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Acute Toxicity of Fresh and Aged Residues of Pesticides to the Parasitoid Tamarixia radiata and to the HLB-Bacteria Vector Diaphorina citri

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Abstract

One method for controlling the Asian citrus psyllid (ACP) Diaphorina citri Kuwayama, the vector of the putative causal agent of Huanglongbing, uses the parasitoid Tamarixia radiata (Waterston). However, the general intensive use of insecticides has reduced the numbers of this parasitoid. This study evaluated the effect of the residual action of 24 insecticides on T. radiata and also determined the differential toxicity of insecticides to D. citri and T. radiata, using three bioassays. In the first, when adults of the parasitoid were exposed to residues of the 24 insecticides, ten were considered short-life (class 1), six slightly persistent (class 2), five moderately persistent (class 3), and three insecticides were considered persistent (class 4), under the IOBC/WPRS classification system. The second bioassay evaluated the sublethal concentrations of the persistent insecticides (formetanate, dimethoate, spinosad). Increasing the concentrations of the insecticides increased the number that were classified as persistent. In the third bioassay, evaluation of the differential toxicity of eight insecticides to the ACP and the parasitoid showed that chlorpyrifos and bifenthrin were more harmful to T. radiata. Therefore, these two insecticides are not recommended for application at the time of parasitoid release. Cypermethrin, imidacloprid, and dimethoate caused higher mortality of D. citri and are most often recommended in IPM programs. The choice of an insecticide for the control of citrus pests must be made with care, aiming to preserve the natural enemies in the ecosystem, and thereby contribute to the success of biological control.

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References

  • Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    Article  CAS  Google Scholar 

  • AGROFIT (2016) Sistema de Agrotóxicos Fitossanitários – Ministério da Agricultura, Pecuária e Abastecimento, Brasil http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons/ Accessed 21 Mar 2016

  • Alemán JH, Baños H, Ravelo J (2007) Diaphorina citri y la enfermedad huanglongbing: una combinación destructiva para la producción citrícola. Ver Prot Veg 22:154–165

    Google Scholar 

  • Belasque J Jr, Bassanezi RB, Yamamoto PT, Ayres AJ, Tachibana A, Violante AR, Tank A Jr, Giorgis 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 

  • Beloti VH, Alves GR, Araújo DFD, Picoli MM, Moral RA, Demétrio CGB, Yamamoto PT (2015) Lethal and sublethal effects of insecticides used on citrus, on the ectoparasitoid Tamarixia radiata. PLoS One 10(7):e0132128. https://doi.org/10.1371/journal.pone.0132128

    Article  PubMed  PubMed Central  Google Scholar 

  • Biondi A, Mommaerts V, Smagghe G, Viñuela E, Zappalà L, Desneux N (2012) The non-target impact of spinosyns on beneficial arthropods. Pest Manag Sci 68:1523–1536

    Article  CAS  PubMed  Google Scholar 

  • Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS One 8(9):e76548. https://doi.org/10.1371/journal.pone.0076548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brunner JF, Dunley JE, Doerr MD, Beers EH (2001) Effect of pesticides on Colpoclypeus florus (Hymenoptera: Eulophidae) and Trichogramma platneri (Hymenoptera: Trichogrammatidae), parasitoids of leafrollers in Washington. J Econ Entomol 94:1075–1084

    Article  CAS  PubMed  Google Scholar 

  • Carver M (1978) A new subgenus and species of Trichogramma Westwood (Hymenoptera: Chalcidoidea) from Australia. Aust J Entomol 17:109–112

    Article  Google Scholar 

  • 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 97:1404–1413

    Article  Google Scholar 

  • Chen X, Song M, Qi S, Wang C (2013) Safety evaluation of eleven insecticides to Trichogramma nubilale (Hymenoptera: Trichogrammatidae). J Econ Entomol 106:136–141

    Article  CAS  PubMed  Google Scholar 

  • Chu YI, Chien CC (1991) Utilization of natural enemies to control of psyllid vectors transmitting citrus greening. In: Kiritani K, Su HJ, Chu YI (eds) Integrated control of plant virus disease. Food and Fertilizer Technology Center for the Asian and Pacific Region, Taipei, pp 135–145

    Google Scholar 

  • Coletta-Filho HD, Targon MLPN, Takita MA, De Negri JD, Pompeu J Jr, Machado MA (2004) First report of the causal agent of Huanglongbing (“Candidatus Liberibacter asiaticus”) in Brazil. Plant Dis 88:1382–1382

    Article  Google Scholar 

  • Cox C, Surgan M (2006) Unidentified inert ingredients in pesticides: implications for human and environmental health. Environ Health Perspect 114:1803–1806. https://doi.org/10.1289/ehp.9374

    CAS  PubMed  PubMed Central  Google Scholar 

  • Degrande PE, Reis PR, Carvalho GA, Belarmino LC (2002) Metodologia para avaliar o impacto de pesticidas sobre inimigos naturais. In: Parra JRP, Botelho PSM, Corrêa-Ferreira BS, Bento JMS (eds) Controle biológico no Brasil: parasitóides e predadores. Manole, SP, Brazil, pp 71–93

  • Demétrio CGB, Hinde J, Moral RA (2014) Models for overdispersed data in entomology. In: Ferreira CP, Godoy WAC (eds) Ecological modelling applied to entomology, Cham, Switzerland

  • Foerster LA (2002) Seletividade de inseticidas a predadores e parasitoides. In: Parra JRP, Botelho PSM, Corrêa-Ferreira BS, Bento JMS (eds) Controle biológico no Brasil: parasitóides e predadores. Manole, SP, Brazil, pp 95–114

  • Gomez-Torres ML, Nava DE, Gravena S, Costa VA, Parra JRP (2006) Registro de Tamarixia radiata (Waterston) (Hymenoptera: Eulophidae) em Diaphorina citri Kuwayama (Hemiptera: Psyllidae) em São Paulo. Rev Agric (Piracicaba, Brazil) 81:112–117

    Google Scholar 

  • Gottwald TR (2010) Current epidemiological understanding of citrus Huanglongbing. Annu Rev Phytopathol 48:119–139

    Article  CAS  PubMed  Google Scholar 

  • Grafton-Cardwell E, Stelinski LL, Stansly PA (2013) Biology and management of Asian citrus psyllid, vector of the Huanglongbing pathogens. Annu Rev Entomol 58:413–432

    Article  CAS  PubMed  Google Scholar 

  • Guedes RNC, Cutler GC (2013) Insecticide-induced hormesis and arthropod pest management. Pest Manag Sci 70:690–697

    Article  PubMed  Google Scholar 

  • Hall DG, Nguyen R (2010) Toxicity of pesticides to Tamarixia radiata, a parasitoid of the Asian citrus psyllid. BioControl 55:601–611

    Article  CAS  Google Scholar 

  • Hall DG, Richardson ML, Ammar ED, Halbert SE (2013) Asian citrus psyllid, Diaphorina citri, vector of citrus Huanglongbing disease. Entomol Exp Appl 146:207–223

    Article  Google Scholar 

  • Khambay B (2002) Pyrethroid insecticides. Pesticide Outlook 2002:49–54. https://doi.org/10.1039/b202996k Available online http://www.researchinformation.co.uk/pest/2002/B202996K.PDF

    Article  Google Scholar 

  • Lapied B, LeCorronc H, Hue B (1990) Sensitive nicotinic and mixed nicotinic-muscarinic receptors in insect neurosecretory cells. Brain Res 533:132–136

    Article  CAS  PubMed  Google Scholar 

  • Lira ACS, Zanardi OZ, Beloti VH, Bordini GP, Yamamoto PT, Parra JRP, Carvalho GA (2015) Lethal and sublethal impacts of acaricides on Tamarixia radiata (Hemiptera: Eulophidae), an important Ectoparasitoid of Diaphorina citri (Hemiptera: Liviidae). J Econ Entomol 108:2278–2288

    Article  CAS  PubMed  Google Scholar 

  • Maienfisch P, Angst M, Brandl F, Fischer W, Hofer D, Kayser H, Kobe W, Rindlisbacher A, Senn R, Steinemann A, Withmer H (2001) Chemistry and biology of thiamethoxam: a second generation neonicotinoid. Pest Manag Sci 57:906–913

    Article  CAS  PubMed  Google Scholar 

  • McCullagh P, Nelder JA (1989) Generalized linear models. Boca Raton, Florida

  • Miranda MP, Yamamoto PT, Garcia RB, Lopes JPA, Lopes JRS (2016) Thiamethoxam and imidacloprid drench applications on sweet orange nursery trees disrupt feeding and settling behaviour of Diaphorina citri (Hemiptera: Liviidae). Pest Manag Sci 72:1785–1793

    Article  CAS  PubMed  Google Scholar 

  • Momanyi G, Maranga R, Sithanantham S, Agong S, Matoka CM, Hassan SA (2012) Evaluation of persistence and relative toxicity of some pest control products to adults of two native trichogrammatid species in Kenya. BioControl 57:591–601

    Article  CAS  Google Scholar 

  • Onagbola EO, Boina DR, Hermann SL, Stelinski LL (2009) Antennal sensilla of Tamarixia radiata (Hymenoptera: Eulophidae), a parasitoid of Diaphorina citri (Hemiptera: Psyllidae). Ann Entomol Soc Am 102:523–531

    Article  Google Scholar 

  • Paiva PEB, Parra JRP (2012) Natural parasitism of Diaphorina citri Kuwayama (Hemiptera, Psyllidae) nymphs by Tamarixia radiata Waterston (Hymenoptera, Eulophidae) in São Paulo orange groves. Rev Bras Entomol 56:499–503

    Article  Google Scholar 

  • Parra JRP, Lopes JRS, Torres MLG, Nava DE, Paiva PEB (2010) Bioecologia do vetor Diaphorina citri e transmissão de bactérias associadas ao huanglongbing. Citrus Res Technol 31:37–51

    Article  Google Scholar 

  • Parra JRP, Alves GR, Diniz AJF, Vieira JM (2016) Tamarixia radiata (Hymenoptera: Eulophidae) × Diaphorina citri (Hemiptera: Liviidae): mass rearing and potential use of the parasitoid in Brazil. J Integ Pest Manag 7:1–11

    Article  Google Scholar 

  • Pluke RWH, Qureshi JA, Stansly PA (2008) Citrus flushing patterns, Diaphorina citri (Hemiptera: Psyllidae) populations and parasitism by Tamarixia radiata (Hymenoptera: Eulophidae) in Puerto Rico. Fla Entomol 91:36–42

    Article  Google Scholar 

  • Qureshi JA, Rogers ME, Hall DG, Stansly PA (2009) Incidence of invasive Diaphorina citri (Hemiptera: Psyllidae) and its introduced parasitoid Tamarixia radiata (Hymenoptera: Eulophidae) in Florida citrus. J Econ Entomol 102:247–256

    Article  PubMed  Google Scholar 

  • R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. URL:https://www.R-project.org/

  • Ripper WE, Greenslade RM, Hartley GS (1951) Selective insecticides and biological control. J Econ Entomol 44:448–458

    Article  CAS  Google Scholar 

  • Rugno GR, Zanardi OZ, Cuervo JB, Morais MR, Yamamoto PT (2016) Impact of insect growth regulators on the predator Ceraeochrysa cincta (Schneider) (Neuroptera: Chrysopidae). Ecotoxicology. https://doi.org/10.1007/s10646-016-1651-9

  • Sieber KP, Rembold H (1983) The effects of Azadirachtin on the endocrine control of molting in Locusta migratoria. J Insect Physiol 29:523–527

    Article  CAS  Google Scholar 

  • Skelley LH, Hoy MA (2004) A synchronous rearing method for the Asian citrus psyllid and its parasitoids in quarantine. BioControl 29:14–23

    Google Scholar 

  • Soderlund DM, Bloomquist JR (1989) Neurotoxic actions of pyrethroid insecticides. Annu Rev Entomol 34:77–96. https://doi.org/10.1146/annurev.en.34.010189.000453

    Article  CAS  PubMed  Google Scholar 

  • Teixeira DC, Danet JL, Eveillard S, Martins EC, Cintra de Jesus W, Yamamoto PT, Lopes SA, Bassanezi RB, Ayres AJ, Saillard C, Bové JM (2005) Citrus Huanglongbing in São Paulo, Brazil: PCR detection of the ‘Candidatus’ Liberibacter species associated with the disease. Mol Cell Probes 19:173–179

    Article  CAS  Google Scholar 

  • Tiwari S, Stelinski LL (2013) Effects of cyantraniliprole, a novel anthranlic diamide insecticide, against Asian citrus psyllid under laboratory and field conditions. Pest Manag Sci 69:1066–1072

    Article  CAS  PubMed  Google Scholar 

  • Tiwari S, Sayed RS, Sayed 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 

  • Van de Veire M, Sterk G, Van der Staaij M, Ramakers PMJ, Tirry L (2002) Sequential testing scheme for the assessment of the side-effects of plant protection products on the predatory bug Orius laevigatus. BioControl 47:101–113

    Article  Google Scholar 

  • Waterston J (1922) On the chalcidoid parasites of psyllids (Hemíptera: Homoptera). Bull Entomol Res 13:41–58

    Article  Google Scholar 

  • Williams T, Valle J, Viñuela E (2003) Is the naturally derived insecticide Spinosad® compatible with insect natural enemies? Biocontrol Sci Tech 13:459–475. https://doi.org/10.1080/0958315031000140956

    Article  Google Scholar 

  • Williams T, Arredondo-Bernal HC, Del Bosque LAR (2013) Biological pest control in Mexico. Annu Rev Entomol 58:119–140

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto PT, Bassanezi RB (2003) Seletividade de produtos fitossanitários aos inimigos naturais de pragas dos citros. Laranja 24:353–382

    Google Scholar 

  • Yamamoto PT, Felippe MR, Sanches AL, Coelho JHC, Garbim 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 

  • Yamamoto PT, Alves GR, Beloti VH (2014) Manejo e controle do huanglongbing (HLB) dos cítricos. Investig Agrar 16:69–82

    Google Scholar 

  • Zhao X, Wu C, Wang Y, Cang T, Chen L, Yu R, Wang Q (2012) Assessment of toxicity risk of insecticides used in rice ecosystem on Trichogramma japonicum, an egg parasitoid of rice lepidopterans. J Econ Entomol 105:92–101

    Article  CAS  PubMed  Google Scholar 

  • Zuparko RL, Queiroz DL, La-Salle J (2011) Two new species of Tamarixia (Hymenoptera: Eulophidae) from Chile and Australia, established as biological control agents of invasive psyllids (Hemiptera: Calophyidae, Triozidae) in California. Zootaxa 2921:13–27

    Google Scholar 

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Acknowledgments

The authors thank Dr. Jaci Mendes Vieira and Dr. Alexandre Diniz from the Insect Biology Laboratory of ESALQ/USP for providing the parasitoids at the beginning of the experiments and Janet W. Reid for revising the English text.

Funding

This study was funded by the CAPES Foundation (Brazilian Ministry of Education), the São Paulo State Foundation for Research Aid (FAPESP), and the National Council for Scientific and Technological Development (CNPq grant 305828/2014-2).

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Authors and Affiliations

  1. Dept of Entomology and Acarology, “Luiz de Queiroz” College of Agriculture/Univ of São Paulo (ESALQ/USP), 13418-900, Piracicaba, São Paulo, Brasil

    V H Beloti, G R Alves & P T Yamamoto

  2. Dept of Agricultural Statistics and Experimentation, “Luiz de Queiroz” College of Agriculture/Univ of São Paulo (ESALQ/USP), Piracicaba, São Paulo, Brasil

    R A Moral & C G B Demétrio

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  1. V H Beloti
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  2. G R Alves
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  3. R A Moral
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  4. C G B Demétrio
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  5. P T Yamamoto
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Correspondence to V H Beloti.

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Edited by Eugenio E de Oliveira – UFV

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Beloti, V.H., Alves, G.R., Moral, R.A. et al. Acute Toxicity of Fresh and Aged Residues of Pesticides to the Parasitoid Tamarixia radiata and to the HLB-Bacteria Vector Diaphorina citri . Neotrop Entomol 47, 403–411 (2018). https://doi.org/10.1007/s13744-017-0575-2

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