Skip to main content
Log in

Imidacloprid-mediated effects on survival and fertility of the Neotropical brown stink bug Euschistus heros

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Enhanced reproductive output after sublethal insecticide exposure, including neonicotinoid exposure, has been reported in a diversity of arthropods. Suspicions of such a phenomenon in the Neotropical brown stink bug, Euschistus heros (Hemiptera: Pentatomidae), were sparked by the increasing densities of naturally occurring populations of this insect pest species in Brazilian soybean fields. Here, we tested whether the sublethal exposure to imidacloprid would induce changes in the survival and reproductive performances of E. heros adult females. The imidacloprid estimated LC50 was 0.83 (0.60–1.25) μg a.i./cm2, and the dose recommended for field applications (4.2 μg a.i./cm2) was within the concentration range of the imidacloprid estimated LC80 [2.66 (1.65–5.49) μg a.i./cm2]. Newly emerged (≤24 h) adult females were exposed for 48 h to dry imidacloprid residues (0.042 μg/cm2, equivalent to 1 % of the field rate dose) and exhibited higher levels of cell damage, greater ovariole length, and a larger area of the most developed follicle in their ovaries up to the 6th day of adulthood. Furthermore, these females exhibited reduced rates of survival but higher fecundity and fertility rates compared with untreated females. Our results thus suggest that females of E. heros increased their reproductive output in response to the imidacloprid sublethal exposure. These findings suggest a potential involvement of sublethal exposure to neonicotinoids in the recent outbreaks of the Neotropical brown stink bug E. heros observed in Brazilian soybean-producing regions.

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

Access this article

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ayyanath M, Cutler G, Scott-Dupree C, Sibley P (2013) Transgenerational shifts in reproduction hormesis in green peach aphid exposed to low concentrations of imidacloprid. PLoS ONE 8:e74532

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bal R, Naziroğlu M, Türk G, Yilmaz Ö, Kuloğlu T, Etem E, Baydas G (2012) Insecticide imidacloprid induces morphological and DNA damage through oxidative toxicity on the reproductive organs of developing male rats. Cell Biochem Funct 30:492–499

    Article  CAS  PubMed  Google Scholar 

  • Bao H, Liu S, Gu J, Wang X, Liang X, Liu Z (2009) Sublethal effects of four insecticides on the reproduction and wing formation of brown planthopper, Nilaparvata lugens. Pest Manag Sci 65:170–174

    Article  CAS  PubMed  Google Scholar 

  • Benzidane Y, Lapied B, Thany SH (2011) Neonicotinoid insecticides imidacloprid and clothianidin affect differently neural Kenyon cell death in the cockroach Periplaneta americana. Pestic Biochem Physiol 101:191–197

    Article  CAS  Google Scholar 

  • Braeckman B, Simoens C, Rzeznik U, Raes H (1997) Effect of sublethal doses of cadmium, inorganic mercury and methylmercury on the cell morphology of an insect cell line (Aedes Albopictus, C6/36). Cell Biol Int 21:823–832

    Article  CAS  PubMed  Google Scholar 

  • Borges M, Lauman RA, Silva CCA, Moraes MCB, Santos HM, Ribeiro DT (2008) Metodologias de criação e manejo de colônias de percevejo da soja (Heteroptera: Pentatomidae) para estudos de comportamento e ecologia química In: Documentos 182, EMBRAPA Recursos Geneticos e Melhoramento, Brasília, Brasil, pp 1–18

  • Calabrese EJ, Baldwin LA (2003) The hormetic dose-response model is more common than the threshold model in toxicology. Toxicol Sci 71:246–250

    Article  CAS  PubMed  Google Scholar 

  • Calabrese EJ, Stanek EJ III, Nascarella MA, Hoffmann GR (2008) Hormesis predicts low-dose responses better than threshold models. Int J Toxicol 27:369–378

    Article  CAS  PubMed  Google Scholar 

  • Cardone A (2014) Imidacloprid induces morphological and molecular damages on testis of lizard (Podarcis sicula). Ecotoxicol. doi:10.1007/s10646-014-1361-0

    Google Scholar 

  • Charpentier G, Louat F, Bonmatin J-M, Marchand PA, Vanier F, Locker D et al (2014) Lethal and sublethal effects of imidacloprid, after chronic exposure, on the insect model Drosophila melanogaster. Environ Sci Technol 48:4096–4102

    Article  CAS  PubMed  Google Scholar 

  • Cordeiro EMG, 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  PubMed Central  CAS  PubMed  Google Scholar 

  • Cutler G, Ramanaidu K, Astatkie T, Isman MB (2009) Green peach aphid, Myzus persicae (Hemiptera: Aphididae), reproduction during exposure to sublethal concentrations of imidacloprid and azadirachtin. Pest Manag Sci 65:205–209

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Farias LR, Paula DP, Zhou JJ, Liu R, Pappas GJ Jr, Moraes MCB et al (2014) Identification and expression profile of two putative odorant-binding proteins from the Neotropical brown stink bug, Euschistus heros (Fabricius) (Hemiptera: Pentatomidae). Neotrop Entomol 43:106–114

    Article  CAS  Google Scholar 

  • Flatt T, Kawecki TJ (2007) Juvenile hormone as a regulator of the trade-off between reproduction and life span in Drosophila melanogaster. Evolution 61:1980–1991

    Article  PubMed  Google Scholar 

  • Ge L-Q, Hu J-H, Wu J-C, Yang G-Q, Gu H (2009) Insecticide-Induced changes in protein, RNA, and DNA contents in ovary and fat Body of female Nilaparvata lugens (Hemiptera: Delphacidae). J Econ Entomol 102:1506–1514

    Article  CAS  PubMed  Google Scholar 

  • Gregorc A, Ellis JD (2011) Cell death localization in situ in laboratory reared honey bee (Apis mellifera L.) larvae treated with pesticides. Pestic Biochem Physiol 99:200–207

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Guedes NMP, Tolledo J, Corrêa AS, Guedes RNC (2010) Insecticide-induced hormesis in an insecticide-resistant strain of the maize weevil, Sitophilus zeamais. J Appl Entomol 134:142–148

    Article  CAS  Google Scholar 

  • Hoshi N, Hirano T, Omotehara T, Tokumoto J, Umemura Y, Mantani Y et al (2014) Insight into the mechanism of reproductive dysfunction caused by neonicotinoid pesticides. Biol Pharm Bull 37:1439–1443

    Article  CAS  PubMed  Google Scholar 

  • Jager T, Barsi A, Ducrot V (2013) Hormesis on life-history traits: is there such thing as a free lunch? Ecotoxicology 22:263–270

    Article  CAS  PubMed  Google Scholar 

  • James DG, Price TS (2002) Fecundity in twospotted spider mite (Acari: Tetranychidae) is increased by direct and systemic exposure to imidacloprid. J Econ Entomol 95:729–732

    Article  CAS  PubMed  Google Scholar 

  • Jeschke P, Nauen R, Beck ME (2013) Nicotinic acetylcholine receptor agonists: a milestone for modern crop protection. Angew Chem Int Ed Engl 52:9464–9485

    Article  CAS  PubMed  Google Scholar 

  • Kapoor U, Srivastava MK, Srivastava LP (2011) Toxicological impact of technical imidacloprid on ovarian morphology, hormones and antioxidant enzymes in female rats. Food Chem Toxicol 49:3086–3089

    Article  CAS  PubMed  Google Scholar 

  • Laycock I, Lenthall K, Barratt A, Cresswell J (2012) Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21:1937–1945

    Article  CAS  PubMed  Google Scholar 

  • Lee CY (2000) Sublethal effects of insecticides on longevity, fecundity and behaviour of insect pests: a review. J Biosci 11:107–112

    Google Scholar 

  • Lee CY, Yap HH, Chong NL (1998) Sublethal effects of deltamethrin and propoxur on longevity and reproduction of German cockroaches, Blattella germanica. Entomol Exp Appl 89:137–145

    Article  CAS  Google Scholar 

  • Liu JL, Yang X, Zhang HM, Chen X, Wu JC (2013) Effects of indoxacarb on total protein, RNA, and DNA contents in the ovaries and fat bodies of Nilaparvata lugens Stål (Hemiptera: Delphacidae) adult females. Pestic Biochem Physiol 106:14–20

    Article  CAS  Google Scholar 

  • Macfadyen S, Hardie DC, Fagan L, Stefanova K, Perry KD, DeGraaf HE et al (2014) Reducing insecticide use in broad-acre grains production: an Australian study. PLoS ONE 9:e89119

    Article  PubMed Central  PubMed  Google Scholar 

  • Mattson M, Calabrese E (2010) Hormesis: What it is and why it matters. In: Mattson MP, Calabrese EJ (eds) Hormesis: a revolution in biology, toxicology and medicine. Humana Press, New York, pp 1–13

    Chapter  Google Scholar 

  • Pan H, Liu Y, Liu B, Lu Y, Xu X, Qian X, Wu K, Desneux N (2014) Lethal and sublethal effects of cycloxaprid, a novel cis-nitromethylene neonicotinoid insecticide, on the mirid bug Apolygus lucorum. J Pest Sci 87:731–738

    Article  Google Scholar 

  • Panizzi AR, Bueno AF, Silva FAC (2014) Insetos que atacam vagens e grãos. In: Hoffman-Campo CB, Corrêa-Ferreira BS, Moscardi F (eds) Soja: Manejo Integrado de Insetos e outros Artrópodes-Praga. EMBRAPA, Brasília-DF, pp 335–420

    Google Scholar 

  • Perveen E (2000) Sublethal effects of chlorfluazuron on reproductivity and viability of Spodoptera litura (F.) (Lep., Noctuidae). J Appl Entomol 124:223–231

    Article  CAS  Google Scholar 

  • Quarcoo F, Bonsi C, Franklin Tackie N, Quarcoo Conrad Bonsi, Tackie Nii (2014) Pesticides, the environment, and human health. In: Larramendy ML, Soloneski S (eds) Agricultural and Biological Sciences: “Pesticides—Toxic Aspects”. InTech Europe, Rijeka, pp 81–103

    Google Scholar 

  • Rattan SIS (2008) Hormesis in aging. Ageing Res Rev 7:63–78

    Article  PubMed  Google Scholar 

  • Rossi CA, Roat T, Tavares D, Cintra-Socolowski P, Malaspina O (2013) Brain morphophysiology of africanized bee Apis mellifera exposed to sublethal doses of imidacloprid. Arch Environ Contam Toxicol 65:234–243

    Article  Google Scholar 

  • Roubos CR, Rodriguez-Saona C, Isaacs R (2014) Mitigating the effects of insecticides on arthropod biological control at field and landscape scales. Biol Cont. 75:28–38

    Article  CAS  Google Scholar 

  • SAS Institute (2008) SAS/STAT User’s Guide. Cary, NC

    Google Scholar 

  • Silva CCA, Lauman RA, Blassioli MC, Pareja M, Borges M (2008) Euschistus heros mass rearing technique for the multiplication of Telenomus podisi. Pesqui Agropecu Bras 43:575–580

    Google Scholar 

  • Silva FAC, Calizotti GS, Panizzi AR (2011) Survivorship and egg production of phytophagous pentatomids in laboratory rearing. Neotrop Entomol. 40:35–38

    Article  CAS  PubMed  Google Scholar 

  • Snodgrass GL, Adamczyk JJ, Gore J (2005) Toxicity of insecticides in a glass-vial bioassay to adult brown, green, and southern green stink bugs (Heteroptera: Pentatomidae). J Econ Entomol 98:177–181

    Article  CAS  PubMed  Google Scholar 

  • Sosa-Gómez DR, Silva JJ (2010) Neotropical brown stink bug (Euschistus heros) resistance to methamidophos in Paraná, Brazil. Pesq Agropec Bras 45:767–769

    Article  Google Scholar 

  • Sosa-Gómez DR, Da Silva JJ, De Oliveira Negrao Lopes I, Corso IC, Almeida AMR, De Moraes GCP et al (2009) Insecticide susceptibility of Euschistus heros (Heteroptera: Pentatomidae) in Brazil. J Econ Entomol 102:1209–1216

    Article  PubMed  Google Scholar 

  • Szczepaniec A, Raupp M (2013) Direct and indirect effects of imidacloprid on fecundity and abundance of Eurytetranychus buxi (Acari: Tetranychidae) on boxwoods. Exp Appl Acarol 59:307–318

    Article  PubMed  Google Scholar 

  • Tan Y, Biondi A, Desneux N, Gao X-W (2012) Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-Dür). Ecotoxicology 21:1989–1997

    Article  CAS  PubMed  Google Scholar 

  • Tomé H, Martins G, Lima M, Campos LAO, Guedes R (2012) Imidacloprid-induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides. PLoS ONE 7:e38406

    Article  PubMed Central  PubMed  Google Scholar 

  • Vilca Mallqui KS, Vieira JL, Guedes RNC, Gontijo LM (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 

  • Wang XY, Yang ZQ, Shen ZR, Lu J, Xu WB (2008) Sublethal effects of selected insecticides on fecundity and wing dimorphism of green peach aphid (Hom., Aphididae). J Appl Entomol 132:135–142

    Article  CAS  Google Scholar 

  • Willrich MM, Leonard BR, Cook DR (2003) Laboratory and field evaluations of insecticide toxicity to stink bugs (Heteroptera: Pentatomidae). J Cotton Sci 7:156–163

    Google Scholar 

  • Yin J-l Xu, H-w Wu, J-c Hu, J-h Yang G-q (2008) Cultivar and insecticide applications affect the physiological development of the brown planthopper, Nilaparvata lugens (Stål) (Hemiptera: Delphacidae). Environ Entomol 37:206–212

    Article  PubMed  Google Scholar 

  • Yu Y, Shen G, Zhu H, Lu Y (2010) Imidacloprid-induced hormesis on the fecundity and juvenile hormone levels of the green peach aphid Myzus persicae (Sulzer). Pestic Biochem Physiol 98:238–242

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from CAPES Foundation, the National Council of Scientific and Technological Development (CNPq), the Minas Gerais State Foundation for Research Aid (FAPEMIG), and the Arthur Bernardes Foundation (FUNARBE). We thank Daniela C. Guedes and Nathaly N. C. Miranda for their excellent technical assistance.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. E. Oliveira.

Additional information

Communicated by E. Roditakis.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Santos, M.F., Santos, R.L., Tomé, H.V.V. et al. Imidacloprid-mediated effects on survival and fertility of the Neotropical brown stink bug Euschistus heros . J Pest Sci 89, 231–240 (2016). https://doi.org/10.1007/s10340-015-0666-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-015-0666-y

Keywords

Navigation