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Squamanitain Britain and Europe
Vol 14 (2)
Squamanita in Britain and Europe Alick Henrici* quamanita is a small genus of parasites on other Agaricales “uniting some of the greatest rarities in the Agaricales” (Ludwig, 2001). It was erected by Imbach in 1946 to accommodate one very distinctive species S. schreieri, the generic name reflecting its squamulose cap and Amanita-like appearance. This had appeared in Switzerland three years running, 1936-38, at three separate sites, causing much surprise and discussion leading to its initial informal publication by its first finder (Schreier, 1938) as ‘Tricholoma X‘ following a suggestion by Konrad. Schreier’s plate is reproduced here as Fig.4. He noted that all three finds had been in the vicinity of Amanita strobiliformis, and that this has a similar but less exaggerated beetroot-shaped stipe base. Nobody suspected a parasitic connection. It wasn’t seen again for another twenty years and then turned up in Germany. There are now at least 10 Squamanita species known worldwide, 7 of them European, 4 British. The British four all have fairly small grey-violet caps. They are: S. contortipes and S. odorata each known from a single British site, S. pearsonii from 3 sites and S. paradoxa from around 25 sites spread over 20 vice-counties. Up until 1999 even S. paradoxa was known in Britain only from single records from Mull and West Kent. These notes have been assembled following the first authentic British collection of S. odorata in 2012, see Leach (2013) in this issue of FM. The coverage here is wider than in my earlier note (Henrici, 2005) that accompanied two articles on Squamanita finds in 2004, but there is inevitably some overlap. This and all recent treatments of Squamanita rely heavily on a landmark review of the genus by Redhead et al. (1994), abbreviated to ‘R94’ when referenced below. That paper, entitled ‘Squamanita contortipes – the Rosetta Stone of a mycoparasitic agaric genus’, put beyond doubt earlier strong suspicions (eg. Reid 1983, Vesterholt 1991) that Squamanita species, as previously understood, were composite organisms, made up of one agaric species growing from a base of parasitized tissue belonging to another agaric host.
Squamanita is the only agaric genus where all species are parasitic on other Agaricales. Asterophora is also wholly parasitic but on Russulales. Collybia (in its restricted sense) and Dendrocollybia fruit largely on Russulales or Polyporales, but only as saprotrophs on their dead remains. The few other agarics in Europe with a parasitic life-style include Volvariella surrecta (on Clitocybe nebularis) and Rhodocybe stangliana (limited to Lyophyllum spp?). This latter is also discussed here as it was originally described in Squamanita. Once Squamanita was known to be parasitic, the evidence for a taxonomic position near Cystoderma disappeared. Was it indeed a good genus at all, rather than just a catch-all for agarics with a parasitic way of life? In several species collections have been found in which some spores become dingy grey while the majority remain hyaline, a phenomenon otherwise unknown in the agarics. A second common feature of many (all?) Squamanita species is their production of chlamydospores (see below) on hyphae that penetrate areas of the host tissue. The authors of R94 cited these two features in support of Squamanita as a natural genus. Now in the DNA era S. odorata and S. umbonata have been confirmed as closely related (Moncalvo et al., 2002). Matheny & Griffith (2010) have added S. paradoxa and show that Squamanita seems after all to be quite close to Cystoderma. Bas (1965) monographed Squamanita long before its parasitic nature was recognised. He coined the term ‘protocarpic tuber‘ for the basal swelling found in most species, now recognised as deformed (galled) material of their host. After the publication of R94 he suggested this term should be replaced by ‘cecidiocarp‘, i.e. ‘galled fruit-body’ (Bas & Thoen, 1998). He also reported that cecidiocarps of S. odorata had been widely found containing large numbers of chlamydospores but no visible Squamanita, and that these “must therefore represent a biologically very important part of the life cycle of S. odorata”. The seeming extreme rarity of all Squamanita species in all countries where they are known raises the question how they manage to survive
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*8 Victoria Cottages, Sandycombe Rd., Richmond, Surrey TW9 3NW
doi:10.1016/j.fldmyc.2013.03.008
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Vol 14 (2) at all. It is suggested in R94 that the chlamydospores (a general term for thick-walled and generally long-surviving propagules) may provide part of the answer. They are a feature shared with Asterophora, so appear to be helpful to the parasitic lifestyle providing continuity and/or an aid to dispersal by insects etc. In Asterophora they develop in chains in the cap or gills of their own fruitbody (often to the exclusion of basidiospores), but in Squamanita they develop on mycelium embedded within the host bulb or stipe. The saprophytic Collybia may achieve the same ends via its sclerotia. Dendrocollybia on dead Russulales employs an additional mechanism: its side-shoots fragment into arthrospores at their tips. It can occur without a terminal cap at all, so again dispensing with basidiospores.
4 Spores amyloid; cheilocystidia present ...........5 – Spores inamyloid or dextrinoid; cheilocystidia absent ...............................................................6 5 Spores ± globose, 5.5–6.5 µm; caps under 1 cm, usually growing singly replacing the host cap (always Galerina?); in Europe in mossy grassland (but the type was on a Galerina on wood); smell faint ....................S. contortipes* – Spores ellipsoid, 5.5–7 x 4–5 µm; caps 1–2 cm, both known collections caespitose on a base of distorted Kuehneromyces tissue on wood; smell aromatic .............................S. fimbriata 6 Stipe short and squat, usually in small dense clumps among lumps of host tissue (these often faintly radishy when cut); basidiospores neither amyloid nor dextrinoid. Smell strong and sweet (‘of grapes‘, ‘amyl acetate’, ‘like Hebeloma sacchariolens’). In parks, gardens and woodlands on sandy or loamy soils. Always growing from Hebeloma spp.?............... ......................................................S. odorata* – Stipe elongated (at least if basal host portion is included): singly or in clumps; basidiospores dextrinoid, though sometimes very weakly; smells various. In poor mossy grassland. Always on Cystoderma? ...................................7
KEY TO EUROPEAN SPECIES (The four species known in Britain are marked with a *.) 1 Spores rough, pinkish en masse; cap ± viscid, ivory to pale pinkish brown; smell mealy. Under conifers, mainly Picea, on calcareous soil in N.Europe. Unknown in Britain. On Lyophyllum spp .........Rhodocybe stangliana – Spores smooth, hyaline; cap dry, fibrillose/ scaly, more strongly coloured; smell not mealy (genuine Squamanita species).........................2
7 Squamanita stipe short and fairly smooth but ‘grafted’ onto the top of a much longer thicker scarcely modified Cystoderma stipe; cap adpressed fibrillose; smell reports differ (see notes below); chlamydospores variable, elongated, ± smooth ...................S. paradoxa* – Squamanita stipe elongated, fusiform, squarrose; cap recurved scaly; smell (at least in the recent Scottish and Welsh collections) ‘strong and unpleasant’; chlamydospores subglobose with pitted surface...S. pearsonii*
2 Cap normally over 3.5 cm, ochre to brown; arising from a large basal bulb of host tissue; spores inamyloid; smell unremarkable. Mainly southerly in Europe, unknown in Britain or Scandinavia......................................................3 – Cap smaller, 0.5–3(-3.5) cm, with violaceous tints; arising from either a basal bulb or the stipe or deformed cap of the host; spores usually amyloid or dextrinoid, if inamyloid then smell strongly aromatic...........................4
SPECIES NOTES Note. All species are described in Ludwig (2001), where many further literature references are cited. Descriptions of the four British species can be found in Watling & Turnbull (1998) and in Funga Nordica (Knudsen & Vesterholt, eds. 2012).
3 Cap ochre-yellow, large, 5–8(–10) cm, scaly; thought to parasitise Amanita echinocephala and/or A. strobiliformis (species of calcareous soils) ...............................................S. schreieri – Cap dull brown, umbonate, 3.5–6 cm, fimbriate; host range unclear, but reported to include Inocybe sp. ......................S. umbonata
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Vol 14 (2) S. contortipes (A.H.Sm. & Stuntz) Heinemann & Thoen 1973 (Fig. 1) Cystoderma contortipes A.H.Sm. & Stuntz 1957 Syn. S. scotica Bas 1965 (nom. prov.) Illust. Lud 81.5 (as 81.4) taken from Stridval & Stridval p.29 Host: In W. North America (Washington State) where it was described, it parasitizes Galerina species (probably G. cerina growing on logs plus at least one other species in grassland). Indeed it was a collection there in 1993 comprising three undoubted Squamanita fruitbodies growing from the distorted cap of an undoubted still partially fertile Galerina that provided the ‘Rosetta Stone‘ that finally revealed the parasitic nature of Squamanita for Redhead et al. in R94 (see their photo p.1813). None of the European reports, from four countries, are definite about the host. The amyloid spores are a key identification feature. – The only British collection was also the first European: Scotland, Easterness, Rothiemurchus, D. Henderson 16.9.1957, one 9 mm fruitbody in mossy grassland without visible host. This was near where the type of S. pearsonii had been
collected in 1950. Both had been deposited in the Edinburgh herbarium as S. odorata until reassessed by Bas (1965) who described it provisionally as S. scotica, though too meagre and lacking in field notes for formal publication. This collection has also so far resisted attempts to extract DNA (Gareth Griffith, pers. comm.). Synonymy with S. contortipes was suggested in R94 despite the absence of host information. This hypothesis was supported when further European collections were found. - Stridvall & Stridvall (1994) reported it from eight sites in southern Sweden 1990-93 in poor grassland among the moss Rhytidiadelphus squarrosus, sometimes in quantity. Their material resembled a miniature S. paradoxa but grafted onto a paler smooth stipe, thus affecting its host in a very different manner from the key collection that gave rise to R94. It is the smallest known Squamanita species and they warned that it can grow among Mycena aetites and superficially resemble that species when seen from above. It has also been reported from the Netherlands in dune grassland and from Germany where it was first found with at least four Galerina species and Cystoderma amianthinum all nearby (Krieglsteiner, 2000). S. fimbriata Gulden, Bendiksen & Brandrud 1977 Illust. Agarica 28: 7,8 (2009), SZP 87(4):163 (2009) Host: Kuehneromyces spp. – Known from just two collections, both on Picea logs in June on large fruitings of Kuehneromyces: Norway (Oppland) 1976 on K. lignicola and Switzerland (Canton Ticino) in 2008 on K. mutabilis. Named for its fimbriate cheilocystidia. The Norwegian site had 40–50 specimens growing along a log, originally said to be on K. mutabilis. A 3 ha zone was established around it to save it from logging, but it never reappeared. The Swiss collection is fully described in English in the Norwegian journal Agarica jointly by the finders of both collections (Cervini et al. 2009). Their account opens with the words “To find a Squamanita is quite an adventure; to find S. fimbriata is a unique adventure”. It stresses the ecological similarities between the two widely separated sites. This same collection received two further write-ups in Swiss and Italian journals.
Fig. 1. Squamanita contortipes, two fruitbodies at right growing on a Galerina. Stützerbach, Germany, 2007. Photo © Andreas Gminder.
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Vol 14 (2) S. odorata (Cool) Imbach ex Bas 1965 Lepiota odorata Cool 1918 Excluded: Tricholoma odoratum sensu Pearson, S. odorata sensu New Check List 1960. These both = S. pearsonii. Illust. B&K4 261, C&D 647, Lud 81.4A/B, FM14(2): 53–55 and back cover. Host: Vesterholt (1991) reported that nine of ten recent Danish collections were all with Hebeloma mesophaeum on which it appeared to be parasitic. Mondiet et al. (2007) have extracted DNA from the host of a French collection and it was indeed H. mesophaeum. Future collections on other Hebeloma hosts must remain a possibility. – The first Squamanita found in Europe. Described from the Netherlands, where found in several places in 1916 and 1917, rising to c.20 sites known to Bas (1965) who wrote “The simultaneous discovery of such a remarkable fungus from several places in the country caused some sensation among the Dutch mycologists, especially after it appeared that it was unknown to such famous mycologists as Patouillard and Ricken”. Unknown outside the Netherlands until a ‘forma bispora’ was described from Denmark in 1953. – Now also known from Norway, Sweden, France, Germany, Switzerland, and in 2012 England - see Leach (2013) in this issue of FM. Moser (1983) had earlier wrongly reported it as British, misled by a painting of Dutch material in Pearson (1952)
where the material that eventually became the type of S. pearsonii was wrongly assigned to this species. – Several recent collections have been from ruderal habitats, eg. mossy lawns near planted conifers in city parks and gardens. S. paradoxa (A.H.Sm. & Singer) Bas 1965 (Fig. 2) Cystoderma paradoxa A.H.Sm. & Singer 1948 Illust. FN6(1): 11, FN10(1): 2, Lud 81.2 ?Syn. S. basii Harmaja 1988 (spores lacking any dextrinoid reaction) ?Syn. S. umbilicata Harmaja 1988 (with umbilicate pileus) Host: Normally Cystoderma amianthinum, DNA confirmation from a Welsh collection in Matheny & Griffith (2010). Eriksen (1997) has reported a Danish collection on C. carcharias. – Described from Oregon in a new subgenus Dissoderma of Cystoderma as it was plainly ‘dissident’ as well as paradoxical in appearance. Dissoderma was later raised to a monotypic genus “differing clearly from both Cystoderma and Squamanita, being intermediate between them” (Singer, 1986). The first two finders of this species in Britain both guessed nearer the truth. The lichenologist Peter James found it in Scotland on Mull in 1969 and noted “Curious and anomalous: base seems to be Lepiota amianthina with a mutant cap”. Joyce Pitt found it in West Kent in 1982 and noted “It seems as if another agaric has been grafted onto the stem of
Fig. 2. Squamanita paradoxa. Nine fruitbodies growing in sheep-grazed grassland, Brown Clee Hill, Shropshire, 2 October, 2004. Photograph © John & Denise Bingham.
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Vol 14 (2) Cystoderma amianthinum”. Both collections were written up (Watling 1974, Reid 1983). – Possibly increasing in Britain (though this may only be a by-product of the attention paid in recent years to ‘waxcap grasslands‘). The two records above were followed by a first Welsh record by Shelley Evans from Monmouth in 1996, and a first from N. Ireland by Liz Holden from Antrim in 2003. There are now 25 records on the database (FRDBI) relating to 15 distinct collections, and there have been a few others. At vicecounty level the spread is now at least England (7), Scotland (3), Wales (5), N. Ireland (1). Kibby (2009) remarked on four widely separated British sites within a fortnight in October 2008 (with a fifth subsequently reported). The most prolific areas (though usually only 1–3 infected hosts at a time, and a maximum of 8) have been in Wales and the adjacent county of Shropshire. – Widespread but seemingly rarer elsewhere in Europe. Known from at least the four Scandinavian countries, Holland, France, Germany, Switzerland, Italy and the Czech Republic. – Smell ‘faintly fruity like oranges or of fresh laundry’ (Læssøe, 2008), but ‘intensely perfumed when young becoming foetid with age’ (Watling & Turnbull, 1998), though they add “may be a result of some decomposition of the host”. Several other suggestions have been made. – Various descriptions refer to a universal veil of sphaerocysts when young. This is a useful confir-
matory character, but these in fact stem from the host Cystoderma. S. pearsonii Bas 1965 (Fig. 3) Misapplied names: Tricholoma odoratum sensu Pearson 1952, S. odorata sensu New Check List 1960 Illust. FM6(1): 10, Lud 81.6 (as 81.5) taken from B&K4 262 Host: Believed to be Cystoderma amianthinum. – Described from a Scottish collection by R.W.G. Dennis in grass under Pinus sylvestris, Scotland, Easterness, Rothiemurchus 24.9.1950, initially identified as the first known collection of S. odoratum outside the Netherlands. This conclusion was accepted with doubts by Pearson (1952) who also illustrated a painting of the type collection of S. odorata for comparison. It certainly resembled that species much more closely than anything else then known in Europe and the theory was that the absent basal bulb had been ‘used up‘. Bas (1965) confirmed that it was distinct. A second Scottish collection in Oct. 2004 was reported by Holden (2005) growing in clumps in ‘waxcap lawns‘ near Aberdeen among much Cystoderma amianthinum. Her photo agrees remarkably closely with Dennis’s painting of the type collection. There has since been one Welsh collection (Caernarvonshire, Tregarth, 2007), now in the Edinburgh herbarium. – Little known but also recorded from eg. Denmark, France, Spain, Germany and
Fig. 3. Squamanita pearsonii collected by John Harold, Caernarvonshire, Tregarth, Wales, 2007. Photograph © Charles Aron.
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Vol 14 (2) Switzerland. – It is probably closer to S. paradoxa (still without published European records when Pearson found it) than to S. odorata. Could it be merely a form of that species, developing at an earlier stage in the development of its C. amianthinum host and so lacking a Cystoderma stipe base? The scaly cap and especially the pitted globose chlamydospores appear to establish conclusively that it is distinct. S. schreieri Imbach 1946 (Fig. 4) Squamamanita schreieri Imbach 1942 (gen. inval.) Illust. C&D 648, Lud 81.1 taken from B&K4 263 Host: Amanita spp, found on calcareous soil associated with A. echinocephala and A. strobiliformis. – Singly or up to five fruitbodies from a common bulb. Cystidia not found on the type, but present on three other more recent Swiss collections fide B&K4. This removes a key distinction from S. umbonata. – Described from lowland Switzerland. Also known from France, S. Germany, Italy, Austria, Hungary, Ukraine, in all cases very rarely. – Listed in error on the first provisional British Red Data List (Ing, 1992) and hence listed as British by C&D.
Fig. 4. Squamanita schreieri illustrated (as Tricholoma X) in Schreier (1938). Photo courtesy of The Royal Botanic Gardens, Kew.
S. umbonata (Sumst.) Bas 1965 (Fig. 5) Vaginata umbonata Sumst. 1914 Illust. C&D 649, Lud 81.3A, 81.3B taken from Cetto Vol.5/1701 Host: Largely unknown, but reported once on Inocybe oblectabilis. – Distinguished from S. schreieri in Bas (1965) and in R94 by presence of cystidia. If this doesn’t work (see above) then less sharply distinguished by the dull brown fimbriate rather than scaly cap, sometimes sharp umbo and seemingly different hosts. – Described from USA in 1914. First European record N. Italy (Novara) 1979 in Castanea woodland on sandy soil; Cetto 1701 is from a second site 15 km away three years later. Reported again from Italy in 1997 growing from Inocybe oblectabilis. Also known from Spain and ?France. A 1990 German record from near the Czech border was believed to be the first from north of the Alps.
Fig. 5. A fruit body of Squamanita umbonata. Huayacocotla, Veracruz, Mexico. 10 February 2010. Photograph © Ehecatl (Alonso) ex Wikimedia.
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Vol 14 (2) Rhodocybe stangliana (Bresinsky & Pfaff) Riousset & Joss. ex Baroni 1981 (Fig. 6) Squamanita stangliana Bresinsky & Pfaff 1968 Illust. B&K4 102, Lud 74.4, Svp22: 25 Host: Lyophyllum spp. Cap 1.5–3(-5) cm, ivory, ageing pinkish brown; stipe concolorous, emerging from a ± volvate base long suspected of belonging to some other species (Læssøe & Rosendahl 1994), and thus looking very Squamanita-like, and indeed first described in Squamanita. Noordeloos (1983) disputed its placement in Rhodocybe but has since included it in the recent merger of the whole of Rhodocybe with Clitopilus (Co-David et al., 2009). Most records from Picea woodland on calcareous soil. – Described from Germany in 1968, also known from France, Switzerland, Italy and the four Scandinavian countries.
S. pearsonii are also known there. Several of the European species are also known in Japan. Only three further species unknown in Europe have been described: S. citricolor Thoen from Zaire, S. granulifera Bas & Læssøe from Ecuador, and S. squarrulosa Ridley from New Zealand. But these three are enough to indicate the possibility of further species being discovered almost anywhere. S. phaeolepioticola Redhead et al. from Japan was only provisionally described in R94 (thought at first to be S. odorata but probably parasitizing Phaeolepiota aurea). S. tropica Bas was also only provisionally described and is best forgotten, being based on a collection from Malaya now lost and never clearly established as parasitic.
Some outstanding issues * All known Squamanita species appear to he narrowly host specific. But the hosts are very Excluded species varied. How did such a state of affairs evolve? Are Squamanita ‘cettoiana’ nom. prov. these the last few descendants of a plurivorous Provisionally named by Moser in his common ancestor surviving precariously on their Kryptogamenflora Edn. 4 (the one with the most favoured hosts? Or have species on one host English translation). It was based on the single somehow from time to time produced spores immature collection illustrated in Cetto Vol.3/855 capable of parasitizing a radically different host? giving the impression of a relative of S. schreieri * Apart from overall rarity, there is the mysteriparasitising Amanita rubescens. Subsequent ous phenomenon exhibited by several species of collections showed that in fact base and cap both popping up over a wide area for two or three belonged to the rare Amanita lepiotoides Barla, years and then disappearing from sight for already illustrated in Cetto Vol.2/390. The decades. This needs an explanation. mistake was corrected in Moser’s 5th edition. * S. odorata persisted at one French site from 1990 to 2003 (Mondiet et al., 2007). I have not Extra-European species heard of S. paradoxa persisting above two years S. paradoxa and S. umbonata were first at any British site. The similarly parasitic described from the USA; S. odorata and Volvariella surrecta recurred on Clitocyhe nebularis for at least five years at a Surrey site in Richmond Park. * Cystoderma amianthinum normally grows singly. This contrasts with the clumps of nine fruitbodies reported by Bingham & Bingham (2005) for S. paradoxa on this host (see Fig. 2) and eight by Holden (2005) for S. pearsonii thought to be on this host. Could the Squamanita mycelium somehow be inducing an abnormal concentration of host mycelium, thus forming a large cecidiocarp favourable to the production of multiple Squamanita fruitbodies? The base of Fig. 6. Rhodocybe stangliana on the deformed remnants of Lyophyllum inolens. In needle litter under pine, Meningen, S. odorata similarly appears to exceed in volume a normal fairly slender Hebeloma Germany, 2008. Photograph © Andreas Gminder. mesophaeum.
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Vol 14 (2) Ongoing research Gareth Griffith, at Aberystwyth University, is making further DNA-based investigations of S. paradoxa, and would much like to receive further fresh material preferably packed in moss. Contact him at [email protected] or phone 01970 622325.
Abbreviations used above BFF8 British Fungus Flora Vol.8 1998 B&K4 Breitenbach & Kränzlin, Fungi of Switzerland Vol.4, 1995 C&D Courtecuisse & Duhem, Mushrooms & Toadstools, HarperCollins, 1995 FM Field Mycology Lud Ludwig, Pilzcompendium, Vol.1 R94 Redhead et al. (1994) - see below Svp Svampe (Danish journal) SZP Schweize Zeitschrift für Pilzkunde
Acknowledgements My thanks to the photographers who generously allowed the use of their photographs.
References
Matheny, P.B. & Griffith, G.W. (2010). Mycoparasitism between Squamanita paradoxa and Cystoderma amianthinum (Cystodermateae, Agaricales). Mycoscience 51: 456-461. Moncalvo, J-M. et al. (2002). One hundred and seventeen clades of Euagarics. Molec. Phylogen. Evol. 23: 357–400. Mondiet, N., Dubois, M.P. & Selosse, M.A. (2007). The enigmatic Squamanita odorata is parasitic on Hebeloma mesophaeum. Mycol. Res. 111: 599– 602. Moser, M.M. (1983). Keys to Agarics & Boleti. English Translation. Roger Phillips. Noordeloos, M.E. (1983). Notulae ad floram agaricinam neerlandicam I–III. Persoonia 12: 29–49. Pearson, A.A. (1952). New records and observations V. Trans. Brit. Mycol. Soc. 35: 97-122. Redhead, S.A., Ammirati J.F., Walker, G.R., Norvell, L.L., and Puccio, M.B. (1994). Squamanita contortipes - the Rosetta Stone of a mycoparasitic agaric genus. Canad. J. Bot. 72: 1 812–1824. Reid, D.A. (1983). A second British collection of Squamanita paradoxa. Bull. Brit. Mycol. Soc. 17: 111-113. Schreier, L. (1938). (Tricholoma X) Ein unbekannte Ritterling?). Schweiz. Zeitschrift für Pilzkunde 16: 96–100. Singer, R. (1986). The Agaricales in Modern Taxonomy, Edn.4. Koeltz. Stridvall, L. & Stridvall, A. (1994). Slaktet Squamanita Imbach i Sverige. Jordstjarnan 15(1): 24–37. Vesterholt, J. (1991). Vellugtende Knoldfold - maske en parasit?. Svampe 24: 11. Watling, R. (1974). Notes on some British Agarics IV. Notes Roy. Bot. Gard. Edinburgh. 33: 325– 331. Watling, R. & Turnbull, E. (1998). British Fungus Flora Vol. 8. Royal Botanic Garden, Edinburgh.
Bas, C. (1965). The genus Squamanita. Persoonia 3: 331–364. Bas, C. & Thoen, D. (1998). Squamanita citricolor, a new species from central Africa. Persoonia 17: 135–139. Bingham, J. & D. (2005). Squamanita paradoxa in Shropshire. Field Mycol. 6(1): 11–12. Cervini, M., Gulden, G., Bendiksen, E. & Brandrud, T.E. (2009). A second find of the mycoparasitic agaric Squamanita fimbriata, and a note on the conservation of its locus classicus. Agarica 28: 6–13. Cetto, B. (1970-93). I funghi dal vero, 7 vols, Saturnia, Trento. Co-David, D., Langeveld, D. & Noordeloos, M.E. (2009). Molecular phylogeny and spore evolution of Entolomataceae. Persoonia 23: 147–176. Eriksen, A. (1997). Another Danish find of Squamanita paradoxa (in Danish). Svampe 35: 55. Henrici, A. (2005). Further notes on Squamanita. Field Mycol. 6(1): 13–14. Holden, E. (2005). Squamanita pearsonii collected in Aberdeenshire. Field Mycol. 6(1): 10-11. Ing, B. (1992). A provisional Red Data List of British Fungi. Mycologist 6(3): 124–128. Kibby, G.G. (2009). Editorial. Field Mycol. 10(2): 38. Knudsen, H. & Vesterholt, J. (eds). (2012). Funga Nordica Edn. 2. Nordsvamp, Copenhagen. Krieglsteiner, L. (2000). Squamanita contortipes neu für Deutschland. Beitr. Kent. Pilze. Mitt. 13: 15–17. Laessøe, T. & Rosendahl, S. (1994). Rhodocybe stangliana, a parasite on other agarics? Mycol. Res. 98: 88–90. Leach, J. (2013). Squamanita odorata found in Britain. Field Mycol. 14(2): 53–55. Ludwig, E. (2001). Pilzkompendium Band 1. Beschreibungen. IHW-Verlag, Germany.
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Squamanita in Britain and Europe Alick Henrici* quamanita is a small genus of parasites on other Agaricales “uniting some of the greatest rarities in the Agaricales” (Ludwig, 2001). It was erected by Imbach in 1946 to accommodate one very distinctive species S. schreieri, the generic name reflecting its squamulose cap and Amanita-like appearance. This had appeared in Switzerland three years running, 1936-38, at three separate sites, causing much surprise and discussion leading to its initial informal publication by its first finder (Schreier, 1938) as ‘Tricholoma X‘ following a suggestion by Konrad. Schreier’s plate is reproduced here as Fig.4. He noted that all three finds had been in the vicinity of Amanita strobiliformis, and that this has a similar but less exaggerated beetroot-shaped stipe base. Nobody suspected a parasitic connection. It wasn’t seen again for another twenty years and then turned up in Germany. There are now at least 10 Squamanita species known worldwide, 7 of them European, 4 British. The British four all have fairly small grey-violet caps. They are: S. contortipes and S. odorata each known from a single British site, S. pearsonii from 3 sites and S. paradoxa from around 25 sites spread over 20 vice-counties. Up until 1999 even S. paradoxa was known in Britain only from single records from Mull and West Kent. These notes have been assembled following the first authentic British collection of S. odorata in 2012, see Leach (2013) in this issue of FM. The coverage here is wider than in my earlier note (Henrici, 2005) that accompanied two articles on Squamanita finds in 2004, but there is inevitably some overlap. This and all recent treatments of Squamanita rely heavily on a landmark review of the genus by Redhead et al. (1994), abbreviated to ‘R94’ when referenced below. That paper, entitled ‘Squamanita contortipes – the Rosetta Stone of a mycoparasitic agaric genus’, put beyond doubt earlier strong suspicions (eg. Reid 1983, Vesterholt 1991) that Squamanita species, as previously understood, were composite organisms, made up of one agaric species growing from a base of parasitized tissue belonging to another agaric host.
Squamanita is the only agaric genus where all species are parasitic on other Agaricales. Asterophora is also wholly parasitic but on Russulales. Collybia (in its restricted sense) and Dendrocollybia fruit largely on Russulales or Polyporales, but only as saprotrophs on their dead remains. The few other agarics in Europe with a parasitic life-style include Volvariella surrecta (on Clitocybe nebularis) and Rhodocybe stangliana (limited to Lyophyllum spp?). This latter is also discussed here as it was originally described in Squamanita. Once Squamanita was known to be parasitic, the evidence for a taxonomic position near Cystoderma disappeared. Was it indeed a good genus at all, rather than just a catch-all for agarics with a parasitic way of life? In several species collections have been found in which some spores become dingy grey while the majority remain hyaline, a phenomenon otherwise unknown in the agarics. A second common feature of many (all?) Squamanita species is their production of chlamydospores (see below) on hyphae that penetrate areas of the host tissue. The authors of R94 cited these two features in support of Squamanita as a natural genus. Now in the DNA era S. odorata and S. umbonata have been confirmed as closely related (Moncalvo et al., 2002). Matheny & Griffith (2010) have added S. paradoxa and show that Squamanita seems after all to be quite close to Cystoderma. Bas (1965) monographed Squamanita long before its parasitic nature was recognised. He coined the term ‘protocarpic tuber‘ for the basal swelling found in most species, now recognised as deformed (galled) material of their host. After the publication of R94 he suggested this term should be replaced by ‘cecidiocarp‘, i.e. ‘galled fruit-body’ (Bas & Thoen, 1998). He also reported that cecidiocarps of S. odorata had been widely found containing large numbers of chlamydospores but no visible Squamanita, and that these “must therefore represent a biologically very important part of the life cycle of S. odorata”. The seeming extreme rarity of all Squamanita species in all countries where they are known raises the question how they manage to survive
S
*8 Victoria Cottages, Sandycombe Rd., Richmond, Surrey TW9 3NW
doi:10.1016/j.fldmyc.2013.03.008
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Vol 14 (2) at all. It is suggested in R94 that the chlamydospores (a general term for thick-walled and generally long-surviving propagules) may provide part of the answer. They are a feature shared with Asterophora, so appear to be helpful to the parasitic lifestyle providing continuity and/or an aid to dispersal by insects etc. In Asterophora they develop in chains in the cap or gills of their own fruitbody (often to the exclusion of basidiospores), but in Squamanita they develop on mycelium embedded within the host bulb or stipe. The saprophytic Collybia may achieve the same ends via its sclerotia. Dendrocollybia on dead Russulales employs an additional mechanism: its side-shoots fragment into arthrospores at their tips. It can occur without a terminal cap at all, so again dispensing with basidiospores.
4 Spores amyloid; cheilocystidia present ...........5 – Spores inamyloid or dextrinoid; cheilocystidia absent ...............................................................6 5 Spores ± globose, 5.5–6.5 µm; caps under 1 cm, usually growing singly replacing the host cap (always Galerina?); in Europe in mossy grassland (but the type was on a Galerina on wood); smell faint ....................S. contortipes* – Spores ellipsoid, 5.5–7 x 4–5 µm; caps 1–2 cm, both known collections caespitose on a base of distorted Kuehneromyces tissue on wood; smell aromatic .............................S. fimbriata 6 Stipe short and squat, usually in small dense clumps among lumps of host tissue (these often faintly radishy when cut); basidiospores neither amyloid nor dextrinoid. Smell strong and sweet (‘of grapes‘, ‘amyl acetate’, ‘like Hebeloma sacchariolens’). In parks, gardens and woodlands on sandy or loamy soils. Always growing from Hebeloma spp.?............... ......................................................S. odorata* – Stipe elongated (at least if basal host portion is included): singly or in clumps; basidiospores dextrinoid, though sometimes very weakly; smells various. In poor mossy grassland. Always on Cystoderma? ...................................7
KEY TO EUROPEAN SPECIES (The four species known in Britain are marked with a *.) 1 Spores rough, pinkish en masse; cap ± viscid, ivory to pale pinkish brown; smell mealy. Under conifers, mainly Picea, on calcareous soil in N.Europe. Unknown in Britain. On Lyophyllum spp .........Rhodocybe stangliana – Spores smooth, hyaline; cap dry, fibrillose/ scaly, more strongly coloured; smell not mealy (genuine Squamanita species).........................2
7 Squamanita stipe short and fairly smooth but ‘grafted’ onto the top of a much longer thicker scarcely modified Cystoderma stipe; cap adpressed fibrillose; smell reports differ (see notes below); chlamydospores variable, elongated, ± smooth ...................S. paradoxa* – Squamanita stipe elongated, fusiform, squarrose; cap recurved scaly; smell (at least in the recent Scottish and Welsh collections) ‘strong and unpleasant’; chlamydospores subglobose with pitted surface...S. pearsonii*
2 Cap normally over 3.5 cm, ochre to brown; arising from a large basal bulb of host tissue; spores inamyloid; smell unremarkable. Mainly southerly in Europe, unknown in Britain or Scandinavia......................................................3 – Cap smaller, 0.5–3(-3.5) cm, with violaceous tints; arising from either a basal bulb or the stipe or deformed cap of the host; spores usually amyloid or dextrinoid, if inamyloid then smell strongly aromatic...........................4
SPECIES NOTES Note. All species are described in Ludwig (2001), where many further literature references are cited. Descriptions of the four British species can be found in Watling & Turnbull (1998) and in Funga Nordica (Knudsen & Vesterholt, eds. 2012).
3 Cap ochre-yellow, large, 5–8(–10) cm, scaly; thought to parasitise Amanita echinocephala and/or A. strobiliformis (species of calcareous soils) ...............................................S. schreieri – Cap dull brown, umbonate, 3.5–6 cm, fimbriate; host range unclear, but reported to include Inocybe sp. ......................S. umbonata
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Vol 14 (2) S. contortipes (A.H.Sm. & Stuntz) Heinemann & Thoen 1973 (Fig. 1) Cystoderma contortipes A.H.Sm. & Stuntz 1957 Syn. S. scotica Bas 1965 (nom. prov.) Illust. Lud 81.5 (as 81.4) taken from Stridval & Stridval p.29 Host: In W. North America (Washington State) where it was described, it parasitizes Galerina species (probably G. cerina growing on logs plus at least one other species in grassland). Indeed it was a collection there in 1993 comprising three undoubted Squamanita fruitbodies growing from the distorted cap of an undoubted still partially fertile Galerina that provided the ‘Rosetta Stone‘ that finally revealed the parasitic nature of Squamanita for Redhead et al. in R94 (see their photo p.1813). None of the European reports, from four countries, are definite about the host. The amyloid spores are a key identification feature. – The only British collection was also the first European: Scotland, Easterness, Rothiemurchus, D. Henderson 16.9.1957, one 9 mm fruitbody in mossy grassland without visible host. This was near where the type of S. pearsonii had been
collected in 1950. Both had been deposited in the Edinburgh herbarium as S. odorata until reassessed by Bas (1965) who described it provisionally as S. scotica, though too meagre and lacking in field notes for formal publication. This collection has also so far resisted attempts to extract DNA (Gareth Griffith, pers. comm.). Synonymy with S. contortipes was suggested in R94 despite the absence of host information. This hypothesis was supported when further European collections were found. - Stridvall & Stridvall (1994) reported it from eight sites in southern Sweden 1990-93 in poor grassland among the moss Rhytidiadelphus squarrosus, sometimes in quantity. Their material resembled a miniature S. paradoxa but grafted onto a paler smooth stipe, thus affecting its host in a very different manner from the key collection that gave rise to R94. It is the smallest known Squamanita species and they warned that it can grow among Mycena aetites and superficially resemble that species when seen from above. It has also been reported from the Netherlands in dune grassland and from Germany where it was first found with at least four Galerina species and Cystoderma amianthinum all nearby (Krieglsteiner, 2000). S. fimbriata Gulden, Bendiksen & Brandrud 1977 Illust. Agarica 28: 7,8 (2009), SZP 87(4):163 (2009) Host: Kuehneromyces spp. – Known from just two collections, both on Picea logs in June on large fruitings of Kuehneromyces: Norway (Oppland) 1976 on K. lignicola and Switzerland (Canton Ticino) in 2008 on K. mutabilis. Named for its fimbriate cheilocystidia. The Norwegian site had 40–50 specimens growing along a log, originally said to be on K. mutabilis. A 3 ha zone was established around it to save it from logging, but it never reappeared. The Swiss collection is fully described in English in the Norwegian journal Agarica jointly by the finders of both collections (Cervini et al. 2009). Their account opens with the words “To find a Squamanita is quite an adventure; to find S. fimbriata is a unique adventure”. It stresses the ecological similarities between the two widely separated sites. This same collection received two further write-ups in Swiss and Italian journals.
Fig. 1. Squamanita contortipes, two fruitbodies at right growing on a Galerina. Stützerbach, Germany, 2007. Photo © Andreas Gminder.
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Vol 14 (2) S. odorata (Cool) Imbach ex Bas 1965 Lepiota odorata Cool 1918 Excluded: Tricholoma odoratum sensu Pearson, S. odorata sensu New Check List 1960. These both = S. pearsonii. Illust. B&K4 261, C&D 647, Lud 81.4A/B, FM14(2): 53–55 and back cover. Host: Vesterholt (1991) reported that nine of ten recent Danish collections were all with Hebeloma mesophaeum on which it appeared to be parasitic. Mondiet et al. (2007) have extracted DNA from the host of a French collection and it was indeed H. mesophaeum. Future collections on other Hebeloma hosts must remain a possibility. – The first Squamanita found in Europe. Described from the Netherlands, where found in several places in 1916 and 1917, rising to c.20 sites known to Bas (1965) who wrote “The simultaneous discovery of such a remarkable fungus from several places in the country caused some sensation among the Dutch mycologists, especially after it appeared that it was unknown to such famous mycologists as Patouillard and Ricken”. Unknown outside the Netherlands until a ‘forma bispora’ was described from Denmark in 1953. – Now also known from Norway, Sweden, France, Germany, Switzerland, and in 2012 England - see Leach (2013) in this issue of FM. Moser (1983) had earlier wrongly reported it as British, misled by a painting of Dutch material in Pearson (1952)
where the material that eventually became the type of S. pearsonii was wrongly assigned to this species. – Several recent collections have been from ruderal habitats, eg. mossy lawns near planted conifers in city parks and gardens. S. paradoxa (A.H.Sm. & Singer) Bas 1965 (Fig. 2) Cystoderma paradoxa A.H.Sm. & Singer 1948 Illust. FN6(1): 11, FN10(1): 2, Lud 81.2 ?Syn. S. basii Harmaja 1988 (spores lacking any dextrinoid reaction) ?Syn. S. umbilicata Harmaja 1988 (with umbilicate pileus) Host: Normally Cystoderma amianthinum, DNA confirmation from a Welsh collection in Matheny & Griffith (2010). Eriksen (1997) has reported a Danish collection on C. carcharias. – Described from Oregon in a new subgenus Dissoderma of Cystoderma as it was plainly ‘dissident’ as well as paradoxical in appearance. Dissoderma was later raised to a monotypic genus “differing clearly from both Cystoderma and Squamanita, being intermediate between them” (Singer, 1986). The first two finders of this species in Britain both guessed nearer the truth. The lichenologist Peter James found it in Scotland on Mull in 1969 and noted “Curious and anomalous: base seems to be Lepiota amianthina with a mutant cap”. Joyce Pitt found it in West Kent in 1982 and noted “It seems as if another agaric has been grafted onto the stem of
Fig. 2. Squamanita paradoxa. Nine fruitbodies growing in sheep-grazed grassland, Brown Clee Hill, Shropshire, 2 October, 2004. Photograph © John & Denise Bingham.
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Vol 14 (2) Cystoderma amianthinum”. Both collections were written up (Watling 1974, Reid 1983). – Possibly increasing in Britain (though this may only be a by-product of the attention paid in recent years to ‘waxcap grasslands‘). The two records above were followed by a first Welsh record by Shelley Evans from Monmouth in 1996, and a first from N. Ireland by Liz Holden from Antrim in 2003. There are now 25 records on the database (FRDBI) relating to 15 distinct collections, and there have been a few others. At vicecounty level the spread is now at least England (7), Scotland (3), Wales (5), N. Ireland (1). Kibby (2009) remarked on four widely separated British sites within a fortnight in October 2008 (with a fifth subsequently reported). The most prolific areas (though usually only 1–3 infected hosts at a time, and a maximum of 8) have been in Wales and the adjacent county of Shropshire. – Widespread but seemingly rarer elsewhere in Europe. Known from at least the four Scandinavian countries, Holland, France, Germany, Switzerland, Italy and the Czech Republic. – Smell ‘faintly fruity like oranges or of fresh laundry’ (Læssøe, 2008), but ‘intensely perfumed when young becoming foetid with age’ (Watling & Turnbull, 1998), though they add “may be a result of some decomposition of the host”. Several other suggestions have been made. – Various descriptions refer to a universal veil of sphaerocysts when young. This is a useful confir-
matory character, but these in fact stem from the host Cystoderma. S. pearsonii Bas 1965 (Fig. 3) Misapplied names: Tricholoma odoratum sensu Pearson 1952, S. odorata sensu New Check List 1960 Illust. FM6(1): 10, Lud 81.6 (as 81.5) taken from B&K4 262 Host: Believed to be Cystoderma amianthinum. – Described from a Scottish collection by R.W.G. Dennis in grass under Pinus sylvestris, Scotland, Easterness, Rothiemurchus 24.9.1950, initially identified as the first known collection of S. odoratum outside the Netherlands. This conclusion was accepted with doubts by Pearson (1952) who also illustrated a painting of the type collection of S. odorata for comparison. It certainly resembled that species much more closely than anything else then known in Europe and the theory was that the absent basal bulb had been ‘used up‘. Bas (1965) confirmed that it was distinct. A second Scottish collection in Oct. 2004 was reported by Holden (2005) growing in clumps in ‘waxcap lawns‘ near Aberdeen among much Cystoderma amianthinum. Her photo agrees remarkably closely with Dennis’s painting of the type collection. There has since been one Welsh collection (Caernarvonshire, Tregarth, 2007), now in the Edinburgh herbarium. – Little known but also recorded from eg. Denmark, France, Spain, Germany and
Fig. 3. Squamanita pearsonii collected by John Harold, Caernarvonshire, Tregarth, Wales, 2007. Photograph © Charles Aron.
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Vol 14 (2) Switzerland. – It is probably closer to S. paradoxa (still without published European records when Pearson found it) than to S. odorata. Could it be merely a form of that species, developing at an earlier stage in the development of its C. amianthinum host and so lacking a Cystoderma stipe base? The scaly cap and especially the pitted globose chlamydospores appear to establish conclusively that it is distinct. S. schreieri Imbach 1946 (Fig. 4) Squamamanita schreieri Imbach 1942 (gen. inval.) Illust. C&D 648, Lud 81.1 taken from B&K4 263 Host: Amanita spp, found on calcareous soil associated with A. echinocephala and A. strobiliformis. – Singly or up to five fruitbodies from a common bulb. Cystidia not found on the type, but present on three other more recent Swiss collections fide B&K4. This removes a key distinction from S. umbonata. – Described from lowland Switzerland. Also known from France, S. Germany, Italy, Austria, Hungary, Ukraine, in all cases very rarely. – Listed in error on the first provisional British Red Data List (Ing, 1992) and hence listed as British by C&D.
Fig. 4. Squamanita schreieri illustrated (as Tricholoma X) in Schreier (1938). Photo courtesy of The Royal Botanic Gardens, Kew.
S. umbonata (Sumst.) Bas 1965 (Fig. 5) Vaginata umbonata Sumst. 1914 Illust. C&D 649, Lud 81.3A, 81.3B taken from Cetto Vol.5/1701 Host: Largely unknown, but reported once on Inocybe oblectabilis. – Distinguished from S. schreieri in Bas (1965) and in R94 by presence of cystidia. If this doesn’t work (see above) then less sharply distinguished by the dull brown fimbriate rather than scaly cap, sometimes sharp umbo and seemingly different hosts. – Described from USA in 1914. First European record N. Italy (Novara) 1979 in Castanea woodland on sandy soil; Cetto 1701 is from a second site 15 km away three years later. Reported again from Italy in 1997 growing from Inocybe oblectabilis. Also known from Spain and ?France. A 1990 German record from near the Czech border was believed to be the first from north of the Alps.
Fig. 5. A fruit body of Squamanita umbonata. Huayacocotla, Veracruz, Mexico. 10 February 2010. Photograph © Ehecatl (Alonso) ex Wikimedia.
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Vol 14 (2) Rhodocybe stangliana (Bresinsky & Pfaff) Riousset & Joss. ex Baroni 1981 (Fig. 6) Squamanita stangliana Bresinsky & Pfaff 1968 Illust. B&K4 102, Lud 74.4, Svp22: 25 Host: Lyophyllum spp. Cap 1.5–3(-5) cm, ivory, ageing pinkish brown; stipe concolorous, emerging from a ± volvate base long suspected of belonging to some other species (Læssøe & Rosendahl 1994), and thus looking very Squamanita-like, and indeed first described in Squamanita. Noordeloos (1983) disputed its placement in Rhodocybe but has since included it in the recent merger of the whole of Rhodocybe with Clitopilus (Co-David et al., 2009). Most records from Picea woodland on calcareous soil. – Described from Germany in 1968, also known from France, Switzerland, Italy and the four Scandinavian countries.
S. pearsonii are also known there. Several of the European species are also known in Japan. Only three further species unknown in Europe have been described: S. citricolor Thoen from Zaire, S. granulifera Bas & Læssøe from Ecuador, and S. squarrulosa Ridley from New Zealand. But these three are enough to indicate the possibility of further species being discovered almost anywhere. S. phaeolepioticola Redhead et al. from Japan was only provisionally described in R94 (thought at first to be S. odorata but probably parasitizing Phaeolepiota aurea). S. tropica Bas was also only provisionally described and is best forgotten, being based on a collection from Malaya now lost and never clearly established as parasitic.
Some outstanding issues * All known Squamanita species appear to he narrowly host specific. But the hosts are very Excluded species varied. How did such a state of affairs evolve? Are Squamanita ‘cettoiana’ nom. prov. these the last few descendants of a plurivorous Provisionally named by Moser in his common ancestor surviving precariously on their Kryptogamenflora Edn. 4 (the one with the most favoured hosts? Or have species on one host English translation). It was based on the single somehow from time to time produced spores immature collection illustrated in Cetto Vol.3/855 capable of parasitizing a radically different host? giving the impression of a relative of S. schreieri * Apart from overall rarity, there is the mysteriparasitising Amanita rubescens. Subsequent ous phenomenon exhibited by several species of collections showed that in fact base and cap both popping up over a wide area for two or three belonged to the rare Amanita lepiotoides Barla, years and then disappearing from sight for already illustrated in Cetto Vol.2/390. The decades. This needs an explanation. mistake was corrected in Moser’s 5th edition. * S. odorata persisted at one French site from 1990 to 2003 (Mondiet et al., 2007). I have not Extra-European species heard of S. paradoxa persisting above two years S. paradoxa and S. umbonata were first at any British site. The similarly parasitic described from the USA; S. odorata and Volvariella surrecta recurred on Clitocyhe nebularis for at least five years at a Surrey site in Richmond Park. * Cystoderma amianthinum normally grows singly. This contrasts with the clumps of nine fruitbodies reported by Bingham & Bingham (2005) for S. paradoxa on this host (see Fig. 2) and eight by Holden (2005) for S. pearsonii thought to be on this host. Could the Squamanita mycelium somehow be inducing an abnormal concentration of host mycelium, thus forming a large cecidiocarp favourable to the production of multiple Squamanita fruitbodies? The base of Fig. 6. Rhodocybe stangliana on the deformed remnants of Lyophyllum inolens. In needle litter under pine, Meningen, S. odorata similarly appears to exceed in volume a normal fairly slender Hebeloma Germany, 2008. Photograph © Andreas Gminder. mesophaeum.
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Vol 14 (2) Ongoing research Gareth Griffith, at Aberystwyth University, is making further DNA-based investigations of S. paradoxa, and would much like to receive further fresh material preferably packed in moss. Contact him at [email protected] or phone 01970 622325.
Abbreviations used above BFF8 British Fungus Flora Vol.8 1998 B&K4 Breitenbach & Kränzlin, Fungi of Switzerland Vol.4, 1995 C&D Courtecuisse & Duhem, Mushrooms & Toadstools, HarperCollins, 1995 FM Field Mycology Lud Ludwig, Pilzcompendium, Vol.1 R94 Redhead et al. (1994) - see below Svp Svampe (Danish journal) SZP Schweize Zeitschrift für Pilzkunde
Acknowledgements My thanks to the photographers who generously allowed the use of their photographs.
References
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