Table 1.
Summary of the studies on the application Metarhizum sp. for controlling pests and vectors of different orders of arthropods.
| Order Lepidoptera | |||||
|---|---|---|---|---|---|
| Family | Species | Economic Relevance | EPFs tested | Effect | Ref. |
| Gelechiidae | Tuta absoluta | Tomato pest | Metarhizium anisopliae (ESALQ9, PL43, PI47, URPE6 URPE19), Beauveria bassiana (ESALQ447, ESALQ900, CG001, CPATC053, CPATC057) plus insecticides chlorfenapyr, spinosad, indoxacarb, abamectin, and neem | M. ansipliae URPE6 and URPE19 were more pathogenic to eggs and first instar larvae. Furthermore, the first mentioned strain was compatible to an average concentration of chlorfenapyr, while the last were compatible with abamectin for optimized application. | (Pires et al., 2010) |
| Phthorimaea operculella | Potato pest | M. anispliae (unidentified strain) | Suspensions at concentrations of 107 to 103 were formulated for mortality tests. The results were heterogeneous, with LCs50 ranging between concentrations of 105, 106 and 107 conidia/mL, resulting in mortality rates ranging from 21.2% to 52.3%. | (Pandey et al., 2015) | |
| Noctuiidae | Spodoptera frugiperda | Cotton, soy, corn | M. anisopliae/B. bassiana plus chlorpyriphos/spinosad | High mortality | (El-Katatny, 2010; Rivero-Borja et al., 2018; Han et al., 2023) |
| Spodoptera littoralis | Cotton, avocado, pea beans, sugar cane | M. brunneum ORP-27, ORP-13, and ORM-40 | Mortalities of 49,79%, 58,78%, and 46% after 13 days post-infection, lethal concentrations of 1.68× 107, 2.10× 107, and 2.25× 107 propagules/mL. | (Şahin and Yanar, 2021) | |
| Alabama argillaceae | Cotton worm | M. anisoplae and B. baussiana with predator bedbug | EPF extinguished the predator bedbug and had no synergistic effects for such circumstances. | (França et al., 2006) | |
| Plutellidae | P. xylostela | Cabbage, broccoli and other cruciferous plants |
Metarhizum brunneum ESALQ E9, IPA-207, ESALQ 860, IPA-204, UFPE 3027 | High lethality for larvae, 58-96%, 105-108 conidia/mL. | (Silva et al., 2003; Hernandez et al., 2010; Callejas-Negrete et al., 2015; Shakeel et al., 2018; Cervantes Quintero et al., 2020) |
| Tortricidae | Thaumatotibia leucotreta | Orange, macadamia,cotton pest | M. brunneum (ICIPE 30, ICIPE 18, ICIPE 78, ICIPE 62, ICIPE 69, ICIPE 63, ICIPE 20, ICIPE 7, ICIPE 74, ICIPE 656, ICIPE 68, ICIPE 40, ICIPE 315, ICIPE 31, ICIPE 22, ICIPE 725, ICIPE 676), and B. bassiana (ICIPE 720, ICIPE 283, ICIPE 273, ICIPE 279, ICIPE 647) | 12 strains with mortality ranging from 58.8 to 94,2% and horizontal transmission from sporulating corpses. | (Mkiga et al., 2020) |
| Lyonetiidae | Leucoptera coffeella | Coffee pest | M. brunneum (RD-20.120) and M. robertsii (RD-20.114) | Lethal and feeding inhibition action. | (Jaber and Ownley, 2018; Franzin et al., 2022) |
| Order Coleoptera | |||||
|---|---|---|---|---|---|
| Family | Species | Economic Relevance | EPFs tested | Effect | Ref. |
| Curculionidae | Listronotus maculicollis | Poaceae pest | M. anisopliae | Mortalities 67-89% and 85-100% (5.2 and 7.3x109 granules/g). Inefficient in semi-field conditions. | (Koppenhöfer et al., 2020) |
| Hylobius abietis | Conifers pest | M. brunneum, B. bassiana, B. caledonica, and Candida albicans | Modulation of insect immunity (PO, glycosidases, antimicrobial peptides) | (Ansari and Butt, 2012; Namara et al., 2018) | |
| Rhynchophorus ferrugineus | Palm beetle | Metarhizium sp. ZJ-1 | Mortality 60% and 100% (106 and 108 propagules/mL) after 10 days. 50% Lethal time of 1.66 days (108 propagules/mL) | (Sun et al., 2016) | |
| Anthonomus grandis | Cotton pest | M. anisopliae, 28 different strains | High integrated lethality with Recommended Field Application Ranges (RFAR) 1.2 x 107 conidia/mL (RFAR 20) and 1.13 x 107 conidia/mL (RFAR 50) | (Nussenbaum and Lecuona, 2012) | |
| Chrysomelidae | Cerotoma arcuata | Legumes pest | B. bassiana, M. anisopliae (multiple strains) and Bacillus thuringiensis | Treatment with conidial suspension (108 conidia/mL) of M. anisopliae CG 210 and CG 321 caused mortality ranging from 80 to 100% within7 days, while B. bassiana strain CG 156 e CG 213 caused 100% mortality in the period. | (Teixeira and Franco, 2007) |
| Brentidae | Cylas formicarius | Sweet potato | M. anisopliae strain QS155 and QS002-3 | High virulence strain QS155 caused over 80% repellence to male adults and over 70% repellence to female adults in comparison to Low virulence strain QS002-3, which caused 29.3% repellence. | (Dotaona et al., 2017) |
| Cerambicidae | Anoplophora glabripennis | Rose bushes, apple trees, mulberry | M. brunneum | High mortality between 22 and 24 days after treatment (108 conidia). | (Clifton et al., 2020) |
| Elateridae | Limonius californicus | Sugar beet, potato | M. brunneum | High mortality dose dependent. | (Ensafi et al., 2018) |
| Scarabeidae | Popillia japonica | Grapes, corn, peas, peaches, plum | M. brunneum | Pure granules LC50 equivalent to 1,9 x 107 was observed for P. japonica and granules plus microesclerotia LC50 equivalent of 5,9 x 107 was detected for P. japonica | (Behle and Goett, 2016) |
| Phyllophaga sp | Soy, wheat, coffee | M. brunneum | Pure granules LC50 equivalent to 7,1 x 106 was observed for Phyllophaga and granules + microesclerotia LC50 equivalent of 5,1 x 107 was detected for Phyllophaga | (Behle and Goett, 2016) | |
| Curculionidae | Hypothenemus hampei | Coffee | Metarhizium sp. MMR-M1 | No significant mortality (105, 107, and 109 conidia/mL). | (Chuquibala-Checan et al., 2023) |
| Order Diptera | |||||
|---|---|---|---|---|---|
| Family | Species | Economic Relevance | EPFs tested | Effect | Ref. |
| Culicidae | Aedes aegypti | Arbovirus vector | M. brunneum strain ARSEFF 4556 | Mechanism of virulence through feeding and apoptosis of intestinal cells. | (Butt et al., 2013) |
| Aedes aegypti | Arbovirus vector | M. anisopliae strain ESALQ818 | Synergism with Neem oil. | (Gomes et al., 2015) | |
| Aedes aegypti | Arbovirus vector | M. anisopliae strain IP46 | Action of propagules with vegetable or mineral oil, and diatomaceous earth. | (Rodrigues et al., 2019) | |
| Aedes aegypti | Arbovirus vector | M. anisopliae/brunneum strains ARSEF V275 and 4556 | Synergism with Phenyl thiourea. | (Prado et al., 2020) | |
| Aedes aegypti | Arbovirus vector | M. anisopliae | Contamination by contact with tissues impregnated with conidia. | (Paula et al., 2013) | |
| Aedes aegypti | Arbovirus vector | M. anisopliae strains ARSEF V275, 4556 and 3297 | Aedes aegypti larvae were more tolerant to the three strains of M. anisopliae in both formulations (wet and dry conidia) | (Greenfield et al., 2015) | |
| Culex quinquefasciatus | Filariasis and Arbovirus vector | M. anisopliae 3 strains ARSEF V275, 4556 and 3297 | Strain ARSEF 4556 was more virulent in comparison to the other two strains, with LT (lethal time) 50 ranging from 0.3 to 1.1 days. Culex quinquefasciatus and Anopheles staphensi were more susceptible than Aedes aegypti to this strain. No significant difference was observed between formulation (dry or aquous/wet). | (Greenfield et al., 2015) | |
| Anopheles stephensi | Malaria vector | M. anisopliae 3 strains ARSEF V275, 4556 and 3297 | Strain ARSEF 4556 was more virulent in comparison to the other two strains, with LT (lethal time) 50 ranging from 0.3 to 1.1 days. Culex quinquefasciatus and Anopheles staphensi were more susceptible than Aedes aegypti to this strain. | (Greenfield et al., 2015) | |
| Culex quinquefasciatus | Filariasis and Arbovirus vector | M. anisopliae and B. bassiana | Synthetic attractants in dry formulations of EPF conidia. | (Paula et al., 2018) | |
| Aedes albopictus | Arbovirus vector | M. anisopliae and B. bassiana | Synthetic attractants in dry formulations of EPF conidia. | (Paula et al., 2018) | |
| Anopheles sp. | Malaria vector | M. anisopliae and B. bassiana | Synthetic attractants in dry formulations of EPF conidia. | (Paula et al., 2018) | |
| Culex quinquefasciatus | Filariasis and Arbovirus vector | M. anisopliae | Virulence and effect on enzymatic activities of chlorpyrifos-resistant strain. | (Ismail et al., 2020) | |
| Aedes albopictus | Arbovirus vector | M. anisopliae | Transgenerational effects and populational control. | (Shoukat et al., 2019) | |
| Anopheles gambiae | Malaria vector | M. anisopliae | Effects of diet and age on treatment outcome. | (Mnyone et al., 2011) | |
| Anopheles stephensi | Malaria vector | M. anisopliae Ma4 and Ma-NBAIR, and B. bassiana Bb5a and Bb-NBAIR | Significant adult mortality (72.5 and 88.75% for Bb5a and BbNBAIR; 57.5% and 48.75% for Ma4 and Ma-NBAIR) after 10 days of exposition to cement or mud panels with 107 propagules/mL. Higher larval mortality for B. baussiana than M. anisopliae. Ma4 delay pupation to 11 days vs 6 days in the control. | (Renuka et al., 2023) | |
| Muscidae | Musca domestica | Mechanical vector (several pathogens) | M. anisopliae with cypermethrin and chlorpyrifos | Administration of sublethal doses of ChCy with a certain concentration of conidia (106 propagules/mL) caused a mortality ranging from 62 to 72% in 5 days. | (Ong et al., 2017) |
| Tephritidae | Ceratitis capitata | Fruit fly | Metarhizium brunneum plus radiation | M. brunneum strain EAMa 01/58-Su showed tolerance to UV-B and was used for testing on insects. C. capitata adults were treated with 5 suspensions (104 - 108 conidia/mL) of conidia and irradiated with UV-B to assess virulence, viability and germination. It was observed that such exposure to UV-B did not significantly interfere with such parameters. The time of exposure to UV-B directly interfered with the mortality exerted by the fungus on the insect, where 6 hours of exposure resulted in 56.7% mortality, 24 hours in 43.3%, and 48 hours resulted in 30% mortality. | (Fernández-Bravo et al., 2017) |
| Zeudogacus cucurbitae | Cucurbitaceae plants, melon, watermelon | M. anisopliae Ma31, MaD, and B. bassiana Bb13, Bb14, Bb337, Bb338, Bb339, and Bb353 | Larval mortality from 1.49-6.33% (MaD) to 5.82-21.70% (Bb337), and from 18.6% (MaD) to 61,1% (Bb337) after 10 days post-treatment. Pupal mortality over 50% (105-1010 propagules/mL). High sporulation rates from insect cadavers (Bb337, Bb338). | (Hintènou et al., 2023) | |
| Ceratopogonidae | Culicoides sp. | Cattle bluetongue virus vector | M. anisopliae | Laboratory and simulated field conditions: strains, doses, population size effects. | (Ansari et al., 2010; Nicholas and Mccorkell, 2014; Ansari et al., 2019; Cazorla and Campos, 2020) |
| Psychodidae | Phlebotomus duboscqui, P. papatasi | Leishmaniasis vectors | M. anisopliae | Effects of population density and number of generations | (Ngumbi et al., 2011; El-Shazly et al., 2012; Zayed et al., 2013) |
| Order Hemiptera | |||||
|---|---|---|---|---|---|
| Family | Species | Economic Relevance | EPFs tested | Effect | Ref. |
| Pentatomidae | Podisus nigrispinus | Predatory bedbug | M. anisopliae and B. bassiana | EPFs extinguished the predator | (França et al., 2006) |
| Delphacidae | Peregrinus maidis | Corn viruses’ vector | M. anisopliae and B. bassiana | Colonization of hemocele and sporulative cycle in 6 days | (Toledo et al., 2010) |
| Pyrrochoridae | Dysdercus peruvianus | Cotton pest | M.anisopliae | Role of host’s ectophosphatase in fungal pathogeneicty | (Cosentino-Gomes et al., 2013) |
| Diaspididae | Aulacaspis tubercularis | Avocado and papaya pest | M. anisopliae and B. bassiana | Efficacy of formulations of 3 strains | (Sayed and Dunlap, 2019) |
| Monophlebidae | Icerya seychellarum | Broad spectrum plant pest | M. anisopliae and B. bassiana | Efficacy of formulations of 3 strains | (Sayed and Dunlap, 2019) |
| Aphidae | Aphis glossypii | Polyphagous plant pest | M. anisopliae with flonicamid, imidacloprid, nitenpyram, dinotefuran, pymetrozine, pyriproxyfen, spirotetramat or matrine | Mortalities from 17.08 (fungi alone) to 91.68% (EPF plus flonicamid) | (Carletto et al., 2009; Nawaz et al., 2022) |
| Reduviidae | Triatoma infestans | Chagas disease vector | M. anisopliae, M. robertsii, M. flavoviridae, and Isaria sp. | Higher mortality rates with Metarhizium than with Isaria | (Rocha and Luz, 2011) |
| Triatoma infestans | Chagas disease vector | B. bassiana, M. anisopliae, Gliocladium virens, and Talaromyces flavus | High efficacy for B. baussiana and G. virens against Mexican insect populations | (Vazquez-Martinez et al., 2014) | |
| Rhodnius prolixus | Chagas disease vector | M. anisopliae and B. bassiana plus Trypanosoma cruzi | Colonization resistance between pathogens | (Rv et al., 2014; Garcia et al., 2016) | |
| Cimicidae | Cimex lectularius | Mechanical vector of several pathogens | M. anisopliae | Effects of moisture, topical or oral treatment | (Ulrich et al., 2014) |
| Order Ixodida | |||||
| Family | Species | Economic Relevance | EPFs tested | Effect | Ref. |
|---|---|---|---|---|---|
| Ixodidae | Riphicephalus microplus | Cattle tick | M. anisopliae with oil formulations | Efficient dispersion with the viability of propagules | (Polar et al., 2005) |
| Rhipicephalus sanguineus | Brown dog tick | M. anisopliae and B. bassiana emulsified with oil and cellulose gel | Higher mortality with fungal viability | (Reis et al., 2008) | |
| Ixodes scapularis | Deer tick, Lyme disease vector | M. anisopliae with permethrin | LD50 of 107 (laboratory) or 109 (field).No synergy between treatments | (Hornbostel et al., 2005) | |
| Riphicephalus microplus | Cattle tick | M. anisopliae plus deltamethrin | Low mortalities in treated field populations. Low egg production after treatment | (Bahiense et al., 2008) | |
| Riphicephalus microplus | Cattle tick | M. anisopliae | Two subtilisinic protease inhibitors BmSI-6 and BmSI-7 have no effects on the interaction with the EPF | (Sasaki et al., 2008) | |
| Ixodes scapularis | Deer tick, Lyme disease vector | B. baussiana and M. anisopliae with bifentrin | Higher efficacy with M. anisopliae than with B. baussiana. Higher mortality in the bifentrin controls | (Stafford and Allan, 2010) | |
| R. microplus | Cattle tick | M. anisopliae | Protection of fungi with aqueous or oily formulations against abiotic factors. Integrated management with low doses of chemical insecticides plus EPFs | (Beys-da-Silva et al., 2020) | |