SpringerLink
Log in

Predation and behavioral changes in the neotropical lacewing Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae) exposed to lambda-cyhalothrin

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Pyrethroid insecticides are widely recommended against various defoliating pest species, but usually lack efficacy against sucking pests such as aphids, which are preferred prey of lacewing larvae. Interaction of pyrethroids and lacewings are likely to occur in fields infested by both defoliating and sap-sucking pests and should provide a complementary control. Therefore, our study aimed to estimate dose-mortality curves and behavioral changes by Chrysoperla externa exposed to lambda-cyhalothrin. We tested the susceptibility of two populations from different locations and insecticide history exposure through topical application. Based on the LD50-calculated, the population exhibiting the greater LD50 was exposed to resistance enhancement (Sel) by treating larvae once for seven successive generations. The population with lower LD50 was kept without selection (Nsel). Subsequently, walking, predation and oviposition behavioral after exposure to dried insecticide residues were investigated. After seven generations with insecticide selection, the resistance rations between Sel and Nsel populations were 5.85- and 9.37-fold higher for larvae and 3.38- and 2.75-fold higher for adults, respectively. Selected females caged in partially treated arenas laid similar eggs number on both treated and untreated surfaces, while Nsel females laid fewer eggs on treated surfaces. Insecticide repellency was not observed in either population, although irritability was observed for Nsel larvae. Selected larvae confined on fully and partially treated surfaces walked further, for a longer time, and with greater speeds compared to Nsel larvae. Furthermore, Sel and Nsel larvae had reduced predation rates when confined on treated surfaces, and Nsel larvae consumed less prey than Sel larvae. Results indicate changes in susceptibility, behavior, and predation rate of C. externa following exposure to lambda-cyhalothrin.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

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  Google Scholar 

  • AGROFIT, Sistema de Agrotoxicos Fitossanitarios (2017) Ministerio da Agricultura, Pecuaria e Abastecimento. Available http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed 8 Jan 2016

  • Barros EM, Silva-Torres CSA, Torres JB, Rolim GG (2018) Toxicity of insecticides belonging to different chemical groups to key predators and parasitoids for pest management. Phytoparasitica (submitted).

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bloomquist JR, Miller TA (1985) Carbofuran triggers flight motor output in pyrethroid-blocked reflex pathways of the house fly. Pestic Biochem Physiol 23:247–255

    Article  CAS  Google Scholar 

  • Bortoli SA, Ferreira RJ, Miranda JE, Oliveira JEM (2002) Suscetibilidade de Chrysoperla externa (Hagen) (Neuroptera, Chrysopidae) a Karate® (Lambda-cialotrina) em Condições de Laboratório. Bol San Veg Plagas 28:577–584

    Google Scholar 

  • Broza M (1986) An aphid outbreak in cotton fields in Israel. Phytoparasitica 14:81–85

    Article  Google Scholar 

  • Bueno AF, Carvalho GA, Santos AC, Sosa-Gómez DR, Silva DM (2017) Pesticide selectivity to natural enemies: challenges and constraints for research and field recommendation. Cienc Rural 47:1–10

    Article  Google Scholar 

  • Campanhola C, Plapp AF (1989) Toxicity and synergism of insecticides against susceptible and pyrethroid-resistant neonate larvae and adults of the tobacco budworm (Lepidoptera: Noctuidae). J Econ Entomol 82:1527–1533

    Article  CAS  Google Scholar 

  • Carvalho RA, Omoto C, Field LM, Williamson MS, Bass C (2013) Investigating the molecular mechanisms of organophosphate and pyrethroid resistance in the fall armyworm Spodoptera frugiperda. PLoS ONE 8:e62268

    Article  CAS  Google Scholar 

  • Chareonviriyaphap T, Roberts DR, Andre RG, Harlan H, Bangs MJ (1997) Pesticide avoidance behaviour in Anopheles albimanus Wiedemann. J Am Mosq Control Assoc 13:171–183

    CAS  Google Scholar 

  • Cordeiro EMG, Corrêa AS, Venzon M, Guedes RNC (2010) Insecticide survival and behavioural avoidance in the lacewings Chrysoperla externa and Ceraeochrysa cubana. Chemosphere 81:1352–1357

    Article  CAS  Google Scholar 

  • Croft BA, Theiling KM (1990) Pesticide effects on natural enemies: a database summary. In: Croft BA (ed) Arthropod biological control agents and pesticides. Wiley, New York, pp 17–46

    Google Scholar 

  • Deguine JP, Gozé E, Leclant F (2000) The consequences of late outbreaks of the aphid Aphis gossypii in cotton growing in Central Africa: towards a possible method for the prevention of cotton stickness. Int J Pest Manag 46:86–89

    Article  Google Scholar 

  • Delabie J, Bos C, Fonta C, Masson C (1985) Toxic and repellent effects of cypermethrin on the honeybee: laboratory, glasshouse and field experiments. Pestic Sci 16:409–415

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dutcher JD (2007) A review of resurgence and replacement causing pest outbreaks in IPM. In: Ciancio A, Mukerji KG (eds) General concepts in integrated pest and disease management. Integrated management of plants pests and diseases. Springer, Dordrecht, pp 27–43

    Google Scholar 

  • EFSA (European Food Safety Authority) (2014) Conclusion on the peer review of the pesticide risk assessment of the active substance lambda-cyhalothrin. EFSA J 12(3677):170

  • Ehler LE (2006) Perspective integrated pest management (IPM): definition, historical development and implementation, and the other IPM. Pest Manag Sci 62:787–789

    Article  CAS  Google Scholar 

  • Eveleens KG, Van den Bosch R, Ehler LE (1973) Secondary outbreak induction of beet armyworm by experimental insecticide applications in cotton in California. Environ Entomol 2:497–503

    Article  CAS  Google Scholar 

  • Ferreira ES, Silva-Torres CSA, Rodrigues ARS, Torres JB (2013) Life-history costs associated with resistance to lambda-cyhalothrin in the predatory ladybird beetle Eriopis connexa. Agric Entomol 15:168–177

    Article  Google Scholar 

  • Finney DJ (1971) Probit analysis. Cambridge University Press, London

    Google Scholar 

  • Freitas S (2002) O uso de crisopídeos no controle biológico de pragas. In: Parra JRP, Botelho PSM, Correa-Ferreira BS, Bento JM (eds) Controle biológico no Brasil: parasitóides e predadores. Manole, Piracicaba, pp 209–224

    Google Scholar 

  • Gist GL, Pless CD (1985) Ovicidal activity and ovipositional repellent properties of synthetic pyrethroids to the fall armyworm Spodoptera frugiperda. Fla Entomol 68:462–466

    Article  CAS  Google Scholar 

  • Hardin MR, Benrey B, Coll M, Lamp WO, Roderick GK, Barbosa P (1995) Arthropod pest resurgence: an overview of potential mechanisms. Crop Prot 14:3–18

    Article  Google Scholar 

  • Haynes KF (1988) Sublethal effects of neurotoxic insecticides on insect behavior. Annu Rev Entomol 33:149–168

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hodge S, Longley M (2000) The irritant and repellent effects of organophosphates on the Tasmanian lacewing, Micromus tasmaniae (Neuroptera: Hemerobiidae). Pest Manag Sci 56:916–920

    Article  CAS  Google Scholar 

  • Housset P, Dickmann R (2009) A promise fulfilled—pyrethroid development and the benefits for agriculture and human health. Bayer Crop 62:135–143

    Google Scholar 

  • Kabissa JCB, Kayumbot HY, Yarro JG (1996) Seasonal abundance of chrysopids (Neuroptera: Chrysopidae) preying on Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae) and Aphis gossypii (Glover) (Homoptera: Aphididae) on cotton in eastern Tanzania. Crop Prot 15:5–8

    Article  Google Scholar 

  • Kidd PW, Rummel DR (1997) Effect of insect predators and a pyrethroid insecticide on cotton aphid, Aphis gossypii Glover, population density. Southwest Entomol 22:381–393

    Google Scholar 

  • Knipling EF (1979) The basic principles of insect population suppression and management. In: USDA (ed) Agriculture handbook n. 512. USDA, Washington, D.C., pp 577–623

    Google Scholar 

  • Kranthi KR, Jadhav D, Wanjari R, Kranthi S, Russell D (2001) Pyrethroid resistance and mechanism of resistance in field strains of Helicoverpa armigera (Lepidoptera: Noctuidae). J Econ Entomol 94:253–263

    Article  CAS  Google Scholar 

  • Leonard BR, Boethel DJ, Sparks Junior AM, Layton MB, Mink JS, Pavloff AM, Burris E, Graves JB (1990) Variations in response of soybean looper (Lepidoptera; Noctuidae) to selected insecticides in Louisiana. J Econ Entomol 83:27–34

    Article  CAS  Google Scholar 

  • León-Garcia I, Rodríguez-Lueyva E, Ortega-Arenas LD, Solis-Aguilar JF (2012) Susceptibidad de Spodoptera frugiperda (JE Smith) (Lepidoptera: Noctuidae) a insecticidas asociada a césped em Quintana Roo, México. Agrociencia 46:279–287

    Google Scholar 

  • Little EE (1990) Behavioral toxicology: stimulating challenges for a growing discipline. Environ Toxicol Chem 9:1–2

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Martinou AF, Seraphides N, Stavrinides MC (2014) Lethal and behavioral effects of pesticides on the insect predator Macrolophus pygmaeus. Chemosphere 96:167–173

    Article  CAS  Google Scholar 

  • Moore RF (1980) Behavioral and biological effects of NRDC-161 factors in control of the boll weevil. J Econ Entomol 73:265–267

    Article  CAS  Google Scholar 

  • Mullin CA, Croft BA (1985) An update on development of selective pesticides favoring arthropod natural enemies. In: Hoy MA, Herzog DC (eds) Biological control in agricultural IPM systems. Academic Press, Orlando, pp 123–150

    Chapter  Google Scholar 

  • NPIC (National Pesticide Information Center) (2001) Lambda-cyhalothrin. Technical Fact Sheets, 6pp. Available http://npic.orst.edu/factsheets/archive/l_cyhalotech.pdf. Accessed 9 March 2018

  • Nordlund DA, Cohen AC, Smith RA (2001) Mass-rearing, release techniques, and augmentation. In: McEwen P, New TR, Whittington AE (eds) Lacewings in the crop environment. Cambridge University Press, Cambridge, pp 303–319

    Chapter  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  Google Scholar 

  • Penman DR, Chapman RB (1983) Fenvalerate induced distributional imbalances of two-spotted spider mite on bean plants. Entomol Exp Appl 33:71–78

    Article  CAS  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 

  • Resende ALS, Silva EE, Guerra JGM, Aguiar-Menezes EL (2007) Ocorrência de insetos predadores de pulgões em cultivo orgânico de couve em sistemas solteiro e consorciado com adubos verdes. Seropédica, Rio de Janeiro, Embrapa Agrobiologia, p 6 (Comunicado Técnico 101).

  • Riedl H, Hoying SA (1983) Toxicity and residual activity of fenvalerate to Typhlodromus occidentalis (Acari: Phytoseiidae) and its prey, Tetranychus urticae (Acari: Tetranychidae), on pear. Can Entomol 115:807–813

    Article  CAS  Google Scholar 

  • Rieth JP, Levin MD (1988) The repellent effect of two pyrethroid insecticides on the honey bee. Physiol Entomol 13:213–218

    Article  CAS  Google Scholar 

  • Ripper WE (1956) Effect of pesticides on balance of arthropod populations. Annu Rev Entomol 1:403–438

    Article  CAS  Google Scholar 

  • Robertson JL, Savin NE, Preisler HK, Russel RM (2007) Bioassays with arthropods, 2nd ed. CRC Press, Boca Raton

    Google Scholar 

  • Rodrigues ARS, Spindola AF, Torres JB, Siqueira HAA, Colares F (2013) Response of different populations of seven lady beetle species to lambda-cyhalothrin with record of resistance. Ecotoxicol Environ Saf 96:53–60

    Article  CAS  Google Scholar 

  • Rodrigues AS, Botina E, Nascimento CP, Gontijo LM, Torres JB, Guedes RNC (2016) Ontogenic behavioral consistency, individual variation and fitness consequences among lady beetles. Behav Process 131:32–39

    Article  Google Scholar 

  • Ruscoe CNE (1977) The new NRDC pyrethroids as agricultural insecticides. Pestic Sci 8:236–242

    Article  CAS  Google Scholar 

  • SAS Institute (2002) SAS/STAT User’s guide, version 9.0, TS level 2MO. SAS Institute Inc., Cary

    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 

  • Senior LJ, McEwen PK (2001) The use of lacewings in biological control. In: McEwen PK, New TR, Whittington AE (eds) Lacewings in the crop environment. Cambridge University Press, Cambridge, pp 296–302

    Chapter  Google Scholar 

  • Spindola AF, Silva-Torres CSA, Rodrigues ARS, Torres JB (2013) Survival and behavioural responses of the predatory ladybird beetle, Eriopis connexa populations susceptible and resistant to a pyrethroid insecticide. Bull Entomol Res 103:485–494

    Article  CAS  Google Scholar 

  • Tabashnik BE, Johnson MW (1999) Evolution of pesticide resistance in natural enemies. In: Bellows TS, Fisher TW (eds) Handbook of biological control. Academic Press, San Diego, pp 673–689

    Chapter  Google Scholar 

  • Tan J, McCaffery AR (2007) Efficacy of various pyrethroid structures against a highly metabolically resistant isogenic strain of Helicoverpa armigera (Lepidoptera: Noctuidae) from China. Pest Manag Sci 63:960–968

    Article  CAS  Google Scholar 

  • Tapajós SJ, Lira R, Silva-Torres CSA, Torres JB, Coitinho RLC (2016) Suitability of two exotic mealybug species as prey to indigenous lacewing species. Biol Control 96:93–100

    Article  Google Scholar 

  • Tavares AM, Torres JB, Silva-Torres CSA, Vacari AM (2013) Behavior of Montandoniola confusa Streito & Matocq (Hemiptera: Anthocoridae) preying upon gall-forming thrips Gynaikothrips ficorum Marchal (Thysanoptera: Phlaeothripidae). Biol Control 67:328–336

    Article  Google Scholar 

  • Torres JB (2012) Insecticide resistance in natural enemies - seeking for integration of chemical and biological controls. J Biofert Biopest 3:e104

    Article  Google Scholar 

  • Torres JB, Ruberson JR (2007) Abundance and diversity of ground-dwelling arthropods of pest management importance in commercial Bt and non-Bt cotton fields. Ann Appl Biol 150:27–39

    Article  Google Scholar 

  • Torres JB, Rodrigues ARS, Barros EM, Santos DS (2015) Lambda-cyhalothrin resistance in the lady beetle Eriopis connexa (Coleoptera: Coccinellidae) confers tolerance to other pyrethroids. J Econ Entomol 108:60–68

    Article  CAS  Google Scholar 

  • Torres-Vila LM, Rodriguez-Molina MC, Lacasa-Plasencia A, Bielza-Lino P, Rodriguez-del-Rincon A (2002) Pyrethroid resistance of Helicoverpa armigera in Spain, current status and agroecological perspective. Agric Ecosyst Environ 93:55–66

    Article  CAS  Google Scholar 

  • Ugurlu S, Gurkan MO (2007) Insecticide resistance in Helicoverpa armigera from cotton-growing areas in Turkey. Phytoparasitica 35:376–379

    Article  CAS  Google Scholar 

  • Wang XY, Shen ZR (2002) Effects of sublethal doses of insecticides on predation of multicolored asian ladybird Harmonia axyridis (Pallas) (Coleoptera: Coccinelliodae). Acta Ecol Sin 22:2278–2284

    Google Scholar 

  • Whalon ME, Mota-Sanchez D, Hollingworth RM, Duynslager L (2011) Arthropod pesticide resistance database. Available http://www.pesticideresistance.org/. Acessed 26 June 2015

Download references

Acknowledgements

The authors thank the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)” for grants to R.F.L. and cost support through the project PROCAD CAPES NF No. 3027/2014.

Author information

Authors and Affiliations

  1. Departamento de Agronomia-Entomologia, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, Recife, PE, 52171-900, Brazil

    René Fernando Luna, Luziani Rezende Bestete, Jorge Braz Torres & Christian Sherley Araújo da Silva-Torres

Authors
  1. René Fernando Luna
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Luziani Rezende Bestete
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jorge Braz Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christian Sherley Araújo da Silva-Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jorge Braz Torres.

Ethics declarations

Conflict of interest

The authors declare they have no conflicts of interest, no human subjects were involved in these experiments, and all applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Luna, R.F., Bestete, L.R., Torres, J.B. et al. Predation and behavioral changes in the neotropical lacewing Chrysoperla externa (Hagen) (Neuroptera: Chrysopidae) exposed to lambda-cyhalothrin. Ecotoxicology 27, 689–702 (2018). https://doi.org/10.1007/s10646-018-1949-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-018-1949-x

Keywords

Search

Navigation