Abstract
Kampimodromus aberrans is an effective predatory mite in fruit orchards. The side-effects of insecticides on this species have been little studied. Field and laboratory experiments were conducted to evaluate the effects of insecticides on K. aberrans. Field experiments showed the detrimental effects of etofenprox, tau-fluvalinate and spinosad on predatory mites. Spider mite (Panonychus ulmi) populations reached higher densities on plots treated with etofenprox and tau-fluvalinate than in the other treatments. Single or multiple applications of neonicotinoids caused no detrimental effects on predatory mites. In the laboratory, spinosad and tau-fluvalinate caused 100 % mortality. Etofenprox caused a significant mortality and reduced fecundity. The remaining insecticides did not affect female survival except for imidacloprid. Thiamethoxam, clothianidin, thiacloprid, chlorpyrifos, lufenuron and methoxyfenozide were associated with a significant reduction in fecundity. No effect on fecundity was found for indoxacarb or acetamiprid. Escape rate of K. aberrans in laboratory was relatively high for etofenprox and spinosad, and to a lesser extent thiacloprid. The use of etofenprox, tau-fluvalinate and spinosad was detrimental for K. aberrans and the first two insecticides induced spider mite population increases. The remaining insecticides caused no negative effects on predatory mites in field trials. Some of them (reduced fecundity and repellence) should be considered with caution in integrated pest management programs.
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References
Abbott WS (1925) A method for computing the effectiveness of insecticides. J Econ Entomol 18:265–267
Ahmad S, Pozzebon A, Duso C (2013) Augmentative releases of the predatory mite Kampimodromus aberrans in organic and conventional apple orchards. Crop Prot 52:47–56
Ahn KS, Lee SY, Lee KY, Lee YS, Kim GH (2004) Selective toxicity of pesticides to the predatory mite, Phytoseiulus persimilis and control effects of the two-spotted spider mite, Tetranychus urticae by predatory mite and pesticide mixture on rose. Korean J Appl Entomol 43:71–79
Ako M, Poehling HM, Borgemeister C, Nauen R (2006) Effect of imidacloprid on the reproduction of acaricide-resistant and susceptible strains of Tetranychus urticae Koch (Acari: Tetranychidae). Pest Manag Sci 62:419–424
Amin MM, Mizell RF, Flowers RW (2009) Response of the predatory mite Phytoseiulus macropilis (Acari: Phytoseiidae) to pesticides and kairomones of three spider mite species (Acari: Tetranychidae), and non-prey food. Flo Entomol 92:554–562
Anber HAI, Overmeer WPJ (1998) Resistance to organophosphates and carbamates in the predacious mite Amblyseius potentillae (Garman) due to insensitive acetylcholinesterase. Pest Biochem Physiol 3:91–98
Angeli G, Anfora G, Baldessari M, Germinara SG, Rama F, De Cristofaro A, Ioriatti C (2007) Mating disruption of codling moth Cydia pomonella with high densities of Ecodian sex pheromone dispensers. J Appl Entomol 131:311–318
Auger P, Bonafos R, Kreiter S (2004) Mancozeb resistance patterns among Kampimodromus aberrans and Typhlodromus pyri strains from French vineyards. Can Entomol 13:663–673
Baillod M, Guignard E (1984) Résistance de Typhlodromus pyri Scheuten à l’azinphos et lutte biologique contre les acariens phytophages en arboriculture. Rev Suisse Vitic Arboric Hortic 16:155–160
Beers EH, Brunner JF, Dunley JE, Doerr M, Granger K (2005) Role of neonicotinyl insecticides in Washington apple integrated pest management. Part II. Nontarget effects on integrated mite control. J Insect Sci 5:1–10
Bellows TS, Morse JG, Gaston LK (1992) Residual toxicity of pesticides used for control of lepidopteran insects in citrus to the predaceous mite Euseius stipulatus Athias-Henriot (Acarina, Phytoseiidae). J Appl Entomol 113:493–501
Bernard MB, Cole P, Kobelt A, Horne PA, Altmann J, Wratten SD, Yen AL (2010) Reducing the impact of pesticides on biological control in Australian vineyards: pesticide mortality and fecundity effects on an indicator species, the predatory mite Euseius victoriensis (Acari: Phytoseiidae). J Econ Entomol 103:2061–2071
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
Blommers LHM (1994) Integrated pest management in European apple orchards. Ann Rev Entomol 39:213–241
Blümel S, Hausdorf H (2002) Results of 8th and 9th IOBC joint pesticides testing programme: persistence test with Phytoseiulus persimilis Athias-Heriot (Acari: Phytoseiidae). IOBC/wprs Bull 25:43–51
Bostanian NJ, Balenger A, Revard I (1985) Residues of four synthetic pyrethroids and azinphos-methyl on apple foliage and their toxicity to Amblyseius fallacis (Acari: Phytoseiidae). Can Entomol 117:143–152
Bostanian NJ, Thistlewood HA, 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
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
Bowie MH, Worner SP, Krips OE, Penman DR (2001) Sublethal effects of esfenvalerate residues on pyrethroid resistant Typhlodromus pyri (Acari: Phytoseiidae) and its prey Panonychus ulmi and Tetranychus urticae (Acari: Tetranychidae). Exp Appl Acarol 25:311–319
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
Corino L, Balloid M, Duvernay C (1986) Resistenza di Kampimodromus aberrans (Oudemans) al parathion e lotta biologica contro gli acari fitofagi in viticoltura. Vignevini 4:39–42
Duso C (1989) Role of Amblyseius aberrans (Oud.), Typhlodromus pyri Scheuten and Amblyseius andersoni (Chant) in vineyards. 1. The effects of single or mixed phytoseiid releases on spider mite densities. J Appl Entomol 107:474–492
Duso C (1992) Biological control of tetranychid mites in peach orchards of Northern Italy: role of Amblyseius andersoni (Chant) and Amblyseius finlandicus (Oud.) (Acari: Phytoseiidae). Acta Phytopatol Entomol Hun 27:211–217
Duso C, Vettorazzo E (1999) Mite population dynamics on different grape varieties with or without phytoseiids released (Acari: Phytoseiidae). Exp Appl Acarol 23:741–763
Duso C, Camporese P, Van der Geest LPS (1992) Toxicity of a number of pesticides to strains of Typhlodromus pyri and Amblyseius andersoni (Acari: Phytoseiidae). Entomophaga 37:363–372
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 Cont 47:16–21
Duso C, Fanti M, Pozzebon A, Angeli G (2009) Is the predatory mite Kampimodromus aberrans a candidate for the control of phytophagous mites in European apple orchards? Biocontrol 54:369–382
Duso C, Pozzebon A, Kreiter S, Tixier MS, Candolfi MP (2012) Management of phytophagous mites in European vineyards. In: Bostanian NJ, Vincent C, Isaacs R (eds) Arthropod management in vineyards: pests, approaches, and future directions. Springer, New York, pp 191–217
Espinha IG, Costa-Comelles J, Torres LM, Ferragut F (1995) Contribuicao para o conhecimento dos acaros fitoseideos associados a macieira no norte interior de Portugal. Bol Sanid Veg Plagas 21:223–230
Fischer-Colbrie P, El Borolossy M (1990) Unthersuchungen zum Einfluss des Klimas, der Pflanzenart und der Wirtstiere auf das Vorkommen verschiedener Raubmilbenarten im osterreichischen Obst- und Weinbau. Pflanzenschutzber 51:101–125
Fitzgerald JD, Solomon MG (2000) Differences in biological characteristics in organophosphorus-resistant strains of the phytoseiid mite Typhlodromus pyri. Exp Appl Acarol 24:735–746
Fitzgerald JD, Solomon MG (2002) Distribution of predatory phytoseiid mites in commercial cider apple orchards and unsprayed apple trees in the UK: implications for biocontrol of phytophagous mites. Int J Acarol 28:181–186
Garcia-Marì F, Costa-Comelles J, Ferragut F, Laborda R (1989) Lutte intégrée contre les acariens dans les vergers de pommiers de Lleida (Espagne). In: Proceedings of Colloque sur les acariens des cultures. Montpellier, 24–26 Octobre 1989, pp 501–518
Girolami V, (1987) Mites of vineyards and control strategies. In: Proceedings Meeting EC Experts’ Group “Integrated Pest Control in Viticulture”, Portoferraio 26–28 September 1985, AA Balkema, Rotterdam, pp 185–197
Girolami V, Greguoldo M, Saltarin A (1992) Controllo biologico degli acari sul melo con popolazioni di Amblyseius andersoni (Chant) tolleranti il mancozeb. Inf Agr 48:55–59
Girolami V, Mori N, Marchesini E, Duso C (2001) Organophosphate resistance in grape leafhoppers and IPM strategies. Redia 84:1–17
Grafton-Cardwell EE, Lee JE, Robillard SM, Gorden JM (2008) Role of imidacloprid in integrated pest management of California citrus. J Econ Entomol 10:451–460
Grout TG, Richards GI, Stephen PR (1997) Further non-target effects of citrus pesticides on Euseius addoensis and Euseius citri (Acari: Phytoseiidae). Exp Appl Acarol 21:171–177
Holland JM, Chapman RB, Penman DR (1994) Effects of fluvalinate on two-spotted spider mite dispersal, fecundity and feeding. Entomol Exp Appl 71:145–153
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
Ivancich Gambaro P (1973) I trattamenti fungicidi e gli acari della vite. Inf Agr 28:8141–8143
Ivancich Gambaro P (1975) Selezione di popolazioni di Acari predatori resistenti ad alcuni insetticidi fosforati-organici. Inf Fitopatol 7:21–25
James DG (1997) Imidacloprid increases egg production in Amblyseius victoriensis (Acari: Phytoseiidae). Exp Appl Acarol 21:75–82
James DG (2003) Toxicity of imidacloprid to Galendromus occidentalis, Neoseiulus fallacis and Amblyseius andersoni (Acari: Phytoseiidae) from hops in Washington State, USA. Exp Appl Acarol 31:275–281
James DG, Vogele B (2001) The effect of imidacloprid on survival of some beneficial arthropods. Plant Prot Quart 16:58–62
Jung C, Han S, Lee JH (2004) Release strategies of Amblyseius womersleyi and population dynamics of Amblyseius womersleyi and Tetranychus urticae: II. Test of two release rates on apple. Appl Entomol Zool 39:477–484
Kasap I (2005) Life-history traits of predaceous mites Kampimodromus aberrans (Oudemans) (Acarina: Phytoseiidae) on four different types of food. Biol Cont 35:40–45
Kim SS, Seo SG, Park JD, Kim SG, Kim D (2005) Effects of selected pesticides on the predatory mite, Amblyseius cucumeris (Acari: Phytoseiidae). J Entomol Sci 40:107–114
Kongchuensin M, Takafuji A (2006) Effects of some pesticides on the predatory mite, Neoseiulus longispinosus (Evans) (Gamasina: Phytoseiidae). J Acarol Soc Jpn 15:17–27
Kreiter S, Tixier MS, Auger P, Muckensturm N, Sentenac G, Doublet B, Weber M (2000) Phytoseiid mites of vineyards in France (Acari: Phytoseiidae). Acarologia 41:77–96
Lee SG, Hilton SA, Broadbent AB, Kim JH (2002) Insecticide resistance in phytoseiid predatory mites, Phytoseiulus persimilis and Amblyseius cucumeris (Acarina: Phytoseiidae). J Asia Pacif Entomol 5:123–129
Lefebvre M, Bostanian NJ, Thistlewood HMA, Mauffette Y, Racette G (2011) A laboratory assessment of the toxic attributes of six ‘reduced risk insecticides’ on Galendromus occidentalis (Acari: Phytoseiidae). Chemosphere 84:25–30
Lefebvre M, Bostanian NJ, Mauffette Y, Racette G, Thistlewood HA, Hardman JM (2012) Laboratory-based toxicological assessments of new insecticides on mortality and fecundity of Neoseiulus fallacis (Acari: Phytoseiidae). J Econ Entomol 105:866–871
Lester PJ, Thistlewood HMA, Harmsen R (2000) Some effects of pre-release host-plant on the biological control of Panonychus ulmi by the predatory mite Amblyseius fallacis. Exp Appl Acarol 24:19–33
Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS system for mixed models. SAS Institute, Cary, NC
Marshall DB, Thistlewood HMA, Lester PJ (2001) Release, establishment, and movement of the predator Typhlodromus pyri (Acari: Phytoseiidae) on apple. Can Entomol 133:279–292
Miles M, Dutton R (2003) Testing the effects of spinosad to predatory mites in laboratory, extended laboratory, semi-field and field studies. IOBC/wprs Bull 26:9–20
Mizell RF, Sconyers MC (1992) Toxicity of imidacloprid to selected arthropod predators in the laboratory. Fla Entomol 75:277–280
Mori N, Posenato G, Sancassani G, Tosi L, Girolami V (1999) Insetticidi per il controllo delle cicaline nei vigneti. Inf Agr 55:93–97
Nicòtina M, Cioffi E (1998) Distribution of phytoseiid mites (Acarina, Phytoseiidae) in hazel-nut-growing areas in Campania. Redia 81:115–124
Petit FL, Karan DJ (1991) Influence of pesticide treatments on consumption of Tetranychus urticae (Acarina, Tetranychidae) eggs by Phytoseiulus persimilis (Acarina, Phytoseiidae). Entomophaga 36:539–545
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 Cont 40:30–36
Posenato G (1994) Popolazioni di Amblyseius aberrans (Oud.) resistenti ad esteri fosforici e ditiocarbammati. Inf Agr 50:41–43
Pozzebon A, Duso C, Pavanetto E (2002) Side effects of some fungicides on phytoseiid mites (Acari, Phytoseiidae) in north-Italian vineyards. Anz Schadlingskd J Pest Sci 75:132–136
Pozzebon A, Duso C, Tirello P, Ortiz PB (2011) Toxicity of thiamethoxam to Tetranychus urticae Koch and Phytoseiulus persimilis Athias-Henriot (Acari Tetranychidae, Phytoseiidae) through different routes of exposure. Pest Manag Sci 67:352–359
Prokopy RJ, Christie M (1992) Studies on releases of mass-reared organophosphate resistant Amblyseius fallacis (Garm) predatory mites in Massachusetts commercial apple orchards. J Appl Entomol 114:131–137
Rahman T, Spafford H, Broughton S (2011) Compatibility of spinosad with predaceous mites (Acari) used to control Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae). Pest Manag Sci 67:993–1003
Rodrigues R, Gonçalves R, Silva C, Torres L, Vogt H (2004) Toxicity of five insecticides on predatory mites (Acari: Phytoseiidae) in vineyards in two Portuguese regions. IOBC/wprs Bull 27:37–44
SAS Institute (1999) SAS/STAT 9.2 User’s Guide, second edition. SAS Institute, Cary, NC
Solomon MG, Easterbrook MA, Fitzgerald JD (1993) Mite management programs based on organophosphate-resistant Typhlodromus pyri in UK apple orchards. Crop Prot 12:249–254
Stavrinides MC, Mills NJ (2009) Demographic effects of pesticides on biological control of Pacific spider mite (Tetranychus pacificus) by the western predatory mite (Galendromus occidentalis). Biol Cont 48:267–273
Sterk G, Hassan SA, Baillod M, Bakker F, Bigler F, Blumel S, Bogenschutz H, Boller E, Bromand B, Brun J, Calis JNM, Coremans-Pelseneer J, Duso C, Garrido A, Grove A, Heimbach U, Hokkanen H, Jacas J, Lewis G, Moreth L, Polgar L, Roversti L, Samsoe Petersen L, Sauphanor B, Schaub L, Staubli A (1999) Results of the seventh joint pesticide testing programme carried out by the IOBC/WPRS-Working Group ‘Pesticides and Beneficial Organisms’. Biocontrol 44:99–117
Sterk G, Jans K, Put K, Wulandari OV, Uyttebroek M (2003) Toxicity of chemical and biological plant protection products to beneficial arthropods. In: Colloque international tomate sous abri, protection integrée agriculture biologique, Avignon, France, 17–19 September 2003, pp 113–118
Tirello P, Pozzebon A, Duso C (2012) Resistance to chlorpyriphos in the predatory mite Kampimodromus aberrans. Exp Appl Acarol 56:1–8
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
Tixier MS, Kreiter S, Auger P, Weber M (1998) Colonization of Languedoc vineyards by phytoseiid mites (Acari: Phytoseiidae): influence of wind and crop environment. Exp Appl Acarol 22:523–542
Tosi L, Farinazzo E, Posenato G, Girolami V (2006) Effetti collaterali di insetticidi su Kampimodromus aberrans. Inf Agr 26:54–56
Tsolakis H, Ragusa E, Di Chiara SR (2000) Distribution of phytoseiid mites (Parasitiformes, Phytoseiidae) on hazelnut at two different altitudes in Sicily (Italy). Environ Entomol 29:1251–1257
Van de Baan HE, Kuijpers LAM, Overmeer WPJ, Oppenoorth FJ (1985) Organophosphorous and carbamate resistance in the predacious mite Typhlodromus pyri due to insensitive acetylcholinesterase. Exp Appl Acarol 1:3–10
Van Driesche RG, Lyon S, Nunn C (2006) Compatibility of spinosad with predacious mites (Acari: Phytoseiidae) used to control western flower thrips (Thysanoptera: Thripidae) in greenhouse crops. Fla Entomol 89:396–401
Vettorello G, Girolami V (1992) Popolazioni di Amblyseius aberrans (Oud.) resistenti ai ditiocarbammati. Inf Agr 48:111–112
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
Williams T, Valle J, Viñuela E (2003) Is the naturally derived insecticide spinosad® compatible with insect natural enemies? Biocontrol Sci Technol 13:459–475
Yoo SS, Kim SS (2000) Comparative toxicity of some pesticides to the predatory mite, Phytoseiulus persimilis (Acarina: Phytoseiidae) and the twospotted spider mite Tetranychus urticae (Acarina: Tetranychidae). Korean J Entomol 30:235–241
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This work has been partially supported by PRIN Grants to CD (Ministry for University and research, Italy). We thank Gessica Tolotti and Maddalena Maritan for their assistance.
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Duso, C., Ahmad, S., Tirello, P. et al. The impact of insecticides applied in apple orchards on the predatory mite Kampimodromus aberrans (Acari: Phytoseiidae). Exp Appl Acarol 62, 391–414 (2014). https://doi.org/10.1007/s10493-013-9741-3
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DOI: https://doi.org/10.1007/s10493-013-9741-3