Proc. lndian Acad. Sci. (Plant Sci.), Vol. 94, Nos 2 & 3, April & May 1985, pp Printed in India.

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1 Proc. lndian Acad. Sci. (Plant Sci.), Vol. 94, Nos 2 & 3, April & May 1985, pp Printed in India. New and rare entomogenous fungi from Amazonia ROBERT A SAMSON and HARRY C EVANS * Centraalbureau voor Schimmelcultures, P.O. Box 273, 3740 AG Baarn, the Netherlands 9 Commonwealth Mycological Institute, Ferry Lane, Kew, Surrey TW9 3AF~ UK Abstract, A new sclerotium-producing species on ah ant host, Hirsutella subramanianª anda new Cordyceps species, C. cantharelloides, with agaric-like fruitbodies on a wood-boring coleopteran larva are described and illustrated from specimens collected in the Amazonian rain forests. Keywords. Entomogenous fungÿ Hirsutelta subramanian Cordyceps cantharettoides. 1~ Introduction Entomogenous fungÿ have been collected by the junior author, over a 6-year period from 1974 to 1980, in the tropical forest of the Ecuadorian upper Amazon and the Brazilian lower Amazon, a region commonly known as Amazonia. These forests possess a rich and varied entomogenous mycoflora and some of the Cordyceps species from ant hosts have been the subject of recent papers (Evans and Samson 1982, 1984). In this contribution two new and apparently rare species from Amazonia are described. Despite the relative paucity of material, formal descriptions of these fungi are considered justified, because of their uniqueness and unusual morphology and hence their taxonomic significance. Unfortunately repeated attempts to isolate these fungi on agar media failed. We name the Hirsutella species after Prof. C V Subramanian asa sign of appreciation for his many contributions to hyphomycete taxonomy. 2. Hirsutella subramanianii sp. nov. (figures 1-2) Mycelium internum e catenis corporum hyphalium oblongorum vel rectangulariurn, hyalinorum, tenuitunicatorum, (6-5-)8.5-11(-13) x q compositum. Mycelium externurn inter segmenta corporis protrudens, primum albura, floccosum, hyphis hyalinis, levibus, septatis, 2-3 #m latis compositum, deinde brunnescens et lhsciculatum Phialides laterales sparsae in hyphis aeriis singulis, hyalinae, leyes, subcylindricae, l 5-25 #m longae, deorsum ad #m inflatae, sursum in collulum longum, verrucosum, pro latum, angustatae. Conidia hyalina, obclavata vel curvata (forma musae fructuum), continua, /~m, strato mucido tenui circumdata. Sclerotia copiosa in mycelio externo, primum albae, maturitate brunnescentia, verrucosa, globosa, 70-95/zm diam, e cellulis pseudocollenchymaticis globosis vel irregularibus crassitunicatis composita. Hototypus IMl , ad Pachycondylam sp. (Ponerinae, Formicidae), in terra forestali lectam, Monte Dourado, Rio Jari, Par in Brasilia, H C Evans, 19 Jan

2 310 Robert A Samson and Harry C Evans Figure 1. Hirsutella subramanianii. A. Ponerine ant showing floccose, external mycetium and dark-coloured sclerotia ( x 1.5). B-C. Sclerotia, Note the irregular dark-walled outer cells (B. x 190, C. x 550) D. Phialides ( x 950).

3 Entomooenous fungi from Amazonia I0 p-m it t ~P--~~ ( Figure 2, Hirsutella subramanianii. Camera lucida drawings. A-B. A-phialides with conidia C. B-phialides and conidia D. B-phialides on synnema. E. hyphal bodies. Internal mycelium consisting of compact chains of oblong to rectangular, hyaline, thin-walled hyphal bodies, (6.5-) (-13) x #m. External mycelium arising from body joints, initially white, floccose; hyphae hyaline, smooth, septate, 2-3/~m wide, becoming ginger-brown and uniting into ropes. Phialides borne directly on aerial mycelium (mononematous), as scattered lateral outgrowths; hyaline, smooth, subcylindricat, q in length, swolten at the base ( /~m width) tapering graduauy to a long, verruculose neck region ( pm wide). Conidia hyatine, curved, obclavate (or banana-shaped), aseptate, x pm, encased in a thin mucous sheath, giving the conidia a shape with ah apical projection anda truncate base. Sclerotia formed abundantly on the external mycelium, white at first, when mature chestnut to dark brown, verrucose, globose~ #m diam, composed of globose to irregular, thick-walled pseudocollenchyma. Holotype on Pachycondyla sp. (Ponerinae, Formicidae)0 tbrest soil, Monte Dourado, Rio Jari, Par Brazil, 19 Jan. 1980, H C Evans (IMI ). Paratype on a similar host from the same locality in Herb. cs~ RS The paratype is an older specimen, the sclerotia being predominantly dark brown and the external mycetium ginger brown. A narrow cylindricat synnema, 11 x 0-2 mm, emerges laterally from the thorax; ir is ginger brown at the base, becoming pale yellow of creara towards the fertile apex. Phialides are scattered or!ocally aggregated, variable but usually with a swollen, up to 5/~m wide, often verrucose basal cell, anda narrow, smooth neck. Conidia hyaline, smooth-walled, l-septate, narrowly clavate, q without a mucous sheath. It is considered, therefore, that Hirsutella subramanianii may produce two distinct

4 312 Robert A Samson and Harry C Evans types of phialides and conidia, as described for H. stilbelliformis Evans and Samson from various ant hosts (Evans and Samson 1982). Indeed, H. subramanianii helps to clarify some of the complex relationships within the genus Hirsutella and supports the conclusions reached by Evans and Samson (1982) when they placed the genus Synnematium Speare in synonymy with Hirsutella. The type species of that genus, Synnematium jonesii Speare, has subulate phialides and produces the conidia in mucoid spore balls, being further characterised by the formation of brown sclerotia. Speare (1920) depicted the conidia in groups and also encased them in individual mucous sheaths, as observed in the holotype of H. subramanianii, comparable to the B-conidia of H. stilbelliformis. In analogy with this interpretation, the conidiogenous structures occurring on the synnema of the paratype of H. subramanianii would correspond to the A-phialides and A-conidia; the latter in both species being typically 1-septate and devoid of a mucous covering. In conclusion, H. subramanianii, with its two types of phialide and conidia and its sclerotia, forms a link between H.jonesii (Speare) Evans and Samson, occurring on the homopteran host anda complex series of Hirsutella species occurring on ants (Evans and Samson 1982, 1984). By producing two morphologically distinct anamorphs, the fungus may have adapted both to wind (A-conidia) and rainsplash (B-conidia) dispersal. An added function of the mucous sheath, which characteristically darkens with age, is probably to increase conidial Iongevity by conferring protection from desiccation and solar radiation. The sclerotia are also obviously survival structures possibly enabling H. subramanianii to persist in the soil after the ant host has disintegrated. 3. Cordyceps cantharelloides sp. nov. (figures 3-5) Mycelium internum hyalinum, ex hyphis densis, regulariter septatis, 2"5-3~zm latis compositum, corpora hyphalia pauca, globosa ad ovoidea, #m. Mycelium externum exiguum, in parvis floccis hospitem obtegens, dilute brunneum, ex hyphis septatis, 1 '5-2#m latis compositum. Stromata bina, simplicia, e parte anteriore hospitis oriunda; stipes fere cylindricus, luteo-brunneus, levis (siccus sulcatus), mm; pars fertilis terminalis, lateritia, plus minusve discoidea, Cantharelli similis, x 3-5mm. Paries externa e cetlulis cylindricis palisadiformibus compositum. Perithecia omnino submersa, dense aggregata, papillis sursum protrudentia, anguste obclavata, #m, collo longo periphysibus repleto. Asci cylindrici, x 4-5/~m, sursum inspissati, in medio inflati et deorsum in stipitem longum angustati. Ascoporae hyalinae, filiformes, multiseptatae, guttulatae, utrinque apiculatae, non secedentes, x 2-2-5/~m. Anamorphosis ignota. Holotypus IMl , ad larvam Coleopterorum. in arbore sylvestri, Palora, Pastaza in Ecuadore, H C Evans, 30 Nov Internal mycelium hyaline, consisting of a dense weft of regularly septated hyphae, 2"5-3/an wide; hyphal bodies scarce, globose to ovoid, x pro. External mycelium almost lacking on the cadaver, only present on localized spots and then densely covering the host, pale brown, hyphae septate, 1.5-2#m wide. Stromata paired, unbranched, emerging from the head-region; stalk region yellow-brown, more or less cylindrical, smooth when fresh, but furrowed when dried, x 2-4mm; fertile area brick-red when dry, terminal, more or less discoid, strikingly reminiscent of

5 Entomogenous fungi from Amazonia 313 B C la E Figure 3. Cordyceps cantharelloides. A. Cla vae in situ. Note the fragments of the host and a pencil which has been placed in the tunnel in the living wood, and the two stromata one heavily parasitised, emerging laterally ( x 1). 13-D. Dried clavae. B-C. viewed from different angles ( x 2) D. Stilbella parasitised clava ( x 2) E. Fragments of targe larva of woodboring beetle after extraction (x2). POS.. 30

6 314 Robert A Samson and Harry C Et;ans Figure 4. Cordyceps cantharelloides. A. Perithecia ( x 55). B. Ou~er ceu wall of fertile head ( x 140). C. Asci ( 750). D. Ascospores ( 550).

7 Entomooenous fungi from Amazonia 315 ~os~m~ 1 O0 txrn 13 I0 /~m 10 p.mj ]! O / L~ l E Figure 5. Cordyceps cantharetloides. Camera lucida drawings. A. Clavae, B. Outer cell wau of fertile head. C. Perithecia. D. Asci. E. Ascospores. the cap of a Cantharellus, x 3-5 mm. Outer wall of the fertile head, composed of a palisade ofcylindrical thick-walled cells (figure 4B). Perithecia completely embedded, densely crowded papillae, protruding from the dorsal surface; narrowly obclavate, pm, with a long neck, lined with paraphyse. Asci cylindrical, almost as tong as the perithecial chamber, x 4-5#m, with thickened apical redon or cap, swollen in the centre, narrowing towards the long tail region. Ascospores hyatine, filiform, multiseptate, guttulate, with pointed apices, not breaking into partspores, #m. Anamorph not present, but fruitbodies parasitized by synnemata of the Stilbella type (figure 6). Synnemata consisting of smooth or hirsute stipe, sometimes terminating in a clavate slimy head. Phialides arising singly or in whorls of 2 to 3, either laterally from the hyphae of the synnema or terminally from the apex, flask-shaped with a long neck, x 1.5-2#m. Conidia usually developing in a viscous mucus, 1-4 per phialide, ellipsoidal to obovate, smooth-walled, hyaline, /.tm. Holotype on larva of Coleoptera in tree stem, Palora, Pastaza, Ecuador, 30 Nov. 1975, H C Evans (IMt ). Isotype consisting of one clava parasitised by Stilbella sp., in Herb. css, RS The collecting area was a remote forest in the Andean foothills (ca m alt.) in the Amazonian (eastern region of Ecuador). This species produces fruitbodies strikingly similar to the basidiocarps of some agarics, particularly to those of the genus Cantharellus. Indeed, during the initial collection, the two clavae which were emerging from a hole in a living tree (ca. 2 m above ground level) were mistaken for agarics and removed. Only then was it realised that they were growing out of the tunnel ofa boring

8 316 Robert A Samson and Harry C Evans Figure 6. Stilbet~a species. A. Synnemata ( 20). B-C. Phia[~des atong the synnema. (B. 550, C. x 720) D. conidia ( 1800).

9 Entomogenous fungi from Amazonia 317 insect and that the clavae penetrated laterally and vertically into the tree bole (some cm) and were attached to a large (7 0'8 cm) coleopteran larva. Due to the extreme hardness of the wood, the entire specimen took several hours to extract, which testifies to the bo ability of the insect (see also figure 3A). The characteristic shape of the clavae distinguishes this species from au known Cordyceps species (Kobayasi and Shimizu 1983). It is also possible that this unusual fungus might be macroscopically mistaken for a Hypomyces species parasitic on an agaric, since the crowded, completely immersed perithecia with bluntly rounded, slightly protruding papillae are also typical of representatives of this genus. The stromata were hyperparasitized by a Stilbella-like fungus. Petch (1924) and Kobayasi ( 1941) described Stilbella species (S. barnesii and S.falcata) and considered them as anamorphs of Cordyceps spp. without any firm evidence of the relationship. FoUowing our examination of material in Herb K and an analysis of the original descriptions, we conclude that the Stilbella is hyperparasitizing the clavae of C. barnesii and C.falcata and that the fungus found on C. cantharelloides has a similar parasitic habit. In his revision of Stilbella and related synnematous hyphomycetes, Seifert (in preparation) has shown that the species described here should be assigned a new specific epithet, since Stilbella barnesii and S. falcata are invalid names, being published without a Latin diagnose. Together with Stilbella kervillei (Samson et al 1984), these species should probably be excluded from Stilbella on the basis of phialide shape and synnema characters and placed in another genus possibly Polycephalomyces Kobayasi. Acknowledgements The authors thank Dr W Gatos for helpful suggestions and the Latin descriptions Mr Keith A Seifert kindly provided data on Stilbella. References Evans H C and Samson R A 1982 Cordyceps species and their anamorphs pathogenic on ants (Formicidae) in tropical forest ecosystems. I. The Cephalotes (Myrmicinae) complex; Trans. Br. Mycol. Soc Evans H C and Samson R A 1984 Cordyceps species and their anamorphs pathogenic on ants (Formicidae) in tropical forest ecosystems. II. The Camponotus (Formicinae) r Trans. Br. MycoL Soc Kobayasi Y 1941 The g enus Cordyceps and its allies; Sci. Rep. Tokyo Bunrika Daigaku BIM Kobayasi Y and ShimiziJ D 1983 Iconography of vegetable wasps and plantworms (Osaka: Hoikusha Publishing Co.) Petch T 1924 Studies in entomogenous fungi. IV. Some Ceylon Cordyceps; Trans. Br. Mycol. Soc Samson R A, Rombach M C and Seiferl K A 1984 Hirsutella guignardii and Stilbelta ker~illei, two troglobiotic entomogenous hyphomycetes; Persoonia I 34 Speare A T 1920 On certain entomogenous fungi; Mycologia P,S=3!