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DOI 10.12905/0380.sydowia66(1)2014-0043

Psilocybe s. str. (Agaricales, Strophariaceae) in Africa with description of a new species from the Congo

Gaston Guzmán1*, Stuart C. Nixon2, Florencia Ramírez-Guillén1 & Alonso Cortés-Pérez1

1 Instituto de Ecología, Apartado Postal 63, Xalapa, Veracruz, Mexico 2 313, Avenue du Tulipier, Goma, Nord Kivu, Democratic Republic of Congo, Africa

Guzmán G., Nixon S. C., Ramírez-Guillén F. & Cortés-Pérez A. (2014) Psilocybe s. str. (Agaricales, Strophariaceae) in Africa with description of a new species from the Congo. – Sydowia 66 (1): 43–53.

Eight species of Psilocybe s. l. which have been reported from Africa are discussed. Psilocybe aquamarina, P. cubensis, P. cyanescens, P. goniospora, P. mairei, P. natalensis, P. semilanceata and P. subcubensis are considered, of which P. cyanescens, P. goniospora and P. semilanceata were reported in doubtful way. A new species, Psilocybe congolensis is de-scribed, which is the first hallucinogenic mushroom known from the Democratic Republic of Congo. For the first time we established a connection between P. subcubensis described from Mexico and P. aquamarina from Africa. Traditional use in the past of the Psilocybe cubensis-complex in Africa is discussed.

Keywords: Hallucinogenic agarics, Hymenogastraceae, ethnomycology, taxonomy.

Few species of Psilocybe s. l. are known from Africa despite several pre-vious mycological explorations and studies, e.g. Beeli and Heim, as discussed by Heinemann (1935–1972). Pegler & Rayner (1969) and Pegler (1977) re-ported some species from Kenia and from eastern Africa. Maire (1928), Malençon (1942), and Malençon & Bertault (1970) studied one species from North Africa and Reid & Eicker (1999) described a new species from South Africa. It is surprising to observe that there are no reports of Psilocybe from Madagascar, despite fieldwork by Hennings, Patouillard and Heim, accord-ing to Buyck (2008). Also this is the case for the review by Crous et al. (2006) on the fungi from South Africa, wherein few contributions on macromycetes were considered, and they omitted important references, such as Gartz et al. (1995) and Reid & Eicker (1999). Recently Kinge et al. (2013) presented the first check list of mushrooms from Cameroon, but they did not mention any species of Psilocybe. The presence in Africa of Psilocybe cubensis (Earle) Singer is under discussion because this mushroom is pantropical and a very common species in tropical America on the dung of cattle, where it was prob-

44 Guzmán et al.: Psilocybe in Africa


ably introduced from Africa in the XVI Century during the Spanish Con-quest (Guzmán 1983).

In the present paper the evidence of P. cubensis in Africa and its proba-ble traditional use in the past is discussed. A critical review of the Psilocybe spp. reported from Africa is presented, and a new bluing species from the Congo is described. In spite of recent phylogenetic studies placing the genus Psilocybe s. str. in the family Hymenogastraceae (Ramírez-Cruz et al. 2013), we prefer to consider the genus in the Strophariaceae Singer & A. H. Sm. waiting for new phylogenetic researches on this genus.

Materials and methods

An intensive review of the literature on mushrooms from Africa was made, looking for records of Psilocybe s. l. Specimens were studied macro- and microscopically. For microscopy hand sections of the basidiomata were made, rehydrated with 96 % alcohol, then mounted in a 5 % solution of KOH, with or without 1 % of Congo red added in the slide. Basidiospore measure-ments include length and width in face-view and thickness in side-view. The sizes in parenthesis are rare cases. The holotypes of P. goniospora from K and P. natalensis from LZ were studied. Around 20 basidiomata of the new spe-cies P. congolensis were gathered by S. C. Nixon and are deposited as types in XAL and NY. The concept of Psilocybe s. str. followed here is based on Redhead et al. (2007).

Taxonomy

Psilocybe congolensis Guzmán, Nixon & Cortés-Pérez, sp. nov. – Figs. 1–8.MycoBank no.: MB 801581

D i a g n o s i s . – Pileus (5) 10–15 mm diam., conic or subconic to convex-umbonate, sometimes papillated, subviscid, yellowish-brown. Lamellae subadnexed, violaceus-brown to blackish. Stipe (25)30–65 × 1–1.5 mm, uniform to thicker at base, smooth, white to yel-lowish-brown. Veil as an arachnoid membrane, forming an ephemeral fibrillose annulus. Bluing. Basidiospores (7)8–9(10) × (5.5)6–7(7.5) × 5–6 µm, rhomboid, subrhomboid or subo-void in face-view, subellipsoid in side-view, thick-walled, pale yellowish-brown. Pleurocys-tidia (11)13–18(21)(23) × (4)5–7(8) µm, subventricose or fusoid, mucronate. Cheilocystidia (14)15–24(27)(29) × 4–8(9) µm, like to the pleurocystidia or sublageniform. Pileipellis as ixocutis. Pileocystidia 10–25 × 6–13 µm. Caulocystidia 14–30(35) × (6)7–13 µm. Gregarious in soil.

D e s c r i p t i o n . – B a s i d i o m a mycenoid. P i l e u s (5)10–15 mm diam., conic or subconic to convex or convex-umbonate to subumbonate, sometimes with a small papilla, smooth, glabrous, subviscid to dry, yellow-ish-brown, margin slightly striate. L a m e l l a e subadnexed, violaceous-

Figs. 1–2. Psilocybe congolensis, holotype. Basidiomata, note the subfibrillous annulus in 2. Phot. Nixon. Bar: 10 mm.

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brown to violaceous-black, edges concolorous. S t i p e (25)30–65 × 1–1.5 mm, uniform to somewhat thicker at base, smooth and glabrous, hollow, white to pale yellowish-brown. Ve i l well developed, as white arachnoid membrane, leaving an ephemeral fibrillose subannulus on the stipe. C o n t e x t white, caerulescent. F l a v o r acrid or earthy. S m e l l bitter.

B a s i d i o s p o r e s (7)8–9(10) × (5.5)6–7(7.5) × 5–6 µm, rhomboid, sub-rhomboid or subovoid in face-view, subellipsoid in side-view, thick-walled (0.8–1 µm), pale yellowish-brown, with a truncate germ pore and a short and acute apiculus. B a s i d i a (20)21–25(28) × (5.5)6–8 µm, 4-spored, subvesicu-lose, with acute or plane base, and a middle constriction, hyaline. P l e u r o -c y s t i d i a (11)13–18(21–23) × (4)5–7(8) µm, subventricose, subfusoid, with a narrow or wide base, mucronate or with a short or long neck, common, hya-line. C h e i l o c y s t i d i a (14)15–24(27–29) × 4–8(9) µm, similar to pleurocys-tidia, but more frequently sublageniform, some irregularly branched, hya-line. P i l e i p e l l i s an ixocutis 15–30 µm thick, but with subgelatinous hy-phae, hyaline, 2–5 µm wide, thin-walled. P i l e o c y s t i d i a 10–25 × 6–13 µm, common, as terminal elements of pileipellis hyphae, subglobose or subve-siculose, sometimes submucronate, with a narrow or wide base, hyaline. H y -m e n o p h o r a l t r a m a regular, with hyphae 2.5–24 µm wide, thin-walled, hyaline or encrusted with yellowish-brown pigment. S u b h y m e n i u m in-flated-ramose, with cells 3–10 µm wide, thin-walled, hyaline. P i l e u s t r a m a radial with hyphae 2.5–25 µm wide, thin- or thick-walled up to 1 µm, hyaline or encrusted with yellowish-brown pigment. C a u l o c y s t i d -i a 14–30(35) × (6)7–13 µm, in fascicles, subvesiculose, clavate-ventricose or globose, hyaline. C l a m p c o n n e c t i o n s present.

E t y m o l o g y. – The specific epithet refers to the type locality of the fungus.

H a b i t a t . – Gregarious on soil, in grassland with both local and Euro-pean grasses, at 1422 m a.s.l. In several cases, the mycelium was observed attached to grass roots.

D i s t r i b u t i o n . – Known only from the type locality.

M a t e r i a l e x a m i n e d . – Psilocybe congolensis Guzmán, Nixon & Cortés-Pérez: DEMOCRATIC REPUBLIC OF CONGO, Eastern region, in western Albertine Rift high-lands, Kabasha, 15 km NE of Beni, N 0° 23’ 21.22”, E 29° 23’ 24.82”, 1422 m a.s.l., on soil, in dairy farmer pasture with local and European grasses, 22 Mar 2011, leg. S. C. Nixon 02 (Holotype XAL; Isotype NY).

This species belongs to section Cordisporae Guzmán (1983) for its small, thick-walled, subrhomboid basidiospores, and its bluing reaction. This is the first record of a member of this section in Africa. Psilocybe congolensis is an

Figs. 3–12. Psilocybe congolensis (holotype) and P. natalensis (holotype). 3–8. P. congolensis: 3. Basidiospores. 4. Basidia. 5. Pleurocystidia. 6. Cheilocystidia. 7. Pileocystidia. 8. Caulo-cystidia. 9–12. P. natalensis: 9. Basidiospores. 10. Pleurocystidia. 11. Cheilocystidia. 12. Caulocystidium. Bar: 10 µm.

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hallucinogenic mushroom, following the concept of Redhead et al. (2007). Its basidiomata are similar to P. semilanceata (Fr.) P. Kumm. and to P. fimetaria (P. D. Orton) Watling in their mycenoid habit, and also for the fibrillose sub-annulus in P. fimetaria. However, both have large subellipsoid basidiospores, up to 14(16–18) µm, and belong to section Semilanceatae (Guzmán 1983), which aggregates common temperate species in Europe. Also P. congolensis is something close to the neotropical species P. caerulescens Murrill for its microscopic features; however, this latter presents a robust collybioid ba-sidioma with pileus convex and not papillate, up to 70(100) mm diam., and it is known in the SE of the USA, Mexico and South America, in removed or eroded clay soils, not in grass lands (Guzmán 1983).

There is no information on local uses or common name for Psilocybe congolensis. However, while Nixon was visiting Mt. Tshiaberimu a bluing mushroom resembling P. congolensis was observed frequently, growing gre-garious in ancient afromontane forests, between 2400–2900 m. Unfortunate-ly no collections of this interesting mushroom were possible during the visit, due to the National Park restrictions. In that Mt. Tshiaberimu (locally trans-lated as “mountain of the spirits”), informants referred to old rituals in which visions were sought. It is possible that these rituals historically involved mushrooms, although no indigenous knowledge of a mushroom was found in the region (however, see below some probable ancestral traditional uses of the complex P. cubensis - P. subcubensis in Uganda).

The known species of Psilocybe s. str. from Africa – Figs. 9–12.

There are eight species of Psilocybe s. l. recorded from Africa, although some are doubtful. These species are: Psilocybe aquamarina (Pegler) Guzmán, P. cubensis (Earle) Singer, P. cyanescens Wakef., P. goniospora (Berk. & Broome) Singer, P. mairei Singer, P. natalensis Gartz, D. A. Reid, M. T. Sm. & Eicker, P. semilanceata and P. subcubensis Guzmán, as we will discuss below.

Psilocybe aquamarina vs. P. subcubensis. Psilocybe aquamarina was de-scribed from Kenya by Pegler (1977) as Stropharia aquamarina Pegler. After study of the holotype at K, Guzmán (1995) considered Pegler’s species as P. aquamarina because it has no chrysocystidia, and displays bluing. How-ever, based now on a new review of Guzmán’s notes, it is probable that P. aquamarina is the correct name and synonym of P. subcubensis (Guzmán 1978 a), although more studies are necessary. This latter species presents ba-sidiospores (10)11–13(14) µm long, smaller than those of P. cubensis, with basidiospores (12)13–15(17) µm (Guzmán 1983), while the holotype of P. aquamarina has basidiospores (9)10–11(12) µm. On the other hand, Charters (1957) reported a poisoning in Kenya by a Stropharia sp., with states of eu-phoria, depression moments, laughter, and disorientation of sense of space. This intoxication is very similar to that produced by the Mexican hallucino-genic mushrooms, such as P. cubensis and P. subcubensis (Guzmán 1983). Also another Stropharia was previously implicated in a similar intoxication

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in Nairobi, observed by Cullinan et al. (1945). Heim (Heim & Wasson 1958) supposed that both intoxications were produced by Psilocybe cubensis (as Stropharia cubensis Earle). Nevertheless, Pegler & Rayner (1969) identified the Nairobi mushroom as S. merdaria (Fr.) Quél. [= Deconica merdaria (Fr.) Noordel.], a non-bluing, non-hallucinogenic species which does not agree with the reports by Cullinan et al. (1945) nor Charters (1957). The mush-rooms involved in these cases probably belong to Psilocybe aquamarina for its association with tropical or subtropical habitat. Härkönen et al. (2003) also based on Pegler (1977), stated that the Tanzanian mushroom is P. merdar-ia (Fr.) Ricken, but they considered it as a hallucinogenic species. Obviously this is a mistake, because P. merdaria, now classified in the genus Deconica, is a not bluing mushroom (Guzmán 1983).

Psilocybe cyanescens reported by Gartz (1996) from Africa probably is a misidentification. Gartz’s report most probably belongs to P. natalensis for its strong bluing feature he described (see below discussion on this species). Psilocybe cyanescens is a temperate species known only from Europe and with some doubts also from the USA.

Psilocybe goniospora described from Sri Lanka was considered by Sing-er (1955) as Deconica, but he later (Singer 1961) changed this species to Psil-ocybe. Pegler (1977) reported it from Uganda, but he compared this fungus with P. cordispora R. Heim and P. yungensis Singer & A. H. Sm., two Mexican bluing species (Guzmán 1983). However, type material of P. goniospora in K is in bad conditions, and the bluing feature is not observed. It is probable that in fact P. goniospora belongs to the genus Deconica, as Singer (1955) suggested and also discussed by Ramírez-Cruz et al. (2013).

Psilocybe mairei is a xerophytic mushroom described from Algeria (Maire 1928) as Hypholoma cyanescens Maire. It was later reported from Morocco by Malençon & Bertault (1970) as H. cyanescens. Singer & Smith (1958) discussed this species, and Singer (1973) considered Maire’s mush-room as Psilocybe mairei. The holotype is in poor conditions because it is preserved in alcohol at the Laboratoire de Recherche sur les Zones Arides, in the University of Algeria. This holotype was first found and studied by Guzmán (2012). Psilocybe mairei is related with the Mediterranean mush-room P. serbica Moser & E. Horak, as discussed by Guzmán (2012), and may be Moser & Horak’s mushroom is a synonym.

Psilocybe natalensis (Figs. 9–12) was described from the region of Natal in South Africa in a xerophytic habitat (Gartz et al. 1995, Reid & Eicker 1999). This bluing species is strongly hygrophanous, with a brownish pileus that soon turns white. The holotype (LZ) has subellipsoid, thick-walled ba-sidiospores (10–12)13–15(16) µm long; pleurocystidia 20–35(47) × (5)6–9(10) µm, ventricose, sometimes rostrate, rare; cheilocystidia (16)19–26(30) × (4)6–8(9) µm, similar to the pleurocystidia, more sublageniform and caulocystidi-um 21 × 7 µm, vesiculose-rostrate, very rare. It is interesting to observe that this South African species is closely related to P. aztecorum R. Heim from Mexico, based in the study by Guzmán (1978 b). The basidiomata are similar



in both fungi, and also the basidiospores. However, P. aztecorum grows only in grasslands in mountainous pine forests, up to 2.000 m altitude, the basid-iospores are (9–10)12–14(17) µm long, the pleurocystidia are rare and similar to cheilocystidia, 20–34 × 5.5–8 µm (according to Heim & Wasson 1958, Guzmán 1978 b). It seems that these two species differ only in habitat and geographic distribution. In its xerophytic habitat P. natalensis is also similar to P. mairei, but the latter presents slightly smaller basidiospores, up to 12(20) µm in length, and large cheilocystidia up to 34 (40) µm long (Guzmán 2012). Indeed, these species require further studies and new collections in order to clarify their relationships.

Psilocybe semilanceata is a temperate species common in Europe and the USA as we state above, and its report from Africa by Samorini (2001), Stamets (1996), Guzmán et al. (1998) and Lakhanpal & Agnihotri (2007) ap-pear confused or inexact. It is probable that some of these reports refer to P. natalensis. None of those reports gives morphological macro- and micro-scopic features neither information on herbarium specimens.

Psilocybe subcubensis as we discuss above, is confusedly reported as P. cubensis and probably is a synonym of P. aquamarina.

New evidence of probable use of Psilocybe cubensis-complex in Africa. – Figs. 13–14.

One of the authors (Nixon) found some fimicolous mushrooms growing gregarious on dung, in pastures in western Uganda (Fig. 13), where there is an ancient cattle tradition. Local anecdotes suggest some awareness of the effects of these mushrooms, and perhaps a traditional use in the past. Nixon also observed a farm house with depicting two mushrooms resembling P. cubensis, below the traditional name of the family or “Butiko clan” (Fig. 14). Upon inquiry, the farm owner’s daughter explained that the mushrooms rep-resent the clan to which her family belonged, and that they held sacred meaning for their ancestors. Thus, it is probable that this represents the first evidence of indigenous use of P. cubensis-complex in Africa, confirming the hypothesis by Guzmán (1983) about the African origin of the neotropical P. cubensis-complex. Moreover, there are the neurotropic intoxication cases re-ported by Cullinan et al. (1945), and Charters (1957), which are related with the P. cubensis-complex. The Ugandan mushroom discussed above is tropical and for this reason it probably belongs to P. aquamarina (or P. subcubensis). Unfortunately we do not have herbarium material for study, only the good photograph (fig. 13). More mycological explorations are necessary in the cen-tral part of Africa, to check the real identification of P. cubensis-complex, as well as probably other unknown bluing species of Psilocybe, and further evidence of traditional uses.

Fig. 13–14. 13. Basidiomata of the Psilocybe cubensis-complex from Uganda. Phot. Nixon. Bar: 10 mm. 14. Depicting picture in a local farmhouse at Uganda, with the name of the family and mushrooms resembling Psilocybe cubensis or P. subcubensis.

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Acknowledgements

The authors thank their authorities for field and laboratory research. Also they thank Brian Akers in the USA for review of this paper. Moreover, Manuel Hernández and Juan Lara from Instituto de Ecología gave valuable support. It is also expressed our thanks to the curators of K and LZ Her-baria. An acknowledgement to the two reviewers of this paper, who have improved our writing.

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(Manuscript accepted 21 October 2013; Corresponding Editor: I. Krisai-Greilhuber)



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Your article appeared in Sydowia published by Verlagfiles.shroomery.org/attachments/20405034-Psilocybe.congolensis.pdfaquamarina is the correct name and synonym of P. subcubensis (Guzmán