An update of a green pesticide: Metarhizium anisopliae

Figures & data

Figure 1. Overview of the basic infection cycle depicted by M. anisopliae in invertebrates. The infection process can be divided into: (1) conidia adherence to the host cuticle; (2) conidia germination and development; (3) appressorium formation; (4) cuticle penetration; (5) colonization of hemolymph; (6) extrusion and sporulation.

Figure 2. Mycotoxic effects of M. anisopliae. (A) M. anisopliae cultured on Potato Dextrose Agar Medium. At the initial stage, the colonies were white and hairy. In the sporulation stage, there were clumps of green conidia in the middle of the colony. (B) The cadavers of Aedes aegypti infected by M. anisopliae or not. (C) The cadavers of Anopheles stephensi infected by M. anisopliae or not.

Table 1. Agricultural pests and human disease vectors sensitive to M. anisopliae.

Family	Species	Selected references
Culicidae	Anopheles gambiae adults and larvae	Scholte et al. (2006); Opisa et al. (2019)
	Anopheles stephensi larvae	Riba et al. (1986b); Vivekanandhan et al. (2020)
	Anopheles arabiensis adults and larvae	Choi et al. (2020)
	Aedes aegypti adults and larvae	Riba et al. (1986b); Scholte et al. (2007); Vivekanandhan et al. (2020)
	Aedes albopictus adults and larvae	Scholte et al. (2007); Shoukat et al. (2020)
	Culex pipiens adults and larvae	Daoust and Roberts (1982); Choi et al. (2020); Bilal et al. (2012)
	Culex quinquefasciatus adults and larvae	Lwetoijera et al. (2010); Wassermann et al. (2016); Mohanty et al. (2008)
Ixodidae	Dermacentor variabilis adults	Ren et al. (2014)
	Rhipicephalus microplus larvae and adults	Ojeda-Chi et al. (2010); Beys-da-Silva et al. (2020)
	Rhipicephalus sanguineus nymphs and adults	Kirkland et al. (2004); Abuowarda et al. (2020)
	Rhipicephalus appendiculatus larvae, nymphs and adults	Mwangi et al. (1995)
	Ixodes scapularis larvae, nymphs and adults	Zhioua et al. (1997); Inyang et al. (2000)
	Haemaphysalis qinghaiensis adults, nymphs and adults	Ren et al. (2014); Albernaz et al. (2009)
	Hyalomma excavatum adults	Ment et al. (2010b)
Rhinotermitidae	Coptotermes formosanus	Yanagawa and Shimizu (2007); Keppanan et al. (2018)
	Coptotermes curvignathus	Pikkheng et al. (2009); Kin et al. (2017)
	Reticulitermes flavipes	Zober (1995)
	Reticulitermes speratus	Shimizu and Yamaji (2003); Mitaka et al. (2017)
	Heterotermes tenuis adults	Moino et al. (2002)
Termitidae	Odontotermes formosanus	Dong et al. (2009); Fu et al. (2020)
	Nasutitermes exitiosus	Hänel (1982)
Acrididae	Schistocerca gregaria adults, nymphs, eggs	Xia et al. (2000); Abdellaoui et al. (2020)
	Chortoicetes terminifera adults	Hunter et al. (2001)
	Locusta migratoria nymphs	Peng et al. (2008); Liu et al. (2019); Bilal et al. (2012)
	Oxya chinensis nymphs	Zober (1995); Abro et al. (2019)
Pyralidae	Ostrinia furnacalis larvae	Chiuo and Hou (1993)
	Ostrinia nubilalis larvae	Riba et al. (1986a)
	Diatraea saccharalis larvae	De Oliveira et al. (2018); Destéfano et al. (2004)
	Cnaphalocrocis medinalis larvae	Hong et al. (2017); Destéfano et al. (2004)
	Chilo partellus larvae	Tefera and Pringle (2003)
	Galleria mellonella larvae	Keppanan et al. (2017); Sbaraini et al. (2021)
Noctuidae	Spodoptera litura larvae	Sree et al. (2008)
	Spodoptera littoralis larvae	El Husseini (2019)
	Helicoverpa armigera larvae	Lawo et al. (2008); Santi et al. (2011)
	Hyblaea puera larvae	Remadevi et al. (2010)
Carposinidae	Carposina niponensis larvae	Yaginuma (1990)
Lymantriidae	Pantana phyllostachysae adults	Zhang et al. (2002)
Blattellidae	Blattella germanica adults	Lopes and Alves (2011); Chao et al. (2020)
Lasiocampidae	Dendrolimus punctatus larvae	Zhang et al. (2002)
Reduviidae	Triatoma infestans nymphs and adults	Luz et al. (1998)
	Triatoma sordida nymphs and adults	Rangel et al. (2020)
	Panstrongylus megistus nymphs and adults	Rangel et al. (2020)
Delphacidae	Nilaparvata lugens adults	Tang et al. (2019)
	Sogatella furcifera adults	Tang et al. (2019)
Tephritidae	Anastrepha ludens adults	Toledo-Hernández et al. (2018)
	Zeugodacus cucurbitae adults	Onsongo et al. (2019)
Bruchidae	Callosobruchus maculatus adults	Cherry et al. (2005); Ozdemir et al. (2020)
	Caryedon serratus adults	Ekesi et al. (2001)
House flies	Musca domestica larvae and adults	Oreste et al. (2016); Baker et al. (2018)
Tenebrionidae	Alphitobius diaperinus larvae and adults	Ment et al. (2010a); Cassiano et al. (2008); Inyang et al. (2000)
Pyrrhocoridae	Dysdercus peruvianus nymphs and adults	Santi et al. (2011)
Plutellidae	Plutella xylostella larvae	Zafar et al. (2020)
Aleyrodidae	Trialeurodes vaporariorum adults	Oreste et al. (2016)
Aphelinidae	Encarsia formosa larvae and adults	Oreste et al. (2016)
Thripidae	Frankliniella occidentalis adults	Li et al. (2021)
Curculionidae	Curculio nucum larvae	Sharififard et al. (2011)
Cerambycidae	Monochamus alternatus larvae and adults	Li et al. (2021)
Delphacidae	Peregrinus maidis adults	Toledo et al. (2010)
Bostrychidae	Rhyzopertha dominica adults	Ashraf et al. (2017); Saeed et al. (2020)
Tenebrionidae	Tribolium castaneum adults	Ashraf et al. (2017); Saeed et al. (2020)
Laemophloeidae	Cryptolestes ferrugineus adults	Ashraf et al. (2017); Saeed et al. (2020)
Liposcelididae	Liposcelis paeta adults	Ashraf et al. (2017); Saeed et al. (2020)
Phycitidae	Ephestia kuehniella larvae	Athanassiou et al. (2017)
Tortricidae	Thaumatotibia leucotreta adults	Mkiga et al. (2020); Acheampong et al. (2020)
Crambidae	Spoladea recurvalis adults	Opisa et al. (2019)
Gelechiidae	Tuta absoluta pupae	Contreras et al. (2014)
Tettigoniidae	Anabrus simplex nymphs	Rangel et al. (2021)

Table 2. The major approaches for modifying entomopathogens to enhance the virulence of M. anisopliae.

Modified strain	Principal targeted species	Selected references
Ma-AaIT	Hypothenemus hampei larvae	Pava-Ripoll et al. (2008)
	Manduca sexta caterpillars larvae	Wang and St Leger (2007a)
	Aedes aegypti adults	Wang and St Leger (2007a)
Ma-[SM1]8	Plasmodium falciparum and Anopheles gambiae adults	Fang et al. (2011)
Ma-scorpine	Plasmodium falciparum and Anopheles gambiae adults	Fang et al. (2011)
Ma-PfNPNA-1	Plasmodium falciparum and Anopheles gambiae adults	Fang et al. (2011)
Ma-[SM1]8:scorpine	Plasmodium falciparum and Anopheles gambiae adults	Fang et al. (2011)
Ma-Cat1	Plutella xylostella larvae	Morales Hernandez et al. (2010)
Ma-Vip3Aa1	Spodoptera litura larvae	Zhang et al. (2014)

Table 3. Selected examples of formulations using M. anisopliae in various habitats.

Formulation		Habitat	Principal targeted species	Selected references
Oil	ShellSol T	plastic containers	Anopheles gambiae larvae	Bukhari et al. (2011)
		plastic containers	Anopheles stephensi larvae	Bukhari et al. (2011)
		experimental plots	Phaedon cochleariae larvae	Inyang et al. (2000)
	Ondina oil 917	plastic containers	Anopheles gambiae larvae	Bukhari et al. (2011)
		plastic containers	Anopheles stephensi larvae	Bukhari et al. (2011)
	Mineral oil	culture medium	Rhipicephalus microplus larvae, nymphs and adults	Camargo et al. (2012)
	Mineral oil and diatomaceous earth	plastic cups	Aedes aegypti adults	Rodrigues et al. (2019)
	Cornstarch-oil	petri dishes	Diabrotica undecimpunctata adults	Pereira and Roberts (1991)
	Sunflower oil and Imidacloprid (IMI)	petri dishes	Conotrachelus psidii adults	Brito et al. (2008)
	Sunflower oil-in-water	paper cups	Aedes aegypti eggs	Albernaz et al. (2009)
	Oil-in-water	petri plates	Rhipicephalus Microplus females	Muniz et al. (2020)
	Soybean oil	agar plates	Dysdercus peruvianus	Rangel et al. (2020)
	Coconut/soybean oil	capped graduated tubes	Tetranychus cinnabarinus adults	Batta (2003)
		capped graduated tubes	Bemisia tabaci nymphs	Batta (2003)
	Peanut oil	potted grass	Rhipicephalus appendiculatus larvae, nymphs and adults	Kaaya and Hedimbi (2012)
		potted grass	Amblyomma variegatum larvae, nymphs, and adults	Kaaya and Hedimbi (2012)
	Canola oil	field paddock	Rhipicephalus Microplus	Leemon et al. (2008)
	Neem oil	natural field	Aedes aegypti larvae	Paula et al. (2019)
		natural field	Culex quinquefasciatus larvae and adults	Seye et al. (2012)
		experimental cage	Anopheles stephensi female	Dhar et al. (1996)
		experimental cage	Anopheles culicifacies female	Dhar et al. (1996)
		greenhouse conditions	Anopheles gambiae larvae	Okumu et al. (2007)
Dust	Diatomaceous earth	glass-capped dishes	Tribolium confusum larvae and adults	Michalaki et al. (2006)
		small cylindrical glass vial	Rhyzopertha dominica adults	Rice et al. (2019)
		small cylindrical glass vial	Sitophilus oryzae adults	Rice et al. (2019)
Other	Alginate	tightly sealed plastic tubes	Diabrotica undecimpunctata adults	Pereira and Roberts (1991)
	Aqueous	potted grass	Rhipicephalus appendiculatus adults and eggs	Kaaya and Hedimbi (2012)
		recipientes plásticos	Alphitobius diaperinus larvae and adults	Rohde et al. (2006)
	Granular formulations consisting of ground chicken feed pellets with conidial powder	petri dishes	Lesser mealworm larvae	Rice et al. (2019)
	Polymerized cellulose gel combined with surfactants	Polypropylene bags	Rhipicephalus microplus	Rice et al. (2019)

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Data availability statement

Data sharing is not applicable to this article as no new data were created or analysed in this study.