Skip to main content
SpringerLink
Log in

Azadirachtin-mediated reproductive response of the predatory pirate bug Blaptostethus pallescens

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The little-known pirate bug Blaptostethus pallescens Poppius is a biocontrol agent observed in tropical tomato fields in Brazil regulating fruit borer populations. In this study, the lethal response of B. pallescens to the bioinsecticide azadirachtin and to two synthetic insecticides, chlorpyrifos and deltamethrin, was assessed. The mild effect of the azadirachtin label rate (0.006 mg a.i. ml−1) on the predator (median lethal time (LT50) of 27 days), relative to label rates of deltamethrin (0.02 mg a.i. ml−1) and chlorpyrifos (1.44 mg a.i. ml−1) (with LT50 of 25 and 60 min, respectively) led to the assessment of its potential sublethal effects. Azadirachtin did not cause behavioral avoidance in the pirate bug, but the daily fecundity, adult progeny production and sex ratio were impaired when both male and female parents were exposed. These effects reduced the population growth of the predator in subsequent generations. Therefore, although safer than the conventional synthetic insecticides tested, the bioinsecticide azadirachtin does impair predator reproduction requiring attention when used in fields with this biological control agent.

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

Access this article

Log in via an institution

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

  • Agriculture and Agro-Food Canada (2003) Pesticide risk reduction and minor use programs: improving ways to manage pests with new technology. Government of Canada, Ottawa, Canada

    Google Scholar 

  • Bahlai CA, Xue Y, McCreary CM, Schaafsma AW, Hallett RH (2010) Choosing organic pesticides over synthetic pesticides may not effectively mitigate environmental risks in soybeans. PLoS ONE 5(6):e11250

    Article  PubMed Central  PubMed  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 the predator Orius laevigatus. Chemosphere 87:803–812

    Article  CAS  PubMed  Google Scholar 

  • Cabello T, Gallego JR, Fernandez FJ, Gamex M, Vila E, Del Pino M, Hernandez-Suarez E (2012) Biological control strategies for the South American tomato moth (Lepidoptera: Gelechiidae) in greenhouse tomatoes. J Econ Entomol 105:2085–2096

    Article  PubMed  Google Scholar 

  • Campos MC, Picanço MC, Martins JC, Tomaz AC, Guedes RNC (2011) Insecticide selectivity and behavioral response of the earwig Doru luteipes. Crop Prot 30:1535–1540

    Article  CAS  Google Scholar 

  • Caswell H (2001) Matrix populations models. Sinauer, Sunderland, UK

    Google Scholar 

  • Coats JR (1994) Risk from natural versus synthetic insecticides. Annu Rev Entomol 39:489–515

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cordeiro EMG, de Moura ILT, Fadini MAM, Guedes RNC (2013) Beyond selectivity: are behavioral avoidance and hormesis likely causes of pyrethroid-induced outbreaks of the southern red mite Oligonychus ilicis? Chemosphere 93:1111–1116

    Article  CAS  PubMed  Google Scholar 

  • Cutler GC (2013) Insects, insecticides and hormesis: evidence and considerations for study. Dose-Response 11:154–177

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Desneux N, O’Neil RJ, Yoo HJS (2006) Suppression of population growth of the soybean aphid, Aphis glycines Matsumura, by predators: the identification of a key predator and the effects of prey dispersion, predator abundance, and temperature. Environ Entomol 35:1342–1349

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys KAG, Burgio G, Arpaia S, Narváez-Vazquez CA, Cabrera JG, Catalán Ruescas D, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello T, Urbaneja A (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215

    Article  Google Scholar 

  • Gerwick BC, Sparks TC (2014) Natural products for pest control: an analysis of their role, value and future. Pest Manag Sci 70(8):1169–1185. doi:10.1002/ps.3744

    Article  CAS  PubMed  Google Scholar 

  • Ghomein K (2014) Predatory insects and arachnids as potential biological control agents against the invasive tomato leafminer, Tuta absoluta Meyrick (Lepidoptera: Gelechiidae), in perspective and prospective. J Entomol Zool Stud 2:52–71

    Google Scholar 

  • Gontijo PC, Picanço MC, Pereira EJG, Martins JC, Chediak M, Guedes RNC (2013) Spatial and temporal variation in the control failure likelihood of the tomato leaf miner, Tuta absoluta. Ann Appl Biol 162:50–59

    Article  Google Scholar 

  • Gradish AE, Scott-Dupree CD, Shipp L, Harris CR, Ferguson G (2011) Effect of reduced risk pesticides on greenhouse vegetable arthropod biological control agents. Pest Manag Sci 67:82–86

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Guedes RNC, Picanço MC (2012) The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. Bull OEPP/EPPO Bull 42:211–216

    Article  Google Scholar 

  • Guedes RNC, Siqueira HAA (2012) The tomato borer Tuta absoluta: insecticide resistance and control failure. CAB Rev 7(055):1–7

    Article  Google Scholar 

  • Guedes NMP, Guedes RNC, Ferreira GH, Silva LB (2009a) Flight take-off and walking behavior of insecticide-susceptible and –resistant strains of Sitophilus zeamais exposed to deltamethrin. Bull Entomol Res 99:393–400

    Article  CAS  PubMed  Google Scholar 

  • Guedes RNC, Magalhães LC, Cosme LV (2009b) Stimulatory sublethal response of a generalist predator to permethrin: hormesis, hormoligosis, or homeostatic regulation? J Econ Entomol 102:170–176

    Article  CAS  PubMed  Google Scholar 

  • Hood GM (2010) PopTools version 3.2.3. http://www.poptools.org. Cited 18 April 2014

  • Isman M (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66

    Article  CAS  PubMed  Google Scholar 

  • James KH (1990) Risk perceptions and food choice: an exploratory analysis of organic- versus conventional-produce buyers. Risk Anal 10:367–374

    Article  Google Scholar 

  • Jones E (2004) Grants awarded to develop pesticide risk reduction programs. United States Environmental Protection Agency. Press release 10/14/2004. http://yosemite.epa.gov/opa/admpress.nsf/d0cf6618525a9efb85257359003fb69d/738ef661407a042085257035005831db!OpenDocument&Highlight=2,risk. Cited 18 April 2014

  • Lima DB, Melo JWS, Guedes RNC, Siqueira HAA, Pallini A, Gondim MGC Jr (2013) Survival and behavioural response to acaricides of the coconut mite predator Neoseiulis baraki. Exp Appl Acarol 60:381–393

    Article  PubMed  Google Scholar 

  • Medina P, Budia F, Del Estal P, Vinuela E (2004) Influence of azadirachtin, a botanical insecticide, on Chrysoperla carnea (Stephens) reproduction: toxicity and ultrastructural approach. J Econ Entomol 97:43–50

    Article  CAS  PubMed  Google Scholar 

  • Ministério da Agricultura, Pecuária e Abastecimento [MAPA] (2014) Agrotis. Coordenação Geral de Agrotóxicos e Afins/DFIA/DAS, Brasília, DF, Brazil. http://extranet.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Cited 28 June 2014

  • Mordue (Luntz) AJ, Morgan ED, Nisbet AJ (2005) Azadirachtin, a natural product in insect control. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive molecular insect science. Elsevier, Oxford, UK, pp 117–135

    Chapter  Google Scholar 

  • Mordue (Luntz) AJ, Nisbet AJ (2000) Azadirachtin from the neem tree (Azadirachta indica): its actions against insects. Ann Soc Entomol Brasil 29:615–632

    Article  Google Scholar 

  • Pereira RR, Picanço MC, Santana Jr PA, Moreira SS, Guedes RNC, Corrêa AS (2014) Insecticide toxicity and walking response of three pirate bug predators on the tomato leaf miner Tuta absoluta. Agric For Entomol (in press). doi:10.1111/afe/12059

  • Qi B, Gordon G, Gimme W (2001) Effects of neem-fed prey on the predacious insects Harmonia conformis (Boisduval) (Coleoptera: Coccinellidae) and Mallada signatus (Schneider) (Neuroptera: Chrysopidae). Biol Control 22:185–190

    Article  Google Scholar 

  • Rosell G, Quero C, Coll J, Guerrero A (2008) Biorational insecticides in pest management. J Pestic Sci 33:103–121

    Article  CAS  Google Scholar 

  • SAS Institute (2008) SAS/STAT user’s guide v. 8. SAS Institute, Cary, NC, USA

  • Tedeschi R, Alma A, Tavella L (2001) Side-effects of three neem (Azadirachta indica A. Juss) products on the predator Macrolophus caliginosus Wagner (Het., Miridae). J Appl Entomol 125:397–402

    Article  CAS  Google Scholar 

  • Tomé HVV, Martins JC, Corrêa AS, Galdino TVS, Picanço MC, Guedes RNC (2013) Azadirachtin avoidance by larvae and adult females of the tomato leafminer Tuta absoluta. Crop Prot 46:63–69

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • van de Veire M, Smagghe G, Degheele D (1996) Laboratory test method to evaluate the effect of 31 pesticides on the predatory bug, Orius laevigatus (Het.: Anthocoridae). Entomophaga 41:235–243

    Article  Google Scholar 

  • Vilca Mallqui KS, Vieira JL, Guedes RNC, Gontijo RNC (2014) Azadirachtin-induced hormesis mediating shift in fecundity-longevity trade-off in the Mexican bean weevil (Chrysomelidae: Bruchinae). J Econ Entomol 107:860–866

    Article  Google Scholar 

  • Villaverde JJ, Sevilla-Morán B, Sandín-España P, López-Goti C, Alonso-Prados JL (2014) Biopesticides in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Manag Sci 70:2–5

    Article  CAS  PubMed  Google Scholar 

  • Zehnder G, Gurr GM, Kühne S, Wade MR, Wratter SD, Wyss E (2007) Arthropod pest management in organic crops. Annu Rev Entomol 52:57–80

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We acknowledge the financial support provided by the Minas Gerais State Foundation for Research Aid (FAPEMIG), the National Council of Scientific and Technological Development (CNPq), and the CAPES Foundation (Brazilian Ministry of Education). We also thank Drs. P. De Clercq and E. Wajnberg, and two anonymous reviewers for the comments and suggestions provided.

Author information

Authors and Affiliations

  1. Departamento de Entomologia, Universidade Federal de Viçosa, Viçosa, MG, 36570-900, Brazil

    Daiane Celestino, Guilherme I. Braoios, Rodrigo S. Ramos, Lessando M. Gontijo & Raul Narciso C. Guedes

  2. Central de Ensino e Desenvolvimento Agrário de Florestal (CEDAF), Universidade Federal de Viçosa – Campus Florestal, Florestal, Rod. LMG 818, Km 06, Florestal, MG, 35690-000, Brazil

    Lessando M. Gontijo

Authors
  1. Daiane Celestino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guilherme I. Braoios
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rodrigo S. Ramos
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lessando M. Gontijo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Raul Narciso C. Guedes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Raul Narciso C. Guedes.

Additional information

Handling Editor: Patrick De Clercq.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Celestino, D., Braoios, G.I., Ramos, R.S. et al. Azadirachtin-mediated reproductive response of the predatory pirate bug Blaptostethus pallescens . BioControl 59, 697–705 (2014). https://doi.org/10.1007/s10526-014-9601-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-014-9601-z

Keywords

Search

Navigation