Hebelomina neerlandica, a new species for Ukraine and considerations about the genus Hebelomina

Hebelomina neerlandica Huijsman has been found near Kiev (Ukraine). It is an addition to the Ukrainian mycoflora. The specimens are described and illustrated. A synopsis of the genus Hebelomina is presented, with comments on the systematics and the distribution of its different species, which are all very rare.


INTRODUCTION
During a mycological excursion in a forest near Novobilychi (Kiev, Ukraine), a whitish gilled mushroom has been observed.It was growing on a dead log of Pinus sylvestris lying on the ground.Several sporophores have been collected.Their characters are typical of Hebelomina neerlandica Huijsman, a.o. the general habit, whitish colour, ecology, size and shape of the cheilocystidia, size and shape of the spores, which are smooth, whitish and dextrinoid.This species has never been reported from Ukraine.A short description of the specimens is given below.
Up to now, six species have been described in the genus Hebelomina, most of them are extremely rare or even known only by the type specimens.The taxonomic position of the genus and its species is still under discussion.The nomenclature is also quite complicated.A summary of the data concerning those questions is presented here as well as a list of the descriptions and illustrations published for the different species, an overview of their worldwide distribution and an identification key.

DESCRIPTION OF THE UKRAINIAN COLLECTION
Sporophores completely whitish, drying ochraceous, sometimes with a rather dark rusty brown spot.Pileus 12-22 mm broad, convex with involute margin, smooth, moist, not viscid.Lamellae adnate.Stipe 12-25 x 2-4.5 mm, central, cylindrical, curved, without annulus, small remnants of a cortina-like velum sometimes visible on young specimens.Context whitish.No particular smell detected.Taste not tested.
ECOLOGY.Sporophores not caespitose, growing on a fallen dead trunk of Pinus sylvestris, in a forest of Pinus sylvestris with numerous Quercus robur, on podsolic sand.SPECIMEN DESCRIBED.Ukraine, Kiev, forest near Novobilychi, 14. IX. 2004.Herbarium A. Fraiture 2927 (BR), double in herb.V. Hayova (KW 29993).The taxonomic position of the genus Hebelomina is not easy to circumscribe and the question has been treated by several authors.The most argumented discussion is probably the one proposed by S i n g e r (1986: 611), who finally decides to accommodate the genus in the Cortinariaceae, where he assumes it is related to Cortinarius and Leucocortinarius or, more probably, to Hebeloma.The difficulty in positioning the genus in the systematics is partly due to its very specific characters, a.o. the spores which are whitish, smooth, thick walled, devoid of a pore and dextrinoid.
As it will be seen hereunder, the problem also lies in the fact that the genus Hebelomina is heterogenous.H. domardiana, type species of the genus Hebelomina, seems to be a white spored Hebeloma.Consequently, the genus Hebelomina has been recently included in Hebeloma (Ve s t e r h o l t 2005).However, it will not be possible to transfer to Hebeloma all the species described in Hebelomina.Molecular analysis (M o n c a l v o et al. 2002: 367, 379) has shown that Hebelomina neerlandica is probably a Gymnopilus.Those authors extend however improperly their conclusions to the whole genus Hebelomina.
? Hebelomina amazonensis Sing. 1979, in Singer and Araujo, Acta amazonica 9 (1): 32 [invalid: nomen nudum].This is a simple mention of the name, without any description or citation of a specimen.S i n g e r did not cite the name in his Agaricales in Modern Taxonomy, ed. 4 (1986) and one may thus suppose that he did not believe anymore in the value of this taxon.M a i r e (1935), in the first lines of his paper, already says that H. domardiana is «un Champignon très remarquable, ayant l'aspect extérieur d'un Tricholoma, mais qui est, en réalité, un Hebeloma à spores incolores».The great mycologist also points out that the genus Hebelomina «est aux Hebeloma ce que le genre Cortinellus [ Leucocortinarius] est aux Cortinarius».He adds in his comments that the amygdaliform spores, with an epispore rigid and thin but looking double, becoming violaceouspurple by iodine when young, the edge of the gills entirely covered with filamentous subclaviform and very dense hairs and even the faint raddish smell and the bitterness of the flesh are characters of Hebeloma.It is possible to add other characters corresponding with the genus Hebeloma: big spores (11-15 x 8 μm) with a clearly papil-late top, white cap becoming reddish brown in the centre, white stem very pruinose under the gills ("valde pruinosa", in italics in the latin diagnosis), tricholomoid habit and terricolous ecology.G e n n a r i (2003) says "su legno di Quercus suber", but the original description gives no indication concerning lignicolous ecology.Moreover, Maire compares his species with Hebeloma and Tricholoma and tells that, at first sight, he took it for Hygrophorus eburneus var.pseudodiscoideus; all of those fungi are terricolous.

Hebelomina domardiana
Molecular analysis recently confirmed the intuition of Maire and showed that, despite its white spores, Hebelomina domardiana probably belongs to the genus Hebeloma, where it occupies however a "very isolated position" (Ve s t e r h o l t 2005).
Unfortunately, it seems that the type specimen, collected by Maire, has not been preserved or is lost.Therefore, Vesterholt had to undertake molecular study of material collected in Estonia.The species has also been reported from Lithuania and Latvia (U r b o n a s , K a l a m e e s , L u k i n 1986).If there is no problem to admit that the different collections from the three Baltic states belong to the same taxon, it is less easy to believe that a species growing in the Baltic states can also be present in a Quercus suber wood in Algeria, especially for a taxon which is most probably mycorrhizal.If the type material can not be found again, it would be interesting to make a new collection of the species in its original growth place or in a Quercus suber wood of the Mediterranean region.
DISTRIBUTION: ALGERIA: Forêt de l' Alma, 15. XII. 1933, under Quercus suber (Maire 1935).Maire says "Mauritaniae" but l'Alma is situated about 40 km to the east of Alger; its name is now Boudouaou (P.Bertea and J.F. Trimbach, comm. pers.).No herbarium specimen is formally cited in the protologue.After H o r a k (1968: 266) and H u i j s m a n (1978: 487), the type specimens have been lost.ESTONIA: Surju, 28.VIII. 1989, in  DESCRIPTIONS AND ILLUSTRATIONS: N a t a r a j a n and R a m a n (1980, original description and line drawings of the specimens, spores and basidia).The text and the illustrations, except the latin description, are reproduced in N a t a r a j a n and R a m a n (1983: 137 138 et Fig. 22,  e g).
The classification of this species is very unclear.The limoniform and rather big spores (7-11.2x 5.6-8.4μm) are quite typical of Hebeloma while the presence of rhizomorphs at the base of the stem indicates rather a saprotrophic species growing on litter or in connection with wood.On the other hand, the reddish-brown to orange-brown colours are rather resembling the genus Gymnopilus.Moreover, the lack of cheilocystidia corresponds neither with Hebeloma nor with Gymnopilus and therefore H. maderaspatana could belong to another genus.DISTRIBUTION: INDIA: campus of the Indian Institute of Technology, Guindy (Madras), 23.VIII. 1978, on ground, in groups, coll. N. Raman (MUBL 2421, paratypus) Ibid., 3.XI.1978,on lit ter, in groups, coll.N. Raman (MUBL 2420, holotypus) (N a t a r a j a n , R a m a n 1980, 1983).A. Gennari "2002", publ. 2003, Riv. Micol. 45 (4): 312.

Hebelomina mediterranea
DESCRIPTIONS AND ILLUSTRATIONS: G e n n a r i (2003, original description and colour photo graph of the specimens, spores, cheilocystidia and epicutis; line drawings of the spores, ba sidia, cheilocystidia and epicutis).
The big limoniform to subamygdaliform spores, measuring 9-11 (-12) x 6-8 (-8.5) μm, the subclavate to cylindrical cheilocystidia, the milky white cap, with a cream ochraceous centre, the stem pruinose on the apex, the tricholomatoid habit and the terricolous ecology are connecting the species with the genus Hebeloma.It is very probable that its pertaining to this genus will be demonstrated.
The species appears to be very close to H. domardiana.The comparison of the descriptions (G e n n a r i 2003; M a i r e 1935; U r b o n a s 2005; Ve s t e r h o l t 2005) shows only a few differences between the two species.The specimen of H. mediterranea is more robust than H. domardiana (cap diameter 5-7 cm versus 2.5-4 cm) and its spores are slightly shorter: 9-11 (-12) μm instead of 11-15 or 10.7-13.4μm.Gennari also mentions a germ-pore ("poro germinativo evidente") and represents it on his drawings.However, true germ-pores have not been described in Hebeloma and the structures seen by Gennari correspond probably with a callus rather than a pore (S i n g e r 1986; Pe g l e r , Yo u n g 1971; M e l é n d e z -H o w e l l 1967).The description of Gennari is based on a single collection and can not provide any idea of the variability of the species.In conclusion, we consider as possible that H. mediterranea could be conspecific with H. domardiana.DESCRIPTIONS AND ILLUSTRATIONS: A l e s s i o , N o n i s (1977, original description, aquarelles and photographs of the specimens).Note: A l e s s i o (1981) mentions that the colours of the plate have not been accurately reproduced, that the aquarelles are actually of a very pale cream ivory ochre with which contrast much more coloured patches, reaching the «terra cot ta» colour; he also says the red colour of the photographs is too marked and diffuse.
The affinities of this taxon are difficult to circumscribe.The fusoid to cylindrical cheilocystidia, the top of the stem slightly white pruinose and the creamy white cap, becoming pale ochre and finally slightly brownish with irregular pale clay-orange patches are characters of Hebeloma.But, on the other hand, the ovoid to amygdaloid spores, measuring 6-8 (-9) x 4-4.5 μm, and the lignicolous ecology are rather in favour of the genus Gymnopilus.DESCRIPTIONS: G a r n w e i d n e r (1996), H u i j s m a n (1946, 1978, original  The publication of a valid name for this taxon has not been easy.The species is first described by H u i j s m a n (1946), under the name Hebelomina microspora.Unfortunately, no Latin diagnosis is provided and the name is thus invalid (Art.36.1).
About thirty years later, A l e s s i o and N o n i s (1977) publish a latin diagnosis in order to validate the name created by Huijsman.However, they choose another type than the specimen cited by Huijsman and, consequently, at a nomenclatural point of view, they create a new taxon.On the other hand, as pointed out by different authors (a.o.H u i j s m a n 1978; N e v i l l e , Ro u x 1997), there are several morphological differences between the two specimens : the Italian collection has a inocyboid habit, reddish brown colours on the pictures, amyloid spores and twice bigger cheilocystidia.Therefore, they probably belong to two different taxa at a systematic point of view as well.That hypothesis is not accepted by A l e s s i o (1981), who believes that a single taxon is involved.We consider that conspecificity possible, while unlikely.
A few months after A l e s s i o and N o n i s (1977) and H u i j s m a n (1978) also decides to validate his species by publishing a Latin diagnosis.His paper is at the point to be sent to the printer when he discovers the "validation" made by Alessio and Nonis.He publishes nevertheless his own "validation" (which is illegitimate: later homonym, Art.53.1) but, thinking that his fungus is not the same that the one of the Italian authors, he adds, at the end of his text, a note in which he proposes Hebelomina neerlandica as a new name for his species.Would the synonymy be proven in the future, then the species should be named H.microspora Alessio and Nonis and H. neerlandica would be reduced to a superfluous synonym.
Finally, S i n g e r (1986), reading the H u i j s m a n (1978) paper, overlooks its final note and introduces Hebelomina huijsmaniana as a new name to replace H. microspora Huijsman.The name published by Singer is illegitimate (superfluous name, Art.52.1).
The nomenclatural changes are not finished yet.The species will probably be transferred to the genus Gymnopilus, since molecular analyses have shown that the species is likely a white spored Gymnopilus, rather close to G. penetrans (M o nc a l v o et al. 2002: 367, 379).Regarding the macro-and microscopic characters of the species as well as its ecology on Pinus wood, it seems reasonable to consider H. microspora as a whitish Gymnopilus, with white and smooth spores.Within that genus, the absence of a membranous ring, the relatively small size of the spores and the growth on coniferous wood correspond with the group of G. stabilis, G. sapineus, G. penetrans and G. hybridus.The status of the three last species is still uncertain and varies considerably in the recent literature: three (M o s e r 1983; O r t o n 1993) or two independent species (H o l e c 2005) or one single species (H ø i l a n d 1990).
«De Fonteintjes», south of Rijssen, 1988, under Picea abies, coll. C. Bas, and1990, leg The authors of the species point out that H. pallida is close to H. neerlandica and they list the following characters to separate the two species: the carpophores of H. pallida have a white colour remaining nearly unchanged during their whole life, they are completely devoid of a veil even in very young stage, they have bigger and non amygdaliform spores and they grow on dead wood of Eucalyptus.Those differences are not much significative.H. neerlandica is also a whitish species and the colour modifications described by Huijsman (becoming pale ochraceous-aluta-ceous, often more or less mixed with incarnate) may considerably vary depending on ecological conditions.The veil of that species is fugacious and often difficult if not impossible to see.As for the spore size, the figures are indeed a bit bigger: 7.5-9.0(-10.3)x 5.2-6.0 (-6.9) μm for H. pallida versus 6.5-7.8 x 4.2-4.6 μm for H. neerlandica (H u i j s m a n 1978), but some collections of the latter species have shown bigger spores (a.o.Vo l d e r s 1997).The difference between the two species is mainly significative for the spore width.Since the estimation of the spore length/width ratio (Q) for H. pallida is about 1.47 when calculated on the spore size reported by C o n t u , D e s s i (1993) and about 1.77 when calculated after the drawings provided by the same authors, it seems possible that the spore size given by Dessi and Contu is not perfectly accurate.The habitat on Eucalyptus wood is indeed unusual but not sufficient to create a new species.In conclusion, we think that H. pallida is very close to H. neerlandica and even possibly conspecific with that species.............................................................................................................. H. neerlandica 5) Spores 5.2 6.0 ( 6.9) μm wide.Carpophores whitish and remaining so.On Eucalyptus wood.December January.

SUMMARY AND CONCLUSIONS
The genus Hebelomina is heterogenous.It can be divided into at least two groups of species.
1) The hebelomoid species (H.domardiana and H. mediterranea).They are terricolous and probably ectomycorrhizal, with a tricholomoid or hebelomoid habit, a stem which is pruinose in its upper part, rather big spores (usually above 9 x 6 μm), more or less citriform or amygdaliform with a papillate top, cheilocystidia usually irregularly cylindrical or clavate, eventually narrowly lageniform but not lecythiform.Both species have been described from Mediterranean oak forests but, rather unexpectedly, the first one has also been reported from the three Baltic countries, in pine forests and in mixed forests.The two species are very close to the genus Hebeloma.This has been recently confirmed by molecular analysis for H. domardiana (specimen from Estonia), which has consequently been transferred to that genus (Ve s t e r h o l t 2005).We suggest that the two species are close to each other and even possibly conspecific.On the other hand, the Baltic collections attributed to H. domardiana could belong to a separate, undescribed species of this group.
2) The gymnopiloid species (H.neerlandica, H. pallida and probably H. microspora).They are lignicolous and saprotrophic, with a gymnopiloid habit, a stem not or only slightly pruinose, medium sized to small spores (usually under 9 x 6 μm), which are amygdaliform, ellipsoid or ovoid and neither citriform nor papillate; the cheilocystidia are usually narrowly lecythiform.Most of the collected specimens of H. neerlandica were growing on coniferous wood, mainly Pinus sylvestris, but also P. nigra, Larix decidua and Picea abies; there are two reports on Salix in Great Britain.H. microspora has been observed on wood of Pinus strobus and P. pinaster.H. pallida is only known from the type collections, on wood of Eucalyptus camaldulensis.By its morphological characters, H. neerlandica is very close to Gymnopilus.This has been confirmed by molecular analysis (M o n c a l v o et al. 2002) and the species will probably be transferred to that genus.H. pallida is very close to H. neerlandica and could even be conspecific.We believe that H. microspora belongs to this same group; however, its taxonomic position is less easy to interpret.
3) Incertae sedis (H.maderaspatana).This species exhibits characters from the two groups cited above and, besides, the lack of cheilocystidia does not fit with the genera Hebelomina, Hebeloma and Gymnopilus.The taxonomic position of the species is thus still unclear.
In conclusion, it seems probable that most of the species of the genus Hebelomina will be transferred to either Hebeloma or Gymnopilus and that the genus Hebelomina will disappear.It is nevertheless noteworthy that most of the species described in Hebelomina share some original characteristics which separate them from those two genera.The carpophores are often whitish or very pale, at least when young.The spores are very particular, being whitish and smooth under the light microscope when the spores in Hebeloma and Gymnopilus are brown and rather coarsely ornamented.It seems that it is difficult to obtain a good spore print because the spores, while being usually produced in large amount, are remaining on the gills.When it was possible to obtain a spore deposit from a Hebelomina collection, it has been observed that it was not pure white but very pale brownish.The pictures of the spores of H. neerlandica, seen by SEM (Fig. 2) show a kind of shallow ornamentation although it could be an artefact due to insufficient reinflation.The presence of those special features in the different Hebelomina species could be explained by a mutation, inducing the loss of pigmentation of the carpophores and changing the brown and ornamented spores of Hebeloma and Gymnopilus into whitish and smooth "hebelominoid" spores.
Maire 1935, Bull.Soc.Hist.nat.Afrique du Nord 26: 13. ≡Hebeloma domardianum (Maire) Beker, Eberhardt and Vesterholt 2005, in Vesterholt, The genus Hebeloma: 102 [note: this is probably the correct name of the species].DESCRIPTIONS: M a i r e (1935, original description), Ve s t e r h o l t (2005), U r b o n a s (2005: 174).ILLUSTRATIONS: M a i r e (1935, line drawings of the specimens and microscopic characters), Ve s t e r h o l t (2005, aquarelle of the specimen and line drawings of spores and cheilocysti dia), U r b o n a s (2005, pl.21,1: a f, aquarelle of the specimens and line drawings of micro scopic characters).
mixed forest, specimen Ve s t e r h o l t JV89 497 (Ve s t e r h o l t 2005: 133).LATVIA: on humus in pine forests; no locality and no collecting date indicated (U r b o n a s et al. 1986: 71).G e n n a r i (2003) men tions a personal communication from Kalamees, after which the collections have been lost.After N e z d o i m i n o g o (1996), those records are quite doubtful.LITHUANIA (U r b o n a s 2005: 174): Rūdininkų, Šalčininkų distr., 03.VIII.1974, in mixed forest with Pinus, young Quercus and Betula.Viešvilés reserve, Jurbarko distr., 19.VII.2000,young Picea abies forest.Biržų forest, Biržų distr., 16.VIII.2001,in mixed forest.See also U r b o n a s et al. (1986: 71, cf.comments given here above for Latvia)Hebelomina maderaspatanaNatarajan and Raman 1980, Kavaka 8: 72.
description), N e v i l l e , Ro u x (1997), S p o o n e r (1993), Vo l d e r s (1997), U r b o n a s (2005).ILLUSTRATIONS: A n o n y m o u s (2003, colour photograph of the specimens), G a r n w e i d n e r (1996, colour photograph of the specimens and line drawings of spores and cheilocystidia), H u i j s m a n (1946, line drawings of microscopic characters of the typus; 1978, line drawings of the type specimens), N e v i l l e and Ro u x (1997, colour photograph and line drawings of microscopic characters), S p o o n e r (1993, line drawings of spores and cheilocystidia), Vo l d e r s (1997, line drawings of microscopic characters; the author also mentions a slide JVDM 7677 and an aquarelle O. Van De Kerckhove 295, BR, both unpublished), U r b o n a s (2005, line drawings of microscopic characters).
. W. Ligterink (L) (unpublished data, cited fide Vo l d e r s 1997; A r n o l d s , K u y p e r and N o o r d e l o o s 1995; see also the distribution map in A n o n y m o u s 2000).UKRAINE: forest near Novo bilychi (Kiev), Kiev obl., 14.IX.2004, on dead log of Pinus sylvestris lying on the ground, herb. A. Fraiture 2927 (BR) and V. Hayova (KW 29993) (this publication).UNITED KINGDOM: Surrey, Oxshott Heath, nr bog N of Sandy Lane, 14.X.1984, under Pinus and Betula on damp sandy ground, coll.L. Spooner (K) Ibid., 13.X.1991, on dead twig in litter, herb.Kew (K) (S p o o n e r 1993).South Hampshire, 1999, clustered on fallen branch of Salix (BMSFRD n°480383).North Hampshire, 1999, on mossy fallen branch of Salix in broadleaf semi natu ral woodland (BMSFRD n° 493526) (British Mycological Society Fungus Record Database).Hebelomina pallida Dessi and Contu 1993, in Contu and Dessi, Micol.Veget.Medit.8 (2): 104.DESCRIPTIONS AND ILLUSTRATIONS: C o n t u , D e s s i (1993, original description, with colour photograph [the legend of which erroneously mentions (Hebelomina candida) and habit sketch of the carpophores and line drawings of the spores, basidia and cheilocystidia).