The genus CZurkeittdu (Basidiomycotina:
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1 Botanical Journal of the Linncan Sociely (1985), 91: With 1 figure The genus CZurkeittdu (Basidiomycotina: Agaricaceae) DAVID N. PEGLER, F.L.S. The Herbarium, Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3AE Received May 1984, acctpted for publication Jub 1984 PEGLER, D. N., The gmum C/arkeinda (Besidiomycodnu Aguiacae). A modem, illustrated description of Clarkeinda trachodes, the only species of a little known genus from SE Asia, is provided, together with an outline of the historical background. The outstanding problems concerning basidiospore colour, spore-wall structure and metachromasy, the status of clampconnections and the partial veil, and the pileipcllis structure are established on the basis of recent collections. The position of the genus within the family Agaricaceae is considered, and a close relationship with Chlorophyllurn and Hymmcrgaricus is confirmed. ADDITIONAL KEY WORDS:-Agariceae - Chitonia - Chitoniella - Leucocoprineae. CONTENTS Introduction Historical account Discussion of characters Classification Taxonomy References I INTRODUCTION Clarkeinda 0. Kuntze is a little known, monotypic genus belonging to the family Agaricaceae (Basidiomycotina: Agaricales). It is found only in SE Asia. Earlier accounts were based upon poorly preserved material and incomplete information. Although it is most often associated with the genus Chlorophyllurn Massee, an examination of more recently collected material shows it to represent an interesting link between the tribes Agariceae P. Henn. and Leucocoprineae Singer. HISTORICAL ACCOUNT Clarkeinda truchodes (Berk.) Singer has a long and complex history. In 1846, George Gardner, the Superintendent of the Royal Botanic Garden, Peradeniya in the Kandy District of Sri Lanka, sent a collection of dried fleshy fungi, together with water-colour sketches, to the Reverend M. J. Berkeley in England /85/ SOS.OO/O The Linnean Society of London
2 246 D. N. PEGLER Berkeley (1847: 487 bis) described as new one of the agaric specimens, Gardner no. 64, under the name Agaricus trachodes, n. sp. with the following diagnosis: Pileo carnoso e convex0 expanso demum depress0 verrucoso interstitiis sericeis; stipite sursum attenuato farcto albo; annulo amplissimo deflexo; lamellis angustis subliberis pallidis demum fuscus. The species was stated to have the appearance of a Lepiota Pers.: S. F. Gray, but the lamellae finally darkened to brown, hence the choice of Agaricus L.: Fr. subgen. Psalliota (Fr.) Loudon. Berkeley & Broome (1873) was based upon a large collection of fungi sent by G. H. K. Thwaites, also from the Royal Botanic Garden, Peradeniya. In this account two new species were proposed, namely Agaricus pedilius Berk. & Br. and A. poderes Berk. & Br., the latter was stated to be closely related but differing above all in the presence of a large white ring on the stipe. The material of both these collections was accompanied by excellent water-colour paintings by a local artist, William de Alwis. The following year, Fries (1874: 277) proposed, in his account of the European Hymenomycetes, a new subgenus, Chitonia Fr., for species closely allied to Agaricus but with the universal veil persisting as a volva at the stipe base. Only one species, Agaricus coprinus Fr., from Europe was described but the subgeneric diagnosis contained the statement Species typicae extra-europeae V.C. A. podileus Berkl. [recte, pedilius] volva laxa, stipite exannulato, et A. podeces Berkl. [recte, poderes] volva circumscissa, annulo amplo, habitu omnino Amanitae, quarum ceylonicorum icones misit Berkeley. Karsten ( 1879: 482) raised the subgenus to generic rank but excluded the annulate species and made no mention of the tropical species, dealing only with species occurring in Finland. It therefore became necessary to select a type species for the genus Chitonia (Fr.) P. Karst. As the annulate species, namely A. poderes, was explicitly excluded by Karsten, it was necessary to choose one of the other original species cited by Fries, and Donk (1962: 50) selected A. pedilius. Hennings (1898: 240) introduced the generic name Chitoniella for the annulate species (A. poderes), which was a generic name provisionally used by Massee (1892: 418). As A. pedilius and A. poderes have subsequently been confirmed to be conspecific, and since both have an annulus, the typification becomes a matter of nomenclatural rather than of taxonomic interest. Unfortunately, Chilonia (Fr.) P. Karst. is impriorable on account of three earlier angiospermal homonyms, namely Chitonia D. Don (Don, 1823: 285) in Melastomaceae, Chitonia Mociiio & Sesse (De Candolle, 1824: 707) in Zygophyllaceae, and Chitonia R. A. Salisbury (Salisbury, 1866: 51) in Liliaceae. In order to remedy this situation, Clarkeinda was proposed by Kuntze ( : 848), and although he did not give a diagnosis, he did provide a reference to the Fries taxon, Agaricus subgenus Chitonia, and Clarkeinda pedilia (Berk. & Br.) 0. Kuntze was selected as the type species by Donk ( 1962: 54). The etymology of Clarkeinda honours Charles Baron Clarke, the former Kew botanist, and also refers to Iv66a, pertaining to India. DISCUSSION OF CHARACTERS Although all of the type and authentic material of Agaricus pedilius, A. poderes and A. trachodes has proved to be immature, Petch (1910: 396) indicated that the three names represented the same species and this has been confirmed by subsequent examination and comparison with additional material. The species
3 CLARKEINDA 247 is correctly named Clarkeinda trachodes (Berk.) Singer, and two detailed accounts have been published by Petch (1908) and Boedijn (1934), based on a personal knowledge of fresh specimens. In both cases, the generic name C hitoniella P. Henn. was employed. The account by Petch comprises a revision of the type material, together with additional information obtained from collections made by him in Sri Lanka. Boedijn (1934) reported the species from Java, where he found it to be not uncommon, and this is the only published record of the species outside of Sri Lanka. However, material received in recent years at Kew has established its occurrence also in Selangor State (Malay Peninsula), so that the species may eventually prove to be widespread throughout SE Asia. Berkeley (1847) and Berkeley & Broome (1 873) always referred the species to Agaricus subgenus Psalliota on the basis of the overall stature of the basidiomes and the apparent fuscescent character of the hymenophore, although no spore details were given on either occasion. It was Petch (1908: 115) who emphasized that the spores shed by fresh specimens were not the anticipated purplish-brown colour but rather olive-green. On this basis, Petch compared and related the species to another green-spored genus, Chlorophyllurn Massee, belonging to Agaricaceae Cohn tribe Leucocoprineae Singer, and not to tribe Agariceae P. Henn. Boedijn also considered the other chlorosporic agarics but commented that any classification based on spore colour alone was artificial and failed to show a true relationship between the different species. He also indicated that the very unusual epithelial structure of the pileipellis was very reminiscent of that found in Psalliota alphitochroa (Berk. & Br.) Petch ( = Agaricus alphitochrous Berk. & Br.), a species recently placed by Heinemann (1981) in the genus Hymenagaricus Heinem. of the tribe Agariceae. Singer (1951: 412) closely allied Clarkeinda and Chlorophyllurn within in the Leucocoprineae although recognizing several important separating characters, including the smaller spores and the formation of a persistent volva. Owing to the immaturity and poor preservation of all the type material, Singer was unable to confirm the final colour of the spores, the presence or absence of clamp-connections, or the metachromatism of the spores with cresyl blue. Examination of recent material has ascertained these characters: Spore print: A recent collection (Hong Lay Thong 247/4), gathered in 1975 in Selangor, is accompanied by a spore print deposited on to a glass microscope slide. The colour of this print ranges from Sulphine Yellow (Ridgway, 1912) (Munsell notation 5Y/6.5/6.3) to Orange-Citrine (M. 2.5Y/4.9/6.0). The collector s notes described the fresh deposit as straw-citrine and the fresh hymenophore as sulphur yellow. This range closely matches that found in Chlorophyllurn and would support a classification within the Leucocoprineae. The dried hymenophore has darkened considerably to fuscous brown. Metachromay: Cresyl blue mounts of mature basidiospores do not demonstrate a positive metachromatic reddening of the endosporium, but rather the spore wall shows a uniform orthochromatic reaction. This is the reaction also shown with Chlorophyllurn spores, and it separates the two genera from the other members of the Leucocoprineae. Spores of genera belonging to the Agariceae are not metachromatic with cresyl blue. Spore-wall structure (Fig. ID): The ovoid spores are apically truncated by a
4 248 D. N. PEGLER Figure I. Clarkcinda trachodcs. A. Habit of basidiome (after Petch). B-C. Sketch of Agaricus pcdilius TYPE, Thwaifcs I221 (after de Alwis). D. Spores. E. Basidia. F. Cheilocystidia. G. VS. pileipellis pellicle.
5 CLARKEINDA 249 small but distinct germ-pore, as is typically found in the Leucocoprineae. However, it should be noted that Hymenagaricus hymenopileus (Heinem.) Heinem., from Singapore, also has truncated spores with an indistinct germ-pore, although differently pigmented. Clamp-connections: Hyphae from all parts of the basidiome were examined but no clamp-connections at the septa could be demonstrated. Pileipellis (Fig. lc): The pileal surface of C. trachodes is characterized by an unexpanded cartilaginous pellicle over the central region. The pileipellis is formed by a trichodermial palisade consisting of chains of shortened doliiform elements, which more closely resemble the structure of Hymenagaricus species than of the genus Chlorophyollum. Partial veil: A persistent membranous annulus is formed on all basidiomes examined, attached to the upper stipe. The original description of A. pedilius was largely based on a water-colour painting (Fig. 1B-C) of a small unopened basidiome so that the partial veil was not immediately apparent. Nevertheless a more careful observation confirms its presence. The illustrations of Agaricus poderes, A. trachodes, and an additional illustration by Petch, all show a large, hanging membranous annulus. CLASSIFICATION Clarkeinda holds an interesting intermediate position within the natural classification of the Agaricaceae. There can be no doubt that it belongs to this family, but the precise position is open to conjecture, and it may be best regarded as representing an intermediate link between the tribes Agariceae and Leucocoprineae. The extremely unusual pileipellis structure recalls Hymenagaricus, a genus with a similar equatorial-palaeotropical distribution. The spores of H. hymenopileus further support a relationship, for although the spores of Clarkeinda are pale coloured they are not metachromatic as in typical members of the Leucocoprineae. This character is also shared with Chlorophyllum, as is the green colour of the spore deposit and the spore wall. The three tropical genera, Chlorophyllum, Clarkeinda and Hymenagaricus have a pale-coloured context which rapidly discolours to orange-red on exposure. It is likely that these genera are closely related and may ultimately form a separate tribe within the Agaricaceae which will be distinct both from the Agariceae and Leucocoprineae. TAXONOMY Clarkeinda Clarkeinda 0. Kuntze, Revisio generum plantarum, 2: 848 ( ). SYNONYMS: Agaricus L.: Fr. subgen. Chitonia Fr., Hymenomycetes Europaei: 277 (1874). Chitonia (Fr.) P. Karst. in Bidrag till Kannedom af Finlands Natur och Folk, 32: 482 (1879), non D. Don (1823, Melastomaceae), Mociiio & Sesst in DC ( 1824, Zygophyllaceae), R. A. Salisbury ( 1866, Liliaceae).
6 250 D. N. PEGLER Chitoniella Massee, British Fungus-Jlora, 1: 4 18 ( 1892), nomen provisiorum. Chitoniella P. Henn. in Engler & Prantl, Die natiirlichen PJlanzenfamilien, 1, Abt. 1** (13-15): 240 (1898). Chitonis Clements, Genera of Fungi: 114 (1909). BASIDIOME large, fleshy, lepiotoid. PILEUS hemispherical to applanate, retaining an unexpanded, cartilaginous pellicle over the central region, not hygrophanous, dry, becoming rimose. LAMELLAE free, remote, white to greenish, fuscescent, crowded. STIPE central, annulate and volvate. ANNULUS complex, membranous. VOLVA persistent, closely applied to stipe base. CONTEXT thick, pale discolouring orange-red on exposure. Hyphal system monomitic, with inflated generative hyphae; clamp-connections absent. SPORE PRINT yellowish green. SPORES < 10 pm long, ovo-ellipsoid, apically truncated by a germ-pore, yellowish-green, dextrinoid, not metachromatic with cresyl blue, smooth, thick walled. Lamella edge heteromorphous to sterile, with inflated cheilocystidia. Pleurocystidia none. Pileipellis a trichodermium formed by agglutinated chains of doliiform elements. Development bivelangiocarpic. Terrestrial, SE Asia. TYPE SPECIES: Clarkeinda trachodes (Berk.) Singer. (BASIONYM of LECTOTYPE: Agaricus pedilius Berk. & Br. (Donk, 1962: 55). Clarkeinda trachodes (Berk.) Singer in Lilloa, 22: 4 13 ( ). SYNONYMS: Agaricus trachodes Berk. in Hooker s London Journal of Botany, 6: 487 bis (1847). Agaricus pedilius Berk. & Br. in Journal of the Linnean Sociely (Botany), 14: 32 (1873). TYPE: SRI LANKA, Peradeniya, Thwaites 1221 (K, holotype). Agaricus poderes Berk. & Br. in Journal of the Linnean Sociep (Botany), 14: 32 ( 1873). TYPE: SRI LANKA, Peradeniya, Thwaites 1220 (K, holotype). Chitonia pedilia (Berk. & Br.) Sacc., Sylloge Fungorum, 5: 992 (1887). Chitonia poderes (Berk. & Br.) Sacc., Sylloge Fungorum, 5: 992 (1887). Clarkeinda pedilia (Berk. & Br.) 0. Kuntze, Revisio generum plantarum, 2: 848 (1891). Clarkeinda poderes (Berk. & Br.) 0. Kuntze, Revisio generum plantarum, 2: 848 (1891). Chitoniella poderes (Berk. & Br.) P. Henn. in Engl. & Prantl, Die nnturlichen PJlanzenfamilien, 1, Abt. 1** (13-15): 240 (1898). Chitoniella trachodes (Berk.) Petch in Annals of the Royal Botanic Garden, Peradeniya, 4: 396 (1910). TYPE: SRI LANKA, Peradeniya, Gardner, 64 (K, holotype). PILEUS (-190) mm in diameter, hemispherical expanding to convex or almost applanate; surface pale brown, greyish-brown or clay colour, sometimes white, with the central region forming a large, non-expanding, cartilaginous, vinaceous brown pellicle, often with a recurved margin; remainder of surface radially rimose, finally disrupting to form narrow, revolute, greyish-brown to vinaceous brown squamules, together with numerous, small, loosely floccose verrucae; margin appendiculate with velar remnants. LAMELLAE free, remote from stipe, at first white, becoming sulphur-green, drying fuscescent, narrow up to 7 mm wide, very crowded, with lamellulae of two lengths; edge entire. STIPE x 7-20 mm, up to 30 mm in diameter at the swollen base, obclavate to
7 CLARKEINDA almost cylindric, solid to fistulose; surface concolorous with the pileus or greyer, paler above the annulus, bruising reddish-brown, striate, with minute, furfuraceous squamules. ANNULUS present, attached to upper stipe, complex, thick, very broad, white, lobed, spreading or pendulous, with floccose squamules on underside. VOLVA present, mm deep, grey or purplish-grey, floccose, lobed, usually closely appressed to stipe and often inconspicuous. CONTEXT of pileus up to 10 mm thick at the disk, white, rapidly discolouring to orange-red on exposure, consisting of loosely woven, much inflated, thin-walled, hyaline hyphae, 6-40 pm in diameter; clamp-connections absent. SPORE PRINT Sulphine Yellow (M.5Y/6.5/6.3) to Orange-Citrine (M.2.5Y/4.9/6.0). SPORES x (6.2 k0.5 x 4.3 f 0.3) pm, Q = 1.44; ovoid to ellipsoid, pale yellowish-green to greenish-brown, dextrinoid, not metachromatic with cresyl blue, smooth, with a thickened wall, truncated by an apical germ-pore. BASIDIA x 7-9 pm, clavate, bearing four short sterigmata. Lamella edge heteromorphous to sterile, with scattered to crowded cheilocystidia. CHEILOCYSTIDIA x pm, piriform or inflated clavate, at times clavatocylindric with a long pedicel, hyaline, thin walled, occasionally crystalline encrusted. Hymenophoral trama regular or nearly so, hyaline, with inflated hyphae, pm diameter. Subhymenial layer well developed, pm wide, pseudoparenchymatous. Pileipellis pellicle formed by an agglutinated, stratified trichodermium, consisting of short, branching chains of about 5-8, subisodiametric elements, x 4-15 pm; terminal elements 8-23 x 7-13 pm, globose to short piriform, thin walled, with a pale brown vacuolar pigment. Towards the pileal margin the exposed hypodermium consists of radially repent hyphae, with short doliiform elements. ILLUSTRATIONS: Boedijn (1934: 277, fig. 1, spores and cheilocystidia only); Horak (1968: 160); Petch (1908: pl. 1-11). Figure IA-G. DISTRIBUTION: SE Asia: Java, Selangor (Malay Peninsula), Sri Lanka. OTHER SPECIMENS EXAMINED: MALAY PENINSULA: Selangor, Kepong, 2 1 : 1972, Ivory FP51 (K); 5 ix 1972, Hong Lay Thong FP124/9 (K); Pasoh Forest Reserve, ix 1975, Hong Lay Thong 247/4 (K). 25 I REFERENCES BERKELEY, M. J., Decades of fungi XV-XIX. Ceylon fungi. Hooker s London Journal of Botay. 6: 479 bis-514. BERKELEY, M. J. & BROOME, C. E., Enumeration of the fungi of Ceylon. Part 11, containing the remainder of the Hymenomycetes, with the remaining established tribes of fungi. Journal of the Linnean Sociely (Botany), 14: BOEDIJN, K. B., The genus Chiloniella with remarks on the Chlorosporae. Buflrtin du Jardin Botanique, Buitenzorg, shie 3, 13: DE CANDOLLE, A. P., Prodromus systematis naturalis regni uegetabilis, I. Paris: Truettel & Wiirtz. DON, D., An illustration of the natural family of plants called Melastomaceae..2ltmoirs.J thr Hirnrrian.Vaturn1 History Socieb, 4: DONK, M. A,, The generic names proposed for Agaricaceae. BeiheJie zur NoNova Hedwigia, 5: FRIES, E., Hvmenomycetes Europaei sive epicriseos systematis mycologici. Upsaliae. HEINEMANN, P., Hymenagaricus Heinem. gen. nov. Bulletin du Jardin botanique national dt Belgique, 51: HENNINGS, P., Hymenomycetineae. In 4. Engler & K. Prantl (Eds), Die naturlirhen PJanzenfamilien, I, I, Abt. I** (13-15): HORAK, E., Synopsis generum Agaricalium (Die Gattungstypen der Agaricales). Beitrdge tur KyptogamrnJora der Schweiz, 13: 1-74 I.
8 252 D. N. PEGLER KARSTEN, P. A., Rysslands, Finlands och den Skandinaviska haihns. Hattsvampar. 1. Skifsvampar. Bidrag till Kanncdorn af Finlandr Natur och Folk, 32: KUNTZE, O., RcUiSio Gcncrurn Planfarum, 2: Leipzig: Arthur Felix. MASSEE, G., British FungUr-poru. London: George Bell C Sons. PETCH, T., The genus Chifoniclla. Annals of thc Royal Botanic Cardcn, Pcradcniya, 4: PETCH, T., Revision of Ceylon fungi (Part 11). Annals of thc Royal Eofanic Gardcn, Pcradcniya, 4: RIDGWAY, R., Color Sfandards and Color Norncnclafure. Washington. SALISBURY, R. A., Thc Ccncra of Plants. London: John van Voorst. SINGER, R., The Agaricales (Mushrooms) in modern taxonomy. Lilloa, 22:
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