Access to this full-text is provided by Pensoft Publishers.
Content available from Mycokeys
This content is subject to copyright. Terms and conditions apply.
Novel taxa and species diversity of Cordyceps sensu lato
(Hypocreales, Ascomycota) developing on wireworms
(Elateroidea and Tenebrionoidea, Coleoptera)
Ling-Sheng Zha1,2,3, Vadim Yu Kryukov4, Jian-Hua Ding1,
Rajesh Jeewon5, Putarak Chomnunti2,3
1School of Life Sciences, Huaibei Normal University, Huaibei 235000, P.R. China 2School of Sciences, Mae
Fah Luang University, Chiang Rai 57100, ailand 3Center of Excellence in Fungal Research, Mae Fah
Luang University, Chiang Rai 57100, ailand 4Institute of Systematics and Ecology of Animals, Siberian
Branch of Russian Academy of Sciences, Frunze str., 11, Novosibirsk 630091, Russia 5Department of Health
Sciences, Faculty of Medicine and Health Sciences, University of Mauritius, Reduit 80837, Mauritius
Corresponding author: Putarak Chomnunti (putarak.cho@mfu.ac.th)
Academic editor: N. Wijayawardene |Received 9 December 2020|Accepted 12 March 2021|Published 29 March 2021
Citation: Zha L-S, Kryukov VY, Ding J-H, Jeewon R, Chomnunti P (2021) Novel taxa and species diversity of
Cordyceps sensu lato (Hypocreales, Ascomycota) developing on wireworms (Elateroidea and Tenebrionoidea,
Coleoptera). MycoKeys 78: 79–117. https://doi.org/10.3897/mycokeys.78.61836
Abstract
Species of Cordyceps sensu lato (Hypocreales, Sordariomycetes) have always attracted much scientic at-
tention for their abundant species diversity, important medicinal values and biological control applica-
tions. e insect superfamilies Elateroidea and Tenebrionoidea are two large groups of Coleoptera and
their larvae are generally called wireworms. Most wireworms inhabit humid soil or fallen wood and are
often infected with Cordyceps s.l. However, the species diversity of Cordyceps s.l. on Elateroidea and Ten-
ebrionoidea is poorly known. In the present work, we summarise taxonomic information of 63 Cordyceps
s.l. species that have been reported as pathogens of wireworms. We review their hosts and geographic
distributions and provide taxonomic notes for species. Of those, 60 fungal species are accepted as natural
pathogens of wireworms and three species (Cordyceps militaris, Ophiocordyceps ferruginosa and O. variabi-
lis) are excluded. Two new species, O. borealis from Russia (Primorsky Krai) and O. spicatus from China
(Guizhou), are described and compared with their closest allies. Polycephalomyces formosus is also described
because it is reported as a pathogen of wireworms for the rst time. Phylogeny was reconstructed from a
combined dataset, comprising SSU, LSU and TEF1-α gene sequences. e results, presented in this study,
support the establishment of the new species and conrm the identication of P. formosus.
Keywords
Two new species, Elateridae, molecular phylogeny, Ophiocordyceps, taxonomy, Tenebrionidae
MycoKeys 78: 79–117 (2021)
doi: 10.3897/mycokeys.78.61836
https://mycokeys.pensoft.net
Copyright Ling-Sheng Zha et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC
BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
RESEARCH ARTICLE
A peer-reviewed open-access journal
Launched to accelerate biodiversity research
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
80
Introduction
e superfamilies Elateroidea and Tenebrionoidea are two large groups of Coleoptera.
Species within these superfamilies are phytophagous, xylophagous, saprophagous or
omnivorous and most of them are important agricultural pests (Gullan and Cranston
2010; Ren et al. 2016). Elateroidea larvae are the well-known wireworms, closely re-
sembling Tenebrionoidea larvae which are known as mealworms or pseudo-wireworms
(Ren et al. 2016). As a result, in practice, larvae of both Elateroidea and Tenebrio-
noidea are generally referred to as wireworms. Most wireworms inhabit humid soil,
humus layer or decayed wood and are, thus, easily encountered and infected with
entomopathogenic fungi (Kabaluk et al. 2017; Rogge et al. 2017).
Cordyceps sensu lato (Hypocreales, Sordariomycetes) is a well-known group of en-
tomopathogenic fungi. Previously, most species of this group were assigned to the previ-
ous Cordyceps Fr. genus, so they had commonly been called ‘Cordyceps’. It was not until
2007 that Sung et al. revised the classication system of this group, based on substantial
molecular and morphological data. In the new classication system, all these fungi are
assigned to three families (Cordycipitaceae, Ophiocordycipitaceae and, in part, Clavi-
cipitaceae) and only a few species were retained in the revised Cordyceps Fr. emend. G.H.
Sung et al. genus (Sung et al. 2007). As a result, the concept of ‘Cordyceps’ has been
extended from the previous genus Cordyceps Fr. to Cordyceps s.l. So far, more than 1000
Cordyceps s.l. species have been reported (Wei et al. 2020) and these entomopathogenic
hypocrealean fungi are widely distributed in all terrestrial regions (except Antarctica),
especially tropics and subtropics (Kobayasi 1941; Sung et al. 2007).
Ophiocordyceps Petch and Polycephalomyces Kobayasi are two morphologically, phy-
logenetically and ecologically closely-related genera placed in Ophiocordycipitaceae.
ey produce rigid, pliant or wiry stipes that are usually darkly coloured; their asexual
morphs are mainly Hirsutella-like, but phialides of Polycephalomyces lack the swollen
base and are concentrated at the tips of synnemata; and they are typically found on
hosts buried in soil or in rotting wood, especially wireworms (Sung et al. 2007; Kepler
et al. 2013). Ophiocordyceps is the largest genus of Cordyceps s.l., with O. blattae (Petch)
Petch as the type species, linking with Didymobotryopsis-, Hirsutella-, Hymenostilbe-,
Sorosporella-, Synnematium- and Troglobiomyces-like asexual states (Quandt et al. 2014)
and currently comprising approximately 200 species (Wei et al. 2020). Polycephalomy-
ces, with P. formosus Kobayasi as its type and linking with Acremonium-, Hirsutella- and
Polycephalomyces-like asexual states, includes 19 known species thus far, some of which
are found on stromata of Ophiocordyceps spp. (Kepler et al. 2013; Wang 2016; Index
Fungorum 2021).
In nature, Cordyceps s.l. species develop mainly on insects, spiders, other Cordyceps
s.l. species and hypogeous fungi of the genus Elaphomyces. ese ascomycetes can re-
produce via ascospores, conidia and mycelia that generally inhabit soil, plants, inver-
tebrates, nematodes, mushrooms and other organisms (Zha et al. 2020). e ecology
and habits of dierent host groups are generally dierent and this often determines the
species specicity of Cordyceps s.l. on them. As a result, in practice, Cordyceps s.l. species
Cordyceps species on wireworms 81
have commonly been classied according to their host groups. With respect to the tax-
onomy of Cordyceps s.l. on insects, early systematic work mainly came from Petch (e.g.
1934), Kobayasi (e.g. 1941) and Shimizu (1997) who all classied Cordyceps s.l. species
according to their host orders. Later, Shrestha et al. (2016, 2017) reviewed Cordyceps
s.l. species on their Coleoptera, Lepidoptera, Hymenoptera and Hemiptera hosts. Re-
cently, Zha et al. (2020) systematically studied the Orthoptera hosts and investigated
the relationships with their pathogens.
A diverse range of Cordyceps s.l. species have been reported as pathogens of wire-
worms. Due to the diculities in identifying wireworms, hosts of these fungal species
have generally been recorded as Elateridae larvae, Tenebrionidae larvae or Coleoptera
larvae (e.g. Petch 1933, 1937; Kobayasi 1941; Kobayasi and Shimizu 1982b, 1983).
Shimizu (1997) provided beautiful drawings for many Cordyceps s.l. species, which in-
cluded more than 30 species on wireworms and wireworm-like insects. A recent report
for wireworm-infecting Cordyceps s.l. involved only 20 species (Shrestha et al. 2016),
which is fewer than the number recorded by Shimizu (1997). It should be noticed that
these fungi aect the populations of wireworms and have the potential to control these
agricultural pests (Barsics et al. 2013; Rogge et al. 2017). erefore, we need a deeper
knowledge of species diversity, taxonomy, distribution and lifestyle of these wireworm-
infecting Cordyceps s.l.
In this study, the species diversity of wireworm-infecting Cordyceps s.l. (Elateroidea
and Tenebrionoidea) is reviewed. We discuss their hosts and geographic distribution
and provide taxonomic notes for species. In addition, we describe two new members
of this group, Ophiocordyceps borealis sp. nov. and O. spicatus sp. nov. Polycephalomyces
formosus Kobayasi is also described because it represents the rst report of this species
on wireworms (Elateroidea). We reconstructed a multilocus (SSU, LSU and TEF1-α)
phylogeny to support morphological results.
Material and methods
Sample collections and morphological studies
Wireworm-infecting species of Cordyceps s.l. were collected from south-western China
and the Russian Far East. Specimens were placed in plastic boxes and carried to the
laboratory for further study. e macro-characteristics and ecology were photographed
using a Nikon Coolpix P520 camera in the eld. Specimens were examined and pho-
tographed using an Optec SZ660 stereo dissecting microscope and a Nikon Eclipse
80i compound microscope connected with a Canon EOS 600D camera. Microscopic
measurements were made using Tarosoft (R) Image Framework software. Images were
processed using Adobe Photoshop CS v. 8.0.1 (Adobe Systems Incorporated, San Jose,
California, USA). Voucher specimens are deposited in the Fungarium of the Centre
of Excellence in Fungal Research, Mae Fah Luang University (MFLU), Chiang Rai,
ailand and the Herbarium of Guizhou University (GACP), Guiyang, China.
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
82
DNA extraction, sequencing, sequence assembly and alignment
Total DNA was extracted from dried specimens using E.Z.N.A.TM Fungal DNA
MiniKit (Omega Biotech, CA, USA). e ribosomal internal transcribed spacers (ITS),
small and large subunits (SSU and LSU) and translation elongation factor 1α (TEF1-α)
genes were amplied and sequenced using the PCR programmes and primer pairs listed
in Table 1. PCR amplication reactions were performed in an ABI 2720 thermal cy-
cler (Applied Biosystems, Foster City, CA, USA). PCR products were puried using
Bioteke’s Purication Kit (Bioteke Corporation, Beijing, China) and were sequenced
using an ABI 3730 DNA analyser and an ABI BigDye 3.1 terminator cycle sequencing
kit (Sangon Co., Shanghai, China). Sequences were aligned and assembled visually and
manually using Clustalx1.81, Chromas230, ContigExpress and MEGA6 software.
Construction of molecular phylogenetic trees
BLAST searches were performed to reveal the closest matches in the GenBank data-
base that would allow the selection of appropriate taxa for phylogenetic analyses. Each
gene region was independently aligned and improved manually, then the SSU, LSU and
TEF1-α gene sequences were combined to form a concatenated dataset. e ITS region
was not included in our multilocus analyses because of: 1) insucient ITS sequence
data (Table 2) which may lead to inaccurate phylogenetic results; 2) distinct dierent
rate of evolution from SSU, LSU and TEF genes and with many irregular insertions and
deletions of bases. Maximum Likelihood (ML), Maximum Parsimony (MP) and Bayes-
ian Inference (BI) analyses were performed using the concatenated sequence dataset.
Sequence information of the three described species and their allies is listed in Table 2.
Maximum Likelihood (ML) analysis was done via the CIPRES Science Gate-
way platform (Miller et al. 2010) using RAxML-HPC2 on XSEDE (8.2.10) with the
GTRGAMMA nucleotide substitution model and 1000 bootstrap iterations (Jeewon
et al. 2003; Hongsanan et al. 2017). An MP tree was constructed with PAUP* 4.0b10
(Swoord 2002) using the heuristic search option with TBR branch swapping and
bootstrapping with 1,000 replicates (Cai et al. 2006; Tang et al. 2007). BI analysis
was conducted using MrBayes v. 3.1.2 with Markov Chain Monte Carlo sampling to
Table 1. Primers and PCR programmes used in this study (White et al. 1990, Spatafora et al. 2006, Ban
et al. 2015).
Locus Primers PCR programs (optimised)
ITS ITS4: 5’-TCCTCCGCTTATTGATATGC-3’ (94 °C for 30 s, 51 °C for 50 s, 72 °C for 45 s) × 33 cycles
ITS5: 5’-GGAAGTAAAAGTCGTAACAAGG-3’
SSU NS1: 5’-GTAGTCATATGCTTGTCTC-3’ (94 °C for 30 s, 51 °C for 30 s, 72 °C for 2 min) × 33 cycles
NS4: 5’-CTTCCGTCAATTCCTTTAAG-3’
LSU LROR: 5’-ACCCGCTGAACTTAAGC-3’ (94 °C for 30 s, 55 °C for 30 s, 72 °C for 1 min) × 30 cycles
LR5: 5’-TCCTGAGGGAAACTTCG-3’
TEF1-αEF1-983F: 5’-GCYCCYGGHCAYCGTGAYTTYAT-3’ (94 °C for 1 min, 55 °C for 30 s, 72 °C for 2 min) × 35 cycles
EF1-2218R: 5’-ATGACACCRACRGCRACRGTYTG-3’
Cordyceps species on wireworms 83
Table 2. Sequence information of samples used in this study. Our sequencing results are displayed in bold.
Fungal species Specimen/ strain No. Host/substratum ITS SSU LUS TEF1–αReferences
Cordyceps militaris (outgroup) OSC 93623 Lepidoptera (larva) JN049825 AY184977 AY184966 DQ522332 Kepler et al. (2012)
Ophiocordyceps annulata CEM303 Coleoptera – KJ878915 KJ878881 KJ878962 Quandt et al. (2014)
O. aphodii ARSEF 5498 Coleoptera – DQ522541 DQ518755 DQ522323 Spatafora et al. (2007)
O. borealis sp. nov. MFLU 18-0163 Coleoptera: Elateroidea (larva) MK863251 MK863044 MK863051 MK860189 is study
GACP R16002 Coleoptera: Elateroidea (larva) MK863252 MK863045 MK863052 MK860190
GACP R16003 Coleoptera: Elateroidea (larva) MK863253 MK863046 MK863053 MK860191
O. clavata NBRC 106962 Coleoptera (larva) JN943328 JN941726 JN941415 AB968587 Schoch et al. (2012)
O. cossidarum MFLU 17-0752 Lepidoptera (larva) – MF398186 MF398187 MF928403 Hyde et al. (2018)
O. entomorrhiza KEW 53484 Lepidoptera JN049850 EF468954 EF468809 EF468749 Quandt et al. (2014)
O. formosana MFLU 15-3889 Tenebrionoidea (larva) – – – KU854950 Li et al. (2016)
O. formosana MFLU 15-3888 Tenebrionoidea (larva) – KU854951 –KU854949 Li et al. (2016)
O. konnoana EFCC 7315 Coleoptera (larva) – EF468959 –EF468753 Sung et al. (2007)
O. lanpingensis YHOS0707 Lepidoptera: Hepialidae (larva) – KC417459 KC417461 KC417463 Chen et al. (2013)
O. longissima NBRC 108989 Hemiptera (cicada nymph) AB968407 AB968394 AB968421 AB968585 Sanjuan et al. (2015)
O. macroacicularis NBRC 105888 Lepidoptera (larva) AB968401 AB968389 AB968417 AB968575 Ban et al. (2015)
O. melolonthae OSC 110993 Coleoptera: Scarabeidae (larva) – DQ522548 DQ518762 DQ522331 Spatafora et al. (2007)
O. nigra TNS 16252 Hemiptera – KJ878941 KJ878906 KJ878986 Quandt et al. (2014)
O. nigrella EFCC 9247 Lepidoptera (larva) JN049853 EF468963 EF468818 EF468758 Sung et al. (2007)
O. purpureostromata TNS F18430 Coleoptera – KJ878931 KJ878897 KJ878977 Quandt et al. (2014)
O. ravenelii OSC 110995 Coleoptera (larva) – DQ522550 DQ518764 DQ522334 Spatafora et al. (2007)
O. robertsii KEW 27083 Lepidoptera: Hepialidae (larva) AJ309335 –EF468826 EF468766 Sung et al. (2007)
O. sinensis EFCC 7287 Lepidoptera (pupa) JN049854 EF468971 EF468827 EF468767 Sung et al. (2007)
O. sobolifera NBRC 106967 Hemiptera (cicada nymph) AB968409 AB968395 AB968422 AB968590 Ban et al. (2015)
O. spicatus sp. nov. MFLU 18-0164 Coleoptera: Tenebrionoidea (larva) MK863254 MK863047 MK863054 MK860192 is study
O. variabilis OSC 111003 Diptera (larva) – EF468985 EF468839.EF468779 Sung et al. (2007)
O. xuefengensis GZUH2012HN19 Lepidoptera: Endoclita nodus (larva) KC631803 KC631788 –KC631794 Wen et al. (2013)
Paraisaria amazonica Ophama2026 Orthoptera: Acrididae (nymph) – KJ917562 KJ917571 KM411989 Sanjuan et al. (2015)
P. coenomyiae NBRC 108993 Diptera: Coenomyia (larva) AB968396 AB968384 AB968412 AB968570 Ban et al. (2015)
P. gracilis EFCC 8572 Lepidoptera (larva) JN049851 EF468956 EF468811 EF468751 Kepler et al. (2012)
P. heteropoda OSC106404 Hemiptera (cicada nymph) – AY489690 AY489722 AY489617 Castlebury et al. (2004)
Polycephalomyces formosus MFLU 18-0162 Ophiocordyceps sp. (stroma) on an Elateroidea larva MK863250 MK863043 MK863050 MK860188 is study
P. formosus ARSEF 1424 Coleoptera KF049661 KF049615 KF049634 DQ118754 Chaverri et al. (2005)
P. lianzhouensis GIMYY9603 Lepidoptera EU149922 KF226249 KF226250 KF226252 Wang et al. (2014)
P. ramosopulvinatus EFCC 5566 Hemiptera KF049658 –KF049627 KF049682 Kepler et al. (2013)
P. sinensis CN 80-2 O. sinensis (stroma) HQ832884 HQ832887 HQ832886 HQ832890 Wang et al. (2012)
P. tomentosus BL 4 Trichiales KF049666 KF049623 KF049641 KF049697 Kepler et al. (2013)
P. yunnanensis YHHPY1006 O. nutans (stroma) KF977849 – – KF977851 Wang et al. (2015)
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
84
calculate posterior probabilities (PP) (four simultaneous Markov chains running for
1,000,000 generations; sampling every 100 generations, rst 25% of sampled trees
discarded) (Rannala and Yang 1996).
Results
Molecular phylogeny of the three described species
e combined concatenated dataset included 36 samples including 32 species of
Ophiocordycipitaceae (Ophiocordyceps, Paraisaria and Polycephalomyces) as ingroups
and Cordyceps militaris (L.) Fr. (strain OSC 93623, Kepler et al. 2012) as the outgroup.
e aligned dataset was deposited in the TreeBASE database (http://purl.org/phylo/
treebase/phylows/study/TB2:S26977?x-access-code=cb3474ce0fd0327526b6fd2465
d6c53d&format=html). e aligned dataset was composed of 2,843/2,837 (includ-
ing/excluding outgroup) characters (including gaps), of which 740/681 were variable
and 527/520 were parsimony-informative. ML, MP and BI analyses resulted in phy-
logenies with similar topologies and the best-scoring ML tree (–lnL= 15804.4393) is
shown in Fig. 1.
According to the phylogenetic tree (Fig. 1), three Ophiocordyceps borealis sp. nov.
samples (specimens MFLU 18-0163, GACP R16002 and GACP R1600) group to-
gether (100% ML/100% MP/1.00 PP) and are related to, but phylogenetically dis-
tinct from, O. purpureostromata (specimen TNS F18430). Ophiocordyceps spicatus sp.
nov. (specimen MFLU 18-0164) constitutes a strongly supported independent lineage
and is related to O. formosana. e two Polycephalomyces formosus samples (specimens
MFLU 18-0162 and ARSEF 1424) group together and are related to P. sinensis (speci-
men CN 80-2) and P. tomentosus (specimen BL 4).
New species and new record of Cordyceps s.l. developing on wireworms
Ophiocordyceps borealis L.S. Zha & P. Chomnunti, sp. nov.
Index Fungorum number: IF558114
Facesoungi number: FoF04101
Fig. 2
Etymology. Referring to the region (south of boreal zone of the Russian Far East) from
where the species was collected.
Sexual morph. Parasitising Elateroidea larvae (Coleoptera) living in fallen wood.
e larvae are cylindrical, 11 mm long and 1.1–1.3 mm thick, yellowish-brown; their
body cavity stued with milky yellow mycelia and their intersegmental membranes
covered with many milky yellow and occulent funiculi. Stromata arising from any
part of larval body, single or paired, unbranched. Stipe grey, slender and cylindrical,
brous and exible, curved more or less, 10–13 mm long and 0.25–0.6 mm thick, sur-
Cordyceps species on wireworms 85
Figure 1. Maximum Likelihood (ML) tree of Ophiocordyceps borealis sp. nov., O. spicatus sp. nov. and
their allies inferred from a combined SSU, LSU and TEF1-α gene dataset. Bootstrap support values of
ML and Maximum Parsimony (MP) > 60% and posterior probabilities (PP) of Bayesian Inference > 0.9,
are indicated above the nodes and separated by ‘/’ (ML/MP/PP).
face relatively smooth but with many longitudinal wrinkles, apex pointed. Fertile part
irregularly attached on one side of the surface of distal part of stipe, which resembles a
mass of insect eggs that are clustered together or separated into several lumps; substrate
layer milky white, surface milky yellow accompanied by lavender and dotted with
numerous black ostioles. Perithecia immersed, densely arranged, obliquely or at right
angles to the surface of stipe, pyriform, neck unconspicuous, 220–290 × 120–150 µm
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
86
Figure 2. Ophiocordyceps borealis a–c stromata arising from the dierent parts of larval bodies d apical
ends of stromata e transverse section of fertile part, on which densely arranged perithecia are shown f asci
g ascospores. Scale bars: 2 mm (a–c); 1 mm (d); 100 µm (e), 10 µm (f, g).
Cordyceps species on wireworms 87
and their tops obtuse; walls dark brown and 25–32 µm thick; ostioles slightly thick-
ened and slightly protruding over the surface of fertile part. Asci cylindrical, 6–8 µm
in diameter; caps hemispherical, 5–6 (x
– = 5.5, n = 30) µm wide and 3.5–5 (x
–=4.2, n
= 30) µm high. Ascospores liform and elongate, multi-septate (far more than 3), not
easy to break into part-spores; part-spores cylindrical, truncated at both ends, 10–15
(x
–=12.2, n = 30) × 2 µm. Asexual morph. Unknown.
Material examined. R, the Russian Far East, Primorskiy Krai, National Park
Land of the Leopard, Natural Reserve Kedrovaya Pad, 43°05'53.8"N, 131°33'17.8"E,
10 August 2016, Oksana Tomilova & Vadim Yu Kryukov (MFLU 18-0163, holotype;
GACP R16002 and GACP R16003, paratypes).
Known distribution. Russia (Primorskiy Krai).
Hosts. Growing on Elateroidea larvae (Coleoptera) living in fallen wood in a de-
ciduous forest.
Notes. e new species is morphologically similar to O. purpureostromata (≡ C.
purpureostromata), but their stipes and ascospores are distinct. In O. purpureostromata,
stipe is thicker (0.6–1 mm in diameter) and has hairs (0.25–0.6 mm in diameter and
without hair in O. borealis), ascospores are only 65–75 × 10 µm long and 3-septate
(elongate and far more than 3-septate in O. borealis) and part-spores are 13–23 µm
long (10–15 µm long in O. borealis) (Kobayasi and Shimizu 1980b).
Nucleotide sequences of O. borealis are most similar to those of O. purpureostro-
mata (specimen TNS F18430, Quandt et al. 2014), but there is 2.3% bp dierence
across the 804 bp in TEF1-α, 0.5% bp dierence across the 845 bp in LSU and 0.1%
bp dierence across 1,061 bp in SSU. ITS of O. borealis is > 14.1% dierent to all
ITS available in GenBank (ITS are not available for O. purpureostromata). On the
phylogenetic tree, the new species is also nearest (100% ML/100% MP/1.00 PP) to O.
purpureostromata, but they form into two distinct branches which support them being
two separate species (Fig. 1).
Ophiocordyceps spicatus L.S. Zha & P. Chomnunti, sp. nov.
Index Fungorum number: IF558115
Facesoungi number: FoF04102
Fig. 3
Etymology. Referring to the spicate fertile head.
Sexual morph. Parasitising a Tenebrionoidea larva (Coleoptera) living in humid
and decayed wood. e larva is cylindrical, 7.5 mm long and 1.0–1.1 mm thick, yel-
lowish-brown. White mycelia stu the body cavity, also partially cover the interseg-
mental membranes of the body surface. Stroma arising from the rst quarter of the
larval body, single, eshy, 5 mm in length. Stipe yellow, cylindrical, 3.5 mm long and
0.35–0.4 mm thick, surface rough and pubescent. Fertile head spicate, unbranched,
orange, 1.5 mm long and 0.5–0.7 mm thick, obviously dierentiated from stipe; its
surface rugged and consisting of many humps (outer portions of perithecia), tops of
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
88
Figure 3. Ophiocordyceps spicatus (MFLU 18-0164) a infected larva in decayed wood b habitat environ-
ment c fertile head of stroma d transverse section of fertile head, on which sparse arranged perithecia are
shown e Asci f Ascospores and part-spores. Scale bars: 200 µm (c); 100 µm (d) 10 µm (e, f).
Cordyceps species on wireworms 89
the humps obtuse and with opening ostioles, darker in colour. Perithecia partially im-
mersed and obliquely or at right angles to the surface of stipe, broadly pyriform, 200–
250 × 170–200 µm; walls 25–35 µm thick. Asci cylindrical, 5–9 µm thick, middle part
wider than two terminal parts; caps hemispheric, 4.6–5.3 (x
– = 4.9, n = 30) µm wide
and 4.0–4.6 (x
– = 4.3, n = 30) µm high. Ascospores liform; part-spores cylindrical, trun-
cated at both ends, 3.5–6.5 (x
– = 4.7, n = 30) µm long and 1.7–2.0 µm thick. Asexual
morph. Unknown.
Material examined. C, Guizhou Province, Leishan County, Leigongshan
Mountain, 26°22'18"N, 108°11'28"E, 1430 m alt., 2 August 2016, Ling-Sheng Zha
(MFLU 18-0164, holotype).
Known distribution. China (Guizhou).
Host. Growing on a Tenebrionoidea larva (Coleoptera) living in humid and de-
cayed wood in a broad-leaved forest.
Notes. Ophiocordyceps spicatus is morphologically somewhat similar to O. for-
mosana (Kobayasi and Shimizu 1981; Li et al. 2016), but it has a much smaller stroma
(stipes 6–10 (or 19–37) mm long and 1.5–1.7 (or 2–4) mm wide in O. formosana), a
spicate and rugged fertile head (surface entire and attened, never spicate or rugged in
O. formosana) and partially immersed perithecia (immersed in O. formosana).
Nucleotide sequences of O. spicatus are most similar to those of O. formosana,
but there is 5.2% bp dierence in ITS, 2.0% bp dierence in TEF1-α and 0.1% bp
dierence in SSU (LSU rDNA sequence unavailable for O. formosana). LSU of O.
spicatus is > 5.6% bp dierent to all LSU available in GeneBank. Additionally, on the
phylogenetic tree, O. spicatus is closely related (100% ML/100% MP/1.00 PP) to O.
formosana, but they form into two distinct branches which also support them being
two separate species (Fig. 1).
Polycephalomyces formosus Kobayasi
MycoBank No: 289806
Facesoungi number: FoF04100
Fig. 4
Remarks. Polycephalomyces formosus was reported on Coleoptera larvae, stromata of
Ophiocordyceps barnesii (waites) G.H. Sung et al., O. falcata (Berk.) G.H. Sung et
al. and O. cantharelloides (Samson & H.C. Evans) G.H. Sung et al. and distributed in
Ecuador, Japan and Sri Lanka (Kobayasi 1941; Samson and Evans 1985; Wang 2016).
We collected a P. formosus-like specimen on the stroma of Ophiocordyceps sp. on an
Elateroidea larva from Guizhou, China. Morphological and phylogenetic data showed
that it is P. formosus. is is the rst report of P. formosus on wireworms.
Asexual morph. Growing on the stroma of Ophiocordyceps sp. on an Elateroidea
larva. Stroma single, arising from the body end of the host larva, unbranched. e larva
reddish-brown, cylindrical, 21 × 1.3–1.6 mm, intersegmental membranes conspicu-
ous. Stipe of the stroma shiny black, sti, band-like, but twisted and deeply wrinkled
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
90
Figure 4. Polycephalomyces formosus (MFLU 18-0162) a collected on the ground in a bamboo forest
b produced on the stroma of Ophiocordyceps sp. (the fertile head was missing) on an Elateroidea larva
c, d synnemata e–g A-type phialides and A-type conidia h B-type phialides and B-type conidia. Scale
bars: 20 µm (e); 5 µm (f); 10 µm (g, h).
(dry specimen), more than 20 mm long and 1.0–1.3 mm thick, surface smooth (the
fertile head was missing). Synnemata solitary or caespitose, arising from the interseg-
mental membranes of the larva and the surface of the stroma, mostly unbranched,
generally straight, capitate, 1–3.5 mm long and 50–600 µm thick. Stipe basally broad
and compressed, then gradually cylindrical upwards, white, greyish-white to yellow-
ish-brown, surface smooth. Fertile head (including spore mass) abruptly expanded,
ellipsoidal, 100–300 × 80–250 µm, located at the top of every synnema and distinctly
separated from the stipe. Spore mass covers the surface of every fertile head, 15–25 µm
Cordyceps species on wireworms 91
thick, yellowish-brown and composed of hymenia. Phialides of two types, A-phialides
produced on fertile heads, B-phialides arising laterally along the entire stipe. A-phi-
alides 3–5 in terminal whorl on basal conidiophores, cylindrical to narrowly conical,
straight or curved, non-uniform, 10–20 (x
– = 15.1, n = 30) µm long and 1.5–2 µm
(x
–=1.7, n=30) wide, basally and terminally narrow, neck narrow to 0.5 µm, collar-
ettes and periclinal thickening not visible; A-conidia obovate to obpyriform, smooth-
walled, hyaline, 2.1–3.2 (x
– = 2.6, n = 30) µm long and 1.5–2.2 (x
– = 1.8, n = 30) µm
wide. B-phialides single or in terminal whorls of 2–3 on basal conidiophores, straight,
symmetrical or asymmetrical, hyaline, generally cylindrical, 10–25 (x
– = 17, n = 30) µm
long, 2–3.5 (x
– = 2.8, n = 30) µm thick at the base, 0.5–0.8 (x
– = 0.65, n =30) µm thick
at the end, collarettes and periclinal thickening not visible; B-conidia fusiform, hyaline,
smooth-walled, 3.2–6.0 (x
– = 4.6, n = 30) µm long and 1–1.8 (x
– = 1.4, n = 30)µm
wide. Sexual morph. Not observed.
Material examined. CHINA, Guizhou, Tongzi County, Baiqing Natural Reserve,
28°52'31"N, 107°9'10"E, about 1300 m alt., 13 July 2016, Ling-Sheng Zha (MFLU
18-0162).
Notes. Polycephalomyces formosus was originally described from Japan as: growing on
Coleoptera larvae; synnemata solitary or caespitose, 1–3.5 mm long and 100–250 µm
thick; spore mass covering the surface of the fertile head, 15–25 µm thick; A-phialides
3–4 in terminal whorl on basal conidiophores, cylindrical to narrowly conical, 10–20
× 1.5–2 µm, neck 0.5 µm; A-conidia obovate to obpyriform, 2.0–2.8 × 1.6–2.0 µm;
B-conidia fusiform, 3.2–4.8 × 0.8–1.6 µm (Kobayasi 1941; Wang 2016). ese charac-
teristics are all consistent with our specimen. Sequences of SSU, ITS, LSU and TEF1-α
are all identical to those of P. formosus (specimen ARSEF 1424); and in our phylogenetic
tree, these two samples grouped together and have a same branch length (Fig. 1).
Host and ecology. On the stroma of Ophiocordyceps sp. on an Elateroidea larva on
the ground in a humid bamboo (Chimonobambusa quadrangularis (Franceschi) Maki-
no) forest in Guizhou karst regions.
e larva might live in soil or decayed wood at rst, but was then infected by
Ophiocordyceps sp. and produced a sexual stroma. Following heavy rainfall, the host,
together with the stroma of Ophiocordyceps sp., was washed away and exposed on the
ground and at last, was parasitised by Polycephalomyces formosus. e fertile head of the
stroma might have been lost during the oods.
Annotated list of recorded Cordyceps s.l. species developing on wireworms
Order Hypocreales Lindau
Family Cordycipitaceae Kreisel ex G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora
Akanthomyces lecanii (Zimm.) Spatafora, Kepler & B. Shrestha
≡ Cephalosporium lecanii Zimm.
≡ Verticillium lecanii (Zimm.) Viégas
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
92
≡ Lecanicillium lecanii (Zimm.) Zare & W. Gams
= Cephalosporium lecanii f. coccorum (Petch) Bałazy
= Sporotrichum lichenicola Berk. & Broome
= Hirsutella confragosa Mains
= Torrubiella confragosa Mains
= Cordyceps confragosa (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora
= Cephalosporium coccorum Petch
= Verticillium coccorum (Petch) Westerd.
= Cephalosporium coccorum var. uredinis U.P. Singh & Pavgi
= Cephalosporium subclavatum Petch
For further doubtful synonyms, see Zare and Gams (2001).
Hosts. Spiders, insects from various orders, including Coleoptera (e.g. Tenebrionidae:
Alphitobius diaperinus); inhabiting phytopathogenic fungi and plant-parasitic nema-
todes (Humber and Hansen 2005; Shinya et al. 2008).
Distribution. Widely distributed in tropical and temperate regions, for example:
Dominican Republic, Jamaica, Indonesia, Peru, Sri Lanka, the West Indies, Turkey
and USA (Zare and Gams 2001).
Notes. e species was originally and frequently reported on scale insects (Hemip-
tera: Coccidae (syn. Lecaniidae)) (Zare and Gams 2001). Humber and Hansen (2005)
listed its hosts involving spiders, many insect orders and found on the mushroom
Puccinia striiformis (Pucciniaceae). e species was also found on phytopathogenic
fungi and plant-parasitic nematodes (Shinya et al. 2008). Zare and Gams (2001) sys-
tematically studied the species and listed its synonyms. Kepler et al. (2017) rejected
Torrubiella and Lecanicillium and transferred the species to Akanthomyces.
Beauveria bassiana sensu lato
Hosts. Many insect orders, including Coleoptera (e.g. Elateroidea and Tenebrionoidea
spp., Humber and Hansen 2005; Reddy et al. 2014; Sufyan et al. 2017); inhabiting
soil, plant surfaces and plant internal tissues (Bamisile et al. 2018).
Distribution. Widely distributed.
Note. Beauveria bassiana sensu lato includes a large complex of cryptic species with
wide host ranges, including many Coleoptera families (Rehner et al. 2011; Imoulan
et al. 2017).
Cordyceps aurantiaca Lohwag
Hosts. Elateridae larvae (Keissler and Lohwag 1937).
Known distribution. China (Keissler and Lohwag 1937).
Note. Taxonomically uncertain species which was described from the previous Cordyceps
Fr. (diers from the current Cordyceps Fr. emend. G.H. Sung et al., same as below).
Cordyceps species on wireworms 93
Cordyceps chiangdaoensis Tasanathai, anakitpipattana, Khonsanit & Luangsa-ard
Hosts. Elateroidea or Tenebrionoidea larvae.
Known distribution. ailand (Tasanathai et al. 2016).
Note. Hosts of the species were recorded as Coleoptera larvae (Tasanathai et al.
2016). According to the picture provided, the hosts are wireworms.
Cordyceps chishuiensis Z.Q. Liang & A.Y. Liu
Host. Elateroidea or Tenebrionoidea larva.
Known distribution. China (Guizhou) (Liang 2007).
Notes. Taxonomically uncertain species from the previous Cordyceps. e species
was originally reported on a wireworm (Liang 2007).
Cordyceps farinosa (Holmsk.) Kepler, B. Shrestha & Spatafora
≡ Ramaria farinosa Holmsk.
≡ Clavaria farinosa (Holmsk.) Dicks.
≡ Corynoides farinosa (Holmsk.) Gray
≡ Isaria farinosa (Holmsk.) Fr.
≡ Spicaria farinosa (Holmsk.) Vuill.
≡ Penicillium farinosum (Holmsk.) Biourge
≡ Paecilomyces farinosus (Holmsk.) A.H.S. Br. & G. Sm.
For further doubtful synonyms, see Index Fungorum (2021).
Hosts. Mites, spiders, insects from various orders, including Coleoptera (e.g. Tenebri-
onidae spp.); inhabiting soil, humus, plants, fungi and other organisms (Humber and
Hansen 2005; Zimmermann 2008).
Distribution. Widely distributed (Zimmermann 2008).
Note. According to Domsch et al. (1980) and Zimmermann (2008), the species is
ubiquitous in temperate and tropical zones.
Cordyceps fumosorosea (Wize) Kepler, B. Shrestha & Spatafora
≡ Isaria fumosorosea Wize
≡ Spicaria fumosorosea (Wize) Vassiljevsky
≡ Paecilomyces fumosoroseus (Wize) A.H.S. Br. & G. Sm.
= Paecilomyces fumosoroseus var. beijingensis Q.X. Fang & Q.T. Chen
Hosts. Mites, insects from various orders (e.g. Lagriidae and Tenebrionidae spp. in
Tenebrionoidea) (Humber and Hansen 2005; Zimmermann 2008).
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
94
Distribution. Widely distributed (Zimmermann 2008).
Note. e species was previously confused with C. farinosa or regarded as a com-
plex species (Zimmermann 2008).
Cordyceps huntii Giard [as ‘hunti’, ‘lunti’]
Host. Elateridae larva (Massee 1899).
Known distribution. Gaul (Massee 1899).
Notes. Taxonomically uncertain species from the previous Cordyceps. Sung et al.
(2007) treated it as a synonym of Nigelia martiale (≡ C. martialis).
Cordyceps militaris (L.) Fr.
≡ Clavaria militaris L.
≡ Sphaeria militaris (L.) J.F. Gmel.
≡ Hypoxylon militare (L.) Mérat
≡ Xylaria militaris (L.) Gray
≡ Corynesphaera militaris (L.) Dumort.
≡ Torrubia militaris (L.) Tul. & C. Tul.
= Clavaria granulosa Bull.
= Sphaeria militaris var. sphaerocephala J.C. Schmidt
= Cordyceps militaris f. sphaerocephala (J.C. Schmidt) Sacc.
= Cordyceps militaris f. alba Kobayasi & Shimizu ex Y.J. Yao [as ‘albina’]
Hosts. Commonly on Lepidoptera larvae and pupae, infrequently on Hymenoptera
(Kobayasi 1941; Kryukov et al. 2011).
Distribution. Widely distributed.
Note. Under laboratory conditions and injection of hyphal bodies into the haemo-
coel of insects, C. militaris can infect many insect orders (Shrestha et al. 2012), in-
cluding pupae of Tenebrio molitor (Tenebrionidae) (De Bary 1867; Sato and Shimazu
2002). erefore, the conclusion that wireworms (e.g. Tenebrio molitor) are the natural
hosts of C. militaris is probably untenable and we temporarily reject it.
Cordyceps nanatakiensis Kobayasi & Shimizu
Host. Tenebrionidae larva (Shimizu 1997).
Known distribution. Japan (Kobayasi and Shimizu 1983).
Notes. Taxonomically uncertain species from the previous Cordyceps. Its host
was originally recorded as a Coleoptera larva (Kobayasi and Shimizu 1983) and then
Shimizu (1997) identied it as a Tenebrionidae larva.
Cordyceps species on wireworms 95
Cordyceps nirtolii Negi, Koranga, Ranj. Singh & Z. Ahmed
Host. Larva of Elateridae (Melanotus communis (Gyllenhal)).
Known distribution. India (Himalaya) (Negi et al. 2012).
Note. Host of the species was recorded as a larva of Melanotus communis (Negi et
al. 2012). Melanotus communis (Gyllenhal) represents an Elateridae insect, while Mel-
anotus communis E. Horak is a mushroom (Agaricales: Strophariaceae).
Cordyceps roseostromata Kobayasi & Shimizu
Host. Tenebrionidae larva (Shimizu 1997).
Known distribution. Japan (Kobayasi and Shimizu 1983).
Note. Host of the species was originally recorded as a Coleoptera larva (Kobayasi
and Shimizu 1983) and then Shimizu (1997) identied it as a Tenebrionidae larva.
Cordyceps rubiginosistipitata Kobayasi & Shimizu [as ‘rubiginosostipitata’]
Host. Tenebrionoidea or Elateroidea larva.
Known distribution. Japan (Kobayasi and Shimizu 1983).
Note. Taxonomically uncertain species from the previous Cordyceps. Its host was
recorded as a Coleoptera larva (Kobayasi and Shimizu 1983; Shimizu 1997). Accord-
ing to the illustration by Shimizu (1997), the host is a wireworm.
Cordyceps rubra Möller
Host. Elateridae larva (Möller 1901).
Known distribution. Brazil (Möller 1901).
Note. Taxonomically uncertain species from the previous Cordyceps.
Cordyceps shanxiensis B. Liu, Rong & H.S. Jin
Hosts. Elateridae larvae (Melanotus caudex? and Pleonomus canaliculatus?) (Liu et al.
1985).
Known distribution. China (Shanxi) (Liu et al. 1985).
Notes. Taxonomically uncertain species from the previous Cordyceps. According
to the original description, the species is morphologically similar to Paraisaria gracilis
(Grev.) Luangsa-ard et al. on Lepidoptera larvae. Notably, the two host names pro-
vided by Liu et al. (1985) cannot be retrieved in GBIF (2021).
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
96
Cordyceps submilitaris Henn.
Hosts. Elateroidea or Tenebrionoidea larvae.
Known distribution. South America (Petch 1933).
Notes. Taxonomically uncertain species from the previous Cordyceps. Hosts of the
species were recorded as beetle larvae in rotten wood (Petch 1933). Petch (1933) con-
sidered the species as a synonym of Nigelia martiale (≡ C. martialis). According to the
information given by Petch (1933), hosts of the species are wireworms.
Cordyceps velutipes Massee
Hosts. Larvae of Elateridae and Scarabaeidae (Melolontha sp.) (Massee 1895;
Moureau 1949).
Known distribution. Africa (Massee 1895).
Note. Taxonomically uncertain species from the previous Cordyceps.
Family Clavicipitaceae (Lindau) Earle ex Rogerson, emend. G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora
Metarhizium anisopliae species complex
Hosts. More than seven insect orders, including Coleoptera (e.g. Elateridae and Ten-
ebrionidae spp., Kabaluk et al. 2005, 2017; Humber and Hansen 2005; Reddy et al.
2014); inhabiting soil, plant surfaces and plant internal tissues (Hu et al. 2014; Bami-
sile et al. 2018; Brunner-Mendoza et al. 2019).
Distribution. Widely distributed.
Note. Metarhizium anisopliae species complex includes several cryptic species, for
example, M. anisopliae (Metschn.) Sorokīn, M. brunneum Petch and M. robertsii J.F.
Bisch., S.A. Rehner & Humber (Bischo et al. 2009; Kepler et al. 2014; Mongkol-
samrit et al. 2020). Amongst them, M. brunneum was most often noted as a wireworm
pathogen (e.g. Kabaluk et al. 2017).
Metarhizium atrovirens (Kobayasi & Shimizu) Kepler, S.A. Rehner & Humber
≡ Cordyceps atrovirens Kobayasi & Shimizu
≡ Metacordyceps atrovirens (Kobayasi & Shimizu) Kepler, G.H. Sung & Spatafora
Hosts. Tenebrionidae larvae (Shimizu 1997).
Known distribution. Japan (Kobayasi and Shimizu 1978; Shimizu 1997).
Note. Hosts of the species were originally recorded as Coleoptera larvae (Kobayasi
and Shimizu 1978) and then Shimizu (1997) identied them as Tenebrionidae larvae.
Cordyceps species on wireworms 97
Metarhizium brachyspermum Koh. Yamam., Ohmae & Orihara
Hosts. Elateridae larvae and pupae (Yamamoto et al. 2020).
Known distribution. Japan (Yamamoto et al. 2020).
Metarhizium campsosterni (W.M. Zhang & T.H. Li) Kepler, S.A. Rehner & Humber
≡ Cordyceps campsosterni W.M. Zhang & T.H. Li [as ‘campsosterna’]
≡ Metacordyceps campsosterni (W.M. Zhang & T.H. Li) G.H. Sung, J.M. Sung, Hywel-
Jones & Spatafora
Hosts. Larva and adult of Campsosternus auratus (Elateridae) (Zhang et al. 2004).
Known distribution. China (Guangdong) (Zhang et al. 2004).
Metarhizium clavatum Luangsa-ard, Mongkolsamrit, Lamlertthon, anakitpi-
pattana & Samson
Hosts. Elateridae (Oxynopterus) larvae (Mongkolsamrit et al. 2020).
Known distribution. ailand (Mongkolsamrit et al. 2020).
Metarhizium avum Luangsa-ard, Mongkolsamrit, anakitpipattana & Samson
Hosts. Tenebrionoidea or Elateroidea larvae.
Known distribution. ailand (Mongkolsamrit et al. 2020).
Note. Hosts of the species were originally recorded as Coleoptera larvae (Mong-
kolsamrit et al. 2020). According to the illustration and the information provided, the
hosts are wireworms.
Metarhizium kalasinense Tasan., Khons., anakitp., Mongkols. & Luangsa-ard
Hosts. Elateroidea larvae.
Known distribution. ailand (Luangsa-ard et al. 2017).
Note. Hosts of the species were originally recorded as elaterid larvae (Coleoptera)
(Luangsa-ard et al. 2017).
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
98
Metarhizium pseudoatrovirens (Kobayasi & Shimizu) Kepler, S.A. Rehner &
Humber
≡ Cordyceps pseudoatrovirens Kobayasi & Shimizu
≡ Metacordyceps pseudoatrovirens (Kobayasi & Shimizu) Kepler, G.H. Sung & Spatafora
Hosts. Larvae of Tenebrionoidea and/or Elateroidea (Shimizu 1997; Liang 2007).
Known distribution. China (Guizhou), Japan (Kobayasi and Shimizu 1982b; Li-
ang 2007).
Notes. e host of the species was originally recorded as a Coleoptera larva (Kob-
ayasi and Shimizu 1982b), then Shimizu (1997) identied it as a Tenebrionidae larva.
Liang (2007) recorded the species with pictures (four specimens) and wireworm hosts.
Metarhizium purpureonigrum Luangsa-ard, Tasanathai, anakitpipattana &
Samson
Hosts. Elateridae larvae (Campsosternus sp.).
Known distribution. ailand (Mongkolsamrit et al. 2020).
Notes. According to the description and pictures provided (Mongkolsamrit et al.
2020), the species is probably a synonym of O. jiangxiensis, a traditional Chinese me-
dicinal mushroom (Zha et al. 2018, also see O. jiangxiensis below). Hosts of the species,
which were recorded as Coleoptera larvae, are Elateridae larvae (Campsosternus sp.).
Metarhizium purpureum Luangsa-ard, Mongkolsamrit, Lamlertthon anakitpi-
pattana & Samson
Hosts. Elateridae (Oxynopterus) larvae (Mongkolsamrit et al. 2020).
Known distribution. ailand (Mongkolsamrit et al. 2020).
Nigelia martiale (Speg.) Luangsa-ard & anakitp.
≡ Cordyceps martialis Speg.
≡ Metacordyceps martialis (Speg.) Kepler, G.H. Sung & Spatafora
≡ Metarhizium martiale (Speg.) Kepler, S.A. Rehner & Humber
Hosts. Larvae of Coleoptera (e.g. Elateridae, Shrestha et al. 2016; Cerambycidae,
Spegazzini 1889) and Lepidoptera (Liang 2007; Kepler et al. 2012).
Known distribution. Brazil, China (Guangdong, Zhejiang, Taiwan), the West In-
dies (Kobayasi 1941; Liang 2007).
Cordyceps species on wireworms 99
Family Ophiocordycipitaceae G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora
Ophiocordyceps acicularis (Ravenel) Petch
≡ Cordyceps acicularis Ravenel
Hosts. Elateridae larvae (Shimizu 1997).
Known distribution. China (Jiangsu, Guangdong, Guizhou, Hainan, Taiwan),
Japan, Russia (Far East), U.S.A. (Carolina) (Massee 1895; Kobayasi and Shimizu
1980a, Koval 1984; Liang 2007).
Note. Hosts of the species were generally identied as wireworms or Coleoptera
larvae (Kobayasi and Shimizu 1980a, Liang 2007). Shimizu (1997) identied the hosts
of the species from Japan and Taiwan as Elateridae larvae.
Ophiocordyceps agriotis (Kawam.) G.H. Sung, J.M. Sung, Hywel-Jones & Spata-
fora [as ‘agriotidis’]
≡ Cordyceps agriota Kawam. [as ‘agriotidis’ in Index Fungorum (2021) ]
Hosts. Elateridae (e.g. Agriotes) larvae (Kobayasi and Shimizu 1980a, Shimizu 1997).
Known distribution. China (Guizhou, Jilin), Japan (Kobayasi and Shimizu
1980a, Yang 2004; Liang 2007).
Notes. e specic epithet of this species was adopted from the generic name of
its host insect ‘Agriotes’ (Kobayasi and Shimizu 1980a). e epithet ‘agriotidis’, used in
Index Fungorum (2021) and related literature (e.g. Sung et al. 2007), is incorrect. Yang
(2004) and Liang (2007) also recorded its hosts as Elateridae larvae.
Ophiocordyceps annulata (Kobayasi & Shimizu) Spatafora, Kepler & C.A. Quan-
dt [as ‘annulata’ in Index Fungorum (2021)]
≡ Cordyceps annulata Kobayasi & Shimizu [as ‘annulata’ in Index Fungorum (2021)]
Host. Tenebrionoidea or Elateroidea larva.
Known distribution. Japan (Kobayasi and Shimizu 1982a).
Note. Host of the species was originally recorded as a Coleoptera larva (Kobayasi and
Shimizu 1982a). According to the illustration by Shimizu (1997), the host is a wireworm.
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
100
Ophiocordyceps appendiculata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hy-
wel-Jones & Spatafora
≡ Cordyceps appendiculata Kobayasi & Shimizu
Host. Tenebrionidae larva (Shimizu 1997).
Known distribution. Japan (Kobayasi and Shimizu 1983).
Note. Host of the species was originally recorded as a Coleoptera larva (Kobayasi
and Shimizu 1983). Shimizu (1997) identied it as a Tenebrionidae larva.
Ophiocordyceps asyuensis (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-
Jones & Spatafora [as ‘asyuënsis’]
≡ Cordyceps asyuensis Kobayasi & Shimizu
Hosts. Elateroidea or Tenebrionoidea larva.
Known distribution. Japan (Kobayasi and Shimizu 1980b).
Note. Host of the species was originally recorded as a Coleoptera larva (Kobayasi
and Shimizu 1980b). According to the illustration by Shimizu (1997), the host is a
wireworm.
Ophiocordyceps brunneipunctata (Hywel-Jones) G.H. Sung, J.M. Sung, Hywel-
Jones & Spatafora
≡ Cordyceps brunneipunctata Hywel-Jones [as ‘brunneapunctata’]
Hosts. Elateridae larvae (Hywel-Jones 1995).
Known distribution. ailand (Hywel-Jones 1995).
Ophiocordyceps clavata (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-
Jones & Spatafora
≡ Cordyceps clavata Kobayasi & Shimizu
Hosts. Tenebrionidae larvae (Shimizu 1997).
Known distribution. Japan (Shimizu 1997).
Note. e host of the species was originally recorded as a Coleoptera larva (Kob-
ayasi and Shimizu 1980b). Shimizu (1997) identied the hosts of the species as Ten-
ebrionidae larvae.
Cordyceps species on wireworms 101
Ophiocordyceps elateridicola (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hyw-
el-Jones & Spatafora
≡ Cordyceps elateridicola Kobayasi & Shimizu
Host. Elateridae larvae (Kobayasi and Shimizu 1983; Shimizu 1997).
Known distribution. China (Taiwan), Japan (Shimizu 1997).
Ophiocordyceps entomorrhiza (Dicks.) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora
≡ Sphaeria entomorrhiza Dicks.
≡ Xylaria entomorrhiza (Dicks.) Gray
≡ Cordyceps entomorrhiza (Dicks.) Fr.
= Isaria eleutheratorum Nees
= Torrubia cinerea Tul. & C. Tul.
= Cordyceps cinerea (Tul. & C. Tul.) Sacc.
= Cordyceps meneristitis F. Muell. & Berk. [as ‘menesteridis’]
= Cordyceps entomorrhiza var. meneristitis (F. Muell. & Berk.) Cooke [as ‘mesenteridis’]
= Cordyceps carabi Quél.
= Tilachlidiopsis nigra Yakush. & Kumaz.
= Hirsutella eleutheratorum (Nees) Petch
Hosts. Larvae and adults of many Coleoptera families, for example, Tenebrionidae
larva (Shrestha et al. 2016) and Lampyridae larvae.
Distribution. Widely distributed.
Note. According to the illustrations by Shimizu (1997), we identify the hosts of
the species from Japan as Lampyridae larvae (Elateroidea).
Ophiocordyceps falcatoides (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-
Jones & Spatafora
≡ Cordyceps falcatoides Kobayasi & Shimizu
Host. Tenebrionoidea or Elateroidea larva.
Known distribution. Japan (Kobayasi and Shimizu 1980a).
Note. Host of the species was originally recorded as a Coleoptera larva (Kobayasi
and Shimizu 1980a). According to the illustration by Shimizu (1997), the host is a
wireworm.
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
102
Ophiocordyceps ferruginosa (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-
Jones & Spatafora
≡ Cordyceps ferruginosa Kobayasi & Shimizu
Hosts. Xylophagidae larvae (Diptera).
Known distribution. Japan (Kobayasi and Shimizu 1980b).
Notes. Hosts of the species were originally identied as Coleoptera larvae living
in decayed wood (Kobayasi and Shimizu 1980b, Shimizu 1997). According to the il-
lustrations by Shimizu (1997), the hosts are actually Diptera (Xylophagidae) larvae.
Considering the very similar morphology and the same hosts between O. ferruginosa
and O. variabilis, the former might be a synonym of the latter (see notes of O. variabilis
below). As a result, O. ferruginosa is not a pathogen of wireworms.
Ophiocordyceps formosana (Kobayasi & Shimizu) Yen W. Wang, S.H. Tsai, Tzean
& T.L. Shen
≡ Cordyceps formosana Kobayasi & Shimizu
Hosts. Tenebrionoidea larvae (Li et al. 2002, 2016).
Known distribution. China (Anhui, Fujian, Hunan, Taiwan) (Kobayasi and
Shimizu 1981; Li et al. 2002, 2016).
Notes. e host of the species was originally recorded as a Coleoptera larva (Kob-
ayasi and Shimizu 1981). According to the illustration by Shimizu (1997), it appears
to be a Tenebrionoidea larva. Li et al. (2002) identied the host of their collection as a
Tenebrionidae larva. We cautiously identify these hosts as Tenebrionoidea larvae (used
in Li et al. 2016).
Ophiocordyceps jiangxiensis (Z.Q. Liang, A.Y. Liu & Yong C. Jiang) G.H. Sung,
J.M. Sung, Hywel-Jones & Spatafora
≡ Cordyceps jiangxiensis Z.Q. Liang, A.Y. Liu & Yong C. Jiang
Hosts. Elateridae larvae (Campsosternus sp.) (Liang et al. 2001; Zha et al. 2018).
Known distribution. China (Jiangxi, Fujian, Yunnan) (Zha et al. 2018).
Notes. e species was originally described by Liang et al. (2001) with specimens
from Jiangxi, China. Sung et al. (2007) revised it to O. jiangxiensis only based on the
original morphological description. e species is closely similar to Metarhizium pur-
pureonigrum, a recently-described species from ailand (Mongkolsamrit et al. 2020).
Future studies are warranted to clarify its taxonomic placement.
Cordyceps species on wireworms 103
Ophiocordyceps larvicola (Quél.) Van Vooren
≡ Cordyceps larvicola Quél.
Hosts. Larvae of Cerambycidae, Scarabaeidae and Tenebrionidae (e.g. Cylindronotus
sp., Helops spp.) (Kobayasi 1941; Shrestha et al. 2016).
Known distribution. France (Kobayasi 1941), the European part of Russia (Koval
1984).
Ophiocordyceps melolonthae (Tul. & C. Tul.) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora
≡ Torrubia melolonthae Tul. & C. Tul.
≡ Cordyceps melolonthae (Tul. & C. Tul.) Sacc.
= Cordyceps rickii Lloyd
= Cordyceps melolonthae var. rickii (Lloyd) Mains
= Ophiocordyceps melolonthae var. rickii (Lloyd) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora
Hosts. Scarabaeidae larvae (Shrestha et al. 2016), Elateridae larvae (Shimizu 1997).
Distribution. North, Central and South America, the West Indies (Kobayasi 1941;
Mains 1958), Japan (Shimizu 1997), Belarus, the Russian Far East (Koval 1984).
Ophiocordyceps nigripoda (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-
Jones & Spatafora [as ‘nigripes’]
≡ Cordyceps nigripoda Kobayasi & Shimizu
Host. Elateroidea or Tenebrionoidea larva.
Known distribution. Japan (Kobayasi and Shimizu 1982b).
Note. Host of the species was originally recorded as a Coleoptera larva (Kobayasi and
Shimizu 1982b). According to the illustration by Shimizu (1997), the host is a wireworm.
Ophiocordyceps purpureostromata (Kobayasi) G.H. Sung, J.M. Sung, Hywel-
Jones & Spatafora
≡ Cordyceps purpureostromata Kobayasi
= Cordyceps purpureostromata f. recurvata Kobayasi
= Ophiocordyceps purpureostromata f. recurvata (Kobayasi) G.H. Sung, J.M. Sung, Hy-
wel-Jones & Spatafora
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
104
Hosts. Elateridae larvae (Shimizu 1997).
Known distribution. Japan (Kobayasi and Shimizu 1980b).
Ophiocordyceps rubiginosiperitheciata (Kobayasi & Shimizu) G.H. Sung, J.M.
Sung, Hywel-Jones & Spatafora
≡ Cordyceps rubiginosiperitheciata Kobayasi & Shimizu [as ‘rubiginosoperitheciata’]
Hosts. Elateroidea or Tenebrionoidea larvae.
Known distribution. Japan (Shimizu 1997).
Note. e host of the species was originally recorded as a Coleoptera larva (Kob-
ayasi and Shimizu 1983). According to the illustration by Shimizu (1997), hosts of the
species are wireworms.
Ophiocordyceps rubripunctata (Moreau) G.H. Sung, J.M. Sung, Hywel-Jones &
Spatafora
≡ Cordyceps rubripunctata Moreau
= Hirsutella rubripunctata Samson, H.C. Evans & Hoekstra
Hosts. Elateridae larvae (Samson et al. 1982).
Known distribution. Congo, Ghana (Samson et al. 1982).
Ophiocordyceps salebrosa (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora
≡ Cordyceps salebrosa Mains
Host. Elateridae adult (Mains 1947).
Known distribution. Panama Canal Zone (Barro Colorado Island) (Mains 1947).
Note. Notably, the host of the species is an adult.
Ophiocordyceps sporangifera Y.P. Xiao, T.C. Wen & K.D. Hyde
Host. Elateroidea or Tenebrionoidea larva.
Known distribution. ailand (Xiao et al. 2019).
Note. e host of the species was originally identied as an Elateridae larva (Xiao
et al. 2019).
Cordyceps species on wireworms 105
Ophiocordyceps stylophora (Berk. & Broome) G.H. Sung, J.M. Sung, Hywel-Jones
& Spatafora
≡ Cordyceps stylophora Berk. & Broome
= Hirsutella stylophora Mains
Hosts. Larvae of Coleoptera (Cerambycidae, Elateridae, Scarabaeidae) (Shrestha et
al. 2016).
Known distribution. Canada (Nova Scotia), China (Guangxi, Jilin, Zhejiang),
Japan, Russia (Far East), U.S.A. (Carolina) (Kobayasi 1941; Mains 1941; Koval 1984;
Liang 2007).
Note. Liang (2007) recorded the hosts of the species as Lepidoptera larvae, but his
provided picture (a specimen collected from Jilin, China) appears to be a wireworm host.
Ophiocordyceps subavida (Mains) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora
≡ Cordyceps albida Pat. & Gaillard
≡ Cordyceps subavida Mains
Hosts. Elateridae larvae (Shimizu 1997).
Known distribution. Japan (Shimizu 1997), Venezuela (Mains 1959).
Note. e species was originally reported from Venezuela and its host was recorded
as an insect larva (Mains 1959). Shimizu (1997) identied the host of a specimen from
Japan as an Elateridae larva.
Ophiocordyceps variabilis (Petch) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora
≡ Cordyceps variabilis Petch
= Cordyceps viperina Mains
Hosts. Xylophagidae larvae (Diptera) (Hodge et al. 1998; Yaroslavtseva et al. 2019).
Known distribution. China (Shaanxi),Europe, Russia (Far East, Western Siberia),
North America (Petch 1937; Liang 2007; Hodge et al. 1998; Yaroslavtseva et al. 2019).
Notes. In early literature, O. variabilis was recorded on Coleoptera (e.g. Elateridae) and
Diptera larvae in rotten wood (Petch 1937; Mains 1958; Liang 2007). Hodge et al. (1998)
checked many samples and conrmed the hosts to be Xylophagidae larvae (Diptera). More
than 40 samples of O. variabilis were collected in Russia (Far East, Western Siberia) and
all of them developed on Xylophagidae larvae (Yaroslavtseva et al. 2019; Kryukov et al.,
unpublished). Ecological habits and morphology of Xylophagidae larvae and wireworms
are closely similar, but their last abdominal segments are distinctly dierent. As with O.
ferruginosa listed above, we conclude that O. variabilis is not a pathogen of wireworms.
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
106
Paraisaria gracilioides (Kobayasi) C.R. Li, M.Z. Fan & Z.Z. Li
≡ Isaria gracilioides Kobayasi
= Cordyceps gracilioides Kobayasi
= Ophiocordyceps gracilioides (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora
= Paraisaria gracilioides (Kobayasi) Luangsa-ard, Mongkolsamrit & Samson, syn. nov.
Hosts. Elateridae larvae (Shimizu 1997; Yahagi 2008).
Known distribution. China (Anhui, Fujian), Japan, Russia (Far East) (Kobayasi
1941; Koval 1984; Liang 2007).
Notes. e species is similar to Paraisaria gracilis (Grev.) Luangsa-ard et al., but the
former grows on Coleoptera larvae (Elateridae), while the latter on Lepidoptera larvae
(Kobayasi 1941; Yahagi 2008). Hosts of the sexual C. gracilioides and its asexual Isaria
gracilioides were both originally mistakenly identied as Cossidae larvae (Lepidoptera
instead of Coleoptera) (Kobayasi 1941). Fan et al. (2001) collected a sexual specimen
of the species on a Coleoptera larva (wireworm); Li et al. (2004) successfully isolated
its asexual morph and revised the asexual Isaria gracilioides to the asexual Paraisaria
gracilioides (Kobayasi) C.R. Li et al., linked with the sexual C. gracilioides. Later, the
sexual C. gracilioides has been revised in an orderly manner to O. gracilioides (Sung et
al. 2007) and Paraisaria gracilioides (Kobayasi) Luangsa-ard et al. (Mongkolsamrit et
al. 2019). Considering the rules of priority and one fungus, one name (Kepler et al.
2013), we combine Paraisaria gracilioides (Kobayasi) Luangsa-ard et al. with Paraisaria
gracilioides (Kobayasi) C.R. Li et al.
Paraisaria phuwiangensis Mongkolsamrit, Noisripoom, Himaman, Jangsantear
& Luangsa-ard
Hosts. Elateridae larvae (Mongkolsamrit et al. 2019).
Known distribution. ailand (Mongkolsamrit et al. 2019).
Paraisaria yodhathaii Mongkolsamrit, Noisripoom, Lamlertthon & Luangsa-ard
Hosts. Elateridae larva (Mongkolsamrit et al. 2019).
Known distribution. ailand (Mongkolsamrit et al. 2019).
Perennicordyceps cuboidea (Kobayasi & Shimizu) Matočec & I. Kušan
≡ Cordyceps cuboidea Kobayasi & Shimizu
≡ Ophiocordyceps cuboidea (Kobayasi & Shimizu) S. Ban, Sakane & Nakagiri
≡ Polycephalomyces cuboideus (Kobayasi & Shimizu) Kepler & Spatafora
= Cordyceps alboperitheciata Kobayasi & Shimizu
Cordyceps species on wireworms 107
Hosts. Tenebrionoidea and/or Elateroidea larvae (Shimizu 1997; Ban et al. 2009);
stroma of O. stylophora (Ban et al. 2009).
Known distribution. Japan (Kobayasi and Shimizu 1980b).
Note. e host of the species was originally recorded as a Coleoptera larva (Kob-
ayasi and Shimizu 1980b). According to the illustrations by Shimizu (1997) and Ban
et al. (2009), hosts of the species are wireworms.
Perennicordyceps ryogamiensis (Kobayasi & Shimizu) Matočec & I. Kušan
≡ Cordyceps ryogamiensis Kobayasi & Shimizu
≡ Ophiocordyceps ryogamiensis (Kobayasi & Shimizu) G.H. Sung, J.M. Sung, Hywel-
Jones & Spatafora
≡ Polycephalomyces ryogamiensis (Kobayasi & Shimizu) Kepler & Spatafora
Host. Tenebrionoidea larva.
Known distribution. Japan (Kobayasi and Shimizu 1983).
Note. Host of the species was originally recorded as a Coleoptera larva (Kobayasi
and Shimizu 1983). According to the illustration by Shimizu (1997), the host is a
Tenebrionoidea larva.
Polycephalomyces phaothaiensis Mongkols., Noisrip., Lamlertthon & Luangsa-ard
Hosts. Tenebrionoidea or Elateroidea larvae.
Known distribution. ailand (Crous et al. 2017).
Note. Hosts of the species were recorded as Coleoptera larvae (Crous et al. 2017).
According to the picture provided, the hosts are wireworms.
Tolypocladium cylindrosporum W. Gams
≡ Beauveria cylindrospora (W. Gams) Arx
Hosts. Coleoptera (e.g. Elateridae sp.), Diptera, Hymenoptera and Lepidoptera
(Humber and Hansen 2005); inhabit soil (Scorsetti et al. 2012).
Distribution. Widely distributed.
Tolypocladium inatum W. Gams
= Pachybasium niveum O. Rostr.
= Tolypocladium niveum (O. Rostr.) Bissett
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
108
= Cordyceps subsessilis Petch
= Elaphocordyceps subsessilis (Petch) G.H. Sung, J.M. Sung & Spatafora
= Cordyceps facis Kobayasi & Shimizu [as ‘Codyceps’]
Hosts. Tenebrionidae larvae (Shimizu 1997).
Distribution. Widely distributed (Petch 1937; Kobayasi 1982; Sung et al. 2007).
Note. Hosts of the species were previously recorded as Coleoptera larvae (Petch
1937; Kobayasi 1982). Shimizu (1997) identied them as Tenebrionidae larvae.
Discussion
e superfamilies Elateroidea and Tenebrionoidea are two very large groups of beetles
and comprise more than 50 families of Coleoptera (Catalogue of Life 2021). ese
include Lampyridae (reies), Elateridae (click beetles), Phengodidae (glowworm bee-
tles), Cantharidae (soldier beetles) and their relatives in Elateroidea; and Meloidae
(blister beetles), Anthicidae (ant-like ower beetles), Mordellidae (tumbling ower
beetles), Tenebrionidae (darkling beetle), Ciidae (the minute tree-fungus beetles), Zo-
pheridae (ironclad beetles) and their relatives in Tenebrionoidea. Most of Elateroidea
and Tenebrionoidea larvae (wireworms) are closely similar and morphology alone could
hardly distinguish them. In practice, hosts of many wireworm-infecting Cordyceps s.l.
species are commonly identied as Elateridae (mainly) or Tenebrionidae larvae. Con-
sidering the diculties in identifying wireworms, we suggest to use the superfamily
names (Elateroidea or Tenebrionoidea) to record the hosts of the fungi, unless we can
denitely know the species identity (e.g. by barcoding techniques).
In present paper, we summarised the data of wireworm-infecting species of
Cordyceps s.l. To date, a total of 63 species have been reported, including 17 species
(Akanthomyces, Beauveria and Cordyceps) in Cordycipitaceae, 11 species (Metarhizium
and Nigelia) in Clavicipitaceae and 35 species (Ophiocordyceps, Paraisaria, Perenni-
cordyceps, Polycephalomyces and Tolypocladium) in Ophiocordycipitaceae. Amongst
these, C. militaris, O. ferruginosa and O. variabilis are rejected; the remaining 60 spe-
cies are accepted as natural pathogens of wireworms. It is likely that a signicant por-
tion of fungi, associated with wireworms, is represented by specialised forms. irteen
of the reported species (20%) have broad host ranges, that is, they can infect dierent
arthropod taxa and may also parasitise fungi and nematodes. e other 47 species
(80%) have, thus far, been registered on wireworms only. Generalist fungi are mostly
widespread, whereas specialised fungi are generally reported from warm and humid en-
vironments of Southeast Asia (Japan, south-western China and ailand), the Amazon
of South America and the Russian Far East. It should be noted that many animal-as-
sociated fungi are awaiting description, especially in groups, such as Hypocreales (An-
tonelli et al. 2020; Cheek et al. 2020) and many taxonomically-uncertain Cordyceps s.l.
species infecting Elateroidea and Tenebrionoidea remain to be studied. Apart from the
description of novel taxa, further studies should focus on revisions of these uncertain
Cordyceps species on wireworms 109
species and further information of wireworm hosts. Limited by lack of information
and taxonomic knowledge of larvae, species diversity of wireworm-infecting Cordyceps
s.l. may not have been completely accounted for and many wireworm hosts cannot be
or are incorrectly assigned to their families.
is is the rst study summarising species diversity of wireworm-infecting Cordyceps
s.l. A checklist of 60 species is provided and two novel species are described. Our work
provides basic information for future research on species diversity of Cordyceps s.l. as-
sociated with wireworms, management and biocontrol of wireworm populations, as
well as on edible and medicinal insects and fungi.
Acknowledgements
e study was supported by the Russian Foundation for Basic Research (projects nos.
16-54-53033 and 20-516-53009), the Federal Fundamental Scientic Research Pro-
gram (no. FWGS-2021-0001) and the Provincial Natural Science Foundation of An-
hui, China (1908085MC84).
References
Antonelli A, Fry C, Smith RJ, et al. (2020) State of the World’s Plants and Fungi 2020. Royal
Botanic Gardens, Kew. https://doi.org/10.34885/172
Bamisile BS, Dash CK, Akutse KS, Keppanan R, Afolabi OG, Hussain M, Qasim M, Wang L
(2018) Prospects of endophytic fungal entomopathogens as biocontrol and plant growth
promoting agents: an insight on how articial inoculation methods aect endophytic colo-
nization of host plants. Microbiological Research 217: 34–50. https://doi.org/10.1016/j.
micres.2018.08.016
Ban S, Sakane T, Toyama K, Nakagiri A (2009) Teleomorph-anamorph relationships and reclas-
sication of Cordyceps cuboidea and its allied species. Mycoscience 50: 261–272. https://
doi.org/10.1007/S10267-008-0480-Y
Ban S, Sakane T, Nakagiri A (2015) ree new species of Ophiocordyceps and overview of an-
amorph types in the genus and the family Ophiocordyceptaceae. Mycological Progress
14(1): 1017–1028. https://doi.org/10.1007/s11557-014-1017-8
Barsics F, Haubruge E, Verheggen FJ (2013) Wireworms’ management: an overview of the
existing methods, with particular regards to Agriotes spp. (Coleoptera: Elateridae). Insects
4: 117–152. https://doi.org/10.3390/insects4010117
Bischo JF, Rehner SA, Humber RA (2009) A multilocus phylogeny of the Metarhizium an-
isopliae lineage. Mycologia 101(4): 512–530. https://doi.org/10.3852/07-202
Brunner-Mendoza C, Reyes-Montes MDR, Moonjely S, Bidochka MJ, Toriello C (2019) A re-
view on the genus Metarhizium as an entomopathogenic microbial biocontrol agent with
emphasis on its use and utility in Mexico. Biocontrol Science and Technology 29(1): 83–102.
https://doi.org/10.1080/09583157.2018.1531111
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
110
Cai L, Jeewon R, Hyde KD (2006) Molecular systematics of Zopella and allied genera: evi-
dence from multigene sequence analyses. Mycological Research 110: 359–368. https://doi.
org/10.1016/j.mycres.2006.01.007
Catalogue of Life (2021) [accessed 1 March 2021]
Chaverri P, Bischo JF, Evans HC, Hodge KT (2005) Regiocrella, a new entomopathogenic
genus with a pycnidial anamorph and its phylogenetic placement in the Clavicipitaceae.
Mycologia 97(6): 1225–1237. https://doi.org/10.1080/15572536.2006.11832732
Cheek M, Lughadha EN, Kirk P, Lindon H, Carretero J, Looney B, Douglas B, Haelewaters D,
Gaya E, Llewellyn T, Ainsworth AM, Gaorov Y, Hyde K, Crous P, Hughes M, Walker BE,
Forzza RC, Wong KM, Niskanen T (2020) New scientic discoveries: Plants and fungi.
Plants, People, Planet 2(5): 371–388. https://doi.org/10.1002/ppp3.10148
Chen ZH, Dai YD, Yu H, Yang K, Yang ZL, Yuan F, Zeng WB (2013) Systematic analyses of
Ophiocordyceps lanpingensis sp. nov., a new species of Ophiocordyceps in China. Microbio-
logical Research 168(8): 525–532. https://doi.org/10.1016/j.micres.2013.02.010
Crous PW, Wingeld MJ, Burgess TI, Carnegie AJ, StJ Hardy GE, Smith D, Summerell BA,
Cano-Lira JF, Guarro J, Houbraken J, Lombard L, Martín MP, Sandoval-Denis M, Al-
exandrova AV, Barnes CW, Baseia IG, Bezerra JDP, Guarnaccia V, May TW, Hernández-
Restrepo M, Stchigel AM, Miller AN, Ordoñez ME, Abreu VP, Accioly T, Agnello C,
Agustincolmán A, Albuquerque CC, Alfredo DS, Alvarado P, Araújo-Magalhães GR,
Arauzo S, Atkinson T, Barili A, Barreto RW, Bezerra JL, Cabral TS, Rodríguez FC, Cruz
RHSF, Daniëls PP, da silva BDB, de Almeida DAC, de Carvalhojúnior AA, Decock CA,
Delgat L, Denman S, Dimitrov RA, Edwards J, Fedosova AG, Ferreira RJ, Firmino AL,
Flores JA, García D, Gené J, Giraldo A, Góis JS, Gomes AAM, Gonçalves CM, Goulia-
mova DE, Groenewald M, Guéorguiev BV, Guevara-Suarez M, Gusmão LFP, Hosaka K,
Hubka V, Huhndorf SM, Jadan M, Jurjevi Kraak B, Kuera V, Kumar TKA, Kušan I, Lac-
erda SR, Lamlertthon S, Lisboa WS, Loizides M, Luangsa-Ard JJ, Lysková P, Maccormack
WP, Macedo DM, Machado AR, Malysheva EF, Marinho P, Matoec N, Meijer M, Meši
A, Mongkolsamrit S, Moreira KA, Morozova OV, Nair KU, Nakamura N, Noisripoom
W, Olariaga I, Oliveira RJV, Paiva LM, Pawar P, Pereira OL, Peterson SW, Prieto M, Rod-
ríguez-Andrade E, Rojodeblas C, Roy M, Santos ES, Sharma R, Silva GA, Souza-Motta
CM, Takeuchi-Kaneko Y, Tanaka C, akur A, Smith MTH, Tkalec Z, Valenzuela-Lopez
N, Vanderkleij P, Verbeken A, Viana MG, Wang XW, Groenewald JZ (2017) Fungal Planet
description sheets: 625–715. Persoonia -Molecular Phylogeny and Evolution of Fungi 39:
270–467. https://doi.org/10.3767/persoonia.2017.39.11
De Bary A (1867) Zur Kenntniss insectentoedtender Pilze. Botanische Zeitung 25: 17–21.
https://doi.org/10.1007/BF01650457
Domsch KH, Gams W, Anderson TH (1980) Compendium of Soil Fungi. London: Academic
Press, 136–140.
Fan MZ, Li CR, Chen YY, Li ZZ (2001) Cordyceps gracilioides, a new record for China. Myco-
systema 20: 273–274.
GBIF (2021) (GBIF = Global Biodiversity Information Facility) [accessed 1 March 2021]
Gullan PJ, Cranston PS (2010) e Insects: An Outline of Entomology (4th edition). Wiley-
Blackwell, Oxford.
Cordyceps species on wireworms 111
Hu X, Xiao G, Zheng P, Shang Y, Su Y, Zhang X, Liu X, Zhan S, St Leger RJ, Wang C (2014)
Trajectory and genomic determinants of fungal-pathogen speciation and host adaptation.
Proceedings of the National Academy of Sciences, USA 111: 16796–16801. https://doi.
org/10.1073/pnas.1412662111
Humber RA, Hansen KS (2005) USDA-ARS Collection of Entomopathogenic Fungal Cul-
tures (ARSEF), ARSEF-Index: Host by Fungus. http://arsef.fpsnl.cornell.edu./
Hodge KT, Humber RA, Wozniak AC (1998) Cordyceps variabilis and the genus Syngliocla-
dium. Mycologia 90(5): 743–753. https://doi.org/10.1080/00275514.1998.12026966
Hongsanan S, Maharachchikumbura SSN, Hyde KD, Samarakoon MC, Jeewon R, Zhao
Q, Al-Sadi AM, Bahkali AH (2017) An updated phylogeny of Sordariomycetes based
on phylogenetic and molecular clock evidence. Fungal Diversity 84: 25–41. https://doi.
org/10.1007/s13225-017-0384-2
Hyde KD, Chaiwan N, Norphanphoun C, Boonmee S, Camporesi E, Chethana KWT, Dayar-
athne MC, de Silva NI, Dissanayake AJ, Ekanayaka AH, Hongsanan S, Huang SK, Jayasiri
SC, Jayawardena RS, Jiang HB, Karunarathna A, Lin CG, Liu JK, Liu NG, Lu YZ, Luo
ZL, Maharachchimbura SSN, Manawasinghe IS, Pem D, Perera RH, Phukhamsakda C,
Samarakoon MC, Senwanna C, Shang QJ, Tennakoon DS, ambugala KM, Tibpromma
S, Wanasinghe DN, Xiao YP, Yang J, Zeng XY, Zhang JF, Zhang SN, Bulgakov TS, Bhat
DJ, Cheewangkoon R, Goh TK, Jones EBG, Kang JC, Jeewon R, Liu ZY, Lumyong S,
Kuo CH, McKenzie EHC, Wen TC, Yan JY, Zhao Q (2018) Mycosphere notes 169–224.
Mycosphere 9(2): 271–430. https://doi.org/10.5943/mycosphere/9/2/8
Hywel-Jones NL (1995) Cordyceps brunneapunctata sp. nov. infecting beetle larvae in ai-
land. Mycological Research 99(10): 1195–1198. https://doi.org/10.1016/S0953-
7562(09)80277-3
Imoulan A, Hussain M, Kirk PM, Meziane AE, Yao YJ (2017) Entomopathogenic fungus Beau-
veria: host specicity, ecology and signicance of morpho-molecular characterization in
accurate taxonomic classication. Journal of Asia-Pacic Entomology 20(4): 1204–1212.
https://doi.org/10.1016/j.aspen.2017.08.015
Index Fungorum (2021) [accessed 1 March 2021]
Jeewon R, Liew ECY, Simpson JA, Hodgkiss IJ, Hyde KD (2003) Phylogenetic signicance of
morphological characters in the taxonomy of Pestalotiopsis species. Molecular Phylogenet-
ics and Evolution 27: 372–383. https://doi.org/10.1016/S1055-7903(03)00010-1
Kabaluk T, Goettel M, Erlandson M, Ericsson J, Duke G, Vernon B (2005) Metarhizium an-
isopliae as a biological control for wireworms and a report of some other naturally-occur-
ring parasites. IOBC/WPRS Bulletin 28: 109–115.
Kabaluk T, Li-Leger E, Nam S (2017) Metarhizium brunneum – an enzootic wireworm disease
and evidence for its suppression by bacterial symbionts. Journal of Invertebrate Pathology
150: 82–87. https://doi.org/10.1016/j.jip.2017.09.012
Keissler K, Lohwag H (1937) Part II, Fungi. In: Handel-Mazzetti H (Ed.) Symbolae Sinicae.
Springer, Wien, Germany.
Kepler RM, Sung GH, Ban S, Nakagiri A, Chen MJ, Huang B, Li Z, Spatafora JW (2012)
New teleomorph combinations in the entomopathogenic genus Metacordyceps. Mycologia
104(1): 182–197. https://doi.org/10.3852/11-070
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
112
Kepler RM, Ban S, Nakagiri A, Bischo JF, Hywel-Jones NL, Owensby CA, Spatafora JW
(2013) e phylogenetic placement of hypocrealean insect pathogens in the genus
Polycephalomyces: an application of one fungus one name. Fungal Biology 117: 611–622.
https://doi.org/10.1016/j.funbio.2013.06.002
Kepler RM, Humber RA, Bischo JF, Rehner SA (2014) Clarication of generic and species
boundaries for Metarhizium and related fungi through multigene phylogenetics. Mycolo-
gia 106(4): 811–829. https://doi.org/10.3852/13-319
Kepler RM, Luangsa-ard JJ, Hywel-Jones NL, Quandt CA, Sung GH, Rehner SA, Aime MC,
Henkel TW, Sanjuan T, Zare R, Chen MJ, Li ZZ, Rossman AY, Spatafora JW, Shrestha B
(2017) A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales). IMA
Fungus 8: 335–353. https://doi.org/10.5598/imafungus.2017.08.02.08
Kobayasi Y (1941) e genus Cordyceps and its allies. Science Reports of the Tokyo Bunrika
Daigaku (Section B, No. 84) 5: 53–260.
Kobayasi Y (1982) Key to the taxa of the genera Cordyceps and Torrubiella. Transactions of the
Mycological Society of Japan 23: 329–364.
Kobayasi Y, Shimizu D (1978) Cordyceps species from Japan. Bulletin of the National Science
Museum, Tokyo, Series B, Botany 4(2): 43–63.
Kobayasi Y, Shimizu D (1980a) Cordyceps species from Japan 2. Bulletin of the National Sci-
ence Museum, Tokyo, Series B, Botany 6(3): 77–96.
Kobayasi Y, Shimizu D (1980b) Cordyceps species from Japan 3. Bulletin of the National
Science Museum, Tokyo, Series B, Botany 6(4): 125–145.
Kobayasi Y, Shimizu D (1981) e genus Cordyceps and its allies from Taiwan (Formosa).
Bulletin of the National Science Museum, Tokyo, Series B, Botany 7: 113–122
Kobayasi Y, Shimizu D (1982a) Cordyceps species from Japan 4. Bulletin of the National
Science Museum, Tokyo, Series B, Botany 8(3): 79–91.
Kobayasi Y, Shimizu D (1982b) Cordyceps species from Japan 5. Bulletin of the National
Science Museum, Tokyo, Series B, Botany 8(4): 111–123.
Kobayasi Y, Shimizu D (1983) Cordyceps species from Japan 6. Bulletin of the National Science
Museum, Tokyo B, Botany 9(1): 1–21.
Koval EZ (1984) Clavicipitalean Fungi of the USSR. Kiev, Naukova Dumka.
Kryukov VY, Yaroslavtseva ON, Lednev GR, Borisov BA (2011) Local epizootics caused by
teleomorphic cordycipitoid fungi (Ascomycota: Hypocreales) in populations of forest lepi-
dopterans and sawies of the summer-autumn complex in Siberia. Microbiology 80(2):
286–295. https://doi.org/10.1134/S0026261711020093
Li CR, Fan MZ, Huang B, Wang SB, Li ZZ (2002) e genus Cordyceps and its allies from
Anhui I. Mycosystema 21(2): 167–171.
Li CR, Ming L, Fan MZ, Li ZZ (2004) Paraisaria gracilioides comb. nov., the anamorph of
Cordyceps gracilioides. Mycosystema 23(1): 165–166.
Li GJ, Hyde KD, Zhao RL, Hongsanan S, Abdel-Aziz F, Abdel-Wahab M, Alvarado P, Alves-
Silva G, Ammirati J, Ariyawansa H, Baghela A, Bahkali A, Beug MW, Bhat DJ, Bojantchev
D, Boonpratuang T, Bulgakov T, Erio C, Boro MC, Ceska O, Chakraborty D, Chen JJ,
Kandawatte TC, Chomnunti P, Consiglio G, Cui BK, Dai DQ, Dai YC, Daranagama DA,
Das K, Dayarathne M, Crop ED, Oliveira R, Fragoso de Souza CA, Ivanildo de Souza J,
Cordyceps species on wireworms 113
Dentinger BTM, Dissanayake AJ, Doilom M, Drechsler-Santos ER, Ghobad-Nejhad M,
Gilmore SP, Góes-Neto A, Gorczak M, Haitjema CH, Hapuarachchi K, Hashimoto A, He
MQ, Henske JK, Hirayama K, Iribarren MJ, Jayasiri S, Jayawardena RS, Jeon SJ, Jerônimo
GH, Lucia de Jesus A, Jones EBG, Kang JC, Karunarathna SC, Kirk PM, Konta S, Kuh nert
E, Langer EJ, Lee HS, Lee HB, Li WJ, Li XH, Liimatainen K, Lima D, Lin CG, Liu JK,
Liu X, Liu ZY, Luangsa-Ard JJ, Lücking R, Lumbsch T, Lumyong S, Leano E, Marano AV,
Matsumura M, McKenzie EHC, Mongkolsamrit S, Mortimer PE, Nguyen TTT, Niskanen
T, Norphanphoun C, O’Malley MA, Parnmen S, Pawłowska J, Perera RH, Phookamsak R,
Phukhamsakda C, Zottarelli C, Raspé O, Reck MA, Rocha SCO, Santiago A, Senanay ake I,
Setti L, Shang QJ, Singh S, Sir EB, Solomon KV, Song J, Srikitikulchai P, Stadler M, Suetrong
S, Takahashi H, Takahashi T, Tanaka K, Tang LP, ambugala K, anak itpipattana D, e-
odorou M, ongbai B, ummarukcharoen T, Tian Q, Tibpromma S, Verbeken A, Vizzini
A, Vlasák J, Voigt K, Wanasinghe DN, Wang Y, Weerakoon G, Wen HA, Wen TC, Wijaya-
wardene N, Wongkanoun S, Wrzosek M, Xiao YP, Xu JC, Yan JY, Yang J, Yang SD, Hu Y,
Zhang JF, Zhao J, Zhou LW, Persoh D, Phillips AJL, Maha rachchikumbura S, Amoozegar
MA (2016) Fungal diversity notes 253–366: taxonomic and phylogenetic contributions to
fungal taxa. Fungal Diversity 78(1): 1–237. https://doi.org/10.1007/s13225-016-0366-9
Liang ZQ (2007) Flora Fungorum Sinicorum, Vol. 32, Cordyceps. Science Press, Beijing.
Liang ZQ, Liu AY, Jiang YC (2001) Two new species of Cordyceps from Jinggang Mountains.
Mycosystema 20(3): 306–309.
Liu B, Rong F, Jin H (1985) A new species of the genus Cordyceps. Journal of Wuhan Botanical
Research 3(1): 23–24.
Luangsa-ard J, Mongkolsamrit S, anakitpipattana D, Khonsanit A, Tasanathai K, Nois-
ripoom W, Humber RA (2017) Clavicipitaceous entomopathogens: new species in
Metarhizium and a new genus Nigelia. Mycological Progress 16: 369–391. https://doi.
org/10.1007/s11557-017-1277-1
Mains EB (1941) Cordyceps stylophora and Cordyceps ravenelii. Mycologia 33: 611–617. https://
doi.org/10.1080/00275514.1941.12020857
Mains EB (1947) New and interesting species of Cordyceps. Mycologia 39(5): 535–545. https://
doi.org/10.1080/00275514.1947.12017632
Mains EB (1958) North American entomogenous species of Cordyceps. Mycologia 50: 169–222.
https://doi.org/10.1080/00275514.1958.12024722
Mains EB (1959) Cordyceps species. Bulletin of the Torrey Botanical Club 86(1): 46–58. https://
doi.org/10.2307/2482660
Massee G (1895) A revision of the genus Cordyceps. Annals of Botany 9(33): 1–44. https://doi.
org/10.1093/oxfordjournals.aob.a090724
Massee G (1899) Revision du genre Cordyceps. Revue Mycologique 21: 1–16.
Miller MA, Pfeier W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference
of large phylogenetic trees. In: 2010 Gateway Computing Environments Workshop (GCE),
14 Nov. 2010, New Orleans, LA, 1–8. https://doi.org/10.1109/GCE.2010.5676129
Möller A (1901) Phycomyceten und Ascomyceten, Untersuchungen aus Brasilien, Botanische
Mittheilungen aus den Tropen 9 (edited by Schimper AFW). Gustav Fischer, Jena, Ger-
many, 378 pp. https://doi.org/10.5962/bhl.title.31997
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
114
Mongkolsamrit S, Khonsanit A, anakitpipattana D, Tasanathai K, Noisripoom W, Lamlert-
thon S, Himaman W, Houbraken J, Samson RA, Luangsa-ard J (2020) Revisiting Metarhi-
zium and the description of new species from ailand. Studies in Mycology 95: 171–251.
https://doi.org/10.1016/j.simyco.2020.04.001
Mongkolsamrit S, Noisripoom W, Arnamnart N, Lamlertthon S, Himaman W, Jangsantear P,
Samson RA, Luangsa-ard JJ (2019) Resurrection of Paraisaria in the Ophiocordycipitaceae
with three new species from ailand. Mycological Progress 18(9): 1213–1230. https://
doi.org/10.1007/s11557-019-01518-x
Moureau J (1949) Cordyceps du Congo Belge. Mémoires de l’Institut Royal Colonial Belge 7: 1–58.
Negi PS, Singh R, Koranga PS, Ahmed Z (2012) Two new for science species of genus Cordyceps
Fr. (Ascomycetes) from Indian Himalaya. International Journal of Medicinal Mushrooms
14(5): 501–506. https://doi.org/10.1615/IntJMedMushr.v14.i5.80
Petch T (1933) Notes on entomogenous fungi. Transactions of the British Mycological Society
18(1): 48–75. https://doi.org/10.1016/S0007-1536(33)80026-X
Petch T (1934) Notes on entomogenous fungi. Transactions of the British Mycological Society
19: 160–194. https://doi.org/10.1016/S0007-1536(35)80008-9
Petch T (1937) Notes on entomogenous fungi. Transactions of the British Mycological Society
21(1–2): 34–67. https://doi.org/10.1016/S0007-1536(37)80005-4
Quandt CA, Kepler RM, Gams W, Araújo JP, Ban S, Evans HC, Hughes D, Humber R,
Hywel-Jones N, Li Z, Luangsa-Ard JJ, Rehner SA, Sanjuan T, Sato H, Shrestha B, Sung
GH, Yao YJ, Zare R, Spatafora JW (2014) Phylogenetic-based nomenclatural proposals
for Ophiocordycipitaceae (Hypocreales) with new combinations in Tolypocladium. IMA
Fungus 5(1): 121–134. https://doi.org/10.5598/imafungus.2014.05.01.12
Rannala B, Yang Z (1996) Probability distribution of molecular evolutionary trees: a new
method of phylogenetic inference. Journal of Molecular Evolution 43: 304–311. https://
doi.org/10.1007/BF02338839
Reddy GVP, Tangtrakulwanich K, Wu SH, Miller JH, Ophus VL, Prewett J, Jaronski ST
(2014) Evaluation of the eectiveness of entomopathogens for the management of wire-
worms (Coleoptera: Elateridae) on spring wheat. Journal of Invertebrate Pathology 120:
43–49. https://doi.org/10.1016/j.jip.2014.05.005
Rehner SA, Minnis AM, Sung GH, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylog-
eny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia
103(5): 1055–1073. https://doi.org/10.3852/10-302
Ren GD, Ba YB, Liu HY, Niu YP, Zhu XC, li Z, Shi AM (2016) Fauna Sinica. Insecta. Vol. 63.
Coleoptera: Tenebrionidae (I). Science Press, Beijing, 532 pp.
Rogge SA, Mayerhofer J, Enkerli J, Bacher S, Grabenweger G (2017) Preventive application
of an entomopathogenic fungus in cover crops for wireworm control. BioControl 62(5):
613–623. https://doi.org/10.1007/s10526-017-9816-x
Samson RA, Evans HC, Hoekstra S (1982) Notes on entomogenous fungi from Ghana, VI.
Mycology 85(4): 589–605.
Samson RA, Evans HC (1985) New and rare entomogenous fungi from Amazonia. Proceed-
ings of the Indian Academy of Sciences (Plant Science) 94: 309–317.
Cordyceps species on wireworms 115
Sanjuan TI, Franco-Molano AE, Kepler RM, Spatafora JW, Tabima J, Vasco-Palacios AM,
Restrepo S (2015) Five new species of entomopathogenic fungi from the Amazon and
evolution of neotropical Ophiocordyceps. Fungal Biology 119(10): 901–916. https://doi.
org/10.1016/j.funbio.2015.06.010
Sato H, Shimazu M (2002) Stromata production for Cordyceps militaris (Clavicipitales: Clavi-
cipitaceae) by injection of hyphal bodies to alternative host insects. Applied Entomology
and Zoology 37(1): 85–92. https://doi.org/10.1303/aez.2002.85
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W, Bol chacova
E, Voigt K, Crous PW, Miller AN (2012) Nuclear ribosomal internal tran scribed spacer
(ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National
Academy of Sciences 109(16): 6241–6246. https://doi.org/10.1073/pnas.1117018109
Scorsetti AC, Elíades LA, Stenglein SA, Cabello MN, Pelizza SA, Saparrat MC (2012) Patho-
genic and enzyme activities of the entomopathogenic fungus Tolypocladium cylindrosporum
(Ascomycota: Hypocreales) from Tierra del Fuego, Argentina. Revista de Biología Tropical
60(2): 833–841. https://doi.org/10.15517/rbt.v60i2.4006
Shimizu D (1997) Illustrated Vegetable Wasps and Plant Worms in Color. Ie-No-Hikari
Association, Tokyo.
Shinya R, Watanabe A, Aiuchi D, Tani M, Kuramochi K, Kushida A, Koike M (2008) Potential
of Verticillium lecanii (Lecanicillium spp.) hybrid strains as biological control agents for
soybean cyst nematode: is protoplast fusion an eective tool for development of plant-
parasitic nematode control agents. Japanese Journal of Nematology 38(1): 9–18. https://
doi.org/10.3725/jjn.38.9
Shrestha B, Zhang WM, Zhang YJ, Liu XZ (2012) e medicinal fungus Cordyceps militaris:
research and development. Mycological Progress 11(3): 599–614. https://doi.org/10.1007/
s11557-012-0825-y
Shrestha B, Tanaka E, Hyun MW, Han JG, Kim CS, Jo JW, Han SK, Oh J, Sung GH (2016)
Coleopteran and Lepidopteran hosts of the entomopathogenic genus Cordyceps sensu lato.
Journal of Mycology 2016: e7648219. https://doi.org/10.1155/2016/7648219
Shrestha B, Tanaka E, Hyun MW, Han JG, Kim CS, Jo JW, Han SK, Oh J, Sung JM, Sung GH
(2017) Mycosphere Essay 19, Cordyceps species parasitizing hymenopteran and hemipteran
insects. Mycosphere 8: 1424–1442. https://doi.org/10.5943/mycosphere/8/9/8
Spatafora JW, Sung GH, Johnson D, Hesse C, O’Rourke B, Serdani M, Spotts R, Lutzoni
F, Hofstetter V, Miadlikowska J, Reeb V, Gueidan C, Fraker E, Lumbsch T, Lücking R,
Schmitt I, Hosaka K, Aptroot A, Roux C, Miller AN, Geiser DM, Hafellner J, Hestmark
G, Arnold AE, Büdel B, Rauhut A, Hewitt D, Untereiner WA, Cole MS, Scheidegger C,
Schultz M, Sipman H, Schoch CL (2006) A ve gene phylogeny of Pezizomycotina. My-
cologia 98: 1018–1028. https://doi.org/10.1080/15572536.2006.11832630
Spatafora JW, Sung GH, Sung JM, Hywel-Jones NL, White JJF (2007) Phylogenetic evidence
for an animal pathogen origin of ergot and the grass endophytes. Molecular Ecology 16(8):
1701–1711. https://doi.org/10.1111/j.1365-294X.2007.03225.x
Spegazzini C (1889) Fungi Puiggariani, Pugillus 1. Boletín De La Academia Nacional De Ciencias
De Córdoba 11(4): 381–622. https://doi.org/10.5962/bhl.title.3624
Ling-Sheng Zha et al. / MycoKeys 78: 79–117 (2021)
116
Sufyan M, Abbasi A, Gogi MD, Arshad M, Nawaz A, Neuho D (2017) Ecacy of Beau-
veria bassiana for the management of economically important wireworm species (Co-
leoptera: Elateridae) in organic farming. Gesunde Panzen 69(4): 197–202. https://doi.
org/10.1007/s10343-017-0406-8
Sung GH, Hywel-Jones NL, Sung JM, Luangsa-ard JJ, Shrestha B, Spatafora JW (2007) Phy-
logenetic classication of Cordyceps and the clavicipitaceous fungi. Studies in Mycology 57:
5–69. https://doi.org/10.3114/sim.2007.57.01
Tang AMC, Jeewon R, Hyde KD (2007) Phylogenetic utility of protein (RPB2, β-tubulin) and
ribosomal (LSU, SSU) gene sequences in the systematics of Sordariomycetes (Ascomycota,
Fungi). Antonie van Leeuwenhoek 91: 327–349. https://doi.org/10.1007/s10482-006-
9120-8
Tasanathai K, anakitpipattana D, Noisripoom W, Khonsanit A, Kumsao J, Luangsa-ard JJ
(2016) Two new Cordyceps species from a community forest in ailand. Mycological Pro-
gress 15: e28. https://doi.org/10.1007/s11557-016-1170-3
Wang WJ, Wang XL, Li Y, Xiao SR, Kepler RM, Yao YJ (2012) Molecular and morphologi-
cal studies of Paecilomyces sinensis reveal a new clade in clavicipitaceous fungi and its new
systematic position. Systematics and Biodiversity 10: 221–232. https://doi.org/10.1080/1
4772000.2012.690784
Wang L, Li HH, Chen YQ, Zhang WM, Qu LH (2014) Polycephalomyces lianzhouensis sp. nov.,
a new species, co-occurs with Ophiocordyceps crinalis. Mycological Progress 13: 1089–1096.
https://doi.org/10.1007/s11557-014-0996-9
Wang YB, Yu H, Dai YD, Chen ZH, Zeng WB, Yuan F, Liang ZQ (2015) Polycephalomyces yun-
nanensis (Hypocreales), a new species of Polycephalomyces parasitizing Ophiocordyceps nutans
and stink bugs (hemipteran adults). Phytotaxa 208(1): 34–44. https://doi.org/10.11646/
phytotaxa.208.1.3
Wang YB (2016) Studies on Phylogeny of Polycephalomycetaceae Fam. Nov., with Microbial
Diversities of Polycephalomyces Multiramosus and its Host. Doctorate Dissertation, Yun-
nan University, Kunming, China.
Wei DP, Wanasinghe DN, Hyde KD, Mortimer PE, Xu JC, To-Anun C, Yu FM, Zha LS
(2020) Ophiocordyceps tianshanensis sp. nov. on ants from Tianshan mountains, PR China.
Phytotaxa 464(4): 277–292. https://doi.org/10.11646/phytotaxa.464.4.2
Wen TC, Zhu RC, Kang JC, Huang MH, Tan DB, Ariyawansha H, Hyde KD, Liu H (2013)
Ophiocordyceps xuefengensis sp. nov. from larvae of Phassus nodus (Hepialidae) in Hunan
Prov ince, southern China. Phytotaxa 123(1): 41–50. https://doi.org/10.11646/phyto-
taxa.123.1.2
White TJ, Bruns T, Lee S, Taylor JW (1990) Amplication and direct sequencing of fungal
ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ
(Eds) PCR Protocols: A Guide to Methods and Applications. Academic Press, New York,
315–322. https://doi.org/10.1016/B978-0-12-372180-8.50042-1
Xiao YP, Hongsanan S, Hyde KD, Brooks S, Xie N, Long FY, Wen TC (2019) Two new en-
tomopathogenic species of Ophiocordyceps in ailand. MycoKeys 47: 53–74. https://doi.
org/10.3897/mycokeys.47.29898
Cordyceps species on wireworms 117
Yahagi N (2008) Illustrated catalogue of Japanese Cordyceps (entomogenous fungi): the Yahagi
collection of Japanese Cordyceps stored in the Tohoku University Museum. Bulletin of the
Tohoku University Museum (8): 29–89.
Yamamoto K, Ohmae M, Orihara T (2020) Metarhizium brachyspermum sp. nov. (Clavicipi-
taceae), a new species parasitic on Elateridae from Japan. Mycoscience 61: 37–42. https://
doi.org/10.1016/j.myc.2019.09.001
Yang SB (2004) e Taxonomic Diversity and Conservation of Cordyceps Fr. from Changbai
Mountains. Masters Dissertation, Jilin Agricultural University, Changchun, China.
Zare R, Gams W (2001) A revision of Verticillium section Prostrata, IV, the genera Lecanicil-
lium and Simplicillium gen. nov. Nova Hedwigia 73: 1–50. https://doi.org/10.1127/nova.
hedwigia/73/2001/1
Yaroslavtseva ON, Ageev DV, Bulyonkova TM, Kryukov VY (2019) First records of the en-
tomopathogenic fungus Ophiocordyceps variabilis (Petch) G.H. Sung, J.M. Sung, Hywel-
Jones et Spatafora from Siberia. Euroasian Entomological Journal 18(6): 379–381. https://
doi.org/10.15298/euroasentj.18.6.01
Zha LS, Huang SK, Xiao YP, Boonmee S, Eungwanichayapant PD, McKenzie EHC, Kryukov
V, Wu XL, Hyde KD, Wen TC (2018) An evaluation of common cordyceps species found
in Chinese markets. International Journal of Medicinal Mushrooms 20(12): 1149–1162.
https://doi.org/10.1615/IntJMedMushrooms.2018027330
Zha LS, Ye L, Huang SK, Boonmee S, Eungwanichayapant PD, Hyde KD, Wen TC (2020)
Species diversity and host associations of cordyceps (Hypocreales) parasitic on Orthoptera
insects. Mycosystema 39(4): 407–722. https://doi.org/10.13346/j.mycosystema.190195
Zhang WM, Li TH, Chen VQ, Qu LH (2004) Cordyceps campsosterna, a new pathogen of
Campsosternus auratus. Fungal Diversity 17: 239–242.
Zimmermann G (2008) e entomopathogenic fungi Isaria farinosa (formerly Paecilomyces
farinosus) and the Isaria fumosorosea species complex (formerly Paecilomyces fumosoroseus):
biology, ecology and use in biological control. Biocontrol Science and Technology 18(9):
865–901. https://doi.org/10.1080/09583150802471812
Content uploaded by Vadim Kryukov
Author content
All content in this area was uploaded by Vadim Kryukov on Mar 30, 2021
Content may be subject to copyright.
