Skip to main content
SpringerLink
Log in

Insecticide Resistance in Natural Enemies

  • Chapter
  • First Online:
Advances in Insect Control and Resistance Management

Abstract

Pesticide resistance in pests has severe negative consequences but can be used as a positive trait for natural enemies as an opportunity to improve the simultaneous use of two very valuable tools in pest management: chemical and biological control. Biological control adoption is limited in some areas, crops, or seasons due to the imperative use of pesticides needed to control diseases and pests. Most studies on pesticides and natural enemies try to establish the degree of compatibility using only a population, not considering the natural variation in insecticide susceptibility. However, there is variation in the response to pesticides among populations of a beneficial species, similarly to the response in any pest species. Knowledge of the natural and potential variation in the tolerance of natural enemies to pesticides may improve the design of robust IPM strategies by extending the role of biological control in some agricultural systems and by increasing the number of available compounds to control diseases and key, secondary, and invasive pests. There are a number of excellent revisions on pesticide resistance in natural enemies. In the present review, new cases of insecticide resistance in natural enemies are discussed, as a better understanding of pesticide resistance in natural enemies will allow us to enhance the integration of chemical and biological tools in IPM programs.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abbas N, Mansoor MM, Shad SA, Pathan AK, Waheed A, Ejaz M, Razaq M, Zulfiqar MA (2014) Fitness cost and realized heritability of resistance to spinosad in Chrysoperla carnea (Neuroptera: Chrysopidae). Bull Entomol Res 104:707–715

    Article  CAS  PubMed  Google Scholar 

  • Adams CH, Cross WH (1967) Insecticide resistance in Bracon mellitor, a parasite of the boll weevil. J Econ Entomol 60:1016–1020

    Article  CAS  Google Scholar 

  • Argolo PS, Jacas JA, Urbaneja A (2014) Comparative toxicity of pesticides in three phytoseiid mites with different life-style occurring in citrus: Euseius stipulatus, Neoseiulus californicus and Phytoseiulus persimilis. Exp Appl Acarol 62:33–46

    Article  CAS  PubMed  Google Scholar 

  • APRD – Arthropod Pesticide Resistance Database, Michigan State University. http://ww.pesticideresistance.org. Accessed 4 Aug 2015

  • Avella M, Fournier D, Pralavorio M, Berge JB (1985) Sélection pour la résistance à la deltaméthrine d’une souche de Phytoseiulus persimilis Athias-Henriot. Agronomie 5:177–180

    Article  Google Scholar 

  • Bacci L, Picanço MC, Rosado JF, Silva GA, Crespo ALB, Pereira EJG, Martins JC (2009) Conservation of natural enemies in brassica crops: comparative selectivity of insecticides in the management of Brevicoryne brassicae (Hemiptera: Sternorrhyncha: Aphididae). Appl Entomol Zool 44:103–113

    Article  CAS  Google Scholar 

  • Baker JE, Fabrick JA, Zhu KY (1998) Characterization of esterases in malathion-resistant and susceptible strains of the pteromalid parasitoid Anisopteromalus calandrae. Insect Biochem Mol Biol 28:1039–1050

    Article  CAS  Google Scholar 

  • Barbar Z, Tixier M-S, Kreiter S (2007) Assessment of pesticide susceptibility for Typhlodromus exhilaratus and Typhlodromus phialatus strains (Acari: Phytoseiidae) from vineyards in the south of France. Exp Appl Acarol 42:95–105

    Article  CAS  PubMed  Google Scholar 

  • Bielza P (2008) Insecticide resistance management strategies against the western flower thrips, Frankliniella occidentalis. Pest Manag Sci 64:1131–1138

    Article  CAS  PubMed  Google Scholar 

  • Bielza P, Denholm I, Sterk G, Leadbeater A, Leonard P, Jørgensen LN (2008). Declaration of Ljubljana–the impact of a declining European pesticide portfolio on resistance management. Outlooks Pest Manag 19:246–248

    Google Scholar 

  • Bielza P, Fernández E, Grávalos C, Izquierdo J (2009) Testing for non-target effects of spiromesifen on Eretmocerus mundus and Orius laevigatus under greenhouse conditions. BioControl 54:229–236

    Article  Google Scholar 

  • Bonafos R, Serrano E, Auger P, Kreiter S (2007) Resistance to deltamethrin, lambda-cyhalothrin and chlorpyrifos-ethyl in some populations of Typhlodromus pyri Scheuten and Amblyseius andersoni (Chant)(Acari: Phytoseiidae) from vineyards in the south-west of France. Crop Prot 26:169–172

    Article  CAS  Google Scholar 

  • Calvo FJ, Bolckmans K, Belda JE (2011) Control of Bemisia tabaci and Frankliniella occidentalis in cucumber by Amblyseius swirskii. Biocontrol 56:185–192

    Article  Google Scholar 

  • Calvo FJ, Bolckmans K, Belda JE (2012) Release rate for a pre-plant application of Nesidiocoris tenuis for Bemisia tabaci control in tomato. BioControl 57(6):809–817

    Article  Google Scholar 

  • Croft BA, Aliniazee MT (1983) Differential resistance to insecticides in Typhlodromus arboreus Chant and associate phytoseiid mites of apple in the Willamette Valley, Oregon. Environ Entomol 12:1420–1423

    Article  CAS  Google Scholar 

  • Croft BA, Brown AWA (1975) Responses of arthropod natural enemies to insecticides. Annu Rev Entomol 20:285–335

    Article  CAS  PubMed  Google Scholar 

  • Croft BA, Meyer RH (1973) Carbamate and organophosphorus resistance patterns in populations of Amblyseius fallacis. Environ Entomol 2:691–696

    Article  CAS  Google Scholar 

  • Croft BA, Morse JG (1979) Research advances on pesticide resistance in natural enemies. Entomophaga 24:3–11

    Article  Google Scholar 

  • Croft BA, Van de Baan HE (1988) Ecological and genetic factors influencing evolution of pesticide resistance in tetranychid and phytoseiid mites. Exp Appl Acarol 4:277–300

    Article  CAS  Google Scholar 

  • Croft BA, Briozzo J, Carbonell JB (1976) Resistance to organophosphorus insecticides in a predaceous mite, Amblyseius chilenensis. J Econ Entomol 69:563–565

    Article  CAS  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 

  • Dunley JE, Messing RH, Croft BA (1991) Levels and genetics of organophosphate resistance in Italian and Oregon biotypes of Amblyseius andersoni (Acari: Phytoseiidae). J Econ Entomol 84:750–755

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Espinosa PJ, Bielza P, Contreras J, Lacasa A (2002) Insecticide resistance in field populations of Frankliniella occidentalis (Pergande) in Murcia (south‐east Spain). Pest Manag Sci 58:967–971

    Article  CAS  PubMed  Google Scholar 

  • Fernández E, Grávalos C, Haro PJ, Cifuentes D, Bielza P (2009) Insecticide resistance status of Bemisia tabaci Q‐biotype in south‐eastern Spain. Pest Manag Sci 65:885–891

    Article  PubMed  Google Scholar 

  • Georghiou GP (1986) The magnitude of the resistance problem. In: Pesticide resistance: strategies and tactics for management. National Academy Press, Washington, DC

    Google Scholar 

  • Grávalos C, Fernández E, Belando A, Moreno I, Ros C, Bielza P (2014) Cross‐resistance and baseline susceptibility of Mediterranean strains of Bemisia tabaci to cyantraniliprole. Pest Manag Sci 71:1030–1036

    Article  PubMed  Google Scholar 

  • Graves JB, Mohamad RB, Clower DF (1978) Beneficial insects also developing “resistance”. Lousiana Agric 22:10–11

    Google Scholar 

  • Hadam JJ, AliNiazee MT, Croft BA (1986) Phytoseiid mites (Parasitiformes: Phytoseiidae) of major crops in Willamette Valley, Oregon, and pesticide resistance in Typhlodromus pyri Scheuten. Environ Entomol 15:1255–1263

    Article  CAS  Google Scholar 

  • Hassan SA, Bigler F, Blaisinger P, Bogenschütz H, Brun J, Chiverton P et al (1985) Standard methods to test the side‐effects of pesticides on natural enemies of insects and mites developed by the IOBC/WPRS Working Group ‘Pesticides and Beneficial Organisms’. EPPO Bull 15:214–255

    Article  Google Scholar 

  • Havron A, Kenan G, Rosen D (1991a) Selection for pesticide resistance in Aphytis. II. A.lingnanensis, a parasite of the California red scale. Entomol Exp Appl 61:229–235

    Article  Google Scholar 

  • Havron A, Rosen D, Prag H, Rössler Y (1991b) Selection for pesticide resistance in Aphytis: I. A. holoxanthus, a parasite of the Florida red scale. Entomol Exp Appl 61:221–228

    Article  Google Scholar 

  • Head R, Neel WW, Sartor CF, Chambers H (1977) Methyl parathion and carbaryl resistance in Chrysomela scripta and Coleomegilla maculata. Bull Environ Contam Toxicol 17:163–164

    Article  CAS  PubMed  Google Scholar 

  • Hodek I (2014) Biology of coccinellidae. Springer, Dordrecht

    Google Scholar 

  • Hoy MA (1990) Pesticide resistance in arthropod natural enemies: variability and selection responses. In: Richard TR, Bruce ET (eds) Pesticide resistance in arthropods. Springer, New York, pp 203–236

    Google Scholar 

  • Hoy MA, Cave FE, Beede RH, Grant J, Krueger WH, Olson WH et al (1990) Release, dispersal, and recovery of a laboratory-selected strain of the walnut aphid parasite Trioxys pallidus (Hymenoptera: Aphidiidae) resistant to azinphosmethyl. J Econ Entomol 83:89–96

    Article  CAS  Google Scholar 

  • Jalali SK, Singh SP, Venkatesan T, Murthy KS, Lalitha Y (2006) Development of endosulfan tolerant strain of an egg parasitoid Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae). Indian J Exp Biol 44:584

    CAS  PubMed  Google Scholar 

  • Javier PA, Havron A, Morallo‐Rejesus B, Rosen D (1991) Selection for pesticide resistance in Aphytis: III. Male selection. Entomol Exp Appl 61:237–245

    Article  Google Scholar 

  • Johnson MW, Tabashnik BE (1994) Laboratory selection for pesticide resistance in natural enemies. In: Narang SK, Bartlett AC, Faust RM (eds) Applications of genetics to arthropods of biological control significance. CRC Press, London, pp 91–105

    Google Scholar 

  • Kawai A (1997) Prospect for integrated pest management in tea cultivation in Japan. Jpn Agric Res Q 31:213–218

    Google Scholar 

  • Kennett CE (1970) Resistance to parathion in the phytoseiid mite Amblyseius hibisci. J Econ Entomol 63:1999–2001

    Article  Google Scholar 

  • Kumral NA, Gencer NS, Susurluk H, Yalcin C (2011) A comparative evaluation of the susceptibility to insecticides and detoxifying enzyme activities in Stethorus gilvifrons (Coleoptera: Coccinellidae) and Panonychus ulmi (Acarina: Tetranychidae). Int J Acarol 37:255–268

    Article  Google Scholar 

  • Liu SS, Li ZM, Liu YQ, Feng MG, Tang ZH (2007) Promoting selection of resistance to spinosad in the parasitoid Cotesia plutellae by integrating resistance of hosts to the insecticide into the selection process. Biol Control 41:246–255

    Article  Google Scholar 

  • Mansoor MM, Abbas N, Shad SA, Pathan AK, Razaq M (2013) Increased fitness and realized heritability in emamectin benzoate-resistant Chrysoperla carnea (Neuroptera: Chrysopidae). Ecotoxicology 22:1232–1240

    Article  CAS  PubMed  Google Scholar 

  • Markwick NP (1986) Detecting variability and selecting for pesticide resistance in two species of phytoseiid mites. Entomophaga 31:225–236

    Article  CAS  Google Scholar 

  • Mochizuki M (1994) Variations in insecticide susceptibility of the predatory mite, Amblyseius womersleyi Schicha (Acarina: Phytoseiidae), in the Tea Fields of Japan. Appl Entomol Zool 29:203–209

    CAS  Google Scholar 

  • Motoyama N, Rock GC, Dauterman WC (1970) Organophosphorus resistance in an apple Orchard population of Typhlodromus (Amblyseius) fallacis. J Econ Entomol 63:1439–1442

    Article  CAS  Google Scholar 

  • Pathan AK, Sayyed AH, Aslam M, Razaq M, Jilani G, Saleem MA (2008) Evidence of field-evolved resistance to organophosphates and pyrethroids in Chrysoperla carnea (Neuroptera: Chrysopidae). J Econ Entomol 101:1676–1684

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Mendoza J, Fabrick JA, Zhu KY, Baker JE (2000) Alterations in esterases are associated with malathion resistance in Habrobracon hebetor (Hymenoptera: Braconidae). J Econ Entomol 93:31–37

    Article  PubMed  Google Scholar 

  • Pielou DP, Glasser RF (1952) Selection for DDT resistance in a beneficial insect parasite. Science 115:117–118

    Article  CAS  PubMed  Google Scholar 

  • Poletti M, Omoto C (2005) Variabilidades inter e intraespecífica na suscetibilidade de ácaros fitoesídeos à deltametrina em citros no Brasil. Man Integr Plagas Agroecol 75:32–37

    Google Scholar 

  • Poletti M, Omoto C (2012) Susceptibility to deltamethrin in the predatory mites Neoseiulus californicus and Phytoseiulus macropilis (Acari: Phytoseiidae) populations in protected ornamental crops in Brazil. Exp Appl Acarol 58:385–393

    Article  CAS  PubMed  Google Scholar 

  • Pollen KM, Johnson MW, Tabashnik BE (1995) Stability of fenvalerate resistance in the leaf miner parasitic Diglyphs begin (Hymenoptera: Eulophidae). J Econ Entomol 88:192–197

    Article  Google Scholar 

  • Posenato G (1994) Popolazioni di Amblyseius aberrans (Ouid.) resistenti ad esteri fosforici e ditiocarbammati. Inf Agric 50:41–43

    Google Scholar 

  • Pree DJ, Archibald DE, Morrison RK (1989) Resistance to insecticides in the common green lacewing Chrysoperla carnea (Neuroptera: Chrysopidae) in southern Ontario. J Econ Entomol 82:29–34

    Article  CAS  Google Scholar 

  • Rathman RJ, Johnson MW, Tabashnik BE, Spollen KM (1995) Variation in susceptibility to insecticides in the leafminer parasitoid Ganaspidium utilis (Hymenoptera: Eucoilidae). J Econ Entomol 88:475–479

    Article  CAS  Google Scholar 

  • Roditakis E, Skarmoutsou C, Staurakaki M, Martínez‐Aguirre MR, García‐Vidal L, Bielza P et al (2013) Determination of baseline susceptibility of European populations of Tuta absoluta (Meyrick) to indoxacarb and chlorantraniliprole using a novel dip bioassay method. Pest Manag Sci 69:217–227

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues ARS, Ruberson JR, Torres JB, Siqueira HÁA, Scott JG (2013a) Pyrethroid resistance and its inheritance in a field population of Hippodamia convergens (Guérin-Méneville)(Coleoptera: Coccinellidae). Pestic Biochem Physiol 105:135–143

    Article  CAS  Google Scholar 

  • Rodrigues AR, Torres JB, Siqueira HA, Lacerda DP (2013b) Inheritance of lambda-cyhalothrin resistance in the predator lady beetle Eriopis connexa (Germar)(Coleoptera: Coccinellidae). Biol Control 64:217–224

    Article  CAS  Google Scholar 

  • Rosenheim JA, Hoy MA (1988) Sublethal effects of pesticides on the parasitoid Aphytis melinus (Hymenoptera: Aphelinidae). J Econ Entomol 81:476–483

    Article  CAS  Google Scholar 

  • Roush RT, Hoy MA (1980) Selection improves Sevin resistance in spider mite predator. Calif Agric 34:11–14

    Google Scholar 

  • Roush RT, Hoy CW, Ferro DN, Tingey WM (1990) Insecticide resistance in the Colorado potato beetle (Coleoptera: Chrysomelidae): influence of crop rotation and insecticide use. J Econ Entomol 83:315–319

    Article  CAS  Google Scholar 

  • Sanchez JA, Alcázar A, Lacasa A, Llamas A, Bielza P, Albajes R, Sekeroglu E (2000) Integrated pest management strategies in sweet pepper plastic houses in the Southeast of Spain. Bull OILB/SROP 23:21–30

    Google Scholar 

  • Sato ME, Silva M, Gonçalves LR, Souza Filho MF, Raga A (2002) Toxicidade diferencial de Agroquímicos a Neoseiulus californicus (McGregor) (Acari: Phytoseiidae) e Tetranychus urticae Koch (Acari: Tetranychidae) em Morangueiro. Neotr Entomol 31:449–456

    Article  CAS  Google Scholar 

  • Sato ME, Tanaka T, Miyata T (2006) Monooxygenase activity in methidathion resistant and susceptible populations of Amblyseius womersleyi (Acari: Phytoseiidae). Exp Appl Acarol 39:13–24

    Article  CAS  PubMed  Google Scholar 

  • Sato ME, Silva MZ, Souza Filho MF, Matioli AL, Raga A (2007) Management of Tetranychus urticae (Acari: Tetranychidae) in strawberry fields with Neoseiulus californicus (Acari: Phytoseiidae) and acaricides. Exp Appl Acarol 42:107–120

    Article  PubMed  Google Scholar 

  • Sayyed AH, Pathan AK, Faheem U (2010) Cross-resistance, genetics and stability of resistance to deltamethrin in a population of Chrysoperla carnea from Multan, Pakistan. Pestic Biochem Physiol 98:325–332

    Article  CAS  Google Scholar 

  • Silva MZ, Sato ME, Oliveira CAL, Rais DS (2011) Toxicidade diferencial de agrotóxicos utilizados em citros para Neoseiulus californicus, Euseius concordis e Brevipalpus phoenicis. Bragantia 70:87–95

    Article  Google Scholar 

  • Sparks TC, Nauen R (2014) IRAC: mode of action classification and insecticide resistance management. Pestic Biochem Physiol 121:122–128

    Article  PubMed  Google Scholar 

  • Tabashnik BE, Johnson MW (1999) Evolution of pesticide resistance in natural enemies. In: Fisher TW, Bellows TS, Caltagirone LE, Dahlsten DL, Huffaker CB, Gordh G (eds) Handbook of biological control: principles and applications of biological control. Academic, San Diego, pp 673–689

    Chapter  Google Scholar 

  • Takeda T, Nakamatsu Y, Tanaka T (2006) Parasitization by Cotesia plutellae enhances detoxifying enzyme activity in Plutella xylostella. Pestic Biochem Physiol 86:15–22

    Article  CAS  Google Scholar 

  • Tang ZH, Gong KY, You ZP (1988) Present status and countermeasures of insecticide resistance in agricultural pests in China. Pestic Sci 23:189–198

    Article  CAS  Google Scholar 

  • Tang L-D, Qiu B-L, Cuthbertson AGS, Ren S-X (2015) Status of insecticide resistance and selection for imidacloprid resistance in the ladybird beetle Propylaea japonica (Thunberg). Pestic Biochem Physiol 123:87–92

    Article  CAS  PubMed  Google Scholar 

  • Theiling KM, Croft BA (1988) Pesticide side-effects on arthropod natural enemies: a database summary. Agric Ecosyst Environ 21:191–218

    Article  CAS  Google Scholar 

  • Tirello P, Pozzebon A, Duso C (2012) Resistance to chlorpyrifos in the predatory mite Kampimodromus aberrans. Exp Appl Acarol 56:1–8

    Article  PubMed  Google Scholar 

  • Urbaneja A, Montón H, Molla O (2009) Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. J Appl Entomol 133(4):292–296

    Article  Google Scholar 

  • Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol 40:563–572

    Article  PubMed  Google Scholar 

  • Whitten MJ, Hoy MA (1999) Genetic improvement and other genetic considerations for improving the efficacy and success rate of biological control. In: Fisher TW, Bellows TS, Caltagirone LE, Dahlsten DL, Huffaker CB, Gordh G (eds) Handbook of biological control: principles and applications of biological control. Academic, San Diego, pp 271–295

    Chapter  Google Scholar 

  • Wu G, Lin YW, Miyata T, Jiang SR, Xie LH (2009) Positive correlation of methamidophos resistance between Lipaphis erysimi and Diaeretiella rapae and effects of methamidophos ingested by host insect on the parasitoid. Insect Sci 16:165–173

    Article  CAS  Google Scholar 

  • Xu J, Shelton AM, Cheng X (2001) Variation in susceptibility of Diadegma insulare (Hymenoptera: Ichneumonidae) to permethrin. J Econ Entomol 94:541–546

    Article  CAS  PubMed  Google Scholar 

  • Yorulmaz Salman S, Aydinli F, Ay R (2015) Selection for resistance: cross-resistance, inheritance, synergists and biochemical mechanisms of resistance to acequinocyl in Phytoseiulus persimilis AH (Acari: Phytoseiidae). Crop Prot 67:109–115

    Article  CAS  Google Scholar 

  • Zhao HM, Yi X, Deng YY, Hu MY, Zhong GH, Wang PD (2013) Resistance to fenpropathrin, chlorpyrifos and abamectin in different populations of Amblyseius longispinosus (Acari: Phytoseiidae) from vegetable crops in South China. Biol Control 67:61–65

    Article  CAS  Google Scholar 

  • Zhuang HM, Li CW, Wu G (2014) Identification and characterization of ace2-type acetylcholinesterase in insecticide-resistant and-susceptible parasitoid wasp Oomyzus sokolowskii (Hymenoptera: Eulophidae). Mol Biol Rep 41:7525–7534

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Departamento de Producción Vegetal, Universidad Politécnica de Cartagena, Paseo Alfonso XIII 48, 30203, Cartagena, Spain

    Pablo Bielza

Authors
  1. Pablo Bielza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pablo Bielza .

Editor information

Editors and Affiliations

  1. Department of Entomology, Agricultural Research Organization, Gilat Research Center, Negev, Israel

    A. Rami Horowitz

  2. Department of Entomology, Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel

    Isaac Ishaaya

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Bielza, P. (2016). Insecticide Resistance in Natural Enemies. In: Horowitz, A., Ishaaya, I. (eds) Advances in Insect Control and Resistance Management. Springer, Cham. https://doi.org/10.1007/978-3-319-31800-4_16

Download citation

Publish with us

Policies and ethics

Search

Navigation