Current status and perspectives of fungal entomopathogens used for microbial control of arthropod pests in Brazil

Agrofit - Sistema de agrotóxicos fitossanitários - Ministério da Agricultura, Pecuária e Abastecimento, 2017. <http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons> (accessed 25 August 2017). Almeida, 2009, Seleção de isolados de Beauveria bassiana para o controle de Cosmopolites sordidus (Germar, 1824) (Coleoptera: Curculionidae), Arq. Inst. Biol., 76, 489, 10.1590/1808-1657v76p4892009 Alves, 2017, Heat-stressed Metarhizium anisopliae: viability (in vitro) and virulence (in vivo) assessments against the tick Rhipicephalus sanguineus, Parasitol. Res., 116, 111, 10.1007/s00436-016-5267-z Alves, 2008, 414 Amóra, 2009, Evaluation of the fungus Beauveria bassiana (Deuteromycotina: Hyphomycetes), a potential biological control agent of Lutzomyia longipalpis (Diptera, Psychodidae), Biol. Control, 50, 329, 10.1016/j.biocontrol.2009.05.004 Amóra, 2010, The effects of the fungus Metarhizium anisopliae var. acridum on different stages of Lutzomyia longipalpis (Diptera: Psychodidae), Acta Trop., 113, 214, 10.1016/j.actatropica.2009.10.018 Ausique, 2017, Efficacy of entomopathogenic fungi against adult Diaphorina citri from laboratory to field applications, J. Pest. Sci., 90, 947, 10.1007/s10340-017-0846-z Belasque, 2010, Lessons from Huanglongbing management in São Paulo state, Brazil, J. Plant Pathol., 92, 285 Bettiol, 2011, Biopesticide use and research in Brazil, Outlooks Pest Manage., 2, 280, 10.1564/22dec10 Bustillo, 1999, Dynamics of Beauveria bassiana and Metarhizium anisopliae infecting Hypothenemus hampei (Coleoptera: Scolytidae) populations emerging from fallen coffee berries, Fl. Entomol., 82, 491, 10.2307/3496468 Camargo, 2014, Commercial formulation of Metarhizium anisopliae for the control of Rhipicephalus microplus in a pen study, Vet. Parasitol., 205, 271, 10.1016/j.vetpar.2014.07.011 Camargo, 2016, Metarhizium anisopliae for controlling Rhipicephalus microplus ticks under field conditions, Vet. Parasitol., 223, 38, 10.1016/j.vetpar.2016.04.014 Carolino, 2014, Monitoring persistence of the entomopathogenic fungus Metarhizium anisopliae under simulated field conditions with the aim of controlling adult Aedes aegypti (Diptera: Culicidae), Parasite Vector, 7, 198, 10.1186/1756-3305-7-198 Conceschi, 2016, Transmission potential of the entomopathogenic fungi Isaria fumosorosea and Beauveria bassiana from sporulated cadavers of Diaphorina citri and Toxoptera citricida to uninfected D. citri adults, Biocontrol, 61, 567, 10.1007/s10526-016-9733-4 Costa, 2002, Ocorrência de Beauveria bassiana (Bals.) Vuill. em broca-do-café (Hypothenemus hampei, Ferrari) no estado de Rondônia, Brasil, Acta Amazon, 32, 517, 10.1590/1809-43922002323519 Cure, 1998, Fenologia e dinâmica populacional da broca do café Hypothenemus hampei (Ferr.) relacionadas às fases de desenvolvimento do fruto, An. Soc. Entomol. Brasil, 27, 325, 10.1590/S0301-80591998000300002 Dias, 2016, Patterns of land use, extensification, and intensification of Brazilian agriculture, Glob. Change Biol., 22, 2887, 10.1111/gcb.13314 Dinardo-Miranda, 2002, Efeito de inseticidas no controle de Mahanarva fimbriolata (Stål) (Hemiptera: Cercopidae) e de nematóides fitoparasitos na qualidade tecnológica e na produtividade da cana-de-açúcar, Neotrop. Entomol., 31, 609, 10.1590/S1519-566X2002000400014 Dufour, 2008, Optimization of coffee berry borer, Hypothenemus hampei Ferrari (Col., Scolytidae), mass trapping with an attractant mixture, J. Appl. Entomol., 132, 591, 10.1111/j.1439-0418.2008.01291.x FAO, 2015 Fancelli, M., Dias, A.B., Delalibera Jr., I., Jesus, S.C., Nascimento, A.S., Silva, S.O., Caldas, R.C., Ledo, C.A.S., 2013. Beauveria bassiana strains for biological control of Cosmopolites sordidus (Germ.) (Coleoptera: Curculionidae) in Plantain. BioMed. Res. Int. Article ID 184756. http://doi.org/10.1155/2013/184756. Faria, P., 2017. Biocontrol in Brazil: opportunities and Challenges. AgroPages: Biopesticide Supplement. Oct. 2017. <http://www.agropages.com/magazine/detail-8-179.htm> (accessed 20 December 2017). Faria, 2002, Effects of two dosages of Metarhizium anisopliae var. acridum on Rhammatocerus schistocercoides Rehn (Orthoptera: Acrididae) in field conditions, Pesq. Agrop. Bras., 37, 1531, 10.1590/S0100-204X2002001100003 Faria, 2007, Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types, Biol. Control, 43, 237, 10.1016/j.biocontrol.2007.08.001 Faria, 2012, Application of modified atmosphere packaging (gas flushing and active packaging) for extending the shelf life of Beauveria bassiana conidia at high temperatures, Biol. Control, 61, 78, 10.1016/j.biocontrol.2011.12.008 Faria, 2015, Conidial vigor vs. viability as predictors of virulence of entomopathogenic fungi, J. Invertebr. Pathol., 125, 68, 10.1016/j.jip.2014.12.012 Faria, 2017, Susceptibility of the biocontrol fungi Metarhizium anisopliae and Trichoderma asperellum (Ascomycota: Hypocreales) to imbibitional damage is driven by conidial vigor, Biol. Control, 107, 87, 10.1016/j.biocontrol.2017.01.015 Fernandes, 2008, Entomopathogenic fungi against South American tick species, Exp. Appl. Acarol., 46, 71, 10.1007/s10493-008-9161-y Gomes, 2015, Neem oil increases the efficiency of the entomopathogenic fungus Metarhizium anisopliae for the control of Aedes aegypti (Diptera: Culicidae) larvae, Parasit. Vectors, 8, 669, 10.1186/s13071-015-1280-9 Humber, 2013, Morphology and molecular taxonomy of Evlachovaea-like fungi, and the status of this unusual conidial genus, Fungal Biol., 117, 1, 10.1016/j.funbio.2012.10.001 Jackson, 1997, Optimizing nutritional conditions for the liquid culture production of effective fungal biological control agents, J. Ind. Microbiol. Biotechnol., 19, 180, 10.1038/sj.jim.2900426 Jackson, 2009, Production of microsclerotia of the fungal entomopathogen Metarhizium anisopliae and their potential for use as a biocontrol agent for soil-inhabiting insects, Mycol. Res., 113, 842, 10.1016/j.mycres.2009.03.004 Jackson, M.A., Mascarin, G.M., 2015. Stable fungal blastospores and methods for their production, stabilization and use. Patent US20160075992. Jaramillo, 2015, Beauveria bassiana y Metarhizium anisopliae para el control de broca del café en frutos del suelo, Rev. Colomb. Entomol., 41, 95 Jenkins, 2000, Quality control of fungal and viral biocontrol agents – assurance of product performance, Biocontrol Sci. Technol., 10, 753, 10.1080/09583150020011717 Infante, 2014, The coffee berry borer: the centenary of a biological invasion in Brazil, Braz. J. Biol., 74, S125, 10.1590/1519-6984.15913 Lecoq, M., 1991. Les criquets du Brésil; nature du problème et bibliographie. EMBRAPA/NMA and CIRAD/PRIFAS (Montpellier), 157 pp. Leles, 2010, Pathogenicity of some hypocrealean fungi to adult Aedes aegypti (Diptera: Culicidae), Parasitol. Res., 107, 1271, 10.1007/s00436-010-1991-y Li, 2010, Biological control of insects in Brazil and China: history, current programs and reasons for their successes using entomopathogenic fungi, Biocontrol Sci. Technol., 20, 117, 10.1080/09583150903431665 Lobo, 2016, Effectiveness of Metarhizium anisopliae formulations against dengue vectors under laboratory and field conditions, Biocontrol Sci. Technol., 26, 386, 10.1080/09583157.2015.1123220 Lopes, 2007, Eficiência de formulações de Beauveria bassiana e Metarhizium anisopliae para o controle de ninfas de Amblyomma cajennense (Fabricius, 1787), Rev. Bras. Parasitol. Vet., 16, 27 Lopes, 2011, Virulence and horizontal transmission of selected Brazilian strains of Beauveria bassiana against Cosmopolites sordidus under laboratory conditions, Bull. Insectol., 64, 201 Lopes, 2013, Diversity of indigenous Beauveria and Metarhizium spp. in a commercial banana field and their virulence toward Cosmopolites sordidus (Coleoptera: Curculionidae), Fungal Ecol., 6, 356, 10.1016/j.funeco.2013.06.007 Lopes, 2013, Genetic diversity and pathogenicity of Metarhizium spp. associated with the white grub Phyllophaga capillata (Blanchard) (Coleoptera: Melolonthidae) in a soybean field, Neotrop. Entomol., 42, 436, 10.1007/s13744-013-0146-0 Lopes, 2014, Combination of the fungus Beauveria bassiana and pheromone in an attract-and-kill strategy against the banana weevil, Cosmopolites sordidus, Entomol. Exp. Appl., 151, 75, 10.1111/eea.12171 Lopes, 2014, MALDI-TOF mass spectrometry applied to identifying species of insect-pathogenic fungi from the Metarhizium anisopliae complex, Mycologia, 106, 865, 10.3852/13-401 Lopes, 2015, The fungistatic and fungicidal effects of volatiles from metathoracic glands of soybean-attacking stink bugs (Heteroptera: Pentatomidae) on the entomopathogen Beauveria bassiana, J. Invertebr. Pathol., 132, 77, 10.1016/j.jip.2015.08.011 Lopes, 2017, Metarhizium alvesii sp. nov.: a new member of the Metarhizium anisopliae species complex, J. Invertebr. Pathol. Luz, 2004, Activity of oil-formulated Beauveria bassiana against Triatoma sordida in peridomestic areas in Central Brazil, Mem. I. Oswaldo Cruz, 99, 211, 10.1590/S0074-02762004000200017 Luz, 2007, Ovicidal activity of entomopathogenic Hyphomycetes on Aedes aegypti (Diptera: Culicidae) under laboratory conditions, J. Med. Entomol., 44, 799, 10.1093/jmedent/44.5.799 Luz, 1998, Selection of Beauveria bassiana and Metarhizium anisopliae isolates to control Triatoma infestans, Mem. I. Oswaldo Cruz, 93, 839, 10.1590/S0074-02761998000600026 Luz, 2008, Impact of moisture on survival of Aedes aegypti eggs and ovicidal activity of Metarhizium anisopliae under laboratory conditions, Mem. I. Oswaldo Cruz, 103, 214, 10.1590/S0074-02762008000200016 Luz, 2012, Diatomaceous earth and oil enhance effectiveness of Metarhizium anisopliae against Triatoma infestans, Acta Trop., 122, 29, 10.1016/j.actatropica.2011.11.014 Magalhães, 2000, Field trial with the entomopathogenic fungus Metarhizium anisopliae var. acridum against bands of the grasshopper Rhammatocerus schistocercoides in Brazil, Biocontrol Sci. Technol., 10, 427, 10.1080/09583150050115016 Mascarin, 2010, Culture media selection for mass production of Isaria fumosorosea and Isaria farinosa, Braz. Arch. Biol. Technol., 53, 753, 10.1590/S1516-89132010000400002 Mascarin, 2017, First record of epizootics in the ocola skipper, Panoquina ocola (Lepidoptera: Hesperiidae), caused by Isaria tenuipes in flooded rice fields of Central Brazil, J. Appl. Microbiol., 122, 1020, 10.1111/jam.13390 Mascarin, 2016, The production and uses of Beauveria bassiana as a microbial insecticide, World J. Microbiol. Biotechnol., 32, 1, 10.1007/s11274-016-2131-3 Mascarin, 2016, Seasonal prevalence of the insect pathogenic fungus Colletotrichum nymphaeae in Brazilian citrus groves under different chemical pesticide regimes, Fungal Ecol., 22, 43, 10.1016/j.funeco.2016.04.005 Mascarin, 2016, Improved shelf life of Beauveria bassiana blastospores by convective drying methods and active packaging, Appl. Microbiol. Biotechnol., 100, 8359, 10.1007/s00253-016-7597-2 Mascarin, 2015, Liquid culture fermentation for rapid production of desiccation tolerant blastospores of Beauveria bassiana and Isaria fumosorosea strains, J. Invertebr. Pathol., 127, 11, 10.1016/j.jip.2014.12.001 Mascarin, 2015, Glucose concentration alters dissolved oxygen levels in liquid cultures of Beauveria bassiana and affects the formation and efficacy of blastospores, Appl. Microbiol. Biotechnol., 99, 6653, 10.1007/s00253-015-6620-3 Mascarin, 2014, Production of microsclerotia by Brazilian strains of Metarhizium spp. using submerged liquid culture fermentation, World J. Microbiol. Biotechnol., 30, 1583, 10.1007/s11274-013-1581-0 Mascarin, 2013, The virulence of entomopathogenic fungi against Bemisia tabaci biotype B (Hemiptera: Aleyrodidae) and their conidial production using solid substrate fermentation, Biol. Control, 66, 209, 10.1016/j.biocontrol.2013.05.001 Michereff-Filho, 2009, Micoinseticidas e micoacaricidas no Brasil: como estamos após quatro décadas?, Arq. Inst. Biol., 76, 769, 10.1590/1808-1657v76p7692009 Montalva, 2016, A natural fungal infection of a sylvatic cockroach with Metarhizium blattodeae sp. nov., a member of the M. flavoviride species complex, Fungal Biol., 120, 655, 10.1016/j.funbio.2016.03.004 Montalva, 2016, Conidiobolus macrosporus (Entomophthorales), a mosquito pathogen in Central Brazil, J. Invertebr. Pathol., 139, 102, 10.1016/j.jip.2016.08.003 Montalva, 2016, First report of Leptolegnia chapmanii (Peronosporomycetes: Saprolegniales) affecting mosquitoes in Central Brazil, J. Invertebr. Pathol., 136, 109, 10.1016/j.jip.2016.03.012 Moscardi, 1999, Assessment of the application of Baculoviruses for control of Lepidoptera, Annu. Rev. Entomol., 44, 257, 10.1146/annurev.ento.44.1.257 Mota, 2017, Autoinoculation trap for management of Hypothenemus hampei (Ferrari) with Beauveria bassiana (Bals.) in coffee crops, Biol. Control, 111, 32, 10.1016/j.biocontrol.2017.05.007 Parra, 2014, Biological control in Brazil: an overview, Sci. Agric., 71, 345, 10.1590/0103-9016-2014-0167 Paula, 2013, Efficiency of fungus-impregnated black cloths combined with imidacloprid for the control of adult Aedes aegypti (Diptera: Culicidae), Lett. Appl. Microbiol., 57, 157, 10.1111/lam.12090 Pignati, 2017, Spatial distribution of pesticide use in Brazil: a strategy for health surveillance, Cienc. Saude Colet., 22, 3281, 10.1590/1413-812320172210.17742017 Powell, 1982, Project tick control, Queensland Agr. J., 12, 279 Quintela, 2013, Enhanced susceptibility of Tibraca limbativentris (Heteroptera: Pentatomidae) to Metarhizium anisopliae with sublethal doses of chemical insecticides, Biol. Control, 66, 56, 10.1016/j.biocontrol.2013.03.018 Rosa, 2000, Effect of Beauveria bassiana and Metarhizium anisopliae (Deuteromycetes) upon the Coffee Berry Borer (Coleoptera: Scolytidae) under field conditions, J. Econ. Entomol., 93, 1409, 10.1603/0022-0493-93.5.1409 Rezende, 2015, Phylogenetic diversity of Brazilian Metarhizium associated with sugarcane agriculture, Biocontrol, 60, 495, 10.1007/s10526-015-9656-5 Rocha, 2011, Activity of Metarhizium spp. and Isaria spp. from the Central Brazilian Cerrado against Triatoma infestans nymphs, T. Roy. Soc. Trop. Med. H., 105, 417, 10.1016/j.trstmh.2011.04.012 Rodrigues, 2015, Effect of formulated Metarhizium anisopliae on eggs and ecloding nymphs of Triatoma infestans, J. Appl. Entomol., 139, 146, 10.1111/jen.12183 Rueda-Páramo, 2017, First report of Coelomomyces santabrancae sp. nov. (Blastocladiomycetes: Blastocladiales) infecting mosquito larvae (Diptera: Culicidae) in central Brazil, J. Invertebr. Pathol., 149, 114, 10.1016/j.jip.2017.08.010 Silva, 2004, Effect of Metarhizium anisopliae isolated from soil samples of the central Brazilian cerrado against Aedes aegypti larvae under laboratory conditions, Rev. Patol. Trop., 33, 207 Sosa-Gomez, 1997, Attachment of Metarhizium anisopliae to the southern green stink bug Nezara viridula cuticle and fungistatic effect of cuticular lipids and aldehydes, J. Invertebr. Pathol., 69, 31, 10.1006/jipa.1996.4619 Sousa, 2013, New insights on the effectiveness of Metarhizium anisopliae formulation and application against Aedes aegypti eggs, Lett. Appl. Microbiol., 57, 193, 10.1111/lam.12097 van Lenteren, 2017, Biological control using invertebrates and microorganisms: plenty of new opportunities, Biocontrol Vicentini, 2001, Screening of Beauveria bassiana (Deuteromycotina: Hyphomycetes) isolates against nymphs of Bemisia tabaci (Genn.) biotype B (Hemiptera: Aleyrodidae) with description of a new bioassay method, Neotrop. Entomol., 30, 97, 10.1590/S1519-566X2001000100015 Wilcken, 2015, Gorgulho-do-eucalipto Gonipterus platensis Marelli, 779