· PPS PSP !
doi:10.5598/imafungus.2017.08.02.08
Cordycipitaceae Hypocreales
Ryan M. Kepler1, J. Jennifer Luangsa-ard2, Nigel L. Hywel-Jones3, C. Alisha Quandt4, Gi-Ho Sung5, Stephen A. Rehner6, M.
Catherine Aime7, Terry W. Henkel8, Tatiana Sanjuan9, Rasoul Zare10, Mingjun Chen11, Zhengzhi Li3, Amy Y. Rossman12, Joseph
W. Spatafora12, and Bhushan Shrestha13
ART I CLE
('*$ " #$$*>)# % $# 1
USDA-ARS, Sustainable Agriculture Systems Laboratory, Beltsville, MD 20705, USA; corresponding author e-mail: ryan.kepler@ars.usda.gov
Microbe Interaction and Ecology Laboratory, BIOTEC, National Science and Technology Development Agency, 113 Thailand Science Park,
Phahonyothin Rd, Klong Neung, Klong Luang, Pathum Thani, 12120 Thailand
1
2
Zhejiang BioAsia Institute of Life Sciences, 1938 Xinqun Road, Economic and Technological Development Zone, Pinghu, Zhejiang, 314200
China
4
Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48104, USA
5
Institute for Bio-Medical Convergence, International St Mary’s Hospital and College of Medicine, Catholic Kwandong University, Incheon 22711,
Korea
6
USDA-ARS, Mycology and Nematology Genetic Diversity and Biology Laboratory, Beltsville, MD 20705, USA
7
Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907, USA
8
Department of Biological Sciences, Humboldt State University, Arcata, CA, 95521, USA
9
Laboratorio de Taxonomía y Ecología de Hongos, Universidad de Antioquia, calle 67 No. 53 – 108, A.A. 1226, Medellin, Colombia
10
Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran
11
Anhui Provincial Key Laboratory of Microbial Control, Anhui Agricultural University, Hefei 230036, Peoples’ Republic of China
12
Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA
13
Mushtech Cordyceps Institute, Cheongil-ro 453 Beon-gil 55-9, Cheongil-myeon, Hoengseong-gun, Gangwon Province 25255, Korea
3
) # The ending of dual nomenclatural systems for pleomorphic fungi in 2011 requires the reconciliation
of competing names, ideally linked through culture based or molecular methods. The phylogenetic systematics
of Hypocreales and its many genera have received extensive study in the last two decades, however resolution
of competing names in Cordycipitaceae has not yet been addressed. Here we present a molecular phylogenetic
investigation of Cordycipitaceae@HB@GLBFXG?EVGL@EQOB@E<L<[O<>MG@ELZLB>G?EL@HE?[B>EXWBLVMD<EVG?@HGFB?E?
upon which these names can be maintained or suppressed. The taxonomy presented here seeks to harmonize
competing names by principles of priority, recognition of monophyletic groups, and the practical usage of affected
taxa. In total, we propose maintaining nine generic names, Akanthomyces, Ascopolyporus, Beauveria, Cordyceps,
Engyodontium, Gibellula, Hyperdermium, Parengyodontium, and Simplicillium and the rejection of eight generic
names, Evlachovaea, Granulomanus, Isaria, Lecanicillium, Microhilum, Phytocordyceps, Synsterigmatocystis, and
Torrubiella. Two new generic names, Hevansia and Blackwellomyces, and a new species, Beauveria blattidicola,
are described. New combinations are also proposed in the genera Akanthomyces, Beauveria, Blackwellomyces,
and Hevansia.
$1
3*4
Akanthomyces
Ascopolyporus
Beauveria
Blackwellomyces
Cordyceps
Dual nomenclature
Engyodontium
Gibellula
Hevansia
Hyperdermium
Parengyodontium
Simplicillium
Submitted: 21 April 2017; Accepted: 30 October 2017; Published: 21 November 2017.
INTRODUCTION
A molecular phylogenetic investigation of Clavicipitaceae, with
an emphasis on Cordyceps, was conducted by Sung et al. (2007)
and revealed that both Clavicipitaceae and Cordyceps were not
monophyletic. Two additional families, Cordycipitaceae and
Ophiocordycipitaceae, were recognized and species previously
OXB??EQGVELCordyceps were supported as members of all three
families. Clavicipitaceae and Ophiocordycipitaceae collectively
formed a monophyletic group, whereas CordycipitaceaeVGQLGV
by the phylogenetic position of the type species of Cordyceps,
C. militaris, shared a more recent common ancestor with
Hypocreaceae. The majority of sexually reproducing species
in Cordyceps s. str. produce stalked, erect stromatic ascomata
@HB@BDGG?HWEL@G@=DGF=@?<>G?MGOEG?BDGOHBDBO@GDEGVFW
reduced stipes or subiculate stromata. Stromata are frequently
bright yellow to orange or red, but others are pallid to cream or
white according to species.
In addition to Cordyceps, numerous genera for sexual
morphs have been included in Cordycipitaceae, the most
speciose and taxonomically problematic being Torrubiella.
Torrubiella has traditionally been used to classify pathogens
of spiders or less frequently scale insects that produce
?=MGDQOEBX MGDE@HGOEB [DG=GL@XW <L B ?=FEO=X=> §<DJ FW
Johnson et al. (2009) showed the genus to be polyphyletic
with species of Torrubiella being placed in Cordyceps and
© 2017 International Mycological Association
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VOLUME 8 · NO. 2
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3($ et al.
336
Ophiocordyceps (Ophiocordycipitaceae) as well as the new
genera Conoideocrella and Orbiocrella of Clavicipitaceae.
Torrubiella is now restricted to Cordycipitaceae infecting
spiders with most possessing asexual morphs that had
been referred to as Akanthomyces or Gibellula (Johnson
et al. 2009, Evans 2013). Other genera in Cordycipitaceae
produce perithecia on a subiculum, including Ascopolyporus
and Hyperdermium, but these differ from Torrubiella in
being pathogens of scale insects (Bischoff et al. 2005).
Phytocordyceps is a monotypic genus described for P.
ninchukispora, which molecular data determined to be
nested within Cordyceps (Sung et al. 2007), although, it is
=L=?=BX [<D @HG ZGL=? IE@H DG?MGO@ @< H<?@ B[QXEB@E<L BLV
ascospore morphology. The host is reported as a seed of
Beilschmiedia erythrophloia (Lauraceae), although closely
related Cordyceps species attack pupae of Limacodidae,
IHEOH?=MGDQOEBXXWDG?G>FXGZX<F<?G?GGV?HGB?O<?M<DG?
feature swollen ends connected by a long, narrowed midsection, a morphology referred to as bola-ascospores
(Eriksson 1982) that are also present in C. bifusispora and C.
cf. pruinosa (Sung et al. 2007).
Asexual morphs in CordycipitaceaeHBGFGGLOXB??EQGV
under many different names, and species of Cordyceps have
been associated with a diversity of asexual reproductive
><DMH<X<ZEG?BLW<[@HG?GB?G=BXXW@WMEQGVZGLGDBHBG
been demonstrated to be polyphyletic across Hypocreales.
¢LG <[ @HG <XVG?@ LB>G? [<D BL B?G=BXXW @WMEQGV ZGL=? EL
Cordycipitaceae is Isaria. The use of Isaria has varied greatly
over time and many associations outside of Hypocreales have
been observed (Samson 1974, Luangsa-ard et al. 2004). The
currently accepted concept of the genus was established by
Hodge et al. (2005), who designated a drawing of I. farinosa
by Holmskjold from 1781 as the lectotype for the genus. This
VGQLE@E<L?G@BD@HD<M<VEL[GO@ELZ?MGOEG?ELHypocreales apart
from morphologically similar Paecilomyces in Eurotiales.
Molecular data supported this distinction (Luangsa-ard et al.
2004), but also revealed a polyphyletic distribution of Isaria
species in Hypocreales (Luangsa-ard et al. 2005). Taxonomic
transfers for species with isarioid morphologies in the families
Clavicipitaceae and Ophiocordycipitaceae have also been
made in more inclusive investigations (Johnson et al. 2009,
Luangsa-ard et al. 2011, Kepler et al. 2014, Quandt et al.
2014, Ban et al. 2015, Spatafora et al. 2015).
Within Cordycipitaceae @HG B?G=BXXW @WMEQGV ZGLGDEO
names Lecanicillium and Simplicillium were described for
verticillium-like taxa. Species in Lecanicillium are distributed
throughout Cordycipitaceae and do not form a single
monophyletic clade (Sukarno et al. 2009). The type of
Lecanicillium is L. lecanii, known as the asexual morph of C.
confragosa, which was described as a Torrubiella based on
its host association with scale insects and the production of
?=MGDQOEBX @<DD=FEGXX<EV MGDE@HGOEB )BL? B>?<L
The asexual morph of C. militaris is also morphologically
similar to Lecanicillium (Gams & Zare 2001). Relationships
for species of Lecanicillium ELOX=VG B[QLE@EG? IE@H E?<XB@G?
morphologically similar to I. farinosa and a unique clade of
species characterized by L. psalliotae (Sung et al. 2001,
2007). Simplicillium EVGL@EQG? B OXBVG <[ ?MGOEG? @HB@ E?
sister to the remaining Cordycipitaceae; no known sexual
form has been linked to the genus (Nonaka et al. 2013).
The morphology is that of slender, elongate, mostly solitary
phialides producing singular or short chains of conidia (Zare
& Gams 2001). These species are mostly pathogens of fungi,
although occurrence on other substrates (e.g. air, soil, plants)
is known (Nonaka et al. 2013).
GDHBM? @HG FG?@JL<IL B?G=BXXW @WMEQGV ZGLGDEO
name in Cordycipitaceae is Beauveria, due to its role
in the development of the germ theory of disease and
its long-standing use as a biocontrol agent against pest
insects. Agostino Bassi demonstrated in 1834 that B.
bassiana (a fungus that bears his name) was the cause
of white muscardine disease of silkworm, which resulted
in considerable loss to the silk industry in Europe (Yarrow
HE?DGMDG?GL@GV@HGQD?@VG><L?@DB@E<L<[MB@H<ZGLEO
activity by a disease agent, predating Pasteur, who cited
Bassi in his papers (Porter 1973). Today, the pathogenic
ability of B. bassiana is intensely scrutinized in the effort to
improve control of insect pests (Xiao et al. 2012). Beauveria
E?VGQLGVFW@HGVE?@ELO@EGO<LEVE<ZGL<=?OGXX?@HB@GX<LZB@G
in a sympodial pattern to produce a zig-zag rachis-like
structure. Molecular phylogenies support the monophyly of
Beauveria O<LQD>ELZ @HG MHWX<ZGLG@EO =@EXE@W <[ @HE? [<D>
of conidiogenesis, especially when combined with other
characters (e.g., hydrophobic conidia, insect pathogenicity;
Rehner et al. 2011). The genus is highly diverse, with many
ODWM@EO?MGOEG?BLVXELJ?@<?GGDBX?G=BXXW@WMEQGV?MGOEG?
in Cordyceps (Rehner & Buckley 2005, Rehner et al. 2011).
These include the moth pathogen C. bassiana (Huang et al.
2002), and the beetle pathogens C. brongniartii (Shimazu
et al. 1988) and C. scarabaeicola (Shrestha et al. 2014a),
as well as pathogens of grasshoppers, stick insects, and
cockroaches from South America (Sanjuan et al. 2014), and
crickets from Thailand (Ariyawansa et al. 2015).
¢@HGDB?G=BXXW@WMEQGVZGLGDB@HB@MD<V=OGO<LEVEB<LB
rachis-like conidiophore include Evlachovaea, Engyodontium,
and Parengyodontium. A molecular investigation of Evlachovaea based on ITS and TEF data, including material from
the ex-type strain of E. kintrischica, revealed a close
association with some species placed in Isaria (Humber et
al. 2013). They demonstrated this generic name was a later
synonym of Isaria, but no formal transfer to the genus was
made at that time. Likewise, molecular data have supported
the separation of Engyodontium from Beauveria, and the
OXB??EQOB@E<L <[ P. album as distinct from Engyodontium
(Tsang et al. 2016). Finally, the monotypic genus Microhilum
was described for the asexual morph of a Cordyceps (Yip &
Rath 1989). It produces short conidiophores that give rise to
conidium-producing denticles and is morphologically similar
to Beauveria and Isaria; molecular data, however, place this
species close to C. militaris and C. kyusyuensis (Sung et al.
2007).
GGDBX B?G=BXXW @WMEQGV ZGLGDB BDG B??<OEB@GV IE@H
Torrubiella, the two most common being Akanthomyces
and Gibellula. A revision of Akanthomyces by Mains (1950)
included species forming hyaline conidia of various shapes on
phialides covering a cylindrical synnema in a hymenium-like
XBWGD IE@H ?=MGDQOEBX ?E>EXBDE@W @< ?MGOEG? <[ Hymenostilbe.
The type species of Akanthomyces, A. aculeatus, primarily
infects Lepidoptera. Cordyceps tuberculata is linked to A.
pistillariiformis, a pathogen of moths and a close relative of
IMA FUNGUS
2'*$ "*# % $# 1Cordycipitaceae
;< =<;59=
This work employs the data used in name reconciliation for
Ophiocordycipitaceae by Quandt et al. (2014), additional
published sequences obtained from GenBank (Bischoff et al.
2005, Rehner et al. 2011, Humber et al. 2013, Sanjuan et al.
2014), and sequences determined as part of this work (Table
HWX<ZGLG@EO BLBXW?G? =@EXEGV VB@B [D<> QG L=OXGBD
genes, including the small and large subunits of nuclear
encoded ribosomal DNA genes (SSU and LSU), the protein
coding genes translation elongation factor 1 alpha (TEF), and
the largest (RPB1) and second largest (RPB2) subunits of
RNA polymerase II, and representatives for the type species
of sexual and asexual genera throughout the family (Table
1). After assembly of raw sequencing reads with CodonCode
Aligner, version 2.0.6 (Dedham, MA) sequences were aligned
with representative sequences from throughout Hypocreales
as in Quandt et al. (2014) using MAFFT v.6 (Katoh et al.
2002, Katoh & Toh 2008). After alignment, gaps, introns and
B>FEZ=<=?XWBXEZLGVDGZE<L?EVGL@EQGVIE@HFX<OJ?BXBGDB
& Castresana 2007) were removed using the editing capacity
of Geneious v. 7.0.6 (Biomatters; available from http://www.
geneious.com). Maximum likelihood analysis was performed
with RAxML v. 8.2.8 employing a GTRGAMMA model of
nucleotide substitution. The dataset was divided into eleven
separate partitions, one for each ribosomal gene and one
each for of the three codon positions in protein coding genes.
The resulting phylogenetic framework serves as a guide to
DG?<XGO<LEO@?FG@IGGLO<>MG@ELZLB>G?[<D?G=BXXWBLV
B?G=BXXW@WMEQGVZGLGDEOLB>G?
For description of new species, collections were
rehydrated in sterilized water. Perithecia, asci, ascospores
and part-spores were examined on a Leica DMRB compound
microscope and Leica M28 stereomicroscope. Methuen
Handbook of Color (Kornerup et al. 1984) was used for colour
descriptions of stromata.
VOLUME 8 · NO. 2
< ;
The overall topology recovered in this analysis agrees with
that of previous works (Fig. 1; Sung et al. 2007, Johnson et
al. 2009, Nonaka et al. 2013, Quandt et al. 2014). The family Cordycipitaceae is well supported, as are many of the internal nodes, and this phylogenetic hypothesis for the family
supports the recognition of the genera Akanthomyces, Ascopolyporus, Beauveria, Cordyceps, Engyodontium, Gibellula,
Hyperdermium, and Simplicillium. Parengyodontium was not
?B>MXGV V=G @< EL?=[QOEGL@ ?G=GLOG VB@B&VVE@E<LBXXW IG
describe two new genera, Hevansia and Blackwellomyces,
to accommodate two clades of species without available
generic names, and a new species of Beauveria, B. blattidicola, that infects cockroaches. We do not use Evlachovaea,
Isaria, Lecanicillium, Microhilum, and Torrubiella and propose
that they be rejected along with other lesser-known names
(Table 2). There exist clades and lineages containing species named in Cordyceps, Lecanicillium and Torrubiella that
are not members of the clades containing the type species of
those genera; these are effectively treated as incertae sedis.
Below we discuss the major genera of Cordycipitaceae for
IHEOH?=[QOEGL@?B>MXELZE?BBEXBFXGLBXXOB?G?MD<M<?GV
ZGLGDBBDG@HGXGB?@ELOX=?EGOXBVG?VGQLGVEL@HGDG[GDGLOG
phylogeny as the terminal generic clade (Fig. 1).
ART I CLE
A. aculeatus. Gibellula species are pathogens of spiders and
produce synnemata with swollen conidiophores reminiscent
of Aspergillus. Other minor asexual genera include
Granulomanus, which is now considered to be a synonym of
Gibellula (Humber & Rombach 1987), and Pseudogibellula,
which is a synonym of Ophiocordyceps (Spatafora et al.
2015).
As summarized above, the taxonomic history of
Cordycipitaceae is complex and involves numerous sexual
BLVB?G=BXXW@WMEQGVLB>G?@HB@HBGFGGL=?GV@HD<=ZH<=@
Hypocreales. Here we present a phylogenetically informed
resolution of competing generic names in Cordycipitaceae
in order to determine the generic names to use since the
end of dual nomenclature for different morphs of the same
fungus in 2011 (McNeill et al. 2012). In making decisions
on names, we sought to harmonize the competing interests
among name priority, preferences of user communities,
the number of name changes required, and recognition of
monophyletic groups from molecular phylogenetic analyses.
We also introduce new generic and species names where
data support a straightforward taxonomic solution.
TAXONOMY
6#' %* Lebert, Z. Wiss. Zool. +: 449 (1858).
Type: Akanthomyces aculeatus Lebert, Z. Wiss. Zool. +: 449
(1858).
The genus Akanthomyces as proposed by Lebert (1858),
including the type A. aculeatus, primarily infects Lepidoptera
and forms a clade distinct from Beauveria and Cordyceps. It
includes the moth pathogen Cordyceps tuberculata, which is
linked to an asexual morph described as A. pistillariiformis
(Samson & Evans 1974). Other fungi in this clade include
C. coccidioperitheciata and C. confragosa, pathogens of
spiders and scales insects, respectively, which produce
torrubielloid perithecia (Kobayasi & Shimizu 1982). The
MD<V=O@E<L <[ ?=MGDQOEBX MGDE@HGOEB <L B ?@EMG VE?@ELZ=E?HG?
C. coccidioperitheciata from other sexual forms infecting
spiders in Cordycipitaceae, which either lack a stipe or
XBOJ ?=MGDQOEBX MGDE@HGOEB E[ B ?@EMG E? MDG?GL@ Cordyceps
confragosa was described by Mains (1949) in Torrubiella,
and while the morphology is torrubielloid, Akanthomyces has
taxonomic priority by date over Torrubiella (Boudier 1885).
In addition, the sexual morph C. confragosa is linked to
Lecanicillium lecanii, the type species of Lecanicillium, now
considered a synonym of Akanthomyces, which has priority
over Lecanicillium (Gams & Zare 2001). Chiriví-Salomón
et al. (2015) also showed that L. lecanii (as C. confragosa)
as well as some other species of Lecanicillium, namely L.
attenuatum, L. muscarium, and L. sabanense, fall within
Akanthomyces. Akanthomyces also includes asexually
@WMEQGV ?MGOEG? LB>G? MDGE<=?XW B??EZLGV @< @HG ZGL=?
Isaria, but not the type species, I. farinosa, which belongs
337
3($ et al.
ART I CLE
;#)$ LProposed list of generic names in Cordycipitaceae to be protected and their competing synonyms.
Proposed to protect
Proposed to reject
Akanthomyces Lebert in Z. Wiss. Zool. 9: 449. 1858.
(=) Torrubiella Boud. in Rev Mycol. (Toulouse) 7: 226. 1885.
Typus: Akanthomyces aculeatus Lebert 1858.
Typus: T. aranicida Boud. 1885.
(=) Lecanicillium W. Gams & Zare in Nova Hedwigia 72: 50.
2001.
Typus: L. lecanii (Zimm.) Zare & W. Gams 2001, now
regarded as Akanthomyces lecanii (Zimm.) Spatafora et al.
2017.
Ascopolyporus Möller in Bot. Mitt. Tropen 9: 300. 1901.
Typus: Ascopolyporus polychrous Möller 1901.
BeauveriaVuill. in Bull. Soc. Bot. France. 59: 40. 1912.
Typus: Beauveria bassiana (Bals.-Criv.) Vuill. 1912 (Botrytis bassiana Bals.Criv. 1835).
BlackwellomycesSpatafora & Luangsa-ard in IMA Fungus 8: PMS. 2017.
Typus:Blackwelliella cardinalis (G.H. Sung & Spatafora) Spatafora & Luangsaard 2017) Cordyceps cardinalisG.H. Sung & Spatafora 2004).
Cordyceps Fr., Observ. Mycol. 2: 316 [cancellans)] 1818, nom. cons.
(=) Isaria Pers. in Neues Mag.Bot.1: 121. 1794.
Typus: Cordyceps militaris(L.) Fr. 1818 (Clavaria militaris L.1753).
Typus: I. farinosa (Holmsk.) Fr. 1832, now regarded as
Cordyceps farinosa (Holmsk.) Kepler et al. 2017.
(=) Microhilum H.Y. Yip & A.C. Rath in J. Invert. Path. 53:
361. 1989.
Typus: M. oncoperae H.Y. Yip & A.C. Rath 1989, now
regarded as Cordyceps oncoperae (H.Y. Yip & A.C. Rath)
Kepler et al. 2017.
(=) Phytocordyceps C.H. Su & H.H. Wang in Mycotaxon 26:
338. 1986.
Typus: P. ninchukispora C.H. Su & H.H. Wang 1986. now
regarded as Cordyceps ninchukispora (C.H. Su & H.H.
Wang) G.H. Sung et al. 2007.
(=) Evlachovaea Borisov & Tarasov in Mikol. Fitopatol. 33:
250. 1999.
Typus: E. kintrischica B.A. Borisov & Tarasov 1999, now
regarded as Cordyceps kintrischica (B.A. Borisov & Tarasov)
Kepler et al. 2017.
Engyodontiumde Hoog in Persoonia 10: 53. 1978.
Typus: Engyodontium parvisporum (Petch) de Hoog 1978 (Rhinotrichum
parvispora Petch 1932).
Gibellula Cavara in Atti Ist. Bot. R. Univ. Pavia, ser. 2 3: 347. 1894.
Typus: Gibellula pulchra Cavara 1894.
(=) Synsterigmatocystis Costantin in Bull. Soc. Mycol.
France 4: 63. 1888.
Typus: S. arachnophila Costantin ex Vuill. 1888, now
regarded as Gibellula arachnophila (Ditmar) Vuill. 1910.
(=) Granulomanus de Hoog & Samson in Persoonia 10: 70.
1978.
Typus: G. aranearum (Petch) de Hoog & Samson 1978,
basionym: Cylindrophora aranearum Petch 1944.
Hevansia Luangsa-ard, Hywel-Jones & Spatafora in IMA Fungus 8: PM. 2017.
Typus: Hevansia novoguineensis (Samson & B.L. Brady) Luangsa-ard, HywelJones & Spatafora 2017 (Akanthomyces novoguineensis Samson & B.L. Brady
1982).
HyperdermiumJ.F. White et al. in Mycologia 92: 910. 2000.
Typus: Hyperdermium caulium (Berk. & M.A. Curtis) Chaverri & K.T. Hodge
2008 (Corticium caulium Berk. & M.A. Curtis 1854 [1853]).
Parengyodontium C.C. Tsang et al. in Medical Mycology 54: 708. 2016.
Typus: Parengyodontium album (Limber) C.C. Tsang et al. 2016 (Tritirachium
album Limber 1940).
SimplicilliumW. Gams &Zare in Nova Hedwigia 73: 38, 2001.
Typus: Simplicillium lanosiniveum (J.F.H. Beyma) Zare & W. Gams 2001
(Phalosporium lanosoniveum J.F.H. Beyma 1942).
338
IMA FUNGUS
2'*$ "*# % $# 1Cordycipitaceae
Hypocreales
Cordyceps bifusispora spat 08-133.1
Cordyceps bifusispora spat 08-129
Cordyceps albocitrina spat 07-174
100
Cordyceps bifusispora EFCC 5690
Cordyceps bifusispora EFCC 8260
Cordyceps sp. EFCC 2535
Isaria cicadae RCEF HP090724-31
Isaria coleopterorum CBS 110.73
Cordyceps cf. ochraceostromata ARSEF 5691
90 Isaria tenuipes ARSEF 5135
97 100
Cordyceps takaomontana MCA 1806
Isaria tenuipes OSC 111007
100
Cordyceps cf. takaomontana BCC 12688
Isaria fumosorosea CBS 107.1
100
Isaria fumosorosea CBS 244.31
Isaria fumosorosea CBS 375.7
Isaria farinosa CBS 111113
100
Cordyceps polyarthra MCA 1009
100
Cordyceps exasperata MCA 2155
100
Cordyceps polyarthra MCA 996
99
Cordyceps exasperata MCA 2288
Isaria cf. farinosa OSC 111004
99 Cordyceps ninchuckispora NHJ 10684
88
Cordyceps ninchuckispora NHJ 10627
Cordyceps ninchukispora EGS 38.165
96 100
Cordyceps ninchukispora EGS 38.166
100
91
Mariannaea pruinosa ARSEF 5413
100
Cordyceps ninchuckispora EFCC 5197
100
Cordyceps ninchuckispora EFCC 5693
100
Cordyceps morakotii BCC 55820
77
Cordyceps morakotii BCC 68398
100
Cordyceps chiangdaoensis BCC 75734
Cordyceps chiangdaoensis BCC 75733
100
Verticillium sp. CBS 102184
99
Cordyceps cf. pruinosa spat 09-021
Cordyceps cf. pruinosa spat 08-115
98
100
Cordyceps militaris OSC 93623
97
97
Cordyceps kyusyuensis EFCC 5886
100
Cordyceps rosea spat 09-053
Microhilum oncoperae AFSEF 4358
100
Cordyceps caloceroides MCA 2249
Cordyceps caloceroides QCNE 186715
100
Evlachovaea kintrischica ARSEF 7218
Evlachovaea kintrischica ARSEF 8058
100
Cordyceps sp. RCEF HP090724-04C
100
Isaria amoenerosea CBS 729.73
Isaria amoenerosea CBS 107.73
92
Cordyceps cf. takaomontana NHJ 12623
100
Isaria fumosorosea CBS 337.52
Isaria javanica CBS 134.22
95
Cordyceps acridophila HUA 179219
98 Cordyceps acridophila HUA 179221
100
Cordyceps acridophila HUA 179220
100
Cordyceps acridophila MCA 1181
100
Cordyceps locustiphila HUA 179218
100
Cordyceps locustiphila HUA 179219
100
Cordyceps diapheromeriphila QCNE 186272
100
99
Cordyceps diapheromeriphila QCNE 186714
Cordyceps diapheromeriphila MCA 1557
99100
Cordyceps staphylinidicola ARSEF 5718
Beauveria bassiana ARSEF 1564
100
Cordyceps brongniartii BCC 16585
Beauveria brongniartii ARSEF 617
100
100
Beauveria blattidicola MCA 1727
100
Beauveria blattidicola MCA 1814
Beauveria caledonica ARSEF 2567
79
Beauveria malawiensis ARSEF 7760
Beauveria pseudobassiana ARSEF 3405
Cordyceps scarabaeicola ARSEF 5689
95
Cordyceps tuberculata BCC 16819
94
Cordyceps tuberculata OSC 111002
92
Akanthomyces aculeatus HUA 186145
Akanthomyces pistillariaeformis HUA 186131
100
Cordyceps coccidioperitheciata NHJ 6709
96
Isaria farinosa CBS 541.81
Cordyceps coccidioperitheciata NHJ 5112
87
80 Lecanicillium sabanense ANDES-F 1011
100
Lecanicillium sabanense ANDES-F 1023
94
82
Lecanicillium sabanense ANDES-F 1024
82
Lecanicillium lecanii CBS 101247
100
Cordyceps confragosa spat 08-146
Lecanicillium attenuatum CBS 402.78
87
100
Isaria farinosa CBS 262.58
99
Isaria farinosa CBS 240.32
95
Cordyceps cf. cardinalis spat 09-052
100
Isaria farinosa OSC 111005
98
85
Isaria farinosa OSC 111006
100 100
Isaria sp. spat 09-050
Isaria sp. spat 09-051
Isaria sp. TNS 16333
100
Cordyceps piperis CBS 116719
Hyperdermium pulvinatum P.C. 602
100
Lecanicillium psalliotae CBS 532.81
Lecanicillium psalliotae CBS 363.86
Lecanicillium psalliotae CBS 101270
Lecanicillium fusisporum CBS 164.7
100
Cordyceps pseudomilitaris BCC 2091
99
Cordyceps pseudomilitaris BCC 1919
Blackwelliella
100
Cordyceps cardinalis OSC 93610
Cordyceps cardinalis OSC 93609
100
Ascopolyporus villosus ARSEF 6355
Ascopolyporus
Ascopolyporus polychrous P.C. 546
Hyperdermium caulium GenBank AF242354
92
Cordyceps nelumboides BCC 2190
Akanthomyces novoguineensis NHJ 13161
Akanthomyces arachnophilus NHJ 10469
98 100
Akanthomyces novoguineensis NHJ 13117
100
Akanthomyces novoguineensis NHJ 11923
98
100
Cordyceps nelumboides BCC 2093
Akanthomyces novoguineensis NHJ 4314
99
Cordyceps nelumboides TNS 16306
Akanthomyces cinereus NHJ 3510
99
Gibellula sp. NHJ 5401
98
Gibellula sp. NHJ 10788
100
100
Gibellula sp. NHJ 13158
100
Gibellula pulchra NHJ 10808
100
Torrubiella sp. NHJ 7859
100
Gibellula
longispora NHJ 12014
91
Gibellula leiopus BCC 16025
Torrubiella ratticaudata ARSEF 1915
Engyodontium aranearum CBS 309.85
Lecanicillium antillanum CBS 350.85
Lecanicillium aranearum CBS 726.73a
Torrubiella wallacei CBS 101237
99
Simplicillium lanosoniveum CBS 101267
100
Simplicillium lanosoniveum CBS 704.86
Simplicillium
Simplicillium obclavatum CBS 311.74
Simplicillium lamellicola CBS 116.25
ART I CLE
100
100
99
Ophiocordycipitaceae
Cordyceps
Clavicipitaceae
Cordycipitaceae
Hypocreaceae
Nectriaceae
Bionectriaceae
Beauveria
Akanthomyces
Hevansia
Gibellula
100
98
100
100
"L LRAxML tree of Cordycipitaceae. Dataset included 392 taxa and BO<LOB@GLB@GVBXEZL>GL@<[ FM[D<>QGL=OXGBDZGLG?ÒÒ
TEF, RPB1, and RPB2). Tips in bold represent examples of type species for their associated genera. Proposed genus level names to protect
are delimited, but names of individual species have not been changed on the leaves of the tree, demonstrating diversity of taxa sampled. Values
above branches are bootstrap proportions.
VOLUME 8 · NO. 2
339
3($ et al.
ART I CLE
;#)$L Voucher information and Genbank numbers for samples appearing in Figure 1.
340
(
. $$
;<
Akanthomyces aculeatus
HUA 186145
MF416572
MF416520
MF416465
Akanthomyces
arachnophilus
NHJ 10469
EU369090
EU369031
EU369008
2,
2,
EU369047
Akanthomyces cinereus
NHJ 3510
EU369091
EU369009
EU369048
EU369070
Akanthomyces
novoguineensis
NHJ 13117
EU369092
EU369010
EU369049
EU369073
Akanthomyces
novoguineensis
NHJ 13161
EU369093
EU369011
EU369050
Akanthomyces
novoguineensis
NHJ 4314
EU369094
EU369012
EU369051
EU369071
Akanthomyces
novoguineensis
NHJ 11923
EU369095
EU369032
EU369013
EU369052
EU369072
Akanthomyces
pistillariaeformis
HUA 186131
MF416573
MF416521
MF416466
Ascopolyporus polychrous
P.C. 546
DQ118737
DQ118745
DQ127236
Ascopolyporus villosus
ARSEF 6355
AY886544
DQ118750
DQ127241
Beauveria bassiana
ARSEF 1564
HQ880974
HQ880833
Beauveria blattidicola
MCA 1727
MF416593
MF416539
MF416483
MF416640
HQ880905
Beauveria blattidicola
MCA 1814
MF416594
MF416540
MF416484
MF416641
Beauveria brongniartii
ARSEF 617
HQ880991
HQ880854
Beauveria caledonica
ARSEF 2567
AF339570
AF339520
EF469057
EF469086
Beauveria malawiensis
ARSEF 7760
DQ376246
HQ880897
HQ880969
Beauveria pseudobassiana
ARSEF 3405
AY531931
HQ880864
HQ880936
Cordyceps acridophila
MCA 1181
MF416574
MF416522
Cordyceps acridophila
HUA 179220
JQ895527
JQ895536
Cordyceps acridophila
HUA 179219
JQ895541
JQ958613
JX003857
JX003841
Cordyceps acridophila
HUA 179221
JQ895526
JQ895537
JQ958615
JX003853
JX003843
Cordyceps albocitrina
spat 07-174
MF416575
MF416467
MF416629
Cordyceps bifusispora
EFCC 5690
EF468952
EF468806
EF468746
EF468854
EF468909
Cordyceps bifusispora
EFCC 8260
EF468953
EF468807
EF468747
EF468855
EF468910
Cordyceps bifusispora
spat 08-129
MF416576
MF416523
MF416468
MF416630
Cordyceps bifusispora
spat 08-133.1
MF416577
MF416524
MF416469
MF416631
MF416434
Cordyceps brongniartii
BCC 16585
JF415951
JF415967
JF416009
JN049885
JF415991
Cordyceps caloceroides
MCA 2249
MF416578
MF416525
MF416470
MF416632
Cordyceps caloceroides
QCNE 186715
MF416579
MF416526
Cordyceps cardinalis
OSC 93609
AY184973
AY184962
DQ522325
DQ522370
DQ522422
Cordyceps cardinalis
OSC 93610
AY184974
AY184963
EF469059
EF469088
EF469106
Cordyceps cf. cardinalis
spat 09-052
MF416580
MF416527
MF416471
MF416633
MF416435
Cordyceps cf.
ochraceostromata
ARSEF 5691
EF468964
EF468819
EF468759
EF468867
EF468921
Cordyceps cf. pruniosa
spat 08-115
MF416586
MF416532
MF416476
MF416635
MF416439
Cordyceps cf. pruniosa
spat 09-021
MF416587
MF416533
MF416477
MF416636
Cordyceps cf.
takaomontana
NHJ 12623
EF468984
EF468838
EF468778
EF468884
Cordyceps cf.
takaomontana
BCC 12688
MF416599
MF416545
MF416489
MF416646
Cordyceps
coccidioperitheciata
NHJ 5112
EU369109
EU369043
EU369026
EU369066
Cordyceps
coccidioperitheciata
NHJ 6709
EU369110
EU369042
EU369025
EU369067
EU369086
Cordyceps confragosa
spat 08-146
MF416581
MF416528
MF416472
MF416634
MF416436
Cordyceps
diapheromeriphila
MCA 1557
MF416582
MF416529
HQ880926
MF416628
JQ958614
JX003852
JX003842
EF468932
IMA FUNGUS
2'*$ "*# % $# 1Cordycipitaceae
;#)$L (Continued).
. $$
Cordyceps
diapheromeriphila
QCNE 186714
MF416601
Cordyceps
diapheromeriphila
QCNE 186272
Cordyceps exasperata
Cordyceps exasperata
;<
2,
2,
MF416547
MF416491
MF416648
JQ895530
JQ895534
JQ958610
JX003848
MCA 2155
MF416596
MF416542
MF416486
MF416643
MCA 2288
MF416592
MF416538
MF416482
MF416639
Cordyceps kyusyuensis
EFCC 5886
EF468960
EF468813
EF468754
EF468863
EF468917
Cordyceps locustiphila
HUA 179218
JQ895525
JQ895535
JQ958619
JX003846
JX003845
Cordyceps locustiphila
HUA 179219
JQ958598
JQ958597
Cordyceps militaris
OSC 93623
AY184977
AY184966
DQ522332
DQ522377
Cordyceps nelumboides
BCC 2093
MF416583
MF416530
MF416473
Cordyceps nelumboides
BCC 2190
MF416584
MF416531
MF416474
Cordyceps nelumboides
TNS 16306
MF416585
Cordyceps ninchuckispora
EFCC 5197
EF468965
EF468820
EF468760
EF468868
Cordyceps ninchuckispora
EFCC 5693
EF468966
EF468821
EF468762
EF468869
Cordyceps ninchuckispora
NHJ 10627
EF468967
lEF468822
EF468763
EF468870
Cordyceps ninchuckispora
NHJ 10684
EF468968
EF468823
EF468761
EF468871
Cordyceps ninchukispora
EGS 38.165
EF468991
EF468846
EF468795
EF468900
Cordyceps ninchukispora
EGS 38.166
EF468992
EF468847
EF468794
EF468901
Cordyceps piperis
CBS 116719
AY466442
DQ118749
DQ127240
Cordyceps polyarthra
MCA 996
MF416597
MF416543
MF416487
MF416644
Cordyceps polyarthra
MCA 1009
MF416598
MF416544
MF416488
MF416645
Cordyceps pseudomilitaris
BCC 1919
MF416588
MF416534
MF416478
MF416440
Cordyceps pseudomilitaris
BCC 2091
MF416589
MF416535
MF416479
MF416441
Cordyceps rosea
spat 09-053
MF416590
MF416536
MF416480
MF416637
MF416442
Cordyceps scarabaeicola
ARSEF 5689
AF339574
AF339524
DQ522335
DQ522380
DQ522431
Cordyceps sp.
EFCC 2535
EF468980
EF468835
EF468772
Cordyceps sp.
RCEF
HP090724-04C
MF416591
MF416537
MF416481
MF416638
MF416443
Cordyceps staphylinidicola
ARSEF 5718
EF468981
EF468836
EF468776
EF468881
Cordyceps takaomontana
MCA 1806
MF416595
MF416541
MF416485
MF416642
Cordyceps tuberculata
OSC 111002
DQ522553
DQ518767
DQ522338
DQ522384
DQ522435
Cordyceps tuberculata
BCC 16819
MF416600
MF416546
MF416490
MF416647
MF416444
Engyodontium aranearum
CBS 309.85
AF339576
AF339526
DQ522341
DQ522387
DQ522439
Evlachovaea kintrischica
ARSEF 7218
Evlachovaea kintrischica
ARSEF 8058
Gibellula leiopus
BCC 16025
MF416602
Gibellula longispora
NHJ 12014
EU369098
JX003847
AY545732
MF416437
MF416475
MF416438
EU369083
GU734751
GU734750
MF416548
MF416492
MF416649
EU369017
EU369055
EU369075
Gibellula pulchra
NHJ 10808
EU369099
EU369035
EU369018
EU369056
EU369076
Gibellula sp.
NHJ 10788
EU369101
EU369036
EU369019
EU369058
EU369078
Gibellula sp.
NHJ 13158
EU369100
EU369037
EU369020
EU369057
EU369077
Gibellula sp.
NHJ 5401
EU369102
EU369059
EU369079
Hyperdermium caulium
GenBank
AF242354
Hyperdermium pulvinatum
P.C. 602
DQ118738
DQ118746
DQ127237
Isaria amoenerosea
CBS 107.73
AY526464
MF416550
MF416494
MF416651
MF416445
Isaria amoenerosea
CBS 729.73
MF416604
MF416551
MF416495
MF416652
MF416446
Isaria cf. farinosa
OSC 111004
EF468986
EF468840
EF468780
EF468886
Isaria cicadae
RCEF
HP090724-31
MF416605
MF416552
MF416496
MF416653
VOLUME 8 · NO. 2
ART I CLE
(
AF242354
MF416447
341
3($ et al.
ART I CLE
;#)$L (Continued).
(
. $$
Isaria coleopterorum
CBS 110.73
JF415965
JF415988
Isaria farinosa
OSC 111005
DQ522558
DQ518772
Isaria farinosa
OSC 111006
EF469127
EF469080
EF469065
EF469094
Isaria farinosa
CBS 240.32
JF415958
JF415979
JF416019
JN049895
JF415999
Isaria farinosa
CBS 262.58
AB023943
AB080087
MF416497
MF416654
MF416448
Isaria farinosa
CBS 541.81
MF416606
MF416553
MF416498
MF416655
MF416449
Isaria farinosa
CBS 111113
AY526474
MF416554
MF416499
MF416656
MF416450
Isaria fumosorosea
CBS 337.52
MF416607
MF416555
MF416500
MF416657
MF416451
Isaria fumosorosea
CBS 375.70
AB083035
AB083035
MF416501
MF416658
MF416452
Isaria fumosorosea
CBS 107.10
MF416608
MF416556
MF416502
MF416659
MF416453
Isaria fumosorosea
CBS 244.31
MF416609
MF416557
MF416503
MF416660
MF416454
;<
2,
2,
JF416028
JN049903
JF416006
DQ522348
DQ522394
MF416558
Isaria javanica
CBS 134.22
MF416610
Isaria sp.
TNS 16333
MF416611
MF416504
MF416661
MF416455
MF416505
MF416662
MF416456
Isaria sp.
spat 09-050
MF416613
MF416559
MF416506
MF416663
MF416457
Isaria sp.
spat 09-051
Isaria tenuipes
OSC 111007
MF416614
MF416560
MF416507
MF416664
MF416458
DQ522559
DQ518773
DQ522349
DQ522395
DQ522449
Isaria tenuipes
ARSEF 5135
MF416612
JF415980
Lecanicillium antillanum
CBS 350.85
AF339585
AF339536
JF416020
JN049896
JF416000
DQ522350
DQ522396
DQ522450
Lecanicillium aranearum
CBS 726.73a
AF339586
AF339537
Lecanicillium attenuatum
CBS 402.78
AF339614
AF339565
EF468781
EF468887
EF468934
EF468782
EF468888
EF468935
Lecanicillium fusisporum
CBS 164.7
AF339598
Lecanicillium lecanii
CBS 101247
AF339604
AF339549
EF468783
EF468889
AF339555
DQ522359
DQ522407
DQ522466
Lecanicillium psalliotae
CBS 532.81
Lecanicillium psalliotae
CBS 101270
AF339609
AF339560
EF469067
EF469096
EF469112
EF469128
EF469081
EF469066
EF469095
Lecanicillium psalliotae
CBS 363.86
EF469113
AF339608
AF339559
EF468784
EF468890
Mariannaea pruinosa
ARSEF 5413
AY184979
AY184968
DQ522351
DQ522397
DQ522451
Microhilum oncoperae
AFSEF 4358
AF339581
AF339532
EF468785
EF468891
EF468936
Simplicillium lamellicola
CBS 116.25
AF339601
AF339552
DQ522356
DQ522404
DQ522462
Simplicillium lanosoniveum
CBS 101267
AF339603
AF339554
DQ522357
DQ522405
DQ522463
Simplicillium lanosoniveum
CBS 704.86
AF339602
AF339553
DQ522358
DQ522406
DQ522464
Simplicillium obclavatum
CBS 311.74
AF339567
AF339517
EF468798
DQ518777
DQ522360
Torrubiella ratticaudata
ARSEF 1915
DQ522562
Torrubiella sp.
NHJ 7859
EU369107
DQ522408
DQ522467
EU369064
EU369085
Torrubiella wallacei
CBS 101237
AY184978
AY184967
EF469073
EF469102
EF469119
Verticillium sp.
CBS 102184
AF339613
AF339564
EF468803
EF468907
EF468948
in Cordyceps. In general, the host range for asexual and
sexual forms of Akanthomyces are similar, although L.
attenuatum (CBS 402.78) was cultured from leaf litter with no
host reported. The morphological characters associated with
Akanthomyces are also found in a clade of spider-pathogenic
species sister to the Gibellula clade (see Hevansia below).
The type species of Torrubiella, T. aranicida, known from a
spider in France, was not available for inclusion in molecular
phylogenetic analyses. However, several morphological
characteristics of T. aranicida suggest that it may belong in
AkanthomycesHG?GELOX=VG@HG?=MGDQOEBXBLV?GMBDB@GV
arrangement of the perithecia and the lack of a subiculum
in the type specimen as shown in Johnson et al. (2009). A
number of sexual morphs now placed in Akanthomyces have
@<DD=FEGXX<EV B?O<>B@B ?MGOEQOBXXW A. coccidioperitheciatus
342
on spiders, A. lecanii on scale insects, and A. tuberculata on
moths.
6#' %* ## (Zare & W. Gams)
Spatafora, Kepler & B. Shrestha, %)L &L
MycoBank MB820860
Basionym: Lecanicillium attenuatum Zare & W. Gams, Nova
Hedwigia !P: 19 (2001).
6#' %*
( ' # (Kobayasi &
Shimizu) Spatafora, Kepler & B. Shrestha,
%)L
&L
MycoBank MB820880
Basionym: Cordyceps coccidioperitheciata Kobayasi & Shimizu,
Bull. Natl. Sci. Mus. Tokyo, B : 79 (1982).
IMA FUNGUS
2'*$ "*# % $# 1Cordycipitaceae
Basionym: Cephalosporium dipterigenum Petch, Naturalist
(Hull) SW: 102 (1931).
Synonyms: Cephalosporium longisporum Petch, Trans. Brit.
Mycol. Soc. : 166 (1925).
Lecanicillium longisporum (Petch) Zare & W. Gams, Nova
Hedwigia !P: 16 (2001).
? Acrostalagmus aphidum Oudem., Nederl. Kruidk. Arch.
P(2): 759 (1902) [no type collection found in L, only a
VDBIELZIHEOHV<G?L<@BXX<IBVGQLE@GO<LOX=?E<L®
Non Verticillium longisporum (Stark) Karapappa et al., Mycol.
Res. : 1293 (1997).
Non Akanthomyces longisporus B. Huang et al., Mycosystema
+: 172 (2000).
6#' %* $ # (Zimm.) Spatafora, Kepler &
B. Shrestha, %)L &L
MycoBank MB820881
Basionym: Cephalosporium lecanii Zimm., Teysmania +: 241
(1899).
Synonyms: Verticillium lecanii (Zimm.) Viégas, Revista Inst.
Café Estado São Paulo M: 754 (1939).
Lecanicillium lecanii (Zimm.) Zare & W. Gams, Nova Hedwigia
!P: 10 (2001).
Torrubiella confragosa Mains, Mycologia M : 305 (1949).
Cordyceps confragosa (Mains) G.H. Sung et al., Stud. Mycol.
S!: 49 (2007).
Hirsutella confragosa Mains, Mycologia M : 303 (1949).
For further synonyms see Zare & Gams (2001).
6#' %* % # (Petch) Spatafora, Kepler
& B. Shrestha, %)L &L
MycoBank MB820861
Basionym: Cephalosporium muscarium Petch, Naturalist
(Hull) SW: 102 (1931).
Synonyms: Lecanicillium muscarium (Petch) Zare & W.
Gams, Nova Hedwigia !P: 13 (2001).
Cephalosporium aphidicola Petch, Trans. Brit. Mycol. Soc.
W: 71 (1931).
Verticillium hemileiae Bouriquet, Encycl. Mycol. : 155
(1946).
For further synonyms see Zare & Gams (2001).
6#' %* #)# (J.S. Chiriví-Salomón et
al.) J.S. Chiriví-Salomón, T. Sanjuan & S. Restrepo,
%)L &L
MycoBank MB820862
Basionym: Lecanicillium sabanense J.S. Chiriví-Salomón et
al., Phytotaxa PM: 68 (2015).
6#' %* ) $# (Lebert) Spatafora,
Kepler & B. Shrestha, %)L &L
MycoBank MB820863
Basionym: Akrophyton tuberculatum Lebert, Z. Wiss. Zool.
+: 448 (1858).
Synonyms: Cordyceps tuberculata (Lebert) Maire, Bull. Soc.
Hist. Nat. Afrique N. : 165 (1917).
Isaria pistillariiformis Pat., Bull. Soc. Mycol. Fr. +: 163 (1893);
VOLUME 8 · NO. 2
as “pistillariaeformis”.
Insecticola pistillariiformis (Pat.) Mains, Mycologia M: 579
(1950); as “pistillariaeformis”.
Akanthomyces pistillariiformis (Pat.) Samson & H.C. Evans,
Acta Bot. Neerl. P: 29 (1974).
( $*(
ART I CLE
6#' %* ( " (Petch) Spatafora,
Kepler, Zare & B. Shrestha, %)L &L
MycoBank MB823235
Möller, Bot. Mitt. Tropen +: 300 (1901).
Type: Ascopolyporus polychrous Möller, Bot. Mitt. Tropen +:
300 (1901).
Ascopolyporus is a genus containing seven species,
represented in this study by the type A. polychrous and
A. villosus. These two species are strongly supported as
monophyletic, however their relationship to other taxa in
Cordycipitaceae remains poorly resolved. Sexual or asexual
morphologies have been observed in individual collections of
Ascopolyporus, and they co-occur in some species (Bischoff
et al. 2005). In the sexual form perithecia are produced
in a dense hyphal mat directly on top of the scale insect
host, and the appearance is similar to that of species in
Hypocrella or Moelleriella in Clavicipitaceae. Ascopolyporus
species produce multiseptate conidia, a feature also found in
Hyperdermium. Ascopolyporus shares another characteristic
with some species in Hypocrella in the apparent utilization of
plant resources via the scale insect cadaver to attain sizes
greatly in excess of the original host (Hywel-Jones & Samuels
1998, Bischoff et al. 2005, Chaverri et al. 2008).
,#& #Vuill., Bull. Soc. Bot. France S+: 40 (1912).
Type: Beauveria bassiana(Bals.-Criv.) Vuill., Bull. Soc. Bot.
France S+: 40 (1912).
The recognition of Beauveria as a genus separate from
Cordyceps E? B ?EZLEQOBL@ OHBLZG [<D Cordycipitaceae;
their respective type species are not congeneric. The
morphological features that unite species of Beauveria
have proved remarkably durable over time and no isolates
VG?ODEFGV [D<> <@HGD B?G=BXXW @WMEQGV ZGLGDB BDG JL<IL
in this clade. Direct links between species of Beauveria and
cordyceps-like sexual morphs are well established from
molecular data and culture-based experiments, including B.
bassiana (Li et al. 2001, Huang et al. 2002), B. brongniartii
(Shimizu et al. 1988), and B. sungii (Shrestha et al. 2014a).
The host range for the asexual morphs is extensive, infecting
many insect species across multiple orders (de Faria &
Wraight 2007) as well as being isolated from soil and as
foliar endophytes (Vega et al. 2009). The sexual morphs
are known from Coleoptera, Lepidoptera, Orthoptera, and
Phasmatodea, and here we also describe a new species
from Blattodea, expanding the known host range of sexual
morphs of Beauveria.
,#& ## ('$# (T. Sanjuan & Franco-Mol.) T.
Sanjuan, B. Shrestha, Kepler & Spatafora,
%)L
&L
MycoBank MB820883
Basionym: Cordyceps acridophila T. Sanjuan & Franco-Mol.,
Mycologia W: 268 (2014).
343
ART I CLE
3($ et al.
"LL Beauveria blattidicola (MCA1727 – holotype). A. Fresh stroma on cockroach. B. Dried stroma on cockroach. C. Stroma with partially
immersed perithecia. D. Perithecia. <LAscus showing prominent ascus cap. L Ascus showing cylindrical ascospores. G. Part-spores. H. End of
B?O=??H<IELZB?O=?[<<@$BD?&¥$!>>#(! Ó>#*! Ó>#)¥ª!Ó>
,#& #)###(Bals.-Criv.) Vuill., Bull. Soc. Bot.
Fr. S+: 40 (1912).
Basionym: Botrytis bassiana Bals.-Criv., Linnaea : 611
(1835).
Synonyms: Spicaria bassiana (Bals.-Criv.) Vuill., Bull. Soc.
Sc. Nancy, ser. 3, : 153 (1910).
Penicillium bassianum (Bals.-Criv.) Biourge, Cellule PP: 101
(1923).
Cordyceps bassiana Z.Z. Li et al., Chin. Sci. Bull. +: 751
(2001).
,#& #)$# $# M. Chen, Aime, T.W. Henkel &
Spatafora, (L &L(Fig. 2)
MycoBank MB821050
Etymology: The species epithet refers to the fungus’
occurrence on the host insect family Blattidae.
Diagnosis: Similar in host association to Ophiocordyceps
blattarioides F=@VE[[GD?EL@HGWGXX<I<DBLZGG?HW?@D<>B@B
long, sinuous stipe, and cylindrical to narrowly clavate fertile
region with partially immersed perithecia.
Type: *##: Region 8, Potaro-Siparuni: Pakaraima
Mountains, Upper Potaro River Basin, within a 4 km radius
of Potaro base camp at 5°18’04.8”N, 59°54’40.4”W, 710750
m elev.; on adult cockroach, 31 May, 2001, M.C. Aime MCA
1727 (BRG – holotype).
Description: Stromata solitary or paired, unbranched, arising
[D<>HGBV<D@H<DB<[EL[GO@GVBV=X@<[O<OJD<BOHIE@HG?HW
texture, total length 50–60(–90) mm long; stalk 0.8–1.5 mm
broad, light yellow (4A3–4A4); fertile area apical, cylindrical to
narrowly clavate, 6-8 × 1.2–1.4 mm, yellowish orange (4A7–
4A8). Perithecia partially immersed, darker concolorous,
interspersed with white mycelial wefts, presented at right
344
angle to the surface of stroma, in longitudinal section oval
@< <<EV ¥ Ô
¥ Ó> Asci hyaline, cylindrical,
¥ Ô¥Ó>IE@HBMD<>ELGL@BMEOBXOBM ¥ Ó>
diam. AscosporesQXE[<D>LGBDXWB?X<LZB?@HGB?OE?><<@H
hyaline, distinct irregularly multiseptate, not easily breaking
into part-spores. Part-spores ¥ Ô Ó> OWXELVDEOBX
with truncate ends.
Known distribution: Guyana.
Additional specimens examined: *##: Region 8, PotaroSiparuni: Pakaraima Mountains, Upper Potaro River Basin, within
a 4 km radius of Potaro base camp at 5°18’04.8”N, 59°54’40.4”W,
710750 m elev., on adult cockroach adhered to leaf in litter, 12 June
2000, M.C. Aime MCA 1203 (PUL); on adult cockroach in leaf litter,
14 July 2000, T.W. Henkel TH 7645 (HSC); on adult cockroach, 25
May 2001, M.C. Aime MCA 1628 (PUL); on adult cockroach, 7 June
2001, M.C. Aime MCA 1814 (PUL); on adult cockroach in leaf litter,
24 July 2003, T.W. Henkel TH 8607 (HSC); on adult cockroach on
mineral soil below leaf litter, 17 July 2009, T.W. Henkel TH 9049
(OSC); on adult cockroach, partially buried in litter, 27 May 2010,
M.C. Aime & L. Williams MCA 4043 (PUL); on adult cockroach, 9
June 2012, M.C. Aime MCA 4883 (PUL).
GenBank: MCA1727 MF416593, MF416539, MF416483,
MF416640; MCA1814 MF416594, MF416540, MF416484,
MF416641
Commentary: Species of Cordyceps s. lat. infecting cockroaches have rarely been collected in nature. Only two
cockroach-associated species are recorded in the literature:
Ophiocordyceps blattarioides (Sanjuan et al. 2015) and O. blattae
G@OH F<@HOXB??EQGVELOphiocordycipitaceae. The
Neotropical O. blattarioides is associated with adult Blattodea,
and is closely related to the morphologically similar adult
Orthoptera-associated O. amazonica (Sanjuan et al. 2015).
IMA FUNGUS
2'*$ "*# % $# 1Cordycipitaceae
Diagnosis: Blackwellomyces is the least inclusive genuslevel clade that includes the species B. cardinalis and B.
pseudomilitaris. Blackwellomyces is diagnosed by the unique
characters of the ascospore, which have irregularly spaced
septa and do not disarticulate into part-spores at maturity.
Type: Blackwellomyces cardinalis (G.H. Sung & Spatafora)
Spatafora & Luangsa-ard 2017.
,#& # #(' % ('$# (T. Sanjuan & S.
Restrepo) T. Sanjuan, B. Shrestha, Kepler &
Spatafora, %)L &.
MycoBank MB820882
Description: Sexual morph: Stromata solitary or multiple,
?E>MXG <D FDBLOHGV @EMG G?HW <DBLZG @< DGV OWXELVDEOBX
to enlarging apically, 4–50 × 0.5–3.0 mm. Fertile area
terminal, cylindrical, fusiform to clavate to irregularly shaped,
2–9 × 1–4 mm. Perithecia crowded, loosely embedded,
ordinal in orientation, elliptical to fusiform to obclavate. Asci
8-spored, hyaline, cylindrical, possessing a prominent apex.
Ascospores?><<@HQXE[<D>HWBXELGEDDGZ=XBDXW>=X@E?GM@B@G
not fragmenting into part-spores.
Asexual morph: Cultures moderately fast growing in
PDA and may turn the media red. Aerial mycelium is whitish
to whitish yellow and the reverse side of cultures is red or
cream. Conidiogenous cells phialides, solitary or in whorls
<[<D?I<XXGLB@@HGFB?G<D?XEZH@XWB?J?HBMGVIEVGD
near the base and tapering at the apex. Conidia hyaline,
aseptate, ellipsoidal to elliptical, in some species produced
in sympodially imbricate chains. Asexual morphs have been
described as similar to species in Clonostachys, Hirsutella,
Isaria, and Mariannaea.
Basionym: Cordyceps diapheromeriphila T. Sanjuan & S.
Restrepo, Mycologia W: 270 (2014).
Hosts: On larva of Lepidoptera.
,#& # ) "# (Sacc.) Petch, Trans. Brit.
Mycol. Soc. : 249 (1926).
Basionym: Botrytis brongniartii Sacc., Syll. Fung. : 540
(1892).
Synonym: Cordyceps brongniartii Shimazu, Trans. Mycol.
Soc. Japan +: 328 (1989).
,#& #$ ('$# (Henn.) B. Shrestha, Kepler &
Spatafora, %)L &.
MycoBank MB820884
Distribution: Southeastern USA, eastern China, Japan,
Korea, and Thailand.
Basionym: Cordyceps locustiphila Henn., Hedwigia MP: 246
(1904).
Commentary: The species placed here are supported
as a distinct clade and separate from other genera of
Cordycipitaceae based on the placement of their type
species. We describe these taxa as Blackwellomyces on the
basis of their phylogenetic novelty and irregularly septate
ascospores that do not disarticulate into part-spores. This
contrasts with other members of the family in which septation
and disarticulation is common.
,#& # # #)#
Kepler, %)L &L
MycoBank MB820891
$#(Kobayasi) S.A. Rehner &
Basionym: Cordyceps scarabaeidicola Kobayasi, Bull. Natl.
Sci. Mus. Tokyo, B : 137 (1976); as “scarabaeicola”.
Synonym: Beauveria sungii S.A. Rehner & R.A. Humber,
Mycologia P: 1070 (2011).
,#& ##('*$ $# (Kobayasi & Shimizu) B.
Shrestha, Kepler & Spatafora, %)L &.
MycoBank MB820895
Basionym: Cordyceps staphylinidicola Kobayasi & Shimizu,
Bull. Natl. Sci. Mus. Tokyo, B : 88 (1982); as “staphylinidaecola”.
,$# 64$$ %* Spatafora & Luangsa-ard, "L
&L
MycoBank MB820864
,$# 64$$ %* # #$ (G.H. Sung & Spatafora)
Spatafora & Luangsa-ard,
%)L &L MycoBank
MB820865
Basionym: Cordyceps cardinalis G.H. Sung & Spatafora,
Mycologia +W: 660 (2004).
,$# 64$$ %* ( %$# (Hywel-Jones &
Sivichai) Spatafora & Luangsa-ard, %)L &L
MycoBank MB820866
Basionym: Cordyceps pseudomilitaris
Sivichai, Mycol. Res. +: 940 (1994).
.
Etymology: This genus is named for Meredith Blackwell and
honours her invaluable contributions to our knowledge of
insect-associated fungi.
VOLUME 8 · NO. 2
ART I CLE
Ophiocordyceps blattae was described originally from Sri Lanka
(as Cordyceps blattae), but the species remains poorly known,
as sequence data are lacking, and current taxonomic concepts
are based entirely on the original description and drawings of
Petch (1924). Based on the possession of ophio-ascospores
and clavate asci with reduced apices, O. blattae is likely closely
related to O. unilateralis (Petch 1931) and is the type of the genus
Ophiocordyceps (Sung et al. 2007). Beauveria blattidicola is
easily distinguished from both O. blattarioides and O. blattae by
@HGO<>FELB@E<L<[WGXX<I@<WGXX<IE?H<DBLZGG?HW?@D<>B@B
the long and sinuous stalk, cylindrical to narrowly clavate fertile
region, and partially immersed perithecia typical of other sexual
morphs of Beauveria. Molecular data also strongly support
the placement of B. blattidicola in Beauveria (Fig. 1). While B.
blattidicola cultures are currently unavailable, its phylogenetic
placement predicts a Beauveria-type asexual morph.
Hywel-Jones
&
* ( Fr., Observ. Mycol. : 316 [cancellans]
(1818), nom. cons.
Type: Cordyceps militaris (L.) Fr., Observ. Mycol. : 317
[cancellans] (1818).
345
ART I CLE
3($ et al.
346
In this analysis, many species of Cordyceps, including the
type, are resolved as a well-supported clade interspersed
with genera described originally for asexual morphs, including
Evlachovaea, Isaria, and Microhilum (Fig. 1). Additionally, our
analysis indicates this core Cordyceps is not monophyletic
with C. cardinalis and C. pseudomilitaris, a result consistent
with Sung et al. (2007); the latter two species are proposed
in the new genus Blackwellomyces here (see above). Within
the core Cordyceps clade, internal relationships are generally
well-supported, giving rise to a phylogenetic structure that
roughly corresponds to stromatal colour (red to orange vs.
white to yellow). A thorough review of the taxonomic history
of Cordyceps was provided by Shrestha et al. (2014b), who
concluded that Cordyceps is the oldest accepted generic
LB>GEL@HE?OXBVGBLVE?@WMEQGVFWB?G=BX><DMH$B?GV
on the cylindrical shape of the stroma, pre-Linnaean literature
of the 17th and early 18th century had recorded C. militaris, the
type species of Cordyceps, under the old but obsolete generic
names Fungus and Fungoides (Shrestha et al. 2014b). The
species was transferred to Clavaria by Linnaeus (1753).
Clavaria militaris was then transferred to the ascomycete
genus Sphaeria (now rejected in favour of Hypoxylon), a
OXB??EQOB@E<L @HB@ IB? [<XX<IGV =L@EX @HG GBDXW th century
(Shrestha et al. 2014b). The genus Cordyceps was
established (Fries 1818, Link 1833) and over the years was
circumscribed to include pathogens of more than 12 insect
orders and the fungal genera Elaphomyces and Claviceps
(Kobayasi 1941, Mains 1958, Sung et al. 2007, Kepler
et al. 2012, Araújo & Hughes 2016, Shrestha et al. 2016).
This generic concept of Cordyceps stood for approximately
200 years until the polyphyletic nature of Cordyceps as it
had been understood by Kobayasi and Mains was revealed
(Sung et al. (2007).
Three monotypic generic names are now considered to
be synonyms of Cordyceps¢=DVB@BO<LQD>GV@HGQLVELZ?
of Humber et al. (2013) who demonstrated that the type
species of the monotypic Evlachovaea, E. kintrischica, is a
synonym of Isaria (see below). Similarly, the type species
of Microhilum, M. oncoperae, known to have a Cordyceps
sexual morph, was nested within Cordyceps, as is the type
species of Phytocordyceps, P. ninchukispora.
The generic name Isaria is the oldest available name
for the entire group of taxa considered here, including
Cordyceps. However, the concept of Isaria has a long
and convoluted history, with many changes of status and
differences of opinion in how the name should be applied
(e.g. Hodge et al. 2005, Gams et al. 2005). Petch (1934)
concluded the name was too confusing to use and suggested
it be applied to a subgenus of Spicaria. However, Hodge et
al XGO@<@WMEQGVIsaria sensu Fries using an illustration
of I. farinosa that appeared in the original description of this
species as Ramaria farinosa (Holmskjold 1781). Gams et
al. (2005) proposed the use of Isaria for Paecilomyces sect.
Isarioidea, now also regarded as a synonym of Cordyceps.
Entomogenous species morphologically similar to Isaria can
be found distributed throughout Hypocreales (Luangsa-ard
et al. 2004), and here are shown to be polyphyletic within
Cordycipitaceae. The ex-epitype isolate of I. farinosa (CBS
111113, Gams et al. 2005) is here determined to belong within
Cordyceps. We therefore propose the rejection of Isaria in
favour of Cordyceps owing to the confusion surrounding the
application of Isaria. Additionally, rejecting Cordyceps would
be disruptive to a large user community while the name Isaria
is not as widely used. Species of Isaria are herein integrated
into the monophyletic application of Cordyceps. The diversity
of species infecting cicada nymphs complicates the transfer
of I. cicadae, and will be addressed in a subsequent paper
focused on the group.
* ( #% > # (Henn.)
Shrestha & Spatafora, %)L &L
MycoBank MB820975
.
Kepler,
B.
Basionym: Isaria amoene-rosea Henn., Hedwigia M : 66
(1902).
Synonym: Paecilomyces amoeneroseus (Henn.) Samson,
Stud. Mycol. 6: 37 (1974).
* ( ##$## (Z.Q. Liang) Kepler, B.
Shrestha & Spatafora, %)L &L
MycoBank MB820976
.
Basionym: Paecilomyces cateniannulatus Z.Q. Liang, Acta
Phytopathol. Sin. : 10 (1981).
Synonym: Isaria cateniannulata (Z.Q. Liang) Samson &
Hywel-Jones, Mycol. Res. +: 588 (2005).
* ( # )$@# (Z.Q. Liang) Kepler, B.
Shrestha & Spatafora, %)L &L
MycoBank MB820977
.
Basionym: Paecilomyces cateniobliquus Z.Q. Liang, Acta
Phytopathol. Sin. : 9 (1981).
Synonym: Isaria cateniobliqua (Z.Q. Liang) Samson & HywelJones, Mycol. Res. +: 588 (2005).
* ( $ ( % (Samson & H.C. Evans)
Kepler, B. Shrestha & Spatafora, %)L &L
MycoBank MB820978
.
Basionym: Paecilomyces coleopterorum Samson & H.C.
Evans, Stud. Mycol. 6: 47 (1974).
Synonym: Isaria coleopterorum (Samson & H.C. Evans)
Samson & Hywel-Jones, Mycol. Res. +: 588 (2005); as
“coleopterora”.
* (1# # (Holmsk.) Kepler, B. Shrestha &
Spatafora, %)L &L
MycoBank MB820979
.
Basionym: Ramaria farinosa Holmsk., K. Danske Vidensk.
Selsks. Skr., Nye Samling : 279 (1781).
Synonyms: Clavaria farinosa (Holmsk.) Dicks., Fasc. Pl.
Crypt. Brit. : 25 (1790).
Isaria farinosa (Holmsk.) Fr., Syst. Mycol. P: 271 (1832); nom.
sanct.
Corynoides farinosa (Holmsk.) Gray, Nat. Arr. Brit. Pl. : 654
(1821).
Spicaria farinosa (Holmsk.) Vuill., Bull. Soc. Mycol. France
!: 76 (1911).
Penicillium farinosum (Holmsk.) Biourge, Cellule PP: 102
(1923).
Paecilomyces farinosus (Holmsk.) A.H.S. Br. & G. Sm.,
Trans. Brit. Mycol. Soc. M : 50 (1957).
IMA FUNGUS
2'*$ "*# % $# 1Cordycipitaceae
* (1%
# (Wize) Kepler, B. Shrestha
& Spatafora, %)L &L
MycoBank MB820980
Cordyceps takaomontana Yakush. & Kumaz., Sci. Rep.
Tokyo Bunrika Daig., B S: 108 (1941).
Basionym: Isaria fumosorosea Wize, Bull. Int. Acad. Sci.
Cracovie, Cl. Sci. Math. Nat.: 721 (1905) [“1904”].
Synonyms: Spicaria fumosorosea (Wize) Vassiljevski, Morbi
Plant. :146 (1929).
Paecilomyces fumosoroseus (Wize) A.H.S. Br. & G. Sm.,
Trans. Brit. Mycol. Soc. M : 67 (1957).
<"* %de Hoog, Persoonia : 53 (1978).
* ( "'# (Samson & H.C. Evans)
Kepler, B. Shrestha & Spatafora, %)L &L
MycoBank MB820981
.
Basionym: Paecilomyces ghanensis Samson & H.C. Evans,
Stud. Mycol. 6: 46 (1974).
Synonym: Isaria ghanensis (Samson & H.C. Evans) Samson
& Hywel-Jones, Mycol. Res. +: 588 (2005).
* ( #&# # (Frieder. & Bally) Kepler, B.
Shrestha & Spatafora, %)L &L
MycoBank MB820982
.
Basionym: Spicaria javanica Frieder. & Bally, Meded.
{ 6: 146 (1923).
Synonyms: Paecilomyces javanicus (Frieder. & Bally) A.H.S.
Br. & G. Sm., Trans. Brit. Mycol. Soc. M : 65 (1957).
Isaria javanica (Frieder. & Bally) Samson & Hywel-Jones,
Mycol. Res. +: 588 (2005).
* ( 6 ' # B.A. Borisov & Tarasov)
Kepler, B. Shrestha & Spatafora, %)L &L
MycoBank MB820983
Type: Engyodontium parvisporum
Persoonia : 53 (1978).
(Petch)
de
Hoog,
ART I CLE
.
Engyodontium was erected by de Hoog (1978) to accommodate the type species, E. parvisporum, and E. album,
@HG XB@@GD ?MGOEG? IB? [<D>GDXW OXB??EQGV EL Beauveria, and
most recently placed in Parengyodontium (see below).
Gams et al. (1984) added four more species. The genus
is restricted here to species with cobweb-like colonies that
produce dense clusters of denticles on elongated rachides.
Conidia are hyaline and globose to subglobose. No sexual
reproductive morph has been linked to Engyodontium.
Molecular phylogenetic analyses based on E. aranearum
support the distinction from Beauveria, but additional study
of the type species is required. Species are isolated from soil
and arthropod cadavers, and as opportunistic cutaneous and
subcutaneous infections of animals including humans.
)$$$# Cavara, Atti Ist. Bot. R. Univ. Pavia, 2 ser. P:
347 (1894).
Type: Gibellula pulchra Cavara, Atti Ist. Bot. Univ. Lab.
Crittog. Pavia P: 347 (1894).
.
Basionym: Evlachovaea kintrischica B.A. Borisov & Tarasov,
Mikol. Fitopatol. PP: 250 (1999).
* ( $ $# (Z.Q. Liang et al.) Kepler, B.
Shrestha & Spatafora, %)L &L
MycoBank MB820984
.
Basionym: Isaria locusticola Z.Q. Liang et al., Mycotaxon
S: 31 (2008).
* ( ( # (H.Y. Yip & A.C. Rath) P.J.
Wright, J. Invert. Path. WM: 146 (1994).
MycoBank MB363549
.
Basionym: Microhilum oncoperae H.Y. Yip & A.C. Rath, J.
Invert. Path. SP: 362 (1989).
* ( ( ( #46 (Cabanillas et al.) Kepler, B.
Shrestha & Spatafora, %)L &L
MycoBank MB820985
.
Basionym: Isaria poprawskii Cabanillas et al., Mycoscience
SM: 162 (2013).
The genus Gibellula is recognized here for spiderpathogenic fungi that produce primarily synnematous,
aspergillus-like conidiophores with terminal vesicles, which
give rise to phialides produced on metulae. Molecular
phylogenies place all sampled Gibellula species in a single
clade along with torrubiella-like sexual morphs. Torrubiella
has been shown to be polyphyletic, including astipitate
taxa throughout Cordycipitaceae and Hypocreales. The
status of Torrubiella is complicated further by the uncertain
phylogenetic placement of the type species, T. aranicida. The
original description indicated an asexual morphology that
more closely approximates Lecanicillium or Simplicillium.
Further, the production of scattered perithecia directly
from the host, rather than aggregated on a subiculate
pad, do not suggest inclusion of Gibellula in Torrubiella.
Rather, the genus Torrubiella is regarded as a synonym of
Akanthomyces here based on the perithecial arrangement
and lack of a subiculum in the type specimen (discussed
under Akanthomyces). The genus Granulomanus, based
on G. aranearum IHEOH E? XELJGV @< @HG ?G=BXXW @WMEQGV
T. albolanata, was regarded as a synonym of Gibellula by
Humber & Rombach (1987), but no molecular data exist to
O<LQD><DDG[=@G@HE??=ZZG?@E<L
* ( ( (Peck) Kepler, B. Shrestha &
Spatafora, %)L &L
MycoBank MB820986
)$$$# # # ' ('$# (Ditmar) Vuill., Bull. Séanc.
Soc. Sci. Nancy, sér. 3 : 156 (1910).
Basionym:Isaria tenuipes Peck, Ann. Rep. N.Y. St. Mus. Nat.
Hist. P : 44 (1879).
Synonyms: Paecilomyces tenuipes (Peck) Samson, Stud.
Mycol. 6: 49 (1974).
Basionym: Isaria arachnophila Ditmar, in Sturm, Deutschl.
Fl., 3 Abt. (Pilze Deutschl.) (4): tab. 55 (1817).
Synonyms: Hymenostilbe arachnophila (Ditmar) Petch,
Naturalist (Hull) SW: 249 (1931).
.
VOLUME 8 · NO. 2
347
ART I CLE
3($ et al.
Synsterigmatocystis arachnophila Costantin ex Vuill., Bull.
Soc. Mycol. France !: 81 (1911).
Gibellula arachnophila f. macropus Vuill., Bull. Soc. Mycol.
France PW: 41 (1920).
Torrubiella arachnophila f. alba Kobayasi & Shimizu, Kew
Bull. P : 561 (1977).
Cordyceps arachnophila J.R. Johnst., Bull. Puerto Rico
Insula Exp. Sta. : 23 (1915).
Torrubiella arachnophila (J.R. Johnst.) Mains, Mycologia M:
316 (1950).
)$$$# # ## % P. Syd., Just’s Bot. Jahresber.
S!: 321 (1922).
Synonym: Torrubiella gibellulae Petch, Ann. Mycol P : 391
(1932).
)$$$# $#&## Samson & H.C. Evans, Mycologia
M: 306 (1992).
Synonym: Torrubiella clavata Samson & H.C. Evans,
Mycologia M: 306 (1992).
)$$$# #)'# B. Huang et al., Mycosystema !: 110 (1998).
Synonym: Torrubiella dabieshanensis B. Huang et al.,
Mycosystema !: 110 (1998).
)$$$# % ('# Tzean et al., Mycol. Res. :
1350 (1998).
Synonym: Torrubiella dimorpha Tzean et al., Mycol. Res.
: 1350 (1998).
)$$$# "$ ) # Kobayasi & Shimizu, Bull. Natn.
Sci. Mus. Tokyo, B : 45 (1982).
Synonym: Torrubiella globosa Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, B : 45 (1982).
)$$$#"$ ) (## Kobayasi & Shimizu, Bull.
Natn. Sci. Mus. Tokyo, B : 49 (1982).
Basionym: Torrubiella globosostipitata Kobayasi & Shimizu,
Bull. Natn. Sci. Mus. ; 6* , B : 49 (1982).
)$$$#$ ( (Vuill. ex Maubl.) Mains, Mycologia
M: 313 (1950).
Diagnosis: Hevansia is the least inclusive genus-level
clade that includes H. novoguineensis and H. nelumboides.
Hevansia is diagnosed by the immersed perithecia, an
Akanthomyces-like asexual morph, and parasitism on
spiders.
Type: Hevansia novoguineensis (Samson & B.L. Brady)
Luangsa-ard et al. 2017 (see below)
Description: Sexual morph: Stroma arising from dorsal
abdomen, stipe 1–2 mm, fertile part ca 1 mm, white to cream,
or in astipitate perithecial cushions surrounding host abdomen
or sides of legs. Perithecia immersed, crowded at stipe apex
or in cushions, few (<5) to numerous (30+), narrowly ovoid
or sickle-shaped. Asci?M<DGVB?O<?M<DG?QXE[<D>HWBXELG
whole, or disarticulating into part-spores.
Asexual morph: Stroma white, cream-yellow, brown
or grey mycelium completely covering host. Synnemata
erect, simple or branched, solitary to numerous, cylindrical
to clavate, cream to ash-grey or brownish white. In some
species 2–4 prominent synnemata up to 6 mm long
interspersed with numerous tiny synnemata scattered
over host. Phialides in a monolayer, sparsely scattered or
crowded, on a basal cell or arising from lateral cells, usually
single, occasionally two or three on lateral basal cell,
smooth-walled, cylindrical, globose, obovoid, obpyriform or
ellipsoid, terminating in short but distinct neck or tapering
into a long neck. Conidia catenate, usually one-celled,
smooth-walled, hyaline, clavate, cylindrical, cymbiform,
fusiform to narrowly obclavate. Colony on PDA white front,
reverse cream, orange to pale red, some species with pale
wine-red pigment on the agar.
Hosts: On spiders on the underside of leaves of forest plants.
Distribution: Primarily in tropical regions globally, although
specimens are known from temperate regions.
)$$$#($ ' #Cavara, Atti Ist. bot. R. Univ. Pavia,
2 sér. P: 347 (1894).
Commentary: A biphyletic split is observed among the astipitate species previously considered in Torrubiella with asexual
morphs in Gibellula forming a clade of species pathogenic
on spiders. Another clade includes species on spiders in the
tropics, many of which were previously considered members
of Akanthomyces. These species constitute the new genus
Hevansia described here. Placement of the spider pathogen
C. nelumboides in this genus demonstrates the diverse morphology of Hevansia species, as C. nelumboides produces
perithecia in a disc sitting atop a well-formed stipe.
Synonyms: Torrubiella arachnophila var. pulchra Mains,
Mycologia M: 316 (1950).
Torrubiella pulchra (Mains) Koval, Klavitsipital’nye Griby
SSSR: 71 (1984).
5&### # ' ('$# (Petch) Luangsa-ard, HywelJones & Spatafora, %)L &L
MycoBank MB820886
5&## Luangsa-ard, Hywel-Jones & Spatafora,
"L &L
MycoBank MB820885
Basionym: Trichosterigma arachnophilum Petch, Trans. Brit.
Mycol. Soc. : 215 (1923); as “arachnophila”.
Synonyms: Hirsutella arachnophila (Petch) Petch, Trans. Brit.
Mycol. Soc. +: 93 (1923).
Basionym: Gibellula arachnophila f. leiopus Vuill. ex Maubl.,
Bull. Soc. Mycol. France PW: 42 (1920).
Torrubiella arachnophila var. leiopus Mains, Mycologia M:
318 (1950).
Torrubiella leiopus (Mains) Kobayasi & Shimizu, Kew Bull.
P : 564 (1977); as “pleiopus”.
348
Etymology: This genus is named for Harry C Evans and
honours his invaluable contributions to our knowledge of
insect associated fungi.
IMA FUNGUS
2'*$ "*# % $# 1Cordycipitaceae
5&## # (Hywel-Jones) Luangsa-ard, HywelJones & Spatafora, %)L &L
MycoBank MB820887
Basionym: Akanthomyces cinereus Hywel-Jones, Mycol.
Res. : 1068 (1996).
5&## 6 # (Hywel-Jones) Luangsa-ard,
Hywel-Jones & Spatafora, %)L &L
MycoBank MB820888
Basionym: Akanthomyces koratensis Hywel-Jones, Mycol.
Res. : 1067 (1996).
genus, was found to have an earlier epithet, so the name
was corrected to H. caulium by Chaverri (et al. 2008). In
these analyses H. caulium, with C. piperis, is placed in an
unresolved position.
2# "* % C.C. Tsang et al., Med. Mycol. SM:
708 (2016).
Type: Parengyodontium album (Limber) C.C. Tsang et al.,
Med. Mycol. SM: 709 (2016).
Based on molecular phylogenetic analyses, Parengyodontium
was erected by Tsang et al. (2016) to recognize Engyodontium
album as a distinct taxon relative to E. parvisporum. To date
it is a monotypic genus.
5&##$ "( # (B. Huang et al.)Luangsa-ard,
Hywel-Jones & Spatafora, %)L &L
MycoBank MB820889
%($ $$%W. Gams &Zare, Nova Hedwigia !P: 38
(2001).
Basionym: Akanthomyces longisporus B. Huang et al.,
Mycosystema +: 172 (2000).
Type: Simplicillium lanosiniveum (J.F.H. Beyma) Zare & W.
Gams, Nova Hedwigia !P: 39 (2001).
5&##$%) (Kobayasi & Shimizu) Luangsaard, Hywel-Jones & Spatafora, %)L &L
MycoBank MB820890
Simplicillium includes species isolated from other fungi
and soil environments (Zare & Gams 2001, Nonaka et al.
2013). Current phylogenetic analyses resolve Simplicillium
as the earliest diverging lineage in Cordycipitaceae (Fig. 1).
Simplicillium species are morphologically reduced, producing
conidia on the tips of long, slender, solitary phialides. No
sexual forms have been associated with Simplicillium.
Basionym: Cordyceps nelumboides Kobayasi & Shimizu,
Kew Bull. P : 557 (1977).
5&## & " (Samson & B.L. Brady)
Luangsa-ard, Hywel-Jones & Spatafora, %)L &L
MycoBank MB820892
Basionym: Akanthomyces novoguineensis Samson & B.L.
Brady, Trans. Brit. Mycol. Soc. !+: 571 (1982).
5&## & $ "## (L.S. Hsieh et al.) Luangsa-ard,
Hywel-Jones & Spatafora, %)L &L
MycoBank MB820893
Basionym: Akanthomyces ovalongatus L.S. Hsieh et al.,
Mycologia +: 321 (1997).
5&## 4) (Hywel-Jones) Luangsa-ard,
Hywel-Jones & Spatafora, %)L &L
MycoBank MB820894
Basionym: Akanthomyces websteri Hywel-Jones, Mycol.
Res. : 1068 (1996).
5*( %% J.F. White et al., Mycologia +: 910
(2000).
Type: Hyperdermium caulium (Berk. & M.A. Curtis) Chaverri
& K.T. Hodge, Stud. Mycol. W : 63 (2008) [syn. H. bertonii
(Speg.) J.F. White et al., Mycologia +: 910 (2000)].
Hyperdermium was erected by Sullivan et al. (2000) for
Epichloë bertonii and H. pulvinatum, which parasitize scale
EL?GO@?EL@HG@D<MEO?@D<>B@BBDGB@@GLGV<DM=XELB@GBLV
vary in colour from white to orange. Perithecia are immersed
to sub-immersed with asci and ascospores characteristic of
Cordycipitaceae, but are unique in producing multiseptate
conidia. Hyperdermium bertonii, the type species of the
VOLUME 8 · NO. 2
ART I CLE
Akanthomyces arachnophilus (Petch) Samson & H.C. Evans,
Acta Bot. Neerl. P: 33 (1974).
Petch, Trans. Brit. Mycol. Soc. +: 127 (1923).
.9. 9
In this paper we used a multigene phylogeny (Fig. 1) to guide
a taxonomic revision of Cordycipitaceae in compliance with
changes to Art. 9 of the ICN to no longer permit the separate
naming of fungal morphs (McNeill et al. 2012). The resulting
analysis provides the basis for recognition of 11 genera in
Cordycipitaceae regardless of life-stage or the associated
morphological differences (Fig. 3). The generic name
Cordyceps is retained, and we sought to circumscribe that
genus in the most inclusive way possible. The ex-epitype isolate
of the type of Isaria, I. farinosa, is nested within Cordyceps,
yet we recommend the rejection of Isaria, to avoids further
splitting of Cordyceps. Here, Beauveria includes the traditional
species known from asexual morphs, but also several taxa
previously described for sexual morphs in Cordyceps and a
LGI ?G=BXXW @WMEQGV ?MGOEG? VG?ODEFGV HGDG ¢=D BMMD<BOH
allows continuity for the use of names of taxa important for
biocontrol and historical concepts of diversity for the group.
We propose to use the name Gibellula for a clade of spider
pathogens, rather than Torrubiella. This decision is based on
morphology of the type species, T. aranicida, which includes
?=MGDQOEBX MGDE@HGOEB MD<V=OGV EL B ?OB@@GDGV >BLLGD BLV
not on a subiculum, and an asexual morph described as
more similar to Akanthomyces than Gibellula. Akanthomyces
has priority over Torrubiella, although we cannot discount a
MHWX<ZGLG@EOB[QLE@W<[Torrubiella to T. wallacei or Simplicillium.
Therefore, we recommend the rejection of Torrubiella against
Akanthomyces. Finally, the use of Lecanicillium is resolved.
349
ART I CLE
3($ et al.
B
A
D
350
C
E
F
G
H
I
J
IMA FUNGUS
2'*$ "*# % $# 1Cordycipitaceae
.39F <=<<;
This manuscript is dedicated to our colleague and esteemed
mycologist Walter Gams (1934-2017) whose contributions to
taxonomy and nomenclature of fungi made this work possible.
We would like to acknowledge the following individuals for their
contribution to this manuscript: Ryan Woolverton, Yi-jian Yao,
Shenghua Wu, and also members of the Japan Society for Vegetable
Wasps and Plant Worms. This research was supported by Bioindustry Technology Development Program (316025-05) of IPET
(Korea Institute of Planning and Evaluation for Technology in Food,
Agriculture, Forestry and Fisheries) of Ministry for Food, Agriculture,
Forestry and Fisheries, Korea and the National Center for Genetic
Engineering and Biotechnology (BIOTEC), National Science
and Technology Development Agency, Thailand. This material is
based upon work supported by the National Science Foundation
Foundation (DEB-1258162, DEB-0529752 to JWS; DEB-0918591,
DEB-1556339 to TWH; OISE-0714106, OISE-0914288 to RMK). Any
<MELE<L?QLVELZ?BLVO<LOX=?E<L?<DDGO<>>GLVB@E<L?GMDG??GV
in this material are those of the author(s) and do not necessarily
DGGO@ @HG EGI? <[ @HG B@E<LBX OEGLOG <=LVB@E<LHG >GL@E<L
of trade names or commercial products in this publication is solely
[<D @HG M=DM<?G <[ MD<EVELZ ?MGOEQO EL[<D>B@E<L BLV V<G? L<@
imply recommendation or endorsement by the US Department of
Agriculture (USDA); the USDA is an equal opportunity provider and
employer.
<<<.<
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