StuDIES IN MYCOLOGY 7: –9. 2007.
doi:10.3114/sim.2007.7.01
Phylogenetic classiication of Cordyceps and the clavicipitaceous
fungi
Gi-Ho Sung1, Nigel L. Hywel-Jones2, Jae-Mo Sung3, J. Jennifer Luangsa-ard4, Bhushan Shrestha3 and Joseph W.
Spatafora1
1
Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331–2902, U.S.A.; 2Mycology Laboratory, National Center for
Genetic Engineering and Biotechnology, Science Park, Pathum Thani, Thailand; 3Department of Applied Biology and Entomopathogenic Fungal
Culture Collection (EFCC), Kangwon National University, Chuncheon 200-701, Republic of Korea; 4Phylogenetics Laboratory, National Center
for Genetic Engineering and Biotechnology, Science Park, Pathum Thani, Thailand.
*Correspondence: Gi-Ho Sung, sungg@science.oregonstate.edu
Abstract: Cordyceps, comprising over 400 species, was historically classiied in the Clavicipitaceae, based on cylindrical asci, thickened
ascus apices and iliform ascospores, which often disarticulate into part-spores. Cordyceps was characterized by the production of welldeveloped often stipitate stromata and an ecology as a pathogen of arthropods and Elaphomyces with infrageneric classiications emphasizing
arrangement of perithecia, ascospore morphology and host afiliation. To reine the classiication of Cordyceps and the Clavicipitaceae, the
phylogenetic relationships of 162 taxa were estimated based on analyses consisting of ive to seven loci, including the nuclear ribosomal
small and large subunits (nrSSU and nrLSU), the elongation factor 1α (tef1), the largest and the second largest subunits of RNA polymerase
ІІ (rpb1 and rpb2), β-tubulin (tub), and mitochondrial ATP6 (atp6). Our results strongly support the existence of three clavicipitaceous clades
and reject the monophyly of both Cordyceps and Clavicipitaceae. Most diagnostic characters used in current classiications of Cordyceps (e.g.,
arrangement of perithecia, ascospore fragmentation, etc.) were not supported as being phylogenetically informative; the characters that were
most consistent with the phylogeny were texture, pigmentation and morphology of stromata. Therefore, we revise the taxonomy of Cordyceps
and the Clavicipitaceae to be consistent with the multi-gene phylogeny. The family Cordycipitaceae is validated based on the type of Cordyceps,
C. militaris, and includes most Cordyceps species that possess brightly coloured, leshy stromata. The new family Ophiocordycipitaceae is
proposed based on Ophiocordyceps Petch, which we emend. The majority of species in this family produce darkly pigmented, tough to pliant
stromata that often possess aperithecial apices. The new genus Elaphocordyceps is proposed for a subclade of the Ophiocordycipitaceae, which
includes all species of Cordyceps that parasitize the fungal genus Elaphomyces and some closely related species that parasitize arthropods.
The family Clavicipitaceae s. s. is emended and includes the core clade of grass symbionts (e.g., Balansia, Claviceps, Epichloë, etc.), and
the entomopathogenic genus Hypocrella and relatives. In addition, the new genus Metacordyceps is proposed for Cordyceps species that are
closely related to the grass symbionts in the Clavicipitaceae s. s. Metacordyceps includes teleomorphs linked to Metarhizium and other closely
related anamorphs. Two new species are described, and lists of accepted names for species in Cordyceps, Elaphocordyceps, Metacordyceps
and Ophiocordyceps are provided.
Taxonomic novelties: New family: Ophiocordycipitaceae G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora. New genera: Elaphocordyceps
G.H. Sung & Spatafora, Metacordyceps G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora. New species: Metacordyceps yongmunensis G.H.
Sung, J.M. Sung & Spatafora; Ophiocordyceps communis Hywel-Jones & Samson. New combinations: Cordyceps confragosa (Mains) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, C. ninchukispora (C.H. Su & H.-H. Wang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora;
Elaphocordyceps capitata (Holmsk.) G.H. Sung, J.M. Sung & Spatafora, E. delicatistipitata (Kobayasi) G.H. Sung, J.M. Sung & Spatafora, E.
fracta (Mains) G.H. Sung, J.M. Sung & Spatafora, E. inegoënsis (Kobayasi) G.H. Sung, J.M. Sung & Spatafora, E. intermedia (S. Imai) G.H.
Sung, J.M. Sung & Spatafora, E. japonica (Lloyd) G.H. Sung, J.M. Sung & Spatafora, E. jezoënsis (S. Imai) G.H. Sung, J.M. Sung & Spatafora,
E. longisegmentis (Ginns) G.H. Sung, J.M. Sung & Spatafora, E. minazukiensis (Kobayasi & Shimizu) G.H. Sung, J.M. Sung & Spatafora, E.
miomoteana (Kobayasi & Shimizu) G.H. Sung, J.M. Sung & Spatafora, E. ophioglossoides (Ehrh.) G.H. Sung, J.M. Sung & Spatafora, E.
paradoxa (Kobayasi) G.H. Sung, J.M. Sung & Spatafora, E. ramosa (Teng) G.H. Sung, J.M. Sung & Spatafora, E. rouxii (Cand.) G.H. Sung, J.M.
Sung & Spatafora, E. subsessilis (Petch) G.H. Sung, J.M. Sung & Spatafora, E. szemaoënsis (M. Zang) G.H. Sung, J.M. Sung & Spatafora, E.
tenuispora (Mains) G.H. Sung, J.M. Sung & Spatafora, E. toriharamontana (Kobayasi) G.H. Sung, J.M. Sung & Spatafora, E. valliformis (Mains)
G.H. Sung, J.M. Sung & Spatafora, E. valvatistipitata (Kobayasi) G.H. Sung, J.M. Sung & Spatafora, E. virens (Kobayasi) G.H. Sung, J.M. Sung
& Spatafora; infraspeciic: E. intermedia f. michinokuënsis (Kobayasi & Shimizu) G.H. Sung, J.M. Sung & Spatafora, E. ophioglossoides f.
alba (Kobayasi & Shimizu ex Y.J. Yao) G.H. Sung, J.M. Sung & Spatafora, E. ophioglossoides f. cuboides (Kobayasi) G.H. Sung, J.M. Sung &
Spatafora; Metacordyceps brittlebankisoides (Z.Y. Liu, Z.Q. Liang, Whalley, Y.J. Yao & A.Y. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
M. campsosterni (W.M. Zhang & T. H. Li) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, M. chlamydosporia (H.C. Evans) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, M. liangshanensis (M. Zang, D. Liu & R. Hu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, M. taii (Z.Q.
Liang & A.Y. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora; Ophiocordyceps agriotidis (A. Kawam.) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora, O. ainictos (A. Möller) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. amazonica (Henn.) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora, O. aphodii (Mathieson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. appendiculata (Kobayasi & Shimizu) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, O. arachneicola (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. arbuscula (Teng) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, O. armeniaca (Berk. & M.A. Curtis) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. asyuënsis
(Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. aurantia (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora, O. australis (Speg.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. barnesii (Thwaites) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora, O. bicephala (Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. bispora (Stiler) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, O. brunneipunctata (Hywel-Jones) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cantharelloides (Samson & H.C. Evans) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, O. carabidicola (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cicadicola
(Teng) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. clavata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O.
coccidiicola (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. coccigena (Tul. & C. Tul.) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, O. cochlidiicola (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. corallomyces (A. Möller) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, O. crassispora (M. Zang, D. R. Yang & C.D. Li) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. crinalis
(Ellis ex Lloyd) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cucumispora (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora, O. curculionum (Tul. & C. Tul.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cusu (Pat.) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora, O. cylindrostromata (Z.Q. Liang, A.Y. Liu & M.H. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. dayiensis (Z.Q. Liang)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. dermapterigena (Z.Q. Liang, A.Y. Liu & M.H. Liu) G.H. Sung, J.M. Sung, Hywel-Jones &
SuNG ET AL.
Spatafora, O. dipterigena (Berk. & Broome) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. discoideicapitata (Kobayasi & Shimizu) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, O. ditmarii (Quél.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. dovei (Rodway) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, O. elateridicola (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. elongata
(Petch) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. elongatiperitheciata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, O. elongatistromata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. emeiensis (A.Y. Liu & Z.Q. Liang)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. engleriana (Henn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. entomorrhiza
(Dicks.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. evdogeorgiae (Koval) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. falcata
(Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. falcatoides (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
O. fasciculatistromata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. ferruginosa (Kobayasi & Shimizu) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, O. iliformis (Moureau) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. formicarum (Kobayasi) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, O. forquignonii (Quél.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. furcicaudata (Z.Q.
Liang, A.Y. Liu & M.H. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. gansuënsis (K. Zhang, C. Wang & M. Yan) G.H. Sung, J.M. Sung,
Hywel-Jones & Spatafora, O. geniculata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. gentilis (Ces.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, O. glaziovii (Henn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. goniophora (Speg.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, O. gracilioides (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. gracilis (Grev.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, O. heteropoda (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. hiugensis (Kobayasi &
Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. huberiana (Henn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. humbertii
(C.P. Robin) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. insignis (Cooke & Ravenel) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
O. irangiensis (Moureau) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. japonensis (Hara) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, O. jiangxiensis (Z.Q. Liang, A.Y. Liu & Y.C. Jiang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. jinggangshanensis (Z.Q. Liang,
A.Y. Liu & Y.C. Jiang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. kangdingensis (M. Zang & Kinjo) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora, O. kniphoioides (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. koningsbergeri (Penz. & Sacc.) G.
H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. konnoana (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O.
lachnopoda (Penz. & Sacc.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. larvarum (Westwood) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, O. lloydii (H.S. Fawc.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. longissima (Kobayasi) G.H. Sung, J.M. Sung, HywelJones & Spatafora, O. lutea (Moureau) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. melolonthae (Tul. & C. Tul.) G.H. Sung, J.M. Sung,
Hywel-Jones & Spatafora, O. michhganensis (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. minutissima (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. monticola (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. mrciensis (J.C.
Jung, Z.Q.Liang, Soytong & K.D. Hyde) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. multiaxialis (M. Zang & Kinjo) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, O. myrmecophila (Ces.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. neovolkiana (Kobayasi) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, O. nepalensis (M. Zang & Kinjo) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. nigra
(Samson, H.C. Evans & Hoekstra) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. nigrella (Kobayasi & Shimizu) G.H. Sung, J.M. Sung,
Hywel-Jones & Spatafora, O. nigripes (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. nutans (Pat.) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, O. obtusa (Penz. & Sacc.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. octospora (M. Blackwell & Gilb)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. odonatae (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. osuzumontana
(Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. ouwensii (Höhn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
O. owariensis (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. oxycephala (Penz. & Sacc.) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora, O. pentatomae (Koval) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. petchii (Mains) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, O. proliferans (Henn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. pseudolloydii (H.C. Evans & Samson) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, O. pseudolongissima (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. purpureostromata
(Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. ravenelii (Berk. & M.A. Curtis) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
O. robertsii (Hook.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. rubiginosiperitheciata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung,
Hywel-Jones & Spatafora, O. rubripunctata (Moureau) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. ryogamiensis (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. salebrosa (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. scottiana (Olliff)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. selkirkii (Olliff) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. sichuanensis (Z.Q.
Liang & B. Wang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. sinensis (Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O.
smithii (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. sobolifera (Hill ex Watson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
O. sphecocephala (Klotzsch ex Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. stipillata (Z.Q. Liang & A.Y. Liu) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, O. stylophora (Berk. & Broome) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. sublavida (Mains) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, O. supericialis (Peck) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. takaoënsis (Kobayasi)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. taylorii (Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. thyrsoides (A. Möller)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. tricentri (Yasuda) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. uchiyamae (Kobayasi
& Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. variabilis (Petch) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. voeltzkowii
(Henn.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. volkiana (A. Möller) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O.
wuyishanensis (Z.Q. Liang, A.Y. Liu & J.Z. Huang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. yakusimensis (Kobayasi) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, O. zhangjiajiensis (Z.Q. Liang & A.Y. Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora; infraspeciic:
O. amazonica var. neoamazonica (Kobayasi & Hara) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. cucumispora var. dolichoderi (H.C.
Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. kniphoioides var. dolichoderi (H.C. Evans & Samson) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, O. kniphoioides var. monacidis (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O.
kniphoioides var. ponerinarum (H.C. Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. lloydii var. binata (H.C. Evans &
Samson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. melolonthae var. rickii (Lloyd) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
O. owariensis f. viridescens (uchiyama & udagawa) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. purpureostromata f. recurvata
(Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, O. supericialis f. crustacea (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, HywelJones & Spatafora; Pochonia parasitica (G.L. Barron) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora.
Key words: Clavicipitaceae, Cordyceps, Cordycipitaceae, Elaphocordyceps, Metacordyceps, multigene phylogeny, Ophiocordyceps,
Ophiocordycipitaceae.
INTRODUCTION
Cordyceps Fr. is the most diverse genus in the family
Clavicipitaceae in terms of number of species and host
range (Kobayasi 1941, 1982, Mains 1957, 1958). There
are estimated to be more than 400 species (Mains 198,
Kobayasi 1982, Stensrud et al. 200) although this is
expected to be an underestimation of the extant global
diversity (Hawksworth & Rossman 1997). Its host range
is broad, ranging from ten orders of arthropods to the
trufle-like genus Elaphomyces, although most species
are restricted to a single host species or a set of closely
related host species (Kobayasi 1941, 1982, Mains
1957, 1958). The distribution is cosmopolitan, including
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
all terrestrial regions except Antarctica, with the height
of known species diversity occurring in subtropical and
tropical regions, especially East and Southeast Asia
(Kobayasi 1941, 1982, Samson et al. 1988). The genus
is generally included in the family Clavicipitaceae,
based on its cylindrical asci, thickened ascus apices,
and iliform ascospores that often disarticulate into partspores (Mains 198, Kobayasi 1982, Rossman et al.
1999, Hywel-Jones 2002). Cordyceps is characterized
and distinguished from other genera of the family by
its production of supericial to completely immersed
perithecia on stipitate and often clavate to capitate
stromata and its ecology as a pathogen of arthropods
and the fungal genus Elaphomyces (Kobayasi 1941,
Mains 197, 198, Kobayasi & Shimizu 190, Rogerson
1970).
Modern infrageneric classiications of Cordyceps
have been based primarily on the taxonomic studies
of Kobayasi (1941, 1982) and Mains (198) (but see
Massee 189). Kobayasi (1941, 1982) recognized
three subgenera (C. subg. Cordyceps, C. subg.
Ophiocordyceps, and C. subg. Neocordyceps),
emphasizing arrangement of perithecia and morphology
of asci, ascospores and part-spores. Species of C.
subg. Cordyceps (type C. militaris) were characterized
by the production of either immersed or supericial
perithecia produced at approximately right angles
(ordinal) to the surface of the stroma and ascospores
that disarticulate into part-spores at maturity. Cordyceps
subg. Ophiocordyceps (Petch) Kobayasi (type C. blattae
Petch) was distinguished by the production of whole
ascospores that do not disarticulate into part-spores
and, in some species, asci lacking pronounced apical
hemispheric caps. Cordyceps subg. Neocordyceps
Kobayasi (type C. sphecocephala (Klotzsch ex Berk.)
Berk. & M.A. Curtis) was characterized by perithecia
immersed at oblique angles in the clava region of the
stroma and ascospores that disarticulate into partspores upon maturity.
(198)
expanded
the
infrageneric
Mains
classiication with a different emphasis on diagnostic
characters and recognized two additional subgenera,
C. subg. Racemella (Ces.) Sacc. and C. subg.
Cryptocordyceps Mains. Cordyceps subg. Racemella
(type C. memorabilis (Ces.) Sacc.) included species
that produce supericial perithecia and asci with
hemispheric to short cylindrical caps. Cordyceps
subg. Cryptocordyceps (type C. ravenelii Berk. & M.A.
Curtis) was diagnosed by the production of brown,
partly immersed to supericial perithecia in a palisadelike layer at more or less right angles to the surface
of the stroma. Kobayasi and Mains also differed in
their treatments of C. subg. Ophiocordyceps and C.
subg. Neocordyceps. In contrast to Kobayasi (1941),
who essentially adopted the diagnosis of Petch (1931)
but at the rank of subgenus, Mains (198) placed
only C. blattae and C. peltata Wakef. in C. subg.
Ophiocordyceps based on their lack of a thickened
ascus apex, thus deemphasizing the importance of
ascospore disarticulation at the subgeneric level.
Furthermore, Mains (198) did not recognize C. subg.
Neocordyceps, rather he included species with oblique
perithecia in C. subg. Cordyceps sect. Cremastocarpon
subsect. Entomogenae. Currently, the subgenera C.
subg. Cordyceps, C. subg. Ophiocordyceps, and C.
subg. Neocordyceps sensu Kobayasi (1941) have
been arguably the most widely used infrageneric taxa
of Cordyceps (Zang & Kinjo 1998, Artjariyasripong
et al. 2001, Hywel-Jones 2002, Sung & Spatafora
2004, Stensrud et al. 200) with the relatively recent
addition of C. subg. Bolacordyceps O.E. Erikss., which
is characterized by the production of bola-ascospores
(Eriksson 198). Although this ascospore form has
been likened to the South American bola or the East
Asian ninchuk (martial arts weapon), the overall form is
best likened to that of a skipping rope. The two handles
of the skipping rope are two terminal sets of four cells.
The ‘rope’ is a slender hyphal thread, which appears to
lack cytoplasm or, at most, has relic quantities.
In addition to the morphological characters discussed
above, host afiliation has played an important role
in the classiication of Cordyceps (Massee 189,
Kobayasi 1982). Cordyceps species that parasitize
the trufle genus Elaphomyces have been recognized
as a unique taxon. The genus Cordylia Fr. (1818) was
once assigned for the mycogenous Cordyceps species
(Massee 189) although it is a homonym of Cordylia
Pers. 1807. Kobayasi (1941, 1982) also recognized the
mycogenous Cordyceps species as taxonomic units
(e.g., C. subg. Cordyceps sect. Cystocarpon subsect.
Eucystocarpon ser. Mycogenae) and emphasized the
utility of host afiliations in delimiting closely related
species of arthropod pathogens. Mains (198) adopted
Kobayasi’s treatment of the parasites of Elaphomyces,
but questioned whether morphologically similar species
on different insect hosts (e.g., C. irangiensis Moureau
and C. sphecocephala attacking ants and wasps,
respectively) are conspeciic. The applicability of hosts
as a taxonomic character is complicated, however,
due to the dificulty in identifying immature hosts (e.g.,
larvae and pupae) and insuficient host identiication for
many herbarium collections.
Several phylogenetic studies employing ribosomal
DNA (Artjariyasripong et al. 2001, Sung et al. 2001,
Stensrud et al. 200) have been conducted to test and
reine the classiication of Cordyceps. Such studies
were restricted by both limited taxon sampling and
the inadequate resolution power of ribosomal DNA,
resulting in limited conclusions regarding systematics of
the genus. Recent phylogenetic studies (Spatafora et al.
2007, Sung et al. 2007) based on multiple independent
loci provided a greater level of resolution and support,
and revealed that neither Cordyceps nor the family
Clavicipitaceae is monophyletic. Three monophyletic
groups of the clavicipitaceous fungi were recognized,
all of which include species of Cordyceps. These
results reject the current infrafamilial classiication
(Diehl 190) and indicate that the phylogenetic
diversity of Cordyceps is representative of the entire
family Clavicipitaceae (Spatafora et al. 2007, Sung et
al. 2007). Therefore, a new classiication of Cordyceps
and the Clavicipitaceae is necessary to relect the
current hypotheses of phylogenetic relationships and
to be predictive in nature.
7
SuNG ET AL.
Here, we conducted the most extensive multigene phylogenetic analyses to provide a basis for
the phylogenetic classiication of Cordyceps and
the clavicipitaceous fungi. The main objectives of
this study are to 1) reassess the morphological traits
used in the current classiications of Cordyceps in the
context of phylogeny, 2) investigate the taxonomic
utility of the anamorphic forms in classiication of
Cordyceps and better understand the teleomorph–
anamorph connections, and 3) revise the classiication
of Cordyceps and Clavicipitaceae to be consistent with
phylogenetic relationships.
MATERIALS AND METHODS
Taxon and character sampling
A total of 12 taxa were sampled from Clavicipitaceae
and other families of Hypocreales with Glomerella
cingulata (Stoneman) Spauld. & H. Schrenk
(Glomerellaceae) and Verticillium dahliae Kleb.
(Plectosphaerellaceae) included as outgroups (Table 1).
DNA extractions from cultures or herbarium specimens
were conducted using a FastDNA kit (Qbiogene)
following the manufacturer’s instruction, with minor
modiications. Polymerase chain and sequencing
reactions were performed as previously described
(Sung et al. 2007). DNA sequence data unique to this
study were determined from ive genes, including the
nuclear ribosomal small and large subunits (nrSSU and
nrLSU), the elongation factor 1α (tef1), and the largest
and second largest subunits of RNA polymerase ІІ
(rpb1 and rpb2). These sequences were combined with
data from 91 taxa, which were obtained from Sung et
al. (2007). Information pertaining to voucher numbers
concerning the sequences is provided in Table 1.
Sequence alignment and phylogenetic analyses
Sequences were edited using SeqEd 1.0.3 (Applied
Biosystems Inc.) and contigs were assembled using
CodonCode Aligner 1.4 (CodonCode Inc.). Sequences
of each gene partition were initially aligned with Clustal
W 1.64 (Thompson et al. 1994) and appended to
an existing alignment (Sung et al. 2007). This initial
alignment was manually edited as necessary in
MacClade 4.0 (Maddison & Maddison 2000). All ive
gene regions sampled in this study were concatenated
into a single, combined data set (12-taxon -gene data
set) with ambiguously aligned regions excluded from
phylogenetic analyses. Sequences from two additional
gene regions, β-tubulin (tub) and mitochondrial ATP6
(atp6), from Sung et al. (2007) were also combined
with the 12-taxon -gene data set to generate a
supermatrix of 12-taxon 7-gene data set.
In order to detect incongruence among the ive
individual gene regions sampled in this study, bootstrap
proportions were used for each individual data set with
the 107 taxa that was complete for all ive genes (Table
1). Bootstrap proportions (BP) were determined in a
maximum-parsimony framework using the program
PAUP* 4.0b10 (Swofford 2002). Only parsimony-
8
informative characters were used with the following
search options: 100 replicates of random sequence
addition, TBR branch swapping, and MulTrees OFF.
The incongruence was assumed to be signiicant
if two different relationships for the same set of taxa
were both supported with greater than 70 % bootstrap
proportions by different genes (Mason-Gamer & Kellogg
1996, Wiens 1998). Previous studies revealed that tub
was double copy in some clavicipitaceous species
(Spatafora et al. 2007), and Sung et al. (2007) also
showed that while atp6 possessed conlicting data for
a limited number of taxa, the conlict was localized and
the locus simultaneously provided increased level of
support for other nodes. Thus, although we focused our
sampling and analyses of the ive aforementioned loci,
we also conducted phylogenetic supermatrix analyses
with tub and atp6 (12-taxon 7-gene) to detect any
increased nodal support provided by those two loci.
Maximum parsimony (MP) analyses were
conducted on the 12-taxon -gene and the 12taxon 7-gene data set (Table 1, Fig. 3). All characters
were equally weighted and unordered. MP analyses
were performed using only parsimony-informative
characters with the following settings: 100 replicates of
random sequence addition, TBR branch swapping, and
MulTrees ON. Phylogenetic conidence was assessed
by nonparametric bootstrapping (Felsenstein 198). A
total of 200 bootstrap replicates were used to calculate
bootstrap proportions; bootstrapping used the same
search options with ive replicates of random sequence
addition per bootstrap replicate.
Maximum likelihood (ML) analyses were performed
with RAxML-VI-HPC v2.2. using a GTRCAT model of
evolution with 2 rate categories (Stamatakis et al.
200). The model was separately applied to each of the
eleven partitions, which consisted of nrSSU, nrLSU and
the nine codon positions of three protein-coding genes
(tef1, rpb1, and rpb2). Nodal support was assessed
with nonparametric bootstrapping using 200 replicates.
Bayesian Metropolis coupled Markov chain Monte
Carlo (B-MCMCMC) analyses were performed on
combined datasets using MrBayes 3.0b4 (Huelsenbeck
& Ronquist 2001). In estimating the likelihood of each
tree, we used the general time-reversible model, with
invariant sites and gamma distribution (GTR+I+Γ) and
employed the model separately for each partition. In
an initial analysis, a B-MCMCMC analysis with ive
million generations and four chains was conducted in
order to test the convergence of log-likelihood. Trees
were sampled every 100 generations, for a total of
50,000 trees. For a second analysis, ive independent
Bayesian runs with two million generations and random
starting trees were conducted to reconirm log-likelihood
convergence and mixing of chains.
In addition to the analyses with 12-taxon -gene
data set, a series of analyses were conducted in MP, ML,
and Bayesian frameworks with different taxon samplings
(107- and 12-taxon -gene data sets) to address the
potential topological effects of missing data. Previous
phylogenetic and simulation studies demonstrated that
the phylogenetic analyses are often not negatively
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
affected if less than 0 % characters are missing for
each taxon in the phylogenetic analyses (Wiens 2003,
Phylippe et al. 2004). In this study, we assumed that the
phylogenetic analysis is not confounded if the taxa were
complete for at least three out of ive gene partitions.
Therefore, ten taxa (Table 1) in the 162-taxon 5-gene
data set that were complete for only two gene partitions
were excluded to generate the 12-taxon -gene data
set. A 107-taxon -gene data set that does not contain
any missing data in gene partitions was also prepared
to compare the phylogenetic relationships between
107-taxon and 152-taxon 5-gene analyses. MP, ML,
and Bayesian analyses based on the 12-taxon -gene
data set (Figs 1–2) showed that the C. sphecocephala
clade is characterized by long-branch lengths relative
to the rest of the clavicipitaceous fungi. To address
the impact of the C. sphecocephala clade on the
phylogenetic resolution, we excluded all members of
the C. sphecocephala clade from the 12-taxon -gene
data set and constructed a 147-taxon -gene data set.
RESULTS
Sequence alignment
The combined 162-taxon 5-gene dataset consisted of
4927 base pairs of sequence data (nrSSU 1102 bp,
nrLSU 94 bp, tef1 1020 bp, rpb1 803 bp, rpb2 1048
bp). As a result of excluding ambiguously aligned
regions, the inal alignment comprised 4600 base pairs
(nrSSU 1088 bp, nrLSU 77 bp, tef1 1020 bp, rpb1
77 bp, rpb2 1048 bp), 1882 of which were parsimonyinformative (nrSSU 233 bp, nrLSU 220 bp, tef1 4 bp,
rpb1 382 bp, rpb2 81 bp). A total of 107 taxa were
complete for all ive genes and the number of complete
taxa for each gene was as follows: nrSSU 18 taxa,
nrLSU 17 taxa, tef1 149 taxa, rpb1 143 taxa, rpb2 122
taxa (Table 1).
Phylogenetic analyses
The reciprocal comparisons of 70 % bootstrap trees from
individual data sets of the 12-taxon -gene dataset
did not reveal any signiicantly supported contradictory
nodes (data not shown). These results were interpreted
as indicating that no strong incongruence existed
among the individual data sets that would be indicative
of different phylogenetic gene histories (e.g., lineage
sorting or horizontal gene transfer). As a result, all ive
individual data sets were combined in simultaneous
analyses.
MP analyses of the 162-taxon 5-gene data set
resulted in 156 equally parsimonious trees. These
trees were 21,323 steps with a consistency index (CI)
of 0.198 and a retention index (RI) of 0.131. One
of 1 equally parsimonious trees is shown in Fig. 1.
Nodes that collapse in the strict consensus tree
are denoted with asterisks. ML analyses of the 12taxon -gene data set resulted in a tree with a loglikelihood (–ln) of 92019.9. In the Bayesian analyses,
the ive-million generation analysis converged on
the log-likelihood (harmonic mean = –ln 991.22)
at approximately around 250,000 generations. The
results from ive of two-million generation analyses
also showed a convergence on the log-likelihood at
approximately 20,000 generations and the topologies
were identical. As a result, the 3,000 trees from the irst
300,000 generations were deleted from the ive million
generation analysis to generate a 0 % majority-rule
consensus tree.
A 0 % majority consensus tree (Fig. 2) was
generated from the million generation analysis.
Since the topology of ML analyses (tree not shown)
was nearly identical to that of the Bayesian consensus
tree of Fig. 2, the bootstrap proportions of ML analyses
are provided above the corresponding nodes in Fig. 2.
Previous studies have shown that in interpreting the
supports of the phylogenetic estimates of relationships,
the posterior probability tends to overestimate the
phylogenetic conidence (Doaudy et al. 2003, Lutzoni
et al. 2004, Reeb et al. 2004). As a result, the posterior
probabilities were used as a supplementary indicator
to bootstrap proportions. In this study, nodes were
considered strongly supported when supported by
both bootstrap proportions (BP ≥ 70 %) and posterior
probabilities (PP ≥ 0.95) (Lutzoni et al. 2004).
Phylogenetic relationships of the clavicipitaceous
fungi
All MP, ML, and Bayesian analyses of the ive-gene
12-taxon -gene data set recognized three wellsupported clades of clavicipitaceous fungi (Figs 1–2),
designated here as Clavicipitaceae clades A, B, and
C (Figs 1–2), following the convention of the previous
phylogenetic studies (Spatafora et al. 2007, Sung et al.
2007). These clades were statistically well supported
by the bootstrap proportions of the MP (MP-BP) and
ML (ML-BP) analyses and posterior probabilities (PP)
of the Bayesian analyses (clade A: MP-BP = 98 %, MLBP = 99 %, PP = 1.00; clade B: MP-BP = 93 %, ML-BP
= 98 %, PP = 1.00; clade C: MP-BP = 100 %, ML-BP =
100 %, PP = 1.00). A sister-group relationship between
clades A and B was also strongly supported (MP-BP =
72 %, ML-BP = 90 %, PP = 1.00). The monophyletic
group of clade C and Hypocreaceae was moderately
to strongly supported (MP-BP = 63 %, ML-BP = 92 %,
PP = 1.00).
Clavicipitaceae clade A comprised ive statistically
well-supported subclades (Figs 1–2, 4). These were
labelled in Figs 1, 2, and 4 as the C. taii clade (MPBP = 73 %, ML-BP = 78 %, PP = 1.00), the Claviceps
clade (MP-BP = 95 %, ML-BP = 98 %, PP = 1.00), the
Hypocrella clade (MP-BP = 99 %, ML-BP = 99 %, PP =
1.00), the Shimizuomyces clade (MP-BP = 100 %, MLBP = 100 %, PP = 1.00), and the Torrubiella luteorostrata
clade (MP-BP = 100 %, ML-BP = 100 %, PP = 1.00).
As indicated previously by Sung et al. (2007), internal
relationships among these ive subclades were not
strongly supported in MP and ML analyses (Figs 1–2,
4).
Clavicipitaceae clade B consisted of ive
major subclades designated as the C. gunnii, C.
ophioglossoides, C. sphecocephala, C. unilateralis,
and Pa. lilacinus clades (Figs 1–2, ). Nearly all of
9
SuNG ET AL.
Glomerella cingulata
Glomerella cingulata
100
100
88
10
Verticillium dahliae
100 Bionectria cf. aureofulva
Bionectria ochroleuca
100
Hydropisphaera peziza
100
Bionectriaceae
84
Hydropisphaera erubescens
100
Roumegueriella rufula
Roumegueriella rufula
Ophionectria trichospora
94
Pseudonectria rousseliana
90
Cosmospora coccinea
Nectriaceae
Nectria cinnabarina
87
Leuconectria clusiae
Viridispora diparietispora
Verticillium incurvum
100
Hypomyces polyporinus
Sphaerostilbella berkeleyana
Hypocreaceae
100
Aphysiostroma stercorarium
Hypocrea lutea
Torrubiella wallacei
Simplicillium lamellicola
100
100
100
Simplicillium obclavatum
Simplicillium clade
Simplicillium lanosoniveum
Simplicillium lanosoniveum
98
Lecanicillium antillanum
Lecanicillium aranearum
Torrubiella ratticaudata
98
Engyodontium aranearum
100 Cordyceps cardinalis
Cordyceps cardinalis
Lecanicillium fusisporum
Cordyceps clade
Lecanicillium psalliotae
92
Lecanicillium psalliotae
Lecanicillium dimorphum
Isaria farinosa
99
Isaria farinosa
Cordyceps tuberculata
Lecanicillium attenuatum
Clavicipitaceae clade C
Torrubiella confragosa
98
100 Beauveria caledonica
* Cordyceps scarabaeicola
Cordyceps staphylinidicola
99
Cordyceps cf. takaomontana
Isaria cf. farinosa
100
Isaria tenuipes
97
100 Cordyceps cf. ochraceostromata
100 Cordyceps sp. EFCC 2535
Cordyceps takaomontana
87
Cordyceps bifusispora
80
Cordyceps bifusispora
100
Microhilum oncoperae
100
100 Cordyceps kyusyuensis
Cordyceps militaris
Verticillium sp. CBS 102184
99
100 Cordyceps cf. pruinosa EFCC 5197
81
Cordyceps cf. pruinosa EFCC 5693
100
Mariannaea pruinosa
99Cordyceps cf. pruinosa EFCC 10627
98 Cordyceps cf. pruinosa EFCC 10684
92 Phytocordyceps ninchukispora
Phytocordyceps ninchukispora
100
Aschersonia
badia
99
Hypocrella schizostachyi
Hypocrella clade
70
Aschersonia placenta
Hypocrella sp. GJS 89604
100 Shimizuomyces paradoxus
*
Shimizuomyces clade
Shimizuomyces paradoxus
100 Torrubiella luteorostrata
T. luteorostrata clade
Torrubiella luteorostrata
Epichloë typhina
91
Claviceps paspali
100
Claviceps fusiformis
100 Claviceps purpurea
95
Claviceps purpurea
100
Claviceps clade
Verticillium epiphytum
98
74
Verticillium epiphytum
Myriogenospora
atramentosa
100
Balansia pilulaeformis
100
100
Balansia epichloë
Balansia henningsiana
Paecilomyces marquandii
*
100 Paecilomyces carneus
Paecilomyces carneus
Clavicipitaceae clade A
100 Cordyceps sp. EFCC 2131
Cordyceps sp. EFCC 2135
73
*
Nomuraea rileyi
73
Metarhizium album
98
100
Cordyceps sp. NHJ 12118
93
Metarhizium flavoviride
100 Cordyceps sp. OSC 110996
*
Metarhizium anisopliae
C. taii clade
72
Cordyceps taii
100 Cordyceps liangshanensis
Cordyceps liangshanensis
Rotiferophthora angustispora
*
100
Cordyceps chlamydosporia
Pochonia chlamydosporia
Tolypocladium parasiticum
100
Pochonia rubescens
100 Pochonia bulbillosa
Pochonia gonioides
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Cordyceps sphecocephala
Cordyceps tricentri
Cordyceps nutans
C. sphecocephala clade
Hymenostilbe aurantiaca
* 100
100 Cordyceps irangiensis
Cordyceps irangiensis
Nomuraea atypicola
99 Paecilomyces lilacinus
P. lilacinus clade
100Paecilomyces lilacinus
Paecilomyces lilacinus
Cordyceps gunnii
97
Haptocillium zeosporum
100
C. gunnii clade
100
Haptocillium balanoides
Haptocillium sinense
93
Cordyceps capitata
Cordyceps longisegmentis
71
Cordyceps japonica
Cordyceps fracta
Cordyceps paradoxa
C. ophioglossoides clade
Cordyceps inegoensis
Cordyceps
jezoensis
*
Cordyceps ophioglossoides
Clavicipitaceae clade B
Cordyceps subsessilis
100 Cordyceps gracilis
*
Cordyceps gracilis
100
Cordyceps heteropoda
71
Cordyceps heteropoda
Cordyceps melolonthae
100 Cordyceps variabilis
*
Cordyceps variabilis
Cordyceps konnoana
96
Cordyceps konnoana
*
Cordyceps superficialis
99
100 Cordyceps nigrella
Cordyceps ravenelii
Cordyceps entomorrhiza
Cordyceps elongata
100 Cordyceps rhizoidea
*
Cordyceps rhizoidea
*
100 Cordyceps sp. NHJ 12581
Cordyceps sp. NHJ 12582
C. unilateralis clade
*
*
100
Cordyceps sp. OSC 110997
Cordyceps unilateralis
78
Cordyceps aphodii
100
Cordyceps brunneipunctata
96 Cordyceps sobolifera
*
Cordyceps longissima
96 Cordyceps yakusimensis
Cordyceps agriotidis
Cordyceps coccidiicola
100 Cordyceps cf. acicularis
93
Cordyceps cochlidiicola
100 Hirsutella sp. NHJ 12525
Hirsutella sp. NHJ 12527
86 Cordyceps robertsii
Cordyceps
sinensis
98
100 Cordyceps acicularis
Cordyceps acicularis
100 Cordyceps stylophora
Cordyceps stylophora
100
*
93
*
*
100
Fig. 1. Continued.
the subclades in clade B were strongly supported by
bootstrap proportions and posterior probabilities (C.
gunnii clade: MP-BP = 97 %, ML-BP = 100 %, PP =
1.00; C. ophioglossoides clade: MP-BP = 71 %, MLBP = 88 %, PP = 1.00; C. sphecocephala clade: MPBP = 100 %, ML-BP = 100 %, PP = 1.00, Pa. lilacinus
clade: MP-BP = 64 %, ML-BP = 76 %, PP = 1.00). It
should be noted, however, that the C. unilateralis
subclade was not resolved in the MP analyses (Fig.
1). This lack of resolution was due to the instability of
the C. sphecocephala clade, which is characterized
by long-branch lengths relative to the rest of the
clavicipitaceous fungi. Multiple placements of the
C. sphecocephala subclade, ranging from a basal
lineage of the Clavicipitaceae clade B to a terminal
clade nested within the C. unilateralis subclade, were
present among the most parsimonious trees (data not
shown). Our ML and Bayesian results (Fig. 3) indicate
that the C. sphecocephala subclade is either a sister-
group of the C. unilateralis subclade (107-taxon -gene
data set) or in the terminal group of the C. unilateralis
subclade (152-taxon 5-gene data set). In MP, ML, and
Bayesian analyses with a supermatrix of 12-taxon 7gene data set (Fig. 3), the C. sphecocephala subclade
was placed as a terminal group of the C. unilateralis
subclade with strong support (MP-BP = 89 %, ML-BP
= 94 %, PP = 1.00) as seen in the previous analyses
(Sung et al. 2007). In the light of long-branch attraction
problems associated with the MP analyses (Fig. 1),
we use the Bayesian tree (Fig. 2) to further discuss
the relationships in clade B and we conclude that the
C. sphecocephala subclade was best included as a
member of the C. unilateralis subclade (Figs 2, ). In
interpreting the C. unilateralis subclade in terms of
statistical support, we used the bootstrap proportions
and posterior probabilities (MP-BP = 88 %, ML-BP =
88 %, PP = 1.00) based on the results of 147-taxon 5gene data set (Fig. 3).
Fig. 1 (Page 10/11). Phylogenetic relationships among 162 taxa in the Clavicipitaceae and other families in the Hypocreales. One of 1 equally
parsimonious trees is shown based on maximum parsimony analyses with combined data set of ive genes (i.e., nrSSU, nrLSU, tef1, rpb1 &
rpb2). Bootstrap proportions (MP-BP) of ≥ 70 % are provided above corresponding nodes and in a thicker line. Internodes that are collapsed in
strict consensus tree are marked with an asterisk (*).
11
SuNG ET AL.
100
Bionectria cf. aureofulva
Bionectria ochroleuca
Hydropisphaera peziza
100
Bionectriaceae
Hydropisphaera erubescens
85
100
Roumegueriella rufula
100
Roumegueriella rufula
100
Ophionectria trichospora
Pseudonectria rousseliana
100
73
Cosmospora coccinea
100
Nectriaceae
Nectria cinnabarina
100
97
Leuconectria clusiae
Viridispora diparietispora
100
Verticillium incurvum
100
100
Aphysiostroma stercorarium
100 80
Hypocrea lutea
Hypocreaceae
100
Hypomyces
polyporinus
100
Sphaerostilbella
berkeleyana
98
92
Simplicillium lamellicola
100
100
Simplicillium obclavatum
100
Simplicillium clade
100
100
Simplicillium lanosoniveum
100
100
Simplicillium lanosoniveum
100
Torrubiella wallacei
100
Engyodontium aranearum
91
Lecanicillium antillanum
100
Lecanicillium aranearum
100
Torrubiella ratticaudata
100
100 Cordyceps cardinalis
100 Cordyceps cardinalis
100
Lecanicillium dimorphum
Lecanicillium psalliotae
100
Lecanicillium fusisporum
100
Cordyceps clade
92
100
99
Lecanicillium psalliotae
100
Isaria farinosa
99
Isaria farinosa
99
100
Cordyceps tuberculata
100
82
Lecanicillium attenuatum
Torrubiella
confragosa
Clavicipitaceae clade C
100
98
Beauveria caledonica
100
100
Cordyceps scarabaeicola
100
Cordyceps staphylinidicola
98
Cordyceps cf. takaomontana
Isaria cf. farinosa
100
100
Cordyceps cf. ochraceostromata
88
Isaria tenuipes
100
100
100
Cordyceps sp. EFCC 2535
100
100
100 Cordyceps takaomontana
76 100 Cordyceps bifusispora
100 100 Cordyceps bifusispora
88
Microhilum oncoperae
100
95
100 Cordyceps kyusyuensis
100
97
Cordyceps militaris
100
Verticillium sp. CBS 102184
100
98
100 Cordyceps cf. pruinosa EFCC 5197
100
100 100 Cordyceps cf. pruinosa EFCC 5693
96
Mariannaea pruinosa
100 99
Cordyceps cf. pruinosa NHJ 10627
100
96
Cordyceps cf. pruinosa NHJ 10684
100 100
100 Phytocordyceps ninchukispora
94
100100 Phytocordyceps ninchukispora
100 Shimizuomyces paradoxus
Shimizuomyces clade
100 Shimizuomyces paradoxus
Aschersonia badia
99
97
Hypocrella schizostachyi Hypocrella clade
96
100
90
Aschersonia placenta
100
99
Hypocrella
sp. GJS 89104
100
100
Torrubiella luteorostrata
100
T. luteorostrata clade
Torrubiella luteorostrata
100
Epichloë typhina
100
Claviceps paspali
100
100
96
Claviceps fusiformis
100
Claviceps purpurea
100
98
Claviceps purpurea
100
100
100
Verticillium epiphytum
Claviceps clade
Verticillium epiphytum
99
76
100
Myriogenospora atramentosa
100
100
100
Balansia pilulaeformis
86
100
100
Balansia epichloë
100
Balansia henningsiana
100
100 Pochonia bulbillosa
Clavicipitaceae clade
100
100 Pochonia gonioides
Pochonia rubescens
100
Tolypocladium parasiticum
Rotiferophthora angustispora
84
78
100
Cordyceps chlamydosporia
100
Pochonia
chlamydosporia
100
100
Nomuraea rileyi
98
Metarhizium album
99 100
Cordyceps sp. NHJ 12118
100 100
C. taii clade
Metarhizium flavoviride
100 79100
Cordyceps taii
100
100
Cordyceps
sp.
OSC
110996
100
90
Metarhizium anisopliae
Paecilomyces marquandii
100
100
Paecilomyces carneus
Paecilomyces carneus
100
100
Cordyceps liangshanensis
100 Cordyceps liangshanensis
100 Cordyceps sp. EFCC 2131
100 Cordyceps sp. EFCC 2135
100
Outgroup
100
100
12
100
A
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Nomuraea atypicola
Paecilomyces lilacinus
P. lilacinus clade
Paecilomyces lilacinus
100
100 Paecilomyces lilacinus
100
Cordyceps gunnii
100
Haptocillium zeosporum
100
C. gunnii clade
100
Haptocillium balanoides
100
Haptocillium sinense
97
99
Cordyceps capitata
Cordyceps longisegmentis
88 100
Cordyceps japonica
98
100
Cordyceps fracta
100
C. ophioglossoides clade
Cordyceps paradoxa
Cordyceps jezoensis
Cordyceps inegoensis
Clavicipitaceae
Cordyceps ophioglossoides
Cordyceps subsessilis
100
Cordyceps variabilis
Cordyceps variabilis
100
100
Cordyceps gracilis
98
70
100 Cordyceps gracilis
98
100
Cordyceps heteropoda
Cordyceps heteropoda
100
Cordyceps melolonthae
100 Cordyceps konnoana
99
Cordyceps konnoana
100
C. unilateralis clade
Cordyceps superficialis
100 100
100
Cordyceps nigrella
100
100
Cordyceps
ravenelii
100
Cordyceps entomorrhiza
100
Cordyceps aphodii
100 100
Cordyceps brunneipunctata
99
Cordyceps
sobolifera
100
100
Cordyceps longissima
100
Cordyceps yakusimensis
100
100
Cordyceps tricentri
100
Cordyceps nutans
100
Cordyceps sphecocephala
Hymenostilbe aurantiaca
100
96
100 Cordyceps irangiensis
100
100
C. sphecocephala clade
100 Cordyceps irangiensis
Cordyceps elongata
100 Cordyceps rhizoidea
100 Cordyceps rhizoidea
100
Cordyceps sp. NHJ 12581
100
Cordyceps sp. NHJ 12582
100
100
Cordyceps sp. OSC 110997
99
Cordyceps unilateralis
100
70
Cordyceps agriotidis
Cordyceps coccidiicola
100
100 Hirsutella sp. NHJ 12525
96
C. unilateralis clade
100 Hirsutella sp. NHJ 12527
100
100
Cordyceps cf. acicularis
99
Cordyceps cochlidiicola
81
100
Cordyceps robertsii
100
Cordyceps sinensis
94 99
100
Cordyceps acicularis
100
0.1 substitutions/site
Cordyceps acicularis
100
100
Cordyceps stylophora
100 Cordyceps stylophora
72
100
100
100
clade B
Fig. 2. Continued.
Clavicipitaceae clade C comprised two wellsupported subclades (Figs 1–2, 8). The Simplicillium
subclade (MP-BP = 100 %, ML-BP = 100 %, PP =
1.00) consisted of isolates of the anamorph genus
Simplicillium, most of which were isolated as parasites
of other fungi. The Cordyceps subclade (MP-BP = 98 %,
ML-BP = 100 %, PP = 1.00) included numerous species
of Torrubiella and species of Cordyceps that produce
pallid to brightly coloured stromata with ascospore
morphologies ranging from whole ascospores to
part-spores to bola-ascospores according to species.
Importantly, the Clavicipitaceae clade C included C.
militaris and represents the core Cordyceps clade. The
remaining species, Torrubiella wallacei H.C. Evans,
was also a member of the Cordyceps clade with strong
support (ML-BP = 91 %, PP = 1.00) in ML and Bayesian
analyses (Figs 2, 8), but could not be conidently
assigned to either subclade in MP analyses (Fig. 1).
DISCUSSION
Phylogenetic implications on the systematics
of the genus Cordyceps
The present and previous phylogenetic analyses
(Spatafora et al. 2007, Sung et al. 2007) have revealed
that species in the Clavicipitaceae form three strongly
supported monophyletic groups based on combined
data sets of six or seven genes (the genes analyzed
herein with and without atp6). Although more taxa were
used in our study, these results were consistent with
the previous studies, recognizing three monophyletic
groups designated as Clavicipitaceae clades A–C (Figs
1–2). In addition, our results also support the paraphyly
of the Clavicipitaceae as deined by the monophyly of
Clavicipitaceae clade C and Hypocreaceae (Figs 1–2).
Although the paraphyly of the Clavicipitaceae (clade C
Fig. 2 (Page 12/13). Phylogenetic relationships among 162 taxa in the Clavicipitaceae and other families in the Hypocreales. A 0 %
majority consensus tree is shown based on Bayesian analyses with combined data set of ive genes (i.e., nrSSU, nrLSU, tef1, rpb1 & rpb2).
Outgroups (Glomerella cingulata and Verticillium dahliae) are not shown. Posterior probabilities (PP) of ≥ 0.95 are provided in percentage below
corresponding nodes. Bootstrap proportions (ML-BP) are obtained in maximum likelihood analyses and shown above corresponding nodes for
≥ 70 %. Internodes that are supported with both bootstrap proportions (ML-BP ≥ 70 %) and posterior probabilities (PP ≥ 0.95) are considered
strongly supported and drawn in a thicker line.
13
SuNG ET AL.
+ Hypocreaceae) was moderately supported (MP-BP
= 63 %) in the 162-taxon 5-gene MP analyses (Fig. 1),
it was strongly supported (ML-BP = 92 %, PP = 1.00)
in the ML and Bayesian analyses (Fig. 2) and more
robustly addressed in the previous MP analyses, which
investigated localized conlicts among gene partitions
and compared bootstrap proportions among alternative
sampling strategies (Sung et al. 2007).
The phylogenetic hypothesis presented here
contradicts current infrafamilial classiication of
the Clavicipitaceae. Diehl (190) proposed three
subfamilies, Oomycetoideae, Clavicipitoideae, and
Cordycipitoideae, based on the development of stromata,
anamorphic characters and host afiliations. However,
these three subfamilies do not coincide with the three
clades of the Clavicipitaceae inferred in the present
MP analyses
100
100
107-taxon
5-gene
100
100
100
89
100
100
83
99
100
147-taxon
5-gene
100
100
72
100
100
88
100
152-taxon
5-gene
98
100
100
100
96
100
100
162-taxon
5-gene
100
98
100
72
98
93
71
100
162-taxon
7-gene
100
98
70
96
96
70
89
100
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. sphecocephala clade
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
ML analyses
100
90
100
96
86
100
100
99
100
85
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. sphecocephala clade
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
91
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
P. lilacinus clade
C. gunnii clade
C. ophioglossoide clade
C. unilateralis clade
C. sphecocephala clade
C. unilateralis clade
100
100
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. sphecocephala clade
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
analyses (Figs 1–2). Clavicipitaceae clade A includes
members of all three subfamilies (e.g., Claviceps of
Clavicipitoideae, Cordyceps of Cordycipitoideae, and
Hypocrella of Oomycetoideae), whereas the remaining
clades only comprise members of Cordycipitoideae
(e.g., Cordyceps and Torrubiella). Importantly, all
three major clades include members of Cordyceps,
indicating that Cordyceps, like Clavicipitaceae, is
not monophyletic (Figs 1–2). As a result, the three
recognized well-supported clades (clades A–C) of the
clavicipitaceous fungi represent a robust phylogenetic
framework for the taxonomic revision of Cordyceps and
the Clavicipitaceae.
In the current infrageneric classiication of the
genus, Cordyceps comprises four subgenera (C.
subg. Bolacordyceps, C. subg. Cordyceps, C. subg.
100
100
100
91
100
72
74
100
100
88
100
100
100
92
100
76
79
99
100
100
100
92
100
99
100
90
72
98
88
100
100
72
100
100
100
84
98
88
94
100
Bayesian analyses
100
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
C. sphecocephala clade
100
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
100
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
C. sphecocephala clade
C. unilateralis clade
100
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
C. sphecocephala clade
C. unilateralis clade
100
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
C. sphecocephala clade
C. unilateralis clade
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
99
100
100
100
100
100
100
100
100
100
100
95
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
100
97
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
C. sphecocephala clade
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
C. sphecocephala clade
C. unilateralis clade
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
C. sphecocephala clade
C. unilateralis clade
Hypocreaceae
Clavicipitaceae C
Clavicipitaceae A
C. gunnii clade
P. lilacinus clade
C. ophioglossoide clade
C. unilateralis clade
C. sphecocephala clade
C. unilateralis clade
Fig. 3. Schematic diagrams of phylogenetic relationships from MP, ML, and Bayesian analyses that differ in character or taxon sampling. In
addition to 162-taxon 5-gene and 7-gene data sets, 107-taxon and 152-taxon 5-gene data sets were generated with taxa complete for ive genes
(i.e., nrSSU, nrLSU, tef1, rpb1 and rpb2) and at least three genes, respectively. To address the impact of C. sphecocephala clade to nodal
support of C. unilateralis clade in Fig. 1, a 147-taxon -gene data set was constructed after members of C. sphecocephala clade were excluded.
Bootstrap proportions (BP ≥ 70 %) or posterior probabilities (PP ≥ 0.95 in percentage) are shown above corresponding nodes and in a thicker
line.
14
100
Shimizuomyces clade
Hypocrella clade
Shimizuomyces paradoxus
Shimizuomyces paradoxus
99
Aschersonia badia
97
96
Hypocrella schizostachyi
100
90
Aschersonia placenta
100
99
Hypocrella sp. GJS 89104
100100
Torrubiella luteorostrata
100
Torrubiella luteorostrata
100
Epichloë typhina
100
Claviceps paspali
100
100
96
Claviceps fusiformis
100
100
98
Claviceps purpurea
Claviceps purpurea
100
100
100
Verticillium epiphytum
99
76
Verticillium epiphytum
100
Myriogenospora atramentosa
100
100
100
86
Balansia pilulaeformis
100
100
Balansia epichloë
100
Balansia henningsiana
100
100 Pochonia bulbillosa
100
Pochonia gonioides
100
Pochonia rubescens
100
Tolypocladium parasiticum
84
Rotiferophthora angustispora
78
100
Cordyceps chlamydosporia (Pochonia) C. subg. Ophiocordyceps
100
100
Pochonia chlamydosporia
100
Nomuraea rileyi
98
Metarhizium
album
100
100 99
Cordyceps sp. NHJ 12118 (Metarhizium)
100
Metarhizium flavoviride
100 79
100
100
Cordyceps taii
100
C. subg. Neocordyceps
Cordyceps sp. OSC 110996 (Metarhizium)
100
Metarhizium anisopliae
Paecilomyces marquandii
100
Paecilomyces carneus
Paecilomyces carneus
100
100
Cordyceps liangshanensis
C. subg. Cordyceps
100100 Cordyceps liangshanensis
Cordyceps sp. EFCC 2131
100 Cordyceps sp. EFCC 2135
0.1 substitutions/site
100
T. luteorostrata clade
C. taii clade
1
Fig. 4. Enlargement of Bayesian consensus tree in Fig. 2, showing Clavicipitaceae clade A, to emphasize relationships within the clade. Respective subgenera of Cordyceps species in current classiication are
provided to the right of species. Known anamorphic genera of Cordyceps species are in parentheses. Tree description is the same as in Fig. 2.
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Clavicepsclade
SuNG ET AL.
Neocordyceps, and C. subg. Ophiocordyceps) based
on ascospore morphology and arrangement of the
perithecia in the stromata (Kobayasi 1941, 1982,
Eriksson 198). However, most of these characters are
not consistent with the new phylogenetic hypothesis
and are not diagnostic of monophyletic taxa (e.g.,
subgenera and genera) (Figs 1–2). For example,
Kobayasi (1941, 1982) emphasized ascospore
morphology and the lack of ascospore disarticulation
into part-spores to delimit C. subg. Ophiocordyceps from
the other subgenera. Species with non-disarticulating
ascospores, however, are included in all three major
clades (C. acicularis Ravenel of clade B, C. cardinalis
G.H. Sung & Spatafora of clade C, and Cordyceps
sp. EFCC 2131 and 213 of clade A described
below as Metacordyceps yongmunensis) (Figs 1–2),
indicating that non-disarticulating ascospores are not
phylogenetically informative at this level (Figs 1–2).
Therefore, a reassessment of diagnostic characters, in
the previous and current classiications of Cordyceps,
is necessary for the three major clades to provide a
basis for taxonomic revisions of Cordyceps and the
Clavicipitaceae.
Species in Clavicipitaceae clade A
Clavicipitaceae clade A comprises ive well-supported
subclades (Fig. 4). All known species of Cordyceps in
the clade are included in the C. taii clade. Species of
Cordyceps in the clade possess partially or completely
immersed perithecia on clavate to cylindrical fertile parts
of the stromata (Zang et al. 1982, Liang et al. 1991,
Zare et al. 2001). They produce ascospores that either
disarticulate or remain intact at maturity and include
species that possess ordinal and obliquely embedded
perithecia. In the current classiication, clade A includes
species of Cordyceps that were formerly classiied in
three
subgenera
of
Cordyceps.
Cordyceps
liangshanensis M. Zang, D. Liu & R. Hu forms ordinal
perithecia and possess disarticulating ascospores,
consistent with C. subg. Cordyceps (Kobayasi 1982,
Zang et al. 1982). Cordyceps chlamydosporia H.C.
Evans possesses nondisarticulating ascospores,
consistent with C. subg. Ophiocordyceps (Zare et
al. 2001). Cordyceps taii Z.Q. Liang & A.Y. Liu, a
known teleomorph species linked to the anamorph
genus Metarhizium Sorokin, produces disarticulating
ascospores and obliquely embedded perithecia
in the stromata, a trait used to recognize C. subg.
Neocordyceps (Liang et al. 1991). Importantly,
Cordyceps sp. EFCC 2131 and 213 (described below
as Metacordyceps yongmunensis) produce nondisarticulating ascospores and obliquely embedded
perithecia in the stromata, characters inconsistent with
any of the subgenera in the current classiication.
These results suggest that ascospore morphology
and arrangement of perithecia are not phylogenetically
informative in recognizing either the C. taii clade, or
higher clades of clavicipitaceous fungi. Rather, they are
more useful at species level classiication. For example,
our phylogenetic analyses revealed that C. taii is closely
related to C. brittlebankisoides Z. Y. Liu, Z.Q. Liang,
Whalley, Y.J. Yao & A.Y. Liu, the purported teleomorph
of M. lavoviride (Huang et al. 200). Although these
species are similar to each other in macromorphology
(e.g., greenish clavate stromata), they differ in the
arrangement of the perithecia. C. brittlebankisoides
possesses perithecia that are ordinally placed in the
stromata, whereas C. taii has obliquely embedded
perithecia. These results therefore suggest that
arrangement of the perithecia in the stromata is useful
in delimiting these closely related species in the C. taii
clade (Fig. 4).
Fig. 5. A–E. Representative species of Cordyceps and its allies in Clavicipitaceae clade A. F-K. Morphology of Cordyceps sp. (described here
as Metacordyceps yongmunensis sp. nov. below). A. C. liangshanensis on lepidopteran larva, EFCC 142. B. Cordyceps sp. on lepidopteran
pupa, EFCC 1228. C. Hypocrella schizostachyi on scale insect (Hemiptera). D. Shimizuomyces paradoxus on seed of plant (Smilax sieboldii:
Smilacaceae). E. Metarhizium sp. on adult of cicada. F. Section of perithecium, EFCC 2131. G. Asci and fascicle, EFCC 2131. H. Asci showing
prominent ascus cap, EFCC 2131. I. Asci showing ascus foot, EFCC 2131. J. Ascospores showing indistinct septation, EFCC 2131. K. Discharged
intact ascospores on SDAY agar, EFCC 2131. Scale bars: A–E = 10 mm, F = 200 μm, G = 100 μm, H–J = 10 μm, K = 100 μm.
1
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Species in Clavicipitaceae clade B
Species of Cordyceps in Clavicipitaceae clade B possess
disarticulating or non-disarticulating ascospores and
produce supericial to completely immersed perithecia
that are ordinally or obliquely inserted in the stromata.
As with the Cordyceps species of clade A, this
clade also includes members of the former C. subg.
Cordyceps (e.g., C. ophioglossoides (Ehrh.) Link and
C. variabilis Petch), C. subg. Ophiocordyceps (e.g., C.
acicularis and C. unilateralis (Tul. & C. Tul.) Sacc.), and
C. subg. Neocordyceps (e.g., C. nutans Pat. and C.
sphecocephala). The majority of Cordyceps species in
this clade produce wiry to pliant or ibrous stromata that
typically are completely or partially darkly pigmented
and parasitize subterranean or wood-inhabiting hosts,
which are buried in soil or embedded in decaying wood.
Exceptions to this morphology and ecology do exist,
however; for example, C. melolonthae (Tul. & C. Tul.)
Sacc. is pigmented bright yellow but stains darkly upon
handling, and members of the C. sphecocephala clade
parasitize adult insects.
Clade B consists of ive subclades. All subclades
include either species of Cordyceps or anamorphs with
potential links to Cordyceps (e.g., Nomuraea atypicola
(Yasuda) Samson linked to C. cylindrica Petch) (Fig. 6,
Evans & Samson 1987). The well-resolved tree in the
present study (Fig. ) provides the basis to characterize
three of the ive subclades of clade B. Due to insuficient
taxon sampling, it is not possible to characterize the
members of the Cordyceps species in the C. gunnii and
Pa. lilacinus subclades. In the light of this, we focus
on the remaining three subclades that include suficient
numbers of Cordyceps species.
The C. ophioglossoides subclade primarily consists
of Cordyceps species that parasitize species of the
genus Elaphomyces (e.g., C. ophioglossoides and C.
capitata (Holmsk.) Link) and the nymphs of cicadas (e.g.,
C. inegoënsis Kobayasi and C. paradoxa Kobayasi)
buried in soil (Kobayasi 1939, Mains 197, Kobayasi &
Shimizu 190, 193). Species in this subclade produce
partially or completely immersed perithecia, in clavate
to capitate fertile parts of stromata that are darkly
pigmented with olivaceous tints (Kobayasi & Shimizu
190, 193). Because they produce disarticulating
ascospores and ordinal perithecia, all known species
of this clade are classiied in C. subg. Cordyceps.
Cordyceps subsessilis Petch is unique to the
C. ophioglossoides subclade (Fig. ). It produces
perithecia on white or pallid reduced stromata, arising
from a rhizomorph-like structure from scarabaeid beetle
larvae (Hodge et al. 199). It is the only member of the
subclade that parasitizes beetles embedded in decaying
wood (Hodge et al. 1996). Therefore, C. subsessilis
differs greatly in ecology and morphology of its stromata
from most other taxa in the C. ophioglossoides clade,
but it possesses several characters shared by its close
relative, C. ophioglossoides (Kobayasi & Shimizu
190, Hodge et al. 199). Both species grow axenically
on simple media, produce verticilliate anamorphs (C.
subsessilis has a Tolypocladium anamorph, whereas
C. ophioglossoides has verticillium-like conidiophores),
possess nearly identical part-spore morphologies, and
produce stromata that are connected to their hosts via
rhizomorph-like structures. In contrast, C. capitata/C.
longisegmentis have not successfully been grown in
culture, they are attached directly to the host, and an
anamorph is unknown.
The C. ophioglossoides subclade (Fig. ) also
includes parasites of subterranean cicada nymphs
(e.g., C. inegoënsis and C. paradoxa), which are
grouped with their close relatives (e.g., C. jezoënsis
S. Imai and C. ophioglossoides) that parasitize
subterranean trufles of Elaphomyces. Despite low
support of inter-species relationships within the C.
ophioglossoides subclade due to short branch lengths,
C. paradoxa and C. inegoënsis are morphologically
more similar to C. jezoënsis and C. ophioglossoides
than to any other members of the clade. These taxa
produce clavate fertile parts of the stromata rather than
capitate stromata like other members of the clade (e.g.,
C. capitata and C. fracta Mains). Many of these species
(e.g., C. jezoënsis and C. paradoxa) are also known
to connect to their hosts via rhizomorph-like structures
(Kobayasi & Shimizu 190, 193), supporting a close
phylogenetic relationship.
The C. unilateralis subclade includes the most
morphologically diverse assemblages of Cordyceps
species (Fig. ). Most of the species in the clade
parasitize larval, pupal or nymph stages of arthropods
(Kobayasi 1941, Mains 198). Species of this clade
produce supericial to completely immersed perithecia
on the stromata with morphologies ranging from
capitate to clavate to iliform (Kobayasi 1941, Mains
1958). They typically possess tough, pliant, or ibrous
stromata that are entirely or partially darkly pigmented,
although some exceptions (e.g., C. melolonthae and C.
variabilis) do exist, which produce brightly pigmented
stromata (Mains 198). Many species in the clade (e.g.,
C. brunneipunctata Hywel-Jones, C. stylophora Berk.
& Broome, and C. unilateralis) are also differentiated
by aperithecial stromatal apices while the production of
perithecia occurs in subterminal regions of the stroma.
Similar to Cordyceps species in clade A, the C.
unilateralis subclade includes species that produce
disarticulating or non-disarticulating (intact) ascospores.
For example, some species in the C. unilateralis subclade
(e.g., C. sinensis (Berk.) Sacc. and C. unilateralis) were
formerly classiied in C. subg. Ophiocordyceps. But
these species are interspersed among other species
(e.g., C. agriotidis A. Kawam. and C. robertsii (Hook.)
Berk.) that are classiied in C. subg. Cordyceps. This
indicates that, while ascospore morphology is useful
in delimiting closely related Cordyceps species and
uniting others in species complexes, it is not diagnostic
of the C. unilateralis subclade itself (Fig. ).
Most members of C. subg. Neocordyceps, as
classically treated by Kobayasi (1941, 1982) and
others (e.g., Artjariyasripong et al. 2001, Stensrud et
al. 200), form a monophyletic group labelled as the C.
sphecocephala subclade within the C. unilateralis group
(Fig. 6). The majority of species in the C. sphecocephala
subclade produce long, thin, pliant, brightly coloured
(or dark marasmioid in a few species) stromata,
17
SuNG ET AL.
18
Fig. 6. Enlargement of Bayesian consensus tree in Fig. 2, showing Clavicipitaceae clade B, to emphasize relationships within the clade. Respective subgenera of Cordyceps species in current classiication
are provided to the right or below of species. Known anamorphic genera of Cordyceps species are in parentheses. Numbers above corresponding nodes are bootstrap proportions of ML analyses (before the
backslash) and posterior probabilities (after the backslash) from 147-taxon -gene data set in Fig. 3. Numbers below corresponding nodes are bootstrap proportions of ML analyses (before the backslash)
and posterior probabilities (after the backslash) from 162-taxon 5-gene data set in Fig. 2. Bootstrap proportions of ≥ 70 % or posterior probabilities of ≥ 0.95 (in pergentage) are shown in corresponding nodes.
Internodes in a thicker line are supported by the bootstrap proportions and posterior probabilities from either 147-taxon or 12-taxon -gene data sets. Numbers in a circle correspond to internode that is informative
for placing the C. sphecocephala clade.
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Fig. 7. A–S. Representative species of Cordyceps and its allies in Clavicipitaceae clade B. T–X. Ascus and ascospore of Cordyceps species in this
clade. A. C. ophioglossoides on trufle (Elaphomyces sp.: Eurotiomycetes). B. C. japonica on trufle (Elaphomyces muricatus: Eurotiomycetes), OSC
110991. C. C. subsessilis on scarabaeid beetle in decaying wood (Coleoptera), OSC 12881. D. C. gracilis on lepidopteran larva, EFCC 10121. E.
C. heteropoda on nymph of cicada (Hemiptera), EFCC 1012. F. C. nigrella on coleopteran larva, EFCC 3438. G. C. sobolifera on nymph of cicada
(Hemiptera), EFCC 778. H. C. longissima on nymph of cicada (Hemiptera), EFCC 87. I. C. unilateralis on ant (Hymenoptera). J. C. cochlidiicola on
lepidopteran larva, EFCC 377. K. C. agriotidis on coleopteran larva, EFCC 274. L. C. sinensis on larva of Hepialus sp. (Lepidoptera), EFCC 3248. M.
C. brunneipunctata on coleopteran larva. N. C. sphecocephala on wasp (Hymenoptera). O. C. nutans on stink bug (Hemiptera). P. C. tricentri on adult
of Tricentrus sp. (Hemiptera), EFCC 1001; bar = 10 mm. Q. Hymenostilbe odonatae on adult of dragonly (Odonata), EFCC 12459; bar = 10 mm. R.
Hirsutella sp. on wasp (Hymenoptera). S. Paecilomyces lilacinus. T. C. robertsii, ascus with disarticulating ascospores, MICH 2874. U. C. acicularis,
ascus and nondisarticulating ascospores, OSC 110987. V. C. paludosa, non-disarticulating ascospores, MICH 143. W. C. variabilis, disarticulated
part-spores in ascus, and X. Part-spores, OSC 128581. Scale bars: A–B = 10 mm, C = 1 mm, D–H = 10 mm, I = 5 mm, J–S = 10 mm, T–X = 10 μm.
19
SuNG ET AL.
which terminate in clavate to elongated fertile parts,
and possess ascospores that disarticulate into sixtyfour part-spores (Kobayasi 1941, 1982, Hywel-Jones
2002). Species in this clade produce perithecia, which
are partially or completely immersed in the stromata at
strongly oblique angles (Kobayasi 1941, 1982, Mains
1958, Hywel-Jones 1996). This clade is one of the best
characterized by its morphology (obliquely embedded
perithecia in a well-deined clava) and its ecology of
parasitizing adult stages of insects.
Species in Clavicipitaceae clade C
Clavicipitaceae clade C includes C. militaris, the
type species of the genus Cordyceps (Fig. 8). Most
Cordyceps species in this clade are currently classiied
in C. subg. Cordyceps (Kobayasi 1941, 1982). This
clade also contains the members of the former C. subg.
Ophiocordyceps and C. subg. Bolacordyceps, resulting
in C. subg. Cordyceps being paraphyletic within
clade C (Eriksson 1982, Hywel-Jones 1994, Sung &
Spatafora 2004). Species of Cordyceps in this clade
produce three ascospore types, including disarticulating
ascospores (e.g., C. militaris), intact ascospores (e.g.,
C. cardinalis and C. pseudomilitaris Hywel-Jones &
Sivichai), and bola-ascospores (e.g., C. bifusispora
O.E. Erikss.). Of particular note, this clade includes
Phytocordyceps ninchukispora C.H. Su & H.-H. Wang
in the unispeciic genus Phytocordyceps C.H. Su & H.H. Wang. The genus Phytocordyceps was originally
described based on bola-ascospores and its host
afiliation as a pathogen of Beilschmiedia erythrophloia
Hayata (Lauraceae) plant seeds (Su & Wang 198).
Morphologically, this species is most similar to C.
bifusispora in that it produces bola-ascospores typical
of C. subg. Bolacordyceps. However, the phylogenetic
analyses in this study reveal that species producing bolaascospores (e.g., C. bifusispora and P. ninchukispora)
do not form a monophyletic group (Fig. 8). Rather,
they are interspersed among other Cordyceps species
possessing disarticulating ascospores, most notably C.
militaris.
Species of Cordyceps in clade C produce supericial
to partially immersed perithecia on leshy stromata that
are pallid to brightly pigmented. This is in contrast to
Cordyceps species in clade B, which produce darkly
pigmented, wiry to pliant or ibrous stromata. This
suggests that pigmentation and texture of stromata
may be phylogenetically informative at a higher level of
classiication. It should be noted, however, that some
Cordyceps species in clade C are morphologically
similar to distantly related Cordyceps species (e.g., C.
melolonthae and C. variabilis) in stromatal pigmentation.
Although these characters are useful in recognizing
Cordyceps species of clade C, the utility of these
characters for any future infrageneric classiication
is probably limited (Fig. 8). For example, C. militaris
is macroscopically similar to C. cardinalis and C.
pseudomilitaris. All three species produce orangish
to red-coloured and leshy stromata; however, these
species differ in ascospore and anamorph morphology
(Sung & Spatafora 2004). Furthermore, C. militaris is
20
known as exhibiting considerable variability in stroma
morphology (Sung & Spatafora 2004). Potentially
conspeciic species, such as C. roseostromata Kobayasi
& Shimizu and C. kyusyuënsis A. Kawam., differ in stroma
morphology, but are closely related to C. militaris and
possess identical ascospore and ascus morphologies
(Fig. 8, Hywel-Jones 1994, Sung & Spatafora 2004).
The variation in ascospore morphology of
Clavicipitaceae clade C combined with old descriptions
and unavailable type material complicates species
identiication for many taxa, as is the case for much
of Cordyceps. For example, this study reveals a
close relationship between the anamorphic species,
Mariannaea pruinosa Z.Q. Liang from China, C. cf.
pruinosa from Korea and Thailand, and Phytocordyceps
ninchukispora from Taiwan (Fig. 8). The teleomorph of
M. pruinosa is C. pruinosa Petch, which was originally
described as producing disarticulating ascospores and
reddish orange stromata, parasitizing lepidopteran
cocoons (Petch 1924, Kobayasi 1941, Liang 1991).
Although the isolate of M. pruinosa was obtained
from ascospores (Liang 1991), the morphology of the
ascospores was not well characterized. The species
was identiied primarily based on its host afiliation and
macroscopic characters. In our study, C. cf. pruinosa
EFCC 197 and N.H.J. 1027 were collected from
the same host family (Lepidoptera, Limacodidae) in
Korea and Thailand. They are also closely related and
produce reddish orange stromata (Fig. 8) and bolaascospores and not the typical C. subg. Cordyceps
part-spores. It should be noted, however, that Petch did
not provide any drawings or images of ascospores and
it is possible that the terminal cells of bola-ascospores
could easily be interpreted as part-spores. Thus, at this
time we use the name C. pruinosa for the Chinese,
Korean and Thai collections and, if further attempts fail
to locate type material for C. pruinosa, one of these
may have to be designated a neotype. The C. pruinosa
collections are closely related to and morphologically
indistinguishable from P. ninchukispora with the
exception of host afiliation, suggesting the possibility
of host misidentiication in the original description of
P. ninchukispora. Because the tree topology of the
C. pruinosa/P. ninchukispora complex is indicative of
greater phylogenetic species diversity, i.e., the Korean,
Thai, and Taiwanese material may represent unique
phylogenetic species (Fig. 8), we retain the use of both
names until more detailed sampling and analyses have
been conducted.
Clavicipitaceae clade C not only includes members
of Cordyceps but also species of the genus Torrubiella,
which generally parasitize spiders and scale insects
(Kobayasi & Shimizu 1982). The genus Torrubiella
is morphologically characterized by the production
of supericial perithecia on a mycelial subiculum that
partially or completely surrounds the host (Kobayasi
& Shimizu 1982, Humber & Rombach 1987). Species
of Torrubiella also produce disarticulating (e.g., T.
ratticaudata Humber & Rombach) and intact (e.g., T.
wallacei) ascospores. Among species of Cordyceps,
C. tuberculata (Lebert) Maire, a pathogen of adult
100
100
100
Simplicillium lamellicola
Simplicillium obclavatum
100
Simplicillium lanosoniveum
100
Simplicillium lanosoniveum
100
Torrubiella wallacei (Simplicillium)
Engyodontium aranearum
91
Lecanicillium antillanum
100
Lecanicillium aranearum
100
Torrubiella ratticaudata
100 Cordyceps cardinalis (Mariannaea or Clonostachys)
100
C. subg. Ophiocordyceps
Cordyceps cardinalis (Mariannaea or Clonostachys)
100
100
Lecanicillium dimorphum
Lecanicillium psalliotae
100
Lecanicillium fusisporum
100
100
Lecanicillium psalliotae
Isaria farinosa
99
99
Isaria farinosa
Cordyceps tuberculata (Akanthomyces)
100
100 82
Lecanicillium attenuatum
Torrubiella
confragosa (Lecanicillium)
98
100
Beauveria caledonica
100
100
Cordyceps scarabaeicola (Beauveria)
100
Cordyceps staphylinidicola (Beauveria)
98
Cordyceps cf. takaomontana
Isaria cf. farinosa
100
C. subg. Cordyceps
100
Cordyceps cf. ochraceostromata
88
Isaria tenuipes
100
100
100
Cordyceps sp. EFCC 2535
100
100
Cordyceps takaomontana (Isaria)
100
Cordyceps bifusispora
76 100
C. subg. Bolacordyceps
100 100 Cordyceps bifusispora
88
100
Microhilum oncoperae
95
100
Cordyceps kyusyuensis
C. subg. Cordyceps
100
97
Cordyceps militaris (Lecanicillium)
100
Verticillium
sp.
CBS
102184
100 98
100 Cordyceps cf. pruinosa EFCC 5197
100 100 Cordyceps cf. pruinosa EFCC 5693
100
Mariannaea pruinosa
100
99
Cordyceps cf. pruinosa NHJ 10627
C. subg. Bolacordyceps
96
100 Cordyceps cf. pruinosa NHJ 10684
100 94 100
0.1 substitutions/site
Phytocordyceps ninchukispora
100 100 Phytocordyceps ninchukispora
100
100
Simplicillium clade
21
Fig. 8. Enlargement of Bayesian consensus tree in Fig. 2, showing Clavicipitaceae clade C, to emphasize relationships within the clade. Respective subgenera of Cordyceps species in previous classiication are
provided to the right of the species. Known anamorphic genera of Cordyceps species are in parentheses. Tree description is the same as in Fig. 2.
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Cordyceps clade
SuNG ET AL.
Lepidoptera, has been considered an intermediate
species between Torrubiella and Cordyceps (Humber
& Rombach 1987, Kobayasi 1941, Mains 198).
Phylogenetic analyses in this study indicate that the
members of Torrubiella do not form a monophyletic
group within clade C and are interspersed among
species of Cordyceps. This suggests that the stipitate
stromata of Cordyceps have been gained or lost
several times during the evolution of these fungi.
Currently, more than 0 species of Torrubiella have
been described and the members of genus Torrubiella
are clearly undersampled in this study (Kobayasi &
Shimizu 1982).
In summary, the characters of ascospore morphology
and the arrangement of perithecia used in the current
classiication of the genus Cordyceps are not congruent
with the three higher clades inferred in these analyses.
These characters are likely to prove useful, however,
in lower level classiications, such as the delimitation
of closely related species and species complexes. The
characters most congruent with the three higher clades
of clavicipitaceous fungi are texture, pigmentation
and morphology of the stromata, but with exceptions.
Although we have divided Cordyceps species into three
major clades, it is dificult to characterize Cordyceps
species within the Clavicipitaceae clade A due to the
relatively few teleomorph species that are part of this
clade (see key on p. 54). They tend to produce green
to white stromata, often with lilac tints, but additional
sampling is needed to more deinitively characterize the
teleomorphs of these species. However, the majority of
species within clades B and C are morphologically and/
or ecologically distinct (Figs 1–2).
The majority of Cordyceps species in clade B are
characterized by darkly pigmented, wiry, pliant or
ibrous stromata. The dominant form of parasitism
exhibited by these species is on subterranean or woodinhabiting hosts, buried in soil or embedded in decaying
wood, such as larval and pupal stages of arthropods.
In contrast, Cordyceps species of clade C have brightly
pigmented and leshy stromata and parasitize their hosts
in relatively more accessible environments, such as
leaf litter, moss, or the uppermost soil layer. Exceptions
to these morphological and ecological traits are found
in some Cordyceps species in clade B. Cordyceps
melolonthae, for example, produces brightly-coloured
stromata, although it bruises dark upon handling and
its hosts are the larvae of cockchafers or June beetles
buried in soil (Mains 198). Cordyceps unilateralis
parasitizes adult ants, but is darkly pigmented with a
wiry stroma and subterminal production of perithecia,
and members of the C. sphecocephala clade are at least
partially brightly pigmented and are restricted to adult
stages of insects. These indings suggest that the traits
described above are not universally informative, but
collectively useful in characterizing Cordyceps species
within clade B. That is, there have been gains, losses,
and diversiications of most if not all traits during the
evolution of these fungi, but general trends in character
state evolution are evident.
22
The taxonomic utility of anamorphic forms in
classiication of Cordyceps
The genus Cordyceps is characterized by a diverse
assemblage of more than 2 anamorph genera (e.g.,
Beauveria vuill., Hirsutella Pat., Hymenostilbe Petch,
Isaria Fr., Lecanicillium W. Gams & Zare, Metarhizium,
and Tolypocladium W. Gams) (Kobayasi 1982, Samson
et al. 1988, Gams & Zare 2003, Hodge 2003). The
anamorph genera of Cordyceps are hyphomycetes
with conidiogenous cells that are hyaline to brightly
coloured and produce conidia in dry chains or
slimy drops (Samson et al. 1988). Some anamorph
genera (e.g., Hymenostilbe) are known as a useful
diagnostic character in recognizing monophyletic
groups of Cordyceps species (Artjariyasripong et al.
2001, Kobayasi 1941, 1982), while other anamorph
morphologies and genera are placed in more than one
clade of the Clavicipitaceae. Therefore, the distribution
of anamorphic forms is discussed to evaluate their
phylogenetic utility in characterizing the three clades of
Cordyceps and Clavicipitaceae and to better understand
teleomorph–anamorph connections.
Anamorphs of Clavicipitaceae clade A
Clavicipitaceae clade A includes isolates of the
anamorph genera Aschersonia Mont., Metarhizium,
Nomuraea Maublanc, Pochonia Bat. & O.M. Fonseca,
Paecilomyces s. l., Rotiferophthora G.L. Barron,
Tolypocladium W. Gams, and verticillium-like (Fig.
4). Nomuraea, Paecilomyces, and Tolypocladium
are found in other clades of Clavicipitaceae (Figs
1–2). Signiicantly, Verticillium s. s. is known from the
Plectosphaerellaceae, which is closely related with
the Glomerellaceae in the Sordariomycetidae (Zare
et al. 2007). Paecilomyces s. s. is in the Eurotiales
(Eurotiomycetidae), but species of Paecilomyces
s. l. are also present elsewhere in the Hypocreales
(Luangsa-ard et al. 2004). In contrast, the anamorph
genera Aschersonia, Metarhizium, Pochonia and
Rotiferophthora are restricted to clade A (Figs 1–2).
Anamorph taxa of the C. taii subclade include
Nomuraea rileyi (Farl.) Samson, Paecilomyces
carneus (Duché & R. Heim) A.H.S. Brown & G. Smith
and Pa. marquandii (Massee) S. Hughes, Pochonia,
Tolypocladium parasiticum, and Metarhizium (Fig. 4).
The genera Nomuraea, Pochonia and Tolypocladium
are not monophyletic, although Pochonia is restricted
to clade A. Nomuraea rileyi and Metarhizium are
entomogenous; Pa. carneus is a common soil fungus
considered a weak insect pathogen, while Pa.
marquandii, Pochonia and T. parasiticum are also
common soil fungi and can be parasitic on nematodes.
Metarhizium is the only monophyletic anamorph genus
of clade A (Fig. 4). The conidiogenous cells in the
genus Metarhizium are cylindrical to clavate without
a neck and produced in candelabrum-like or palisadelike fashion (Rombach et al. 198, Driver et al. 2000,
Evans 2003). The genus is most similar to Nomuraea
and differs in the compact conidiophores that form a
hymenial layer (Evans 2003). Nomuraea rileyi groups
with species of Metarhizium, while N. atypicola
(Yasuda) Samson belongs to the Pa. lilacinus clade
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
in clade B. Interestingly, N. rileyi produces greenishcoloured conidia, as do species of Metarhizium in the
C. taii subclade, while N. atypicola possesses lavendercoloured conidia similar to those of Pa. lilacinus
(Coyle et al. 1990, Hywel-Jones & Sivichai 199,
Evans 2003). Currently, three teleomorphic species of
Metarhizium (C. brittlebankisoides, C. campsosterni,
and C. taii) have been reported (Liang et al. 1991,
Liu et al. 2001, Zhang et al. 2004). The species M.
taii was described with its teleomorph species, C. taii
(Liang et al. 1991) and recently synonymized with M.
anisopliae var. majus (Huang et al. 200). Cordyceps
brittlebankisoides was once also considered to have the
anamorph M. anisopliae var. 0majus (Liu et al. 2001),
but it is likened to M. lavoviride (Huang et al. 200). In
general, Metarhizium species show extensive variation
in size and colour of conidia (Driver et al. 2000, Evans
2003) and more intensive sampling of anamorphs and
teleomorphs is needed for this group.
The genus Tolypocladium is characterized by
producing single or whorled (verticillate) conidiogenous
cells (phialides), which are lask-shaped with enlarged
bases that taper into a needle-like neck usually bent
from the axis of the phialides (Gams 1971, Bissett
1983). The type of the genus Tolypocladium, T. inlatum
W. Gams, is linked to the teleomorph C. subsessilis
(Hodge et al. 199, Gams & Zare 2003). Tolypocladium
inlatum is placed in clade B and is distantly related
to T. parasiticum in the C. taii clade. Tolypocladium
parasiticum was described from the rotifer host
Adineta and described with underwater conidiation
(Barron 1980). Morphologically, T. parasiticum differs
from other species of Tolypocladium, as it is the only
member of the genus that produces chlamydospores
in vivo (Barron 1980) and in culture (Bissett 1983, Zare
et al. 2001, Gams & Zare 2003). In a recent treatment
of Verticillium sect. Prostrata W. Gams, the genus
Pochonia was also reclassiied based on production of
dictyochlamydospores or at least swollen hyphal cells
(Gams & Zare 2001, Zare et al. 2001), supporting the
close phylogenetic relationship of T. parasiticum and
Pochonia species demonstrated in this study (Fig. 4).
Hence, T. parasiticum is transferred to Pochonia below,
rendering the remaining species in Tolypocladium
monophyletic. Paecilomyces marquandii also produces
infrequent chlamydospores in culture, as does the
anamorph of Metacordyceps yongmunensis sp. nov.
(discussed below). As suggested by Barron & Onions
(19), the presence of chlamydospores can be a
taxonomically informative character.
The genus Aschersonia is a monophyletic lineage
labelled as Hypocrella subclade (Fig. 4). The genus
Aschersonia is characterized by its pycnidial or acervular
conidiomata with hymenial phialides and its ecology
of parasitizing only the nymphs of scale insects and
whitelies (Petch 1921, Hywel-Jones & Evans 1993).
The teleomorphs of Aschersonia have long been linked
to the species of Hypocrella and more than 2 species
have been reported (Petch 1921, Mains 1959). While
this study does not focus on sampling of Hypocrella
and Aschersonia, these indings corroborate that the
unique morphology of Aschersonia is phylogenetically
informative and diagnostic of a monophyletic group of
clavicipitaceous fungi (Fig. 4).
Anamorphs of Clavicipitaceae clade B
Clavicipitaceae clade B includes several anamorph
genera including Haptocillium W. Gams & Zare,
Hirsutella, Hymenostilbe and Tolypocladium (Fig.
). Several of the anamorphic forms in the clade
are phylogenetically informative. Hirsutella and
Hymenostilbe occur dominantly in the C. unilateralis
subclade.
Hirsutella is characterized by its typical basallysubulate phialides, narrowing into one (usually) or
more (occasionally) very slender needle-like necks,
on synnemata or mononematous mycelium (Hodge
1998, Gams & Zare 2003). Hirsutella species normally
produce a few (<) conidia in mucus and the phialides
are not usually bent in their needle-like necks such as in
the genus Tolypocladium, but also single conidia as in
Hi. thompsonii F.E. Fisher. Not all Cordyceps species in
the C. unilateralis subclade are connected to Hirsutella
anamorphs. Some are connected to Paecilomyces s. l.,
Paraisaria Samson & B.L. Brady, and Syngliocladium
Petch, whereas anamorphic forms are not known for
many of the Cordyceps species, especially in the C.
ravenelii subclade (e.g., C. heteropoda Kobayasi).
However, most Cordyceps species in the rest of the
C. unilateralis subclade have been linked to Hirsutella
anamorphs (Fig. ). These results suggest that
Hirsutella anamorphs are phylogenetically informative
for at least part of the C. unilateralis subclade or possibly
symplesiomorphic for the C. unilateralis subclade as a
whole.
The taxonomic utility of Hirsutella anamorphs is
exempliied by the teleomorph–anamorph connection of
the genus Cordycepioideus Stiler, a termite pathogen,
which does not have typical ascospore and ascus
morphologies of clavicipitaceous fungi (Blackwell &
Gilbertson 1984, Suh et al. 1998). It possesses thickwalled multiseptate ellipsoid ascospores and its asci
lack the thickened ascus tip characteristic of most
clavicipitaceous fungi (Blackwell & Gilbertson 1984,
Ochiel et al. 1997). The anamorph of Cordycepioideus
bisporus Stiler is a synnematous Hirsutella that is either
conspeciic with or closely related to Hi. thompsonii
(Ochiel et al. 1997, Suh et al. 1998, Sung et al. 2001).
Although Cordycepioideus bisporus differs greatly
from other members of the C. unilateralis subclade in
its teleomorphic characters, molecular data strongly
support it as a member of the C. unilateralis subclade,
a inding consistent with its Hirsutella anamorph. It
should be noted that species of Cordyceps outside of
clade B have been described with atypical Hirsutella
anamorphs (e.g., C. pseudomilitaris), but upon further
investigation were more accurately characterized in
other anamorph genera (e.g., Simplicillium W. Gams
& Zare).
The C. unilateralis clade includes the members
of the C. sphecocephala subclade, which possess a
Hymenostilbe anamorph. The genus Hymenostilbe
usually produces cylindrical to clavate conidiogenous
cells, which are produced in a more or less dense
23
SuNG ET AL.
palisade in synnemata (Samson et al. 1988). It is
differentiated from closely related genera (e.g.,
Akanthomyces Lebert and Hirsutella) by its polyblastic
conidiogenous cells, which holoblastically produce
single conidia on short denticles or scars (Samson
et al. 1988, Hywel-Jones 1996). The results from the
present study indicate that Hymenostilbe anamorphs
may be derived from within Hirsutella (Fig. 6). The
close phylogenetic relationship between Hirsutella
and Hymenostilbe anamorphs is exempliied by the
morphologically intermediate synnematous Hirsutella/
Hymenostilbe species. For example, Hy. lecaniicola
(Jaap) Mains, the anamorph of C. clavulata (Schwein.)
Ellis & Everh. (Hodge 1998), was previously classiied
in Hirsutella although it possesses extensively
polyphialidic conidiogenous cells in a discontinuous
layer (Mains 190, 198, Samson & Evans 197,
Hodge 1998). In addition, some Hirsutella species (e.g.,
Hi. rubripunctata Samson, H.C. Evans & Hoekstra)
produce only a single conidium without a mucous sheath
on denticles of extensively polyphialidic conidiogenous
cells. Therefore, the modes of asexual reproduction
in Hirsutella and Hymenostilbe may overlap to some
extent and additional work is necessary to address the
relationships between the two genera (Hodge 1998,
Gams & Zare 2003).
In addition to the C. unilateralis subclade, the
remaining three subclades contain Haptocillium,
Tolypocladium and verticillium-like anamorphs. The
genus Haptocillium was reclassiied from the former
Verticillium sect. Prostrata primarily based on its
adhesive conidia and its ability to parasitize free-living
nematodes (Zare & Gams 2001b). This study shows
that the genus is a monophyletic group in the C. gunnii
subclade (Fig. ). However, the teleomorph–anamorph
connection has not been established for any of the
species in the clade or its close relative, C. gunnii,
and thus its taxonomic utility remains unclear. The C.
ophioglossoides and Pa. lilacinus subclades include
anamorphic forms of Paecilomyces s. l., Nomu-raea,
Tolypocladium, and verticillium-like, all of which are
polyphyletic as previously discussed (Figs 1–2; Oborník
et al. 2001, Luangsa-ard et al. 2004, 200). Several
teleomorph–anamorph connections have been reported
for Cordyceps species in the C. ophioglossoides and
Pa. lilacinus subclades although their taxonomic utility
is limited. Cordyceps subsessilis is known to be the
teleomorph of Tolypocladium inlatum (Hodge et al.
199) and C. ophioglossoides produces a verticilliumlike anamorph (Gams 1971). In the Pa. lilacinus
subclade, N. atypicola is linked to C. cylindrica (Evans
& Samson 1987, Hywel-Jones & Sivichai 199).
Anamorphs of Clavicipitaceae clade C
The anamorph genera sampled that are members
of clade C include Beauveria, Isaria, Lecanicillium,
Microhilum H.Y. Yip & A.C. Rath, and Simplicillium.
Species of Lecanicillium and Simplicillium were
previously placed in Verticillium sect. Prostrata and
recently reclassiied based on the phylogenetic studies
of Sung et al. (2001) and Zare & Gams (2001a, b).
The genus Lecanicillium is characterized by producing
24
slender aculeate phialides that are produced singly or
in whorls and usually arise from prostrate aerial hyphae
(Zare & Gams 2001a). Conidia are mostly produced at
the tip of phialides and attached in heads or fascicles
(Zare & Gams 2001a). The morphological delimitation
of Simplicillium from Lecanicillium is dificult although
the species of Simplicillium tend to produce phialides
that more or less arise singly from prostrate aerial
hyphae (Zare & Gams 2001a). This study shows again
that the species of Lecanicillium form a paraphyletic
group, as species of other well-delimited anamorphic
genera (e.g., Beauveria, Engyodontium G.S. de
Hoog, and Isaria) are interspersed among species of
Lecanicillium (Fig. 8).
Some Lecanicillium species are known to be
anamorphic forms of Cordyceps and Torrubiella (Petch
1932, Evans & Samson 1982, Zare & Gams 2001a).
For example, C. militaris produces a Lecanicillium
anamorph in culture (Zare & Gams 2001a) and the
anamorph of Torrubiella alba Petch is L. aranearum
(Petch) Zare & W. Gams (Petch 1932). The type
species of Lecanicillium is L. lecanii (Zimm.) Zare &
W. Gams, which is connected to the teleomorph T.
confragosa Mains, a pathogen of scale insects (Evans
& Samson 1982), which we transfer here to Cordyceps.
In addition to Lecanicillium anamorphs, other genera
(e.g., Akanthomyces, Gibellula Cavara, Hirsutella,
Paecilomyces (Isaria), and Simplicillium) have also
been linked to Torrubiella (Kobayasi & Shimizu 1982,
Samson et al. 1988, 1989, Zare & Gams 2001a).
Clavicipitaceae clade C also includes the species of
Isaria, the generic name of which has been conserved
with I. farinosa (Holmsk.) Fr. as the type, for some of
the clavicipitaceous Paecilomyces species (Gams
et al. 200, Luangsa-ard et al. 2005). The genus
Paecilomyces was a diverse genus, with molecular
studies indicating its polyphyletic status (Oborník et
al. 2001, Luangsa-ard et al. 2004, 2005). The type
species, Pa. variotii Bainier, belongs to the order
Eurotiales (Ascomycota) and is distantly related to
the clavicipitaceous Paecilomyces species that were
previously classiied in Paecilomyces sect. Isarioidea
(Samson 1974, Luangsa-ard et al. 2004). The previous
taxonomy of Paecilomyces was primarily based on the
monographic study by Samson (1974), which included
approximately 22 species in Paecilomyces sect.
Isarioidea. In a recent molecular study, Luangsa-ard et
al. (200) demonstrated that species in Paecilomyces
sect. Isarioidea are subdivided into four monophyletic
groups, three of which are statistically supported. As a
result, eleven species of Paecilomyces sect. Isarioidea
were reclassiied in Isaria (e.g., I. fumosorosea Wize,
I. javanica (Frieder. & Bally) Samson & Hywel-Jones
and I. tenuipes Peck) (Luangsa-ard et al. 2005). The
present study indicates that the four isolates of Isaria
do not form a monophyletic group in clade C, as they
are interspersed among other anamorphic forms in the
clade. Thus, the taxonomic utility of Isaria anamorph
is limited to clade C, as seen with Lecanicillium
and Simplicillium anamorphs. Furthermore, few
connections have been made between teleomorphs
of the Clavicipitaceae and species of Isaria. Kobayasi
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
(1941) reported that the anamorph of C. takaomontana
Yakush. & Kumaz. is Isaria japonica Yasuda, which
Samson (1974) synonymized with Pa. tenuipes (=
I. tenuipes). Isaria farinosa is the anamorph of C.
memorabilis (Pacioni & Frizzi 1978), but was once
mistakenly linked to C. militaris (Petch 1936). Isaria
farinosa was also connected to two Torrubiella species,
T. gonylepticida (A. Möller) Petch and T. pulvinata Mains.
The anamorph of the latter was reported as Spicaria
pulvinata Mains, and Petch described the conidial
state of T. gonylepticida as Spicaria longipes Petch,
two Spicaria species that Samson (1974) synonymized
with Paecilomyces farinosus (= I. farinosa). Although T.
gonylepticida was originally described in combination
with Cordyceps, Petch (1937) transferred the species
to its current combination and redescribed the species.
Isaria farinosa has been reported to occur on six
insect orders (Lepidoptera, Coleoptera, Hemiptera,
Homoptera, Diptera, and Hymenoptera) and also on
spiders (Araneae). The simplicity and plasticity in the
morphology of most Isaria species make it dificult to
set boundaries among and between sister-taxa and the
search for better markers in species delimitation must
be a goal for further studies.
The closely related species, C. scarabaeicola
Kobayasi and C. staphylinidicola Kobayasi & Shimizu
produce Beauveria anamorphs (Fig. 8; Sung 199),
and C. bassiana Z.Z. Li, C.R. Li, B. Huang & M.Z. Fan
and C. brongniartii Shimazu are known as teleomorphs
of B. bassiana (Bals.) vuill. and B. brongniartii
(Sacc.) Petch, respectively (Shimazu et al. 1988, Li
et al. 2001). The genus Beauveria is morphologically
well-characterized by producing basally-inlated
conidiogenous cells that sympodially produce conidia
on divergent denticles (MacLeod 194, de Hoog 1972).
Beauveria has a cosmopolitan distribution with quite a
broad host range (Mugnai et al. 1989, Evans 2003,
Rehner & Buckley 200). A recent molecular study
(Rehner & Buckley 200) that included 87 isolates of
ive Beauveria species (B. amorpha (Höhn.) Samson &
H.C. Evans, B. bassiana, B. brongniartii, B. caledonica
Bissett & Widden, and B. vermiconia de Hoog & v. Rao)
demonstrated that the genus is monophyletic and one
of the more phylogenetically-informative anamorphs of
clade C.
In fungal systematics, the naming of anamorphic
forms is allowed for Phyla Ascomycota and Basidiomycota by Article 9 of the International Code of Botanical
Nomenclature (McNeill et al. 200) and multiple names
exist for the same organisms of teleomorphic and
anamorphic taxa. Recently, molecular phylogenetics
has played an important role in integrating teleomorphic
and anamorphic forms in a uniied classiication system
in the clavicipitaceous fungi (Reynolds & Taylor 1993,
Sung et al. 2001, Luangsa-ard et al. 200). In such
efforts, Verticillium sect. Prostrata and Paecilomyces
sect. Isarioidea have recently been reclassiied
into several anamorphic genera (e.g., Haptocillium,
Isaria, Lecanicillium, Pochonia, Rotiferophthora,
and Simplicillium) to be consistent with the current
hypotheses of relationships (Zare & Gams 2001a, Zare
et al. 2001, Luangsa-ard et al. 2005). The phylogeny
presented here further improves our understanding of
the teleomorph–anamorph connections in Cordyceps
and implies that several anamorphic genera (e.g.,
Beauveria, Hirsutella, Hymenostilbe, and Metarhizium)
are more restricted in their phylogenetic distribution and
therefore phylogenetically informative in characterizing
Cordyceps species (Figs 4, , 8).
TAXONOMIC REVISION
The present phylogenetic analyses reveal three strongly
supported monophyletic groups (i.e., Clavicipitaceae
clades A, B, and C) of clavicipitaceous fungi (Figs 1–2),
a result consistent with studies involving fewer taxa
(Spatafora et al. 2007, Sung et al. 2007). In reviewing
the diagnostic characters used in previous classiication
schemes, most characters are not consistent with
the phylogeny presented here. Therefore, the phylogenetic relationships of Cordyceps and the related
clavicipitaceous fungi provide the evidence for rejecting
most of the previous classiications of Cordyceps and
Clavicipitaceae (Kobayasi 1941, 1982, Diehl 190,
Mains 198). Here, we propose a new phylogenetic
classiication for Cordyceps and Clavicipitaceae as
follows (Fig. 10).
Clavicipitaceae Clade A
Clavicipitaceae clade A is a well-supported monophyletic group that represents the Clavicipitaceae s. s.
(MP-BP = 98 %, ML-BP = 99 %, PP = 1.00 in Figs
1–2, 10). The name Clavicipitaceae was irst used in
1901 by Earle for the former Hypocreaceae subfam.
Clavicipiteae Lindau (Earle 1901). However, Earle
(1901) used it without description and without reference
to its basionym. The name was then invalidly used
by subsequent workers, such as Nannfeldt (1932)
and Diehl (190), until it was validated by Rogerson
(1970) as conirmed by Eriksson & Hawksworth (1985).
Although Clavicipitaceae is well characterized by
cylindrical asci, thickened ascus apices, and iliform
ascospores that tend to disarticulate at maturity as in
the original description, we restrict the application of
Clavicipitaceae s. s. to the members of Clavicipitaceae
clade A because of the non-monophyly of Clavicipitaceae
s. l. (Fig. 10). These indings suggest that the character
states of cylindrical asci and iliform ascospores that
disarticulate at maturity are plesiomorphic for the
Clavicipitaceae s. l./Hypocreaceae clade. Importantly,
the Hypocreaceae also possesses cylindrical asci and
while its ascospores are subglobose to fusiform and
easily distinguished from those of Clavicipitaceae s. l.,
they show a similarly high frequency of disarticulation
(Rogerson 1970, Rossman et al. 1999).
The family Clavicipitaceae s. s. includes the
grass-associated genera Balansia Speg., Claviceps,
Epichloë (Fr.) Tul. & C. Tul., and Myriogenospora G.F.
Atk., which were classiied in Clavicipitaceae subfam.
Clavicipitoideae sensu Diehl 190 (Fig. 10). Recent
molecular studies show that Aciculosporium I. Miyake,
Atkinsonella Diehl, Heteroëpichloë E. Tanaka, C.
2
SuNG ET AL.
Fig. 9. A–M. Representative species of Cordyceps and its allies in Clavicipitaceae clade C. N–S. Perithecia, asci, and ascospores. A. C. militaris
on lepidopteran pupa, EFCC 192. B. C. kyusyuënsis on lepidopteran larva, EFCC 1098. C. C. chichibuënsis on coleopteran pupa, EFCC
422. D. C. cf. ochraceostromata on lepidopteran larva, EFCC 1184. E. C. scarabaeicola on scarabaeid beetle (Coleoptera), EFCC 014. F.
C. staphylinidicola on coleopteran larva, EFCC 783. G. C. bifusispora on lepidopteran pupa, EFCC 22. H. C. cf. pruinosa on lepidopteran
pupa (Limacodidae), EFCC 117. I. C. cardinalis on lepidopteran larva, EFCC 12212. J. C. tuberculata on adult of moth (Lepidoptera), EFCC
207. K. Torrubiella sp. on spider (Arachnida), EFCC 10882. L. Beauveria sp. on adult of beetle (Coleoptera), EFCC 137. M. Isaria tenuipes
on lepidopteran pupa, EFCC 1497. N. C. cardinalis, section of perithecia in stroma, OSC 9309. O. C. militaris, ascus with disarticulating
ascospores, OSC 9323. P. C. cardinalis, ascus with nondisarticulating ascospores, OSC 9309. Q. C. cf. pruinosa, fusiform terminal parts
of ascospores in ascus, EFCC 7481. R. C. militaris, multiseptated ascospores in ascus, OSC 9323. S. C. cf. pruinosa, thread-like structures
connecting fusiform terminal parts of ascospores, EFCC 7481. Scale bars: A–M = 10 mm, N = 100 μm, O–S = 5 μm.
2
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Tanaka, Gafur & Tsuda, Neoclaviceps J.F. White, Bills,
S.C. Alderman & Spatafora, and Parepichloë J.F. White
& P.V. Reddy are also members of this clade, thus
supporting their classiication in the Clavicipitaceae s.
s. (White & Reddy 1998, Sullivan et al. 2001, Tanaka
et al. 2002). Clavicipitaceae s. s. also includes the
plant-associated Shimizuomyces paradoxus Kobayasi,
which occurs on seeds of Smilax (Smilacaceae). In
addition to plant-associated fungi, Clavicipitaceae
s. s. contains four arthropod-associated lineages.
Three of the four arthropod-associated lineages are
characterized as pathogens of scale insects, including
Hypocrella (pathogens of scale insects and white lies;
Hywel-Jones & Evans 1993, Hywel-Jones & Samuels
1998), Regiocrella P. Chaverri & K.T. Hodge (pathogen
of scale insects; Chaverri et al. 200), and Torrubiella
luteorostrata Zimm. (pathogen of scale insects; HywelJones 1993). The fourth lineage is described here
as Metacordyceps; it comprises former species of
Cordyceps and their related anamorphs and as a genus
displays relatively broad arthropod host associations.
ClaviCiPitaCEaE (Lindau) Earle ex Rogerson,
Mycologia 2 : 900. 1970, emend. G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora
Stromata or subiculum darkly or brightly coloured,
leshy or tough. Perithecia supericial to completely
immersed, ordinal or oblique in arrangement. Asci
cylindrical with thickened ascus apex. Ascospores
usually cylindrical and multiseptate, disarticulating into
part-spores or non-disarticulating.
Type: Claviceps Tul., Ann. Sci. Nat. Bot., Sér. 3, 20: 43.
183.
Teleomorphic genera: Aciculosporium, Atkinsonella,
Balansia, Claviceps, Epichloë, Heteroepichloë,
Hypocrella, Metacordyceps gen. nov., Myriogenospora,
Neoclaviceps, Parepichloë, Regiocrella, Shimizuomyces.
Anamorphic genera: Aschersonia, Ephelis Fr.,
Metarhizium, Neotyphodium A.E. Glenn, C.W. Bacon
& Hanlin, Nomuraea, paecilomyces-like, Pochonia,
Sphacelia Lév., verticillium-like.
MEtaCOrdyCEPs G.H. Sung, J.M. Sung, HywelJones & Spatafora, gen. nov. MycoBank MB04182.
Stromata solitaria vel nonnulla aggregata, simplicia vel ramosa.
Stipes carnosus vel tenax, albidus, viridi-luteus vel viridulus,
cylindricus vel sursum dilatatus. Pars fertilis cylindrica vel clavata.
Perithecia partim vel omnino in stromate immersa, perpendicularia
vel oblique inserta. Asci cylindrici, apice inspissato. Ascosporae
cylindricae, multiseptatae, in cellulas diffrangentes vel maturae
integrae remanentes.
Stromata solitary or several, simple or branched. Stipe
leshy or tough, whitish, greenish yellow to greenish,
cylindrical to enlarging in fertile part. Fertile part
cylindrical to clavate. Perithecia partially or completely
immersed in stromata, ordinal or oblique in arrangement.
Asci cylindrical with thickened ascus apex. Ascospores
cylindrical, multiseptate, disarticulating into part-spores
or remaining intact at maturity.
Type: Cordyceps taii Z.Q. Liang & A.Y. Liu
Etymology: Greek meta = behind, a genus close
to Cordyceps (and suggesting relationship to
Metarhizium).
Anamorphic
genera:
Metarhizium,
paecilomyces-like, Pochonia.
Nomuraea,
Commentary: The genus Metacordyceps is proposed
for species of Cordyceps s. l. in the Clavicipitaceae s.
s. based on the phylogenetic placement of C. taii (Figs
1–2, 10). The genus is applied to the C. taii clade, which
is strongly supported (MP-BP = 73 %, ML-BP = 78 %,
PP = 1.00 in Figs 1–2, 10). Among the members of the
clade, the best-known taxon is the anamorphic genus
Metarhizium, because of its importance in biological
control (Samson et al. 1988, Evans 2003). Currently,
three species of Cordyceps (viz., C. brittlebankisoides,
C. campsosterni, and C. taii) are known as teleomorphs
of Metarhizium (Liang et al. 1991, Liu et al. 2001,
Zhang et al. 2004). The genus name Metacordyceps
is here used to emphasize that the clade includes the
species of Cordyceps s. l. that produce Metarhizium
anamorphs although other species of Cordyceps (e.g.,
C. chlamydosporia) in the clade are not connected to
Metarhizium anamorphs.
Metacordyceps yongmunensis G.H. Sung, J.M.
Sung & Spatafora, sp. nov. MycoBank MB04183.
Figs B, F-K, 11A-G.
Anamorph: pochonia-like.
Stromata nonnulla vel raro singula, clavata, simplicia vel saepius
ramosa, in chrysalidibus Lepidopterarum. Pars fertilis alba vel dilute
lutea, a stipite haud distincta. Perithecia sparsa vel dense aggregata,
partim immersa, brunneo-lutea, dilute brunnea vel aurantiobrunnea, oblique inserta, fusiformia vel clavata, 0–800 × 40–
00 µm. Asci 8-spori, hyalini, cylindrici, 20–30 × –7 µm, apice
conspicue inspissato. Ascosporae iliformes, hyalinae, inconspicue
multiseptatae, haud fragmentatae, 180–34 × 1 µm. Anamorphe
Pochoniae similis.
Stromata several or rarely solitary, clavate, simple or
more usually branched, on pupa of Lepidoptera. Fertile
area white to pale yellow, not differentiated from stipe.
Perithecia scattered or crowded, loosely immersed,
brownish yellow, pale brown to orangish brown,
oblique in arrangement, fusiform to clavate, 0–800 ×
40–00 µm. Asci 8-spored, hyaline, cylindrical, 20–
30 × –7 µm, possessing a prominent apical cap.
Ascospores iliform, hyaline, multiseptate with indistinct
septation, not fragmenting into part-spores, 180–34
× 1 µm. Conidiophores erect, produced in prostrate
aerial hyphae. Phialides hyaline, solitary, awl-shaped,
20–28 × 2–2.2 μm. Conidia hyaline, elliptical to oblong,
in slimy heads, 2–3.5 × 1.5–2.4 μm. Chlamydospores
present.
Etymology: yongmunensis in reference to the known
locality of the irst record of the species being Mt.
Yongmun, Republic of Korea.
27
GenBank Accession Number
Species
Voucher Info.
Host/Substratum
nrssU
nrlsU
tef1
rpb1
rpb2
tub
Aphysiostroma stercorarium
ATCC 62321 T
Cow dung
AF4379
AF43792
AF43782
AY48933
EF49103
EF49132
AY489
Aschersonia badia
BCC 810
Scale insect (Hemiptera)
DQ2273
DQ1872
DQ22317
DQ2233
DQ22411
DQ22472
EF4899
Aschersonia placenta
BCC 789
Scale insect (Hemiptera)
EF49121
EF49074
EF490
EF4908
EF49104
EF49133
EF48998
Balansia epichloë
A.E.G. 9-1a
Poaceae
EF48949
EF48743
EF4881
EF48908
Balansia henningsiana
GAM 1112
Panicum sp. (Poaceae)
AY4723
AY4727
AY48910
AY48943
DQ22413
DQ22474
AY4897
Balansia pilulaeformis
A.E.G. 94-2
Poaceae
AF4374
AF43788
DQ22319
DQ223
DQ22414
DQ2247
EF48999
Soil
AF33970
AF33920
EF4907
EF4908
EF49134
EF49000
DQ82044
DQ82027
DQ82029
DQ82013
EF4913
EF49001
DQ2241
DQ2247
EF49002
1
T
atp6
Beauveria caledonica
ARSEF 27
Bionectria cf. aureofulva
G.J.S. 71-328
Bionectria ochroleuca
CBS 1140
Bark
AY48984
AY48971
AY48911
Claviceps fusiformis
ATCC 26019
Poaceae
DQ2238
u17402
DQ22320
DQ223
Claviceps paspali
ATCC 13892
Poaceae
u32401
u4782
DQ22321
DQ2237
DQ2241
DQ22478
Claviceps purpurea
GAM 1288
Dactylis glomerata (Poaceae)
AF437
AF43789
AF43778
AY48948
DQ22417
DQ22479
Claviceps purpurea
S.A. cp11
Poaceae
EF49122
EF4907
EF4908
EF49087
EF4910
EF4913
Cordyceps acicularis
OSC 110987
Coleopteran larva
EF4890
EF4880
EF48744
EF4882
Cordyceps acicularis
OSC 110988
Coleopteran larva
EF4891
EF48804
EF4874
EF4883
Cordyceps cf. acicularis
OSC 12880
Coleoptera
DQ2243
DQ1877
DQ2232
DQ22371
DQ22423
DQ2248
EF49003
Cordyceps agriotidis
ARSEF 92
Coleoptera
DQ2240
DQ1874
DQ22322
DQ2238
DQ22418
DQ22480
EF49004
Cordyceps aphodii
ARSEF 498 T
Aphodius hewitti (Coleoptera)
DQ2241
DQ187
DQ22323
DQ22419
DQ22481
EF4900
Cordyceps bifusispora
EFCC 90
Lepidopteran pupa
EF4892
EF4880
EF4874
EF4884
EF48909
Cordyceps bifusispora
EFCC 820
Lepidopteran pupa
EF4893
EF48807
EF48747
EF488
EF48910
Coleoptera
DQ2242
DQ187
DQ22324
DQ2239
DQ22420
AUT
DQ22477
Cordyceps brunneipunctata
OSC 1287
Cordyceps capitata
OSC 71233
Elaphomyces sp. (Eurotiomycetes)
AY48989
AY489721
AY4891
AY48949
DQ22421
DQ22483
AY48981
Cordyceps cardinalis
CBS 113411 T
Lepidopteran larva
AY184973
AY18492
DQ2232
DQ22370
DQ22422
DQ22484
EF4900
Cordyceps cardinalis
CBS 113412 AUT
Lepidopteran larva
AY184974
AY18493
EF4909
EF49088
EF4910
EF49137
EF49007
Cordyceps chlamydosporia
CBS 101244 AUT
Egg of slug (Diplopoda)
DQ2244
DQ1878
DQ22327
DQ22372
DQ22424
DQ2248
EF49008
Cordyceps coccidiicola
Scale Insect (Hemiptera)
AB03119
AB03119
Cordyceps cochlidiicola
Lepidopteran pupa
AB027331
AB027377
EF48808
EF48748
EF488
EF48809
EF48749
EF4887
Cordyceps elongata
OSC 110989
Lepidopteran larva
Cordyceps entomorrhiza
KEW 3484
Coleopteran larva
EF4894
EF48911
DQ22482
SuNG ET AL.
28
Table 1. Taxa used in molecular phylogenetic analyses. (AUT Authentic material, T ex-type culture).
GenBank Accession Number
Species
Voucher Info. 1
Host/Substratum
nrssU
nrlsU
tef1
rpb1
rpb2
tub
atp6
Cordyceps fracta
OSC 110990
Elaphomyces sp. (Eurotiomycetes)
DQ224
DQ1879
DQ22328
DQ22373
DQ2242
DQ22487
EF49009
Cordyceps gracilis
EFCC 3101
Lepidopteran larva
EF489
EF48810
EF4870
EF4888
EF48913
Cordyceps gracilis
EFCC 872
Lepidopteran larva
EF489
EF48811
EF4871
EF4889
EF48912
Cordyceps gunnii
OSC 7404
Lepidopteran larva
AF33972
AF33922
AY4891
AY4890
DQ2242
DQ22488
AY48982
Cordyceps heteropoda
EFCC 1012
Nymph of cicada (Hemiptera)
EF4897
EF48812
EF4872
EF4880
EF48914
Cordyceps heteropoda
OSC 10404
Nymph of cicada (Hemiptera)
AY48990
AY489722
AY48917
AY4891
Nymph of cicada (Hemiptera)
AB027322
AB02738
Ant (Hymenoptera)
DQ224
DQ1870
DQ22329
DQ22374
DQ22427
DQ22489
Cordyceps inegoënsis
OSC 12877
Cordyceps irangiensis
OSC 12879
Ant (Hymenoptera)
EF49123
EF4907
EF4900
EF49089
EF49107
EF49138
Cordyceps japonica
OSC 110991
Elaphomyces sp. (Eurotiomycetes)
DQ2247
DQ1871
DQ22330
DQ2237
DQ22428
DQ22490
Elaphomyces sp. (Eurotiomycetes)
AB027320
AB0273
EF4882
EF4891
EF4873
EF4881
EF4891
EF4883
EF48917
Cordyceps jezoënsis
Cordyceps konnoana
EFCC 729
Coleopteran larva
EF4898
Cordyceps konnoana
EFCC 731
Coleopteran larva
EF4899
Cordyceps kyusyuënsis
EFCC 88
Lepidopteran pupa
EF4890
EF48813
EF4874
Cordyceps liangshanensis
EFCC 142
Lepidopteran pupa
EF4892
EF4881
EF487
Cordyceps liangshanensis
EFCC 123
Lepidopteran pupa
EF4891
EF48814
EF487
Cordyceps longisegmentis
OSC 110992
Elaphomyces sp. (Eurotiomycetes)
EF4881
Cordyceps longissima
EFCC 814
Nymph of cicada (Hemiptera)
EF48817
Cordyceps melolonthae
OSC 110993
Scarabaeid larva (Coleoptera)
DQ2248
DQ1872
DQ22331
DQ2237
Cordyceps militaris
OSC 9323
Lepidopteran pupa
AY184977
AY1849
DQ22332
DQ22377
AY4732
Cordyceps nigrella
EFCC 9247
Lepidopteran larva
EF4893
EF48818
EF4878
EF488
EF48920
Cordyceps nutans
OSC 110994
Stink bug (Hemiptera)
DQ2249
DQ1873
DQ22333
DQ22378
Cordyceps cf. ochraceostromata
ARSEF 91
Lepidoptera
EF4894
EF48819
EF4879
EF4887
EF48921
Cordyceps ophioglossoides
OSC 1040
Elaphomyces sp. (Eurotiomycetes)
AY48991
AY489723
AY48918
AY4892
DQ22429
Nymph of cicada (Hemiptera)
AB027323
AB02739
Cordyceps paradoxa
EF48918
EF4884
EF4877
EF49010
EF48919
EF488
29
Cordyceps cf. pruinosa
EFCC 197
limacodid pupa (Lepidoptera)
EF489
EF48820
EF4870
EF4888
Cordyceps cf. pruinosa
EFCC 93
limacodid pupa (Lepidoptera)
EF489
EF48821
EF4872
EF4889
Cordyceps cf. pruinosa
N.H.J. 1027
limacodid pupa (Lepidoptera)
EF4897
EF48822
EF4873
EF48870
DQ22491
EF49011
DQ22492
EF49012
DQ22493
DQ22494
AY48983
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Cordyceps irangiensis
GenBank Accession Number
Species
Voucher Info. 1
Host/Substratum
nrssU
nrlsU
tef1
rpb1
Cordyceps cf. pruinosa
N.H.J. 1084
Limacodid pupa (Lepidoptera)
EF4898
EF48823
EF4871
EF48871
Cordyceps ravenelii
OSC 11099
Coleopteran larva
DQ220
DQ1874
DQ22334
Cordyceps rhizoidea
N.H.J. 1222
Termite (Isoptera)
EF48970
EF4882
Cordyceps rhizoidea
N.H.J. 1229
Termite (Isoptera)
EF4899
Cordyceps robertsii
KEW 27083
Lepidoptera
Cordyceps scarabaeicola
ARSEF 89
Scarabaeid adult (Coleoptera)
Cordyceps sinensis
EFCC 7287
Cordyceps sobolifera
rpb2
tub
DQ22379
DQ22430
DQ2249
EF4874
EF48873
EF48923
EF48824
EF487
EF48872
EF48922
EF4882
EF487
AF33974
AF33924
DQ2233
DQ22380
DQ22431
Lepidopteran pupa
EF48971
EF48827
EF4877
EF48874
EF48924
KEW 78842
Nymph of cicada (Hemiptera)
EF48972
EF48828
EF4887
EF4892
Cordyceps sphecocephala
OSC 110998
Wasp (Hymenoptera)
DQ221
DQ187
DQ2233
DQ22381
DQ22432
Cordyceps staphylinidicola
ARSEF 718
Staphylinid pupa (Coleoptera)
EF48981
EF4883
EF4877
EF48881
Cordyceps stylophora
OSC 110999
Coleopteran larva
EF48982
EF48837
EF48777
EF48882
EF48931
Cordyceps stylophora
OSC 111000
Elaterid larva (Coleoptera)
DQ222
DQ187
DQ22337
DQ22382
DQ22433
DQ22497
Cordyceps subsessilis
OSC 7123
Scarabaeid larva (Coleoptera)
EF49124
EF49077
EF49090
EF49108
EF49139
EF4901
Cordyceps supericialis
MICH 323
Coleopteran larva
EF48983
Cordyceps taii
ARSEF 714
Lepidoptera
AF4373
AF43787
DQ22498
EF4901
Lepidoptera
AB04431
AB04437
Lepidoptera
EF48984
EF48838
Spittlebug (Hemiptera)
AB027330
AB02737
DQ22499
EF49017
DQ2200
EF49018
Cordyceps takaomontana
Cordyceps cf. takaomontana
N.H.J. 1223
Cordyceps tricentri
EF49013
EF49014
EF48883
AF4377
DQ22383
DQ22434
EF48778
EF48884
EF48932
Cordyceps tuberculata
OSC 111002
Lepidoptera
DQ223
DQ1877
DQ22338
DQ22384
DQ2243
Cordyceps unilateralis
OSC 12874
Ant (Hymenoptera)
DQ224
DQ1878
DQ22339
DQ2238
DQ2243
Cordyceps variabilis
ARSEF 3
Dipteran larva
DQ22
DQ1879
DQ22340
DQ2238
DQ22437
Cordyceps variabilis
OSC 111003
Dipteran larva
EF4898
EF48839
EF48779
EF4888
EF48933
Nymph of cicada (Hemiptera)
AB04432
AB04433
Cordyceps yakusimensis
DQ2249
atp6
Cordyceps sp.
EFCC 2131
Lepidopteran pupa
EF48977
EF48833
EF48770
EF4887
Cordyceps sp.
EFCC 213
Lepidopteran pupa
EF48979
EF48834
EF4879
EF48877
Cordyceps sp.
EFCC 23
Coleoptera
EF48980
EF4883
EF48772
Cordyceps sp.
N.H.J. 12118
Lepidoptera
EF48978
EF48829
EF4878
Cordyceps sp.
N.H.J. 1281
Termite (Isoptera)
EF48973
EF48831
EF4877
EF48930
Cordyceps sp.
N.H.J. 1282
Termite (Isoptera)
EF4897
EF48830
EF48771
EF4892
EF48878
EF48927
SuNG ET AL.
30
Table 1. Continued.
GenBank Accession Number
Species
Voucher Info. 1
Host/Substratum
nrssU
nrlsU
tef1
rpb1
rpb2
Cordyceps sp.
OSC 11099
Lepidoptera
EF48974
EF48832
EF48773
EF48880
EF48928
Cordyceps sp.
OSC 110997
Ant (Hymenoptera)
EF4897
EF48774
EF48879
EF48929
Cosmospora coccinea
CBS 11400
Inonotus nodulosus (Hymenomycetes)
AY489702
AY489734
AY48929
AY4897
Engyodontium aranearum
CBS 309.8
spider (Arachnida)
AF3397
AF3392
DQ22341
tub
atp6
DQ22438
DQ2201
AY4899
DQ22387
DQ22439
DQ2202
EF49019
Epichloë typhina
ATCC 56429
Festuca rubra (Poaceae)
u3240
u1739
AF43777
AY4893
DQ22440
DQ2203
AY48984
Glomerella cingulata
CBS 11404
Fragaria sp. (Rosaceae)
AF4372
AF4378
AF43773
AY4899
DQ22441
DQ2204
AY48990
Glomerella cingulata
F.A.u. 13
Fragaria rp. (Rosaceae)
u48427
u48428
AF43772
DQ8844
DQ884
EF49140
EF49020
Haptocillium balanoides
CBS 20.82
Nematode
AF33988
AF33939
DQ22342
DQ22388
DQ22442
DQ220
EF49021
T
Haptocillium sinense
CBS 7.9
Nematode
AF33994
AF3394
DQ22343
DQ22389
DQ22443
DQ220
EF49022
Haptocillium zeosporum
CBS 33.80
Nematode
AF33989
AF33940
EF4902
EF49091
EF49109
EF49141
EF49023
Hirsutella sp.
N.H.J. 122
Hemipteran adult
EF4912
EF49078
EF4903
EF49092
EF49111
EF49142
EF49143
OSC 1287
Hemipteran adult
EF4912
EF49079
EF4904
EF49093
EF49110
Hydropisphaera erubescens
ATCC 36093
Cordyline banksii (Laxmanniaceae)
AY4722
AY472
DQ22344
DQ22390
AY4731
DQ223
EF49024
Hydropisphaera peziza
CBS 102038
On bark
AY48998
AY489730
AY4892
AY4891
DQ22444
DQ2207
AY48991
Hymenostilbe aurantiaca
OSC 12878
Ant (Hymenoptera)
DQ22
DQ18770
DQ2234
DQ22391
DQ2244
DQ2208
Hypocrea lutea
ATCC 208838
On decorticated conifer wood
AF4378
AF43791
AF43781
AY4892
DQ2244
DQ2209
Hypocrella schizostachyi
BCC 14123
Scale insect (Hemiptera)
DQ227
DQ18771
DQ2234
DQ22392
DQ22447
DQ2210
EF4902
Hypocrella sp.
G.J.S. 89-104
Scale insect (Hemiptera)
u32409
u47832
DQ22347
DQ22393
DQ22448
DQ2211
EF4902
Hypomyces polyporinus
ATCC 76479
Trametes versicolor (Hymenomycetes)
AF43771
AF43793
AF43784
AY4893
Isaria cf. farinosa
OSC 111004
Lepidopteran pupa
EF4898
EF48840
EF48780
EF4888
Isaria farinosa
OSC 11100
Lepidopteran pupa
DQ228
DQ18772
DQ22348
DQ22394
Isaria farinosa
OSC 11100
Lepidopteran pupa
EF49127
EF49080
EF490
EF49094
EF49144
EF49027
Isaria tenuipes
OSC 111007
Lepidopteran pupa
DQ229
DQ18773
DQ22349
DQ2239
DQ22449
DQ2213
EF49029
Lecanicillium antillanum
CBS 30.8 T
Agaric (Hymenomycetes)
AF3398
AF3393
DQ2230
DQ2239
DQ2240
DQ2214
EF49030
Lecanicillium aranearum
CBS 72.73a
Spider (Arachnida)
AF3398
AF33937
EF48781
EF48887
EF48934
Lecanicillium attenuatum
CBS 402.78
Leaf litter of Acer saccharum
AF33914
AF339
EF48782
EF48888
EF4893
Lecanicillium dimorphum
CBS 33.8 T
Agaricus bisporus (Hymenomycetes)
AF33908
AF3399
EF48784
EF48890
Lecanicillium fusisporum
CBS 14.70 T
Coltricia perennis (Hymenomycetes)
AF33998
AF33949
EF48783
EF48889
Lecanicillium psalliotae
CBS 101270
Soil
EF49128
EF49081
EF490
EF4909
EF4914
EF49031
AY48992
AY48993
DQ2212
EF49113
EF49028
31
Lecanicillium psalliotae
CBS 32.81
Soil
AF33909
AF3390
EF4907
EF4909
EF49112
EF4914
EF49032
Leuconectria clusiae
ATCC 22228 T
Soil
AY489700
AY489732
AY48927
AY4894
EF49114
EF49147
AY4899
Mariannaea pruinosa
ARSEF 413 AUT
Iragoides fasciata (Lepidoptera)
AY184979
AY18498
DQ2231
DQ22397
DQ2241
DQ221
EF49033
Metarhizium album
ARSEF 2082
Cofana spectra (Hemiptera)
DQ220
DQ1877
DQ2232
DQ22398
DQ2242
DQ221
EF49034
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Hirsutella sp.
GenBank Accession Number
Species
Voucher Info.
Host/Substratum
nrssU
nrlsU
tef1
rpb1
rpb2
tub
atp6
Metarhizium anisopliae
ARSEF 314
Oryctes rhinoceros (Coleoptera)
AF33979
AF33930
AF43774
DQ22399
DQ2243
DQ223
EF4903
Metarhizium lavoviride
ARSEF 2037 T
Nilaparvata lugens (Hemiptera)
AF33980
AF33931
DQ2233
DQ22400
DQ2244
DQ2217
EF4903
Microhilum oncoperae
AFSEF 438 AUT
Oncopera intricate (Lepidoptera)
AF33981
AF33932
EF4878
EF48891
EF4893
Myriogenospora atramentosa
A.E.G. 9-32
Andropogon virginicus (Poaceae)
AY489701
AY489733
AY48928
AY489
DQ224
DQ2218
Nectria cinnabarina
CBS 1140
Betula sp. (Betulaceae)
u32412
u00748
AF4378
AY489
DQ224
DQ2219
EF49037
Nomuraea `typicola
CBS 744.73
Spider (Arachnida)
EF48987
EF48841
EF4878
EF48892
Nomuraea rileyi
CBS 80.71
Lepidoptera
AY2420
AY2420
EF48787
EF48893
EF48937
Ophionectria trichospora
CBS 10987
On liana
AF437
AF43790
AF43779
AY4899
DQ2247
DQ2220
EF49039
Paecilomyces carneus
CBS 239.32 T
Sand dune
EF48988
EF48843
EF48789
EF48894
EF48938
Paecilomyces carneus
CBS 399.9
Soil
EF48989
EF48842
EF48788
EF4889
EF48939
Paecilomyces cinus
ARSEF 2181
Meloidogynesp. (Nematoda) AF33983
AF33934
EF48790
EF4889
Soil
AY24189
AY24227
EF48792
EF48898
EF48941
Meloidogynesp. (Nematoda)
AY24188
EF48844
EF48791
EF48897
EF48940
EF48942
T
Paecilomyces lilacinus
CBS 284.3
Paecilomyces lilacinus
CBS 431.87
Paecilomyces marquandii
CBS 182.27 T
Phytocordyceps ninchukispora
Phytocordyceps ninchukispora
1
Soil
EF48990
EF4884
EF48793
EF48899
E.G.S. 38.1
AUT
Beilschmiedia erythrophloia (Lauraceae)
EF48991
EF4884
EF4879
EF48900
E.G.S. 38.1
AUT
Beilschmiedia erythrophloia (Lauraceae)
EF48992
EF48847
EF48794
EF48901
T
Pochonia bulbillosa
CBS 14.70
Root of Picea abies
AF33991
AF33942
EF4879
EF48902
EF48943
Pochonia chlamydosporia
CBS 04. T
Nematode
AF33993
AF33944
EF4909
EF49098
EF49120
EF49149
EF49040
Pochonia gonioides
CBS 891.72
Nematode
AF33999
AF3390
DQ2234
DQ22401
DQ2248
DQ2221
EF49041
Heterodera avenae (Nematoda)
AF3391
AF339
EF48797
EF48903
EF48944
AY48998
T
Pochonia rubescens
CBS 44.88
Pseudonectria rousseliana
CBS 114049
Buxus sempervirens (Buxaceae)
AF4377
u1741
AF43780
AY48970
DQ2249
DQ2222
Rotiferophthora angustispora
CBS 101437
Rotifer (Rotifera)
AF33984
AF3393
AF4377
DQ22402
DQ2240
DQ2223
EF49042
Roumegueriella rufula
CBS 34.8
Globodera rostochiensis (Nematoda)
DQ221
DQ1877
DQ223
DQ22403
DQ2241
DQ2224
EF49043
Roumegueriella rufula
G.J.S. 91-14
Globodera rostochiensis (Nematoda)
EF49129
EF49082
EF49070
EF49099
EF4911
EF4910
EF49044
Shimizuomyces paradoxus
EFCC 279
Smilax sieboldii (Smilacaceae)
EF49131
EF49084
EF49071
EF49100
EF49117
EF4911
EF4904
Shimizuomyces paradoxus
EFCC 4
Smilax sieboldii (Smilacaceae)
EF49130
EF49083
EF49072
EF49101
EF49118
EF4912
EF4904
Simplicillium lamellicola
CBS 11.2 T
Agaricus bisporus (Hymenomycetes)
AF33901
AF3392
DQ223
DQ22404
DQ2242
DQ222
EF49047
Simplicillium lanosoniveum
CBS 10127
Hemileia vastatrix (Uredinales)
AF33903
AF3394
DQ2237
DQ2240
DQ2243
DQ222
EF49048
Simplicillium lanosoniveum
CBS 704.8
Hemileia vastatrix (Uredinales)
AF33902
AF3393
DQ2238
DQ2240
DQ2244
DQ2227
EF49049
Simplicillium obclavatum
CBS 311.74 T
Air above sugarcane ield
AF3397
AF33917
EF48798
Sphaerostilbella berkeleyana
CBS 102308
Polypore (Hymenomycetes)
AF43770
u007
AF43783
AY48971
DQ224
DQ2228
EF4900
SuNG ET AL.
32
Table 1. Continued.
A.E.G., A. E. Glenn personal collection; ARSEF, USDA-ARS Collection of Entomopathogenic Fungal cultures, Ithaca, NY; ATCC, American Type Culture Collections, Manassas, VA; BCC, BIOTEC Culture
Collection, Klong Luang, Thailand; CBS, Centraalbureau voor Schimmelcultures, Utrecht, the Netherlands; EFCC, Entomopathogenic Fungal Culture Collection, Chuncheon, Korea; F.A.U., F. A. Uecker
personal collection; E.G.S., E, G. Simmons personal collection; GAM, Julian H. Miller Mycological Herbarium Athens, GA; G.J.S., G. J. Samuels personal collection; KEW, mycology collection of Royal Botanical
Garden, KEW, Surrey, uK; MICH, university of Michigan Herbarium, Ann Arbor, MI; N.H.J., Nigel Hywel-Jones personal collection; OSC, Oregon State university Herbarium, Corvallis, OR; S.A., S. Alderman
personal collection.
DQ22471
AY4898
Crataegus crus-galli (Rosaceae)
CBS 102797
Viridispora diparietispora
AY489703
AY48973
AY48930
EF48948
EF48907
EF48803
AF3394
AF33913
Spider (Arachnida)
CBS 102184
Verticillium sp.
1
EF490
DQ2234
EF4904
DQ22470
CBS 40.88
T
Verticillium incurvum
Ganoderma lipsiense (Hymenomycetes)
AF33900
AF3391
DQ2232
DQ22410
DQ2233
EF4903
DQ2249
EF48947
EF48802
DQ2231
AF33947
AF33947
CBS 384.81
Verticillium epiphytum
AF3399
Hemileia vastatrix (Uredinales)
Hemileia vastatrix (Uredinales)
CBS 14.1 T
Verticillium epiphytum
AF3399
DQ22409
DQ2232
AY48900
DQ2248
AY48973
DQ2231
EF49119
EF49102
EF49073
AY18497
AY489737
AY48970
ATCC 16535
Verticillium dahliae
Lepidoptera
Crataegus crus-galli (Rosaceae)
CBS 101237
Torrubiella wallacei
AY184978
AY48932
DQ2247
DQ22408
T
AUT
Spider (Arachnida)
ARSEF 191
Torrubiella ratticaudata
DQ222
DQ18777
DQ2230
EF4894
EF4890
EF48800
EF48849
Scale insect (Hemiptera)
N.H.J. 121
Torrubiella luteorostrata
EF48994
EF4890
EF48801
EF4880
Scale insect (Hemiptera)
N.H.J. 11343
Torrubiella luteorostrata
EF4899
DQ224
DQ22407
Coccus viridis (Hemiptera)
CBS 101247
Torrubiella confragosa
AF33904
AF339
DQ2239
EF4894
EF48904
EF48799
EF48848
Bdelloid rotifer (Rotifera)
ARSEF 343 AUT
Tolypocladium parasiticum
EF48993
EF4913
DQ2230
EF4901
DQ2229
atp6
tub
rpb2
GenBank Accession Number
rpb1
tef1
nrlsU
Host/Substratum
Voucher Info. 1
Species
nrssU
EF4902
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Known distribution: Republic of Korea.
Specimens examined: Mt. Yongmun, Gyunggi
Province, Republic of Korea: 13 June 1998, EFCC
2131 (holotype); 13 June 1998, EFCC 2134; 13 June
1998, EFCC 213; 30 June 1999, EFCC 3379; 30
June 1999, EFCC 3380; 29 Aug. 1999, EFCC 4342;
8 Aug. 1999, EFCC 4343; 8 June 2000, EFCC 491;
30 June 2004, EFCC 12287; 30 June 2004, EFCC
12288; 30 June 2004, EFCC 12291; 8 Aug. 2004,
EFCC 12467. Mt. Chiak, Kangwon Province, Republic
of Korea: 8 Aug. 2000, EFCC 70. Bukbang-myun,
Kangwon Province, Republic of Korea: 21 June 2002,
EFCC 8808. Living culture in EFCC.
Commentary: Most specimens of M. yongmunensis
possess several stromata (up to 10), on a large pupa
of Lepidoptera deeply buried in soil (Fig. B). Stroma
of the species is typically branched in a dichotomous
way at its basal or upper regions (Fig. 5B). Perithecia
are usually obliquely inserted in the stromata with
a few exceptions that are ordinally arranged, i.e.
at right angles to the surface of the stromata (Fig.
B). While some perithecia are characterized by an
acute narrowing of the perithecium at the ostiole,
producing a narrow terminal end (Fig. F), others
are not signiicantly narrowed (Fig. 11B). In the asci
the ascospores are arranged parallel for their entire
length and almost reach the ascus foot, suggesting
that ascospores are of approximately the same length
as the asci (Figs I, 11A). unlike the distinct septation
of ascospores as seen in C. militaris (Fig. 9O), the
septa of the ascospores are indistinct and discharged
ascospores do not disarticulate into part-spores (Figs
K, 11A).
In the anamorph of M. yongmunensis, cultures
derived from ascospores are moderately fast growing
in SDAY (Sabouraud-dextrose-yeast extract agar) and
the colonies reach 2–3 mm diam at 2 °C in 10 d.
Colonies are slightly cottony without zonation and white
with a green margin, remaining greenish brown at the
reverse side of the cultures. Conidiophores are erect
and produced in prostrate aerial hyphae. Phialides are
solitary, not in whorls, broader at the base and tapering
towards the end, measuring 20–28 × 2.0–2.2 μm (Fig.
11C). Conidia are in slimy heads (with usually 2 or 3
conidia) and ellipsoidal to oblong, measuring 2–3.
× 1.–2.4 μm (Fig. 11C). In submerged areas of the
cultures, chlamydospores are developed in chains or
reduced to intercalary swollen structures (Figs 11E-G).
The anamorph of M. yongmunensis is best classiied
as pochonia-like because of its subulate phialides and
production of chlamydospores, although verticilliumlike whorls of phialides were not observed (Zare et al.
2001). In Metacordyceps, M. yongmunensis is most
similar to M. chlamydosporia (= C. chlamydosporia)
in the shape of perithecia and its anamorph. Both
species produce brownish perithecia that possess long
terminal ends in white or pale yellow stromata (Zare
et al. 2001). The anamorph of M. chlamydosporia is
identical with the type of Pochonia. Thus the production
of chlamydospores can be informative for recognizing
some species of Metacordyceps.
33
SuNG ET AL.
34
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Accepted names and new combinations
for Metacordyceps
The following taxa are accepted species of
Metacordyceps based on their inclusion in molecular
phylogenies presented herein1 (see Table 1) or
morphological descriptions matching the characters
described above2. The known anamorph connection is
provided for the species of Metacordyceps.
New combinations for anamorphs associated
with Metacordyceps
T. parasiticum is transferred to the genus Pochonia
based on molecular phylogenies presented herein1.
1
Pochonia parasitica (G.L. Barron) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04189.
≡ Tolypocladium parasiticum G.L. Barron, Canad. J. Bot. 8:
439. 1980.
2
Metacordyceps brittlebankisoides (ZuoY. Liu,
Z.Q. Liang, Whalley, Y.-J. Yao & A.Y. Liu) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04184.
≡ Cordyceps brittlebankisoides ZuoY. Liu, Z.Q. Liang,
Whalley, Y.-J. Yao & A.Y. Liu, J. Invert. Pathol. 78: 179.
2001.
Anamorph: Metarhizium
Metacordyceps campsosterni (W.M. Zhang & T.H.
Li) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB0418
2
≡ Cordyceps campsosterni W.M. Zhang & T.H. Li, Fungal
Diversity 17: 240. 2004. [as C. ‘campsosterna’].
Anamorph: Metarhizium
1
Metacordyceps chlamydosporia (H.C. Evans) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB0418.
≡ Cordyceps chlamydosporia H.C. Evans, in Zare et al.,
Nova Hedwigia 73: 9. 2001.
Anamorph: Pochonia chlamydosporia (Goddard)
Zare & W. Gams
1
Metacordyceps liangshanensis (M. Zang, D. Liu & R.
Hu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04187.
≡ Cordyceps liangshanensis M. Zang, D. Liu & R. Hu, Acta
Bot. Yunnanica 4: 174. 1982.
1
Metacordyceps taii (Z.Q. Liang & A.Y. Liu) G.H.
Sung, J.M. Sung, Hywel-Jones, Spatafora, comb. nov.
MycoBank MB04188.
≡ Cordyceps taii Z.Q. Liang & A.Y. Liu, Acta Mycol. Sin. 10:
27. 1991.
Anamorph: Metarhizium anisopliae var. anisopliae
(Metschn.) Sorokin
1
Metacordyceps yongmunensis G.H. Sung, J.M.
Sung, Spatafora, sp. nov., see p. 27.
Anamorph: pochonia-like
ClaviCiPitaCEaE Clade B
Clavicipitaceae clade B is strongly supported (MP-BP
= 93 %, ML-BP = 98 %, PP = 1.00 in Figs 1–2, 10)
and the family Ophiocordycipitaceae is proposed for
it with the type genus Ophiocordyceps Petch. Most
species of the Ophiocordycipitaceae produce darkly
pigmented stromata that are pliant to wiry, or ibrous
to tough in texture. Ecologically, many species of the
family are known as pathogens of subterranean or
wood-inhabiting hosts, buried in soil or embedded in
decaying wood. Notable exceptions do exist to these
traits with brightly coloured species that may or may
not attack adult stages of hosts and occur in exposed
habitats.
OPhiOCOrdyCiPitaCEaE G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, fam. nov. MycoBank
MB04190.
Stromata vel subiculum fusca vel raro laete colorata, tenacia, ibrosa
vel lexibilia, raro carnosa, saepe ostiolis peritheciorum prominentibus,
summa saepe peritheciis carentia. Perithecia supericialia vel omnino
immersa, perpendicularia ad supericiem vel oblique inserta. Asci
cylindrici, apice inspissato. Ascosporae cylindricae, multiseptatae,
maturae in cellulas diffrangentes vel integrae remanentes.
Stromata or subiculum darkly pigmented or rarely
brightly coloured, tough, ibrous to pliant, rarely
leshy, often with aperithecial apices or lateral pads.
Perithecia supericial to completely immersed, ordinal
or oblique in arrangement. Asci usually cylindrical with
thickened ascus apex. Ascospores usually cylindrical,
multiseptate, disarticulating into part-spores or nondisarticulating.
Type: Ophiocordyceps Petch, Trans. Brit. Mycol. Soc.
1: 74. 1931.
Teleomorphic genera: Elaphocordyceps, Ophiocordyceps
Anamorphic genera: Haptocillium, Harposporium
Lohde, Hirsutella, Hymenostilbe, paecilomyces-like,
Paraisaria, Syngliocladium, Tolypocladium, verticilliumlike.
Fig. 10 (Page 34). New classiication of Cordyceps and clavicipitaceous fungi based on Bayesian consensus tree in Fig. 2. Portions of
Bionectriaceae and Nectriaceae are not shown. Tree description is the same as in Fig. 2. For internodes that are related with nomenclatural
changes, bootstrap proportions of MP analyses (MP-BP) in Fig. 1 are shown above corresponding nodes before the backslash. Bootstrap
proportions of ML analyses (ML-BP) and posterior probabilities (PP) in Fig. 2 are shown above internodes after backslash and below internodes,
respectively. For the corresponding internode of Ophiocordyceps, bootstrap proportions (MP-BP & ML-BP) and posterior probabilities (PP) were
obtained from analyses based on the 147-taxon 5-gene data set in Fig. 3. Portions of the tree in grey rectangular boxes indicate nomenclatural
changes of Cordyceps.
3
SuNG ET AL.
Fig. 11. A–B. Line drawings of morphology of Metacordyceps yongmunensis. C–G. Line drawings of pochonia-like anamorph of M. yongmunensis.
A. Non-disarticulating ascospore and ascus. B. Oblique arrangement of perithecia in stroma. C. Conidia and phialides. D. Developing conidia
germinated from ascospore. E. Chlamydospores submerged in SDAY agar. F. Developing chlamydospores submerged in SDAY agar. G.
Intercalary swollen hyphae. Scale bars: A, C–G = 10 μm, B = 200 μm.
ElaPhOCOrdyCEPs G.H. Sung & Spatafora,
gen. nov. MycoBank MB04191.
Stromata singula vel nonnulla aggregata, simplicia vel ramosa. Stipes
ibrosus vel tenax, raro carnosus, obscure brunneus vel olivaceoviridulus, raro albidus, cylindricus vel sursum dilatatus. Stromata
hospite insidentia vel rhizomorphis eo conjuncta. Pars fertilis
clavata vel capitata, raro indistincta. Perithecia partim wel omnino
in stromate immersa, perpendicularia ad supericiem. Asci cyindrici,
apice inspissato. Ascosporae cylindricae, multiseptatae, maturae in
cellulas diffrangentes. Anamorphe Verticillii similis vel absens.
Stromata solitary to several, simple or branched. Stipe
ibrous to tough, rarely leshy, dark brownish to greenish
with olivaceous tint, rarely whitish, cylindrical to enlarging
in the fertile part. Stroma connected directly to the
host or indirectly through rhizomorph-like structures.
Fertile part clavate to capitate, rarely undifferentiated.
Perithecia partially or completely immersed in stromata,
ordinal in arrangement. Asci cylindrical with thickened
ascus apex. Ascospores cylindrical, multiseptate,
disarticulating into part-spores.
Type: Cordyceps ophioglossoides (Ehrh.) Link
Etymology: Greek elaphe = deer, from the host fungus,
Elaphomyces.
3
Commentary: The C. ophioglossoides clade is strongly
supported (MP-BP = 71 %, ML-BP = 88 %, PP = 100 in
Figs 1–2, 10) and includes species of Cordyceps s. l.
that parasitize the trufle-like genus Elaphomyces and
cicada nymphs (e.g., C. inegoënsis and C. paradoxa)
and beetles (e.g., C. subsessilis) (Figs , 10).
Currently, 22 species are anticipated to be included
in the C. ophioglossoides clade, of which more than
18 species are known as parasites of Elaphomyces
(Mains 1957, Kobayasi & Shimizu 1960, 1963). The
host afiliation of Elaphomyces parasites has long been
recognized as a diagnostic character in Cordyceps
classiication (Massee 1895, Kobayasi 1941, 1982,
Mains 1957, 1958). The oldest applicable genus
name is Cordylia Fr. 1818 (Massee 189). However,
it cannot be applied to the C. ophioglossoides clade
because it is a homonym of Cordylia Pers. 1807 (Mains
198), which is also homonym of Cordyla Lour. 1790
(Leguminosae). Therefore, the genus Elaphocordyceps
is proposed based on the phylogenetic placement of
C. ophioglossoides and applied to the well-supported
C. ophioglossoides clade. Although C. subsessilis
is morphologically and ecologically distinct, the
genus is well recognized by its dominant ecology as
being pathogens of Elaphomyces and cicadas. The
darkly pigmented, ibrous stromata with more or less
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
olivaceous tint are also good diagnostic characters for
recognizing the species of Elaphocordyceps.
1
Elaphocordyceps jezoënsis (S. Imai) G.H. Sung, J.M.
Sung & Spatafora, comb. nov. MycoBank MB04199.
≡ Cordyceps jezoënsis S. Imai, Trans. Sapporo Nat. Hist.
Soc. 11: 33. 1929.
Anamorphic genera: Tolypocladium, verticillium-like.
Accepted names and new combinations
for Elaphocordyceps
The following taxa are accepted species of
Elaphocordyceps based on their inclusion in molecular
phylogenies presented herein1 (see Table 1) or
morphological descriptions matching the characters
described above2. Where known we provide anamorph
connection for the species of Elaphocordyceps.
1
Elaphocordyceps longisegmentis (Ginns) G.H.
Sung, J.M. Sung & Spatafora, comb. nov. MycoBank
MB04200.
≡ Cordyceps longisegmentis Ginns, Mycologia 80: 219.
1988.
2
Elaphocordyceps minazukiensis (Kobayasi &
Shimizu) G.H. Sung, J.M. Sung & Spatafora, comb.
nov. MycoBank MB04201.
≡ Cordyceps minazukiensis Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 8: 117. 1982.
1
Elaphocordyceps capitata (Holmsk.) G.H. Sung, J.M.
Sung & Spatafora, comb. nov. MycoBank MB04192.
≡ Sphaeria capitata Holmsk., Beata Ruris Otia Fungis Danicis
1: 38. 1790 : Fries, Syst. Mycol. 2: 324, 1823.
≡ Torrubia capitata (Holmsk. : Fr.) Tul. & C. Tul., Sel. Fung.
Carpol. 3: 22. 18.
≡ Cordyceps capitata (Holmsk. : Fr.) Link., Handbuch
zur Erkennung der nutzbarsten und am häuigsten
vorkommenden Gewächse 3: 347. 1833.
= Cordyceps canadensis Ellis & Everh., Bull. Torrey Bot. Club
2: 01. 1898.
≡ Cordyceps capitata var. canadensis (Ellis & Everh.) Lloyd,
Mycol. Writ. : 09. 191.
= Sphaeria agariciformis Bolt., Hist. Fung. Halifax, p. 130. 1789.
≡ Cordyceps agariciformis (Bolt.) Seaver, North Amer. Fl. 3:
33. 1910.
= Cordyceps nigriceps Peck, Bull. Torrey Bot. Club 27: 21.
1900.
2
Elaphocordyceps miomoteana (Kobayasi &
Shimizu) G.H. Sung, J.M. Sung & Spatafora, comb.
nov. MycoBank MB04202.
≡ Cordyceps miomoteana Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 8: 118. 1982.
1
Elaphocordyceps ophioglossoides (Ehrh. : Fr.) G.H.
Sung, J.M. Sung & Spatafora, comb. nov. MycoBank
MB04203.
≡ Sphaeria ophioglossoides Ehrh., in Pers., Comment de
Fung. Clavaef. p. 12. 1797 : Fries, Syst. Mycol. 2: 324.
1823.
≡ Torrubia ophioglossoides (Ehrh. : Fr.) Tul., Sel. Fung.
Carpol. 3: 20. 18.
≡ Cordyceps ophioglossoides (Ehrh. : Fr.) Link, Handbuck
zur Erkennung der nutzbarsten und am häuigsten
vorkommenden Gewächse 3: 347. 1833.
Anamorph unknown, not growing in culture.
2
Elaphocordyceps delicatistipitata (Kobayasi) G.H.
Sung, J.M. Sung & Spatafora, comb. nov. MycoBank
MB04193.
≡ Cordyceps delicatistipitata Kobayasi, Bull. Natn. Sci. Mus.
Tokyo 5: 79. 1960 (as C. ‘delicatostipitata’).
1
Elaphocordyceps fracta (Mains) G.H. Sung, J.M.
Sung & Spatafora, comb. nov. MycoBank MB04194.
Anamorph: verticillium-like
2
Elaphocordyceps
ophioglossoides
f.
alba
(Kobayasi & Shimizu ex Y.J. Yao) G.H. Sung, J.M.
Sung & Spatafora, comb. nov. MycoBank MB04204.
≡ Cordyceps ophioglossoides f. alba Kobayasi & Shimizu ex
Y.J. Yao, in Yao, Li, Pegler & Spooner, Acta. Mycol. Sin. 14:
27. 199.
≡ Cordyceps fracta Mains, Bull. Torrey Bot. Club 84: 250.
197.
2
1
Elaphocordyceps inegoënsis (Kobayasi) G.H.
Sung, J.M. Sung & Spatafora, comb. nov. MycoBank
MB0419.
Elaphocordyceps ophioglossoides f. cuboides
(Kobayasi) G.H. Sung, J.M. Sung & Spatafora, comb.
nov. MycoBank MB0420.
≡ Cordyceps ophioglossoides f. cuboides Kobayasi, Bull.
Natn. Sci. Mus. Tokyo 5: 77. 1960.
≡ Cordyceps inegoënsis Kobayasi, Bull. Natn. Sci. Mus.
Tokyo 6: 292. 1963.
1
2
Elaphocordyceps intermedia (S. Imai) G.H. Sung,
J.M. Sung & Spatafora, comb. nov. MycoBank
MB0419.
Elaphocordyceps paradoxa (Kobayasi) G.H. Sung,
J.M. Sung & Spatafora, comb. nov. MycoBank
MB0420.
≡ Cordyceps paradoxa Kobayasi, Bull. Biogeogr. Soc. Japan
9: 1. 1939.
≡ Cordyceps intermedia S. Imai, Proc. Imp. Acad. Tokyo 10:
77. 1934.
Elaphocordyceps ramosa (Teng) G.H. Sung, J.M.
Sung & Spatafora, comb. nov. MycoBank MB04207.
2
2
Elaphocordyceps intermedia f. michinokuënsis
(Kobayasi & Shimizu) G.H. Sung, J.M. Sung &
Spatafora, comb. nov. MycoBank MB04197.
≡ Cordyceps intermedia f. michinokuënsis Kobayasi &
Shimizu, Bull. Natn. Sci. Mus. Tokyo, Ser. B, 8: 116. 1982.
≡ Cordyceps ramosa Teng, Sinensia 7: 810. 1936.
2
Elaphocordyceps rouxii (Cand.) G.H. Sung, J.M.
Sung & Spatafora, comb. nov. MycoBank MB04208.
≡ Cordyceps rouxii Cand., Mycotaxon 4: 44. 197.
1
Elaphocordyceps japonica (Lloyd) G.H. Sung, J.M.
Sung & Spatafora, comb. nov. MycoBank MB04198.
≡ Cordyceps japonica Lloyd, Mycol. Writ. : 913. 1920.
= Cordyceps umemurae S. Imai, Trans. Sapporo Nat. Hist. Soc.
11: 32. 1929 (as C. ‘umemurai’) .
Elaphocordyceps subsessilis (Petch) G.H. Sung,
J.M. Sung & Spatafora, comb. nov. MycoBank
MB04209.
1
37
SuNG ET AL.
≡ Cordyceps subsessilis Petch, Trans. Brit. Mycol. Soc. 21:
39. 1937.
= Cordyceps facis Kobayasi & Shimizu, Trans. Mycol. Soc. Japan
23: 31. 1982.
Anamorph: Tolypocladium inlatum W. Gams
2
Elaphocordyceps szemaoënsis (M. Zang) G.H.
Sung, J.M. Sung & Spatafora, comb. nov. MycoBank
MB04210.
≡ Cordyceps szemaoënsis M. Zang, Acta Bot. Yunnanica 23:
29. 2001.
2
Elaphocordyceps tenuispora (Mains) G.H. Sung,
J.M. Sung & Spatafora, comb. nov. MycoBank
MB04211.
≡ Cordyceps tenuispora Mains, Bull. Torrey Bot. Club 84:
247. 197.
2
Elaphocordyceps toriharamontana (Kobayasi) G.H.
Sung, J.M. Sung & Spatafora, comb. nov. MycoBank
MB04212.
≡ Cordyceps toriharamontana Kobayasi, Bull. Natn. Sci.
Mus. Tokyo 6: 305. 1963.
2
Elaphocordyceps valliformis (Mains) G.H. Sung,
J.M. Sung & Spatafora, comb. nov. MycoBank
MB04213.
≡ Cordyceps valliformis Mains, Bull. Torrey Bot. Club 84:
20. 197.
2
Elaphocordyceps valvatistipitata (Kobayasi) G.H.
Sung, J.M. Sung & Spatafora, comb. nov. MycoBank
MB04214.
≡ Cordyceps valvatistipitata Kobayasi, Bull. Natn. Sci. Mus.
Tokyo 5: 81. 1960 (as C. volvatostipitata’).
2
Elaphocordyceps virens (Kobayasi) G.H. Sung, J.M.
Sung & Spatafora, comb. nov. MycoBank MB0421
≡ Cordyceps virens Kobayasi, J. Jap. Bot. 8: 222. 1983.
OPhiOCOrdyCEPs Petch, Trans. Brit. Mycol.
Soc. 1: 73. 1931 emend. G.H. Sung, J.M. Sung,
Hywel-Jones & Spatafora
= Cordycepioideus Stiler, Mycologia 33: 83. 1941.
Stromata or subiculum darkly pigmented or rarely
brightly coloured, tough, ibrous, pliant to wiry, rarely
leshy, often with aperithecial apices or lateral pads.
Perithecia supericial to completely immersed, ordinal
or oblique in arrangement. Asci hyaline, cylindrical,
usually with thickened ascus apex, rarely fusoid to
ellipsoid. Ascospores usually cylindrical, multiseptate,
disarticulating into part-spores or non-disarticulating.
Type: Cordyceps blattae Petch, Trans. Brit. Mycol. Soc.
1: 74. 1931.
Anamorphic
genera:
Hirsutella,
Paraisaria, Syngliocladium.
Ophiocordyceps communis Hywel-Jones & Samson,
sp. nov. MycoBank MB0421. Figs 12A–G.
Anamorph: hirsutella/hymenostilbe-like.
Stromata ex duabus (tribus) termitis adultis oriunda, mycelio albo
circumdata, iliformia; 50–100 mm sub supericie stramenti oriunda,
300–600 μm lata, albido-grisea, 70–130 mm super stramentum
emergentia, 600–1000 μm lata, cuius 30–40 mm pars inferior hyphis
sterilibus dematiaceis (luteo-brunneis) tomentosa; pars superior, ca
90 mm longa, fertilis, levis, griseo-brunnea vel grisea, conidia in strato
griseo ferens et perithecia dense aggregata. Perithecia supericialia,
subterminalia, 285–675 × 195–390 μm. Asci apice conspicue
inspissato, 8-spori, iliformes, 215–250 × 15 μm. Ascosporae integrae,
crassitunicatae, dilute pigmentatae, (100–)120–150(–180) × 5–6 μm.
Cellulae conidiogenae hymenium hyalinum formantes, cylindricae,
10–14 × 2.7–3.3 μm, unum (raro duos) denticulos fertiles apicales
ferentes. Blastoconidia hyalina, amygdaliformia, 8–9 × 2.5–3 μm.
Anamorphe Hirsutellae vel Hymenostilbe similis.
Hymenostilbe,
Commentary: The C. unilateralis clade is strongly
supported (MP-BP = 88 %, ML-BP = 88 %, PP = 1.00 in
Figs 3, 10) and includes the species of Ophiocordyceps
(e.g., C. acicularis and C. unilateralis) (Petch 1931,
1933). The genus Ophiocordyceps was proposed
38
by Petch (1931, 1933) for species of Cordyceps
that produce non-disarticulating ascospores. The
genus was not accepted by subsequent workers
who reclassiied the species of Ophiocordyceps as
Cordyceps subg. Ophiocordyceps (Kobayasi 1941)
or in multiple subgenera of Cordyceps (Mains 198).
The type of Ophiocordyceps Petch is O. blattae (=
C. blattae), but it was not available for this taxonomic
treatment. According to the morphological description,
it its in the present generic concept. Because O.
unilateralis is a well-known species that was included
in the original publication of Ophiocordyceps (Petch
1931) and because additional Ophiocordyceps species
(e.g., O. acicularis) are members of this clade, we apply
the name Ophiocordyceps based on the placement of
O. unilateralis. The genus Ophiocordyceps includes
the most morphologically diverse group of the species
of Cordyceps s. l. including the members of C. subg.
Neocordyceps (Figs , 10). For most of the species in
Ophiocordyceps, the stromata are ibrous to tough or
wiry to pliant in texture and darkly pigmented in at least
some part of the stroma. The genus includes many
species of Cordyceps s. l. that produce perithecia
in subterminal regions of the stromata resulting in
aperithecial apices. Of particular note, Ophiocordyceps
is characterized by the dominant occurrence of
Hirsutella and Hymenostilbe anamorphs (Fig. ).
Although the genus Cordycepioideus possesses thickwalled multiseptate ellipsoid ascospores and its asci
lack the thickened ascus tip of most clavicipitaceous
fungi (Blackwell & Gilbertson 1984, Ochiel et al. 1997),
this study indicates that the genus Cordycepioideus
can be merged with Ophiocordyceps according to its
placement in molecular analyses and because of the
Hirsutella anamorph (Fig. 10, Ochiel et al. 1997, Suh
et al. 1998).
Hosts two (rarely three) adult termites surrounded by
loose, coarse white mycelium. Stromata iliform, 50–100
mm below ground, 300–00 µm wide, whitish-grey;
70–130 mm emerging above leaf litter, 00–1000 µm
wide; lower 30–40 mm of above-ground portion usually
hirsute with sterile, dematiaceous (yellow-brown) hairs
becoming smooth, silver-brown to grey along terminal
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
fertile (anamorph) part of ca 90 mm. Perithecia supericial
subterminal; emerging through grey anamorph, tightly
packed around the stipe, 28–7 × 19–390 µm. Asci
with stout cap, 8-spored, iliform, 215–250 × 15 µm.
Ascospores whole, stout, lightly pigmented (100–)120–
10(–180) × – µm. Conidiogenous cells in a palisade,
hyaline, cylindrical, 10–14 × 2.7–3.3 µm, solitary (rarely
two), prominent, terminal denticle. Conidia hyaline,
almond-shaped, 7–9 × 2.–3 µm.
Etymology: refers to the communal nature of the stromata,
i.e. the fact that 00–1000 Cordyceps stromata can be
found in a small area (20 × 20 metres).
Type: Holotype: N.H.J. 1073, isotypes: N.H.J. 1074,
N.H.J. 107, N.H.J. 107, N.H.J. 1077, all on
termites; coll. R. Nasit; Khao Yai National Park, Gong
Giao Nature Trail; 13 June 2000.
Commentary: Most collections of O. communis were
from Khao Yai National Park with the type locality (Gong
Giao Nature Trail) regularly having epizootics containing
(in any one season) several hundred stromata over a
20 × 20 metre area. A few other collections were from
Khao Soi Dao Wildlife Sanctuary (N.H.J. 422 and
N.H.J. 6452) and Sam Lan National Park (N.H.J. 6332).
All collections of the species were from adult termites.
Although surveys were made over an eighteen-year
period from the far north of Thailand to the far south
and from sea level to over 200 metres, O. communis
is only known from these three sites in central Thailand
below 800 metres elevation.
In any year there appeared to be a single ‘lush’
with O. communis irst appearing at the start of the
rainy season in May/June. The earliest collections
were made in May (10 May 1994: N.H.J. 387, N.H.J.
381 and N.H.J. 383, Heo Sawat Waterfall; 23 May
1996; N.H.J. 6330, Gong Giao Nature Trail). In the irst
2–3 weeks after appearance, the stromata appeared
slender and acicular with the lower part having a shiny
silken appearance and the terminal part dull greyish.
The terminal grey region consisted of a palisade of
tightly packed conidiogenous cells with typically a stout
elongate denticle, giving rise to a single conidium.
This anamorph is intermediate between a typical
Hirsutella (e.g., Hi. formicarum, Hi. citriformis, and
Hi. saussurei) and a typical Hymenostilbe (e.g., Hy.
dipterigena – closer to the latter) (Figs 12F–G). The
palisade of crowded conidiogenous cells is indicative
of Hymenostilbe rather than Hirsutella, where
conidiogenous cells are sparse and mostly immature at
any given time (Fig. 12F). The denticulate nature of the
conidiogenous cell also is indicative of Hymenostilbe.
However, in all specimens examined to date there is
no evidence of multiple denticles (ive or more) usually
associated with Hymenostilbe; only a few conidiogenous
cells were seen with two denticles (Figs 12F–G).
The anamorph of O. communis is closest to Hy.
ventricosa Hywel-Jones (Hywel-Jones 1995). That
species infects cockroaches and is found attached to
the under side of leaves. As with the anamorph of O.
communis, Hy. ventricosa produces conidiogenous
cells with only a single terminal stout denticle. Conidia
of Hy. ventricosa have a pronounced point and are
not typical of the clavate shape usually associated
with Hymenostilbe. Similarly, the conidia of the O.
communis anamorph are also fattened naviculate,
appearing similar to those of Hy. ventricosa but without
the processed tip.
The perithecia erupt through the dull greyish
anamorph spike appearing irst as longitudinal splits
in the palisade of conidiogenous cells at the base of
the anamorph spike. Each develops as a supericial
perithecium, but they become crowded and give the
overall appearance of a brown subterminal fertile region
(Kobayasi 1941; Figs 12A–B). The ascus shape and the
form of the ascus cap comes close to Kobayasi’s Figs
12C–D (Kobayasi 1941) being typical of species in the
C. unilateralis clade (with Hirsutella as an anamorph).
Mature perithecia eject pigmented, whole ascospores
(Fig. 12E) and often the ostiole becomes blocked with
these half-emerged ascospores.
Only a few species of Cordyceps sensu Kobayasi
and Mains have been reported from termites. Currently
accepted species include O. koningsbergeri (= C.
koningsbergeri Penz. & Sacc.), which is known only
from the type locality (Java, Indonesia) (Kobayasi
1941), and C. termitophila Kobayasi & Shimizu) which
is known from Japan and Taiwan (Kobayasi & Shimizu
1976, 1978). Penzig & Saccardo (1904) found O.
koningsbergeri to be similar to O. myrmecophila in
that it had a terminal, globose head with immersed
perithecia. In this feature alone it differs signiicantly
from O. communis with its subterminal and supericial
perithecia. However, as with O. communis, Penzig &
Saccardo (1904) described whole ascospores of O.
koningsbergeri, which were 10 × 1 µm compared
with 120–10 × – µm for O. communis. Cordyceps
termitophila differs from O. communis in having a ‘pale
rosy-grey’ stroma, much smaller perithecia (280–320
× 17–190 µm for C. termitophila versus 28–7 ×
19–390 µm for O. communis) and smaller ascospores
(100–12 × 3 µm).
Accepted names and new combinations
for Ophiocordyceps
The following taxa are accepted species of
Ophiocordyceps based on their inclusion in molecular
phylogenies presented herein1 or morphological
descriptions matching the characters described above2.
Where known, the anamorph connection is provided for
the species of Ophiocordyceps.
Ophiocordyceps acicularis (Ravenel) Petch, Trans.
Brit. Mycol. Soc. 18: 0. 1933.
1
≡ Cordyceps acicularis Ravenel, J. Linn. Soc. 1: 18. 187.
= Cordyceps caroliniensis Berk. & Ravenel, Fungi Carolina 4:
29. 18.
Anamorph: Hirsutella
1
Ophiocordyceps agriotidis (A. Kawam.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04217.
39
SuNG ET AL.
≡ Cordyceps agriotidis A. Kawam., Icon. Jap. Fungi 8: 837.
19. [as C. ‘agriota’]
≡ Cordyceps unilateralis var. australis Speg., Anales Soc. Ci.
Argent. 12: 21. 1881.
≡ Cordyceps australis (Speg.) Speg., Syll. Fung. 2: 71.
1883.
Anamorph: Hirsutella
2
Ophiocordyceps ainictos (A. Möller) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04218.
≡ Cordyceps ainictos A.
Ascomyceten, p. 22. 1901.
Möller,
Phycomyceten
u.
Ophiocordyceps barnesii (Thwaites) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04230.
2
≡ Cordyceps barnesii Thwaites, J. Linn. Soc. 14: 110. 1875.
≡ Torrubia barnesii (Thwaites) Ces., Atti Accad. Sci. Fis.
Mat., Napoli 8: 14. 1879.
Anamorph: Hirsutella
2
Ophiocordyceps amazonica (Henn.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04219.
≡ Cordyceps amazonica Henn., Hedwigia 43: 247. 1904.
2
Ophiocordyceps amazonica var. neoamazonica
(Kobayasi & Hara) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora, comb. nov. MycoBank MB04220.
≡ Cordyceps amazonica var. neoamazonica Kobayasi & Hara, J.
Jap. Bot. 57: 17. 1982.
1
Ophiocordyceps aphodii (Mathieson) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04221.
2
Ophiocordyceps bicephala (Berk.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04231.
≡ Cordyceps bicephala Berk., J. Bot. (Hooker) 8: 278. 18.
Ophiocordyceps bispora (Stiler) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB04232.
2
≡ Cordycepioideus bisporus Stiler, Mycologia 33: 85. 1941.
Anamorph: Hirsutella
Ophiocordyceps blattae (Petch) Petch, Trans. Brit.
Mycol. Soc. 1: 74. 1931.
2
≡ Cordyceps blattae Petch, Trans. Brit. Mycol. Soc. 10: 35.
1924.
≡ Cordyceps aphodii Mathieson, Trans. Brit. Mycol. Soc. 32:
134. 1949.
Anamorph: Hirsutella
2
Ophiocordyceps appendiculata (Kobayasi &
Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04222.
1
Ophiocordyceps brunneipunctata (Hywel-Jones)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04233.
≡ Cordyceps brunneipunctata Hywel-Jones, Mycol. Res. 99:
119. 199. [as C. ‘brunneapunctata’]
≡ Cordyceps appendiculata Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 9: 6. 1983.
Anamorph: Hirsutella
2
2
Ophiocordyceps arachneicola (Kobayasi) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04223.
Ophiocordyceps caloceroides (Berk. & M.A. Curtis)
Petch, Trans. Brit. Mycol. Soc. 18: 63. 1933.
≡ Cordyceps caloceroides Berk. & M.A. Curtis, J. Linn. Soc.
10: 37. 188.
= Cordyceps wittii Henn., Bot. Jahrb. Syst. 23: 39. 1897.
≡ Cordyceps arachneicola Kobayasi, Sci. Rep. Tokyo Bunrika
Daigaku, Sect. B, : 123. 1941.
Ophiocordyceps arbuscula (Teng) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0422
2
2
Ophiocordyceps cantharelloides (Samson &
H.C. Evans) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04234.
≡ Cordyceps cantharelloides Samson & H.C. Evans, Proc.
Indian Acad. Sci., Pl. Sci. 94: 312. 1985.
≡ Cordyceps arbuscula Teng, Sinensia 7: 812. 1936.
2
Ophiocordyceps armeniaca (Berk. & M.A. Curtis)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB0422.
≡ Cordyceps armeniaca Berk. & M.A. Curtis, J. Linn. Soc. 1:
18. 187.
2
Ophiocordyceps asyuënsis (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04227.
≡ Cordyceps asyuënsis Kobayasi & Shimizu, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 6: 138. 1980.
2
Ophiocordyceps carabidicola (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB0423.
≡ Cordyceps carabidicola Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 85. 1980. [as C. ‘carabidiicola’]
Ophiocordyceps cicadicola (Teng) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0423.
2
≡ Cordyceps cicadicola Teng, Sinensia 6: 191. 1935.
2
2
Ophiocordyceps aurantia (Kobayasi & Shimizu) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04228.
Ophiocordyceps clavata (Kobayasi & Shimizu) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04237.
≡ Cordyceps clavata Kobayasi & Shimizu, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 6: 140. 1980.
≡ Cordyceps aurantia Kobayasi & Shimizu, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 6: 125. 1980.
Ophiocordyceps clavulata (Schwein.) Petch, Trans.
Brit. Mycol. Soc. 18: 3. 1933.
2
2
Ophiocordyceps australis (Speg.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04229.
40
≡ Sphaeria clavulata Schwein., Trans. Amer. Philos. Soc.
New Ser. 4, 188. 1832.
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
≡ Xylaria clavulata (Schwein.) Berk. & M. A. Curtis, J. Linn.
Soc. 10: 380. 188.
≡ Torrubia clavulata (Schwein.) Peck, Ann. Rep. N. Y. State
Mus. 28: 70. 187.
≡ Cordyceps clavulata (Schwein.) Ellis & Everh., North Amer.
Pyrenom. p. 61. 1892.
= Cordyceps pistillariiformis Berk. & Broome, Ann. Mag. Nat.
Hist. Ser. 3, 7: 41. 181 [as C. ‘pistillariaeformis’].
≡ Torrubia pistillariiformis (Berk. & Broome) Cooke, Handb.
Brit. Fungi 2: 771. 1871.
Anamorph: Hymenostilbe lecaniicola (Jaap) Mains
2
Ophiocordyceps crassispora (M. Zang, D.R. Yang
& C.D. Li) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04242.
≡ Cordyceps crassispora M. Zang, D.R. Yang & C.D. Li,
Mycotaxon 37: 8. 1990.
2
Ophiocordyceps crinalis (Ellis ex Lloyd) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04243.
≡ Cordyceps crinalis Ellis ex Lloyd, Mycol. Writ. : 912.
1920.
1
Ophiocordyceps coccidiicola (Kobayasi) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04238.
≡ Cordyceps coccidiicola Kobayasi, Bull. Natn. Sci. Mus.
Tokyo, Ser. B, 4: 57. 1978.
2
Ophiocordyceps cucumispora (H.C. Evans &
Samson) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04244.
≡ Cordyceps cucumispora H.C. Evans & Samson, Trans. Brit.
Mycol. Soc. 79: 442. 1982.
Ophiocordyceps coccigena (Tul. & C. Tul.) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04239.
2
≡ Torrubia coccigena Tul. & C. Tul., Sel. Fung. Carpol. 3:
19. 18.
≡ Cordyceps coccigena (Tul. & C. Tul.) Sacc., Michelia 1:
320. 1879.
Anamorph: Hirsutella ovalispora H.C. Evans &
Samson
2
Ophiocordyceps cucumispora var. dolichoderi
(H.C. Evans & Samson) G.H. Sung, J.M. Sung,
Hywel-Jones & Spatafora, comb. nov. MycoBank
MB0424.
≡ Cordyceps cucumispora var. dolichoderi H.C. Evans &
Samson, Trans. Brit. Mycol. Soc. 79: 445. 1982.
2
Ophiocordyceps cochlidiicola (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04240.
≡ Cordyceps cochlidiicola Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 128. 1980.
Anamorph: Hirsutella ovalispora var. dolichoderi
H.C. Evans & Samson
Ophiocordyceps curculionum (Tul. & C. Tul.) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB0424.
2
1
Ophiocordyceps communis Hywel-Jones & Samson,
sp. nov., see above.
Anamorph: hirsutella/hymenostilbe-like
2
Ophiocordyceps corallomyces (A. Möller) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04241.
≡ Cordyceps corallomyces A. Möller, Phycomyceten u.
Ascomyceten, p. 217. 1901.
≡ Torrubia curculionum Tul. & C. Tul., Sel. Fung. Carpol. 3:
20. 18.
≡ Cordyceps curculionum (Tul. & C. Tul.) Sacc., Michelia 1:
320. 1879.
≡ Cordyceps bicephala subsp. curculionum (Tul. & C. Tul.)
Moureau, Mém. Inst. Roy. Colon. Belge 7: 0. 1949.
Anamorph: Hymenostilbe
Fig. 12. A–G. Morphology of Ophiocordyceps communis. A. Stromata, bar = 10 mm. B. Arrangement of perithecia. C. Ascus with ascospores.
D. Ascus and ascus apex. E. Non-disarticulating ascospores. F. Conidiophores (Hymenostilbe/Hirsutella anamorph). G. Denticles of phialide
(Hymenostilbe/Hirsutella anamorph). Scale bars: A, C–G = 10 µm, B = 00 µm.
41
SuNG ET AL.
2
Ophiocordyceps cylindrostromata (Z.Q. Liang, A.Y.
Liu & M.H. Liu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04247.
≡ Cordyceps cylindrostromata Z.Q. Liang, A.Y. Liu & M.H.
Liu, Fungal Diversity 14: 97. 2003.
2
Ophiocordyceps elongatiperitheciata (Kobayasi
& Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB0427.
≡ Cordyceps elongatiperitheciata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 6: 126. 1980 (as C.
‘elongatoperitheciata’).
2
Ophiocordyceps dayiensis (Z.Q. Liang) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04248
≡ Cordyceps dayiensis Z.Q. Liang, Fungal Diversity 12: 131.
2003.
2
Ophiocordyceps
elongatistromata
(Kobayasi
& Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB0428.
≡ Cordyceps elongatistromata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 9: 12. 1983 (as C.
‘elongatostromata’).
2
Ophiocordyceps dermapterigena (Z.Q. Liang, A.Y.
Liu & M.H. Liu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04249.
≡ Cordyceps dermapterigena Z.Q. Liang, A.Y. Liu & M.H. Liu,
Fungal Diversity 14: 9. 2003 (as C. ‘dermapteoigena’).
2
Ophiocordyceps emeiensis (A.Y. Liu & Z.Q. Liang)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB0429.
≡ Cordyceps emeiensis A.Y. Liu & Z.Q. Liang, Mycosystema
1: 139. 1997.
2
Ophiocordyceps dipterigena (Berk. & Broome) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB0420.
≡ Cordyceps dipterigena Berk. & Broome, J. Linn. Soc. 14:
111. 187.
= Cordyceps muscicola A. Möller, Phycomyceten u. Ascomyceten,
p. 221. 1901.
= Cordyceps surinamensis Henn., Hedwigia 41: 19 1902.
= Cordyceps oumensis Höhn., Sitzungsber. Kaiserl. Akad. Wiss.
Wien 118: 309. 1909.
= Cordyceps ouwensii Höhn., Sitzungsber. Kaiserl. Akad. Wiss.
Wien 118: 309. 1909.
= Cordyceps thwaitesii Lloyd, Mycol. Writ. : 100. 1921.
= Cordyceps opposita Syd., Bot. Jahrb. Syst. 7: 32. 1922.
2
Ophiocordyceps engleriana (Henn.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0420.
≡ Cordyceps engleriana Henn., Bot. Jahrb. Syst. 23: 38.
1897.
Anamorph: Hymenostilbe
1
Ophiocordyceps entomorrhiza (Dicks.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0421.
≡ Sphaeria entomorrhiza Dicks., Plant. Crypt. Brit., Fasc. 1:
22. 178.
≡ Cordyceps entomorrhiza (Dicks.) Fr., Obs. Mycol. 2: 317.
1818.
≡ Torrubia entomorrhiza (Dicks.) Tul. & C. Tul, Sel. Fung.
Carpol. 3: 13. 18.
= Torrubia cinerea Tul. & C. Tul., Sel. Fung. Carpol. 3: 14. 1865.
≡ Cordyceps cinerea (Tul. & C. Tul.) Sacc., Michelia 1: 320.
1879.
= Cordyceps carabi Quél., Comp. Rend. Assoc. Franç. Avancem.
Sci. 2: 42. 1898.
Anamorph: Hymenostilbe dipterigena Petch
2
Ophiocordyceps
discoideicapitata
(Kobayasi
& Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB0421.
≡ Cordyceps discoideicapitata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 8: 85. 1982 (as C.
‘discoideocapitata’).
Anamorph: Hirsutella eleutheratorum (Nees) Petch
2
Ophiocordyceps ditmarii (Quél.) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB0422.
≡ Cordyceps ditmarii Quél., Bull. Soc. Bot. France 24: 330
1877. [as C. ditmari]
Anamorph: Hymenostilbe
2
Ophiocordyceps evdogeorgiae (Koval) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0422.
≡ Cordyceps evdogeorgiae Koval, Bot. Mater. Otd. Sporov.
Rast. 14: 10. 191.
2
Ophiocordyceps dovei (Rodway) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB0423.
≡ Cordyceps dovei Rodway, Paper Proc. Roy. Soc. Tasmania
for 1898–1899, p. 101. 1900.
= Cordyceps aemonae Lloyd, Mycol. Notes 2: 932. 1920.
2
Ophiocordyceps falcata (Berk.) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB0423.
≡ Cordyceps falcata Berk., J. Bot. (Hooker) : 211. 184
[Decad. Fung. No. 479].
Anamorph: hirsutella-like
2
Ophiocordyceps elateridicola (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB042.
≡ Cordyceps elateridicola Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 9: 4. 1983.
Ophiocordyceps elongata (Petch) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB042.
2
≡ Cordyceps elongata Petch, Trans. Brit. Mycol. Soc. 21: 47.
1937.
Anamorph: Hirsutella
42
Anamorph: Stilbella
2
Ophiocordyceps falcatoides (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB0424.
≡ Cordyceps falcatoides Kobayasi & Shimizu, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 6: 91. 1980.
2
Ophiocordyceps fasciculatistromata (Kobayasi &
Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank MB042.
≡ Cordyceps fasciculatistromata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 8: 83. 1982 (as C.
‘fasciculatostromata’).
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
2
Ophiocordyceps ferruginosa (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB042.
≡ Cordyceps ferruginosa Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 139. 1980.
Ophiocordyceps iliformis (Moureau) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0427.
2
Daigaku, Sect. B, : 140. 1941.
Anamorph: paecilomyces-like
1
Ophiocordyceps gracilis (Grev.) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB04277.
≡ Xylaria gracilis Grev., Scot. Crypt. Fl. 2. t. 8. 1824.
≡ Cordyceps gracilis (Grev.) Durieu & Mont., Fl. Algérie Crypt.
1: 449. 184.
= Cordyceps mawleyi Westwood, Gard. Chron. Ser. 3, 9: 3.
1891.
≡ Cordyceps iliformis Moureau, Mém. Inst. Roy. Colon.
Belge 7: 14. 1949.
Anamorph: Paraisaria dubia (Delacr.) Samson &
B.L. Brady
2
Ophiocordyceps formicarum (Kobayasi) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0428
≡ Cordyceps formicarum Kobayasi, Bull. Biogeogr. Soc.
Japan 9: 28. 1939.
Ophiocordyceps gryllotalpae Petch, Trans. Brit.
Mycol. Soc. 2: 2. 1941.
2
≡ Cordyceps gryllotalpae Kobayasi, Sci. Rep. Tokyo Bunrika
Daigaku : 70. 1942 [non Lloyd 1924].
≡ Cordyceps koreana Kobayasi, Bull. Natn. Sci. Mus. Tokyo,
Ser. B, 7: 8. 1981.
Anamorph: Hymenostilbe
2
Ophiocordyceps forquignonii (Quél.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0429.
≡ Cordyceps forquignonii Quél., 1th Suppl. Champ. Jura et
vosges, p. . 1887.
1
Ophiocordyceps heteropoda (Kobayasi) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04278.
≡ Cordyceps heteropoda Kobayasi, Bull. Biogeogr. Soc.
Japan 9: 18. 1939.
Anamorph: Hymenostilbe muscarium Petch
2
Ophiocordyceps furcicaudata (Z.Q. Liang, A.Y. Liu
& M.H. Liu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04270.
≡ Cordyceps furcicaudata Z.Q. Liang, A.Y. Liu & M.H. Liu,
Fungal Diversity 14: 9. 2003 (as C. ‘furcicaodata’).
2
Ophiocordyceps gansuënsis (K. Zhang, C. Wang
& M. Yan) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04271.
≡ Cordyceps gansuënsis K. Zhang, C. Wang & M. Yan,
Trans. Mycol. Soc. Japan 30: 295. 1989.
2
Ophiocordyceps hiugensis (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04279.
≡ Cordyceps hiugensis Kobayasi & Shimizu, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 9: 3. 1983.
2
Ophiocordyceps huberiana (Henn.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04280.
≡ Cordyceps huberiana Henn., Hedwigia 48: 10. 1909.
Ophiocordyceps humbertii (C.P. Robin) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04281.
2
2
Ophiocordyceps geniculata (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04272.
≡ Cordyceps humbertii C.P. Robin, in Tul. & C. Tul., Sel.
Fung. Carpol. 3: 18. 18 (as C. ‘humberti’).
≡ Cordyceps geniculata Kobayasi & Shimizu, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 6: 85. 1980.
Anamorph: Hirsutella saussurei (Cooke) Speare
2
Ophiocordyceps gentilis (Ces.) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB04273.
≡ Torrubia gentilis Ces., Atti Accad. Sci. Fis. Mat., Napoli, 8:
14. 1879.
≡ Cordyceps gentilis (Ces.) Sacc., Syll. Fung. 2: 9. 1883.
2
Ophiocordyceps glaziovii (Henn.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04274.
2
Ophiocordyceps insignis (Cooke & Ravenel) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04282.
≡ Cordyceps insignis Cooke & Ravenel, Grevillea 12: 38.
1883.
1
Ophiocordyceps irangiensis (Moureau) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04283.
≡ Cordyceps irangiensis Moureau, Lejeunia, Mém. 1: 33.
191.
≡ Cordyceps glaziovii Henn., Naturw. Wochenschr. : 318.
189.
Anamorph: Hymenostilbe
2
Ophiocordyceps goniophora (Speg.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0427.
≡ Cordyceps goniophora Speg., Bol. Acad. Nac. Ci. Córdoba
11: 307 1889.
2
Ophiocordyceps japonensis (Hara) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04284.
≡ Cordyceps japonensis Hara, Bot. Mag. Tokyo 28: 351.
1914.
2
Ophiocordyceps gracilioides (Kobayasi) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0427.
≡ Cordyceps gracilioides Kobayasi, Sci. Rep. Tokyo Bunrika
2
Ophiocordyceps jiangxiensis (Z.Q. Liang, A.Y. Liu &
Yong C. Jiang) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB0428.
43
SuNG ET AL.
≡ Cordyceps jiangxiensis Z.Q. Liang, A.Y. Liu & Yong C.
Jiang, Mycosystema 20: 30. 2001.
2
Ophiocordyceps jinggangshanensis (Z.Q. Liang,
A.Y. Liu & Yong C. Jiang) G.H. Sung, J.M. Sung,
Hywel-Jones & Spatafora, comb. nov. MycoBank
MB0428.
≡ Cordyceps lachnopoda Penz. & Sacc., Malpighia 11: 521.
1897.
2
Ophiocordyceps larvarum (Westwood) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04397.
≡ Sphaeria larvarum Westwood, Proc. Entomol. Soc. Lond.
2: . 183.
≡ Cordyceps larvarum (Westwood) Olliff, Gaz. New South
Wales : 410. 189.
= Cordyceps huegelii Corda, Icon. Fung. 4: 44. 1840.
≡ Cordyceps jinggangshanensis Z.Q. Liang, A.Y. Liu & Yong
C. Jiang, Mycosystema 20: 307. 2001.
2
Ophiocordyceps kangdingensis (M. Zang & N.
Kinjo) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04287.
≡ Cordyceps kangdingensis M. Zang & N. Kinjo, Mycotaxon
: 221. 1998.
2
Ophiocordyceps lloydii (H.S. Fawc.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0429.
≡ Cordyceps lloydii H.S. Fawc., Ann. Mag. Nat. Hist., Ser. ,
18: 317. 188.
= Cordyceps sheeringii Massee, Ann. Bot. : 10. 1890.
= Cordyceps subdiscoidea Henn., Hedwigia 41: 18. 1902.
Ophiocordyceps kniphoioides (H.C. Evans &
Samson) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04288.
2
≡ Cordyceps kniphoioides H.C. Evans & Samson, Trans.
Brit. Mycol. Soc. 79: 434. 1982.
Anamorph: Hirsutella stilbelliformis H.C. Evans &
Samson
Ophiocordyceps kniphoioides var. dolichoderi
(H.C. Evans & Samson) G.H. Sung, J.M. Sung,
Hywel-Jones & Spatafora, comb. nov. MycoBank
MB04289.
Anamorph: Hymenostilbe formicarum Petch
2
Ophiocordyceps lloydii var. binata (H.C. Evans
& Samson) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04297.
≡ Cordyceps lloydii var. binata H.C. Evans & Samson, Trans.
Brit. Mycol. Soc. 82: 133. 18: 31. 1984.
2
≡ Cordyceps kniphoioides var. dolichoderi H.C. Evans &
Samson, Trans. Brit. Mycol. Soc. 79: 437. 1982.
1
Ophiocordyceps longissima (Kobayasi) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04298.
≡ Cordyceps longissima Kobayasi, Bull. Natn. Sci. Mus.
Tokyo 6: 300. 1963.
Anamorph: Hirsutella stilbelliformis var. dolichoderi
H.C. Evans & Samson
2
Ophiocordyceps kniphoioides var. monacidis (H.C.
Evans & Samson) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora, comb. nov. MycoBank MB04290.
2
Ophiocordyceps lutea (Moureau) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB04299.
≡ Cordyceps lutea Moureau, Mém. Inst. Roy. Colon. Belge
7: 41. 1949.
≡ Cordyceps kniphoioides var. monacidis H.C. Evans &
Samson, Trans. Brit. Mycol. Soc. 79: 439. 1982.
Anamorph: Hymenostilbe sulphurea Samson &
H.C. Evans
Anamorph: Hirsutella stilbelliformis var. monacidis
H.C. Evans & Samson
Ophiocordyceps macularis Mains, Proc. Amer.
Philos. Soc. 74: 269. 1934.
2
Ophiocordyceps kniphoioides var. ponerinarum
(H.C. Evans & Samson) G.H. Sung, J.M. Sung,
Hywel-Jones & Spatafora, comb. nov. MycoBank
MB04291.
2
≡ Cordyceps kniphoioides var. ponerinarum H.C. Evans &
Samson, Trans. Brit. Mycol. Soc. 79: 441. 1982.
Anamorph: Hirsutella stilbelliformis var. ponerinarum
H.C. Evans & Samson
Ophiocordyceps koningsbergeri (Penz. & Sacc.)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04292.
≡ Cordyceps macularis (Mains) Mains, Pap. Michigan Acad.
Sci. 2: 82. 1940.
Ophiocordyceps melolonthae (Tul. & C. Tul.) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04300.
1
≡ Torrubia melolonthae Tul. & C. Tul., Sel. Fung. Carpol. 3:
12. 18.
≡ Cordyceps melolonthae (Tul. & C. Tul.) Sacc., Michelia 1:
320. 1879.
2
≡ Cordyceps koningsbergeri Penz. & Sacc., Malpighia 11:
22. 1897.
2
Ophiocordyceps melolonthae var. rickii (Lloyd)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04301.
≡ Cordyceps rickii Lloyd, Mycol. Writ. : 914. 1920.
≡ Cordyceps melolonthae var. rickii (Lloyd) Mains, Mycologia
0: 198 198.
1
Ophiocordyceps konnoana (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04293.
≡ Cordyceps konnoana Kobayasi & Shimizu, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 6: 84. 1980.
Ophiocordyceps lachnopoda (Penz. & Sacc.) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB0429.
2
44
2
Ophiocordyceps michiganensis (Mains) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04302.
≡ Cordyceps michiganensis Mains, Proc. Amer. Philos. Soc.
74: 2. 1934.
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
2
Ophiocordyceps minutissima (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04303.
MB04313.
≡ Cordyceps nutans Pat., Bull. Soc. Mycol. France 3: 127.
1887.
≡ Cordyceps bicephala subsp. nutans (Pat.) Moureau, Mém.
Inst. Roy. Colon. Belge 7: 47. 1949.
≡ Cordyceps minutissima Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 77. 1980.
Anamorph: Hymenostilbe nutans Samson & H.C.
Evans
2
Ophiocordyceps monticola (Mains) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04304.
≡ Cordyceps monticola Mains, Mycologia 32: 310. 1940.
2
Ophiocordyceps mrciensis (Aung, J.C. Kang,
Z.Q.Liang, Soytong & K.D. Hyde) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB0430.
≡ Cordyceps mrciensis Aung, J.C. Kang, Z.Q.Liang, Soytong
& K.D. Hyde, Mycotaxon 97: 23. 200.
Ophiocordyceps obtusa (Penz. & Sacc.) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04314.
2
≡ Cordyceps obtusa Penz. & Sacc., Malpighia 11: 523.
1897.
2
Ophiocordyceps octospora (M. Blackwell & Gilb.)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB0431.
≡ Cordycepioideus octosporus M. Blackwell & Gilb.,
Mycologia 73: 38. 1981.
2
Ophiocordyceps multiaxialis (M. Zang & Kinjo) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB0430.
≡ Cordyceps multiaxialis M. Zang & Kinjo, Mycotaxon :
224. 1998.
Anamorph: Hirsutella
2
Ophiocordyceps odonatae (Kobayasi) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0431.
≡ Cordyceps odonatae Kobayasi, Bull. Natn. Sci. Mus. Tokyo,
Ser. B, 7: . 1981.
2
Ophiocordyceps myrmecophila (Ces.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04307.
≡ Cordyceps myrmecophila Ces., Bot. Zeitung 4: 877. 184.
≡ Torrubia myrmecophila (Ces.) Tul. & C. Tul., Sel. Fung.
Carpol. 3: 18. 18.
Anamorph: Hymenostilbe
Anamorph: Hymenostilbe odonatae Kobayasi
2
Ophiocordyceps osuzumontana (Kobayasi &
Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04317.
≡ Cordyceps osuzumontana Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 77. 1980.
2
Ophiocordyceps neovolkiana (Kobayasi) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04308.
≡ Cordyceps neovolkiana Kobayasi, Sci. Rep. Tokyo Bunrika
Daigaku, Sect. B, : 19. 1941.
Anamorph: Hirsutella neo-volkiana Kobayasi
2
Ophiocordyceps owariensis (Kobayasi) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04318.
≡ Cordyceps owariensis Kobayasi, Bull. Biogeogr. Soc.
Japan 9: 1. 1939.
2
Ophiocordyceps nepalensis (M. Zang & Kinjo) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04309.
≡ Cordyceps nepalensis M. Zang & Kinjo, Mycotaxon :
224. 1998.
2
Ophiocordyceps
owariensis
f.
viridescens
(uchiyama & udagawa) G.H. Sung, J.M. Sung,
Hywel-Jones & Spatafora, comb. nov. MycoBank
MB04319.
≡ Cordyceps owariensis f. viridescens uchiyama & udagawa,
Mycoscience 43: 13. 2002.
2
Ophiocordyceps nigra (Samson, H.C. Evans &
E.S. Hoekstra) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04310.
≡ Cordyceps nigra Samson, H.C. Evans & E.S. Hoekstra,
Proc. K. Ned. Akad. Wet., Ser. C, Biol. Med. Sci. 85: 596.
1982.
1
Ophiocordyceps nigrella (Kobayasi & Shimizu) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04311.
≡ Cordyceps nigrella Kobayasi & Shimizu, Icon. veg. Wasps
and Plant Worms p. 145. 1983.
≡ Cordyceps nigra Kobayasi & Shimizu, Bull. Natn. Sci. Mus.
Tokyo 9(1): 13. 1983 [non Samson et al. 1982]
2
Ophiocordyceps nigripes (Kobayasi & Shimizu) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04312.
≡ Cordyceps nigripes Kobayasi & Shimizu, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 8: 116. 1982 (as C. ‘nigripoda’).
Ophiocordyceps nutans (Pat.) G.H. Sung, J.M. Sung,
Hywel-Jones & Spatafora, comb. nov. MycoBank
1
Anamorph: Nomuraea owariensis uchiyama &
udagawa
Ophiocordyceps oxycephala (Penz. & Sacc.) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04320.
2
≡ Cordyceps oxycephala Penz. & Sacc., Malpighia 11: 521.
1897.
≡ Cordyceps sphecocephala f. oxycephala (Penz. & Sacc.)
Kobayasi, Trans. Mycol. Soc. Japan 23: 361. 1982.
Anamorph: Hymenostilbe
2
Ophiocordyceps paludosa Mains, Proc. Amer.
Philos. Soc. 74: 269. 1934.
≡ Cordyceps paludosa (Mains) Mains, Pap. Michigan Acad.
Sci. 2: 83. 1940.
Anamorph: Polycephalomyces paludosus Mains
2
Ophiocordyceps pentatomae (Koval) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04321.
4
SuNG ET AL.
≡ Cordyceps pentatomae Koval, Nov. Sist. Niz. Rast. 1: 1.
194. (as C. ‘pentatomi’)
nov. MycoBank MB04331.
≡ Cordyceps rubripunctata Moureau, Mém. Inst. Roy. Colon.
Belge 7: 2. 1949.
Anamorph: Hirsutella
Anamorph: Hirsutella rubripunctata Samson, H.C.
Evans & Hoekstra
2
Ophiocordyceps petchii (Mains) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB04322.
≡ Cordyceps petchii Mains, Bull. Torrey Bot. Club 86: 47.
199.
≡ Cordyceps ramosa Petch, Trans. Brit. Mycol. Soc 21: 42.
1937 [non Teng 1936].
2
Ophiocordyceps rubiginosiperitheciata (Kobayasi
& Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04332.
≡ Cordyceps rubiginosiperitheciata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 9: 14. 1983 (as C.
‘rubiginosoperitheciata’).
2
Ophiocordyceps proliferans (Henn.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04323.
≡ Cordyceps proliferans Henn., Hedwigia 43: 248. 1904.
2
Ophiocordyceps ryogamiensis (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04333.
≡ Cordyceps ryogamiensis Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 9: 4. 1983.
2
Ophiocordyceps pseudolloydii (H.C. Evans &
Samson) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04324.
≡ Cordyceps pseudolloydii H.C. Evans & Samson, Trans.
Brit. Mycol. Soc. 82: 133. 1984.
2
Ophiocordyceps salebrosa (Mains) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04334.
≡ Cordyceps salebrosa Mains, Mycologia 39: 41. 1947.
2
Ophiocordyceps pseudolongissima (Kobayasi
& Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB0432.
≡ Cordyceps pseudolongissima Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 119. 1982.
2
Ophiocordyceps purpureostromata (Kobayasi)
ex G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB0432.
≡ Cordyceps purpureostromata Kobayasi, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 6: 136. 1980. Type Shimizu No. 128,
preserved in TNS; therefore the basionym was valid from the
beginning.
2
Ophiocordyceps scottiana (Olliff) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0433.
≡ Cordyceps scottiana Olliff, Agric. Gaz. New South Wales
: 407. 189.
2
Ophiocordyceps selkirkii (Olliff) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB04338.
≡ Cordyceps selkirkii Olliff, Agric. Gaz. New South Wales :
411. 189.
2
2
Ophiocordyceps purpureostromata f. recurvata
(Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04327.
Ophiocordyceps sichuanensis (Z.Q. Liang & B.
Wang) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04339.
≡ Cordyceps sichuanensis Z.Q. Liang & B. Wang, Fungal
Diversity 12: 129. 2003.
≡ Cordyceps purpureostromata f. recurvata Kobayasi, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 6: 138. 1980.
1
1
Ophiocordyceps ravenelii (Berk. & M.A. Curtis) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04328.
Ophiocordyceps sinensis (Berk.) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB04340.
≡ Sphaeria sinensis Berk., J. Bot. (Hooker) 2: 207. 1843.
≡ Cordyceps sinensis (Berk.) Sacc., Michelia 1: 320. 1879.
≡ Cordyceps ravenelii Berk. & M.A. Curtis, J. Linn. Soc. 1:
19. 187.
Ophiocordyceps rhizoidea (Höhn.) Petch, Trans.
Brit. Mycol. Soc. 1: 74. 1931.
Anamorph: Hirsutella sinensis X.J. Liu, Y.L. Guo,
Y.X. Yu & W. Zeng
1
≡ Cordyceps rhizoidea Höhn., Sitzungsber. Kaiserl. Akad.
Wiss. Wien 118: 307. 1909.
Anamorph: Hirsutella
2
Ophiocordyceps smithii (Mains) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB04341.
≡ Cordyceps smithii Mains, J. Elisha Mitchell Sci. Soc. :
127. 1939.
2
Ophiocordyceps ridleyi (Massee) Kobayasi, Bull.
Biogeogr. Soc. Japan 9: 271. 1939.
≡ Cordyceps ridleyi Massee, Bull. Misc. Inform. Roy. Bot.
Gard. Kew, p. 173. 1899.
1
Ophiocordyceps robertsii (Hook.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04329.
≡ Sphaeria robertsii Hook. Icon. Plant. 1 pl. 6. 1837.
≡ Cordyceps robertsii (Hook.) Berk., Fl. New Zealand 2: 202.
18.
2
Ophiocordyceps rubripunctata (Moureau) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
4
1
Ophiocordyceps sobolifera (Hill ex Watson) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB04342.
≡ Clavaria sobolifera Hill ex Watson, Philos. Trans. Roy. Soc.
Lond. 3: 271. 173.
≡ Sphaeria sobolifera (Hill ex Watson) Berk., J. Bot. (Hooker)
2: 207. 1843.
≡ Torrubia sobolifera (Hill ex Watson) Tul. & C. Tul., Sel.
Fung. Carpol. 3: 10. 18.
≡ Cordyceps sobolifera (Hill ex Watson) Berk. & Broome, J.
Linn. Soc. 14: 110. 187.
Anamorph: Beauveria sobolifera Z.Y. Liu, Z.Q.
Liang, Whalley, A.Y. Liu & Y.J. Yao
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
1
Ophiocordyceps sphecocephala (Klotzsch ex Berk.)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04343.
≡ Sphaeria sphecocephala Klotzsch ex Berk., J. Bot.
(Hooker) 2: 20. 1843.
≡ Torrubia sphecocephala (Klotzsch ex Berk.) Tul. & C. Tul.,
Sel. Fung. Carpol. 3: 18. 18.
≡ Cordyceps sphecocephala (Klotzsch ex Berk.) Berk. &
M.A. Curtis, in Berkeley, J. Linn. Soc., Bot. 10: 37. 188.
MycoBank MB0431.
≡ Cordyceps thyrsoides A. Möller, Phycomyceten u.
Ascomyceten, p. 221. 1901.
1
Ophiocordyceps tricentri (Yasuda) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0432.
≡ Cordyceps tricentri Yasuda, in Lloyd, Mycol. Writ. 4: 8.
191 (as C. ‘tricentrus’).
= Cordyceps aphrophorae Yasuda, Bot. Mag. Tokyo 36: 51.
1922.
Anamorph: Hymenostilbe
2
Ophiocordyceps stipillata (Z.Q. Liang & A.Y. Liu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB04344.
≡ Cordyceps stipillata Z.Q. Liang & A.Y. Liu, Mycosystema
21: 11. 2002.
2
Ophiocordyceps uchiyamae (Kobayasi & Shimizu)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB0433.
≡ Cordyceps uchiyamae Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 125. 1980.
1
Ophiocordyceps stylophora (Berk. & Broome) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB0434.
1
Ophiocordyceps unilateralis (Tul. & C. Tul.) Petch,
Trans. Brit. Mycol. Soc. 16: 74. 1931.
≡ Torrubia unilateralis Tul. & C. Tul., Sel. Fung. Carpol. 3: 18.
18.
≡ Cordyceps unilateralis (Tul. & C. Tul.) Sacc., Syll. Fung.
2: 70. 1883.
= Torrubia formicivora Tul. & C. Tul., Sel. Fung. Carpol. 3: 18.
18.
≡ Cordyceps formicivora (Tul. & C. Tul.) J. Schröt., Krypt.Fl. Schlesien 3(2) 27. 1894.
≡ Cordyceps stylophora Berk. & Broome, J. Linn. Soc. 1:
18. 187.
Anamorph: Hirsutella stylophora Mains
Ophiocordyceps sublavida (Mains) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0434.
2
≡ Cordyceps sublavida Mains, Bull. Torrey Bot. Club 86: 47.
199.
≡ Cordyceps albida Pat. & Gaillard, Bull. Soc. Mycol. France
7: 11. 1888 [non Berk. & M.A. Curtis ex Cooke 1884].
Anamorph: Hirsutella formicarum Petch
2
Ophicordyceps unilateralis var. clavata Kobayasi,
Bull. Biogeogr. Soc. Japan 9: 272. 1939.
≡ Cordyceps unilateralis var. clavata (Kobayasi) Kobayasi,
Sci. Rep. Tokyo Bunrika Daigaku, Sect. B, 5: 78. 1941.
2
Ophiocordyceps subunilateralis (Henn.) Kobayasi,
Bull. Biogeogr. Soc. Japan 9: 271. 1939.
≡ Cordyceps subunilateralis Henn., Hedwigia 41: 18. 1902.
Ophiocordyceps supericialis (Peck) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04347.
1
≡ Torrubia supericialis Peck, Rep. N. Y. State Botanist 28:
70. 187.
≡ Cordyceps supericialis (Peck) Sacc., Syll. Fung. 2: 574.
1883.
Ophiocordyceps supericialis f. crustacea (Kobayasi
& Shimizu) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora, comb. nov. MycoBank MB04348.
2
≡ Cordyceps supericialis f. crustacea Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 6: 82. 1980.
2
Ophiocordyceps takaoënsis (Kobayasi) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB04349.
≡ Cordyceps sobolifera var. takaoënsis Kobayasi, Bull.
Biogeogr. Soc. Japan 9: 1. 1939.
≡ Cordyceps takaoënsis (Kobayasi) Kobayasi, Sci. Rep.
Tokyo Bunrika Daigaku, Sect. B, 5: 130. 1941.
2
Ophiocordyceps taylorii (Berk.) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB0430.
≡ Sphaeria taylorii Berk., J. Bot. (Hooker) 2: 209. 1843 (as
S. ‘taylori’).
≡ Cordyceps taylorii (Berk.) Sacc., Michelia 1: 320. 1879.
2
Ophiocordyceps thyrsoides (A. Möller) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
Ophiocordyceps variabilis (Petch) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB0434.
1
≡ Cordyceps variabilis Petch, Trans. Brit. Mycol. Soc. 21: 42.
1937.
= Cordyceps viperina Mains, Mycologia 29: 74. 1937.
Anamorph: Syngliocladium
2
Ophiocordyceps voeltzkowii (Henn.) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB043.
≡ Cordyceps voeltzkowii Henn., in voeltzkow, Reise Ostafrica
3: 29. 1908.
2
Ophiocordyceps volkiana (A. Möller) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, comb. nov.
MycoBank MB043.
≡ Cordyceps volkiana A.
Ascomyceten, p. 233. 1901.
Möller,
Phycomyceten
u.
Anamorph: Hirsutella
2
Ophiocordyceps wuyishanensis (Z.Q. Liang, A.Y.
Liu & J.Z. Huang) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora, comb. nov. MycoBank MB0437.
≡ Cordyceps wuyishanensis Z.Q. Liang, A.Y. Liu & J.Z.
Huang, Mycosystema 21: 12. 2002.
Anamorph: paecilomyces-like
1
Ophiocordyceps yakusimensis (Kobayasi) G.H.
Sung, J.M. Sung, Hywel-Jones & Spatafora, comb.
nov. MycoBank MB0438.
≡ Cordyceps yakusimensis Kobayasi, Bull. Natn. Sci. Mus.
Tokyo 6: 302. 1963.
47
SuNG ET AL.
2
Ophiocordyceps zhangjiajiensis (Z.Q. Liang & A.Y.
Liu) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB0439.
≡ Cordyceps zhangjiajiensis Z.Q. Liang & A.Y. Liu,
Mycosystema 21: 13. 2002.
Anamorph: Hirsutella zhangjiajiensis Z.Q. Liang &
A.Y. Liu
ClaviCiPitaCEaE Clade C
Clavicipitaceae clade C is a strongly supported group
that includes the type species, C. militaris, of Cordyceps
(MP-BP = 100 %, ML-BP = 100 %, PP = 1.00 in Figs
1–2). Because of the non-monophyly of Cordyceps, we
reintroduce the preexisting family name Cordycipitaceae
for Clavicipitaceae clade C. This family name was not
validly published and it is validated herein based on
the type genus Cordyceps. Most of the species in the
family parasitize hosts in leaf litter, moss, or upper soil
layers and produce supericial to partially immersed to
completely immersed perithecia on a leshy stroma or
subiculum that is pallid or brightly coloured. The family
contains species of Cordyceps and Torrubiella (Figs
5, 7). The unispeciic genus Phytocordyceps is also
recognized as a member of this family and transferred
to Cordyceps (Fig. ). In addition, the recent molecular
study shows that species of the genera Ascopolyporus
A. Möller and Hyperdermium J. White, R. Sullivan, G.
Bills & N. Hywel-Jones 2000 [non Link], both pathogens
of scale insects, are also inferred to be members of the
family (Sullivan et al. 2000, Bischoff et al. 200).
COrdyCiPitaCEaE Kreisel 199 ex G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora, fam. nov.
MycoBank MB0430.
Cordycipitaceae Kreisel, Grundz. Natürl. Syst. Pilze:
112. 199 [nom. inval., Art. 3].
Stromata vel subiculum pallida vel laete colorata, carnosa. Perithecia
supericialia vel omnino immersa, perpendicularia ad supericiem. Asci
cylindrici, apice inspissato. Ascosporae cylindricae, multiseptatae,
maturae diffrangentes vel integrae remanentes.
Stromata or subiculum pallid or brightly pigmented,
leshy. Perithecia supericial to completely immersed,
oriented at right angles to the surface of the stroma.
Asci cylindrical with thickened ascus apex. Ascospores
usually cylindrical, multiseptate, disarticulating into
part-spores or remaining intact at maturity.
Type: Cordyceps Fr.
Teleomorphic genera: Ascopolyporus, Cordyceps,
Hyperdermium, Torrubiella.
Stromata or subiculum pallid or brightly pigmented,
leshy. Perithecia supericial to completely immersed,
ordinal in arrangement. Asci hyaline, cylindrical with
thickened ascus apex. Ascospores hyaline, cylindrical,
multiseptate, disarticulating into part-spores or nondisarticulating, rarely possessing a thread-like structure
connecting the fusiform ends.
Type: Cordyceps militaris (L. : Fr.) Fr., Observ. Mycol.
2(revis.): 317. 1818.
Anamorphic genera: Beauveria, Isaria, Lecanicillium,
mariannaea-like, Microhilum, Simplicillium.
Commentary: Species of Cordyceps s. s. are
characterized by possessing leshy stromata that
are pallid or brightly coloured. Because species
of Torrubiella are interspersed among Cordyceps
species in the basal part of the Cordycipitaceae, its
ultimate application to a monophyletic taxon within
the Cordycipitaceae is not clear, however (Fig. 10).
The genus Torrubiella was erected in 188 by Boudier
with the type species T. aranicida Boud. (Kobayasi &
Shimizu 1982). Our sampling included several species
of Torrubiella that were interspersed amongst species
of Cordycipitaceae, but we could not get hold of T.
aranicida. Thus, Cordyceps s. s. is narrowly applied
to the strongly supported clade (MP-BP = 98 %, MLBP = 98 %, PP = 1.00 in Figs 1–2, 10) that includes
Cordyceps species closely related to C. militaris.
Cordyceps species that are placed outside of the
Cordyceps s. s. node, but within the Cordycipitaceae,
are provisionally retained within Cordyceps s. l.
Torrubiella species that are part of the Cordyceps s.
s. are transferred accordingly. The full extent to which
the names Cordyceps and Torrubiella will ultimately
be applied awaits additional sampling of Torrubiella,
especially that of T. aranicida with the possibility that
Torrubiella will need to be synonymized with Cordyceps.
Although Phytocordyceps is characterized by its
possession of bola-ascospores, it is also synonymized
with Cordyceps because of its phylogenetic placement
(Figs 8, 10).
Accepted names and new combinations
for Cordyceps s. s.
The following taxa are accepted species of Cordyceps
s. s. based on their inclusion in molecular phylogenies
presented herein1 (see Table 1) or morphological
descriptions matching the characters described above2.
Where known we provide the anamorph connection for
the species of Cordyceps s. s.
2
Cordyceps ampullacea Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 112. 1982.
Anamorphic genera: Beauveria, Engyodontium,
Isaria, Lecanicillium, mariannaea-like, Microhilum,
Simplicillium.
2
COrdyCEPs Fr., Observ. Mycol. 2 (revis.): 31.
2
1818 emend. G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora
= Phytocordyceps C.H. Su & H.-H. Wang, Mycotaxon 2: 338.
198.
48
Cordyceps bassiana Z.Z. Li, C.R. Li, B. Huang &
M.Z. Fan, Chinese Science Bulletin 4: 71. 2001.
Anamorph: Beauveria bassiana (Bals.) vuill.
Cordyceps belizensis Mains, Mycologia 32: 21.
1940.
1
Cordyceps bifusispora O.E. Erikss., Mycotaxon 1:
18. 1982.
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Anamorph: Septofusidium bifusisporum Z.Y. Liu,
Z.Q. Liang & A.Y. Liu
Cordyceps brongniartii Shimazu, Trans. Mycol. Soc.
Japan 29: 328. 1988.
Anamorph: Beauveria brongniartii (Sacc.) Petch
2
2
Cordyceps miryensis Henn., Hedwigia 43: 247.
1904.
Cordyceps mitrata Pat., Bull. Soc. Mycol. France 14:
19. 1898.
2
Cordyceps nikkoënsis Kobayasi, Sci. Rep. Tokyo
Bunrika Daigaku, Sect. B, : 134. 1941.
2
2
Cordyceps chichibuënsis Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 6: 87. 1980.
1
Cordyceps coccinea Penz. & Sacc., Malpighia 11:
24. 1897.
2
Cordyceps ninchukispora (C.H. Su & H.H. Wang)
G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora,
comb. nov. MycoBank MB0432.
≡ Phytocordyceps ninchukispora C.H. Su & H.-H. Wang,
Mycotaxon 2: 338. 198.
Cordyceps coccinea var. subochracea Penz. &
Sacc., Malpighia 1: 231. 1901.
2
1
Cordyceps confragosa (Mains) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora, comb. nov. MycoBank
MB0431.
≡ Torrubiella confragosa Mains, Mycologia 41: 30. 1949.
Anamorph: Lecanicillium lecanii (Zimm.) Zare & W.
Gams
Cordyceps erotyli Petch, Trans. Brit. Mycol. Soc. 21:
40. 1937.
2
2
Cordyceps exasperata A.F. vital, Anais Soc. Biol.
Pernambuco 14: 65. 1956.
Cordyceps lavobrunnescens Henn., in Warburg,
Monsunia 1: 14. 1900.
Anamorph: acremonium-like
1
Cordyceps ochraceostromata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 6: 132. 1980.
2
Cordyceps ogurasanensis Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 8: 80. 1982.
2
Cordyceps oncoperae P.J. Wright, J. Invert. Pathol.
1: 211. 1994.
Cordyceps polyarthra A. Möller, Phycomyceten u.
Ascomyceten, p. 213. 1901.
2
= Cordyceps subpolyarthra Henn., Hedwigia 41: 11. 1902.
= Cordyceps concurrens Lloyd, Mycol. Writ. 7: 1180. 1923.
Anamorph: Isaria tenuipes Peck
2
2
Cordyceps formosana Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 7: 113. 1981.
Cordyceps pruinosa Petch, Trans. Brit. Mycol. Soc.
10: 38. 1924.
Anamorph: Mariannaea pruinosa Z.Q. Liang
1
2
2
Cordyceps gryllotalpae Lloyd, Mycol. Writ. : 913.
1920.
Cordyceps rosea Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 8: 112. 1982.
1
2
Cordyceps hepialidicola Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 9: 11. 1983.
Cordyceps roseostromata Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 9: 10. 1983.
1
2
Cordyceps isarioides M.A. Curtis, Ann. Bot. 9: 3.
189.
2
Cordyceps kyusyuënsis A. Kawam., Icon. Jap. Fungi
8: 841. 19.
Anamorph: Sporotrichum formosanum Kobayasi
Cordyceps scarabaeicola Kobayasi, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 2: 137. 1976.
Anamorph: Beauveria
Cordyceps singeri Mains, Bull. Torrey Bot. Club 81:
499. 194.
2
Cordyceps locustiphila Henn., Hedwigia 43: 24.
1904.
Cordyceps spegazzinii M.S. Torres, J.F. White & J.F.
Bisch., Mycotaxon 94: 27. 200.
Anamorph: Evlachovaea
1
1
2
2
Cordyceps militaris (L.: Fr.) Fr., Obs. Mycol. 2: 317.
1818.
≡ Clavaria militaris L., Sp. Plantarum, p. 1182. 1753.
≡ Hypoxylon militare (L.) Mérat, Nouv. Fl. Envir. Paris, p. 137.
1821.
≡ Xylaria militaris (L.) Gray, Nat. Arr. Brit. Pl. (London), p.
10. 1821.
≡ Sphaeria militaris (L. : Fr.) Fr., Syst. Mycol. 2: 32. 1823.
≡ Torrubia militaris (L. : Fr.) Tul. & C. Tul., Sel. Fung. Carpol.
3: . 18.
Cordyceps staphylinidicola Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 8: 88. 1982 [as C.
‘staphylinidaecola’]
Anamorph: Beauveria
1
Cordyceps takaomontana Yakush. & Kumaz., Sci.
Rep. Tokyo Bunrika Daigaku, Sect. B, 5: 108. 1941.
Anamorph: Isaria tenuipes Peck
Anamorph: Lecanicillium
2
Cordyceps tarapotensis Henn., Hedwigia 43: 24.
1904.
49
SuNG ET AL.
2
Cordyceps termitophila Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 4: 56. 1978.
2
Cordyceps truncata Moureau, Mém. Inst. Roy. Colon.
Belge 7: 19. 1949.
1
Cordyceps tuberculata (Lebert) Maire, Bull. Soc.
Hist. Nat. Afrique N. 8: 1. 1917.
other molecular phylogenetic studies, or the assessment
of their morphology and ecology was inconclusive.
These species are provisionally retained within
Cordyceps s. l. until further phylogenetic analyses are
conducted to classify them in a phylogenetic system.
Where known we provide the anamorph connection for
the species of Cordyceps s. l.
≡ Acrophyton tuberculatum Lebert, in Sieb & Köll., Z. Wiss.
Zool. 9: 448. 188.
= Torrubia sphingum Tul. & C. Tul., Sel. Fung. Carpol. 3: 12.
18.
≡ Cordyceps sphingum (Tul. & C. Tul.) Berk. & M.A. Curtis, in
Berkeley, J. Linn. Soc. 10: 37. 188.
Cordyceps adpropinquans (Ces.) Sacc., Syll. Fung. 2:
78. 1883.
Anamorph: Akanthomyces pistillariiformis (Pat.)
Samson & H.C. Evans
Cordyceps aerugineosclerotia Z.Q. Liang & A.Y. Liu,
Mycosystema 1: 3. 1997 [as C. ‘æruginosclerota’].
Cordyceps tuberculata var. tuberculata [var. typica
Kobayasi] f. moelleri (Henn.) Kobayasi, Sci. Rep. Tokyo
Bunrika Daigaku, Sect. B, : 88. 1941.
Cordyceps alba Kobayasi & Shimizu, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 8: 114. 1982.
2
≡ Cordyceps moelleri Henn., Hedwigia 3: 221. 1897.
≡ Torrubia adpropinquans Ces., Atti Accad. Sci. Fis. Mat.,
Napoli 8: 14. 1879.
Cordyceps albida Berk. & M.A. Curtis ex Cooke,
Grevillea 12: 78. 1884.
2
Cordyceps tuberculata var. terminalis Kobayasi [f.
genuina Kobayasi], Sci. Rep. Tokyo Bunrika Daigaku,
Sect. B, : 88. 1941.
2
Cordyceps tuberculata var. terminalis Kobayasi f.
crista (A. Möller) Kobayasi, Sci. Rep. Tokyo Bunrika
Daigaku, Sect. B, : 91. 1941.
≡ Cordyceps crista A. Möller, Phycomyceten u. Ascomyceten,
p. 212. 1901.
Cordyceps albocitrina Koval, Nov. Sist. Niz. Rast. 11:
209. 1974.
Cordyceps alboperitheciata Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 84. 1982.
Cordyceps alpicola Kobayasi, Bull. Natn. Sci. Mus.
Tokyo, Ser. B, 2: 138. 1976.
2
Cordyceps tuberculata var. terminalis Kobayasi f.
cockerellii (Ellis & Everh.) Kobayasi, Sci. Rep. Tokyo
Bunrika Daigaku, Sect. B, : 90. 1941.
≡ Ophionectria cockerellii Ellis & Everh., in Cockerell, J. Inst.
Jamaica 1: 141. 1892.
≡ Cordyceps cockerellii (Ellis & Everh.) Ellis, in Seaver, North
Am. Flora 3: 2. 1910.
2
Cordyceps typhuliformis Berk. & Cooke, in Cooke,
Grevillea 12: 78. 1884 (as C. ‘typhulaeformis’).
2
Cordyceps washingtonensis Mains, Mycologia 39:
3. 1947.
Clavicipitaceae incertae sedis
The following teleomorph genera could not be
conidently assigned in the new classiication because
they were either not sampled as part of this study, were
not sampled as part of other molecular phylogenetic
studies, or the assessment of their morphology and
ecology was inconclusive: Berkelella (Sacc.) Sacc.,
Cavimalum Yoshim. Doi, Dargan & K.S. Thind, Dussiella
Pat., Epicrea Petr., Helminthascus Tranzschel, Konradia
Racib., Moelleriella Bres., Mycomalus A. Möller,
Neobarya Lowen, Neocordyceps Kobayasi, Podocrella
Seaver, Romanoa Thirum., Sphaerocordyceps
Kobayasi, and Stereocrea Syd. & P. Syd.
Residual species of Cordyceps
The following species of Cordyceps s. l. could not be
conidently assigned in the new classiication because
they were either not assigned in any of the proposed
genera in this study, were not sampled as part of this or
0
Cordyceps annullata Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 8: 91. 1982.
Cordyceps arachnogena Kobayasi, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 2: 144. 1976.
Cordyceps aspera Pat., J. Bot. (Paris) 7: 344. 1893.
Cordyceps atewensis Samson, H.C. Evans & E.S.
Hoekstra, Proc. K. Ned. Akad. Wet., Ser. C, Biol. Med.
Sci. 8: 90. 1982.
Cordyceps atrobrunnea Penz. & Sacc., Malpighia 11:
22. 1897.
Cordyceps atropuncta Koval, Bot. Mater. Otd. Sporov.
Rast. 14: 18. 191.
Cordyceps atrovirens Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 4: 52. 1978.
Cordyceps aurantiaca Lohwag, in Handel-Mazzetti,
Symb. Sin. 2: 27. 1937.
Cordyceps aurea Moureau, Mém. Inst. Roy. Colon.
Belge 7: 21. 1949.
Cordyceps barberi Giard ex Massee, Ann. Bot. 9: 18.
189.
Cordyceps barnesii Thwaites, Fungi Ceylon, p. 110.
1873.
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
Cordyceps baumanniana Henn., Bot. Jahrb. Syst. 23:
39. 1897.
Cordyceps coronilla Höhn., Sitzungsber. Kaiserl. Akad.
Wiss. Wien 118: 30. 1909.
Cordyceps bicolor Pat., Mém. Acad. Malgache 6: 40.
1928.
Cordyceps cotopaxiana Kobayasi, Bull. Natn. Sci. Mus.
Tokyo, Ser. B, 7: 126. 1981.
Cordyceps bokyoënsis Kobayasi, J. Jap. Bot. 8: 221.
1983.
Cordyceps craigii Lloyd, Mycol. Writ. 4: 27. 191.
Cordyceps bombi Rick ex Lloyd, Mycol. Notes 2: 914.
1920.
Cordyceps brasiliensis Henn., Hedwigia 3: 221.
1897.
Cordyceps brittlebankii McLennan & Cookson, Proc.
Roy. Soc. victoria 38: 74. 192.
Cordyceps bulolensis Kobayasi, Bull. Natn. Sci. Mus.
Tokyo, Ser. B, 2: 142. 1976.
Cordyceps cranstounii Olliff, Agric. Gazette New S.
Wales : 408. 189.
Cordyceps ctenocephala Syd., Bot. Jahrb. Syst. 7:
323. 1922.
Cordyceps cuboidea Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 131. 1980.
Cordyceps cusu Pat., Bull. Soc. Mycol. France 11: 229.
189.
Cordyceps caespitosoiliformis Henn., Hedwigia 41:
11. 1902.
Cordyceps cylindrica Petch, Trans. Brit. Mycol. Soc.
21: 4. 1937.
Anamorph: Nomuraea atypicola (Yasuda) Samson
Cordyceps callidii Quél., Comp. Rend. Assoc. Franç.
Avancem. Sci. 21. Suppl. p. 7. 1897.
Cordyceps delectens Penz. & Sacc., Malpighia 11:
22. 1897.
Cordyceps cardinalis G.H. Sung & Spatafora, Mycologia
9: 0. 2004.
Anamorph: mariannaea/clonostachys-like
Cordyceps dimeropoda Syd., Bot. Jahrb. Syst. 7: 324.
1922.
Cordyceps carnata Moureau, Mém. Inst. Roy. Colon.
Belge 7: 10. 1949.
Cordyceps changpaishanensis Kobayasi, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 7: 12. 1981.
Cordyceps doassansii Pat., Tab. Analyt. Fung., p. 213.
188.
Cordyceps doiana Kobayasi, Bull. Natn. Sci. Mus.
Tokyo, Ser. B, 7: 124. 1981.
Cordyceps chualasae Koval & Nazarova, Nov. Sist.
Niz. Rast. : 11. 199.
Cordyceps ergoticola Tanda & Kawat., J. Jap. Bot. 52:
19. 1977.
Cordyceps chishuiensis Z.Q. Liang & A.Y. Liu,
Mycosystema 21: 9. 2002.
Cordyceps fasciculata Pat., Bull. Soc. Mycol. France
1: 20. 1899.
Cordyceps cinnabarina Petch, Ann. Crypt. Exot. 6: 230.
1933.
Cordyceps leischeri Penz. & Sacc., Malpighia 15: 230.
1901.
Cordyceps citrea Penz. & Sacc., Malpighia 11: 523.
1897.
Cordyceps fuliginosa Ces., Comment. Soc. Crittog.
Ital., Genova 1 : 7. 181.
Cordyceps clavicipiticola Tokugawa & S. Imai, Trans.
Sapporo Nat. Hist. Soc. 14: 104. 193.
Cordyceps furcata McLennan & Cookson, Proc. Roy.
Soc. victoria 3: 17. 1923.
Cordyceps clavicipitis Örtegren, Svensk Bot. Tidskr.
10: 7. 191.
Cordyceps gemella Moureau, Lejeunia, Mém. 1: .
191.
Cordyceps coccidiocapitata Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 91. 1982.
Cordyceps geotrupis Teng, Sinensia 4: 293. 1934.
Cordyceps coccidioperitheciata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 8: 79. 1982.
Cordyceps consumpta G. Cunn., Trans. Proc. New
Zealand Inst. 3: 377. 1921.
Cordyceps gracillima Kobayasi, Bull. Natn. Sci. Mus.
Tokyo, Ser. B, 7: 126. 1981.
Cordyceps grenadensis Mains, Bull. Torrey Bot. Club
81: 499. 194.
1
SuNG ET AL.
Cordyceps grylli Teng, Sinensia 7: 811. 1936.
Cordyceps joaquiensis Henn., Hedwigia 43: 248.
1904.
Cordyceps guizhouensis Z.Y. Liu, Z.Q. Liang & A.Y.
Liu, Mycosystema 1: 98. 1997.
Cordyceps juruensis Henn., Hedwigia 43: 248. 1904.
Cordyceps gunnii Berk., J. Bot., London 7: 77. 1848.
Anamorph: paecilomyces-like
Cordyceps kanzashiana Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 86. 1982.
Cordyceps gunnii var. minor Z.Z. Li, C.R. Li, B. Huang,
M.Z. Fan & M.W. Lee, Korean J. Mycol. 27: 232.
1999.
Cordyceps khaoyaiensis Hywel-Jones, Mycol. Res. 98:
939. 1994.
Anamorph: lecanicillium/simplicillium-like
Cordyceps hauturu Dingley, Trans. Roy. Soc. New
Zealand 81: 334. 193.
Cordyceps kirkii G. Cunn., Trans. Brit. Mycol. Soc. 8:
7. 1922.
Anamorph: Akanthomyces
Cordyceps hawkesii Gray, in Cooke, Grevillea 19: 7.
1891.
Cordyceps kobayasii Koval, Klavitipital’nye Griby SSSR
(Kiev), p. 178. 1984.
Cordyceps henleyae Massee, Ann. Bot. 8: 119. 1894.
Cordyceps hesleri Mains, J. Elisha Mitchell Sci. Soc.
: 12. 1939.
Cordyceps kusanagiensis Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 9: 7. 1983.
Cordyceps hillii Lloyd, Mycol. Notes : 101. 1921.
Cordyceps lacroixii Har. & Pat., Bull. Trimestriel Soc.
Mycol. France 20: 2. 1904.
Cordyceps hirotaniana Kobayasi, J. Jap. Bot. 8: 177.
1983.
Cordyceps langloisii Ellis & Everh., North Amer.
Pyrenom. p. 62. 1892.
Cordyceps hokkaidoënsis Kobayasi, Sci. Rep. Tokyo
Bunrika Daigaku, Sect. B, : 91. 1941.
Anamorph: Sporotrichum hokkaidoense Kobayasi
Cordyceps larvicola Quél., Bull. Soc. Bot. France 2:
292. 1878.
Cordyceps hormospora A. Möller, Phycomyceten u.
Ascomyceten, p. 230. 1901.
Cordyceps ignota Marchion., Physis, B. Aires 2: 17.
194.
Cordyceps imagamiana Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 9: 1. 1983.
Cordyceps incarnata A. Möller, Phycomyceten u.
Ascomyceten, p. 228. 1901.
Cordyceps inconspicua Moureau, Lejeunia, N.S. 14: 4.
192.
Cordyceps indigotica Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 4: 53. 1978.
Cordyceps interrupta Höhn., Sitzungsber. Kaiserl.
Akad. Wiss. Wien 118: 303. 1909.
Cordyceps iriomoteana Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 82. 1982.
Cordyceps ithacensis Bałazy & Bujak., Mycotaxon 25:
11. 198.
Cordyceps javensis Henn., Hedwigia 41: 142. 1902.
Cordyceps lateritia Dingley, Trans. Roy. Soc. New
Zealand 81: 337. 193.
Cordyceps leucocephala Moureau, Lejeunia, N.S. 14:
7. 192.
Cordyceps lignicola Massee, Bull. Misc. Inform. Roy.
Bot. Gard. Kew p. 173. 1899.
Cordyceps lilacina Moureau, Mém. Inst. Roy. Colon.
Belge 7: 2. 1949.
Cordyceps longdongensis A.Y. Liu & Z.Q. Liang,
Mycosystema 1: 140. 1997.
Cordyceps loushanensis Z.Q. Liang & A.Y. Liu,
Mycosystema 1: 1. 1997.
Cordyceps mantidicola Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 9: 12. 1983.
Cordyceps manzhurica Koval, Bot. Mater. Otd. Sporov.
Rast. 14: 11. 191.
Cordyceps maolanensis Z.Y. Liu & Z.Q. Liang,
Mycosystema 1: 4. 1997.
Cordyceps martialis Speg., Bol. Acad. Nac. Ci. Córdoba
11: 30. 1889.
= Cordyceps huntii Giard, Bull. Soc. Entomol. France 4: 171.
2
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
189.
= Cordyceps submilitaris Henn., Hedwigia 3: 222. 1897.
= Cordyceps klenei Pat., Bull. Trimestriel Soc. Mycol. France 24:
11. 1908.
Anamorph: cephalosporium-like
Cordyceps maolanoides Z.Q. Liang, A.Y. Liu & J.Z.
Huang, Mycosystema 21: 14. 2002.
Cordyceps memorabilis (Ces.) Sacc., Michelia 1: 321.
1879.
≡ Racemella memorabilis Ces., Comment. Soc. Crittog. Ital.
1: . 181.
Anamorph: Isaria farinosa (Holmsk.) Fr.
Cordyceps menesteridis F. Muell. & Berk., Gard. Chron.
2: 791. 1878.
Cordyceps michaelisii Henn., Hedwigia 41: 19. 1902.
Cordyceps miniata Moureau, Lejeunia, Mém. 1: 22.
191.
Cordyceps minuta Kobayasi, Bull. Natn. Sci. Mus.
Tokyo 6: 294. 1963.
Cordyceps muscae Henn., Bot. Jahrb. Syst. 2: 07.
1898.
Cordyceps musicaudata Z.Q. Liang & A.Y. Liu, Acta
Mycol. Sin. 1: 2. 199.
Cordyceps myosuroides Henn., Hedwigia 41: 19.
1902.
Cordyceps myrmecogena Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 4: 55. 1978.
Cordyceps nakazawae A. Kawam., Icon. Jap. Fungi 8:
83. 19 (as C. ‘nakazawai’).
Cordyceps nanatakiensis Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 9: 9. 1983.
Cordyceps necator Pat. & Har., Bull. Trimestriel Soc.
Mycol. France 28: 283. 1912.
Cordyceps nelumboides Kobayasi & Shimizu, Kew
Bull. 31: 7. 197.
Cordyceps neogryllotalpae Kobayasi, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 2: 143. 1976.
Cordyceps nipponica Kobayasi, Bull. Biogeogr. Soc.
Japan 9: 11. 1939.
Anamorph: Isaria nipponica Kobayasi
Cordyceps obliqua Kobayasi, Sci. Rep. Tokyo Bunrika
Daigaku, Sect. B, : 177. 1941.
Cordyceps obliquiordinata Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 114. 1982.
Cordyceps odyneri Quél., 14th Suppl. Champ. Jura et
vosges, p. 10. 188.
Cordyceps olivacea Rick, in Lloyd, Mycol. Writ. 7: 1118.
1922.
Cordyceps olivaceovirescens Henn., Hedwigia 39: 78.
1900.
Cordyceps olivascens Mains, Mycologia 39: 37.
1947.
Cordyceps ootakiensis Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 9: 15. 1983.
Cordyceps ovoideoperitheciata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 8: 83. 1982.
Cordyceps pallidiolivacea Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 113. 1982.
Cordyceps parvula Mains, Bull. Torrey Bot. Club 86:
4. 199.
Cordyceps phymatospora C.R. Li, M.Z. Fan & Z.Z. Li,
Mycosystema 21: 17. 2002.
Cordyceps pilifera Kobayasi, Bull. Natn. Sci. Mus.
Tokyo, Ser. B, 7: 126. 1981.
Cordyceps pittieri E. Bommer & M. Rousseau, Bull.
Soc. Bot. Belg. 3: 10. 189.
Cordyceps pluricapitata Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 87. 1982 (as C.
‘pleuricapitata’).
Cordyceps podocreoides Höhn., Sitzungsber. Kaiserl.
Akad. Wiss. Wien 118: 308. 1909.
Cordyceps polycarpica Z.Q. Liang & A.Y. Liu, Acta
Mycol. Sin. 1: 24. 199.
Cordyceps polycephala Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 9: 1. 1983.
Cordyceps proliica Kobayasi, Bull. Natn. Sci. Mus.
Tokyo 6: 289. 1963.
Cordyceps proliica f. terminalis Kobayasi, Bull. Natn.
Sci. Mus. Tokyo 6: 292. 1963.
Cordyceps novaezealandiae Dingley, Trans. Roy. Soc.
New Zealand 81: 337. 193.
Cordyceps pseudoatrovirens Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 8: 111. 1982.
Cordyceps novoguineënsis Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 2: 148. 1976.
Cordyceps pseudoinsignis Moureau, Mém. Inst. Roy.
Colon. Belge 7: 34. 1949.
3
SuNG ET AL.
Cordyceps pseudomilitaris Hywel-Jones & Sivichai,
Mycol. Res. 98: 940. 1994.
Anamorph: lecanicillium/simplicillium-like
Cordyceps pseudonelumboides Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 8: 80. 1982.
Cordyceps puiggarii Speg., Bol. Acad. Nac. Ci. Córdoba
11: 304 1889.
Cordyceps ramosipulvinata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 9: 2. 1983 (as C.
‘ramosopulvinata’).
Cordyceps ramosistipitata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 9: 6. 1983 (as C.
‘ramosostipitata’).
Cordyceps rhizomorpha A. Möller, Phycomyceten u.
Ascomyceten, p. 231. 1901.
Cordyceps riverae Pacioni, Giorn. Bot. Ital. 112: 395.
1978.
Cordyceps subcorticicola Henn., Hedwigia 41: 11.
1902.
Cordyceps sulfurea Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 9: 15. 1983.
Cordyceps suoluoënsis Z.Q. Liang & A.Y. Liu,
Mycosystema 21: 10. 2002.
Cordyceps taishanensis B. Liu, P.G. Yuan & J.Z. Cao,
Acta Mycol. Sin. 3: 192. 1984.
Cordyceps thaxteri Mains, J. Elisha Mitchell Sci. Soc.
: 120. 1939.
Anamorph: Akanthomyces aranearum (Petch)
Mains
Cordyceps translucens Petch, Trans. Brit. Mycol. Soc.
10: 37. 1924.
Cordyceps trinidadensis Mains, Bull. Torrey Bot. Club
8: 4. 199.
Cordyceps uleana Henn., Hedwigia 43: 248. 1904.
Cordyceps rostrata Z.Q. Liang, A.Y. Liu, M.H. Liu,
Fungal Diversity 14: 98. 2003.
Cordyceps rubiginosostipitata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. Tokyo, Ser. B, 9: 3. 1983.
Cordyceps rubra A. Möller, Phycomyceten
Ascomyceten, p. 233. 1901.
Anamorph:’Cephalosporium’ rubrum A. Möller
u.
Cordyceps rubricapitata Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 9: 9. 1983.
Cordyceps rubrostromata Kobayasi, J. Jap. Bot. 8:
221. 1983.
Cordyceps ryogamimontana Kobayasi, Bull. Natn. Sci.
Mus. Tokyo 6: 303. 1963.
Cordyceps sakishimensis Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, Ser. B, 9: 6. 1983.
Cordyceps sclerotium Kobayasi, Trans. Mycol. Soc.
Japan 23: 31. 1982.
Cordyceps shanxiensis B. Liu, F. Rong & H. Jin, J.
Wuhan Bot. Res. 3: 23. 198.
Cordyceps shimaensis Kobayasi, Bull. Natn. Sci. Mus.
Tokyo, Ser. B, 7: 10. 1981.
Cordyceps shimizui Y.J. Yao, Acta Mycol. Sin. 14: 28.
199.
Cordyceps sphaerocapitata Kobayasi, Bull. Natn. Sci.
Mus. Tokyo, Ser. B, 2: 143. 1976.
Cordyceps stiphrodes Syd., Bot. Jahrb. Syst. 7: 324.
1922.
4
Cordyceps variegata Moureau, Mém. Inst. Roy. Colon.
Belge 7: 30. 1949.
Cordyceps velutipes Massee, Ann. Bot. 9: 21. 189.
Cordyceps venezuelensis Mains, Mycologia 39: 43.
1947.
Cordyceps vinosa Moureau, Lejeunia, Mém. 1: 28.
191.
Cordyceps vorobjovii Koval & Nazarova, Nov. Sist. Niz.
Rast. : 108. 199.
Cordyceps wallaysii Westend.,
Bruxelles 7: 81. 189.
Bull.
Acad.
Sci.
Cordyceps yahagiana Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, Ser. B, 6: 88. 1980.
KEy TO THE GENERA OF FUNGI
FORMERLy CLASSIFIED IN COrdyCEPs
This key is designed to emphasize the most conspicuous
ield-, host-, and macroscopic characters available to the
user for Cordyceps sensu Kobayasi and Mains. It is a
key to the monophyletic genera described herein and is
not a key to the species. As relatively few species occur
on Elaphomyces and adult stages of Arthropoda, the
key begins with these characters so as to expeditiously
highlight or remove these taxa from consideration.
Host is an exceedingly important character in most
species descriptions of arthropod-pathogenic fungi.
The host should be collected with the fungal specimen
whenever possible, but this often proves problematic.
The vast majority of arthropod-pathogenic fungi occur
PHYLOGENEtIC CLASSIFICAtION OF CORDyCEPS AND tHE CLAvICIPItACEOuS FuNGI
on immature stages (e.g., larvae, pupae) of arthropods.
Therefore, if the host is lacking from a particular
specimen or collection, we suggest the user to begin
with couplet (6). The multigene phylogeny reveals that
colour, texture, and shape of stromata are particularly
phylogenetically informative, thus we place special
emphasis on these characters where possible but
emphasize that, as with most fungal taxa, exceptions
are to be expected.
To assist the user we briely deine some characters
of stromatal texture and morphology that may not be
intuitive:
Fleshy
– stromata that are composed of
relatively loosely woven hyphae
and are soft in texture (e.g., C.
militaris).
Wiry
– iliform stromata that are
somewhat brittle and stiff (e.g., O.
unilateralis).
Pliant
– iliform stromata that are more
pliable and rubbery to the touch;
when fresh, they bend easily
without breaking; typically slightly
more robust than wiry (e.g., O.
nutans).
Fibrous
– stromata that are composed of
relatively tightly woven hyphae
and are irm in texture, similar to
the stipe of a mushroom (e.g., E.
ophioglossoides, O. heteropoda).
Subicular
– production of perithecia on a
net-like structure of mycelium, not
on the developed stroma (e.g., C.
tuberculata).
Lateral pads
– production of perithecia on a
disc-like or cushion-like structure
on a subterminal region of the
stroma (e.g., O. variabilis, O.
unilateralis).
Aperithecial apices
– production of perithecia in
subterminal regions of the stroma,
resulting in an apical region of
the stroma lacking perithecia.
(Note: The term sterile apices
has also been used to describe
this condition, but the apical
regions of many stromata produce
an anamorph and thus are not
technically sterile.)
Cordyceps s. s. consists almost entirely of pallid to
brightly coloured species that produce soft leshy
stromata (e.g., C. militaris). The majority of species
attack larvae and pupae of Lepidoptera and Coleoptera
in leaf litter, moss or upper soil layers. Numerous
species that produce highly reduced stromata, loosely
organized hyphae, or a subiculum on the host also
occur in this genus (e.g. C. tuberculata), some of
which were previously classiied in Torrubiella (e.g., T.
confragosa).
Elaphocordyceps includes all species that
parasitize Elaphomyces and closely related species
that attack nymphs of cicadas. The morphology of the
Elaphomyces parasites and the cicada pathogens are
remarkably similar and attest to the recent history of
inter-kingdom host-jumps in a common subterranean
environment (Nikoh & Fukatsu 2000). The exception
to this genus is E. subsessilis, which macroscopically
and ecologically is distinct from the rest of the species,
but is well supported as being a member of the genus
based on molecular data and micromorphology.
Metacordyceps includes only a limited number of
described species, of which all but one are only known
from East Asia. The stromatal colour of fresh specimens
ranges from white to lilac, purple or green, and the
darker pigments are almost black in dried specimens.
The texture of the stromata is ibrous and not leshy
like Cordyceps s. s., and the hosts are almost always
buried in soil.
Ophiocordyceps is the largest genus of arthropodpathogenic fungi. Many species are darkly pigmented
and occur on immature stages of hosts buried in soil or
in decaying wood. Notable exceptions exist for both of
these traits among species that attack adult stages of
hosts, however. For example, O. unilateralis is common
on adult ants and occurs on the under sides of leaves,
and O. sphecocephala is common on adult wasps and
is found in leaf litter. Stromatal morphology is diverse,
ranging from iliform and wiry to clavate and ibrous,
according to species, and many species produce their
perithecia in nonterminal regions of the stroma, either
distinctly supericial, or in broad irregular patches, or in
lateral pads.
1. Host – Elaphomyces .........................................................................Elaphocordyceps (e.g., E. ophioglossoides)
1. Host – Arthropods ............................................................................................................................................... 2
2. Host – adult Arthropods ...................................................................................................................................... 3
2. Host – immature stage of Arthropods ............................................................................................................... .
3. Perithecia – colour: pallid, cream to white; arrangement: supericial on a subiculum or highly
educed pallid stroma. Host – adult Lepidoptera ............................................... Cordyceps (e.g., C. tuberculata)
3. On adult Arthropods other than Lepidoptera (e.g., ant, wasp, weevil, dragonly, etc.) and
stroma typically well-developed .......................................................................................................................... 4
SuNG ET AL.
4. Stroma – colour: yellow; texture: leshy; shape: stipitate, clavate. Perithecia – colour: like stroma;
arrangement: partially immersed to pseudoimmersed at right angles to surface of stroma (ordinal).
Host – typically on adult scarab beetles ........................................................Cordyceps (e.g., C. scarabaeicola)
4. Stroma – colour: brightly or darkly pigmented; texture: wiry or pliant, not leshy; shape: stipitate
with or without pronounced fertile head region. Perithecia – arrangement: immersed at an oblique
angle in fertile head region or more or less ordinal in subterminal lateral pads .................................................
. Stroma – colour: at least partly brightly coloured; texture: pliant; shape: stipitate with globose to elongated
fertile head region. Perithecia – arrangement: usually completely immersed at oblique angles, often giving
the surface of the fertile head region a slightly uneven appearance when mature. Host – typically on
adult insects (ants, wasps, weevils, dragonlies, etc.) ........ Ophiocordyceps (e.g., O. nutans, O. sphecocephala)
. Stroma – colour: darkly pigmented; texture: wiry; shape: iliform. Perithecia – colour: darkly pigmented
like stroma or darker; arrangement: produced in subterminal region of stroma in lateral pad(s).
Host – adult ants. ....................................................................................... Ophiocordyceps (e.g., O. unilateralis)
. Stroma – colour: pallid to brightly coloured; texture: leshy to ibrous; shape: usually stipitate,
clavate but stroma highly reduced or subicular in some species. Perithecia – colour: pallid to
brightly coloured like stroma; arrangement: typically partially immersed to pseudoimmersed to
supericial on clava or subiculum in some species............................................................................................... 7
. Stroma – colour: usually darkly pigmented tan to brown to olive or black, rarely white to lilac to purple;
texture: wiry, pliant or ibrous; shape: stipitate, club-shaped, or iliform, rarely subicular.
Perithecia – colour: typically pigmented like stroma or darker; arrangement: immersed to partially
immersed to pseudoimmersed to supericial ....................................................................................................... 8
7. Stroma – colour: pallid, cream to white; texture: ibrous; shape: reduced to pad-like or cushion-like
structure on surface of wood, connected to host buried in wood via rhizomorph-like structures.
Perithecia – colour: like stroma; arrangement: immersed to partially immersed on pad-like stroma.
Host – Scarabid beetle larvae buried in decaying wood .......................... Elaphocordyceps (e.g., E. subsessilis)
7. Stroma – colour: yellow to red to orange; texture: leshy; shape: usually stipitate clavate but
subicular in some species. Perithecia – colour: like stroma; arrangement: ordinal, typically
partially immersed to pseudoimmersed to supericial on clava or subiculum in some species.
Host – typically on larvae or pupae of arthropods in relatively exposed environments,
such as leaf litter, moss, or the uppermost soil layer .................Cordyceps (e.g., C. militaris, C. staphylinidicola)
8. Stroma – colour: olive to brown; texture: ibrous; shape: stipitate, fertile region terminal,
distinctly capitate to clavate. Perithecia – colour: like that of stroma; arrangement: immersed.
Host – cicada nymphs ................................................................................Elaphocordyceps (e.g., E. paradoxa)
8. Stroma – colour: tan to brown to black or lightly pigmented, white to lilac to purple, rarely brightly
pigmented; texture: wiry, pliant, ibrous; shape: stipitate, capitate to clavate to iliform, rarely subicular.
Perithecia – colour: similar to stroma when immersed, often darker when supericial; arrangement:
immersed, pseudoimmersed or supericial .......................................................................................................... 9
9. Stroma – colour: white to lilac to purple to green, then appearing almost black when dry; texture: ibrous;
shape: stipitate, typically with elongated clava. Perithecia – colour: like stroma; arrangement: immersed,
ordinal or oblique. Host – typically buried in soil .......................................................Metacordyceps (e.g., M. taii)
9. Stroma – colour: olive to brown to black rarely brightly coloured; texture: wiry, pliant, or ibrous;
shape: stipitate, club-shaped to clavate or iliform, rarely subiculate. Perithecia – colour: darkly
pigmented like stroma or darker; arrangement: immersed, pseudoimmersed but tightly spaced,
or supericial and widely spaced, produced in terminal clava or subterminal patches or lateral pads.
Host – typically embedded in rotten wood or buried in soil
..............................................................................Ophiocordyceps (e.g., O. sinensis, O. acicularis, O. variabilis)
ACKNOWLEDGEMENTS
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