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Susceptibility of Euseius concordis (Mesostigmata: Phytoseiidae) to pesticides used in citrus production systems

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Abstract

Euseius concordis (Chant) is an important predatory mite found in citrus orchards. The toxicity of 19 pesticides used in citrus orchards on biological and population parameters of this mite was assessed. Our results indicated that formetanate hydrochloride, dimethoate and phosmet were highly harmful (100% mortality) to E. concordis. Carbosulfan, diflubenzuron, fenpropathrin, gamma-cyhalothrin, imidacloprid, lambda-cyhalothrin, lambda-cyhalothrin + thiamethoxam, mineral and vegetable oils, spinosad and thiamethoxam reduced the female’s survival and/or fecundity, and were moderately harmful to E. concordis. Besides the acute toxicity, carbosulfan and formetanate hydrochloride were highly persistent [>30 days after spraying (DAS)]; dimethoate was moderately persistent (16–30 DAS); spinosad, gamma-cyhalothrin, lambda-cyhalothrin and lambda-cyhalothrin + thiamethoxam were slightly persistent (5–15 DAS); and the other pesticides were considered to be short-lived (<5 DAS). All compounds except lambda-cyhalothrin and thiamethoxam increased the pre-oviposition period in the female offspring. Carbosulfan, deltamethrin, diflubenzuron, etofenprox, fenpropathrin, gamma-cyhalothrin, mineral and vegetable oils, pyriproxyfen and tebufenozide reduced offspring fecundity, whereas thiamethoxam increased the fecundity. Mineral and vegetable oils reduced female longevity of the predator mite. Regarding population effects, imidacloprid, lambda-cyhalothrin, lambda-cyhalothrin + thiamethoxam and thiamethoxam led to an increase in net reproductive rate (R o ), intrinsic rate of increase (r), and finite rate of increase (λ) of E. concordis. Diflubenzuron, etofenprox, and mineral and vegetable oils reduced R o , r and λ. All pesticides except beta-cypermethrin, fenpropathrin and imidacloprid reduced the mean generation time (T) of the predator. Therefore, semi-field and field studies are needed to assess the compatibility of these compounds with E. concordis before adoption in IPM programs.

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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://extranet.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed 12 Sept 2016

  • Albuquerque FA, Moraes GJ (2008) Perspectivas para a criação massal de Iphiseiodes zuluagai Denmark & Muma (Acari: Phytoseiidae). Neotrop Entomol 37:328–333

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Bakker FM, Grove A, Blümel S, Calis J, Oomen P (1992) Side-effect test for phytoseiids and their rearing methods. IOBC/WPRS Bull 15:61–81

    Google Scholar 

  • Barati R, Hejazi MJ (2015) Reproductive parameters of Tetranychus urticae (Acari: Tetranychidae) affected by neonicotinoid insecticides. Exp Appl Acarol 66:481–489

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Biondi A, Desneux N, Siscaro G, Zappalà L (2012) Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on predator Orius laevigatus. Chemosphere 87:803–812

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Chi H (2014) TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis, 2012. http://140.120.197.173/Ecology/. Downloaded 7 July 2014

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

    Google Scholar 

  • Costa MA, Moscardini VF, Gontijo PC, Carvalho GA, Oliveira RL, Oliveira HN (2014) Sublethal and transgenerational effects of insecticides in developing Trichogramma galloi (Hymenoptera: Trichogrammatidae). Ecotoxicology 23:1399–1408

    Article  CAS  PubMed  Google Scholar 

  • Croft BA, Blackwood JS, McMurtry JA (2004) Classifying life-style types of phytoseiid mites: diagnostic traits. Exp App Acarol 33:247–260

    Article  Google Scholar 

  • Daam MA, Van Den Brink PJ (2010) Implications of differences between temperate and tropical freshwater ecosystems for the ecological risk assessment of pesticides. Ecotoxicology 19:24–37

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 App Acarol 62:391–414

    Article  CAS  Google Scholar 

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

    Book  Google Scholar 

  • Guedes RNC, Cutler GC (2014) Insecticides-induced hormesis and arthropod pest management. Pest Manag Sci 70:690–697

    Article  CAS  PubMed  Google Scholar 

  • Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62

    Article  CAS  PubMed  Google Scholar 

  • Hassan SA (1992) Guidelines for testing the effects of pesticides on beneficial organisms: description of test methods. IOBC/WPRS Bull 15:1–186

    Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Holt KM, Opit GP, Nechols JR, Margolies DC (2006) Testing for non-target effects of spinosad on twospotted spider mites and their predator Phytoseiulus persimilis under greenhouse conditions. Exp Appl Acarol 38:141–149

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hulbert D, Isaacs R, Vandervoort C, Wise JC (2011) Rainfastness and residual activity of insecticides to control Japanese beetle (Coleoptera: Scarabaeidae) in grapes. J Econ Entomol 104:1656–1664

    Article  CAS  PubMed  Google Scholar 

  • Jacas JA, Garcia-Marí F (2001) Side-effects of pesticides on selected natural enemies occurring in citrus in Spain. IOBC/WPRS Bull 24:103–112

    Google Scholar 

  • Kaplan P, Yorulmaz S, Ay R (2012) Toxicity of insecticides and acaricides to the predatory mite Neoseiulus californicus (McGregor) (Acari: Phytoseiidae). Int J Acarol 38:699–705

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 Israeli citrus orchards. Exp Appl Acarol 63:295–312

    Article  PubMed  Google Scholar 

  • Matioli AL, Oliveira CAL (2007) Biologia de Agistemus brasiliensis Matioli, Ueckermann & Oliveira (Acari: Stigmaeidae) e sua potencialidade de predação sobre Brevipalpus phoenicis (Geijskes) (Acari: Tenuipalpidae). Neotrop Entomol 36:557–582

    Article  Google Scholar 

  • Mattson MP (2009) Hormesis defined. Ageing Res Rev 7:1–7

    Article  Google Scholar 

  • Miles M, Dutton R (2003) Testing the effects of spinosad to predatory mites in laboratory, extended laboratory, semi-weld and weld studies. IOBC/WPRS Bull 26:9–20

    Google Scholar 

  • Moraes GJ, Flechtman CHW (2008) Aspectos biológicos 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 73

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Pascual-Ruiz S, Urbaneja A (2006) Lista de efectos secundarios de plaguicidas sobre fauna útil en cítricos. Rev Int Cítricos 380:186–191

    Google Scholar 

  • Poletti M, Collette LP, Omoto C (2008) Compatibilidade de agrotóxicos com os ácaros predadores Neoseiulus californicus (McGregor) e Phytoseiulus macropilis (Banks) (Acari: Phytoseiidae). BioAssay 3:1–14

    Google Scholar 

  • Pozzebon A, Borgo M, Duso C (2010) The effects of fungicides on non-target mites can be mediated by plant pathogens. Chemosphere 79:8–12

    Article  CAS  PubMed  Google Scholar 

  • Pozzebon A, Tirello P, Moret R, Pederiva M, Duso C (2015) A fundamental step in IPM on grapevine: evaluating the side effects of pesticides on predatory mites. Insects 6:847–857

    Article  PubMed  PubMed Central  Google Scholar 

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

  • Reis PR, Chiavegato LG, Moraes GJ, Alves EB, Sousa EO (1998) Seletividade de agroquímicos ao ácaro predador Iphiseiodes zuluagai Denmark & Muma (Acari: Phytoseiidae). An Soc Entomol Bras 27:265–274

    Article  CAS  Google Scholar 

  • San-Andrés V, Abad-Moyano R, Ansaloni T, Aucejo S, Belliure B, Dembílio O, Jacas JA, Urbaneja A, Mora J, Ripollés JL (2006) Efectos secundarios sobre Euseius stipulatus de tratamientos cebo dirigidos al control de Ceratitis capitata. Phyt España 180:38–45

    Google Scholar 

  • Sato ME (2005) Perspectivas do uso de ácaros predadores no controle biológico de ácaros-praga na citricultura. Laranja 26:291–305

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Silva MZ, Oliveira CAL, Sato ME (2009) Seletividade de produtos fitossanitários sobre o ácaro predador Agistemus brasiliensis Matioli, Ueckermann & Oliveira (Acari: Stigmaeidae). Rev Bras Frutic 31:388–396

    Article  Google Scholar 

  • Silva MZ, Sato ME, Oliveira CAL (2012) Diversidade e dinâmica populacional de ácaros em pomar cítrico. Bragantia 71:210–218

    Article  Google Scholar 

  • Silva RR, Teodoro AV, Silva MJS, Reis PR, Silva SS (2015) Compatibility of pesticides with the generalist predatory mite Amblyseius largoensis (Acari: Phytoseiidae). Rev Colomb Entomol 41:76–80

    Google Scholar 

  • Southwood TRE, Henderson PA (2000) Ecological methods. Blackwell Science, Oxford

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tuelher ES, Verson 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

    Article  Google Scholar 

  • Van Lenteren JCA (2000) greenhouse without pesticides: fact or fantasy. Crop Prot 19:375–384

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Zanardi OZ, Bordini GP, Franco AA, Jacob CRO, Yamamoto PT (2017) Sublethal effects of pyrethroid and neonicotinoid insecticides on Iphiseiodes zuluagai Denmark and Muma (Mesostigmata: Phytoseiidae). Ecotoxicology. doi:10.1007/s10646-017-1844-x

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Zhan Y, Fan S, Zhanga M, Zalom F (2015) Modelling the effect of pyrethroid use intensity on mite population density for walnuts. Pest Manag Sci 71:159–164

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors gratefully acknowledge the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (CAPES), the Fund for Citrus Protection (FUNDECITRUS), and the National Council for Scientific and Technological Development (CNPq—Grant Number 140651/2013-6) for financial support and scholarships. The authors also thank Dr. Mario Eidi Sato of the Economic Entomology Laboratory at the Experimental Center of the Biological Institute, Campinas, São Paulo, Brazil for supplying mite specimens, and Janet W. Reid for revising the English text.

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  1. Department of Entomology and Acarology, ‘Luiz de Queiroz’ College of Agriculture, University of São Paulo (ESALQ/USP), Av. Pádua Dias 11, Agronomia, Piracicaba, São Paulo, 13418-900, Brazil

    Aline Aparecida Franco, Odimar Zanuzo Zanardi, Cynthia Renata de Oliveira Jacob, Monique Bárbara Rosa de Oliveira & Pedro Takao Yamamoto

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  1. Aline Aparecida Franco
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Correspondence to Odimar Zanuzo Zanardi.

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Franco, A.A., Zanardi, O.Z., Jacob, C.R.O. et al. Susceptibility of Euseius concordis (Mesostigmata: Phytoseiidae) to pesticides used in citrus production systems. Exp Appl Acarol 73, 61–77 (2017). https://doi.org/10.1007/s10493-017-0176-0

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