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Efficacy of entomopathogenic fungi against adult Diaphorina citri from laboratory to field applications

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Abstract

The Asian citrus psyllid, Diaphorina citri, is the most serious threat to citrus crops worldwide, and its management relies exclusively on frequent applications of chemical insecticides. Entomopathogenic fungi may play an important role for regulating this citrus pest. Two virulent fungal strains, Isaria fumosorosea ESALQ-1296 and Beauveria bassiana ESALQ-PL63, were selected among 17 fungal isolates under laboratory conditions and caused 77.8 and 78.4% adult mortality, respectively, while in semifield trials the adult mortality reached up to 83.5% with B. bassiana and 80.6% with I. fumosorosea. The bioefficacy of these two fungi on D. citri adults was assessed through monthly applications during 1 year in a commercial citrus grove located in Itapetininga, São Paulo, Brazil. The application of I. fumosorosea ESALQ-1296 and B. bassiana ESALQ-PL63 was as effective as the chemical insecticides in most trials. The fungal-induced mortality of D. citri adults ranged from 96.1% in December 2011 to 57.8% in October 2012. This mortality level tended to build up with the increase in the maximum relative humidity; the percentage of sporulated cadavers was positively correlated with both higher relative humidity and rainfall but negatively associated with maximum temperatures. These results support the use of I. fumosorosea or B. bassiana as an eco-friendly biopesticide for the integrated management of D. citri.

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References

  • Avery PB, Wekesa VW, Hunter WB, Hall DG, Mckenzie CL, Osborne LS, Powell CA, Rogers ME (2011) Effects of the Isaria fumosorosea (Hypocreales: Cordycipitaceae) on reduced feeding and mortality of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Biocontrol Sci Technol 21(9):1065–1078

    Article  Google Scholar 

  • Belasque JJ, Bassanezi RB, Yamamoto PT, Ayres AJ, Tachibana A, Violante AR, Tank AJ Jr, Di Giorgi F, Tersi FEA, Menezes GM, Dragone J, Jank RH Jr, Bové JM (2010) Lessons from huanglongbing management in São Paulo state, Brazil. J Plant Pathol 92:285–302

    Google Scholar 

  • Belotti VH, Rugno GR, Felippe MR, Carmo-uehara A, Garbim LF, Godoy WAC, Yamamoto PT (2013) Population dynamics of Diaphorina citri Kuwayama (Hemiptera: Liviidae) in orchards of ‘Valencia’ orange, ‘Ponkan’ mandarin and ‘Murcott’ tangor trees. Fla Entomol 96(1):173–179

    Article  Google Scholar 

  • Bové JM (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J Plant Pathol 88:7–37

    Google Scholar 

  • Cardoso ER, Freitas S, Nunes HT, Pessoa LGA (2007) Seletividade de Lecanicillium lecanii e Metarhizium anisopliae para larvas de primeiro instar de Ceraeochrysa cincta (Neuroptera: Chrysopidae) em laboratório. Acta Sci Agron 29(4):563–568

    Article  Google Scholar 

  • Casique-Valdes R, Reyes-Martinez AY, Sanchez-Peña SR, Bidochka MJ, Lopez-Arroyo JL (2011) Pathogenicity of Hirsutella citriformis (Ascomycota: Cordycipitaceae) to Diaphorina citri (Hemiptera: Psyllidae) and Bactericera cockerelli (Hemiptera: Triozidae). Fla Entomol 94:703–705

    Article  Google Scholar 

  • Coleta-Filho HD, Targon MLPN, Takita MA, De Negri JD, Pompeu JRJ, Machado MA (2004) First report of the causal agent of Huanglongbing (‘Candidatus Liberibacter asiaticus’) in Brazil. Plant Dis 88:1382

    Article  Google Scholar 

  • Conceschi MR, D’Alessandro CP, Moral RA, Demétrio CGB, Delalibera IJ (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 61:567–577

    Article  Google Scholar 

  • Costa Lima AM (1942) Homópteros. Insetos do Brasil. Escola Nacional de Agronomia, Rio de Janeiro, vol 3, pp 1–327

  • Faria MR, Magalhães BP (2001) O uso de fungos entomopatogênicos no Brasil. Biotecnol Ciênc Desenvolv 4:18–21

    Google Scholar 

  • Ferreira Pinto AP, Batista Filho A, Almeida JEM, Wenzel IM (2012) Patogenicidade de Beauveria bassiana ao psilídeo Diaphorina citri e compatibilidade do fungo com produtos fitossanitários. Pesq Agropec Bras 47:1673–1680

    Article  Google Scholar 

  • Goettel MS, Inglis DG (1997) Fungi: hyphomicetes. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology, 2nd edn. Springer, Dordrecht, pp 249–264

    Google Scholar 

  • Halbert SE, Sun X, Dixon WN (2000) Asian citrus psyllid and citrus greening disease. Citrus Ind 91:22–24

    Google Scholar 

  • Hoy MA, Sing R, Rogers ME (2010) Evaluations of a novel isolate of Isaria fumosorosea for control the Asian Citrus Psyllid, Diaphorina citri (Hemiptera: Psyllidae). Fla Entomol 93:24–32

    Article  Google Scholar 

  • Humber RA (2012) Identification of entomopathogenic fungi. In: Lacey LA (ed) Manual of techniques in invertebrate pathology. Academic Press, London, pp 151–187

    Chapter  Google Scholar 

  • Hunter WB, Avery PB, Pick D, Powell CA (2011) Broad spectrum potential of Isaria fumosorosea against insect pests of citrus. Fla Entomol 94(4):1051–1054

    Article  Google Scholar 

  • Inglis GD, Johnson DL, Goettel MS (1997) Effects of temperature and sunlight on mycosis (Beauveria bassiana) of grasshoppers under field conditions. Environ Entomol 26:400–409

    Article  Google Scholar 

  • Jaronski ST (2010) Ecological factors in the inundative use of fungal entomopathogens. Biocontrol 55:159–185

    Article  Google Scholar 

  • Kuchment A (2013) The end of orange juice. Scientific American, New York, pp 52–59

    Google Scholar 

  • Lezama-Gutiérrez R, Molina-Ochoa J, Chávez-Flores O, Ángel-Sahagún CA, Skoda SR, Reyes-Martínez G, Barba-Reynoso M, Rebolledo-Domínguez O, Ruíz-Aguilar GML, Foster JE (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

    Article  Google Scholar 

  • Lezama-Gutiérrez R, Ramírez-Mancilla A, Castrejón-Agapito H, Peralta-Manzo JJ, Rebolledo-Domínguez O (2014) Uso de Metarhizium anisopliae y Cordyceps bassiana (Ascomycetes) para el control de Diaphorina citri (Hemiptera: Psyllidae) en Limón Mexicano. Entomol Mex 1:219–224

    Google Scholar 

  • Medina CL, Rena AB, Siqueira DL, Machado EC (2005) Fisiologia dos citros. In: Matos Jr D, De Negri JD, Pio RM, Pompeu Jr J (eds) Citros. Campinas, São Paulo. pp 146–195

  • Meyer JM, Hoy MA, Boucias DG (2007) Morphological and molecular characterization of a Hirsutella species infecting the Asian citrus psyllid, Diaphorina citri Kumayama (Hemipstera: Psyllidae), in Florida. J Invertebr Pathol 95:101–109

    Article  CAS  PubMed  Google Scholar 

  • Michaud JP (2010) Natural mortality of the Asian citrus psyllid (Homoptera: Psyllidae) in central Florida. Biol Control 29:260–269

    Article  Google Scholar 

  • Monzo C, Qureshi JA, Stansly PA (2014) Insecticide sprays, natural enemy assemblages and predation on Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Bull Entomol Res 104:576–585

    Article  CAS  PubMed  Google Scholar 

  • Nava DE, Torres MLG, Rodrigues MDL, Bento JMS, Parra JRP (2007) Biology of Diaphorina citri (Hem., Psyllidae) on different hosts and at different temperatures. J Appl Entomol 131:709–715

    Article  Google Scholar 

  • Oliveira DGP, Pauli G, Mascarin GM, Delalibera I (2015) A protocol for determination of conidial viability of the fungal entomopathogens Beauveria bassiana and Metarhizium anisopliae from commercial products. J Microbiol Methods 119:44–52

    Article  PubMed  Google Scholar 

  • Orduño-Cruz N, Guzmán-Franco AW, Rodríguez-Leyva E, Alatorre-Rosas R, González-Hernández H, Mora-Aguilera G (2015) In vivo selection of entomopathogenic fungal isolates for control of Diaphorina citri (Hemiptera: Liviidae). Biol Control 90:1–5

    Article  Google Scholar 

  • Ortelli D, Edder P, Corvi C (2005) Pesticide residues survey in citrus fruits. Food Addit Contam 22:423–428

    Article  CAS  PubMed  Google Scholar 

  • Padulla LFL, Alves SB (2009) Suscetibilidade de ninfas de Diaphorina citri a fungos entomopatogênicos. Arq Inst Biol 76:297–302

    Google Scholar 

  • Ribeiro LP, Santos MS, Padoan GL, Vendramim JD (2015) Toxicity of an acetogenin-based bioinsecticide against Diaphorina citri (Hemiptera: Liviidae) and its parasitoid (Hymenoptera: Eulophidae). Fla Entomol 98:835–842

    Article  Google Scholar 

  • Ritz C, Streibig JC (2008) Nonlinear regression with R. useR! series. Springer, New York, p 148

    Google Scholar 

  • Sanches AL, Felippe MR, Uehara-Carmo A, Rugno GR, Yamamoto PT (2009) Eficiência de inseticidas sistêmicos, aplicados em mudas cítricas, em préplantio, no controle de Diaphorina citri (Kuwayama) (Hemiptera: Psyllidae). BioAssay 4:1–7

    Article  Google Scholar 

  • Stauderman K, Avery P, Aristizábal L, Arthur S (2012) Evaluation of Isaria fumosorosea (Hypocreales: Cordycipitaceae) for control of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Biocontrol Sci Technol 22:747–761

    Article  Google Scholar 

  • Subandiyah S, Nikoh N, Sato H, Wagiman F, Tsuyumyu S, Fukatsu T (2000) Isolation and characterization of two entomopathogenic fungi attacking Diaphorina citri (Homoptera: Psylloidea) in Indonesia. Mycoscience 41:509–513

    Article  Google Scholar 

  • Tanada Y, Kaya HK (1993) Insect pathology. Academic Press, London

    Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org

  • Teixeira DC, Saillard C, Eveillard S, Danned JL, Costa PI, Ayres AJ, Bové J (2005) ‘Candidatus Liberibacter americanus’, associated with citrus Huanglongbing (Greening disease) in São Paulo State, Brazil. Int J Syst Evol Microbiol 55:1857–1862

    Article  CAS  Google Scholar 

  • Tiwari S, Mann RS, Rogers ME, Stelinski LL (2011) Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Manag Sci 67:1258–1268

    Article  CAS  PubMed  Google Scholar 

  • Toledo FR, Barbosa JC, Yamamoto PT (2006) Distribuição espacial de Toxoptera citricida Kirkaldy (Hemiptera: Aphididae) na cultura de citros. Rev Bras Frutic 28(2):194–198

    Article  Google Scholar 

  • Tsai JH, Liu YH (2000) Biology of Diaphorina citri (Homoptera: Psyllidae) on four host plants. J Econ Entomol 93(6):1721–1725

    Article  CAS  PubMed  Google Scholar 

  • Warton DI, Hui FKC (2011) The arcsine is asinine: the analysis of proportions in ecology. Ecology 92:3–10

    Article  PubMed  Google Scholar 

  • Yamamoto PT, Paiva PEB, Gravena S (2001) Flutuação Populacional de Diaphorina citri Kuwayama (Hemiptera: Psyllidae) em Pomares de Citros na Região Norte do Estado de São Paulo. Neotrop Entomol 30(1):165–170

    Article  Google Scholar 

  • Yamamoto PT, Felippe MR, Sanches AL, Coelho JHC, Garim LF, Ximenes NL (2009) Eficácia de inseticidas para o manejo de Diaphorina citri Kuwayama (Hemiptera: Psyllidae) em citros. BioAssay 4:1–9

    Article  Google Scholar 

  • Yang Y, Huang M, Andrew G, Beattie C, Xia Y, Ouyang G, Xiong J (2006) Distribution, biology, ecology and control of the psyllid Diaphorina citri Kuwayama, a major pest of citrus: a status report for China. Int J Pest Manage 52:343–352

    Article  Google Scholar 

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Acknowledgements

We thank the Foundation of Citrus Growers of São Paulo State (Fundecitrus), Koppert Sistemas Biológicos LTDA and the São Paulo State Research Foundation (FAPESP Project No. 2011/51556-3) for financial support. The first author was a recipient of a scholarship from the Coordination of Improvement of Higher Education Personnel (CAPES PEC/PG—Brazil 2010–2014).

Funding

This study was funded by the Foundation of Citrus Growers of São Paulo State (Fundecitrus), Koppert Sistemas Biológicos LTDA and the São Paulo State Research Foundation (FAPESP Project No. 2011/51556-3).

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Correspondence to Celeste Paola D’Alessandro.

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Communicated by E. Quesada-Moraga.

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Saldarriaga Ausique, J.J., D’Alessandro, C.P., Conceschi, M.R. et al. Efficacy of entomopathogenic fungi against adult Diaphorina citri from laboratory to field applications. J Pest Sci 90, 947–960 (2017). https://doi.org/10.1007/s10340-017-0846-z

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