Current nomenclatural changes in Cordyceps sensu lato and its multidisciplinary impacts.

Innumerable name changes have occurred in Cordyceps and allied taxa, after the phylogenetic classification of Cordyceps, coupled by the application of one fungus one name after the amendment of ICN. Complying with one fungus one name, many generic names have been protected for monophyletic clades in Clavicipitaceae and Ophiocordycipitaceae that have made tremendous transfer of Cordyceps spp. to both sexual and asexual genera. Species compositions of the accepted genera Ophiocordyceps, Tolypocladium, Metarhizium, Perennicordyceps, Polycephalomyces and Purpureocillium are briefly discussed to update the readers with the current placements of Cordyceps spp. Some examples of frequent name changes of Cordyceps spp. are also mentioned, with reference to use of older scientific names in non-mycological publications.

Phylogenetic classification of Cordyceps

The genus Cordyceps, established by Fries (1818), was traditionally classified in Clavicipitaceae (Hypocreales, Ascomycota) to accommodate insect and fungal parasites, producing elongated, cylindrical or filamentous stromata with perithecioid type of ascocarp and filamentous, multi-septate ascospores. It is a big hypocrealean genus, comprising more than 400 spp. that parasitise numerous orders of insects, including spiders, in majority (Araújo and Hughes 2016; Shrestha et al. 2016). Cordyceps Fr. and allied species are very curious groups of fungi, with long botanical history starting in pre-Linnaean era (Shrestha et al. 2014). Recent molecular phylogenetic studies showed that Cordyceps sensu lato is not monophyletic and is intercepted by plant pathogenic genera Claviceps Tul., Balansia Speg., Epichloë (Fr.) Tul. and C. Tul. within Clavicipitaceae (Sung et al. 2007). Cordyceps sensu stricto was, hence, circumscribed to a clade that consisted of its type species C. militaris (L.) Fr., and new genera were proposed for other clades outside Cordyceps s.s.: Metacordyceps G.H. Sung et al., Elaphocordyceps G.H. Sung et al., Ophiocordyceps G.H. Sung et al. and Tyrannicordyceps Kepler & Spatafora that together accommodated more than 180 Cordyceps spp. (Sung et al. 2007; Kepler et al. 2012b) (Figure 1). Besides transfer of many Cordyceps spp. to new genera, many more Cordyceps spp. (~ 170 spp.) still remain incertae sedis (of uncertain placement) within Hypocreales, because of lack of molecular phylogenetic studies or inconclusive morphological and ecological assessment (Sung et al. 2007).

Figure 1.

Genera segregated from Cordyceps s.l.

Among the new genera, Metacordyceps shared sister relationship with a clade of plant pathogenic genera (Claviceps, Balansia, Epichloë) and were all retained in the family Clavicipitaceae s.s. (Sung et al. 2007). Tyrannicordyceps is a small genus placed within a clade of Balansia, Claviceps and Epichloë, to which all five spp. were transferred from Cordyceps (Kepler et al. 2012b). All the members of Tyrannicordyceps are pathogens of Claviceps stromata. Elaphocordyceps, Ophiocordyceps and other allied genera formed a separate clade and were placed in a new family Ophiocordycipitaceae that formed a sister clade with Clavicipitaceae s.s. (Sung et al. 2007). Cordyceps s.s. and other allied genera Lecanicillium W. Gams & Zare, Engyodontium de Hoog, Simplicillium W. Gams & Zare, Torrubiella Boud. s.s., etc. were placed in a separate family Cordycipitaceae, which formed a sister clade with Hypocreaceae, a family mostly parasitic on other fungi or plants (Sung et al. 2007).

As mentioned above, Cordyceps s.s. was circumscribed to a clade in Cordycipitaceae that consists of its type species C. militaris (Sung et al. 2007). Chinese caterpillar fungus Cordyceps sinensis (Berk.) Sacc., a highly esteemed medicinal herb in traditional Chinese and Ayurvedic medicine that parasitises hepialid larvae in the Tibetan Plateau and the alpine grassland of the Himalayas, was phylogenetically placed in Ophiocordyceps (outside Cordyceps s.s. clade); hence a new combination Ophiocordyceps sinensis (Berk.) G.H. Sung et al. was made with Cordyceps sinensis as its synonym (Sung et al. 2007; Shrestha et al. 2010).

Cordyceps and allied genera within hypocreales

Cordyceps and allied genera, distributed in three families of Hypocreales (Clavicipitaceae, Ophiocordycipitaceae and Cordycipitaceae), are briefly introduced below (Table 1, Figure 1).

Table 1.

Cordyceps and allied genera distributed in Clavicipitaceae, Cordycipitaceae and Ophiocordycipitaceae.

Family	Sexual (teleomorph) genera	Asexual (anamorph) genera
Clavicipitaceae s.s.	Conoideocrella, Hypocrella, Metacordyceps, Moelleriella, Orbiocrella, Regiocrella, Samuelsia, Tyrannycordyceps	Aschersonia, Metarhizium
Cordycipitaceae	Ascopolyporus, Cordyceps s.s., Hyperdermium, Torrubiella s.s.	Akanthomyces, Beauveria, Engyodontium, Gibellula, Isaria, Lecanicillium, Microhilum, Parengyodontium, Simplicillium
Ophiocordycipitaceae	Elaphocordyceps, Ophiocordyceps, Podocrella	Drechmeria, Harposporium, Hirsutella, Hymenostilbe, Paraisaria, Polycephalomyces, Purpureocillium, Syngliocladium, Tolypocladium

Clavicipitaceae

Besides Metacordyceps and Tyrannicordyceps, six other sexual genera Conoideocrella D. Johnson et al., Hypocrella Sacc., Moelleriella Bres., Orbiocrella D. Johnson et al., Regiocrella P. Chaverri & K.T. Hodge and Samuelsia P. Chaverri & K.T. Hodge are placed in this family (Sung et al. 2007; Chaverri et al. 2008; Johnson et al. 2009) (Table 1). All of them are parasitic on scale insects or white flies. Similarly, asexual genera placed in this family are Aschersonia Mont. and Metarhizium Sorokīn (Sung et al. 2007) (Table 1). Among teleomorphic genera, Conoideocrella and Orbiocrella were formerly classified in Torrubiella s.l. (Johnson et al. 2009). Other four genera Hypocrella, Moelleriella, Regiocrella and Samuelsia are linked to Aschersonia or Aschersonia-like anamorphs (Chaverri et al. 2005a, 2008).

Cordycipitaceae

Besides Cordyceps s.s., three other sexual genera are placed in this family, Ascopolyporus Möller, Hyperdermium J. White et al. and Torrubiella s.s. (Sung et al. 2007; Johnson et al. 2009) (Table 1). They are parasites of scale insects or spiders. Similarly, nine asexual genera placed in this family are Akanthomyces Lebert, Beauveria Vuill., Engyodontium, Gibellula Cavara, Isaria Pers., Lecanicillium, Microhilum H.Y. Yip & A.C. Rath, Parengyodontium C.-C. Tsang et al. and Simplicillium (Sung et al. 2007; Johnson et al. 2009; Vega et al. 2012; Tsang et al. 2016) (Table 1). Among them, Akanthomyces, Beauveria, Isaria, Lecanicillium and Microhilum are linked to Cordyceps, and Gibellula is linked to Torrubiella s.s.

Ophiocordycipitaceae

Elaphocordyceps, Ophiocordyceps and Podocrella Seaver are sexual genera placed in Ophiocordycipitaceae (Sung et al. 2007; Kirk et al. 2013) (Table 1). Anamorphic genera placed in this family are Drechmeria W. Gams & H.B. Jansson, Harposporium Lohde, Hirsutella Pat., Hymenostilbe Petch, Paraisaria Samson & B.L. Brady, Polycephalomyces Kobayasi, Purpureocillium Luangsa-ard et al., Syngliocladium Petch and Tolypocladium W. Gams (Sung et al. 2007; Luangsa-Ard et al. 2011; Quandt et al. 2014) (Table 1). Among them, Hirsutella, Hymenostilbe, Paraisaria and Syngliocladium are linked to Ophiocordyceps (Quandt et al. 2014). Among Elaphocordyceps spp., only E. subsessilis (Petch) G.H. Sung et al. is known to have Tolypocladium anamorph (Quandt et al. 2014). Podocrella is linked to Harposporium, which is mainly known from nematodes (Chaverri et al. 2005b).

Current placement of Cordyceps spp. following amendment of article 59 of ICN (one fungus one name)

It is clear from above that the genus Cordyceps was split into several phylogenetic genera and many name changes occurred after transfer of Cordyceps spp. to new genera (Sung et al. 2007; Kepler et al. 2012b). However, the name changes did not stop there. In April 2011, Amsterdam Declaration decided on one fungus one name that eventually amended Art. 59 of the Botanical Code (renamed as International Code of nomenclature for algae, fungi, and plants (ICN) by the 18th International Botanical Congress held in Melbourne in July 2011, also known as Melbourne Code) to eliminate the dual naming of fungi typified by their sexual and asexual states, effective on 1 January 2013 (Hawksworth et al. 2011; McNeill et al. 2012). The newly amended ICN has significant implications on plant pathogenic fungi (Wingfield et al. 2012; Zhang et al. 2013), medically important fungi (De Hoog et al. 2015) as well as hypocrealean entomopathogenic fungi (Kepler et al. 2013, 2014; Quandt et al. 2014; Spatafora et al. 2015; Humber 2016). Following one fungus one name, only a single generic name regardless of its state will be protected or accepted for a monophyletic clade against all other generic names available in that clade based on nomenclatural priority in principle, so that a single scientific name can be given to a single species. Recently, single generic names have been protected for monophyletic clades of invertebrate pathogens in Ophiocordycipitaceae and Clavicipitaceae. The protected names that accommodate former Cordyceps spp. are briefly discussed below (Figure 2).

Figure 2.

Cordyceps spp. transferred to other genera following one fungus one name. * = total no. of spp. accommodated in a genus, # = no. of spp. transferred from Cordyceps.

Cordyceps s.s. currently comprises around 50 spp. (Figure 2). Recently, two new spp. with cordyceps-like sexual states were named as Beauveria spp. (Beauveria gryllotalpidicola Luangsa-ard et al. and B. loeiensis Luangsa-ard et al.) based on their phylogenetic placement in Beauveria clade within Cordyceps (Ariyawansa et al. 2015) (Figure 2).

Complying with one fungus one name, many sexually and asexually typified generic names are protected for monophyletic clades in Ophiocordycipitaceae. They are Drechmeria, Harposporium, Ophiocordyceps, Perennicordyceps Matočec & Kušan, Polycephalomyces, Purpureocillium and Tolypocladium (Kepler et al. 2013; Matočec et al. 2014; Quandt et al. 2014; Spatafora et al. 2015). All the protected genera in Ophiocordycipitaceae include Cordyceps spp. Species compositions of the protected genera are briefly discussed below.

Ophiocordyceps

It is the largest genus in Ophiocordycipitaceae with 214 spp. Among them, 194 spp. are transferred from Cordyceps or are typified by cordyceps-like sexual states (Figure 2). Besides Cordyceps or cordyceps-like spp., Ophiocordyceps includes other spp. transferred from sexual and asexual genera, based on their phylogenetic placement (Figure 3). Among sexual spp., two spp. from each Podonectria Petch and Torrubiella were transferred to Ophiocordyceps (Spatafora et al. 2015) (Figure 3). Similarly, many other asexually typified spp. were transferred to Ophiocordyceps such as nine Hymenostilbe spp., five Syngliocladium spp. and one sp. from each Paraisaria and Stilbella Lindau (Spatafora et al. 2015) (Figure 3). Ophiocordyceps thus consists of both sexually and asexually typified spp. For such genera as Ophiocordyceps, Metarhizium, Tolypocladium, alternative or suppressed generic names retain the role of morphological descriptors as suggested by Gams (2016).

Figure 3.

Species composition of Ophiocordyceps.

Tolypocladium

As mentioned above, Elaphocordyceps was erected to accommodate 24 Cordyceps spp., mostly growing on Elaphomyces fungi, and few on cicada nymphs and coleopteran larva (Sung et al. 2007). One of them, Elaphocordyceps subsessilis, is linked to Tolypocladium, T. inflatum W. Gams. Tolypocladium was originally established by Gams (1971) to encompass soil-borne asexual fungi and currently consists of 27 spp. (Figure 2). In order to comply with one fungus one name, Tolypocladium was protected against Elaphocordyceps and Chaunopycnis W. Gams, another asexually typified genus in the same clade (Quandt et al. 2014) (Figure 4). All 24 Elaphocordyceps spp. (including E. subsessilis) and 3 Chaunopycnis spp. were transferred to Tolypocladium (Quandt et al. 2014) (Figures 2 and 4).

Figure 4.

Species composition of Tolypocladium. * indicates the no. of spp. transferred from one genus to another.

Perennicordyceps

Matočec and Kušan established a new genus Perennicordyceps to encompass four spp. in Polycephalomyces (Matočec et al. 2014) (Figures 2 and 5). All four spp. in Perennicordyceps were previously classified in either Cordyceps (C. cuboidea Kobayasi & Shimizu, C. prolifica Kobayasi and C. ryogamiensis Kobayasi & Shimizu) or Ophiocordyceps (O. paracuboidea S. Ban et al.) (Figure 5). All spp. were first placed in Ophiocordyceps (Sung et al. 2007; Ban et al. 2009) and then transferred to Polycephalomyces (Kepler et al. 2013) prior to transfer to Perennicordyceps (Matočec et al. 2014) (Figure 5).

Figure 5.

Species composition of Perennicordyceps. * indicates the no. of spp. transferred from one genus to another.

Purpureocillium

Purpureocillium was recently erected to delimit a Paecilomyces sp., P. lilacinus (Thom) Samson and closely allied taxa (Luangsa-Ard et al. 2011). Currently, there are four spp. in Purpureocillium (Figure 2). Among them, C. ryogamimontana Kobayasi & Shimizu (current name Purpureocillium takamizusanense (Kobayasi) S. Ban et al.) and C. cylindrica Petch (current name Purpureocillium atypicolum (Petch) Spatafora et al.) were recently transferred from Cordyceps based on their phylogenetic placement in Purpureocillium (Luangsa-Ard et al. 2011; Ban et al. 2015; Spatafora et al. 2015).

Polycephalomyces

It is an asexually typified genus proposed by Kobayasi (1941). It was recently amended by Kepler et al. (2013) and more recently by Matočec et al. (2014) in more strict sense. Currently, there are 11 spp. in this genus, of which three spp. were transferred from Cordyceps, C. kanzashiana Kobayasi & Shimizu (current name Polycephalomyces kanzashianus (Kobayasi & Shimizu) Kepler & Spatafora), C. nipponica Kobayasi (current name P. nipponicus (Kobayasi) Kepler & Spatafora) and C. ramosopulvinata Kobayasi & Shimizu (current name P. ramosopulvinatus (Kobayasi & Shimizu) Kepler & Spatafora) (Kepler et al. 2013) (Figures 2 and 6).

Figure 6.

Species composition of Polycephalomyces. * indicates the no. of spp. transferred from one genus to another.

Drechmeria and harposporium

Drechmeria was originally established by Gams and Jansson (1985) to accommodate asexual endoparasitic nematophagous fungi. It currently consists of 12 spp., including one Cordyceps sp., C. gunnii (Berk.) Berk. (current name Drechmeria gunnii (Berk.) Spatafora et al.) (Spatafora et al. 2015) (Figure 2). Harposporium is also an asexually typified genus, originally described by Lohde (1874) for nematophagous fungi. It currently consists of 37 spp., with one sp. transferred from Cordyceps, C. peltata Wakef. (current name Harposporium peltatum (Wakef.) Spatafora & Kepler) based on its phylogenetic placement (Spatafora et al. 2015) (Figure 2).

Metarhizium is a protected generic name in Clavicipitaceae that comprises spp. previously classified in Cordyceps. Metarhizium currently consists of 25 spp. Among them, 13 spp. were transferred from Cordyceps or Metacordyceps to Metarhizium, complying with one fungus one name (Figures 2 and 7). As shown in Figure 7, among 11 spp. transferred from Cordyceps, nine spp. were first transferred from Cordyceps to Metacordyceps prior to transfer to Metarhizium (Sung et al. 2007; Kepler et al. 2012a, 2014). Another sp. was first transferred from Cordyceps to Ophiocordyceps and then finally to Metarhizium (Sung et al. 2007; Kepler et al. 2014). The remaining sp. was first transferred from Cordyceps to Ophiocordyceps and then to Metacordyceps prior to transfer to Metarhizium (Sung et al. 2007; Kepler et al. 2012a, 2014). Two more Metacordyceps spp. were transferred to Metarhizium, following one fungus one name (Kepler et al. 2014) (Figure 7).

Figure 7.

Species composition of Metarhizium. * indicates the no. of spp. transferred from one genus to another.

Incertae sedis within hypocreales

Besides nearly 170 Cordyceps spp. incertae sedis within Hypocreales, Sphaerocordyceps Kobayasi also belongs to this group (Kobayasi 1981; Sung et al. 2007) (Figure 2). Sphaerocordyceps comprises three spp., all transferred from Cordyceps, C. helopis Quél. (current name S. helopis (Quél.) Kobayasi), C. palustris Berk. & Broome (current name S. palustris (Berk. & Broome) Kobayasi) and C. ussuriensis Koval (current name S. ussuriensis (Koval) Kobayasi).

Impact of one fungus one name on nomenclature of Cordyceps spp.

The use of entomopathogenic fungi is getting wider due to their economic and environmental importance. Several species of Cordyceps are highly regarded as medicinal herbs in oriental medicine in Asia and have been successfully cultivated for commercial application. Other entomopathogenic fungi, asexual spp. in particular, have been successfully used for biological control of insects and pests. Professionals such as biochemists, pharmacologists, alternative (traditional) medicine practitioners, drug researchers, biocontrol researchers, insect pathologists, forest pathologists and entomologists are widely involved in the research and use of entomopathogenic fungi, besides mycologists.

To cope with name changes of fungal spp., different authors have suggested for the smooth application of one fungus one name for the benefit of their user groups, such as plant pathogenic fungi and medically important fungi (Wingfield et al. 2012; Zhang et al. 2013; De Hoog et al. 2015). De Hoog et al. (2015) have cautioned that nomenclatural changes of medically important fungi may take decades to gain wide acceptance and have suggested some delay in following name changes. With respect to hypocrealean invertebrate-parasitic fungi, Kepler et al. (2013, 2014), Quandt et al. (2014) and Spatafora et al. (2015) have vastly contributed to the application of one fungus one name.

The name changes have been two-fold for hypocrealean invertebrate-parasitic fungi in recent years that have caused multiple name changes within a short duration in some cases: the first one based on the phylogenetic arrangement of Cordyceps spp. and the second one based on the application of one fungus one name. The phylogenetic arrangement of Cordyceps spp. has been discussed above. The name changes following one fungus one name are more diverse. They are briefly discussed here with reference to multiple name changes from Cordyceps to Perennicordyceps, for instance (Figure 8). Cordyceps cuboidea and C. ryogamiensis were transferred to Ophiocordyceps following the phylogenetic split of genus Cordyceps and were renamed as Ophiocordyceps cuboidea and O. ryogamiensis, respectively (Sung et al. 2007). After the application of one fungus one name, they were again named as Polycephalomyces cuboideus and Po. ryogamiensis as Polycephalomyces was protected for a clade where O. cuboidea and O. ryogamiensis were placed (Kepler et al. 2013). However, the clade that included Polycephalomyces cuboideus and Po. ryogamiensis was again delineated as a separate genus Perennicordyceps and consequently the spp. were renamed as Perennicordyceps cuboidea and Pe. Ryogamiensis, respectively (Matočec et al. 2014). De Hoog et al. (2015) recently opined that when clade system is used for naming, there is no delimitation criterion and that when a genus becomes nearly congruent to species, then it becomes a redundant rank.

Figure 8.

Multiple transfers of Cordyceps spp. from one genus to another. * indicates the no. of spp. transferred from one genus to another.

Perennicordyceps cuboidea (Kobayasi & Shimizu) Matočec et al. (2014)

Basionym: Cordyceps cuboidea Kobayasi & Shimizu (1980)

Synonyms: Ophiocordyceps cuboidea (Kobayasi & Shimizu) S. Ban et al. (2009).

Polycephalomyces cuboideus (Kobayasi & Shimizu) Kepler et al. (2013)

Perennicordyceps ryogamiensis (Kobayasi & Shimizu) Matočec et al. (2014)

Basionym: Cordyceps ryogamiensis Kobayasi & Shimizu (1983)

Synonyms: Ophiocordyceps ryogamiensis (Kobayasi & Shimizu) G.H. Sung et al. (2007)

Polycephalomyces ryogamiensis (Kobayasi & Shimizu) Kepler et al. (2013)

Minnis (2015) has rightly pointed out that due to frequent name changes, the users of fungal names get frustrated. Few examples are shown here where older names of Cordyceps spp. are being used in non-mycological publications despite nomenclatural changes. Cordyceps sinensis was established by Saccardo (1883) during the taxonomic revision of Cordyceps that was recently transferred to Ophiocordyceps resulting in O. sinensis as its currently accepted name, after the phylogenetic classification of Cordyceps (Sung et al. 2007) and is now widely accepted by the mycological community. However, the older name C. sinensis is still in frequent use in non-mycological publications (Yan et al. 2014; Yan and Wu 2014; Yu et al. 2016), despite its recent nomenclatural change. Similarly, C. ophioglossoides (Sun et al. 2014) and C. sobolifera (Yang and Zhang 2016) are used in publications, in spite of their recent nomenclatural changes. Though non-mycologists know the name changes, they may ignore in publications. Editors or reviewers of non-mycological journals may also simply not be aware of current nomenclatural changes of fungal species or may not put much emphasis on names changes. It is also true that non-mycologists may not be aware of worldwide online databases of fungi such as MycoBank, IndexFungorum and Fungal Names to be update with the fungal name changes. The more rapidly the name changes take place, other professionals will simply feel safe by using older names.