Sublethal effects of pyrethroid and neonicotinoid insecticides on Iphiseiodes zuluagai Denmark and Muma (Mesostigmata: Phytoseiidae)

Odimar Zanuzo Zanardi1, Gabriela Pavan Bordini1, Aline Aparecida Franco1, Cynthia Renata de Oliveira Jacob1, Pedro Takao Yamamoto1
1Department of Entomology and Acarology, ‘Luiz de Queiroz’ College of Agriculture, University of São Paulo (ESALQ/USP), Piracicaba, Brazil

Tóm tắt

Từ khóa


Tài liệu tham khảo

Abbes K, Biondi A, Kurtulus A, Ricupero M, Russo A, Siscaro G, Chermiti B, Zappalà L (2015) Combined non-target effects of insecticide and high temperature on the parasitoid Bracon nigricans. PLoS ONE 18:1–14

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

Abou-Awad BA, El-Banhawy EM (1985) Comparison between the toxicity of synthetic pyrethroids and other compounds to the predacious mite Amblyseius gossipi (Mesostigmata: Phytoseiidae). Exp Appl Acarol 1:185–191

Agrofit (2015) Sistema de Agrotóxicos Fitossanitários - Ministério da Agricultura, Pecuária e Abastecimento, Brasil. http://extranet.agricultura.gov.br/agrofit_cons/principal_agrofit_cons . Accessed 14 Jan 2015

Alberti G, Coons LB (1999) Acari: mites: integument. In: Harrison FW, Foelix RF (eds) Microscopic anatomy of invertebrates, chelicerate arthropoda 8C. Wiley-Liss, New York, p 681–714

Albuquerque FA, Moraes GJ (2008) Perspectives for mass rearing of Iphiseiodes zuluagai Denmark & Muma (Acari: Phytoseiidae). Neotrop Entomol 37:328–333

Andrade DJ, Pattaro FC, Morais MR, Barbosa CL, Oliveira CAL (2013) Technical and economic aspects of pruning and Brevipalpus phoenicis chemical control in the citrus leprosis management. Rev Bras Frutic 35:409–424

Argolo PS, Banyuls N, Santiago S, Mollá O, Jacas JA, Urbaneja A (2013) Compatibility of Phytoseiulus persimilis and Neoseiulus californicus (Acari: Phytoseiidae) with imidacloprid to manage clementine nursery pests. Crop Prot 43:175–182

Asplen MK, Anfora G, Biondi A, Choi D-S, Chu D, Daane KM, Gibert P, Gutierrez AP, Hoelmer KA, Hutchison WD, Isaacs R, Jiang Z-L, Kárpáti Z, Kimura MT, Pascual M, Philips CR, Plantamp C, Ponti L, Vétek G, Vogt H, Walton VM, Yu Y, Zappalà L, Desneux N (2015) Invasion biology of spotted wing Drosophila (Drosophila suzukii): a global perspective and future priorities. J Pest Sci 88:469–494

Beers E, Schmidt RA (2014) Impacts of orchard pesticides on Galendromus occidentalis: lethal and sublethal effects. Crop Prot 56:16–24

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

Biondi A, Campolo O, Desneux N, Siscaro G, Palmeri V, Zappalà L (2015) Life stage-dependent susceptibility of Aphyti smelinus DeBach (Hymenoptera: Aphelinidae) to two pesticides commonly used in citrus orchards. Chemosphere 128:142–147

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

Bostanian NJ, Hardman JM, Thistlewood HA, Racette G (2010) Effects of six selected orchard insecticides on Neoseiulus fallacis (Acari: Phytoseiidae) in the laboratory. Pest Manag Sci 66:1263–1267

Bostanian NJ, Larocque N (2001) Laboratory tests to determine the intrinsic toxicity of four fungicides and two insecticides to the predacious mite Agistemus fleschneri. Phytoparasitica 29:215–222

Bostanian NJ, Thistlewood HA, Hardman JM, Laurina MC, Racette G (2009) Effect of seven new orchard pesticides on Galendromus occidentalis in laboratory studies. Pest Manag Sci 65:635–639

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

Castagnoli M, Liguori M, Simoni S, Duso C (2005) Toxicity of some insecticides to Tetranychus urticae, Neoseiulus californicus and Tydeus californicus. BioControl 50:611–622

Chi H (1988) Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol 17:26–34

Chi H (2014) TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. http://140.120.197.173/ecology/Download/TWOSEX-MSChart.rar . Accessed 15 Dec 2014

Chi H, Liu H (1985) Two new methods for the study of insect population ecology. Bull Inst Zool 24:225–240

Cônsoli FL, Parra JRP, Hassan SA (1998) Side effects of insecticides used in tomato fields on the egg parasitoid Trichogramma pretiosum Riley (Hym., Trichogrammatidae), a natural enemy of Tuta absoluta (Meyrick) (Lep., Gelechiidae). J Appl Entomol 122:43–47

De Boer JG, Snoeren TAL, Dicke M (2005) Predatory mites learn to discriminate between plant volatiles induced by prey and nonprey herbivores. Anim Behav 69:869–879

Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Ann Rev Entomol 52:81–106

Desneux N, Denoyelle R, Kaiser L (2006a) A multi-step bioassay to assess the effect of the deltamethrin on the parasitic wasp Aphidius ervi. Chemosphere 65:1697–1706

Desneux N, Ramirez-Romero R, Kaiser L (2006b) Multistep bioassay to predict recolonization potential of emerging parasitoids after a pesticide treatment. Environ Toxicol Chem 25:2675–2682

Döker I, Pappas ML, Samaras K, Triantafyllou A, Kazak C, Broufas GD (2014) Compatibility of reduced-risk insecticides with the non-target predatory mite Iphiseius degenerans (Acari: Phytoseiidae). Pest Manag Sci 71:1267–1273

Dukas R (2008) Evolutionary biology of insect learning. Annu Rev Entomol 53:145–160

Duso C, Ahmad S, Tirello P, Pozzebon A, Klaric V, Baldessari M, Malagnini V, Angeli G (2014) The impact of insecticides applied in apple orchards on the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae). Exp Appl Acarol 62:391–414

Duso C, Malagnini V, Pozzebon A, Castagnoli M, Liguori M, Simoni S (2008) Comparative toxicity of botanical and reduced-risk insecticides to Mediterranean populations of Tetranychus urticae and Phytoseiulus persimilis (Acari: Tetranychidae, Phytoseiidae). Biol Control 47:16–21

Efron B, Tibshirani RJA (1993) An introduction to the bootstrap. Springer, London, p 430

Fogel MN, Schneider MI, Desneux N, González B, Ronco AE (2013) Impact of the neonicotinoid acetamiprid on immature stages of the predator Eriopis connexa (Coleoptera: Coccinellidae). Ecotoxicology 22:1063–1071

Fragoso DB, Jusselino-Filho P, Pallini-Filho A, Badji CA (2002) Acão de inseticidas organofosforados utilizados no controle de Leucoptera coffeella (Guérin-Mèneville) (Lepidoptera: Lyonetiidae) sobre o ácaro predador Iphiseiodes zuluagai Denmark & Muma (Acari: Phytoseiidae). Neotrop Entomol 31:463–467

Gerson U, Smiley RL, Ochoa R (2003) Mites (Acari) for pest control. Blackwell Science, Oxford, p 539

Gontijo PC, Moscardini VF, Michaud JP, Carvalho GA (2014) Non-target effects of chlorantraniliprole and thiamethoxam on Chrysoperla carnea when employed as sunflower seed treatments. J Pest Sci 87:711–719

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

Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:3.1–3.20

Hall FR, Thacker JRM (1993) Laboratory studies on effects of three permethrin formulations on mortality, fecundity, feeding, and repellency of the Twospotted spider mite (Acari: Tetranychidae). J Econ Entomol 86:537–543

Hamby KA, Alifano JA, Zalom FG (2013) Total effects of contact and residual exposure of bifenthrin and λ-cyhalothrin on the predatory mite Galendromus occidentalis (Acari: Phytoseiidae). Exp Appl Acarol 61:183–193

Hassan SA, Bigler F, Bogenschutz H, Boller E, Brun J, Calis JNM, Coremans-Pelseneer J, Duso C, Grove A, Heimbach U, Helyer N, Hokkanen H, Lewis GB, Mansour F, Moreth L, Polgar L, Samsøe-Petersen L, Sauphanor B, Staubli A, Sterk G, Vainio A, Van De Veire M, Viggiani G, Vogt H (1994) Results of the sixth joint pesticide testing programme of the IOBC/WPRS – Working Group “Pesticides and Beneficial Organisms”. Entomophaga 39:107–119

He Y, Zhao J, Zheng Y, Desneux N, Wu K (2012) Lethal effect of imidacloprid on the coccinellid predator Serangium japonicum and sublethal effects on predator voracity and on functional response to the whitefly Bemisia tabaci. Ecotoxicology 21:1291–1300

Hinde J, Demétrio CGB (1998) Overdispersion: models and estimation. Comput Stat Data Anal 27:151–170

Huang YB, Chi H (2012) Age-stage, two-sex life tables of Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) with a discussion on the problem of applying female age-specific life tables to insect populations. Insect Sci 19:263–273

James DG (1997) Imidacloprid increases egg production in Amblyseius victoriensis (Acari: Phytoseiidae). Exp Appl Acarol 21:75–82

Kim SS, Seo SG, Park JD, Kim SG, Kim DI (2005) Effects of selected pesticides on the predatory mite Amblyseius cucumeris (Acari: Phytoseiidae). J Entomol Sci 40:107–114

Laurin MC, Bostanian NJ (2007) Laboratory studies to elucidate the residual toxicity of eight insecticides to Anystis baccarum (Acari: Anystidae). J Econ Entomol 100:1210–1214

Liang KY, Zeger SL (1986) Longitudinal data analysis using generalized linear models. Biometrika 73:13–22

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

Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–366

Maoz Y, Gal S, Argov Y, Domeratzky S, Melamed E, Gan-Mor S, Coll M, Palevsky E (2014) Efficacy of indigenous predatory mites (Acari: Phytoseiidae) against the citrus rust mite Phyllocoptruta oleivora (Acari: Eriophyidae): augmentation and conservation biological control in Israel citrus orchards. Exp Appl Acarol 63:295–312

McMurtry JA, Moraes GJ, Sourassou NF (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297–320

Mizell RF, Sconyers MC (1992) Toxicity of imidacloprid to selected arthropod predators in the laboratory. Fla Entomol 75:277–280

Moraes GJ, Flechtman CHW (2008) Aspectos morfológicos específicos dos principais grupos de ácaros de importância agrícola. In: Moraes GJ, Flechtman CHW (eds) Manual de Acarologia: acarologia básica e ácaros de plantas cultivadas no Brasil. Holos, Ribeirão Preto, p 42

Moscardini VF, Gontijo PC, Carvalho GA, Oliveira RL, Maia JB, Silva FF (2013) Toxicity and sublethal effects of seven insecticides to eggs of the flower bug Orius insidiosus (Say) (Hemiptera: Anthocoridae). Chemosphere 92:490–496

Naranjo SE (2001) Conservation and evaluation of natural enemies in IPM systems for Bemisia tabaci. Crop Prot 20:835–852

Nelder JA, Wedderburn RWM (1972) Generalized linear models. J R Stat Soc 135:370–384

Neves MF, Trombin VG, Milan P, Lopes FF, Cressoni F, Kalaki R (2011) O retrato da citricultura brasileira. Markestrat Centro de Pesquisa e Projetos em Marketing e Estratégia, São Paulo, p 71

Obrycki JJ, Kring TJ (1998) Predaceous coccinellidae in biological control. Annu Rev Entomol 43:295–321

Pan H, Liu Y, Liu B, Lu Y, Xu X, Qian X, Wu K, Desneux N (2014) Lethal and sublethal effects of cycloxaprid, a novel cis-nitromethylene neonicotinoid insecticide, on the mirid bug Apolygus lucorum. J Pest Sci 87:731–738

Park CG, Yoo JK, Lee JsO (1996) Toxicity of some pesticides to twospotted spider mite (Acari: Tetranychidae) and its predator Amblyseius womersleyi (Acari: Phytoseiidae). Korean J Appl Entomol 35:232–237

Pasay C, Arlian L, Morgan M, Gunning R, Rossiter L, Holt D, Walton S, Beckham S, McCarthy J (2009) The effect of insecticide synergists on the response of scabies mites to pyrethroid acaricides. Plos Negl Trop Dis 3:e354

Poletti M, Maia AHN, Omoto C (2007) Toxicity of neonicotinoid insecticides to Neoseiulus californicus and Phytoseiulus macropilis (Acari: Phytoseiidae) and their impact on functional response to Tetranychus urticae (Acari: Tetranychidae). Biol Control 40:30–36

Pozzebon A, Duso C, Tirello P, Ortiz PB (2011) Toxicity of thiamethoxam to Tetranychus urticae Koch and Phytoseiulus persimilis Athias-Henriot (AcariTetranychidae, Phytoseiidae) through different routes of exposure. Pest Manag Sci 67:352–359

Provost C, Coderre D, Lucas É, Bostanian NJ (2003) Impact of lambda-cyhalothrin on intraguild predation among three mite predators. Environ Entomol 32:256–263

Provost C, Coderre D, Lucas É, Chouinard G, Bostanian NJ (2005) Impact of intraguild predation and lambda-cyhalothrin on predation efficacy of three acarophagous predators. Pest Manag Sci 61:532–538

Qu Y, Xiao D, Li J, Chen Z, Biondi A, Desneux N, Gao X, Song D (2014) Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology 24:479–487

R Development Core Team (2015) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna

Reis PR, Chiavegato LG, Alves EB (1998) Biologia de Iphiseiodes zuluagai Denmark & Muma (Acari: Phytoseiidae). An Soc Entomol Bras 27:185–191

Reis PR, Franco RA, Pedro-Neto M, Teodoro AV (2006) Selectivity of agrochemicals on predatory mites (Phytoseiidae) found on coffee plants. Coffee Sci 1:64–70

Reis PR, Franco RA, Silva FMA (2011) Selectivity of rynaxypyr for three species of phytoseiid mites relevant to coffee in Brazil. Coffee Sci 6:212–216

Sánchez-Bayo F, Goulson D, Pennacchio F, Nazzi F, Goka K, Desneux N (2016) Are bee diseases linked to pesticides? - A brief review. Environ Int 89-90:7–11

Silva MZ, Oliveira CAL (2006) Seletividade de alguns agrotóxicos em uso na citricultura ao ácaro predador Neoseiulus californicus (McGregor) (Acari: Phytoseiidae). Rev Bras Frutic 28:205–208

Stark JD, Banks JE (2003) Population-level effects of pesticides and other toxicants on arthropods. Ann Rev Entomol 48:505–519

Szczepaniec A, Creary SF, Laskowski KL, Nyrop JP, Raupp MJ (2011) Neonicotinoid insecticide imidacloprid causes outbreaks of spider mites on elm trees in urban landscapes. PLoS ONE 6:e20018

Tan Y, Biondi A, Desneux N, Gao X-W (2012) Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-Dür). Ecotoxicology 21:1989–1997

Teodoro AV, Fadini MAM, Lemos WP, Guedes RNC, Pallini A (2005) Lethal and sub-lethal selectivity of fenbutatin oxide and sulfur to the predator Iphiseiodes zuluagai (Acari: Phytoseiidae) and its prey, Oligonychus ilicis (Acari: Tetranychidae), in Brazilian coffee plantations. Exp Appl Acarol 36:61–70

Teodoro AV, Pallini A, Oliveira C (2009) Sub-lethal effects of fenbutatin oxide on prey location by the predatory mite Iphiseiodes zuluagai (Acari: Phytoseiidae). Exp Appl Acarol 47:293–299

Tirello P, Pozzebon A, Duso C (2013) The effect of insecticides on the non-target predatory mite Kampimodromus aberrans: laboratory studies. Chemosphere 93:1139–1144

Tomizawa M, Casida JE (2003) Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Rev Pharmacol Toxicol 45:339–364

Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247–268

Tuelher ES, Venzon M, Guedes RNC, Pallini A (2014) Toxicity of organic-coffee-approved products to the southern red mite Oligonychus ilicis and to its predator Iphiseiodes zuluagai. Crop Prot 55:28–34

Villanueva RT, Walgenbach JF (2005) Development, oviposition, and mortality of Neoseiulus fallacis (Acari: Phytoseiidae) in response to reduced-risk insecticides. J Econ Entomol 98:2114–2120

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

Yao F-L, Zheng Y, Zhao J-W, Desneux N, He Y-X, Weng Q-Y (2015) Lethal and sublethal effects of thiamethoxam on the whitefly predator Serangium japonicum (Coleoptera: Coccinellidae) through different exposure routes. Chemosphere 128:49–55

Zappalà L, Biondi A, Alma A, Al-Jboory IJ, Arnò J, Bayram A, Chailleux A, El-Arnaouty A, Gerling D, Guenaoui Y, Shaltiel-Harpaz L, Siscaro G, Stavrinides M, Tavella L, Aznar RV, Urbaneja A, Desneux N (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. J Pest Sci 86:635–647

Zeger SL, Liang KY (1986) Longitudinal data analysis for discrete and continuous outcomes. Biometrics 42:121–130

Zeng CX, Wang JJ (2010) Influence of exposure to imidacloprid on survivorship, reproduction and vitellin content of the carmine spider mite, Tetranychus cinnabarinus. J Insect Sci 10:1–9