Advertisement

Autodissemination of pyriproxyfen as a method for controlling the house fly Musca domestica

  • Haim BialeEmail author
  • Elad Chiel
  • Christopher J. Geden
Original Paper
  • 17 Downloads

Abstract

House fly (Musca domestica) control is a major challenge in animal agriculture. Here, we tested the feasibility of applying pyriproxyfen (PPF), an insect-growth regulator that controls house flies effectively, using autodissemination methods, in which the flies themselves deliver PPF to their oviposition sites. First, we tried baiting gravid female flies to walk-through stations, where flies would self-treat with PPF and distribute it. This concept worked well in laboratory and indoor cage experiments, but not in the field, as flies appeared reluctant to alight on and collect PPF. Therefore, we tested a different concept of actively coating flies with PPF and then releasing them in different proportions. This concept was tested in laboratory experiments with various manure types in the USA and in Israel. Twenty percent of PPF-coated flies (corresponding to ≥ 2.3 mg/kg PPF) were sufficient to get high control levels (~ 90%) in most of the tested manure types in the US study. Very similar results were obtained in the experiments in Israel but only with poultry manure, whereas low control levels were obtained when cow manure was used. We conclude that autodissemination of PPF using the collect–treat–release “active coating” concept may be practical, depending on manure type, and should be further tested in the field.

Keywords

Insect-growth regulator Integrated pest management Animal manure 

Notes

Acknowledgements

We thank Mr. Andy Resnick (Agan-Adama, Israel) for supplying us with technical PPF (on the Israeli side). Author CJG thanks Dana Johnson and Roxie White for assisting with the bioassays in the USA. The research was supported by the United States—Israel Binational Agricultural Research and Development Fund (BARD), Grant # 4701-14R to CJG and EC.

Compliance with ethical standards

Conflict of interest

All authors declare they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

10340_2019_1092_MOESM1_ESM.docx (39 kb)
Supplementary material 1 (DOCX 38 kb)

References

  1. Akhoundi M, Jourdain F, Chandre F, Delaunay P, Roiz D (2018) Effectiveness of a field trap barrier system for controlling Aedes albopictus: a “removal trapping” strategy. Parasit vectors 11:101CrossRefGoogle Scholar
  2. Baxter IH, Howard N, Armsworth CG, Barton LE, Jackson C (2008) The potential of two electrostatic powders as the basis for an autodissemination control method of Plodia interpunctella (Hübner). J Stored Prod Res 44:152–161CrossRefGoogle Scholar
  3. Bensebaa F, Kilani-Morakchi S, Aribi N, Soltani N (2015) Evaluation of pyriproxyfen, a juvenile hormone analog, on Drosophila melanogaster (Diptera: Drosophilidae): insecticidal activity, ecdysteroid contents and cuticle formation. Eur J Entomol 112:625–631CrossRefGoogle Scholar
  4. Biale H, Geden CJ, Chiel E (2017) Effects of pyriproxifen on wild populations of the house fly, Musca domestica, and compatibility with its principal parasitoids. Pest Manag Sci 73:2456–2464CrossRefGoogle Scholar
  5. Caputo B, Ienco A, Cianci D, Pombi M, Petrarca V, Baseggio A, Devine GJ, Della Torre A (2012) The “auto-dissemination” approach: a novel concept to fight Aedes albopictus in urban areas. PLoS Negl Trop Dis.  https://doi.org/10.1371/journal.pntd.0001973 Google Scholar
  6. Devine GJ, Perea EZ, Killeen GF, Stancil JD, Clark SJ, Morrison AC (2009) Using adult mosquitoes to transfer insecticides to Aedes aegypti larval habitats. Proc Natl Acad Sci U S A 106:11530–11534CrossRefGoogle Scholar
  7. Dowd PF, Vega FE (2003) Autodissemination of Beauveria bassiana by sap beetles (Coleoptera: Nitidulidae) to overwintering sites. Biocontrol Sci Technol 13:65–75CrossRefGoogle Scholar
  8. Durel L, Estrada-Peña A, Franc M, Mehlhorn H, Bouyer J (2015) Integrated fly management in European ruminant operations from the perspective of directive 2009/128/EC on sustainable use of pesticides. Parasitol Res 114:379–389CrossRefGoogle Scholar
  9. El-Sufty R, Al Bgham S, Al-Awash S, Shahdad A, Al Bathra A (2011) A trap for auto-dissemination of the entomopathogenic fungus Beauveria bassiana by red palm weevil adults in date palm plantations. Egypt J Biol Pest Control 21:271–276Google Scholar
  10. Farkas R, Hogsette J, Papp L, Darvas B (2000) Control possibilities of filth-breeding flies in livestock and poultry production. Man Palearct Diptera 1:889–904Google Scholar
  11. Furlong MJ, Pell JK, Choo OP, Rahman SA (1995) Field and laboratory evaluation of a sex pheromone trap for the autodissemination of the fungal entomopathogen Zoophthora radicans (Entomophthorales) by the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Bull Entomol Res 85:331–337CrossRefGoogle Scholar
  12. Gaugler R, Suman D, Wang Y (2012) An autodissemination station for the transfer of an insect growth regulator to mosquito oviposition sites. Med Vet Entomol 26:37–45CrossRefGoogle Scholar
  13. Geden CJ, Devine GJ (2012) Pyriproxyfen and house flies (Diptera: Muscidae): effects of direct exposure and autodissemination to larval habitats. J Med Entomol 49:606–613CrossRefGoogle Scholar
  14. Geden CJ, Hogsette JA (2001) Research and extension needs for integrated pest management for arthropods of veterinary importance. In: Proceedings of a workshop in Lincoln, Nebraska. http://digitalcommons.unl.edu/usdaarsfacpub/1039/. Accessed Mar 2018
  15. Ishaaya I, Degheele D (1998) Insecticides with novel modes of action: an overview. In: Ishaaya I, Degheele D (eds) Insecticides with novel modes of action mechanisms and application, 1st edn. Springer, Berlin, Heidelberg, New York, pp 1–24CrossRefGoogle Scholar
  16. Kasai S, Sun H, Scott JG (2017) Diversity of knockdown resistance alleles in a single house fly population facilitates adaptation to pyrethroid insecticides. Insect Mol Biol 26:13–24CrossRefGoogle Scholar
  17. Kaufman PE, Nunez SC, Mann RS, Geden CJ, Scharf ME (2010) Nicotinoid and pyrethroid insecticide resistance in houseflies (Diptera: Muscidae) collected from Florida dairies. Pest Manag Sci 66:290–294CrossRefGoogle Scholar
  18. Khan HAA, Shad SA, Akram W (2013) Resistance to new chemical insecticides in the house fly, Musca domestica L., from dairies in Punjab, Pakistan. Parasitol Res 112:2049–2054CrossRefGoogle Scholar
  19. Klein MG, Lacey LA (1999) An attractant trap for autodissemination of entomopathogenic fungi into populations of the Japanese beetle Popillia japonica (Coleoptera: Scarabaeidae). Biocontrol Sci Technol 9:151–158CrossRefGoogle Scholar
  20. Liu H, Wang P, Zhou Z, Liu D (2017) Enantioselective dissipation of pyriproxyfen in soils and sand. Chirality 29:358–368CrossRefGoogle Scholar
  21. Malik A, Singh N, Satya S (2007) House fly (Musca domestica): a review of control strategies for a challenging pest. J Environ Sci Health Part B 42:453–469CrossRefGoogle Scholar
  22. Moslim R, Kamarudin N, Wahid MB (2011) Trap for the auto dissemination of Metarhizium Anisopliae in the management of rhinoceros beetle, Oryctes Rhinoceros. J Oil Palm Res 23:111–117Google Scholar
  23. Sanchez-Arroyo, H, Capinera JL (2014) House fly, Musca domestica Linnaeus. Dissertation, University of FloridaGoogle Scholar
  24. Scott JG (2017) Evolution of resistance to pyrethroid insecticides in Musca domestica. Pest Manag Sci 73:716–722CrossRefGoogle Scholar
  25. Scott JG, Leichter CA, Rinkevihc FD, Harris SA, Su C, Aberegg LC, Moon R, Geden CJ, Gerry AC, Taylor DB, Byford RL, Watson W, Johnson G, Boxler D, Zurek L (2013) Insecticide resistance in house flies from the United States: resistance levels and frequency of pyrethroid resistance alleles. Pest Biochem Physiol 107:377–384CrossRefGoogle Scholar
  26. Shiell J (2015) Manure characteristics affecting the management of house fly (Musca domestica L.) populations in duck production facilities. Dissertation, University of GuelphGoogle Scholar
  27. Sullivan JJ, Goh KS (2008) Environmental fate of pyriproxyfen. J Pestic Sci 33:339–350CrossRefGoogle Scholar
  28. Swale RD, Li Z, Kraft ZJ, Healy K, Liu M, David MC, Liu Z, Foil DL (2018) Development of an autodissemination strategy for the deployment of novel control agents targeting the common malaria mosquito, Anopheles quadrimaculatus say (Diptera: Culicidae). PLoS Negl Trop Dis.  https://doi.org/10.1371/journal.pntd.0006259 Google Scholar
  29. Tunaz H (2004) Insect growth regulators for insect pest control. Turk J Agric For 28:377–387Google Scholar
  30. Tuten HC, Moosmann P, Mathis A, Schaffner F (2016) Effects of pyriproxifen on Aedes japonicus development and its auto-dissemination by gravid females in laboratory trials. J Am Mosq Control Assoc 32:55–58CrossRefGoogle Scholar
  31. Unlu I, Suman DS, Wang Y, Klingler K, Faraji A, Gaugler R (2017) Effectiveness of autodissemination stations containing pyriproxyfen in reducing immature Aedes albopictus populations. Parasit Vectors.  https://doi.org/10.1186/s13071-017-2034-7 Google Scholar
  32. Vickers RA, Furlong MJ, White A, Pell JK (2004) Initiation of fungal epizootics in diamondback moth populations within a large field cage: proof of concept for auto-dissemination. Emtomol Exp Appl 111:7–17CrossRefGoogle Scholar
  33. Wang Y, Suman DS, Bertrand J, Dong L, Gaugler R (2014) Dual-treatment autodissemination station with enhanced transfer of an insect growth regulator to mosquito oviposition sites. Pest Manag Sci 70:1299–1304CrossRefGoogle Scholar
  34. Zhukovskaya M, Yanagawa A, Forschler BT (2013) Grooming behavior as a mechanism of insect disease defense. Insects 4:609–630CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Evolutionary and Environmental BiologyUniversity of HaifaHaifaIsrael
  2. 2.Department of Biology and EnvironmentUniversity of Haifa-OranimQiryat TivonIsrael
  3. 3.Center for Medical, Agricultural, and Veterinary EntomologyUSDA, ARSGainesvilleUSA

Personalised recommendations