, Volume 59, Issue 5, pp 503–511

Sublethal effects of chlorantraniliprole and thiamethoxam seed treatments when Lysiphlebus testaceipes feed on sunflower extrafloral nectar

  • Valéria F. Moscardini
  • Pablo C. Gontijo
  • J. P. Michaud
  • Geraldo A. Carvalho


The extrafloral nectar (EFN) of sunflower, Helianthus annuus L., is an important summer resource for many insects and represents a potential route of exposure to systemic insecticides applied as seed treatments to cultivated varieties. Among the many parasitoids that utilize sunflower EFN, Lysiphlebus testaceipes (Cresson) (Hymenoptera: Braconidae) is an important generalist parasitoid of cereal aphids in North America. This study evaluated the performance of adult wasps fed EFN of sunflower plants grown from seed treated with chlorantraniliprole and thiamethoxam. Consumption of EFN from treated sunflower seedings caused no lethal effects, but reduced the numbers of greenbug nymphs, Schizaphis graminum Rondani, attacked and parasitized when wasps foraged in Petri dish arenas. Whereas control females self-superparasitized every fourth host, those exposed to chlorantraniliprole did not. Offspring developmental time and adult emergence were unaffected by either treatment, but thiamethoxam greatly reduced the proportion of female offspring.


Conservation biological control Ecotoxicology Lysiphlebus testaceipes (Hymenoptera: Braconidae) Schizaphis graminum Systemic insecticides 


  1. Albajes R, López C, Pons X (2003) Predatory fauna in cornfields and response to imidacloprid seed treatment. J Econ Entomol 96:1805–1813PubMedCrossRefGoogle Scholar
  2. Al-Deeb MA, Wilde GE, Zhu KY (2001) Effect of insecticides used in corn, sorghum, and alfalfa on the predator Orius insidiosus (Hemiptera: Anthocoridae). J Econ Entomol 94:1353–1360PubMedCrossRefGoogle Scholar
  3. Bai B, Mackauer M (1992) Influence of superparasitism on development rate and adult size in a solitary parasitoid wasp, Aphidius ervi. Func Ecol 6:302–307CrossRefGoogle Scholar
  4. Baker I, Baker HG (1979) Chemical constituents of the nectars of two Erythrina species and their hybrid. Ann Mo Bot Gard 66:446–450CrossRefGoogle Scholar
  5. Baker HG, Opler PA, Baker I (1978) A comparison of amino-acid complements of floral and extrafloral nectars. Bot Gaz 139:322–332CrossRefGoogle Scholar
  6. Brewer MJ, Noma T, Elliott NC, Kravchenko AN, Hild AL (2008) A landscape view of cereal aphid parasitoid dynamics reveals sensitivity to farm- and region-scale vegetation structure. Eur J Entomol 105:503–511CrossRefGoogle Scholar
  7. Caccia S, Grimaldi A, Casartelli M, Falabella P, de Eguileor M, Pennacchio F, Giordana B (2012) Functional analysis of a fatty acid binding protein produced by Aphidius ervi teratocytes. J Insect Physiol 58:621–627PubMedCrossRefGoogle Scholar
  8. Casida JE (2011) Neonicotinoid metabolism: compounds, substituents, pathways, enzymes, organisms, and relevance. J Agric Food Chem 59:2923–2931PubMedCrossRefGoogle Scholar
  9. Charlet LD, Gavloski J (2011) Insects of sunflower in the Northern Great Plains of North America. In: Floate KD (ed) Arthropods of canadian grasslands: inhabitants of a changing landscape, vol 2. Biological Survey of Canada, pp 159–178Google Scholar
  10. Cloyd RA, Bethke JA (2011) Impact of neonicotinoid insecticides on natural enemies in greenhouse and interiorscape environments. Pest Manag Sci 67:3–9PubMedCrossRefGoogle Scholar
  11. Cordova D, Benner EA, Sacher MD, Rauh JJ, Sopa JS, Lahm GP, Selby TP, Stevenson TM, Flexner L, Gutteridge S, Rhoades DF, Wu L, Smith RM, Tao Y (2006) Anthranilic diamides: A new class of insecticides with a novel mode of action, ryanodine receptor activation. Pestic Biochem Phys 84:196–214CrossRefGoogle Scholar
  12. Delpuech JM, Bardon C, Boulétreau M (2005) Increase of the behavioral response to kairomones by the parasitoid wasp Leptopilina heterotoma surviving insecticides. Arch Environ Con Tox 49:186–191CrossRefGoogle Scholar
  13. Deng YX, Tsai JH (1998) Development of Lysiphlebia japonica (Hymenoptera: Aphidiidae), a parasitoid of Toxoptera citricida (Homoptera: Aphididae) at five temperatures. Fla Entomol 81:415–423CrossRefGoogle Scholar
  14. Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106PubMedCrossRefGoogle Scholar
  15. Dyer LE, Landis DA (1996) Effects of habitat, temperature, and sugar availability on longevity of Eriborus terebrans (Hymenoptera: Ichneumonidae). Environ Entomol 25:1192–1201Google Scholar
  16. Falabella P, Tremblay E, Pennacchio F (2000) Host regulation by the aphid parasitoid Aphidius ervi: the role of teratocytes. Entomol Exp Appl 97:1–9CrossRefGoogle Scholar
  17. Garcia P (2011) Sublethal effects of pyrethroids on insect parasitoids: what we need to further know. In: Stoytcheva M (ed) Pesticides—formulations, effects, fate. InTech, Rijeka, Croatia, pp 477–494Google Scholar
  18. Giles KL, Jones DB, Royer TA, Elliott NC, Kindler SD (2003) Development of a sampling plan in winter wheat that estimates cereal aphid parasitism levels and predicts population suppression. J Econ Entomol 96:975–982PubMedCrossRefGoogle Scholar
  19. Girolami V, Mazzon L, Squartini A, Mori N, Marzaro M, Di bernardo A, Greatti M, Giorio C, Tapparo A (2009) Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: a novel way of intoxication for bees. J Econ Entomol 102:1808–1815PubMedCrossRefGoogle Scholar
  20. Goulson D (2013) Review: an overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50:977–987CrossRefGoogle Scholar
  21. Gurr GM, Scarratt SL, Wratten SD, Berndt L, Irvin NA (2004) Ecological engineering, habitat manipulation and pest management. In: Gurr GM, Wratten SD, Altieri MA (eds) Ecological engineering for pest management. Comstock Press, Ithaca, USA, pp 1–12Google Scholar
  22. Haynes KF (1988) Sublethal effects of neurotoxic insecticides on insect behavior. Annu Rev Entomol 33:149–168PubMedCrossRefGoogle Scholar
  23. Heimpel GE, Collier TR (1996) The evolution of host-feeding behaviour in insect parasitoids. Biol Rev 71:373–400CrossRefGoogle Scholar
  24. Heimpel GE, Rosenheim JA, Kattari D (1997) Adult feeding and lifetime reproductive success in the parasitoid Aphytis melinus. Entomol Exp Appl 83:305–315CrossRefGoogle Scholar
  25. Hopkinson JE, Zalucki MP, Murray DAH (2013) Host selection and parasitism behavior of Lysiphlebus testaceipes: role of plant, aphid species and instar. Biol Control 64:283–290CrossRefGoogle Scholar
  26. Hull L, Beers E (1985) Ecological selectivity: modifying chemical control practices to preserve natural enemies. In: Hoy MA, Herzog DC (eds) Biological control in agricultural IPM systems. Academic Press, New York, USA, pp 103–122CrossRefGoogle Scholar
  27. Hutchins SH (2010) Indifference analysis: a practical method to assess uncertainty in IPM decision making. J Integ Pest Manag 1:D1–D3CrossRefGoogle Scholar
  28. Jamont M, Crépellière S, Jaloux B (2013) Effect of extrafloral nectar provisioning on the performance of the adult parasitoid Diaeretiella rapae. Biol Control 65:271–277CrossRefGoogle Scholar
  29. Jones DB (2001) Natural enemy thresholds for greenbug, Schizaphis graminum Rondani, on winter wheat. Oklahoma State University, Stillwater, USAGoogle Scholar
  30. Kant R, Trewick SA, Sandanayaka WRM, Godfrey AJR, Minor MA (2012) Effects of multiple matings on reproductive fitness of male and female Diaeretiella rapae. Entomol Exp Appl 145:215–221CrossRefGoogle Scholar
  31. Kant R, Minor MA, Sandanayaka WRM, Trewick SA (2013) Effects of mating and oviposition delay on parasitism rate and sex allocation behaviour of Diaeretiella rapae (Hymenoptera: Aphidiidae). Biol Control 65:265–270CrossRefGoogle Scholar
  32. Komeza N, Fouillet P, Boulétreau M, Delpuech JM (2001) Modification, by the insecticide chlorpyrifos, of the behavioral response to kairomones of a parasitoid wasp, Leptopilina boulardi. Arch Environ Con Tox 41:436–442CrossRefGoogle Scholar
  33. Lahm GP, Stevenson TM, Selby TP, Freudenberger JH, Cordova D, Flexner L, Bellin CA, Dubas CM, Smith BK, Hughes KA, Hollingshaus JG, Clark CE, Benner EA (2007) Rynaxypyr: a new insecticidal anthranilic diamide that acts as a potent and selective ryanodine receptor activator. Bioorg Med Chem Lett 17:6274–6279PubMedCrossRefGoogle Scholar
  34. Lahm GP, Cordova D, Barry JD (2009) New and selective ryanodine receptor activators for insect control. Bioorg Med Chem 17:4127–4133PubMedCrossRefGoogle Scholar
  35. Laurent FM, Rathahao E (2003) Distribution of [14C] imidacloprid in sunflowers (Helianthus annuus L.) following seed treatment. J Agric Food Chem 51:8005–8010PubMedCrossRefGoogle Scholar
  36. Lewis WJ, Stapel JO, Cortesero AM, Takasu K (1998) Understanding how parasitoids balance food and host needs: importance to biological control. Biol Control 11:175–183CrossRefGoogle Scholar
  37. Li X, Degain BA, Harpold VS, Marcon PG, Nichols RL, Fournier AJ, Naranjo SE, Palumbo JC, Ellsworth PC (2012) Baseline susceptibilities of B- and Q-biotype Bemisia tabaci to anthranilic diamides in Arizona. Pest Manag Sci 68:83–91PubMedCrossRefGoogle Scholar
  38. Liu F, Bao SW, Song Y, Lu HY, Xu JX (2010) Effects of imidacloprid on the orientation behavior and parasitizing capacity of Anagrus nilaparvatae, an egg parasitoid of Nilaparvata lugens. BioControl 55:473–483CrossRefGoogle Scholar
  39. Liu F, Zhang X, Gui Q–Q, Xu Q-J (2012) Sublethal effects of four insecticides on Anagrus nilaparvatae (Hymenoptera: Mymaridae), an important egg parasitoid of the rice planthopper Nilaparvata lugens (Homoptera: Delphacidae). Crop Prot 37:13–19CrossRefGoogle Scholar
  40. Lundgren JG (2009) Relationships of natural enemies and non-prey foods. Springer, Dordrecht, The NetherlandsGoogle Scholar
  41. Mahi H, Rasekh A, Shishehbor P, Michaud JP (2014) The biology of Lysiphlebus fabarum (Braconidae, Aphidiinae) following cold storage of larvae and pupae under various thermal regimes. Entomol Exp Appl (in press)Google Scholar
  42. Maienfisch P, Angst M, Brandl F, Fischer W, Hofer D, Kayser H, Kobel W, Rindlisbacher A, Senn R, Steinemann A, Widmer HR (2001) Chemistry and biology of thiamethoxam: a second generation neonicotinoid. Pest Manag Sci 57:901–913Google Scholar
  43. Matin SB, Sahragard A, Rasoolian G (2009) Some biological parameters of Lysiphlebus fabarum (Hymenoptera: Aphidiidae) a parasitoid of Aphis fabae (Homoptera: Aphidiidae) under labaratory conditions. Munis Entomol Zool 4:193–200Google Scholar
  44. McAllister MK, Roitberg BD (1987) Adaptive suicidal behavior in pea aphids. Nature 328:797–799CrossRefGoogle Scholar
  45. Michaud JP, Mackauer M (1995) Oviposition behavior of Monoctonus paulensis (Hymenoptera: Aphidiidae): factors influencing reproductive allocation to hosts and host patches. Ann Entomol Soc Am 88:220–226Google Scholar
  46. Moser SE, Obrycki JJ (2009) Non-target effects of neonicotinoid seed treatments; mortality of coccinellid larvae related to zoophytophagy. Biol Control 51:487–492CrossRefGoogle Scholar
  47. Nauen R (2006) Insecticide mode of action: return of the ryanodine receptor. Pest Manag Sci 68:690–692CrossRefGoogle Scholar
  48. Naveed M, Salam A, Saleem MA, Rafiq M, Hamza A (2010) Toxicity of thiamethoxam and imidacloprid as seed treatments to parasitoids associated to control Bemisia tabaci. Pak J Zool 42:559–565Google Scholar
  49. Nicolson S, Nepi I, Pacini E (2007) Nectaries and Nectar. Springer, Heidelberg, GermanyCrossRefGoogle Scholar
  50. Nuyttens D, Devarrewaere W, Verboven P, Foque D (2013) Pesticide-laden dust emission and drift from treated seeds during seed drilling: a review. Pest Manag Sci 69:564–575PubMedCrossRefGoogle Scholar
  51. Olson DM, Andow DA (1998) Larval crowding and adult nutrition effects on longevity and fecundity of female Trichogramma nubilale Ertle & Davis (Hymenoptera: Trichogrammatidae). Environ Entomol 27:507–512Google Scholar
  52. Pacini E, Nepi M, Vesprini JL (2003) Nectar biodiversity: a short review. Plant Syst Evol 238:7–21Google Scholar
  53. Paine TD, Hanlon CC, Byrne FJ (2011) Potential risks of systemic imidacloprid to parasitoid natural enemies of a cerambycid attacking Eucalyptus. Biol Control 56:175–178CrossRefGoogle Scholar
  54. Pemberton RW, Lee JH (1996) The influence of extrafloral nectaries on parasitism of an insect herbivore. Am J Bot 83:1187–1194CrossRefGoogle Scholar
  55. Pike KS, Stary P, Miller T, Graf G, Allison D, Boyd-ston L, Miller R (2000) Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of northwest USA. Proc Entomol Soc Wash 102:688–740Google Scholar
  56. Prabhaker N, Castle SJ, Naranjo SE, Toscano NC, Morse JG (2011) Compatibility of two systemic neonicotinoids, imidacloprid and thiamethoxam, with various natural enemies of agricultural pests. J Econ Entomol 104:773–781PubMedCrossRefGoogle Scholar
  57. Rogers CE (1985) Extrafloral nectar: ecological implications. Bull Entomol Soc Am 31:15–20Google Scholar
  58. Rose USR, Lewis J, Tumlinson JH (2006) Extrafloral nectar from cotton (Gossypium hirsutum) as a food source for parasitic wasps. Funct Ecol 20:67–74CrossRefGoogle Scholar
  59. Royer TA, Walgenbach DD (1991) Predacious arthropods of cultivated sunflower in Eastern South Dakota. J Kansas Entomol Soc 64:112–116Google Scholar
  60. SAS Institute (2008) SAS for windows version 9.0. SAS Institute, Cary, USAGoogle Scholar
  61. Seagraves MP, Lundgren JG (2012) Effects of neonicitinoid seed treatments on soybean aphid and its natural enemies. J Pest Sci 85:125–132CrossRefGoogle Scholar
  62. Sigsgaard S (2000) The temperature-dependent duration of development and parasitism of three cereal aphid parasitoids, Aphidius ervi, A. rhopalosiphi, and Praon volucre. Entomol Exp Appl 95:173–184CrossRefGoogle Scholar
  63. Srivastava M, Singh R (1995a) Sex ratio adjustment by a koinobiotic parasitoid Lysiphlebus delhiensis (Subba Rao & Sharma) (Hymenoptera: Aphidiidae) in response to host size. Biol Agric Hort 12:15–28CrossRefGoogle Scholar
  64. Srivastava M, Singh R (1995b) Influence of age of parents Lysiphlebus delhiensis (Subba Rao and Sharma) (Hym., Aphidiidae) during copulation on progeny production and offspring sex ratio. J Appl Entomol 119:72–77Google Scholar
  65. Stapel JO, Cortesero AM, De Moraes CM, Tumlinson JH, Lewis WJ (1997) Extrafloral nectar, honeydew, and sucrose effects on searching behavior and efficiency of Microplitis croceipes (Hymenoptera: Braconidae) in cotton. Environ Entomol 26:617–623Google Scholar
  66. Stern VM, Smith RF, van den Bosch R, Hagen KS (1959) The integrated control concept. Hilgardia 29:81–101Google Scholar
  67. Taylor AG, Eckenrode CJ, Straub RW (2001) Seed coating technologies and treatments for onion: challenges and progress. HortScience 36:199–205Google Scholar
  68. Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol 45:247–268CrossRefGoogle Scholar
  69. Waage JK (1986) Family planning in parasitoids: adaptive patterns of progeny and sex allocation. In: Waage JK, Greathead D (eds) Insect parasitoids. Academic Press, London, UK, pp 63–95Google Scholar
  70. Zhang JH, Gu LQ, Wang CZ (2010) Superparasitism behavior and host discrimination of Campoletis chlorideae (Ichneumonidae: Hymenoptera) toward Mythimna separata (Noctuidae: Lepidoptera). Environ Entomol 39:1249–1254PubMedCrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2014

Authors and Affiliations

  • Valéria F. Moscardini
    • 1
    • 2
  • Pablo C. Gontijo
    • 1
    • 2
  • J. P. Michaud
    • 2
  • Geraldo A. Carvalho
    • 1
  1. 1.Department of EntomologyFederal University of LavrasLavrasBrazil
  2. 2.Department of Entomology, Agricultural Research Center-HaysKansas State UniversityHaysUSA

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