Abstract
Stable flies (Stomoxys calcitrans Linnaeus, 1758) can have a considerable negative impact on animal well-being, health, and productivity. Since insecticides constitute the mainstay for their control, this study aimed at assessing the occurrence of insecticide resistance in S. calcitrans on dairy farms in Brandenburg, Germany. First, the susceptibility of stable flies from 40 dairy farms to a deltamethrin-impregnated fabric was evaluated using the FlyBox® field test method. Then, S. calcitrans strains from 10 farms were reared in the laboratory, and the offspring was tested against the adulticides deltamethrin and azamethiphos and the larvicides cyromazine and pyriproxyfen. The FlyBox® method indicated 100% resistance in stable flies against deltamethrin. Later, to the offspring of those 10 established laboratory strains previously caught on suspected dairy farms, these field findings could be confirmed with mortalities well below 90% 24 h following topical application of the calculated LD95 of deltamethrin and azamethiphos. The ten strains could therefore be classified as resistant to the tested insecticides. In contrast, exposure to the insect growth regulators cyromazine and pyriproxyfen at their recommended concentrations demonstrated 100% efficacy. Both larvicides inhibited the moulting process of the stable fly larval stages completely, showing that the stable fly strains tested were susceptible to them. The intensive use of insecticides in recent decades has probably promoted the development of insecticide resistance. Systematic surveys in different livestock production systems and vigilance are therefore deemed necessary for estimating the risk of insecticide resistance development on a nationwide scale.
Similar content being viewed by others
References
Abbott W (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267
Acevedo GR, Zapater M, Toloza AC (2009) Insecticide resistance of house fly, Musca domestica (L.) from Argentina. Parasitol Res 105:489–493
Baldacchino F, Muenworn V, Desquesnes M, Desoli F, Charoenviriyaphap T, Duvallet G (2013) Transmission of pathogens by Stomoxys flies (Diptera, Muscidae): a review. Parasite p. 20-26
Bell HA, Robinson KA, Weaver RJ (2010) First report of cyromazine resistance in a population of UK house fly (Musca domestica) associated with intensive livestock production. Pest Manag Sci 66:693–695
Berry I, Stage D, Campbell J (1983) Populations and economic impacts of stable flies on cattle. Trans ASAE 26:873–0877
Bisset J, Rodriguez M, Soca A, Pasteur N, Raymond M (1997) Cross-resistance to pyrethroid and organophosphorus insecticides in the southern house mosquito (Diptera: Culicidae) from Cuba. J Med Entomol 34:244–246
Catangui MA, Campbell JB, Thomas GD, Boxler DJ (1993) Average daily gains of Brahman-crossbred and English× exotic feeder heifers exposed to low, medium, and high levels of stable flies (Diptera: Muscidae). J Econ Entomol 86:1144–1150
Cruz-Vázquez C, García-Vázquez Z, Fernández-Ruvalcaba M, George JE (2005) Susceptibilidad de Stomoxys calcitrans (L.) a la permetrina en establos lecheros de Aguascalientes, México Susceptibility of Stomoxys calcitrans (L.) to permethrin in dairy farms of Aguascalientes, Mexico. Facultad de Medicina Veterinaria y Zootecnia, UNAM 36, 4
Devonshire AL, Moores GD (1982) A carboxylesterase with broad substrate specificity causes organophosphorus, carbamate and pyrethroid resistance in peach-potato aphids (Myzus persicae). Pestic Biochem Physiol 18:235–246
DeVries D, Georghiou G (1980) A wide spectrum of resistance to pyrethroid insecticides in Musca domestica. Cell Mol Life Sci 36:226–227
Dougherty C, Knapp F, Burrus P, Willis D, Burg J, Cornelius P, Bradley N (1993) Stable flies (Stomoxys calcitrans L.) and the behavior of grazing beef cattle. Appl Anim Behav Sci 35:215–233
Geden CJ, Moon RD (2009) Host ranges of gregarious muscoid fly parasitoids: Muscidifurax raptorellus (Hymenoptera: Pteromalidae), Tachinaephagus zealandicus (Hymenoptera: Encyrtidae), and Trichopria nigra (Hymenoptera: Diapriidae). Environ Entomol 38:700–707
Hildebrand J (2017) Vorkommen und Verbreitung von Insektizidresistenzen bei Fliegen (Musca domestica) in Schweinehaltungen im Bundesland Schleswig-Holstein. Freie Universität Berlin, Deutschland
Imai C (1987) Control of insecticide resistance in a field population of houseflies, Musca domestica, by releasing susceptible flies. Res Popul Ecol 29:129–146
Jandowsky A, Clausen P-H, Schein E, Bauer B (2010) Vorkommen und Verbreitung von Insektizidresistenzen bei Fliegen (Musca domestica) in Milchviehbetrieben im Bundesland Brandenburg, Deutschland. Der Praktische Tierarzt 91:590–598
Keiding J (1999) Review of the global status and recent development of insecticide resistance in field populations of the housefly, Musca domestica (Diptera: Muscidae). Bull Entomol Res 89:69
Kirchner T, Liebrich S (2017) EU-Kommission will für Bienen schädliche Pflanzenschutzmittel verbieten. In Süddeutsche Zeitung
Kristensen M, Spencer AG, Jespersen JB (2001) The status and development of insecticide resistance in Danish populations of the housefly Musca domestica L. Pest Manag Sci 57:82–89
Liu N, Yue X (2000) Insecticide resistance and cross-resistance in the house fly (Diptera: Muscidae). J Econ Entomol 93:1269–1275
Lysyk T, Kalischuk-Tymensen L, Rochon K, Selinger L (2010) Activity of Bacillus thuringiensis isolates against immature horn fly and stable fly (Diptera: Muscidae). J Econ Entomol 103:1019–1029
Marçon PC, Thomas GD, Siegfried BD, Campbell JB (1997) Susceptibility of stable flies (Diptera: Muscidae) from southeastern Nebraska beef cattle feedlots to selected insecticides and comparison of 3 bioassay techniques. J Econ Entomol 90:293–298
Patterson R, LaBrecque G, Williams D, Weidhaas D (1981) Control of the stable fly, Stomoxys calcitrans (Diptera: Muscidae), on St. Croix, US Virgin Islands, using integrated pest management measures: III. Field techniques and population control. J Med Entomol 18:203–210
Pinto MC, Prado APd (2001) Resistance of Musca domestica L. populations to cyromazine (insect growth regulator) in Brazil. Mem Inst Oswaldo Cruz 96:729–732
Pospischil R, Szomm K, Londershausen M, Schröder I, Turberg A, Fuchs R (1996) Multiple resistance in the larger house fly Musca domestica in Germany. Pest Manag Sci 48:333–341
Salem A, Bouhsira E, Emmanuel Liénard D (2012) Susceptibility of two European strains of Stomoxys calcitrans (L.) to cypermethrin, deltamethrin, fenvalerate, λ-cyhalothrin, permethrin and phoxim. International Journal of Applied Research in Veterinary Medicine 10(3):249-257
Schaub L, Sardy S, Capkun G (2002) Natural variation in baseline data: when do we call a new sample ‘resistant’? Pest Manag Sci 58:959–963
Scott JG, Alefantis TG, Kaufman PE, Rutz DA (2000) Insecticide resistance in house flies from caged-layer poultry facilities. Pest Manag Sci 56:147–153
Sfara V, Zerba EN, Alzogaray RA (2006) Toxicity of pyrethroids and repellency of diethyltoluamide in two deltamethrin-resistant colonies of Triatoma infestans Klug, 1834 (Hemiptera: Reduviidae). Mem Inst Oswaldo Cruz 101:89–94
Shah RM, Abbas N, Shad SA, Varloud M (2015a) Inheritance mode, cross-resistance and realized heritability of pyriproxyfen resistance in a field strain of Musca domestica L. (Diptera: Muscidae). Acta Trop 142:149–155
Shah RM, Shad SA, Abbas N (2015b) Mechanism, stability and fitness cost of resistance to pyriproxyfen in the house fly, Musca domestica L. (Diptera: Muscidae). Pestic Biochem Physiol 119:67–73
Skovgård H, Jespersen J (1999) Activity and relative abundance of hymenopterous parasitoids that attack puparia of Musca domestica and Stomoxys calcitrans (Diptera: Muscidae) on confined pig and cattle farms in Denmark. Bull Entomol Res 89:263–269
Sømme L (1958) The number of stable flies in Norwegian barns, and their resistance to DDT. J Econ Entomol 51:599–601
Taylor DB, Moon RD, Mark DR (2012) Economic impact of stable flies (Diptera: Muscidae) on dairy and beef cattle production. J Med Entomol 49:198–209
WHO (2016) Test procedures for insecticide resistance monitoring in malaria vector mosquitoes. World Health Organization
Acknowledgments
The authors wish to gratefully thank Dr. Kai Sievert for providing a pyriproxyfen sample and MSD Animal Health Innovation GmbH for showing their stable fly breeding system and for providing Stomoxys calcitrans pupae. They also wish to express their gratitude towards the Federal Environment Office (UBA) for showing their breeding system and the topical application and for providing stable fly pupae; Prof. Dr. Uwe Rösler for supplying a test laboratory; and Dr. Jürgen Krücken, Dr. Roswitha Merle, and Peggy Hoffmann-Köhler for their support during this study.
Funding
S. Reissert benefitted from a grant of the Federal Office of Consumer Protection and Food Safety (BVL, Berlin, Germany) during her study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Additional information
Section Editor: Helge Kampen
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This paper is an excerpt of the doctoral thesis with the title “Occurrence and distribution of insecticide resistance in stable flies (Stomoxys calcitrans) on dairy farms in the Federal State of Brandenburg, Germany” written by Sophia Reissert.
Rights and permissions
About this article
Cite this article
Reissert-Oppermann, S., Bauer, B., Steuber, S. et al. Insecticide resistance in stable flies (Stomoxys calcitrans) on dairy farms in Germany. Parasitol Res 118, 2499–2507 (2019). https://doi.org/10.1007/s00436-019-06400-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-019-06400-z