Revista Mexicana de Ciencias Agrícolas   special publication number 22   March 15 - April 30, 2019

DOI: https://doi.org/10.29312/remexca.v0i22.1866

Article

Analysis of research on Metarhizium anisopliae in the last 40 years

Francisco Hernández-Rosas1

Luis Andrés García-Pacheco1

Katia Angélica Figueroa-Rodríguez1§

Benjamín Figueroa-Sandoval2

Josafhat Salinas Ruiz1

Dora Ma. Sangerman-Jarquín3

Edna Liliana Díaz-Sánchez1

1College of Postgraduates-Campus Córdoba. Sustainable Agri-Food Innovation Program. Highway Córdoba-Veracruz km 348, Congregation Manuel León, Amatlán de los Reyes, Veracruz, Mexico. CP. 94953. (fhrosas@colpos.mx; garcia.andres@colpos.mx; diaz.edna@colpos.mx; salinas@colpos.mx). 2Innovation Program in the Management of Natural Resources-College of Postgraduates-Campus San Luis. Calle de Iturbide 73, Salinas de Hidalgo, SLP. CP. 78622. (benjamin@colpos.mx). 3Valle de México Experimental Field-INIFAP. Highway Los Reyes-Texcoco km 13.5, Coatlinchán, Texcoco, State of Mexico, Mexico. CP. 56250. (sangerman.dora@inifap.gob.mx).

§Corresponding author: fkatia@colpos.mx.

Abstract

Biological control is used for the regulation of pest insect populations and to avoid the induction of insect resistance due to the excessive use of agrochemicals, as well as to solve waste problems for the organic production of food. There are more than 750 species of entomopathogenic fungi that can be used for the biological control of pests, being Metarhizium anisopliae, one of the most used commercially. The objective of this review was to determine the most relevant issues regarding research concerning M. anisopliae during the period from 1976 to 2018. A revision was made in the meta search Scopus®, using as keyword Metarhizium anisopliae only in title for October 9, 2018. The main journals, countries and institutions that have published on the subject were identified. The data was analyzed using VOSviewer® software under the principle of co-occurrence of terms. The results show that this microorganism has been widely studied at an international level, especially in the period from 2008 to 2014. The investigations are concentrated in three clusters: production-activity, Beauveria bassiana and termites. It is concluded that this microorganism continues to be analyzed from a commercial perspective and because biological control agents tend to be local, their investigations will continue to concentrate on the development and characterization at the molecular level of local (native) strains with commercial potential.

Keywords: Beauveria bassiana, biological control, entomopathogens, pests, termites.

Reception date: February 2019

Acceptance date: April 2019

Introduction

The excessive use of chemical products in agricultural crops is a problem, since some insects have developed resistance to them (Lezama-Gutiérrez et al., 2012). Therefore, it has become necessary to look for alternative means for the biological control of pests in order to minimize the use of these chemicals (Mirhaghparast et al., 2013). Biological control provides additional tools for the management of pests that break the resistance cycles of insects, as well as solve waste problems for the production of organic food (Fravel, 2005). There are more than 750 species of entomopathogenic fungi disseminated in the environment that cause fungal infections to certain insects, which can regulate up to 80% of their populations (Lobo et al., 2016). Among the most important genera are: Metarhizium, Beauveria, Aschersonia, Entomophthora, Zoophathora, Hirsutella, Fusarium and Verticillium (Acuña-Jiménez et al., 2015).

In this context Metarhizium anisopliae is a filamentous fungus characterized and used for the control of pests, in addition the use of its enzymes is used as a biological catalyst in the industrial sector (Alonso-Díaz et al., 2007). It is one of the most common species that has been found, studied and used throughout the world mainly as a biological control agent (ACB) (Curran et al., 1994). This fungus has been successfully applied since the 1970s in Brazil to control pests in sugarcane (Rangel et al., 2006). M. anisopliae has also been used as a biological control agent or ACB for pests of various insects: termites (Isoptera), lobsters (Locusta migratoria L.), spittlebugs (Aeneolamia spp., Prosapia spp., Nilaparvata lugens Stål), beetles (Adoryphorus couloni B., Antitrogus parvulus Britton, Aphodius tasmaniae Hope, Oryctes rhinocerus L.), screwworm (Diatraea saccharalis F.) and for the control of mosquito vectors of malaria, including their larval stages (Buti et al., 1994).

Research on the use of microorganisms for the biological control of pests in agriculture, is present in the scientific literature since the seventies, being a subject widely explored from various lines of knowledge (Camargo et al., 2016); however, to date there is no holistic review to understand what research has focused on this fungus. The objective of this review was to determine the most relevant issues regarding research concerning M. anisopliae during the period from 1976 to 2018.

Materials and methods

The analyzed publications were obtained with the search engine Scopus® Elsevier (www.scopus.com) for the period from 1976 to 2018 (October 9). Initially the word Metarhizium was used, only in the title, which generated 1 708 documents. Publications were found regarding several species of the genus Metarhizium such as: M. anisopliae (1 272 publications), M. acridum (107), M. robertsii (173), M. brunneum (121), M. rileyi (16), M. majus (7), M. guizhouhense (6), M. pingshaense (6), the species M. anisopliae was the most studied, by which only the publications of M. anisopliae were retained or used for the analysis. Of the total of documents analyzed, 1 216 were articles, occupying 95.6% of the total. Other documents were: book chapters (7), reviews (14), articles in the press (4), conference documents (14), letters (2), notes (3), surveys (3) and erratum (9). With these data a bibliometric analysis was elaborated using the terms of the keywords, titles and summaries of the publications to show only the elements connected to each other.

Analysis of the results

VOSviewer® software (Center for Science and Technology Studies, 2018) was used for the analysis. An analysis of co-occurrence of key words and academic terms in the titles and abstracts of the publications was made, the method was normalization-force of association (FA), resolution of 1.00, scale of visualization to 100%, weight TLS, tag variation size of 50% and core width of 30%. The complete counting method was established, with a number of records of each term ≥10, and a minimum cluster size of 15 (van Eck and Waltman, 2010). With the terms retained the map was created for the visualization of the network, those terms with more frequency are presented in larger bubbles, the irrelevant terms were eliminated (Heersmink et al., 2011).

Results

The number of publications dealing with aspects related to M. anisopliae is abundant, then the bibliometric indicators related to this microorganism are analyzed.

Performance analysis

The distribution of the publications referring to this research topic is presented in Figure 1. The number of publications on this topic began in 1976 maintaining an irregular growth, for the year of 1998 it reaches its first peak in 2008, year in which that the greatest number of publications is presented (75), followed by 2014 (74). After 2015, the number of publications has been decreasing. Of the total of documents, 1 121 have been cited accumulating a total of 24 504 citations. There are 24 articles that have more than 100 citations, 93 have between 50 and 90 appointments and 623 articles have less than 10 citations.

With regard to the countries, it is observed that Brazil is the country with the highest number of contributions (241). The United States of America has second place with 228 publications, followed by the United Kingdom (139), China (97) and India (82). In Latin America, Mexico stands out with 54 publications, followed by Colombia with 22 and Argentina with 10 publications. The contributions come from authors from 160 institutions: 29 Brazilian, 21 American, 16 belonging to the United Kingdom, 13 Chinese and 11 Mexican. Within the 11 Mexican institutions are, the State University of Colima (12), UNAM (9), the University of Guanajuato (8), the College of Postgraduates (6) and the Autonomous University of Yucatan (4).

Table 1 shows the 10 journals with the highest number of publications, ordered by country and institution. The five journals with the highest number of publications are: Journal of Invertebrate Pathology, Biocontrol Science and Technology, Mycological Research, Biological Control and Biocontrol. They emphasize journals with emphasis on entomology, pathology and mycology, as well as biological control.

Figure 1. Distribution of publications on M. anisopliae by year from 1976 to 2018 (October 9, 2018).

Table 1. Performance analysis: institute, country and magazine.

In Table 2, the 10 most cited articles are presented. These articles allow us to rescue the most relevant topics in this area of knowledge, such as: Genomic sequencing, biological control, genetic groups of Beauveria bassiana fungi, combinations of mycoinsecticides, pathogenicity, among other topics.

Table 2. The 10 most cited articles on control and M. anisopliae.

Mapping of science

An analysis of the co-occurrence of terms was carried out, this provides an overview of the trends of the research, reflecting the topics addressed. The results establish 649 terms, of which those with co-occurrences greater than 10 were conserved, eliminating generic terms related to the research process, 389 terms were retained, organized in 3 clusters with 27 104 relationships. In Figure 2, the three clusters are observed: one referring to the activity/production of Metarhizium anisopliae (green cluster), another referring to the relationship and interaction with Beauveria bassiana (red cluster) and a third related to termites (blue cluster).

Figure 2. Visualization of the co-occurrence network using the VOSviewer® program.

Discussion

This study dealt with bibliometric methods to know the behavior of scientific publications related to M. anisopliae. Based on these results, the three clusters related to this microorganism will be discussed separately below.

Production-activity

Chemical insecticides have been commonly used to control agricultural pests, termites and biological vectors, such as mosquitoes and ticks, these chemicals have generated harmful effects on the environment and resistance in pests and vectors. Due to the growing public concern, research has increased on alternatives, especially biological control agents such as fungi and entomopathogenic bacteria, for their control (Aw and Hue, 2017). The use of these fungi has evolved to become commercial products (bioinsecticides), so variables such as conidia production, sporulation and virulence (Zhang et al., 2018), are strategic in research that focuses on in evaluating culture media or methods of reproduction or propagation of spores or conidia of M. anisopliae (Shah et al., 2005).

The microbial activity refers to the changes that are expressed in the activity of the microorganisms, in the case of M. anisopliae, the investigations have included the biological activity of this microorganism when it is combined with essential oils (Rosas-Garcia et al., 2018), the analysis of the enzymatic activity of proteases obtained from M. anisopliae (St Leger et al., 1999; Shah et al., 200), their antifungal and fungal activity (Wang et al., 2005), insecticide (Charnley, 1991) and biological on various pests such as the white worm (Premnotrypes vorax Hustache) (Villamil et al., 2016), the red spider (Tetranychus evansi Baker & Pritchard) (Azandeme-Hounmalon et al., 2018), the potato moth (Phthorimaea operculella Zeller) (Khorrami et al., 2018), or the rhizosphere (Meyling and Eilenberg, 2007), just to mention a few examples.

Another sub-area of research relevant to this microorganism is the molecular aspect. Several investigations have analyzed the role of several enzymes (Dextruxins, MaNAG1, MaNAG2, MaNAG3 and MaNAG4) during the life cycle of Metarhizium anisopliae (de Oliveira et al., 2018), characterized the toxic ribonucleases of this microorganism as potential insecticides against ribosomes. for the control of disease vectors (Olombrada et al., 2017), as well as the function of some genes on the adaptation to the environment of this microorganism (Zeng et al., 2018) and its level of virulence (Santos et al., 2017).

Beauveria bassiana

B. bassiana is an entomopathogenic fungus (Abdu-Allah et al., 2015). Its mode of action is by contact (Alcala-Gomez et al., 2017), contaminating the microflora of the cuticle of the insect, germinating the spore on the insect pest and the hypha is introduced to the integument (tissue that forms the outer wall of the cuticle of the body of the insects) and enter the hemocoel and then spread by the hemolymph throughout the insect, causing its death by toxins (by toxemia) that this same secret (Petlamul and Prasertsan, 2012). It presents a great genetic diversity and usually develops in agricultural habitats (Bidochka et al., 1998; Rustiguel et al., 2018). Some of the pests it controls are: Whitefly (Trialeurodes vaporariorum Westwood), thrips (Thrips spp), blind hen (Phyllophaga spp. Bates), black donut (Spodoptera littoralis Boisduval), among others (Polanczyk et al., 2010; Mirhaghparast et al., 2013), as well as arthropod pests in poultry production (de Oliveira et al., 2014). It is currently used as a commercial biological control product in combination with M. anisopliae.

B. bassiana and M. anisopliae are combined due to the strategies that each follows, both their mode of action is contact, only that the former has a toxic strategy using oosporeins and invades the host while the latter has a growth strategy with the formation of appressoria and invasion of the host, this makes the effect for the biological control of pests greater (Rustiguel et al., 2018). Although other studies have focused on establishing which of these two fungi has better fungicidal effect (Barbosa et al., 2018), as well as their combinations with some insecticides (Rivero-Borja et al., 2018), with various chemical compounds, such as thymol, and application methods (Sinia and Guzmán-Novoa, 2018), for pest control. In general, the research topics deal with formulations, mortality and virulence (Oliveira et al., 2018), laboratory bioassays, field evaluation, and their evaluation for the control of various pests.

Termites

Termites (Coptotermes curvignathus (Holmgren) Isoptera: Rhinotermitidae, Coptotermes heimi) are a threat to plants and agricultural crops, although they are excellent decomposers of dead wood and other sources of cellulose, they become a serious problem when they attack homes and crops (Hussain et al., 2011). Due to significant losses in annual and perennial crops and damage, different control methods have been adopted such as physical, chemical and biological control (Wright et al., 2005). Chemical control has been a successful method to prevent termite attack, but biological methods are suitable alternatives (Verma et al., 2009), especially when seeking to reduce the use of chemicals that harm the environment and human health (Yii et al., 2016).

M. anisopliae and B. bassiana positively infect termites (Rath, 2000), by invading their host through the integument and causing death by depletion of host metabolites, due to a destruction of vital tissues or a combination of both (Wang and Powell, 2004). Previous research found that M. anisopliae causes a percentage of 71-84% of infections in termites after 15 days of treatment (Kin et al., 2017). Other studies have focused on topics such as: The mortality rate according to different concentrations of conidia per ml (Samsuddin et al., 2015; Riaz et al., 2017; Keppanan et al., 2018), its compatibility with some pesticides (Yii et al., 2016) or its effect on other species when used for termite control (Abonyo et al., 2016).

Conclusions

The objective of this work was to determine the most relevant issues regarding research concerning M. anisopliae during the period from 1976 to 2018, for which a bibliometric review of the concept Metarhizium anisopliae was carried out. In addition to establishing the most influential countries and institutes on the subject. The analysis of co-occurrence of terms and the discussion on the most important terms within the most cited articles was carried out. Derived from this analysis some important conclusions are obtained as it is that the topic has been relevant for the scientific community, with more intense periods in scientific productivity than others (2004-2014). The country with the highest number of publications is Brazil and Mexico ranks 8th worldwide in terms of the number of publications. The investigation could be grouped in that dedicated exclusively to M. anisopliae, the one where this fungus is combined with another (B. bassiana) and the use of M. anisopliae for the control of termites. Finally, it should be noted that this particular topic demonstrates the progress of research from basic science to applied science and finally to the development of technological solutions. Future contributions on this fungus will be about the discovery of new species and strains that have commercial potential with an emphasis on genetic engineering and biotechnology.

Cited literature

Abdu-Allah, G. M.; Abou-Ghadir, N. M. F.; Nasser, M. A. K. and Metwaly, M. R. 2015. Comparative efficiency of the fungi, Beauveria bassiana, Metarhizium anisopliae and the natural product spinosad, using three economic coleopterous stored grain insects. Int. Med. J. 25(3):715-720.

Abonyo, E. A.; Maniania, N. K.; Warui, C. M.; Kokwaro, E. D.; Palmer, T. M.; Doak, D. F. and Brody, A. K. 2016. Effects of entomopathogenic fungus Metarhizium anisopliae on non-target ants associated with Odontotermes spp. (Isoptera: Termitidae) termite mounds in Kenya. Int. J. Trop. Insect. Sci. 36(3):128-134.

Acuña-Jiménez, M.; Rosas-García, N. M.; López-Meyer, M.; Saínz-Hernández, J. C.; Mundo-Ocampo, M. and García-Gutiérrez, C. 2015. Pathogenicity of microencapsulated insecticide from Beauveria bassiana and Metarhizium anisopliae against tobacco budworm, Heliothis virescens (Fabricius). Southwest Entomol. 40(3):531-538.

Alcalá-Gómez, J.; Cruz-Vázquez, C.; Fernández-Ruvalcaba, M.; Ángel-Sahagún, C.; Vitela-Mendoza, I. and Ramos-Parra, M. 2017. Virulence of Metarhizium anisopliae and Beauveria bassiana isolates and the effects of fungal infection on the reproduction potential of Rhiphicephalus microplus engorged females. Biocontrol Sci. Technol. 27(8):931-939.

Alonso-Díaz, M. A.; García, L.; Galindo-Velasco, E.; Lezama-Gutierrez, R.; Angel-Sahagún, C. A.; Rodríguez-Vivas, R. I. and Fragoso-Sánchez, H. 2007. Evaluation of Metarhizium anisopliae (Hyphomycetes) for the control of Boophilus microplus (Acari: Ixodidae) on naturally infested cattle in the Mexican tropics. Vet. Parasitol. 147(3-4):336-340.

Aw, K. M. S. and Hue, S. M. 2017. Mode of infection of metarhizium spp. Fungus and their potential as biological control agents. J. Fungi. 3(2).

Azandémè Hounmalon, G. Y.; Maniania, N. K.; Niassy, S.; Fellous, S.; Kreiter, S.; Delétré, E.; Fiaboe, K. K. M. and Martin, T. 2018. Performance of Metarhizium anisopliae-treated foam in combination with Phytoseiulus longipes Evans against Tetranychus evansi Baker & Pritchard (Acari: Tetranychidae). Pest. Manag. Sci. 74(12):2835-2841.

Barbosa, T. D. S.; De Andrade, D. J.; Polanczyk, R. A. and Duarte, R. T. 2018. Susceptibility of Tetranychus ogmophallos (Acari: Tetranychidae) to Beauveria bassiana and Metarhizium anisopliae. Fla Entomol. 101(2):249-253.

Bidochka, M. J.; Kamp, A. M.; Lavender, T. M.; Dekoning, J. and De Croos, J. N. A. 2001. Habitat association in two genetic groups of the insect-pathogenic fungus Metarhizium anisopliae: Uncovering cryptic species? Appl. Environ, Microbiol. 67(3):1335-1342.

Bidochka, M. J.; Kasperski, J. E. and Wild, G. A. M. 1998. Occurrence of the entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana in soils from temperate and near-northern habitats. Canadian J. Bot. 76(7):1198-1204.

Bischoff, J. F.; Rehner, S. A. and Humber, R. A. 2009. A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia. 101(4):512-530.

Buti, T. M.; Ibrahim, L.; Ball, B. V. and Clark, S. J. 1994. Pathogenicity of the entomogenous fungi Metarhizium anisopliae and Beauveria bassiana against crucifer pests and the honey bee. Bio. Sci. Technol. 4(2):207-214.

Camargo, M. G.; Nogueira, M. R. S.; Marciano, A. F.; Perinotto, W. M. S.; Coutinho-Rodrigues, C. J. B.; Scott, F. B.; Angelo, I. C.; Prata, M. C. A. and Bittencourt, V. R. E. P. 2016. Metarhizium anisopliae for controlling Rhipicephalus microplus ticks under field conditions. Vet. Parasitol. 223:38-42.

Curran, J.; Driver, F.; Ballard, J. W. O. and Milner, R. J. 1994. Phylogeny of Metarhizium: analysis of ribosomal DNA sequence data. Mycol. Res. 98(5):547-552.

Charnley, A. K. 1991. Microbial pathogens and insect pest control. Lett. Appl. Microbiol. 12(5):149-157.

de Oliveira, D. G. P.; Alves, L. F. A. and Sosa-Gómez, D. R. 2014. Advances and perspectives of the use of the entomopathogenic fungi B. bassiana and M. anisopliae for the control of arthropod pests in poultry production. Rev. Brasileira Cienc. Avicola. 16(1):1-12.

de Oliveira, E. S.; Junges, Â.; Sbaraini, N.; Andreis, F. C.; Thompson, C. E.; Staats, C. C. and Schrank, A. 2018. Molecular evolution and transcriptional profile of GH3 and GH20 β-n-acetylglucosaminidases in the entomopathogenic fungus Metarhizium anisopliae. Genet. Mol. Biol. 41(4):843-857.

Fravel, D. R. 2005. Commercialization and implementation of biocontrol. Annu. Rev. Phytopathol. 43:337-359.

Gao, Q.; Jin, K.; Ying, S. H.; Zhang, Y.; Xiao, G.; Shang, Y.; Duan, Z.; Hu, X.; Xie, X. Q. and Zhou, G. 2011. Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet. 7(1).

Heersmink, R.; van den Hoven, J.; van Eck, N. J. and van Berg, J. d. 2011. Bibliometric mapping of computer and information ethics. Ethics Inf. Technol. 13(3):241-249.

Hu, G. and St. Leger, R. J. 2002. Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. Appl. Environ. Microbiol. 68(12):6383-6387.

Hussain, A.; Ahmed, S. and Shahid, M. 2011. Laboratory and field evaluation of Metarhizium anisopliae var. anisopliae for controlling subterranean termites. Neotrop Entomol. 40(2):244-250.

Keppanan, R.; Sivaperumal, S.; Ramos Aguila, L. C.; Hussain, M.; Bamisile, B. S.; Dash, C. K. and Wang, L. 2018. Isolation and characterization of Metarhizium anisopliae TK29 and its mycoinsecticide effects against subterranean termite Coptotermes formosanus. Microb. Pathog. 123:52-59.

Kershaw, M. J.; Moorhouse, E. R.; Bateman, R.; Reynolds, S. E. and Charnley, A. K. 1999. The Role of destruxins in the pathogenicity of Metarhizium anisopliae for three species of insect. J. Invertebr Pathol. 74(3):213-223.

Khorrami, F.; Mehrkhou, F.; Mahmoudian, M. and Ghosta, Y. 2018. Pathogenicity of three different entomopathogenic fungi, Metarhizium anisopliae IRAN 2252, Nomuraea rileyi IRAN 1020C and Paecilomyces tenuipes IRAN 1026C against the potato tuber moth, Phthorimaea operculella Zeller (Lepidoptera: Gelechiidae). Potato Res. 61(4):297-308.

Kin, P. K.; Moslim, R.; Azmi, W. A.; Kamarudin, N. and Ali, S. R. A. 2017. Genetic variation of entomopathogenic fungi, Metarhizium anisopliae and Isaria amoenerosea and their pathogenicity against subterranean termite, Coptotermes curvignathus. J. Oil Palm. Res. 29(1):35-46.

Leger, R. J. S.; Charnley, A. K. and Cooper, R. M. 1987. Characterization of cuticle-degrading proteases produced by the entomopathogen Metarhizium anisopliae. Arch. Biochem, Biophys. 253(1):221-232.

Lezama-Gutiérrez, R.; Molina-Ochoa, J.; Chávez-Flores, O.; Ángel-Sahagún, C. A.; Skoda, S. R.; Reyes-Martínez, G.; Barba-Reynoso, M.; Rebolledo-Domínguez, O.; Ruíz-Aguilar, G. M. L. and Foster, J. E. 2012. Use of the entomopathogenic fungi Metarhizium anisopliae, Cordyceps bassiana and Isaria fumosorosea to control Diaphorina citri (Hemiptera: Psyllidae) in persian lime under field conditions. Int. J. Trop. Insect. Sci. 32(1):39-44.

Lobo, L. S.; Rodrigues, J. and Luz, C. 2016. Effectiveness of Metarhizium anisopliae formulations against dengue vectors under laboratory and field conditions. Bio. Sci. Technol. 26(3):386-401.

Meyling, N. V. and Eilenberg, J. 2007. Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biol. Control. 43(2):145-155.

Mirhaghparast, S. K.; Zibaee, A. and Hajizadeh, J. 2013. Effects of Beauveria bassiana and Metarhizium anisopliae on cellular immunity and intermediary metabolism of Spodoptera littoralis Boisduval (Lepidoptera: Noctuidae). Invertebrate Survival J. 10:110-119.

Oliveira, D. G. P. D.; Lopes, R. B.; Rezende, J. M. and Delalibera, I. 2018. Increased tolerance of Beauveria bassiana and Metarhizium anisopliae conidia to high temperature provided by oil-based formulations. J. Invertebr. Pathol. 151:151-157.

Olombrada, M.; Medina, P.; Budia, F.; Gavilanes, J. G.; Martínez-Del-Pozo, A. and García-Ortega, L. 2017. Characterization of a new toxin from the entomopathogenic fungus Metarhizium anisopliae: The ribotoxin anisoplin. Biol. Chem. 398(1):135-142.

Petlamul, W. and Prasertsan, P. 2012. Evaluation of strains of Metarhizium anisopliae and Beauveria bassiana against Spodoptera litura on the basis of their virulence, germination rate, conidia production, radial growth and enzyme activity. Mycobiology. 40(2):111-116.

Polanczyk, R. A.; Pratissoli, D.; Dalvi, L. P.; Grecco, E. D. and Franco, C. R. 2010. Effect of Beauveria bassiana (Bals.) Vuillemin and Metarhizium anisopliae (Metsch.) Sorokin on the biological parameters of Trichogramma atopovirilia Oatman & Platner (Hymenoptera: Trichogrammatidae). Cienc. Agrotecnol. 34(6):1412-1416.

Rangel, D. E. N.; Anderson, A. J. and Roberts, D. W. 2006. Growth of Metarhizium anisopliae on non-preferred carbon sources yields conidia with increased UV-B tolerance. J. Invertebr. Pathol. 93(2):127-134.

Rath, A. C. 2000. The use of entomopathogenic fungi for control of termites. Biocontrol Sci. Technol. 10(5):563-581.

Riaz, A.; Rasib, K. Z. and Raza, S. 2017. Effect of Metarhizium anisopliae on different group size of Coptotermes heimi. Annu. Res. Rev. Biol. 14(1).

Rivero-Borja, M.; Guzmán-Franco, A. W.; Rodríguez-Leyva, E.; Santillán-Ortega, C. and Pérez-Panduro, A. 2018. Interaction of Beauveria bassiana and Metarhizium anisopliae with chlorpyrifos ethyl and spinosad in Spodoptera frugiperda larvae. Pest. Manage. Sci. 74(9):2047-2052.

Rosas-García, N. M. and Alba-Moreno, I. M.; Villegas-Mendoza, J. M. y Mireles-Martínez, M. 2018. Biological activity of Metarhizium anisopliae strains and essential oils alone and in combination against Diaphorina citri. Southwest Entomol. 43(3):617-624.

Rustiguel, C. B.; Fernández-Bravo, M.; Guimarães, L. H. S. and Moraga, E. Q. 2018. Different strategies to kill the host presented by Metarhizium anisopliae and Beauveria bassiana. Can. J. Microbiol. 64(3):191-200.

Samsuddin, A. S.; Sajap, A. S. and Mohamed, R. 2015. Metarhizium anisopliae of peninsular Malaysia origin poses high pathogenicity toward Coptotermes curvignathus, a major wood and tree pest. Malaysian Forester. 78(1-2):41-48.

Santos, V.; Mascarin, G. M.; da Silva-Lopes, M.; Alves, M. C. D. F.; Rezende, J. M.; Gatti, M. S. V.; Dunlap, C. A. and Delalibera-Júnior, Í. 2017. Identification of double-stranded RNA viruses in Brazilian strains of Metarhizium anisopliae and their effects on fungal biology and virulence. Plant. Gene. 11:49-58.

Shah, F. A.; Wang, C. S. and Butt, T. M. 2005. Nutrition influences growth and virulence of the insect-pathogenic fungus Metarhizium anisopliae. FEMS Microbiol Lett. 251(2):259-266.

Sinia, A. and Guzman-Novoa, E. 2018. Evaluation of the entomopathogenic fungi Beauveria bassiana GHA and Metarhizium anisopliae UAMH 9198 alone or in combination with thymol for the control of Varroa destructor in honey bee (Apis mellifera) colonies. J. Apic. Res. 57(2):308-316.

St Leger, R. J.; Nelson, J. O. and Screen, S. E. 1999. The entomopathogenic fungus Metarhizium anisopliae alters ambient pH, allowing extracellular protease production and activity. Microbiology. 145(10):2691-2699.

St. Leger, R. J.; Frank, D. C.; Roberts, D. W. and Staples, R. C. 1992. Molecular cloning and regulatory analysis of the cuticle‐degrading‐protease structural gene from the entomopathogenic fungus Metarhizium anisopliae. Eur. J. Biochem. 204(3):991-1001.

van Eck, N. J. and Waltman, L. 2010. Software survey: VOSviewer, a computer program for bibliometric mapping. Scientometrics. 84(2):523-538.

Verma, M.; Sharma, S. and Prasad, R. 2009. Biological alternatives for termite control: a review. Int Biodeterior Biodegrad. 63(8):959-972.

Villamil, C. J. and Martínez, O. J. and Pinzón, E. 2016. Actividad biológica de hongos entomopatógenos sobre Premnotrypes vorax Hustache (Coleoptera: Curculionidae). Rev. Cienc. Agríc. 33(1):34-42.

Wang, C.; Hu, G. and St. Leger, R. J. 2005. Differential gene expression by Metarhizium anisopliae growing in root exudate and host (Manduca sexta) cuticle or hemolymph reveals mechanisms of physiological adaptation. Fungal. Genet. Biol. 42(8):704-718.

Wang, C. and Powell, J. E. 2004. Cellulose bait improves the effectiveness of Metarhizium anisopliae as a microbial control of termites (Isoptera: Rhinotermitidae). Biol Control. 30(2):523-529.

Wang, C. and St. Leger, R. J. 2006. A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proc. Natl. Acad. Sci. USA. 103(17):6647-6652.

Wright, M. S.; Raina, A. K. and Lax, A. R. 2005. A strain of the fungus Metarhizium anisopliae for controlling subterranean termites. J. Econ. Entomol. 98(5):1451-1458.

Yii, J. E.; Bong, C. F. J.; King, J. H. P. adn Kadir, J. 2016. Synergism of entomopathogenic fungus, Metarhizium anisopliae incorporated with fipronil against oil palm pest subterranean termite, Coptotermes curvignathus. Plant. Protect. Sci. 52(1):35-44.

Zeng, G.; Zhang, P.; Zhang, Q.; Zhao, H.; Li, Z.; Zhang, X.; Wang, C.; Yin, W. B. and Fang, W. 2018. Duplication of a Pks gene cluster and subsequent functional diversification facilitate environmental adaptation in Metarhizium species. PLoS Genet. 14(6).

Zhang, X. C.; Li, X. X.; Gong, Y. W.; Li, Y. R.; Zhang, K. L.; Huang, Y. H. adn Zhang, F. 2018. Isolation, identification, and virulence of a new Metarhizium anisopliae strain on the German Cockroach. J. Econ. Entomol. 111(6):2611-2616.

Zimmermann, G. 2007. Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Sci. Technol. 17(9):879-920.