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Introduction
Cordyceps sensu lato (s.l.) is a paraphyletic group of Ascomycete fungi comprising approximately 1 000 species (Wei et al. 2020). The members of the group present multiple lifestyles, parasitizing arthropods, grasses, or hypogeous fungi (Sung et al. 2007a, 2007b) while some are saprotrophs or endophytes (Gazis et al. 2014), that includes fungal species of agricultural importance. Asexual stages are important as biological control of several pest and vector insects. Metarhizium has been used to control many groups of the insects in many countries, for example to control Aeneolamia varia (“salivazos”), which affects alfalfa and sugar cane cultivars in Brazil (Alves et al. 2008), and to control of Anopheles mosquitoes, which are vector of malaria (Scholte et al. 2005). Akanthomyces sabanensis (=Lecanicillium sabanense) parasitizes Pulvinaria caballeroramosae females that, in turn, parasitize Ficus suatensis in Colombia (Chiriví-Salomón et al. 2015). In Florida, USA, Beauveria bassiana has been used to control the whitefly Bemisia tabaci (Sani et al. 2020). This host species is considered by the International Union for Conservation of Nature (IUCN) as an invasive pest in North America that affects crops such as alfalfa, broccoli, cabbage, cotton, tomato, squash, peanut, and watermelon, among others (Quesada-Moraga et al. 2006; SEDECO 2014).
Cordyceps s.l. also comprises species with edible and medicinal properties. Cordyceps militaris, C. pruinosa, C. tenuipes, Isaria cicadae, Ophiocordyceps sinensis, and Tolypocladium ophioglossoides, among others are appreciated as edible and medicinal in Asia and are considered as functional foods since they produce metabolites beneficial to health (Ng and Wang 2005, Zhang et al. 2018). Different species of Cordyceps s.l. have antioxidant, anti-cancer, antihyperlipidemic, anti-diabetic, anti-fatigue, anti-aging, anti-depressant, and aphrodisiac properties, since they produce various biomolecules including nucleosides such as cordycepin, sterols, flavonoids, cyclic peptides, phenolic, bioxanthracenes, polyketides, and alkaloids (Das et al. 2021). Cordycepin (3´-deoxyadenosine), a nucleoside analogue of adenosine, is a well-studied metabolite, since it presents some of the properties described above. Its presence and quantity are considered indicators of the quality of the Cordyceps products (Lee et al. 2019).
Isaria cicadae is a species of great cultural importance, which has been used in China for about 1 600 years (Hsu et al. 2015). Another species of cultural, medicinal, and economic importance is Ophiocordyceps sinensis. Known in Tibet as “winter worm” or “summer grass”, this species parasitizes larvae of the moths Thitarodes/Hepialus spp. (Wu et al. 2020). Its distribution is restricted to the Tibetan plateau in the Himalayas at over 5 000 m, and its overexploitation has led to a decline in its populations (Winkler 2009, Kumar et al. 2010, Shrestha 2011). O. sinensis currently has a high economic value worldwide, indeed it was marketed at up to $60 000 USD per kg in 2015 (Lei et al. 2015). Consequently, the IUCN has classed it as vulnerable (VU) (Yang 2020).
Artificial cultivation of O. sinensis is challenging; however, C. militaris can be used as a substitute for O. sinensis and is cultivated at industrial scale (Shrestha et al. 2010). Cordyceps militaris has biological activities, including as an antimalarial, hypoglycemic, anti-cancer, immunomodulatory, antidiabetic, and antiviral against severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) (Khan et al. 2010, Jedrejko et al. 2021).
In Mexico, there is a lack of knowledge regarding the diversity of species of Cordyceps s.l. and research topics have been mainly limited to list or records with descriptions using traditional taxonomy, doing little to facilitate their potential exploitation. Therefore, the objectives of this review were to analyze the records of these fungi cited in Mexico, and list the diversity, hosts, and geographical distribution of the Cordyceps s.l.
Material and methods
This paper analyzes the published information pertaining to Cordyceps s.l. in Mexico. To achieve this, a list of the species recorded in the different states of the country was created through a review of the scientific literature published from 1864 to 2022. Bibliographic reviews as Chacón and Guzmán (1983), or those included in Rubio-Bustos et al. (1999) and Guzmán et al. (2001) were checked. The review of the first reports of entomopathogenic fungi was conducted in the Historical Collection of the Institute of Biology of the National Autonomous University of Mexico (UNAM). We also looked for records of anamorphic states of Cordyceps s.l. used as biological controls. The keywords used in the query were: entomopathogenic fungi, biological control, Beauveria, Cordyceps, Isaria, Metarhizium, Paecilomyces, Paraisaria, and Tolypocladium. Scientific names and their authors were standardized according to the nomenclature published in the Index Fungorum portal (http://www.indexfungorum.org). Geographic distribution maps of Clavicipitaceae, Cordycipitaceae, and Ophiocordycipitaceae were generated with QGIS 3.18.1 Software (QGIS 2021), using presence records from the studies listed in Tables 1, 2, and 3. The dataset for land use and vegetation cover, available from the Mexican National Institute of Statistics and Geography (INEGI 1992), was used with at scale 1:250,000. The coordinate system MEXICO ITRF 2008 LCC was used, along with the Lambert Conformal Conic and Datum projection (https://www.inegi.org.mx/app/biblioteca/ficha.html?upc=702825007020).
Table 1 Clavicipitaceae species recorded in the literature from Mexico
| Metarhizium acridum |
| (Driver & Milner) J.F. Bisch., S.A. Rehner & Humber |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Orthoptera, Acrididae, Schistocerca piceifrons in laboratory assays; Pyrgomorphidae, Sphenarium purpurascens (adults) in field experiments. |
|
Vegetation |
| Agricultural areas with crops such as amaranth, beans, eggplant, maize, and squash, grass and soil. |
|
State (reference) |
| Without locality (Barrientos-Lozano et al. 2005), Puebla (Guerrero-Guerra et al. 2013), Colima (Serna-Domínguez et al. 2019). |
|
M. anisopliae |
| (Metschn.) Sorokin |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Arachnida, Trombidiformes, Tetranychidae, Tetranichus urticae; Ixodidae, *Boophilus microplus in field experiments with bovine; Co leoptera, Curculionidae, Hypothenemus hampei (adults); Scarabaeidae, Anomala sp., Macrodactylus murinus, Paranomala sp. (larvae), Phyllophaga vetula (larvae) in laboratory assays, Phyllophaga spp. (larvae) in laboratory assays; Tenebrinidae, Tenebrio molitor (larvae) in laboratory assays; Hemiptera; Aleyrodidae, *Bemisia tabaci (nymph) in laboratory assays; Cercopidae, *Aeneolamia spp., A. postica; Livii dae, *Diaphorina citri (adults and nymphs) in field experiments; Reduviidae, *Meccus pallidipennis (adults), *Triatoma dimidiata (adults and nymphs) in laboratory assays; Triozidae, *Bactericera cockerelli (nymph) in laboratory assays; Lepidoptera; Pyralidae, Galleria mellonella (larvae) in laboratory assays; Crambidae, Diatraea saccharalis, D. magnifactella; Noctuidae, Spodoptera frugiperda in laboratory assays; Orthoptera, Acrididae, Schistocerca piceifrons; Romaleidae, Brachystola magna (adults) in laboratory assays; Thysanoptera, Thripidae, Frankliniella occidentalis (larvae) in laboratory assays; Diptera, Culicidae, Aedes aegypti (eggs) in laboratory assays. |
|
Vegetation |
| Agricultural areas with crops such as bean, citrus, ebo, maize, oatmeal and, wheat. Coffee and sugar cane plantations. Agroecosystem of Citrus aurantifolia, C. grandis, Saccharum officinalis, and Mangifera indica. Soil. |
|
State (references) |
| Chiapas (De la Rosa et al. 2000; Bautista Gálvez et al. 2017; Torres-Estrada et al. 2020), Tabasco (Bautista-Gálvez and González-Cortes 2005; Hernández-Domínguez et al. 2016; Bautista-Gálvez et al. 2017; Brunner-Mendoza et al. 2017, 2018), Veracruz (Alonso-Díaz et al. 2007; Carrillo-Benítez et al. 2013; Hernández-Domínguez et al. 2016; Brunner-Mendoza et al. 2017, 2018; Navarro-Barranco et al. 2019), without locality (Lezama-Gutiérrez et al. 2012, Vázquez-Martínez et al. 2014), Colima (Carrillo-Benítez et al. 2013; Lezama-Gutiérrez et al. 2014; Serna-Domínguez et al. 2019; Ramírez-Milanes et al. 2022), Guanajuato (Carrillo-Benítez et al. 2013; Cabrera-Mora et al. 2019), Quintana Roo (Carrillo-Benítez et al. 2013), Chihuahua (Rios Velasco et al. 2014; Bustillos-Rodríguez et al. 2016), Nayarit (Bustillos-Ro dríguez et al. 2016), San Luis Potosí (Flores-Villegas et al. 2016; Hernández-Domínguez et al. 2016; Brunner-Mendoza et al. 2017, 2018; Navarro-Barranco et al. 2019), Oaxaca (Hernández-Domínguez et al. 2016; Brunner-Mendoza et al. 2017, 2018; Navarro-Barranco et al. 2019), Morelos (Solis-Perez et al. 2016), Estado de México (Alcantara-Vargas et al. 2020) |
|
*Considered vectors of bacteria, parasites or viruses. |
|
M. brunneum |
| Petch |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Lepidoptera, Pyralidae, Galleria mellonella (larvae) |
|
Vegetation |
| Agricultural areas with crop of bean and avocado plantations. Soil |
|
State (references) |
| Colima (Serna-Domínguez et al. 2019), Puebla (Cabrera-Mora et al. 2019), |
|
M. guizhaense |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Coleoptera, Lepidoptera, Pyralidae, Galleria mellonella; Noctuidae, Spodoptera frugiperda; Orthoptera, Romaleidae, Brachys tola magna (adults) in laboratory assays. |
|
Vegetation |
| Agricultural areas with crop of maize and avocado plantations. Soil. |
|
State (references) |
| Chihuahua (Bustillos-Rodríguez et al. 2016), Colima (Brunner-Mendoza et al. 2017, 2018; Serna-Domínguez et al. 2019), Nayarit (Brun ner-Mendoza et al. 2017, 2018). |
|
M. humberi |
| C. Luz, L. Rocha & I. Delalibera |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Lepidoptera |
|
Vegetation |
| Tropical gallery forest in a cerrado ecosystem and soil. |
|
State (references) |
| Tamaulipas and Oaxaca (Luz et al. 2019) |
|
M. pemphigi |
| (Driver & Milner) Kepler, Humber & S.A. Rehner |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Unspecified |
|
Vegetation |
| Coffee plantations |
|
State (references) |
| Colima (Serna-Domínguez et al. 2019) |
|
M. pinghaense |
| Q.T. Chen & H.L. Guo |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Coleoptera, Scarabaeidae, Anomala cincta, Phyllophaga spp. (larvae) and white grubs; Lepidoptera, Pyralidae, Galleria mellonella; |
| Orthoptera, Romaleidae, Brachystola magna (adults) in laboratory assays |
|
Vegetation |
| Agricultural areas with crop as bean, and maize. Avocado plantations and soil |
|
State (references) |
| Guanajuato (Guzmán-Franco et al. 2012; Carrillo-Benítez et al. 2013), Puebla (Guzmán-Franco et al. 2012), Chihuahua (Bustillos-Rodríguez et al. 2016), Morelos (Brunner-Mendoza et al. 2017, 2018), Colima (Serna-Domínguez et al. 2019) |
|
M. robertsii |
| J.F. Bisch., S.A. Rehner & Humber |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Coleoptera, Scarabaeidae, Phyllophaga spp. (larvae) and white grubs; Lepidoptera, Pyralidae, Galleria mellonella; Orthoptera, Romaleidae, Brachystola magna (adults) in laboratory assays. |
|
Vegetation |
| Agricultural areas with crop as bean, blackberry and, maize. Avocado plantations, tejocote orchard and soil |
|
State (references) |
| Without locality (Carrillo-Benítez et al. 2013; Serna-Domínguez et al. 2019), Guanajuato (Pérez-González et al. 2014), Puebla (Muñiz-Reyes et al. 2014; Cabrera-Mora et al. 2019), Chihuahua and Nayarit (Bustillos-Rodríguez et al. 2016), Jalisco and Morelos (Brunner-Mendoza et al. 2017, 2018), Colima (Brunner-Mendoza et al. 2017, 2018; Serna-Domínguez et al. 2019) |
Table 2 Cordycipitaceae species recorded in the literature from Mexico
| Akanthomyces tuberculatus |
| (Lebert) Spatafora, Kepler & B. Shrestha |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Lepidoptera, Sphingidae (adults) |
|
Vegetation |
| Agricultural areas with citrus |
|
State (references) |
| Tamaulipas (Sánchez-Peña 1990) |
|
Beauveria bassiana |
| (Bals. -Criv) Vuill. |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Arachnida, Ixodida, Ixodidae, *Rhicephalus microplus; Insecta, Coleoptera, Scarabaeidae, Anomala cincta, Phyllophaga polyphilla; Curcu lionoidea, Hypothenemus hampei, Scyphophorus acupunctatus (larvae); Diptera, Tephritidae, Rhagoletis pomonella (larvae and pupae); Hemiptera, Triozidae, *Bactericera cockerelli; Aleyrodidae, *Bemisia tabaci; Liviidae,*Diaphorina citri; Reduviidae,*Triatoma dimidiate; Lepidoptera, Pyraloidea, Galleria mellonella; Noctuidae, Spodoptera exigua (larvae and pupae); Orthoptera, Romaleidae, Brachystola magna (adults); Thysanoptera, Thripidae, *Frankliniella occidentalis (nymph and adults) |
|
Vegetation |
| Agricultural areas with crops such as coffee, lemon, maize, and tejocote orchad, grassland and soil |
|
State (references) |
| Chiapas (De la Rosa et al. 2000; Bautista Gálvez et al. 2017), Chihuahua (Barajas et al. 2011; Rios-Velasco et al. 2014; Bustillos-Rodríguez et al. 2016), Coahuila (Sánchez-Peña et al. 2011), Morelos (Hernández-Velázquez et al. 2011), Guanajuato (Guzmán-Franco et al. 2012; Pé rez-González et al. 2014; Cabrera-Mora et al. 2019), Jalisco & Oaxaca (Carrillo-Benítez et al. 2013), Colima (Lezama-Gutiérrez et al. 2014), without locality (Lezama-Gutiérrez et al. 2012), Estado de México (Muñiz-Reyes et al. 2014), Puebla (Muñiz-Reyes et al. 2014; Cabrera-Mora et al. 2019), Michoacán (García-Munguía et al. 2015), Nayarit (Bustillos-Rodríguez et al. 2016), Tabasco (Bautista-Gálvez et al. 2017), Ta maulipas (Gandarilla-Pacheco et al. 2021) |
|
*Considered vectors of bacteria, parasites or viruses |
|
Beauveria pseudobassiana |
| S.A Rehner & Humber |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Coleoptera, Scarabaeidae, Cyclocephala, Phyllophaga spp., Phyllophaga polyphilla, and unidentified white grubs (larvae) in labo ratory assays; Diptera, Tephritidae, Rhagoletis pomonella (larvae and pupae) in laboratory assays. |
|
Vegetation |
| Agricultural areas with crops such as bean, maize,and tejocote orchard, grassland and soil |
|
State (references) |
| Guanajuato (Carrillo-Benítez et al. 2013; Pérez-González et al. 2014; Cabrera-Mora et al. 2019), Puebla (Carrillo-Benítez et al. 2013; Mu ñiz-Reyes et al. 2014; Cabrera-Mora et al. 2019), Estado de México (Muñiz-Reyes et al. 2014) |
|
Beauveria scarabaeidicola |
| (Kobayasi) S.A. Rehner & Kepler |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Coleoptera, Scarabaeidae, Melolonthinae, and Dynastinae (adults) |
|
Vegetation |
| Quercus-Pinus forest, ecotone between shrubby secondary vegetation of Juniperus forest, agricultural zone and, secondary bushy vege tation of Quercus forest |
|
State (references) |
| Estado de México (Pérez-Villamares et al. 2017, as Cordyceps scarabaeicola) |
|
Cordyceps farinosa |
| (Holmsk.) Kepler, B. Shrestha & Spatafora |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Lepidoptera (pupae) |
|
Vegetation |
| - |
|
State (references) |
| Morelos (Pérez-Silva 1977; Guzmán et al. 2001, as Isaria farinosa), Oaxaca (Pérez-Silva 1977, 1979, Guzmán et al. 2001, as Isaria farinosa) |
|
Cordyceps fumosorosea |
| (Wize) Kepler, B. Shrestha & Spatafora |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Orthoptera, Tetigonidae (adults); Hemiptera, Aleyrodidae, Bermicia sp.; Reduviidae, Meccus pallidipennis (nymphs) in laboratory assays |
|
Vegetation |
| Agricultural areas with crops such as citrus and watermelon |
|
State (references) |
| Veracruz (Pérez-Silva 1978, as Paecilomyces fumoso-roseus), Colima (Flores-Villegas et al. 2016, as Isaria fumosorosea), without locality (Lezama-Gutiérrez et al. 2012, as Isaria fumosorosea) |
|
Cordyceps mexicana |
| L. López-Rodríguez, C. Burrola-Aguilar & R. Garibay-Orijel |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Lepidoptera; Hemileucinae, Paradirphia sp. (pupae) |
|
Vegetation |
| Oak and mixed oak-pine forests |
|
State (references) |
| Estado de México (López-Rodríguez et al. 2022) |
|
Cordyceps militaris |
| (L.) Fr. |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Lepidoptera, Geometridae, Noctuidae, and Sphingidae (larvae and pupae) Coleoptera (adults) (only one record by Castro et al., 2012) |
|
Vegetation |
| Quercus forest, Quercus-Pinus forest, mesophytic and Abies-Pseudotsuga mixed forests, deciduous forest, agricultural zone, grassland and, secundary bushy vegetation of Quercus forest |
|
State (references) |
| Jalisco (Mains 1958; Guzmán-Dávalos and Nieves 1984; Guzmán-Dávalos 1992, as Cordyceps sobolifera; Rubio-Bustos et al. 1999; Guz mán et al. 2001; Gándara et al. 2014), without locality (Guzmán 1977), Hidalgo (Pérez-Silva 1977), Morelos (Pérez-Silva 1977; Rubio-Bustos et al. 1999; Castro et al. 2012), Oaxaca (Pérez-Silva 1977; Rubio-Bustos et al. 1999), Veracruz (Pérez-Silva 1977; Rubio-Bustos et al. 1999), Chiapas (Chacón and Guzmán 1984; Rubio-Bustos et al. 1999; Guzmán et al. 2001), Estado de México (Frutis et al. 1985; Rubio-Bustos et al. 1999; Pérez-Villamares et al. 2017), Michoacán (Díaz-Barriga et al. 1988; Rubio-Bustos et al. 1999, based on the literature), Sonora (Pérez-Silva et al. 1996), Sinaloa (Rubio-Bustos et al. 1999), Nuevo León (Guzmán et al. 2001) |
|
Cordyceps polyarthra |
| Möller |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Lepidoptera (pupae) |
|
Vegetation |
| Tropical forest with some Quercus and deciduous tropical forest |
|
State (references) |
| Jalisco (Rubio-Bustos et al. 1999) |
|
Cordyceps pruinosa |
| Petch |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| - |
|
Vegetation |
| Tropical rain forest |
|
State (references) |
| Quintana Roo (Guzmán et al. 2001) |
|
Cordyceps takaomontana |
| Yakush. & Kumaz. |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Lepidoptera (larvae and pupae) |
|
Vegetation |
| Quercus-Pinus forest, secundary bushy vegetation of Quercus forest, ecotone between shrubby secondary vegetation of Juniperus forest and agricultural zone |
|
State (references) |
| Estado de México (Pérez-Villamares et al. 2017) |
|
Cordyceps tenuipes |
| (Peck) Kepler, B. Shrestha & Spatafora |
| Host: Class, Order, family, species (larvae, pupae or adult). Insecta, unidentified (pupae) |
| Insecta, unidentified (pupae) |
|
Vegetation |
| Mesophyll forest |
|
State (references) |
| Veracruz (López and García 2002b) |
|
Isaria cicadae |
| Miq. 1838 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Hemiptera, Cicadidae (pupae) |
|
Vegetation |
| - |
|
State (references) |
| Jalisco (Petch 1934, 1941-1942) |
Table 3 Ophiocordycipitaceae species recorded in the literature from Mexico
| Hirsutella citriformis |
| Speare 1920 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Hymenoptera, Liviidae, *Diaphorina citri (adults and nymphs) |
|
Vegetation |
| Citrus agricultural areas |
|
State (references) |
| Campeche, Chiapas, Colima, Quintana Roo, Tabasco, Veracruz, and Yucatán (Pérez-González et al. 2015) |
|
*Considered vectors of bacteria, parasites or viruses. |
|
Hirsutella thompsonii |
| F.E. Fisher 1950 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Arachnida, Trombidiformes, Tetranychidae, Tetranychus urticae; Tenuipalpidae, Aceria guerreronis and Brevipalpidos phoenicics; Erioph yidae, Phyllocoptruta oleivora |
|
Vegetation |
| Low rainforest, scrub, and mangrove |
|
State (references) |
| Without locality (Mier et al. 1989, 1992; Sampedro and Rosas 1989; Guzmán et al. 2001), Colima (Rosas-Acevedo and Sampedro-Rosas 2006) |
|
Ophiocordyceps dipterigena |
| (Berk. & Broome) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora 2007 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Diptera, Calliphoridae, Eucalliphora and Lucilia sericata (adults) |
|
Vegetation |
| Mesophytic forest and coffee plantations |
|
State (references) |
| Veracruz (Guzmán et al. 2001, as Cordyceps dipterigena Berk. & Broome; López and García 2009, as C. dipterigena; Medel 2013) |
|
Ophiocordyceps entomorrhiza |
| (Dicks.) G.H Sung, J.M. Sung, Hywel-Jones & Spatafora 2007 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Lepidoptera, Noctuidae (larvae); Coleoptera (larvae) |
|
Vegetation |
| Secondary bushy vegetation of Quercus forest, coffee plantations, mesophytic forest, Cupressus forest |
|
State (references) |
| Veracruz [Pérez-Silva 1978; Chacón and Guzmán 1983, 1995; Chacón et al. 1995; Rubio-Bustos et al. 1999; López and García, 2002a, all the previous as Cordyceps entomorrhiza (Dicks.) Fr.; Medel 2013], Estado de México (Pérez-Villamares et al. 2017). |
| Note: Revision of the collections of C. entomorrhiza reported by Chacón and Guzmán 1983, 1995, Chacón et al. 1995 and Rubio-Bustos et al. 1999, belong to Ophiocordyceps gracilis (Guzmán et al. 2001) |
|
Ophiocordyceps gracilis |
| Grev.) G.H. Sung, J.M. Sung, Hywel-Jones and Spatafora 2007 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Lepidoptera, Noctuidae (larvae) |
|
Vegetation |
| Deciduous tropical forest, mesophytic forest, ecotone between shrubby secondary vegetation of Juniperus forest and agricultural zone |
|
State (references) |
| Jalisco [Rodríguez et al. 1993; Medel et al. 1999, all the previous as Cordyceps gracilis (Grev.) Durieu & Mont; Medel 2013], Veracruz (Cha cón and Guzmán 1995; Chacón et al. 1995; Guzmán et al. 2001), Estado de México (Pérez-Villamares et al. 2017) |
|
Ophiocordyceps humbertii |
| (C.P. Robin) Petch 1935 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Hymenoptera, Vespidae, Polistes (adults) |
|
Vegetation |
| - |
|
State (references) |
| Oaxaca [Ulloa and Benavides 1991, as Hirsutella saussurei (Cooke ex Sacc.) Speare] |
|
Ophiocordyceps melolonthae |
| (Tul. & C. Tul.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora 2007 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Coleoptera, Melolonthidae, Enema endymion, Strategus aloeus (larvae), and Phyllophaga spp. (adults) |
|
Vegetation |
| Quercus-Pinus forest, subtropical humid forest, rainforest, subdeciduous tropical forest, agricultural zone with coffee plantations |
|
State (references) |
| Chiapas (Pérez-Silva 1977; Robles-Porras et al. 2006, Jalisco (Rubio-Bustos et al. 1999, without locality (Herrera and Ulloa 1998), Oaxaca [Guzmán et al. 2001, all the previous as Cordyceps melolonthae var. rickii (Lloyd) Mains], Veracruz (Guzmán et al. 2001), Morelos [Castro et al. 2012, as C. melolonthae (Tul. & C. Tul.) Sacc.] |
|
Ophiocordyceps octospora |
| (M. Blackw. & Gilb.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora 2007 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Blattoidea, Termitidae, Tenuirostritermes tenuirostris (adults) |
|
Vegetation |
| - |
|
State (references) |
| Jalisco (Blackwell and Gilbertson 1984, as Cordycepioideus octosporus M. Blackw. & Gilb) |
|
Ophiocordyceps sobolifera |
| (Hill ex Watson) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora 2007 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Hemiptera, Cicadidae (nymphs) |
|
Vegetation |
| Xerophilous forest with oak, subtropical scrub |
|
State (references) |
| Without locality (Urbina 1881, Petch 1934, Mains 1951, 1955; Pérez-Silva 1979), Guanajuato (Duges 1924; Guzmán et al. 2001), Jalisco (Mains 1958; Guzmán and García-Saucedo, 1973; Guzmán-Dávalos 1992, based on specimens of C. militaris because the host was confu sed with a nymph of Cicadidae), Coahuila (Rubio-Bustos et al. 1999), Sonora [Méndez-Mayboca et al. 2008, all the previous as Cordyceps sobolifera (Hill ex Watson) Berk. & Broome]. |
|
Ophiocordyceps sphecocephala |
| (Klotzsch ex Berk.) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora 2007 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Hymenoptera, Vespidae, Polistes (adults) |
|
Vegetation |
| Tropical rainforest, oak forest in transition to tropical deciduous forest |
|
State (references) |
| Jalisco (Pérez-Silva 1977; Rodríguez et al. 1993; Rubio-Bustos et al. 1999; Guzmán et al. 2001), Morelos [Castro et al. 2012, all the previous as Cordyceps sphecocephala (Klotzsch ex Berk.) Berk. & M.A. Curtis] |
|
Ophiocordyceps stylophora |
| (Berk. & Broome) G.H. Sung, J.M. Sung, Hywel-Jones & Spatafora 2007 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Coleoptera (larvae), also in Hymenoptera, Vespidae, Polistes instabilis (adults) by mistake |
|
Vegetation |
| Deciduous forest, Quercus-Pinus forest |
|
State (references) |
| Jalisco (Pérez-Silva 1978, as Cordyceps stylophora and Hirsutella stylophora; not this species according to Rubio-Bustos et al. 1999; Estado de México (Pérez-Villamares et al. 2017) |
|
Paraisaria gracilioides |
| (Kobayasi) C.R. Li, M.Z. Fan & Z.Z. Li 2004 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Insecta, Coleptera (larvae) |
|
Vegetation |
| Ecotone between shrubby secondary vegetation of Juniperus forest, agricultural zone, and deciduous forest |
|
State (references) |
| Estado de México [Pérez-Villamares et al. 2017, as Ophiocordyceps gracilioides (Kobayasi) G.H. Sung, J.M. Sung, Hywel-Jones & Spata fora], Morelos (Castro et al. 2012) |
|
Tolypocladium capitatum |
| (Holmsk.) C.A. Quandt, Kepler & Spatafora 2014 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Hypogeal fungi, Ascomycota, Eurotiales, Elaphomyces granulatus and E. muricatus |
|
Vegetation |
| Pinus-Quercus forest and Quercus forest |
|
State (references) |
| Estado de México (Heim 1957; Guzmán 1958, 1977, 2008; Heim and Wason 1958; Pérez-Silva 1977), San Luis Potosí (Guzmán 1958; Pé rez-Silva 1977), Hidalgo (García-Romero et al. 1970, as C. canadensis Ellis & Everth; Pérez-Silva 1977), Jalisco (Pérez-Silva 1977; Gándara et al. 2014), Morelos (Pérez-Silva 1977), Oaxaca (Pérez-Silva 1977), Puebla (Martínez et al. 1983), Durango (Quintos et al. 1984), Veracruz (Guzmán and Villareal 1984), Michoacán (Díaz-Barriga et al. 1988), Sonora (Pérez-Silva et al. 1996). In all cases as Cordyceps capitata (Hol msk.) Fr., except when indicated. |
|
Tolypocladium ophioglossoides |
| (J.F. Gmel.) C.A Quandt, Kepler & Spatafora 2014 |
| Host: Class, Order, family, species (larvae, pupae or adult). |
| Hypogeal fungi, Ascomycota, Eurotiales, Elaphomyces granulatus and E. muticatus |
|
Vegetation |
| Pinus-Quercus forest and Quercus forest |
|
State (references) |
| Estado de México (Heim and Wason 1958; Trappe and Guzmán 1971; Pérez-Silva 1977; Guzmán et al. 2001), Durango (Pérez-Silva 1977), Hidalgo (Pérez-Silva 1977), Michoacán (Díaz-Barriga et al. 1988), Oaxaca (Pérez-Silva 1977), Sonora (Pérez-Silva et al. 1996), San Luis Potosí (Guzmán 1958; Guzmán et al. 2001), Tamaulipas (García-Jiménez and Valenzuela 2005) |
| All recorded as Cordyceps ophioglossoides (J.F. Gmel.) P. 1818 |
Results
History of records of Cordycesp s.l. in Mexico
The first report of Cordyceps in Mexico was made by the physician and pharmacist Río de la Loza (1864), who analyzed an “animal-plant rare in nature” and determined it to be an “animal (Cicada communis) with animal excrescence” (Figure 1). In the same year, Milne-Edwards (1864) reviewed the “animal-plant” specimens from Mexico and mentioned that what looked like a plant and emerged from cicada larvae or nymphs was a fungus called Sphaeria sobolifera (=Ophiocordyceps sobolifera). Seventeen years later, Urbina (1881) supported the conclusions made by Milne-Edwards, corroborating that these specimens were insects parasitized by fungi. Then, seventy-seven years after the Milne-Edwards determination, the first species of entomopatogenous fungi was Isaria cicadae (= Isaria sinclairii) in Jalisco, Mexico were recorded in 1941-1942 (Petch 1941-1942)
Figure 1 Illustration of a “rare animal-plant” made by Río de la Loza in 1864. A. Larva-nymph, with ramifications that emerge from the head; B. Ramifications ending in a cauliflower formations, emerging from the anterior part of the thorax; C. Dissected lateral view of a larva-nymph; D. Serrated leg of the insect used to excavate the soil.
The taxonomic identification of herbarium material, collected material, and new records have been carried out mainly by Petch (1941-1942), Mains (1957, 1958), Guzmán (1958), Heim and Wasson (1958), Pérez-Silva (1977, 1978), and Rubio-Bustos et al. (1999). The regional taxonomic studies have been carried out mainly by Castro et al. (2012) and Pérez-Villamares et al. (2017). The most recent research described a new species, Cordyceps mexicana, in which morphology, host, and DNA data were analyzed (López-Rodríguez et al. 2022) (Figure 2).
Diversity of Cordyceps s.l. in Mexico
Currently, there are 35 Cordyceps s.l. species recorded in Mexico, belonging to the families Clavicipitaceae, Cordycipitaceae, and Ophiocordycipitaceae. These species represent 3.5 % of the entomopathogenic fungi worldwide. Most of the records have been made from Colima, Estado de México, Hidalgo, Jalisco, Morelos, and Oaxaca. Estado de México, with 13 species, represented the first place in terms of diversity. There were states, such as Aguascalientes, Baja California, Baja California Sur, Ciudad de México, Guerrero, Querétaro, Yucatán, and Zacatecas, in which no studies have been conducted (Figure 3).
Species and families recorded in Mexico
Clavicipitaceae
Clavicipitaceae in Mexico was the least recorded family, represented by eight entomopathogenic species: Metarhizium acridum, M. anisopliae, M. brunneum, M. guizhaense, M. humberi, M. pemphigi, M. pinghaense, and M. robertsii. These species have been found mainly in agricultural areas of maize and bean crops, in soil or parasitizing Coleoptera, Diptera, Hemiptera, Lepidoptera, Orthoptera, Thysanoptera, and acari (Arachnida) (Table 1). Metarhizium anisopliae had the highest number of records and the widest distribution (Figure 4), it has been isolated from soils and a wide range of insects. Metarhizium acridum, M. brunneum, and M. humberi have been found in a single order of insects, meanwhile M. guizhaense, M. pinghaense, and M. robertsii have been recorded parasitizing Coleoptera, Lepidoptera, and Orthoptera.
Cordycipitaceae
The Cordycipitaceae family was represented in Mexico by 13 species, eight of the genus Cordyceps, three of Beauveria, one of Akanthomyces, and one of Isaria (Table 2). Cordyceps militaris had the largest number of records and a wide geographic distribution (Figure 5). It has been recorded in 12 states, in various vegetation types including temperate forests, rainforests, grasslands, and agricultural areas. It grows on pupae and larvae of Lepidoptera of the families Geometridae, Noctuidae, and Sphingidae, and has only been reported once parasitizing Coleoptera (Table 2). Isaria cicadae was the first species cited in Mexico, however its ubication was not clear, therefore it is not shown on the Figure 5.
Ophiocordycipitaceae
Ophiocordycipitaceae was the family with the greatest diversity recorded in Mexico, comprising 14 species and four genera. Ophiocordyceps had nine species distribuited in seven states. Of these, Estado de México, Jalisco, and Veracruz had the highest number of records. Tolypocladium was represented by two species, with the highest number of records and the largest geographic distribution, widely collected parasitizing Elaphomyces spp. in pine-oak forests. The genus Hirsutella was also represented by two species, while Paraisaria had presented only one species (Figure 6, Table 3).
Asexual states of Cordyceps s.l. recorded as agents of biological control of insect pests and disease vectors
In Mexico, the asexual states of Beauveria bassiana, Cordyceps fumosorosea (Table 2), Hirsutella sp. (Table 3), and Metarhizium anisopliae (Table 1) have been studied as biological control agents of insect pests that affect valuable crops such as beans, citrus, coffee, fruits, maize, and sugar cane. In addition, another application being investigated is its pathogenicity on insects or acarus vectors of bacteria, viruses, or parasites (Tables 1 and 2).
The traditional importance of Tolypocladium in Mexico
Tolypocladium capitatum (=Cordyceps capitata) and T. ophioglossoides (=Cordyceps ophioglossoides) were the only species recorded with an edible use in rituals of the indigenous of central Mexico. These were first recorded in the Estado de México (Table 3). The Nahuas attribute medicinal properties to both species (Heim and Wason 1958). Their consumption was first described in rituals of the nahua people of San Pedro Tlanixco and Tenango del Valle, where they were consumed together with Psilocybe muliercula and Elaphomyces spp. (Heim and Wason 1958). The common names of T. capitatum and T. ophioglossoides are “little men”, while individuals of Psilocybe muliercula are known as “little women” and Elaphomyces spp. is called “great world”. The ritual itself was described by Guzmán (2008); however, the use of Tolypocladium has not been recorded again.
Relationship with the hosts
In Mexico, we found that the members of Clavicipitaceae are mainly associated with nymphs or larvae of Coleoptera, Lepidoptera, and Orthoptera, although Metarhizium anisopliae has a very wide range of insect hosts and even parasitizes Arachnida (Table 1). Cordycipitaceae mainly presented an association with Lepidoptera. Cordyceps militaris and C. takaomontana were associated with Lepidoptera larvae and pupae. Cordyceps farinosa and C. polyarthra were found on Lepidoptera pupae, while only Akanthomyces tuberculatus was found on Lepidoptera adults. However, other species could be associated with Coleoptera, Hemiptera, and Orthoptera adults and Beauveria bassiana has also a very wide range of insect hosts (Table 2). In Ophiocordycipitaceae, Tolypocladium parasitizes Elaphomyces fungi, while Ophiocordyceps was found on Lepidoptera and Coleoptera larvae, on Diptera, Coleoptera, Hymenoptera, Homoptera, and Hemiptera adults, and only Hirsutella thompsonii parasitizes acari (Table 3).
Discussion
Diversity of Cordyceps in Mexico
Currently, Mexico presents 3.5 % of Cordyceps s.l. entomopathogen, considering an overall world diversity of 1 000 species (Wei et al. 2020). However, we assume that the existing records are underestimates, since few studies have focused on these fungi, the studies are mainly regional and involve classic taxonomy, the intervals between investigations are usually long, and there are numerous geographic areas where no studies have been conducted.
Regarding distribution maps, we found that the vegetal stratum has changed from 1980 to 2018. We observed that some temperate and tropical forests have changed to human settlements, suggesting possible biodiversity loss over time. For example, Ophiocordyceps octospora was recorded in Jalisco by Blackwell and Gilbertson (1984), from an agricultural zone that is now occupied by an human settlement. Of the family Cordycipitaceae, at least one record from the forest of Beauveria scarabaeidicola, Cordyceps militaris, and C. takaomontana, now the localities correspond to human settlements. On the other hand, the locations of some records of Hirsutella citriformis, Ophiocordyceps gracilis, O. melolonthae, O. sphecocephala, and Paraisaria gracilioides in agriculural areas now correspond to human settlements.
Fungal biodiversity loss in this group of fungi is a little studied global problem, with few evaluations conducted (Yang 2020). However, it has been recorded that the main factors responsible for this loss are agriculture and aquaculture, biological resource use, comercial-residential development, modifications of natural systems, and others (Lughadha et al. 2020). We recommended investment of time and funds in further research of aspects of the biology of Cordyceps s.l. in Mexico, particularly to explore the genetics, anatomy, and ecology of the group, which would allow the proposal of suitable conservation strategies.
Species recorded in Mexico
Clavicipitaceae
Metarhizium anisopliae is the most dominant species of Clavicipitaceae in Mexico (Pérez-González et al. 2014). We therefore recommend further studies to explore its utility as substitute for chemical insecticides. This species has the highest number of records, being isolated from soils and a wide range of insects, from tropical and temperate regions. It is considered to be generalist (Bischoff et al. 2009) and mesophilic, since it grows at temperatures of 10-40 °C (Roberts and Campbell 1977), and it has been used in the management of crop pests and malaria vectors (Scholte et al. 2005).
Cordycipitaceae
Cordyceps militaris is the most dominant species of Cordycipitaceae in Mexico. This species can be considered cosmopolitan, since it has been reported widely distributed in Asia, Europe, and North America (Mains 1958). Its distribution is not determined by vegetation or climate, but rather by the distribution of its insect hosts (Shrestha et al. 2016). In Asia, it is consumed for its attributed medicinal properties, since it produces secondary metabolites, such as cordycepin, with anticancer, antibiotic, and antifungal activities (Ng and Wang 2005, Shrestha et al. 2016). Despite its importance as food and medicine, studies addressing these aspects have yet to be conducted in Mexico.
Ophiocordycipitaceae
Worldwide, Ophiocordycipitaceae comprises about 160 species that infect 11 orders of insects (Evans et al. 2011, Araújo and Hughes 2016). Ophiocordyceps is considered the most diverse genus of the Hypocreales Sung et al. 2007a). Below, we review some of the important species of this genus present in Mexico. Ophiocordyceps melolonthae has been found in different vegetation types including evergreen forests, pine-oak forest and subtropical humid forests, as well as agroecosystems such as coffee plantations. It is always found parasitizing larvae and adults of Coleoptera of the family Melolonthidae (Pérez-Silva 1977, Rubio-Bustos et al. 1999), and its distribution is therefore considered to be related to that of its host. Ophiocordyceps dipterigena has been recorded only in the humid subtropical forest of the state of Veracruz, where it parasitizes species of Diptera (Guzmán et al. 2001, Medel 2013). This species has biotechnological importance since it produces an exobiopolymer that induces the production of the interleukin IL-8 for fibroblasts (Kocharin et al. 2010). This is useful as a healing material, while its high viscosity and moisturizing properties allows its use as a substitute for hyaluronic acid in the pharmaceutical industry.
Ophiocordyceps entomorrhiza is a species similar to Paraisaria gracilis; indeed, it is difficult to taxonomically distinguish between the two species (Guzmán et al. 2001). Paraisaria gracilis and O. entomorrhiza have been reported on Lepidoptera in various types of vegetation (Chacón and Guzmán 1983, 1995; Chacón et al. 1995, Pérez-Silva 1978, Rubio-Bustos et al. 1999, López and García 2002a, Medel 2013); however, Pérez-Villamares et al. (2017) stated that O. entomorrhiza has only been found parasitizing Coleoptera larvae, and P. gracilis has only been found parasitizing Lepidoptera, so it is probably, each species is restricted to an insect order, respectively. The morphological difference between both species is mainly the coloration of the fertile part and stipe of the stromata, in O. entomorrhiza the fertile part is wine-colored, violet gray or grayish brown and the stipe is brown, in contrast P. gracilis has the fertile part red, orange or ocher and the stipe is yellowish (Pérez-Villamares et al. 2017), both species have been recorded in Mexico (Table 3). Paraisaria gracilioides is a rare species that specializes in parasitizing Coleoptera larvae (Kobayasi 1941, Castro et al. 2012, Pérez-Villamares et al. 2017). Ophiocordyceps sphecocephala has been recorded in Mexico as a parasite of the wasp of the genus Polistes, but in China, Japan, Korea, and Nepal, it has been found parasitizing Aphrophora wasps (Shrestha 2011).
In Mexico, O. stylophora has been described as parasitizing larvae of Coleoptera (Pérez-Villamares et al. 2017) and also on Hymenoptera (Pérez-Silva 1978); however, their identification on Hymenoptera was considered erroneous by Rubio-Bustos et al. (1999), who mentioned that O. stylophora grows on coleopterans, additionally they examined the specimen of Pérez-Silva (1978) and observed a different morphology with respect to O. stylophora, therefore, they suggested it could be a new species. Ophiocordyceps sobolifera has been reported on cicada nymphs and it is probably the species that was first recorded as a “rare plant-animal” (Guzmán et al. 2001).
Unlike the genera described above, Tolypocladium does not parasitize insects but rather hypogeous fungi of the genus Elaphomyces and, some nymphs of Cicadidae. It was hypothesized that, given the same belowground habitat of Cicadas and Elaphomyces, Tolypocladium has performed a host switch (Nikoh and Fukatsu 2000). Tolypocladium ophioglossoides has been reported with a wide distribution in the northern hemisphere: Japan, Russia, and USA, as well as Mexico (Mains 1957, Pérez-Silva 1977). This species is of pharmaceutical importance because it produces ophiocordin with antibiotic and antifungal properties (Kneifel et al. 1997), and ophiosetin with antibiotic properties (Putri et al. 2010).
Asexual states of Cordyceps s.l.
Beauveria bassiana and Metarhizium anisopliae are pathogens of Brachystola magna and Phyllophaga spp., two pests that affect bean (Phaseolus vulgaris) and maize (Zea mays) crops (Lezama et al. 2005, Barajas et al. 2011, Hernández-Velázquez et al. 2011). These fungi are also found on insects in coffee (Coffea spp.) crops (De la Rosa et al. 2000) and have been used to treat sugar cane crop pests (SAGARPA 1999). The pest control properties of these fungi have also been tested in the dengue vector Aedes aegypti (García-Munguía et al. 2015) and in Meccus pallidipennis and Triatoma dimidiata, two vectors of Chagas disease (Vázquez-Martínez et al. 2014, Flores-Villegas et al. 2016). Cordyceps fumosorosea (as Paecilomyces fumosorosea or Hirsutella sp.), has also been used to control Diaphorina citri, an insect that transmits viruses to citrus fruits (Lezama-Gutiérrez et al. 2012, Pérez-González et al. 2015).
Hosts
The main hosts of Cordyceps s.l. have been reported as immature stages of Coleoptera and Lepidoptera (Shrestha et al. 2016), as well as spiders (Shrestha et al. 2019). In this review, the main hosts were in order of importance, Lepidoptera, Coleoptera, and Orthoptera. These host associations are informative taxonomic characters in Cordyceps s.l., since the hosts are probably drivers for speciation (Sanjuan et al. 2015). Lopez-Rodríguez et al. (2022) also suggested that host identification to species or genera level is substancial, as well as analysis in conjunction with morphology and phylogenetic analysis of multilocus DNA sequences. We therefore suggest that future studies should place an emphasis on the taxonomic identification of hosts at species level.
Conclusions
In Mexico, the history of the study of the Cordyceps s.l. dates back to 1864, but the research has advanced sporadically, leaving lapses of up to 77 years with no research at all. Currently, Cordyceps s.l. diversity is represented by 35 species, where the family Ophiocordycipitaceae is the most diverse, followed by Cordycipitaceae, and finally Clavicipitaceae. These species are associated with the distribution of their hosts, as observed mainly in Ophiocordyceps dipterigena, O. entomorrhiza, and O. melolonthae. Most species are associated with a genus or family of the class Insecta and in the case of fungal parasites have only been reported in the genus Elaphomyces. Only Beauveria bassiana, C. militaris, and M. anisopliae have been recorded in more than one order of insects. Beauveria bassiana and M. anisopliae are species with agricultural importance because they are utilized in the control of pest insects and disease vectors that affect animals, humans, and plants. Despite their global agricultural importance, there has been no specific research of specialized entomopathogenic species in Mexico, and the studies that have been conducted to date did not address any effects on other insects, including pollinators or other ecologically important insects. Tolypocladium capitatum and T. ophioglossoides are the only species recorded with ritual use by indigenous people in Mexico. Some of the listed species have medicinal, nutritional or pharmacological importance, such as C. dipterigena, C. militaris, C. pruinosa, and T. ophioglossoides. Given the great taxonomical diversity and nutritional and pharmaceutical importance of these fungi, we consider it crucial to initiate research on integral taxonomy, its in vitro culture and metabolites in order to elucidate the taxonomic identity of the species and evaluate its possible use.
