Leratiomyces ceres (Strophariaceae, Basidiomycota), new to Poland

Leratiomyces ceres, an extra-European species hitherto unknown in Poland, was identified in a public park in Rybnik City (SW Poland). The first Polish collections of the fungus were studied using macroscopic and microscopic features. A brief description and illustration of the species, based on Polish specimens, are presented. The ecology and characteristics distinguishing L. ceres from related Leratiomyces species are also discussed.


Introduction
The name, Leratiomyces, was designated by Bresinsky and Binder [1] as a potentially valid substitute for an older invalid generic name "Le Ratia" that was originally used to represent a small group of secotiaceous fungi from New Caledonia by Patouillard [2]. Leratiomyces was then adopted to define a phylogenetically defined clade of agarics and secotiaceous fungi by Bridge et al. [3], who provided an emended diagnosis of the genus. However, for various nomenclatural reasons, the generic name Leratiomyces, as proposed by Bresinsky and Binder [1], was not validly published. The nomenclatural problems regarding this name were reviewed in detail and finally resolved by Redhead and McNeill [4]. Consequently, the genus was typified by Leratiomyces similis (Sacc. & Trotter) Redhead & McNeill, and the generic name currently in use is Leratiomyces Bresinsky & Manfr. Binder ex Bridge, Spooner, Beever & D. C. Park. The genus Leratiomyces includes saprotrophic mushrooms found on naked soil, rotten wood, wood debris (including saw-dust and woodchip mulch), and other vegetal debris in woodchip beds, dry grasslands, or sandy-soil habitats [5,6]. It is a small genus which contains around ten agaricoid or hymenogasteroid species distributed worldwide [3][4][5]7,8], and so far, two of them have been reported in Poland: Leratiomyces squamosus (Pers.: Fr.) Bridge [9][10][11][12].
In 2018, Leratiomyces ceres (Cooke & Massee) Spooner & Bridge, the species new to Poland, was found on wood debris and soil within municipal shrubberies mulched with bark in Rybnik (SW Poland). It should be noted that the earlier record of the species from a fertile lowland beech forest in the vicinity of Gdańsk announced in Wojewoda [9] with no information about sources or materials traced, reported as "(?) Psilocybe aurantiaca (Cooke) Nordel. ", must remain as doubtful. Today it is believed that L. ceres is an alien invasive species from outside Europe [5,13,14]. It was originally described from material collected in Melbourne (South Australia) by the English botanists and mycologists M. C. Cooke and G. E. Massee under the name of Agaricus (Psilocybe) ceres [15]. Although the species was collected in New Zealand in the 1940s (cf. [16]), it was hardly ever reported under the name, Psilocybe ceres (Cooke & Massee) Sacc. [17] -after its original description -until the 1960s when it became better known in Western Europe under the misapplied name, Stropharia aurantiaca [18]. It is believed that the first reliable observations of this non-native basidiomycete were made on the continent between 1953 and 1957 [19]. During this period, "S. aurantiaca" appeared in disturbed outdoor habitats in the Netherlands (Hengelo), Belgium (Antwerp), and England (Somerset: Bossington; Surrey: Richmond Palace gardens) [18][19][20][21][22]. In 1966, it was recognized in France [19], and in 1968, "S. aurantiaca" was discovered in Germany [23][24][25]. Over the next fifty years, "S. aurantiaca" was also found for the first time in other European countries and regions, including Austria, Balearic Islands, Corsica, Italy, Luxembourg, Portugal, Spain, Switzerland, and the Czech Republic [26][27][28][29][30][31][32][33][34]. It was also recognized in Macaronesia (Madeira) [35], South Africa [36,37], South and North America (Brazil, USA) [38][39][40][41], and Tasmania [42]. After decades of being represented by a false name, the history of "S. aurantiaca" was reviewed, and with the help of genetic analysis, a new name, Leratiomyces ceres was proposed [3]. Currently, the species is considered to be one of the most widespread (and often abundant) and distinctive woodchip mulch fungi [14,43,44]. Our finding in Poland extends the known distribution of L. ceres in Europe. The aim of this paper is to give a detailed description and illustration of the Polish collections and to compare them with reports of this species from other regions available in literature.

Material and methods
Field photographs of fresh basidiomata were taken with the aid of a Tamron SP 90 mm F2.8 macro lens mounted on a Pentax K10D camera. Basidiomata were collected and transported to the laboratory where they were dried for further studies. Characteristics that changed over time (color, smell, and texture of the basidiomata) were noted in the field. The macroscopic description is based on both the study of fresh material (three collections comprising thirty basidiomata at different developmental stages) and the analysis of photos. Microcharacters were observed using a Nikon Eclipse E-400 light microscope equipped with a Nikon digital camera (DS-Fi1). All microscopic structures were observed in preparations from dried material. Freehand sections of rehydrated pieces of basidiomata were examined in squash preparations in 5% NH 3 ·H 2 O and Congo red reagent. Image-grabbing and biometric analyses were done using NIS-Elements D 3.1 imaging software. The dimensions of microcharacters are given as follows: (minimum) 10-90 (maximum) percentile values, average ± standard deviation. Randomly selected mature basidiospores were measured without the hilar appendix. Basidia lengths were measured, excluding sterigmata. Statistical computations were carried out using Statistica software (StatSoft). The following abbreviations are used: L = number of lamellae reaching the stipe; l = number of lamellulae between each pair of lamellae, and Q = the length-width ratio of basidiospores (mean value). The morphological terminology follows that used by Vellinga [45] and Vellinga and Noordeloos [46]. The nomenclature of vascular plants was based on The Plant List (http://www.theplantlist. org/). The studied collections have been deposited in the Museum of Natural History, University of Wrocław, Wrocław, Poland (WRSL).

Results
Leratiomyces ceres (Cooke & Massee) Spooner & Bridge ( Fig. 1-Fig. 3  (rarely slightly hygrophanous with translucently striate margin when moist), orange-red or brown with dark red tint, slightly viscid when wet, initially had white patches of veil on the margin. Lamellae (L = 25-40, l = 3-7), moderately crowded to fairly distant, adnate, pale grey, yellow-grey with olivaceous tint to pale olivaceous when young, then olive-umber and, olive-purple to purple-brown in old age with white, fimbriate edge. Stipe, 20-100 × 3-10 mm, central, cylindrical, slightly broadened towards the base (or rarely narrowed), stuffed then hollow (fistulose), whitish or tinged yellow above, developing reddish-orange stains over the lower half (also when bruised), pruinose (in the upper part), slightly fibrillose-striate below, with patches of annulus (rarely annulate), white tomentose base and sometimes with white to yellow mycelial threads. Veil, thin-membranous, whitish, quickly disappearing or rarely forming a slight, easilyobliterated annulus on the stipe. Context pallid, first cream, then pale ochre to ochre in the central part of stipe and in the cortex of the pileus, then reddish brown at the base of the stipe, sometimes orange-red spotted in pileus. Smell not distinctive, taste not recorded. Spore deposits not obtained. Basidiomata growing in a bundle (fasciculate), in small groups or solitary.

Discussion
The practice of applying wood and bark from chipped or shredded trees, to conserve soil moisture and as a natural weed barrier, to vegetable gardens, flower beds and shrubberies has become more popular since the mid-1980s, contributing to the emergence of a unique habitat for many species of wood-decaying fungi [44,58]. Possibly due to the high levels of terpenes and other inhibitory compounds in bark, mulch fungi are generally known to prefer woodchips than bark chippings [58]. Finely chopped woody material can support diverse saprotrophic fungal communities, including alien species [44,53], although these assemblages are generally known to be short-lived. Additionally, it is well-known that many of the species do not produce fruit bodies in subsequent seasons [14,58].
Leratiomyces ceres is said to be one of the common and most characteristic species of extra-European origin which epitomize the interests of the woodchip communities in West and Central Europe [3,14,44,53]. It is a very distinctive mushroom, considering the striking copper, orange red to dark red coloration of the pileus that often has white veil remnants on the margin and, purplish brown lamellae when mature, in conjunction with its habitat on decaying woodchip mulch, sawdust, and other wood debris in humaninfluenced sites [48]. It is important to note, however, that while the species in general has a clear preference for woody mulch in parks, gardens, cemeteries, and boulevards (this study and [14,25,44,58]), a few instances of the fungus growing away from human habitation (away from woodchips) have also been reported [18,23,42]. Leratiomyces ceres seems to be most frequently found in high abundance on relatively freshly applied mulches [58,59]. Our study also highlights the importance of this kind of substrate on which the species apparently grows best or is favorably disposed towards. However, during field works, we also found a few basidiomata of this mushroom growing directly on rich soil (humus without visible buried wood debris in the immediate vicinity). On the one hand, this supports the suggestions of some authors [14,17,34,39,48,59] that L. ceres may be associated with soil, but, on the other hand, it seems to refute the view that the fungus is only able to fructificate when some factors associated with woodchip mulch are present [59]. This issue evidently needs further research.
It is difficult to interpret the description of Agaricus ceres by Cooke [15]. The original diagnosis is too vague to allow a reliable taxonomic conclusion. Moreover, it is somewhat aberrant regarding the given spore size (14-16 × 6-8 µm). This cannot change the fact that later interpretations of the species in literature (also based on the examination of the holotype) are congruent [3] (also cf. [60]). The Polish material of L. ceres agrees well with the account and iconography of the species given, for instance, by Cleland [17], Orton [21], Engel and Engel [23], Watling and Gregory [47], Pegler and Legon [43], and Noordeloos [5,34], except the hygrophanity of the pileus. This character is generally not reported [42,43] or considered to be atypical of L. ceres [5,34], and only exceptionally, is the hygrophanity confirmed for the species [48]. We found L. ceres to be at least partially hygrophanous and occasionally translucently striate when very moist. We are inclined, however, to consider these features accidental due to the unique weather conditions (abundant rainfall and very high humidity) preceding and accompanying the observation period. According to literature, L. ceres, when fresh, may be similar to a slender Leratiomyces squamosus var. thraustus (Kalchbr.) Bridge & Spooner [syn. Stropharia thrausta (Kalchbr.) Sacc.], but is readily distinguished by its more robust stature, thinner and often incomplete annulus, often disappearing with age, and mostly due to the presence of chrysocystidia [5,34]. Additionally, the cheiloleptocystidia of L. squamosus var. thraustus seem to consistently be a little more slender, more frequently filamentous-flexuous, and tapering towards the apex than those found in L. ceres [5,34]. Balletto [61] described a new species from France, Naematoloma rubrococcineum, which appeared to be like L. ceres based on its gross morphology (colors and stature) and microfeatures (spore characteristics and the possession of chrysocystidia). This was first suggested by Mazza [62], who noted the name, N. rubrococcineum, as a possible synonym of "Stropharia aurantiaca". Although the identity of this taxon was not checked using type material, the macro-and microfeatures published by Balletto [61], supplemented by colored plates by Mazza [62] and Nonis [63] enabled Bridge et al. [3] to conclude that N. rubrococcineum is contaxic with L. ceres. Consequently, the name N. rubrococcineum is to be considered a synonym of L. ceres.
The practical significance, nutritional and biochemical value of L. ceres seem to be insufficiently known. In literature, the edibility of the species is often unspecified [28] or reported as "unknown" [39,40,64], or the fungus is generally considered "inedible" [49,55,57,[65][66][67]. We could not find any official report of use of L. ceres as a psychoactive mushroom, and we did not have the opportunity to investigate the collected specimens for the presence of indole derivatives. However, the findings of Anastos et al. [68] suggest that L. ceres contains psilocybin in relatively large amounts (9,700-9,900 mg/kg dry weight) (cf. [69]).