alnetum incanae association (Alnus incana, Tilia, Corylus), 520 m a.s.l., 2012-10-22, leg. M. Kozak & K. Kozłowska-Kozak, det. M. Kozak & P. Mleczko, KRA F-2012-86.

Notes

The taxonomy of the Alnus-associated species of Boletales related to Paxillus, that is, Alpova and Melanogaster, has long been very complicated and unclear due to uncertain descriptions and misleading interpretations of names and species concepts (Moreau et al., 2011). For that reason, reconstruction of the distribution of species in this group is difficult and often requires the study of original collections. This is also true for M. luteus, which is often referred to as Alpova diplophloeus, especially if specimens are identified according to Kers (1986), Knudsen (2012), Montecchi and Lazzari (1989), and Montecchi and Sarasini (2000). Another name used for this taxon in the European keys is M. microsporus (e.g., Eckblad & Lange, 1997).

The features of the Carpathian specimens correspond well with the description published by Moreau et al. (2011). Small, round-to-slightly flattened sporocarps of up to 1.5 cm in diameter without columella, greenish-yellow-to-greenish-brown, a furfuraceous-to-stringy peridium surface, black, deliquescent, mature gleba with whitish-to-pale yellow septa are characteristic macromorphological features of this species (Figure 2B). In the micromorphological aspect, the most distinguishing features are: peridium that is plectenchymatous throughout (pseudoparenchymatous in the inner layer in Alpova) (Figure 3A,B), yellow-brown, elongated spores 5.3–6.8 × 2.4–3.3 μm with remnants of hyaline sterigmata at their bases (Figure 2G,H), basidia with thin walls and lack of spherical “supporting cells” in the gleba (characteristic for Alpova spp.). The closely related species M. rivularis, known to date only from Corsica, differs in bigger sporocarps, over 1.5 cm in diameter, with distinct columella and basidia with thick walls at their apices (Moreau et al., 2011).

The presence of M. luteus was confirmed in France, Italy, Montenegro, and Scandinavia; however, it is most likely to be more frequent but rarely searched for (Moreau et al., 2011). The only confirmed localities in Central Europe are those in Slovakia (nahuby.sk, 2020), and now its presence has been confirmed in Poland in the Central Western and Outer Eastern Carpathians. The Polish locality in the Bieszczady Mts is the most extreme eastern location known so far. The most frequent mycorrhizal partner of M. luteus is Alnus incana in alluvial places in rivers or stream banks in mountainous areas (Moreau et al., 2011).

Figure 1

Distribution maps of three hypogeous fungi in Poland: (A) Leucangium carthusianum; (B) Rhizopogon melanogastroides; (C) Melanogaster luteus. The points correspond to the ATMOS squares with localities (see the lists of localities). White dots – new localities; black dot – known locality.

Figure 2

Sporocarps and spores of hypogeous fungi: (A) Sporocarp of Leucangium carthusianum; (B) sporocarps of Melanogaster luteus; (C,D) mature (C) and immature (D) sporocarps of Rhizopogon melanogastroides; (E) spores of L. carthusianum; left – spore from fresh specimen, right – spore from dry specimen (8-years old); (F) ascus of L. carthusianum; (G,H) spores of M. luteus. Scale: (A–D) 10 mm; (E–H) 10 μm. Photo: (A–D) M. K.; (E–H) P. M. (A) KRA F-TPN/19-0357; (B,G,H) KRA F-TPN/19-0006; (C,D) KRA F-TPN/19-0056; (E,F) KRA F-2012-38.

Figure 3

Micromorphological structures of hypogeous fungi: (A,B) Cross section of outer (A) and middle (B) peridium layers of Melanogaster luteus; (C,D) mature (C) and immature (D) spores of Rhizopogon melanogastroides (left – in water, right – in Melzer’s reagent); (E) basidia of R. melanogastroides (first from the left – immature basidium); (F) section of dissepiment of R. melanogastroides; (G,H) section ofthe inner (G) and outer (H) peridium layers of R. melanogastroides. Scale: 10 μm. Photo: P. M. (A,B) KRA F-TPN/19-0006; (C–H) KRA F-TPN/19-0056.