Relative humidity impacts development and activity against Aedes aegypti adults by granular formulations of Metarhizium humberi microsclerotia.

Biological control Entomopathogenic fungus Granule Mosquito Pellet

Journal

Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612

Informations de publication

Date de publication:
Apr 2021
Historique:
received: 02 12 2020
accepted: 28 01 2021
revised: 15 01 2021
pubmed: 22 3 2021
medline: 15 5 2021
entrez: 21 3 2021
Statut: ppublish

Résumé

The impact of ambient relative humidity (RH) on conidial production of Metarhizium humberi IP 46 microsclerotia (MS) formulated in pellets or granules was investigated, and a promising granular formulation was tested against Aedes aegypti adults to confirm its efficacy. Microcrystalline cellulose (MC) and diatomaceous earth (DE) or a combination of vermiculite (VE), DE and silicon dioxide (SD) were tested as carriers in granular formulations containing MS. A range of 93-96.5% RH was critical for fungal development, and at least 96.5-98.5% RH was required for high conidial production on pellets or granules. Conidial production was clearly higher on pellets and granules prepared with VE than MC as the main carrier. VE granules containing MS were highly active against A. aegypti adults. Most mosquitoes were killed within 6 days after treatment regardless of the exposure time of adults to the formulation (1 min-24 h) or ambient humidity (75 or >98%). Production of conidia on dead adults varied between 7.3 × 10

Identifiants

pubmed: 33745009
doi: 10.1007/s00253-021-11157-6
pii: 10.1007/s00253-021-11157-6
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2725-2736

Subventions

Organisme : CNPq
ID : 14/2012 48329/2012-0
Organisme : CNPq
ID : PQ 308850/2015-7
Organisme : CNPq
ID : PQ 303096/2019-5
Organisme : Health Promotion Administration, Ministry of Health and Welfare (TW)
ID : 440506/2016

Références

Arthurs SP, Thomas MB (2001) Effects of temperature and relative humidity on sporulation of Metarhizium anisopliae var. acridum in mycosed cadavers of Schistocerca gregaria. J Invertebr Pathol 78:59–65. https://doi.org/10.1006/jipa.2001.5050
doi: 10.1006/jipa.2001.5050 pubmed: 11812107
Arthurs SP, Thomas MB, Lawton JL (2001) Seasonal patterns of persistence and infectivity of Metarhizium anisopliae var. acridum in grasshopper cadavers in the Sahel. Entomol Exp Appl 100:69–76. https://doi.org/10.1046/j.1570-7458.2001.00849.x
doi: 10.1046/j.1570-7458.2001.00849.x
ASTM (American Society for Testing Materials) (1958) Maintaining constant relative humidity by means of aqueous solutions. Standards 6: [F33] 961 p.
Behle RW, Jackson MA (2014) Effect of fermentation media on the production, efficacy, and storage stability of Metarhizium brunneum microsclerotia formulated as a prototype granule. J Econ Entomol 107:582–590. https://doi.org/10.1603/EC13426
doi: 10.1603/EC13426 pubmed: 24772537
Behle RW, Jackson MA, Flor-Weiler LB (2013) Efficacy of a granular formulation containing Metarhizium brunneum F52 (Hypocreales: Clavicipitaceae) microsclerotia against nymphs of Ixodes scapularis (Acari: Ixodidae). J Econ Entomol 106:57–63. https://doi.org/10.1603/EC12226
doi: 10.1603/EC12226 pubmed: 23448015
Behle RW, Richmont DS, Jackson MA, Dunlap CA (2015) Evaluation of Metarhizium brunneum F52 (Hypocreales: Clavicipitaceae) for control of Japanese beetle larvae in turfgrass. J Econ Entomol 108:1587–1595. https://doi.org/10.1093/jee/tov176
doi: 10.1093/jee/tov176 pubmed: 26470299
Boyette CD, Quimby PC, Connick WJ, Daigle DJ, Fulgham FE (2012) Progress in the production, formulation, and application of mycoherbicides. In: TeBeest D (ed) Microbial control of weeds. Chapman and Hall, New York, pp 209–224
Braga GUL, Flint SD, Miller CD, Anderson AJ, Roberts DW (2001) Variability in response to UV-B among species and strains of Metarhizium isolated from sites at latitudes from 61°N to 54°S. J Invertebr Pathol 78:98–108. https://doi.org/10.1006/jipa.2001.5048
doi: 10.1006/jipa.2001.5048 pubmed: 11812112
Burges HD (1998) Formulation of microbial biopesticides. Beneficial microorganisms, nematodes and seed treatments. Kluwer Academic Press, Dordrecht.
Chaerunisaa AY, Sriwidodo S, Abdassah M (2019) Microcrystalline cellulose as pharmaceutical excipient. In: Ahmad U, Akhtar J (eds) Pharmaceutical formulation design—recent practices, IntechOpen Limited, London, pp 1−22.
Coley-Smith JR, Cooke RC (1972) Survival and germination of fungal sclerotia. Annu Rev Phytopathol 9:65–92. https://doi.org/10.1146/annurev.py.09.0900171.000433
doi: 10.1146/annurev.py.09.0900171.000433
Evans HC, Samson RA (1982) Cordyceps species and their anamorphs pathogenic on ants (Formicidae) in tropical forest ecosystems 1. The Cephalotes (Myrmicinae) complex. T Brit Mycol Soc 79:431–453. https://doi.org/10.1016/S0007-1536(82)80037-5
doi: 10.1016/S0007-1536(82)80037-5
Fernandes ÉKK, Marreto RN, Luz C, Catão AML, Paixão FRS, Santos TR, Mascarin GM (2017) Composição e processo de preparação multiparticulada de natureza sólida contendo microescleródios de Metarhizium anisopliae para controle de artrópodes-praga de importância na saúde humana, veterinária e na agropecuária e seus usos. Brazil. Patent registered BR1020170040615.
Gardescu S, Hajek AE, Goble TA, Jackson MA (2017) Metarhizium microsclerotia and hydrogel versus hydromulch: testing fungal formulations against Asian longhorned beetles. Biocontrol Sci Techn 27:918–930. https://doi.org/10.1080/09583157.2017.1362546
doi: 10.1080/09583157.2017.1362546
Goble TA, Hajek AE, Jackson MA, Gardescu S (2015) Microsclerotia of Metarhizium brunneum F52 applied in hydromulch for control of Asian longhorned beetles (Coleoptera: Cerambycidae). J Econ Entomol 108:433–443. https://doi.org/10.1093/jee/tov013
doi: 10.1093/jee/tov013 pubmed: 26470154
Goble TA, Gardescu S, Jackson MA, Hajek AE (2016a) Evaluating different carriers of Metarhizium brunneum F52 microsclerotia for control of adult Asian longhorned beetles (Coleoptera: Cerambycidae). Biocontrol Sci Techn 26:1212–1229. https://doi.org/10.1080/09583157.2016.1192103
doi: 10.1080/09583157.2016.1192103
Goble TA, Gardescu S, Fisher JJ, Jackson MA, Hajek AE (2016b) Conidial production, persistence and pathogenicity of hydromulch formulations of Metarhizium brunneum F52 microsclerotia under forest conditions. Biol Control 95:83–93. https://doi.org/10.1016/j.biocontrol.2016.01.003
doi: 10.1016/j.biocontrol.2016.01.003
Heinig RL, Thomas MB (2015) Interactions between a fungal entomopathogen and malaria parasites within a mosquito vector. Malaria J 14:22. https://doi.org/10.1186/s12936-014-0526-x
doi: 10.1186/s12936-014-0526-x
Heinig RL, Paaijmans KP, Hancock PA, Thomas MB (2015) The potential for fungal biopesticides to reduce malaria transmission under diverse environmental conditions. J Appl Ecol 52:1558–1566. https://doi.org/10.1111/1365-2664.12522
doi: 10.1111/1365-2664.12522 pubmed: 26792946 pmcid: 4716011
Hubner-Campos RF, Leles RN, Rodrigues J, Luz C (2013) Efficacy of entomopathogenic hypocrealean fungi against Periplaneta americana. Parasitol Int 62:517–521. https://doi.org/10.1016/j.parint.2013.07.013
doi: 10.1016/j.parint.2013.07.013 pubmed: 23899866
Jackson MA, Jaronski ST (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 113:842–850. https://doi.org/10.1016/j.mycres.2009.03.004
doi: 10.1016/j.mycres.2009.03.004 pubmed: 19358886
Jackson MA, Payne AR (2016) Liquid culture production of fungal microsclerotia. In: Glare TG, Moran-Diez ME (eds) Microbial based biopesticides. Methods and protocols. Springer Nature, New York, pp 71–83
doi: 10.1007/978-1-4939-6367-6_7
Jackson MA, Schisler DA (1995) Liquid culture production of microsclerotia of Colletotrichum truncatum for use as bioherbicidal propagules. Mycol Res 99:879–884. https://doi.org/10.1016/S0953-7562(09)80745-4
doi: 10.1016/S0953-7562(09)80745-4
Kimberly MSA, Seow MH (2017) Mode of infection of Metarhizium spp. fungus and their potential as biological control agents. J Fungi 3(2):30. https://doi.org/10.3390/jof3020030
doi: 10.3390/jof3020030
Lacey LA (2017) Microbial control of medically important mosquitoes in tropical climates. In: Lacey LA (ed) Microbial control of insect and mite pests from theory to practice. Academic Press, London, pp 409–430
doi: 10.1016/B978-0-12-803527-6.00028-7
Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: Back to the future. J Invertebr Pathol 132:1–41. https://doi.org/10.1016/j.jip.2015.07.009
doi: 10.1016/j.jip.2015.07.009 pubmed: 26225455
Lee SJ, Jeong SK, Jong SY, Kim JC, Nai YS, Kim JS (2015) Biological control of Asian tiger mosquito, Aedes albopictus (Diptera: Culicidae) using Metarhizium anisopliae JEF-003 millet grain. J Asia-Pac Entomol 18:217–221. https://doi.org/10.1016/j.aspen.2015.02.003
doi: 10.1016/j.aspen.2015.02.003
Leles RN, Sousa NA, Rocha LFN, Santos AH, Silva HH, Luz C (2010) Pathogenicity of some hypocrealean fungi to adult Aedes aegypti (Diptera: Culicidae). Parasitol Res 107:1271–1274. https://doi.org/10.1007/s00436-010-1991-y
doi: 10.1007/s00436-010-1991-y pubmed: 20680340
Lima WP, Neto FC, Macoris MLG, Zuccari DAPC, Dibo MR (2009) Estabelecimento de metodologia para alimentação de Aedes aegypti (Diptera-Culicidae) em camundongos swiss e avaliação da toxicidade e do efeito residual do óleo essencial de Tagetes minuta L. (Asteraceae) em populações de Aedes aegypti. Rev Soc Bras Med 42:638–641. https://doi.org/10.1590/S0037-86822009000600005
doi: 10.1590/S0037-86822009000600005
Lira AC, Mascarin GM, Delalibera IJ (2020) Microsclerotia production of Metarhizium spp. for dual role as plant biostimulant and control of Spodoptera frugiperda through corn seed coating. Fungal Biol 124:689–699. https://doi.org/10.1016/j.funbio.2020.03.011
doi: 10.1016/j.funbio.2020.03.011 pubmed: 32690250
Luz C, Fargues J (1998) Factors affecting conidial production of Beauveria bassiana from fungus-killed cadavers of Rhodnius prolixus. J Invertebr Pathol 72:97–103. https://doi.org/10.1006/jipa.1998.4774
doi: 10.1006/jipa.1998.4774 pubmed: 9709008
Luz C, Fargues J (1999) Dependence of the entomopathogenic fungus, Beauveria bassiana, on high humidity for infection of Rhodnius prolixus. Mycopathologia 146:33–41. https://doi.org/10.1023/A:1007019402490
doi: 10.1023/A:1007019402490 pubmed: 10721518
Luz C, Tai MHH, Santos AH, Rocha LFN, Albernaz DAS, Silva HHG (2007) Ovicidal activity of entomopathogenic Hyphomycetes on Aedes aegypti (L.) (Diptera: Culicidae) under laboratory conditions. J Med Entomol 44:799–804. https://doi.org/10.1093/jmedent/44.5.799
doi: 10.1093/jmedent/44.5.799 pubmed: 17915511
Luz C, Rodrigues J, Rocha LFN (2012) Diatomaceous earth and oil enhance effectiveness of Metarhizium anisopliae against Triatoma infestans. Acta Trop 122:29–35. https://doi.org/10.1016/j.actatropica.2011.11.014
doi: 10.1016/j.actatropica.2011.11.014 pubmed: 22155570
Luz C, Rocha LFN, Montalva C, Souza DA, Botelho ABRZ, Lopes RB, Faria M, Delalibera IJ (2019) Metarhizium humberi sp. nov. (Hypocreales: Clavicipitaceae), a new member of the PARB clade in the Metarhizium anisopliae complex from Latin America. J Invertebr Pathol 166:1–9. https://doi.org/10.1016/j.jip.2019.107216
doi: 10.1016/j.jip.2019.107216
Mascarin GM, Kobori NN, Vital RCJ, Jackson MA, Quintela ED (2014) Production of microsclerotia by Brazilian strains of Metarhizium spp. using submerged liquid culture fermentation. World J Microb Biot 30:1583–1590. https://doi.org/10.1007/s11274-013-1581-0
doi: 10.1007/s11274-013-1581-0
Mascarin GM, Lopes RB, Fernandes ÉKK, Delalibera I, Luz C, Faria M (2019) Current status and perspectives of fungal entomopathogens used for microbial control of arthropod pests in Brazil. J Invertebr Pathol 165:46–53. https://doi.org/10.1016/j.jip.2018.01.001
doi: 10.1016/j.jip.2018.01.001 pubmed: 29339191
Mnyone LL, Russell TL, Lyimo IN, Lwetoijera DW, Kirby MJ, Luz C (2009) First report of Metarhizium anisopliae IP 46 pathogenicity in adult Anopheles gambiae s.s. and An. arabiensis (Diptera; Culicidae). Parasite Vector 2:59. https://doi.org/10.1186/1756-3305-2-59
doi: 10.1186/1756-3305-2-59
Moyes CL, Vontas J, Martins AJ, Ng LC, Koou SY, Dusfour I, Raghavendra K, Corbel JPV, David JP, Weetman D (2017) Contemporary status of insecticide resistance in the major Aedes vectors of arboviruses infecting humans. PLoS Neglect Trop D 11(7):e0005625. https://doi.org/10.1371/journal.pntd.0005625
doi: 10.1371/journal.pntd.0005625
Muniz-Paredes F, Miranda-Hernandez F, Loera O (2017) Production of conidia by entomopathogenic fungi: from inoculants to final quality tests. World J Microb Biot 33:57. https://doi.org/10.1007/s11274-017-2229-2
doi: 10.1007/s11274-017-2229-2
Rai M (2009) Advances in fungal biotechnology. IK International Publishing House, New Delhi
Rocha LFN, Luz C (2011) Activity of Metarhizium spp. and Isaria spp. from the Central Brazilian Cerrado against Triatoma infestans nymphs. T Roy Soc Trop Med H 105:417–419. https://doi.org/10.1016/j.trstmh.2011.04.012
doi: 10.1016/j.trstmh.2011.04.012
Rocha LFN, Inglis PW, Humber RA, Kipnis A, Luz C (2013) Occurrence of Metarhizium spp. in Central Brazilian soils. J Bas Microbiol 53:251–259. https://doi.org/10.1002/jobm.201100482
doi: 10.1002/jobm.201100482
Rocha LFN, Sousa NA, Rodrigues J, Catão AML, Marques CS, Fernandes ÉKK, Luz C (2015) Efficacy of Tolypocladium cylindrosporum against Aedes aegypti eggs, larvae and adults. J Appl Microbiol 119:1412–1419. https://doi.org/10.1111/jam.12945
doi: 10.1111/jam.12945 pubmed: 26332164
Rodrigues J, Borges PR, Fernandes ÉKK, Luz C (2019) Activity of additives and their effect in formulations of Metarhizium anisopliae s.l. IP 46 against Aedes aegypti adults and on post mortem conidiogenesis. Acta Trop 193:192–198. https://doi.org/10.1016/j.actatropica.2019.03.002
doi: 10.1016/j.actatropica.2019.03.002 pubmed: 30836061
Rogge SA, Mayerhofer J, Enkerli J, Bacher S, Grabenweger G (2017) Preventive application of an entomopathogenic fungus in cover crops for wireworm control. BioControl 62:613–623. https://doi.org/10.1007/s10526-017-9816-x
doi: 10.1007/s10526-017-9816-x
Sandler N, Rantanen J, Heinämäki J, Römer M, Marola M, Yliruusi J (2005) Pellet manufacturing by extrusion-spheronization using process analytical technology. AAPS Pharm Sci Tech 6:174–183. https://doi.org/10.1208/pt060226
doi: 10.1208/pt060226
Santos AH, Tai MHH, Rocha LFN, Silva HHG, Luz C (2009) Dependence of Metarhizium anisopliae on high humidity for ovicidal activity on Aedes aegypti. Biol Control 50:37–42. https://doi.org/10.1016/j.biocontrol.2009.01.018
doi: 10.1016/j.biocontrol.2009.01.018
Scholte E-J, Knols BGJ, Takken W (2006) Infection of the malaria mosquito Anopheles gambiae with the entomopathogenic fungus Metarhizium anisopliae reduces blood feeding and fecundity. J Invertebr Pathol 91:43–49. https://doi.org/10.1016/j.jip.2005.10.006
doi: 10.1016/j.jip.2005.10.006 pubmed: 16376375
Silva RO, Silva HHG, Luz C (2004) Effect of Metarhizium anisopliae isolated from soil samples of the Central Brazilian cerrado against Aedes aegypti larvae under laboratory conditions. Rev Pat Trop 33:207–213. https://doi.org/10.5216/rpt.v33i2.3446
doi: 10.5216/rpt.v33i2.3446
Skinner M, Gouli S, Frank CE, Parker BL, Kim JS (2012) Management of Frankliniella occidentalis (Thysanoptera: Thripidae) with granular formulations of entomopathogenic fungi. Biol Control 63:246–252. https://doi.org/10.1016/j.biocontrol.2012.08.004
doi: 10.1016/j.biocontrol.2012.08.004
Snetselaar J, Andriessen R, Suer RA, Osinga AJ, Knols BGJ, Farenhorst M (2014) Development and evaluation of a novel contamination device that targets multiple life-stages of Aedes aegypti. Parasite Vector 7:200. https://doi.org/10.1186/1756-3305-7-200
doi: 10.1186/1756-3305-7-200
Song S (2018) Fungal microsclerotia development: essential prerequisites, influencing factors, and molecular mechanism. Appl Microbiol Biotechnol 102:9873–9880. https://doi.org/10.1007/s00253-018-9400-z
doi: 10.1007/s00253-018-9400-z pubmed: 30255231
Song Z, Yin Y, Jiang S, Liu J, Wang Z (2014) Optimization of culture medium for microsclerotia production by Nomuraea rileyi and analysis of their viability for use as a mycoinsecticide. BioControl 59:597–605. https://doi.org/10.1007/s10526-014-9589-4
doi: 10.1007/s10526-014-9589-4
Song Z, Lin Y, Du F, Yin Y, Wang Z (2017) Statistical optimisation of process variables and large-scale production of Metarhizium rileyi (Ascomycetes: Hypocreales) microsclerotia in submerged fermentation. Mycology 8:39–47. https://doi.org/10.1080/21501203.2017.1279688
doi: 10.1080/21501203.2017.1279688
Sousa NA, Lobo LS, Rodrigues J, Luz C (2013) New insights on the effectiveness of Metarhizium anisopliae formulation and application against Aedes aegypti eggs. Lett Appl Microbiol 57:193–199. https://doi.org/10.1111/lam.12097
doi: 10.1111/lam.12097 pubmed: 23638865
Sprenkel RK, Brooks WM (1977) Winter survival of the entomogenous fungus Nomuraea rileyi in North Carolina. J Invertebr Pathol 29:262–266. https://doi.org/10.1016/S0022-2011(77)80031-1
doi: 10.1016/S0022-2011(77)80031-1
Thomas MB (2018) Biological control of human disease vectors: a perspective on challenges and opportunities. BioControl 63:61–69. https://doi.org/10.1007/s10526-017-9815-y
doi: 10.1007/s10526-017-9815-y pubmed: 29391855
Throne JE, Weaker DK, Chew V, Baker JE (1995) Probit analysis of correlated data: multiple observations over time at one concentration. J Econ Entomol 88:1510–1512. https://doi.org/10.1093/jee/88.5.1510
doi: 10.1093/jee/88.5.1510
Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzón A, Ownley BH, Pell JK, Rangel DEN, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fung Ecol 2:149–159. https://doi.org/10.1016/j.funeco.2009.05.001
doi: 10.1016/j.funeco.2009.05.001
Wang C, Wang S (2017) Insect pathogenic fungi: genomics, molecular interactions, and genetic improvements. Annu Rev Entomol 62:73–90. https://doi.org/10.1146/annurev-ento-031616-035509
doi: 10.1146/annurev-ento-031616-035509 pubmed: 27860524
Weaver S, Scott C, Charlier C, Vasilakis N, Lecuit M (2018) Zika, chikungunya, and other emerging vector-borne viral diseases. Annu Rev Med 69:6.1–6.14. https://doi.org/10.1146/annurev-med-050715-105122
doi: 10.1146/annurev-med-050715-105122
Willetts HJ, Bullock S (1992) Developmental biology of sclerotia. Mycol Res 96:801–816. https://doi.org/10.1016/S0953-7562(09)81027-7
doi: 10.1016/S0953-7562(09)81027-7
Winston PW, Bates DH (1960) Saturated solutions for the control of humidity in biological research. Ecology 41:232–237. https://doi.org/10.2307/1931961
doi: 10.2307/1931961
Zhou X, Feng MG (2009) Sporulation, storage and infectivity of obligate aphid pathogen Pandora nouryi grown on novel granules of broomcorn millet and polymer gel. J Appl Microbiol 107:1847–1856. https://doi.org/10.1111/j.1365-2672.2009.04363.x
doi: 10.1111/j.1365-2672.2009.04363.x pubmed: 19457028

Auteurs

Juscelino Rodrigues (J)

Laboratório de Patologia de Invertebrados (LPI), Instituto de Patologia Tropical e Saúde Pública (IPTSP), Universidade Federal de Goiás (UFG), Avenida Esperança s/n, Campus Samambaia, Goiânia, GO, 74690-900, Brazil.

Alaine Maria Lopes Catão (AML)

Laboratório de Patologia de Invertebrados (LPI), Instituto de Patologia Tropical e Saúde Pública (IPTSP), Universidade Federal de Goiás (UFG), Avenida Esperança s/n, Campus Samambaia, Goiânia, GO, 74690-900, Brazil.

Amanda Soares Dos Santos (AS)

Laboratório de Patologia de Invertebrados (LPI), Instituto de Patologia Tropical e Saúde Pública (IPTSP), Universidade Federal de Goiás (UFG), Avenida Esperança s/n, Campus Samambaia, Goiânia, GO, 74690-900, Brazil.

Flávia Regina Santos Paixão (FRS)

Laboratório de Patologia de Invertebrados (LPI), Instituto de Patologia Tropical e Saúde Pública (IPTSP), Universidade Federal de Goiás (UFG), Avenida Esperança s/n, Campus Samambaia, Goiânia, GO, 74690-900, Brazil.

Thainá Rodrigues Santos (TR)

Laboratório de Nanosistemas e Dispositivos de Liberação de Fármacos (NanoSYS), Faculdade de Farmácia, UFG, Goiânia, GO, Brazil.

Juan Mercado Martinez (JM)

Laboratório de Patologia de Invertebrados (LPI), Instituto de Patologia Tropical e Saúde Pública (IPTSP), Universidade Federal de Goiás (UFG), Avenida Esperança s/n, Campus Samambaia, Goiânia, GO, 74690-900, Brazil.

Ricardo Neves Marreto (RN)

Laboratório de Nanosistemas e Dispositivos de Liberação de Fármacos (NanoSYS), Faculdade de Farmácia, UFG, Goiânia, GO, Brazil.

Gabriel Moura Mascarin (GM)

Embrapa Meio Ambiente, Rodovia SP 340, km 127.5, S/N, Tanquinho Velho, Jaguariúna, SP, Brazil.

Éverton Kort Kamp Fernandes (ÉKK)

Laboratório de Patologia de Invertebrados (LPI), Instituto de Patologia Tropical e Saúde Pública (IPTSP), Universidade Federal de Goiás (UFG), Avenida Esperança s/n, Campus Samambaia, Goiânia, GO, 74690-900, Brazil.

Richard Alan Humber (RA)

USDA-ARS Robert W Holley Center for Agriculture and Health, Ithaca, NY, USA.

Christian Luz (C)

Laboratório de Patologia de Invertebrados (LPI), Instituto de Patologia Tropical e Saúde Pública (IPTSP), Universidade Federal de Goiás (UFG), Avenida Esperança s/n, Campus Samambaia, Goiânia, GO, 74690-900, Brazil. wchrisluz@hotmail.com.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH