Skip to main content
SpringerLink
Log in

Effects of spirotetramat treatments on fecundity and carboxylesterase expression of Aphis gossypii Glover

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Spirotetramat is a novel tetramic acid-based insecticide, belonging to keto-enol pesticide family, with a novel mode of action; it interferes with lipid biosynthesis. Its insecticide activity against various agricultural pest insects have been demonstrated (e.g. on Myzus persicae, Bemisia tabaci and Tetranychus urticae). However, information available is currently limited on the efficacy of spirotetramat on the cotton aphid, Aphis gossypii, a key cotton pest worldwide. We assessed the spirotetramat toxicity on A. gossypii and evaluated its effects on aphid fecundity when exposed to a sublethal concentration (LC10) and to increasing lethal concentrations (LC25, LC50, and LC75). A key mechanism involved in insecticide resistance in aphids relates to esterase activity. We estimated the CarE activity and a CarE gene expression in aphids in response to spirotetramat exposure, then we tested tolerance of offspring to spirotetramat when the parents were exposed to the highest concentration tested in our study (LC75). Results showed that spirotetramat showed increasing toxicity to A. gossypii with exposure duration to treated leaves; LC50 ranged from 23,675.68 to 12.27 mg/L for 1 to 5-days exposure. In addition, spirotetramat reduced aphid daily fecundity, in all concentration treatments, especially with up to 90 % reduction in case of exposure to LC75. Total CarE activity increased dramatically and CarE mRNA expression was also up regulated in aphids after exposure to LC75 spirotetramat. Finally, the tolerance to spirotetramat in offspring (when parents were exposed to the LC75) showed a 2.5-fold increase when compared to control aphids. Consequently, spiroteramat showed potential for pest management of cotton aphids owing to both lethal and sublethal activities, notably strong impact on aphid fecundity. However, we also demonstrated that increased tolerance of A. gossypii to spirotetramat may happen through increased CarE- activity and subsequent metabolic degradation of the insecticide in aphids’ body.

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

Similar content being viewed by others

References

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein, utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  Google Scholar 

  • Bretschneider T, Fischer R, Nauen R (2009) Inhibitors of lipid synthesis. In: Kramer W, Schirmer U (eds) Modern crop protection compounds, vol 3. Wiley-vch GmbH & Co. KGaA, Weinheim, pp 909–925

    Google Scholar 

  • Bruck E, Elbert A, Fischer R, Krueger S, Kuhnhold J, Klueken AM, Nauen R, Niebes JF, Reckman U, Schnorbach HJ, Steffens R, van Waetermeulen X (2009) Movento®, an innovative ambimobile insecticide for suckinginsect pest control in agriculture: biological profile and field performance. Crop Prot 28:838–844

    Article  Google Scholar 

  • Cai QN, Han Y, Cao YZ, Hu Y, Zhao X, Bi JL (2009) Detoxification of gramine by the cereal aphid Sitobion avenae. J Chem Ecol 35:320–325

    Article  CAS  Google Scholar 

  • Campolo O, Chiera E, Malacrinò A, Laudani F, Fontana A, Albanese GR, Palmeri V (2014) Acquisition and transmission of selected CTV isolates by Aphis gossypii. J Asia Pac Entomol 17:493–498

    Article  Google Scholar 

  • Cantoni A, De Maeyer L, Izquierdo Casas J, Niebes JF, Peeters D, Roffeni S, Silva J, Villalobos A (2008) Development of Movento® on key pests and crops in European countries. Bayer CropSci J 61:349–376

    CAS  Google Scholar 

  • Cao CW, Zhang J, Gao XW (2008) Overexpression of carboxylesterase gene associated with organophosphorous insecticide resistance in cotton aphids, Aphis gossypii (Glover). Pestic Biochem Phys 90:175–180

    Article  CAS  Google Scholar 

  • Devonshire L, Moores GD (1982) A carboxylesterase with broad substrate specificity causes organophoyus, carbamate and pyrethroid resistance in peachpotato aphids (myzus persicae). Pestic Biochem Phys 18:235–246

    Article  CAS  Google Scholar 

  • Elbert A, Nauen R, Salmon E (2008) Resistance management guidelines for the new ketoenol insecticide Movento®. Bayer CropSci J 61:403–416

    CAS  Google Scholar 

  • Feyereisen R (2005) Insect cytochrome P450. In: Gilbert LI, Latrou K, Gill SS (eds) Comprehensive molecular insect science, vol 4. Elsevier, Amsterdam

    Google Scholar 

  • Garcerá C, Ouyang YL, Scott SJ, Moltó E, Grafton-Cardwell EE (2013) Effects of spirotetramat on Aonidiella aurantii (Homoptera: Diaspididae) and its parasitoid, Aphytis melinus (Hymenoptera: Aphelinidae). J Econ Entomol 106:21–26

    Article  Google Scholar 

  • Hemingway J, Hawkes NJ, Mccarroll L, Ranson H (2004) The molecular basis of insecticide resistance in mosquitoes. Insect Biochem Molec 34:653–665

    Article  CAS  Google Scholar 

  • Hu J, Wang C, Wang J, You Y (2010) Monitoring of resistance to spirodiclofen and five other acaricides in Panonychuscitri collected from Chinese citrus orchards. Pest Manag Sci 66:1025–1030

    Article  CAS  Google Scholar 

  • Kay IR, Herron GA (2010) Evaluation of existing and newinsecticides including spirotetramat and pyridalyl to control Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) on peppers in Queensland. Aust J Entomol 49:175–181

    Article  Google Scholar 

  • Koester J, Klempner A (2006) [Azaspirodecenyl-3-14C]BYI 08330: Absorption, distribution, excretion, and metabolism in the lactating goat; Bayer CropScience AG, Monheim, Germany; Report No.: MEF-05/293; Document No.: M-269256-01-2; 05-MAY-06, p 213

  • Li F, Han ZJ, Wu ZF, Wang YC (2001) Insecticide resistance of Aphis gossypii Glover in cotton in China. Cotton Sci 13:121–124

    Google Scholar 

  • Li X, Schuler MA, Berenbaum MR (2007) Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 52:231–253

    Article  Google Scholar 

  • Lindroth RL, Weisbrod AV (1991) Genetic variation in response of the gypsy moth to aspen phenolic glycosides. Biochem Syst Ecol 19:97–103

    Article  CAS  Google Scholar 

  • Marčić D (2007) Sublethal effects of spirodiclofen on life history and life-table parameters of two-spotted spider mite (Tetranychusurticae). Exp Appl Acarol 42:121–129

    Article  Google Scholar 

  • Marčić D, Ogurlić I, Mutavdžić S, Perić P (2010) The effects of spiromesifen on life history traits and population growth of two-spotted spider mite (Acari: Tetranychidae). Exp Appl Acarol 50:255–267

    Article  Google Scholar 

  • Marčić D, Mutavdžić S, Medjo I, Prijović M, Perić P (2011a) Spirotetramat toxicity to immatures and sublethal effects on fecundity of female adults of Tetranychusurticae Koch. Zoosymposia 6:99–103

    Google Scholar 

  • Marčić D, Perić P, Petronijević S, Prijović M, Drobnjaković T (2011b) Cyclic ketoenols—acaricides and insecticides with a novel mode of action. Pestic Phytomed (Belgrade) 26:185–195

    Article  Google Scholar 

  • Maus C (2008) Ecotoxicological profile of the insecticide spirotetramat. Bayer CropSci J 61:159–180

    CAS  Google Scholar 

  • Moores GD, Gao X, Denholm I, Devonshire AL (1996) Characterisation of insensitive acetylcholines in insecticide-resistant cotton aphids, Aphis gossypii Glover (Homoptera: Aphididae). Pestic Biochem Physiol 56:102

    Article  CAS  Google Scholar 

  • Nauen R, Schnorbach HJ, Elbert A (2005) Biological profile of spiromesifen (Oberon®)—a new tetronic acid insecticide/acaricide. Pflanzenschutz-Nachrichten Bayer 58:417–440

    CAS  Google Scholar 

  • Nauen R, Reckmann U, Thomzik J, Thielert W (2008) Biological profile of spirotetramat (Movento®)—a new two-way systemic (ambimobile) insecticide against sucking pest species. Bayer CropSci J 61:245–278

    CAS  Google Scholar 

  • O’Brien PJ, Abdel-Aal YA, Ottea JA, Graves JB (1992) Relationship of insecticide resistance to carboxylesterases in Aphis gossypii (Homoptera: Apididae) from midsouth cotton. J Econ Entomol 85:651–657

    Article  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:6

    Article  Google Scholar 

  • Planes L, Catalán J, Tena A, Porcuna J, Jacas J, Izquierdo J, Urbaneja A (2013) Lethal and sublethal effects of spirotetramat on the mealybug destroyer Cryptolaemus montrouzieri. J Pest Sci 86:321–327

    Article  Google Scholar 

  • Qiao CL, Cui F, Yan SG (2009) Structure, function and applications of carboxylestrases from insects for insecticide resistance. Protein Pept Lett 16:1181–1188

    Article  Google Scholar 

  • Rauch N, Nauen R (2002) Spirodiclofen resistance risk assessment in Tetranychusurticae (Acari: Tetranychidae): a biochemical approach. Pestic Biochem Phys 74:91–101

    Article  CAS  Google Scholar 

  • Riaz MA, Poupardin R, Reynaud S, Strode C, Ranson H, David JP (2009) Impact of glyphosate and benzo[a]pyrene on the tolerance of mosquito larvae to chemical insecticides. Role of detoxification genes in response to xenobiotics. Aquat Toxicol 93:61–69

    Article  CAS  Google Scholar 

  • Roistacher CN, Bar-Joseph M, Gumpf DJ (1984) Transmission of tristeza and seedling yellows tristeza virus by small populations of Aphis gossypii. Plant Dis 68:494–496

    Article  Google Scholar 

  • Schnorbach J, Elbert A, Laborie B, Navacerrada J, Bangels E, Gobin B (2008) Movento®, an ideal tool for Integrated Pest Management (IPM) in pome fruit, citrus and vegetables. Pflanzenschutz-Nachrichten Bayer 61:411–436

    Google Scholar 

  • Sun YQ, Feng GL, Yuan JG, Zhu P, Gong KY (1987) Biochemical mechanism of resistance of cotton aphids to organophosphorus insecticides. Acta Entomol Sin 30:13–20

    CAS  Google Scholar 

  • Sun YQ, Feng GL, Yuan JG, Gong KY (1994) Insecticide resistance of cotton aphid in North China. Entomol Sin. 1:242–250

    Google Scholar 

  • Suwanchaichinda C, Brattsten LB (2001) Effects of exposure to pesticides on carbaryl toxicity and cytochrome P450 activities in Aedes albopictus larvae (Diptera: Culicidae). Pestic Biochem Physiol 70:63–73

    Article  CAS  Google Scholar 

  • Suwanchaichinda C, Brattsten LB (2002) Induction of microsomal cytochrome P450 s by tire-leachate compounds, habitat components of Aedes albopictus mosquito larvae. Arch Insect Biochem Physiol 49:71–79

    Article  CAS  Google Scholar 

  • Suzuki K, Hama H, Konno Y (1993) Carboxylesterase of the cotton aphid, Aphis gossypii Glover (Homoptera: Aphididae), responsible for fenitrothion resistance as a sequestering protein. Appl Entomol Zool 28:439–450

    CAS  Google Scholar 

  • Van Asperen K (1962) A study of housefly esterases by means of sensitive colorimetric method. J Insect Physiol 8:401–416

    Article  CAS  Google Scholar 

  • van Pottelberge S, Khajehali J, van Leeuwen T, Tirry L (2009a) Effects of spirodiclofen on reproduction in a susceptible and resistant strain of Tetranychusurticae (Acari: Tetranychidae). Exp Appl Acavol 47:301–309

    Article  Google Scholar 

  • van Pottelberge S, van Leeuwen T, Khajehali J, Tirry L (2009b) Genetic and biochemical analysis of a laboratory- selected spirodiclofen-resistant strain of Tetranychusurticae Koch (Acari: Tetranychidae). Pest Manag Sci 65:358–366

    Article  Google Scholar 

  • Van Waetermeulen X, Brück E, Elbert A, Fischer R, Krueger S, Kühnhold J, Nauen R, Niebes JF, Reckmann U, Schnorbach HJ, Steffens R (2007) Spirotetramat, an innovative fully systemic insecticide for sucking insect pest control in agriculture: biological profile and field performance. In: Proceedings of the XVI international plant protection congress, vol 1: pp 60–67

  • Wachendorff U, Nauen R, Schnorbach HJ, Rauch N, Elbert A (2002) The biological profile of spirodiclofen (Envidor®)—a new selective tetronic acid acaricide. Pflanzenschutz-Nachrichten Bayer 55:149–176

    CAS  Google Scholar 

  • Yu SJ (1996) Insect glutathione S-transferases. Zool Stud 35:9–19

    CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by The National Natural Science Foundation of China (No. 31330064).

Author information

Authors and Affiliations

  1. Department of Entomology, China Agricultural University, Beijing, China

    Youhui Gong, Xueyan Shi & Xiwu Gao

  2. French National Institute for Agricultural Research (INRA), UMR 1355-ISA, 400 Route des Chappes, 06903, Sophia-Antipolis, France

    Nicolas Desneux

Authors
  1. Youhui Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xueyan Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicolas Desneux
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiwu Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiwu Gao.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gong, Y., Shi, X., Desneux, N. et al. Effects of spirotetramat treatments on fecundity and carboxylesterase expression of Aphis gossypii Glover. Ecotoxicology 25, 655–663 (2016). https://doi.org/10.1007/s10646-016-1624-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-016-1624-z

Keywords

Search

Navigation