MYCOLOGIA BALCANICA 5: 33–37 (2008) 33

Agaricus species from Greece

Stephanos Diamandis * & Charikleia Perlerou

NAGREF–Forest Research Institute, 570 06 Vassilika, Th essaloniki, Greece

Received 11 January 2008 / Accepted 17 March 2008

Abstract. Th e includes saprotrophic species occurring in a variety of ecosystems. Most of them, however, are confi ned to grasslands. Forty one taxa have been recorded in Greece to date. Some species, although heavily picked for their gastronomic value, seem to appear in abundance while others, which are inedible, seem to be infrequent or rare. As in recent years grass and pasturelands in Greece have been included in “improvement programmes” and subjected to the use of fertilizers, there is concern about the disturbance caused to the habitats of the Agaricus species and consequent changes in the fungal biodiversity. It is obvious that further research on the ecology and particularly the factors governing the fruiting and spreading of Agaricus species is necessary before any concrete conclusions are reached and any conservation measures are imposed.

Key words: Agaricus, conservation, frequency, fungal biodiversity, Greece

Introduction are not able to consume any of the edible Agaricus species including the cultivated Agaricus bisporus because they Th e genus Agaricus L. includes a fair number of saprotrophic experience vomiting and diarrhea. species occurring in a variety of ecosystems. Ninety species Four characteristics are considered to be the most have been recorded in Europe (Cappelli 1984; Bas 1991), important for identifi cation of the Agaricus species: but estimates for the worldwide distribution are likely to the staining reaction, the odour, the veil characteristics exceed 200. Historically, all of the species producing gilled and the size. Unfortunately, again, all of the above were classifi ed in a massive genus, Agaricus. In characteristics, with the exception of spore size, may be the 19th century, Elias Fries divided Agaricus into a number infl uenced or altered by the environment. Specimens growing of smaller genera based on easily ascertainable features such in the open, for instance, may be coloured diff erently when as attachment of the gills, texture of the stalk, presence or compared to other specimens which grow in shady places. absence of a veil, and colour of the (Arora 1986). Similarly, dry or old specimens manifest their staining From both the economic and gastronomic points of reaction and odour more slowly or subtly than young, fresh view, the genus Agaricus is defi nitely the most important individuals, while soggy specimens may not display their group of gilled mushrooms because it includes the widely normal odour and staining reactions at all. It is obvious that cultivated species A. bisporus and its varieties and cultivars. the habitat and the environmental conditions should always It also includes a number of delicious collectables which are be taken into consideration when attempting to identify not easy to recognize in the fi eld. Even though several species unfamiliar Agaricus species (Arora 1986). are favourites for many pickers, the genus Agaricus Some Agaricus species are notable for their beauty and is also characterized by some confusingly polymorphic elegance while others are large and fl eshy. Th ey can be found species (variable size, shape, colour, etc.), which make their in urban and suburban habitats such as gardens and parks, identifi cation a diffi cult task. Fortunately, no member of the cemeteries and roadsides, along grassy trails and on compost genus is deadly poisonous, but some species cause mild to piles. Th ey also grow in rural areas such as forests and pastures severe vomiting and diarrhea in most people. A few people where they fruit in large quantities.

*Corresponding author: e-mail: [email protected] 34 Diamandis, S. & Perlerou, C. — Agaricus species from Greece

Th e Agaricus species in Greece fruit in late spring and & Politis (1940 – in Pantidou 1973). It resembles its close from late summer through autumn whenever the conditions relative A. bitorquis (Quél.) Sacc. but diff ers in staining are favourable, moist and mild. Most species, however, can reddish when cut and it is more apt to have a warty or be found right after the fi rst late summer or autumn rains scaly cap (Arora 1986). while the temperatures are still high. A few species fruit even A. bisporus (J.E. Lange) Imbach in December and January in lowland areas and during years Th ought to be rare, however, it is now considered frequent. with mild winters. Carpophores were found mainly under cypress on bare Th e objective of the present work was to report all the soil and less often on sheep dung heaps. It fruits in spring species of the genus Agaricus recorded in Greece to date along and in September–October. Edible. Reported by Callac with details in regard to their frequency, habitat, fruiting time, et al. (2000). edibility and fi rst reporting author/s. A. bitorquis (Quél.) Sacc. (A. edulis (Vittad.) Konrad & Maubl.) Infrequent, it was recorded under Eucalyptus spp. along Recorded species country roads and paths and also in parks on sandy, dry soil. Carpophores appear in April–May and again from Forty one taxa have been recorded in the genus Agaricus August to October. Edible and very good. Reported in Greece to date. Frequency information is based on long by Athanasiou & Th eochari (2001). Features which collecting experience and database citations. Th e taxa are distinguish this species from other Agaricus spp. are the arranged here in alphabetical order. band like or sheathing ring usually with two free limbs, its solid stem and fi rm texture, the fl esh that does not stain Agaricus abruptibulbus sensu auct. eur. yellow or red and the lack of or phenol odour. Rare, it was found in Greek fi r (Abies cephalonica Loudon) A. bresadolanus Bohus forests. Its carpophores appear in late summer and autumn. Frequent, it was recorded in manured pastures, around Edible. Reported by Pantidou (1980). manure piles and occasionally under broadleaved trees A. albertii Bon (in particular poplar, black locust, oak) and conifers. Frequent, it was recorded in large numbers in Macedonia Carpophores appear from April to November. Edibility (N Greece) and Th essaly (C Greece). It fruits from confusing. Some authors consider it as edible and good late April to November. Edible, good. Reported by and others as toxic. Reported by Konstantinides (2004). Konstantinides (2004). A. campestris L. : Fr. A. arvensis Schaeff . (A. cretaceus sensu Ricken, Pilát, non Fr.) Probably the most common of all. It grows in pastures. Common, it was recorded in a variety of habitats such Although heavily picked, it can be found in abundance as grassy places, pastures, forest edges (Fagus sylvatica from April to November. Edible and good. Reported by L., Castanea sativa Mill.) on rich or manured soil. Its Landerer (1858 – in Pantidou 1973). carpophores appear from April to November. Edible, A. campestris var. squamulosus (Rea) Pilát excellent. Reported by Landerer (1858 – in Pantidou Infrequent, it occurs in mountain pastures from May to 1973). It can be separated from the poisonous A. September. Edible and good. Reported by Diamandis xanthodermus Genev. by the base of its stem which does (1985). not turn yellow immediately after rubbing. A. comtulus Fr. A. augustus Fr. (A. perrarus Schulzer) Rare, it is found in pastures, at the edge of country roads Infrequent, it was found in hardwood and coniferous forests and always among grass and other vegetation. Carpophores (Abies borisii-regis Mattf., Quercus frainetto Ten., Fagus appear solitary or in small groups in autumn. Not edible. sylvatica). It fruits more often gregariously or in groups Reported by Maire & Politis (1940 – in Pantidou 1973). from August to October. Edible and good. Reported by A. cupreobrunneus (Jul. Schäff . & Steer ex F.H. Møller) Pilát Diamandis & Perlerou (1990). Important morphological (Psalliota cupreo-brunnea Jul. Schäff . & Steer ex F.H. Møller) features are its almond extract odour, yellow-staining cap Infrequent, it was found in old wheat fi elds. It fruits with brown fi brils or scales, prominent ring, brown spores from April to November. Edible. Reported by Perlerou & and shaggy stem at young age. Diamandis (2000). A. benesii (Pilát) Singer A. dulcidulus Schulzer Infrequent, it occurs in broadleaved and more rarely in Frequent, it occurs in coniferous and mixed forests in the coniferous forests. It fruits in late summer and autumn. needle litter. It produces its carpophores singly or in small Edible. Reported by Konstantinides (2006). groups in late summer and autumn. Edible. Reported by A. bernardii (Quél.) Sacc. Konstantinides (2004). Frequent, it grows in saline pastureland along the coast, A. fuscofi brillosus (F.H. Møller) Pilát along roads that are salted in winter against ice and also Rare, it grows in forests on rich, calcareous soil. Carpophores around sheep folds where shepherds set salt feeders. It can be found in small groups or singly from August to fruits in spring and autumn. Edible. Reported by Maire October. Edible. Reported by Konstantinides (2004). Mycologia Balcanica 5 (2008) 35

A. gennadii (Chatin & Boud.) P.D. Orton and again in the autumn. Poisonous, it may cause gastric Rare, it is found in a wide range of habitats such as pastures, upsets. Reported by Konstantinides (2004). parks, along country roads, in greenhouses and even at the A. niveolutescens Huijsman edges of coniferous forests on sandy soils. It fruits from Rare, it grows in hardwood forests and especially beech, April to October. Edible. Reported by Konstantinides in grassy places and along country roads and paths on (2004). calcareous soils. Carpophores appear solitary or gregarious A. haemorrhoidarius Schulzer in autumn to early winter. Not edible. Reported by Rare, it was recorded in grassy places in coppice oak forest. Athanasiou & Th eochari (2001). It fruits in the autumn. Reported by Pantidou (1973). A. nivescens (F.H. Møller) F.H. Møller A. impudicus (Rea) Pilát Rare, it was recorded in Greek fi r (Abies cephalonica) forests. Rare, it was recorded only in one location. It usually Edible. It was reported by Pantidou (1973). Closely related grows along trails, in forests, preferably on sandy soil. to A. arvensis, it diff ers in its more globose and pure white Carpophores grow in late summer and in autumn. Edible. or slightly yellowing cap, its longer remaining whitish gills Reported by Konstantinides (2006). and shorter spores. A. koelerionensis (Bon) Bon A. pampeanus Speg. Rare, it was recorded in grassland near the coastline. Rare, it is found in pastures and fi elds on rich, basic soils. Edible but not particularly good. Recorded by Diamandis It fruits in small groups or solitary in late summer and (2008). autumn. Edible. Reported by Athanasiou & Th eochari A. langei (F.H. Møller) F.H. Møller (A. haemorrhoidarius sensu (2001). It belongs to the wider group of A. campestris, auct. J.E. Lange, Pilát) diff ering from other forms by the size of its spores which Infrequent in Greece, it grows in coniferous forests, are much longer, up to 10.8 μm. especially fi r (Abies borisii-regis) forests. Carpophores A. porphyrizon P.D. Orton (A. purpurascens (Cooke) Pilát, found in small groups in late summer to October. Edible non Fr.) and good. Reported by Konstantinides (2004). Infrequent, in broadleaved forests, parks and gardens on A. lanipes (F.H. Møller & Jul. Schäff .) Hlaváček rich, sandy soil, in warm places. It fruits solitary or in small Rare, it was collected only in one location. It grows in groups in late summer and autumn. Edible. Reporded by forests, parks and river banks on sandy soils. Carpophores Polemis (1998). appear from August to November in groups. Edible, but A. porphyrocephalus F.H. Møller it is recommended not to pick it because of its rarity. Rare, it was recorded only once. It grows in rich, manured Reported by Konstantinides (2006). pastures. Its carpophores appear in the autumn. Edible A. litoralis (Wakef. & A. Pearson) Pilát and good. It was reported by Konstantinides (2006). Infrequent, it can be found in pastures, roadsides and A. praeclaresquamosus (F.H. Møller) Bon & Capelli (A. along the coast on sandy soil. It often fruits in groups placomyces Peck) from April to November. Edible and good. Reported by Infrequent, it grows in forests, parks and shrubland. Konstantinides (2004). Carpophores appear in autumn. Toxic, it may cause gastric A. luteomaculatus (F.H. Møller) F.H. Møller upsets. A. placomyces was reported by Diamandis (1985). Rare, it occurs in Greek fi r (Abies cephalonica) forests. Its A. romagnesii Wasser (A. radicatus (Vittad.) Romagn.) carpophores appear in late summer to mid-autumn. Not Rare, it was collected only once in Quercus frainetto forests. edible. Reported by Pantidou (1973). Inedible. Reported by Zervakis et al. (2002b). A. macrocarpus (F.H. Møller) F.H. Møller A. semotus Fr. (A. rubellus (Gill.) Sacc.) Locally common, it was collected in black pine (Pinus Rare, it was collected once under Quercus frainetto. nigra) and Greek fi r forests. Diff ers from A. abruptibulbus Inedible. Reported by Zervakis et al. (2002b). Peck. in its cheilocystidia which have papillate apex. A. sylvaticus Schäff . (Psalliota sanguinaria (P. Karst.) J.E. Reported by Zervakis et al. (2002a). Lange) A. macrosporus (Jul. Schäff . & F.H. Møller) Pilát (Psalliota Frequent, it was recorded in coniferous (Pinus radiata D. arvensis subsp. macrospora Jul. Schäff . & F.H. Møller) Don, P. pinea L., Abies cephalonica, A. borisii-regis, Picea Infrequent, it was found in grassy places, in chestnut abies (L.) Karst.) and also in hardwood forests (Quersus forests and, less often, in pastures. It fruits in the autumn. frainetto, Castanea sativa, Fagus sylvatica). It fruits from Edible. Reported by Diamandis & Perlerou (2002). August to October. Edible. Reported by Landerer (1858 A. mediofuscus (F.H. Møller) Pilát – in Pantidou 1973). Rare, it was found in alpine pastures in October. Reported A. sylvicola (Vittad.) Lév. (Psalliota sylvicola (Vittad.) Richon by Dimou et al. (2002). & Roze) A. moelleri Wasser (A. praeclaresquamosus var. terricolor (F.H. Common, it occurs in coniferous and broadleaved forests. Møller) Bon & Cappelli) It was found under Cedrus libani A. Rich., C. deodara Infrequent, it occurs in pastures, shrubland, parks and (D. Don) G. Don, Pinus halepensis Mill., P. brutia Ten., forest edges. Carpophores appear in groups in spring Cupressus sempervirens L., Abies borisii-regis, Quercus 36 Diamandis, S. & Perlerou, C. — Agaricus species from Greece

frainetto, Fagus sylvatica. Carpophores appear solitary or molecular weight antitumor and antimetastatic substances in clusters in the autumn and even mid-winter. Reported were also isolated from A. blazei and other Agaricus species by Maire & Politis (1940 – in Pantidou 1973). It rather (Kimura 2005). resembles A. arvensis, but is often more erect and less Work carried out in Greece by Th eochari et al. (2003) robust, has smaller spores and grows on bare soil. towards fi nding carpophores in the fi eld of autochthonous A. subfl occosus (J.E. Lange) Pilát mycelium of A. bisporus revealed some very interesting results. Rare, it was recorded in fi r (Abies cephalonica) forest among Th e was recorded repeatedly in quite a few places in needle litter. It fruits solitary to gregarious in the autumn. Greece on sheep manure piles and under cypress (Cupressus Edible. Reported by Pantidou (1980). sempervirens). In the former habitat, carpophores appeared A. xanthodermus Genev. from early autumn until late spring because of its fast soaking Frequent, it is frequently found in grasslands, parks and with water after the fi rst rains while on the latter, they emerged forest openings. Its carpophores may appear from April to later in winter until early spring because of slower hydration November every time there is enough moisture. It causes of the cypress litter and faster drying out in spring. One out gastric upsets. Reported by Maire & Politis (1940 – in of 117 isolations of the fungus was a 4-haploid-basidiospore Pantidou 1973). isolation, a rare and valuable event as such haploid spores are A. xanthodermus var. griseus (A. Pearson) Bon & Cappelli unique for breeding and can produce new genetic material for Frequent, it occurs in grassy openings of hardwood the mushroom cultivation industry. Furthermore, one more forests, pastures and gardens. It fruits in groups in spring isolate was obtained from original mycelium collected from and autumn. Toxic. It causes gastric upsets. Reported by cypress litter under natural cypress in Crete. Such an isolate Konstantinides (2004). can be considered as particularly important for evaluation and A. xanthodermus var. lepiotoides Maire preservation of the biodiversity. Frequent, it occurs in grassy openings of hardwood forests, Th e genus Agaricus is thought to be mainly distributed in pastures and gardens. It often fruits in small groups from the tropics and subtropics. It would be expected that Greece, April to October. It causes gastric upsets. Reported by at the southern end of the Balkan Peninsula, would host Konstantinides (2004). more species than other parts of Europe. Forty one taxa (39 species and 2 varieties) are reported here but more intensive surveys should be carried out, especially in Peloponnese, Discussion Crete and the southern Aegean islands, for that purpose. Similarly in Turkey, 37 taxa (33 species and 4 varieties) have Despite the fact that carpophores of the genus Agaricus are been recorded so far, a number which can be substantially considered as favorite among mushroom pickers, this is not increased (Sesli & Denchev 2005). Recently, Lacheva (2006) an easy group of macromycetes to identify. Furthermore, reported 31 new taxa in Bulgaria bringing the total number even though there are no members of the group causing fatal of Agaricus taxa in this neighboring country to 59 (50 species poisoning, a few can cause really unpleasant gastric disorders and 9 varieties). for many people. It appears that the phenol-smelling species Th e information cited here on the frequency and are responsible for the poisoning in the majority of people abundance of the recorded species also needs some critical who are sensitive to eating them. Th eir smell may not be comments. Popular species among mushroom pickers such evident in the fi eld, however, it becomes more pronounced as A. albertii, A. arvensis, A. campestris, A. macrosporus and A. when they are cooked. sylvicola, which are heavily collected every season, tend to fruit Th e cultivated mushroom A. bisporus is defi nitely the most in abundance. Although systematic surveys on permanent well known, however, it is considered as mediocre from the plots have not been carried out, it seems that mushroom culinary point of view. A. campestris is a popular species too, pickers have not experienced any noticeable reduction in their but the very best to eat are A. augustus, A. arvensis, A. bernardii collections. On the contrary, other species which are confi ned and A. bitorquis which, in fact, are not very popular. to grasslands and are considered as rare and infrequent, Naturally occurring hydrazines, such as agaritine, are although not picked at all or only occasionally because found in edible mushrooms. According to Schulzová et al. their edibility is confusing or not established, seem not to (2002) the content of agaritine in cultivated A. bitorquis be able to extend their range or to increase their numbers. varied from 165 to 457 mg kg(-¹) on average being 272 ± It is widely accepted that natural grasslands typically have 69 mg kg(-¹), while in A. bisporus it was detected at the level an associated mycota (Spooner & Roberts 2005). In recent of 228.2 mg kg(-¹) (Hashida et al. 1990). As agaritine and years grass and pasturelands in Greece have been included in its putative metabolites are suspected for mutagenic and “improvement programmes” by using fertilizers spread from carcinogenic potential in mammalian cells, more research the air. It is established that fertilizers destroy the natural should be focused on its eff ects to human cells because of the mycota of grasslands, replacing waxcaps (Hygrocybe species increasing consumption of cultivated Agaricus mushrooms. and other fungi with commonplace nitrophilic species of Such concern, of course, should not discourage the public the genera Panaeolus, Coprinus, Psilocybe and Stropharia from consuming mushrooms, as it has been proven that low (Spooner & Roberts 2005). Th e eff ects of such programmes Mycologia Balcanica 5 (2008) 37 on biodiversity and particularly on fungal biodiversity have carcinogenicity of mushroom methanol extracts on the mouse bladder not been thoroughly considered before application, and even epithelium. – Nippon Koshu Eisei Zasshi 37(6): 400-405. worse, the programmes have not been monitored or evaluated Kimura, Y. 2005. New anticancer agents: in vitro and in vivo evaluation of the in depth after application. antitumor and antimetastatic actions of various compounds isolated from It is obvious that research on the ecology and particularly medicinal plants. – In Vivo 19(1): 37-60. the factors governing the fruiting and spreading of Agaricus Konstantinides, G. 2004. [Mushrooms, a fi eld guide]. Zarzonis Publ. Co, species is necessary before any concrete conclusions are Th essaloniki. (In Greek) reached and any conservation measures are imposed. Konstantinides, G. [ed.] 2006. [1000 Mushrooms and toadstools of W. Macedonia]. Mycological Society of W. Macedonia (MSWM), Kastoria. (In Greek) References Lacheva, M. 2006. [Genus Agaricus L. : Fr. emend. P. Karst. (Mushroom) in Bulgaria – , ecology, chorology and economical importance]. PhD Arora, D. 1986. Mushrooms demystifi ed. Ten Speed Press, Berkeley. thesis. Agricultural University, Plovdiv. (In Bulgarian) Athanasiou, Z. & Theochari, I. 2001. 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