Effects of low concentrations of deltamethrin are dependent on developmental stages and sexes in the pest moth Spodoptera littoralis

Abstract

Effects of low concentrations of pesticides, with no or moderate mortality of targeted species, are poorly studied even though these low concentrations are common under natural conditions. Studying their effects is critical because they can induce positive hormetic responses, possibly leading to greater pest multiplication and promoting the evolution of pest resistance. Here, we investigated the responses of the pest moth Spodoptera littoralis to low concentrations of deltamethrin, and tested for variation in effects of the pesticide between developmental stages and sexes. Indeed, we show that a given concentration of deltamethrin has different effects between stages, and even between sexes. Two experimental concentrations led to very high mortality early in S. littoralis development (4th larval instar), but only to low mortality rates in adults. Moreover, our highest experimental concentration had only detrimental effects in adult females, but improved the reproductive success of adult males. Model projections showed that the lethality from treatments at the 4th larval instar was the predominant effect. Because of the high multiplication rate of S. littoralis, it was also found that treatments with very similar effects on larval mortality can lead to either population extinction or rapid pest resurgence.

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References

  1. Abdullah F, Subramanian P, Ibrahim H, Abdul Malek SN, Lee GS, Hong SL (2015) Chemical composition, antifeedant, repellent, and toxicity activities of the rhizomes of Galangal, Alpinia galanga against asian subterranean termites, Coptotermes gestroi and Coptotermes curvignathus (Isoptera: Rhinotermitidae). J Insect Sci 15:1–7. https://doi.org/10.1093/jisesa/ieu175

    CAS  Article  Google Scholar 

  2. Baker CRB, Miller GW (1974) Some effects of temperature and larval food on development of Spodoptera littoralis (Boisd.) (Lep., Noctuidae). B Entomol Res 63:495–511

    Article  Google Scholar 

  3. Bessa-Gomes C, Legendre S, Clobert J (2010) Discrete two-sex models of population dynamics: on modelling the mating function. Acta Oecol 36:439–445 https://doi-org.inee.bib.cnrs.fr/10.1016/j.actao.2010.02.010

    Article  Google Scholar 

  4. Bewick S (2016) Current and future challenges of predictive insect population modelling. Funct Ecol 30:1028–1029. https://doi.org/10.1111/1365-2435.12678

    Article  Google Scholar 

  5. Bouvier JC, Boivin T, Beslay D, Sauphanor B (2002) Age-dependent response to insecticides and enzymatic variation in susceptible and resistant codling moth larvae. Arch Insect Biochem 51:55–66. https://doi.org/10.1002/arch.10052

    CAS  Article  Google Scholar 

  6. Bradbury SP, Coats JR (1989) Toxicokinetics and toxicodynamics of pyrethroid insecticides in fish. Environ Toxicol Chem 8:373–380

    CAS  Article  Google Scholar 

  7. CABI (2020) Spodoptera littoralis (cotton leafworm). In: Invasive species compendium. Wallingford, UK: CAB International. http://www.cabi.org/isc/datasheet/51070

  8. Casida JE (2009) Pest toxicology: the primary mechanisms of pesticide action. Chem Res Toxicol 22:609–619. https://doi.org/10.1021/tx8004949

    CAS  Article  Google Scholar 

  9. Caswell H (2001) Matrix population models: construction, analysis, and interpretation, 2nd edn. Sinauer Associates Inc, Sunderland

    Google Scholar 

  10. Chowdhury ABMNU, Jepson PC, Howse PE, Ford MG (2001) Leaf surfaces and the bioavailability of pesticide residues. Pest Manag Sci 57:403–412. https://doi.org/10.1002/ps.311

    CAS  Article  Google Scholar 

  11. Christie PT, Wright DJ (1990) Activity of abamectin against larval stages of Spodoptera littoralis boisduval and Heliothis armigera hübner (Lepidoptera: Noctuidae) and possible mechanisms determining differential toxicity. Pestic Sci 29:29–38

    CAS  Article  Google Scholar 

  12. Costantini D, Metcalfe NB, Monaghan P (2010) Ecological processes in a hormetic framework. Ecol Lett 13:1435–1447. https://doi.org/10.1111/j.1461-0248.2010.01531.x

    Article  Google Scholar 

  13. Cutler GC (2013) Insects, insecticides and hormesis: evidence and considerations for study. Dose-Response 11:154–177. https://doi.org/10.2203/dose-response.12-008.Cutler

    CAS  Article  Google Scholar 

  14. Ferrière R, Sarrazin F, Legendre S, Baron J-P (1996) Matrix population models applied to viability analysis and conservation: theory and practice with ULM software. Acta Oecol 17:629–6356

    Google Scholar 

  15. Gerhardt A (2007) Aquatic behavioral ecotoxicology-prospects and limitations. Hum Ecol Risk Assess 13:481–491. https://doi.org/10.1080/10807030701340839

    Article  Google Scholar 

  16. Germano MD, Picollo MI (2018) Stage-dependent expression of deltamethrin toxicity and resistance in Triatoma infestans (Hemiptera: Reduviidae) from Argentina. J Med Entomol XX:1–5. https://doi.org/10.1093/jme/tjy017

    CAS  Article  Google Scholar 

  17. Goulding AT, Shelley LK, Ross PS, Kennedy CJ (2013) Reduction in swimming performance in juvenile rainbow trout (Oncorhynchus mykiss) following sublethal exposure to pyrethroid insecticides. Comp Biochem Phys C 157:280–286. https://doi.org/10.1016/j.cbpc.2013.01.001

    CAS  Article  Google Scholar 

  18. Guedes RNC, Cutler GC (2014) Insecticide-induced hormesis and arthropod pest management: insecticide-induced hormesis. Pest Manag Sci 70:690–697. https://doi.org/10.1002/ps.3669

    CAS  Article  Google Scholar 

  19. Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62. https://doi.org/10.1146/annurev-ento-010715-023646

    CAS  Article  Google Scholar 

  20. Guedes RNC, Walse SS, Throne JE (2017) Sublethal exposure, insecticide resistance, and community stress. Curr Opin Insect Sci 21:47–53. https://doi.org/10.1016/j.cois.2017.04.010

    Article  Google Scholar 

  21. Haug G, Hoffman H (1990) Chemistry of plant protection 4: synthetic pyrethroid insecticides: structures and properties. Springer, New York

    Google Scholar 

  22. Hinks CF, Byers JR (1976) Biosystematics of the genus Euxoa (Lepidoptera: Noctuidae). V. Rearing procedures and life cycles of 36 species. Can Entomol 108:1345–1357

    Article  Google Scholar 

  23. Hooper MJ, Ankley GT, Cristol DA, Maryoung LA, Noyes PD, Pinkerton KE (2013) Interactions between chemical and climate stressors: a role for mechanistic toxicology in assessing climate change risks. Environ Toxicol Chem 32:32–48. https://doi.org/10.1002/etc.2043

    CAS  Article  Google Scholar 

  24. Johnson M, Luukinen B, Buhl K, Stone D (2010) Deltamethrin technical fact sheet. National Pesticide Information Center, Oregon State University Extension Services. http://npic.orst.edu/factsheets/archive/Deltatech.html

  25. Kehat M, Gordon D (1975) Mating, longevity, fertility and fecundity of the cotton leaf-worm, Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidea). Phytoparasitica 3:87–102

    Article  Google Scholar 

  26. Khafagi WE, Hegazi EM, Aamer NA (2016) Effects of temperature on the development, food consumption and utilization parameters of the last two larval instars of Spodoptera littoralis (Boisd.). J Agric Sci Technol 2:93–99

    Google Scholar 

  27. Köhler HR, Triebskorn R (2013) Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science 341:759–765. https://doi.org/10.1126/science.1237591

    CAS  Article  Google Scholar 

  28. Kraikrathok C, Ngamsaeng S, Bullangpoti V, Pluempanupat W, Koul O (2013) Bio efficacy of some Piperaceae plant extracts against Plutella xylostella L. (Lepidoptera: Plutellidae). Comm Appl Biol Sci 78:305–309

    CAS  Google Scholar 

  29. Lalouette L, Pottier MA, Wycke MA, Boitard C, Bozzolan F, Maria A, Demondion E, Chertemps T, Lucas P, Renault D, Maibeche M, Siaussat D (2016) Unexpected effects of sublethal doses of insecticide on the peripheral olfactory response and sexual behavior in a pest insect. Environ Sci Pollut R 23:3073–3085. https://doi.org/10.1007/s11356-015-5923-3

    CAS  Article  Google Scholar 

  30. 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. https://doi.org/10.1046/j.1570-7458.1998.00392.x

    CAS  Article  Google Scholar 

  31. Legendre S, Clobert J (1995) ULM, a software for conservation and evolutionary biologists. J Appl Stat 22:817–834

    Article  Google Scholar 

  32. Metcalf CJE, Pavard S (2007) Why evolutionary biologists should be demographers. Trends Ecol Evol 22:205–212. https://doi.org/10.1016/j.tree.2006.12.001

    Article  Google Scholar 

  33. Miles M, Lysandrou M (2002) Evidence for negative cross resistance to insecticides in field collected Spodoptera littoralis (Boisd.) from Lebanon in laboratory bioassays. Meded Rijksuniv Gent Fak Landbouwkd Toegep Biol Wet 67:665–669

    CAS  Google Scholar 

  34. Moe SJ, De Schamphelaere K, Clements WH, Sorensen MT, Van den Brink PJ, Liess M (2013) Combined and interactive effects of global climate change and toxicants on populations and communities. Environ Toxicol Chem 32:49–61. https://doi.org/10.1002/etc.2045

    CAS  Article  Google Scholar 

  35. Riskallah MR (1980) Reduced sensitivity of cholinesterase as a factor of resistance in leptophos selected strain in the Egyptian cotton leafworm. J Environ Sci Heal B 15:181–192

    CAS  Article  Google Scholar 

  36. Riskallah MR (1984) Influence of posttreatment temperature on the toxicity of pyrethroid insecticides to susceptible and resistant larvae of the Egyptian cotton leafworm, Spodoptera littoralis (Boisd.). Experientia 40:188–190

    CAS  Article  Google Scholar 

  37. Sharma N, Banerjee H, Pal S, Sharma KK (2018) Persistence of thiacloprid and deltamethrin residues in tea grown at different locations of North-East India. Food Chem 253:88–92. https://doi.org/10.1016/j.foodchem.2018.01.132

    CAS  Article  Google Scholar 

  38. Sinclair BJ, Marshall KE, Sewell MA, Levesque DL, Willett CS, Slotsbo S, Dong Y, Harley CDG, Marshall DJ, Helmuth BS, Huey RB (2016) Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures? Ecol Lett 19:1372–1385. https://doi.org/10.1111/ele.12686

    Article  Google Scholar 

  39. Soderlund DM (2004) Pyrethroids and sodium channels. In: Beadle DJ, Mellor IR, Usherwood PNR (eds) Neurotox’ 03: neurotoxicological targets from functional genomics and proteomics. Society of Chemical Industry, London, p 79e86

    Google Scholar 

  40. Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  41. WHO (1989) Deltamethrin health and safety guide N°30. IPCS International Programme On Chemical Safety. World Health Organization, Geneva, ISBN 924154351 5

  42. Yang ZH, Du JW (2003) Effects of sublethal deltamethrin on the chemical communication system and PBAN activity of Asian corn borer, Ostrinia furnacalis (Güenee). J Chem Ecol 29:1611–1619 https://doi-org.inee.bib.cnrs.fr/10.1023/A:1024222830332

    CAS  Article  Google Scholar 

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This research was supported by the CNRS (PEPS FaiDoRA).

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Correspondence to David Siaussat.

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Malbert-Colas, A., Drozdz, T., Massot, M. et al. Effects of low concentrations of deltamethrin are dependent on developmental stages and sexes in the pest moth Spodoptera littoralis. Environ Sci Pollut Res 27, 41893–41901 (2020). https://doi.org/10.1007/s11356-020-10181-9

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Keywords

  • Pesticide
  • Low-dose effect
  • Hormesis
  • Population growth rate
  • Projection models
  • Crop insect pest