Susceptibility of Diaphorina citri (Hemiptera: Liviidae) and Its Parasitoid Tamarixia radiata (Hymenoptera: Eulophidae) to Entomopathogenic Fungi under Laboratory Conditions

  • K. H. Ibarra-Cortés
  • A W Guzmán-Franco
  • H. González-Hernández
  • L. D. Ortega-Arenas
  • J. A. Villanueva-Jiménez
  • A. Robles-Bermúdez
Biological Control

Abstract

Diaphorina citri (Kuwayama) is a global pest of citrus that transmits the bacteria associated with the disease, Huanglongbing. Entomopathogenic fungi and the parasitoid Tamarixia radiata (Waterston) are important biological control agents of this pest and likely to interact in D. citri populations. As a basis for interaction studies, we determined the susceptibility of nymphs and adults of D. citri and adults of the parasitoid T. radiata to six fungal isolates from the species Beauveria bassiana s.l. (Bals.-Criv.) Vuill. (isolates B1 and B3), Metarhizium anisopliae s.s. (Metsch.) (Ma129 and Ma65) and Isaria fumosorosea Wize (I2 and Pae). We conducted experiments evaluating infection levels in all three insect groups following inoculation with a series of conidial concentrations (1 × 104–1 × 108 conidia mL−1). Results showed that D. citri nymphs and T. radiata were more susceptible to fungal isolates than D. citri adults. Overall, B. bassiana and M. anisopliae isolates caused the greatest infection compared with I. fumosorosea isolates in all three groups of insects. Isolates B1 (B. bassiana) and Ma129 (M. anisopliae) infected a greater proportion of adults and nymphs of D. citri, respectively. Both isolates of B. bassiana caused greater infection in T. radiata compared with isolates of the other fungal species. We propose that isolates B1 and Ma129 are the strongest candidates for control of D. citri. Our results represent the first report of entomopathogenic fungi infecting T. radiata, and the basis for future studies to design a biological control programme that uses both agents more efficiently against D. citri populations.

Keywords

Biological control, Asian citrus psyllid, bioassay, citrus, entomopathogens 

References

  1. Avery PB, Hunter WB, Hall DG, Jackson MA, Powell CA, Rogers ME (2009) Diaphorina citri (Hemiptera: Psyllidae) infection and dissemination of the entomopathogenic fungus Isaria fumosorosea (Hypocreales: Cordycipitaceae) under laboratory conditions. Fla Entomol 92:608–618CrossRefGoogle Scholar
  2. Avery PB, Wekesa VW, Hunter WB, Hall DG, McKensie CL, Osborne LS, Powell CA, Rogers ME (2011) Effects of the fungus Isaria fumosorosea (Hypocreales: Cordycipitaceae) on reduced feeding and mortality of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Biocon Sci Technol 21:1065–1078CrossRefGoogle Scholar
  3. Bové JM (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. J Plant Pathol 88:7–37Google Scholar
  4. Butt TM, Jackson CW, Magan N (2001) Introduction—fungal biological control agents: progress, problems, potential. In: Butt TM, Jackson CW, Magan N (eds) Fungi as biocontrol agents: progress, Problems and Potential. CAB International, Wallingford, pp 1–8CrossRefGoogle Scholar
  5. Cabanillas HE, Jones WA (2009) Pathogenicity of Isaria sp. (Hypocreales: Clavicipitaceae) against the sweet potato whitefly B biotype, Bemisia tabaci (Hemiptera: Aleyrodidae). Crop Prot 28:333–337CrossRefGoogle Scholar
  6. Chen X, Stansly PA (2014) Biology of Tamarixia radiata (hymenoptera: Eulophidae), parasitoid of the citrus greening disease vector Diaphorina citri (Hemiptera: Psylloidea): a mini review. Fla Entomol 97:1404–1413CrossRefGoogle Scholar
  7. Cortez-Madrigal H, Sánchez-Saavedra JM, Díaz-Godínez G, Mora-Aguilera G (2014) Enzymatic activity and pathogenicity of entomopathogenic fungi from Central and Southeastern Mexico to Diaphorina citri (Hemiptera: Psyllidae). Southwest Entomol 39:491–502CrossRefGoogle Scholar
  8. Fernández M, Miranda I (2005) Comportamiento de Diaphorina citri Kuwayama (Hemiptera:Psyllidae) Parte I: Características morfológicas, incidencia y enemigos naturales asociados. Rev Prot Veg 2:27–31Google Scholar
  9. Ferreira Pinto AP, Batista Filho A, Marcondes de Almeida JE, Marchizeli Wenzel I (2012) Beauveria bassiana pathogenicity to Diaphorina citri and compatibility of the fungus with phytosanitary products. Pesq Agrop Brasileira 47:1673–1680CrossRefGoogle Scholar
  10. Gandarilla-Pacheco FL, Galán-Wong LJ, López-Arroyo JI, Rodríguez-Guerra R, Quintero-Zapata I (2013a) Optimization of pathogenicity tests for selection of native isolates of entomopathogenic fungi isolated from citrus-growing areas of México on adults of Diaphorina ciri Kuwayama (Hemiptera: Liviidae). Fla Entomol 96:187–195CrossRefGoogle Scholar
  11. Gandarilla-Pacheco FL, López-Arroyo JI, Galán-Wong LJ, Quintero-Zapata I (2013b) Patogenicity of native entomopathogenic fungi from the Mexican citrus-growing area against Diaphorina citri Kuwayama (Hemiptera: Liviidae). Southwest Entomol 38:325–338CrossRefGoogle Scholar
  12. Goettel MS (1994) Host range and specificity in relation to safety of exotic fungi. In “VI th International Colloquium on Invertebrate Pathology and Microbial Control, XXVII th Annual Meeting of the Society for Invertebrate Pathology, Montpellier, France 28 August–2 September, 1994,” pp. 325–329Google Scholar
  13. Hajek AE, Goettel MS (2007) Guidelines for evaluating effects of entomopathogens on non-target organisms. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology. Springer, Dordrecht, pp 815–833Google Scholar
  14. Hall DG, Hentz MG, Meyer JM, Kriss AB, Gottwald TR, Boucias DG (2012) Observations on the entomopathogenic fungus Hirsutella citriformis attacking adult Diaphorina citri (Hemiptera: Psyllidae) in managed citrus grove. BioControl 57:663–675CrossRefGoogle Scholar
  15. Ibarra-Cortés KH, Guzmán-Franco AW, González-Hernández H, Suarez-Espinosa J, Baverstock J (2013) Selection of a fungal isolate for the control of the pink hibiscus mealybug Maconellicoccus hirsutus. Pest Manag Sci 69:874–882CrossRefPubMedGoogle Scholar
  16. Inglis GD, Enkerli J, Goettel MS (2012) Laboratory techniques used for entomopathogenic fungi: Hypocreales. In: Lacey LA (ed) Manual of techniques in invertebrate pathology, Second edn. Academic Press Inc., San Diego, pp 189–253CrossRefGoogle Scholar
  17. Khan S, Guo L, Maimaiti Y, Mijit M, Qiu D (2012) Entomopathogenic fungi as microbial biocontrol agent. Mol Plant Breed 3:63–79Google Scholar
  18. 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 132:1–41CrossRefPubMedGoogle Scholar
  19. 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 32:39–44CrossRefGoogle Scholar
  20. Moore DPC (1993) The potential of mycoinsecticides. Biocontrol News Inf 14:31–40Google Scholar
  21. Orduño-Cruz N, Guzmán-Franco AW, Rodríguez-Leyva E, Alatorre-Rosas R, González-Hernández H, Mora-Aguilera G (2015a) In vivo selection of entomopathogenic fungal isolates for control of Diaphorina citri (Hemiptera: Liviidae). Biol Control 90:1–5CrossRefGoogle Scholar
  22. Orduño-Cruz N, Guzmán-Franco AW, Rodríguez-Leyva E, Alatorre-Rosas R, González-Hernández H, Mora-Aguilera G, Rodriguez-Maciel JC (2015b) In vitro selection of a fungal pathogen for use against Diaphorina citri. Biol Control 90:6–15CrossRefGoogle Scholar
  23. Orduño-Cruz N, Guzmán-Franco AW, Rodríguez-Leyva E (2016) Diaphorina citri populations carrying the bacterial plant pathogen, Candidatus Liberibacter asiaticus, are more susceptible to infection by entomopathogenic fungi than bacteria-free populations. Agric For Entomol 18:95–98CrossRefGoogle Scholar
  24. Payne RW, Murray DM, Harding SA, Baird DB, Soutar DM (2005) GenStat for windows (8th edition) introduction. VSN international, Hemel HempsteadGoogle Scholar
  25. Petersen-Silva R, Inácio L, Henriques J, Naves P, Sousa E, Pugade-Villara J (2015) Susceptibility of larvae and adults of Monochamus galloprovincialis to entomopathogenic fungi under controlled conditions. Int J Pest Manag 61:106–112CrossRefGoogle Scholar
  26. Posada FJ, Vega FE (2005) A new method to evaluate the biocontrol potential of single spore isolates of fungal entomopathogens. J Insect Sci 5:37, 10 ppCrossRefPubMedPubMedCentralGoogle Scholar
  27. Shah PA, Pell JK (2003) Entomopathogenic fungi as biological control agents. Appl Microbiol Biotechnol 61:413–423CrossRefPubMedGoogle Scholar
  28. Stauderman K, Avery P, Aristizábal L, Arthurs S (2012) Evaluation of I. fumosorosea (Hypocreales: Cordycipitaceae) for control of the Asian citrus psyllid, Diaphorina citri (Hemiptera: Psyllidae). Biocontrol Sci Tech 22:747–761CrossRefGoogle Scholar
  29. Trujillo-Arriaga J (2010) Situación actual, regulación y manejo del HLB en México. Memorias del Segundo Taller Internacional del HLB, MéridaGoogle Scholar
  30. Vega FE, Meyling NV, Luangsa-ard JJ, Blackell M (2012) Fungal Entomopathogens. In: Vega FE, Kaya HK (eds) Inset pathology, Second edn. Academic Press Inc., San Diego, pp 171–220CrossRefGoogle Scholar

Copyright information

© Sociedade Entomológica do Brasil 2017

Authors and Affiliations

  • K. H. Ibarra-Cortés
    • 1
  • A W Guzmán-Franco
    • 1
  • H. González-Hernández
    • 1
  • L. D. Ortega-Arenas
    • 1
  • J. A. Villanueva-Jiménez
    • 2
  • A. Robles-Bermúdez
    • 3
  1. 1.Posgrado en Fitosanidad - Entomología y Acarología, Colegio de PostgraduadosTexcocoMexico
  2. 2.Colegio de Postgraduados, Campus VeracruzVeracruzMexico
  3. 3.Facultad de AgronomíaUniv Autónoma de NayaritXaliscoMexico

Personalised recommendations