(Musca Domestica) from a Livestock Farm in Tyumen Region, Russia

Bulgarian Journal of Veterinary Medicine, 2017 ONLINE FIRST ISSN 1311-1477; DOI: 10.15547/bjvm.2027

Short communication

INSECTICIDE SUSCEPTIBILITY OF HOUSE FLIES (MUSCA DOMESTICA) FROM A LIVESTOCK FARM IN TYUMEN REGION, RUSSIA

M. A. LEVCHENKO, E. A. SILIVANOVA, G. F. BALABANOVA & R. H. BIKINYAEVA All-Russian Scientific Research Institute of Veterinary Entomology and Arachnology, Branch of Tyumen Scientific Centre, Siberian Branch of the Russian Academy of Sciences

Summary Levchenko, M. A., E. A. Silivanova, G. F. Balabanova & R. H. Bikinyaeva, 2017. Insecti- cide susceptibility of house flies (Musca domestica) from a livestock farm in Tyumen region, Russia. Bulg. J. Vet. Med. (online first).

The susceptibility of the field populations of the house fly Musca domestica L. (Diptera:Muscidae) from a livestock farm of the Tyumen region, Russia, to six insecticides (deltamethrin, cypermethrin, thiamethoxam, permethrin, fipronil, chlorfenapyr) is reported. After a forced contact of adult flies of susceptible strains and first generation of field populations with the residues of insecticides at the bottom of glass cups, the median lethal dose of each insecticide was determined by probit analysis. According to the resistance ratio, the susceptibility of the evaluated field population to insecticides increased in the order: cypermethrin < deltamethrin < permethrin ≤ chlorfenapyr < thiamethoxam < fipronil. Key words: field population, insecticides, Musca domestica L., resistance ratio, susceptibility

The house fly Musca domestica L. (Dip- using insecticides. In Russia, pyrethroid tera:Muscidae) is a typical representative and neonicotinoid insecticides are most of zoophilous flies that cause significant commonly used to combat ectoparasites of harm to the animals as ectoparasites and animals. Fipronil and chlorfenapyr are interfere with the work of the maintenance among the new classes of insecticides in staff. Flies disturb the animals, reduce the Russia. Fipronil is used in crop produc- sanitary condition of farms and animal tion, medical pest control (mainly in the feed, may be carriers of infectious and form of gels and baits to control cock- parasitic diseases of animals (Förster et roaches), in veterinary medicine for com- al., 2007; Wang et al., 2011; Scott et al., bating ectoparasites on small domestic 2014). The main method of house flies animals. Chlorfenapyr is a promising pyr- control worldwide is chemical control role insecticide to control the insect popu- Insecticide susceptibility of house flies (Musca domestica) from a livestock farm in Tyumen region, Russia lation. Chlorfenapyr, a pro-insecticide, has not been carried out for more than 10 a unique mechanism of insecticidal activi- years (Pavlov, 2006). ty connected to the ability of its metabo- For effective control of the number of lites to block the ATP synthesis in insect pests, including the housefly, it is neces- body cells (US EPA, 2001). In world sary to carry out monitoring of the level of practice, chlorfenapyr is mainly used in susceptibility in field populations to the crop production and termite control, it is used insecticides. The aim of this study promising as a means to control the ma- was to assess the susceptibility to insecti- laria vectors and other synanthrope insects cides of different groups in the M. domes- (N'Guessan et al., 2007; Romero et al., tica population from a livestock farm in 2010). It is not introduced widely in Rus- the Tyumen region, where pyrethroid in- sia and is mostly used for plant protection. secticides had been used for a long time. It is known that M. domestica quickly For the experiment, 3–5-day old labo- develops resistance to insecticides used ratory susceptible and field populations against it (Scott et al., 2013; Khan et al., adult flies were used. Field population of 2015). Previously, researchers reported on flies was collected in the facilities (pigger- the formation of house fly populations ies, cowsheds) of a livestock farm in the resistant to pyrethroids and neonicotinoids Tyumen region (Chervishevo village, on livestock and poultry farms around the 56°56′08″ N. 65°25′34″ E.). Then insects world (Marçon et al., 2003; Kaufman et were transferred in an insectarium and al., 2010; Khan et al., 2013; Scott et al., kept in cages made of metal frame 25 × 25 2013; Abbas et al.. 2015). Development × 25 cm of size, covered with fine mesh, of cross-resistance to insecticides of other with a special sleeve to run insects. The groups is also possible. For example, it is cages also had food (milk powder: glu- known that house fly population resistant cose 1:1) in Petri dishes and cups with to permethrin develops resistance to water with a cotton wicks in them. The fipronil (Liu & Yue, 2000). first generation of adult flies (F1) has been Information on the susceptibility of M. obtained in the laboratory out of the col- domestica field populations to the insecti- lected population of flies; it has been cides used on the territory of Russia is tested for susceptibility to insecticides. sporadic and mainly refers to flies of Susceptible insect culture was obtained towns (inhabited localities). Thus, in the from the laboratory of the Novosibirsk 1990s, a study of 19 populations of flies Agrarian University in 2009 and was from central (Moscow, Kaluga, Tver re- reared in the insectarium without contact gions) and southern (Astrakhan) regions with insecticides for more than 50 genera- of Russia, demonstrated their high resis- tions. tance to organophosphorus insecticides The testing was carried out using (chlorophos, carbofos) and tolerance or commercial insecticides containing del- sensitivity to such pyrethroids as perme- tamethrin (Deltsid 4% EC, Agrovetzash- thrin, neopinamine, fenvalerate hita, Russia; FAS 1% tablets, Agrovit on (Polyakova, 1995). It has also been re- scientific and technological orders of ported that the flies of the Moscow popu- Gigiena-Bio, Russia), cypermethrin (Sa- lation were highly resistant to pyrethroids marovka insecticide 25% EC, Samarovo, (Roslavtseva, 2001). Such studies of flies Russia), thiamethoxam (Agita 10% WG, on livestock complexes are rare and have NOVARTIS ANIMAL HEALTH Inc.,

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Switzerland), as well as industrial perme- to LD50 for laboratory strain of flies. Sus- thrin (97%, crystals, China), fipronil ceptibility of the field population to the (97%, powder, China), chlorfenapyr insecticides was determined based on the (97%, crystals, China). following criteria: RR<1 – high suscepti- To determine the toxicity of the insec- bility to the insecticide, RR=1 – absence ticides for flies the method of dosed con- of resistance (the population is sensitive to tacting of insects was used (Pavlov & the insecticide), RR=2–10 – very low re- Pavlova, 2005). The insect groups were sistance (the insects are tolerant to the exposed to the test drug without anaes- insecticide), RR=11–20 – low resistance thetic by forced contact with an insecti- (the insects are moderately resistant), cide residues on the bottom of a glass cup RR=21–50 – medium resistance, RR=51– for 30 min. Acetone solutions of insecti- 100 – high resistance (the insects are re- cide were prepared in 5–6 concentrations. sistant to the insecticide), RR>100 – very Then, 1 mL of each solution was added to high resistance (the insects are highly re- glass cups with diameter 35–40 mm and sistant to the insecticide) (Dremova et al., 40–45 mm height. After evaporation of 1999; Abbas et al., 2015). acetone a certain amount of active sub- Laboratory tests have shown that for stance – the dose – was left in each cup. flies of both laboratory and field popula- Then 10 flies were placed into each cup tions the pyrethroid deltamethrin had the by a piston, consisting of a mesh cloth and highest toxicity. Next came the pyrethroid a spring spacer ring, achieving close con- cypermethrin, pyrazole fipronil and neo- tact of the insects with the insecticide nicotinoid thiamethoxam. The permethrin residues on the bottom of a cup. After a toxicity was significantly lower. The low- 30–min exposure, pistons in cups were est toxicity against adults M. domestica of raised to supply insects with drinking both laboratory and field populations was bowls with 5% glucose solution. The death that of pyrrole chlorfenapyr (Table 1). of the insects was registered during one According to our results, the field day. Experiments with each dose of the populations of flies did not have a high insecticide were performed at least 3 resistance to deltamethrin, cypermethrin times. and permethrin. A very low resistance to The results of insect mortality depend- cypermethrin (RR = 3.66) and deltame- ing on the dose were analysed by probit thrin in the composition of the FAS prepa- analysis (Finney, 1971) using Free ration (RR = 3.07) should be noted. A LD50/LC50 Calculator (July 7, 2016; Dr. higher sensitivity to permethrin in the M. Alpha Raj by Calcuating LD50/LC50 studied population of flies is probably due using Probit Analysis in Excel Blog) for to the fact that insecticides containing this calculating LD50 for 95% confidence in- pyrethroid are quite rare. tervals (CI), slopes, standard errors, and House fly populations with varying χ2. Median lethal dose was expressed as a degrees of resistance to pyrethroids were microgram of the active substance per found around the world on livestock and gram of tested insects’ weight. To deter- poultry farms. For example, in the USA, mine the susceptibility of the field popula- Musca domestica caught in pens for cattle tion to the insecticides the resistance ratio in the southeast Nebraska showed reason- (RR) was calculated as the ratio of LD50 able resistance to permethrin: resistance of the insecticide for field population flies ratio of 7.3 when contacting with insecti-

BJVM, ××, No × 3 Insecticide susceptibility of house flies (Musca domestica) from a livestock farm in Tyumen region, Russia igh

1.88) 2.82) 2.75) 1.29) 1.18) 0.66) 1.13) – – – – – – – very h – of susceptible 50 RR (95% CI) 1.97 (2.06 3.07 (3.35 3.66 (4.90 1.25 (1.20 1.12 (1.06 0.80 (0.97 1.28 (1.45 μg of active substance per –

χ2 units

0.544 0.010 0.794 0.909 0.016 0.007 0.809 0.913 0.894 0.826 0.190 0.361 0.112 0.197 50 LD collected population/LD ; - low low resistance (the insects are moderately –

20 20 - 2015)

of field 50 et al., the absence of resistance (the resistance of population to sensitive theis absence – 0.911±0.166 1.701±0.109 1.017±0.156 2.218±0.090 1.116±0.168 1.444±0.104 2.550±0.093 2.118±0.101 2.399±0.085 1.965±0.098 0.891±0.165 1.369±0.123 1.565±0.107 2.569±0.080 Slope (±SE) 1999; Abbas

et al., 0.938) 0.666) 1.767) 1.877) 3.328) 9.137) 24.45) 31.66) 5.988) 7.074) 9.060) 6.001) 45.96) 52.12) – – – – – – – – – – – – – – Resistance Resistance ratio (RR) = LD ; (95% CI) 50 high resistance (the insects are resistant to the insecticide), RR>100 – LD 0.443(0.210 0.407(0.249 0.873(0.432 1.251(0.834 1.561(0.727 5.707(3.565 16.11(10.61 20.11(12.78 4.073(2.771 4.555(2.933 4.308(2.048 3.449(1.983 28.29(17.42 36.32(25.32 100 - high susceptibility to the high susceptibility insecticide, RR=1 –

in the numerator as FAS,denominator inthe in the numerator as Delcid.

– N 265 532 328 200 298 980 210 210 397 240 457 539 440 420

very low very resistance (the insects are tolerant to the insecticide), RR=11 – or deltamethrin f usceptibility: RR<1 usceptibility: medium resistance, RR=51 ; 10 – -

insecticides to adult house flies of field population (Chervishevo village, Tyumen municipal region, Russia) compared to Population Susceptible Chervishevo Susceptible Chervishevo Susceptible Chervishevo Susceptible Chervishevo Susceptible Chervishevo Susceptible Chervishevo 50 50 -

Criteria of s Criteria of

. Toxicity of

the number of adult flies used in bioassay including control – Table Table 1. susceptible population Insecticide Deltamethrin Cypermethrin Permethrin Thiamethoxam Fipronil Chlorfenapyr N population the insecticide), RR=2 resistant), RR=21 resistance (the insects are highly resistant to the insecticide) (Dremova one insects’ weight of g

4 BJVM, ××, No × M. A. Levchenko, E. A. Silivanova, G. F. Balabanova & R. H. Bikinyaeva cide residues on glass surfaces (Marçon et susceptible was chlorfenapyr (RR = 1.28). al., 2003). In Florida dairy farms, popula- As can be seen from the results, chlor- tion of flies resistant to pyrethroids have fenapyr is inferior to fipronil and pyre- been also found: more than 20-fold resis- throids in toxicity for flies of both lab- tant to permethrin and 10-fold to the beta- susceptible and field populations. In the cyfluthrin (Kaufman et al., 2010). In Paki- available literature, there is no informa- stan, population of flies resistant to pyre- tion about the formation of house fly throids have been also found on dairy populations resistant to chlorfenapyr. This farms: resistance ratio (at LC50) 30.22– is probably due to the absence of chlor- 70.02 for cypermethrin and 5.73–18.31 fenapyr containing preparations for com- for deltamethrin (Khan et al., 2013). bating flies, and its predominant use for In Russia, in the Tyumen region, an plant protection. exceptionally high resistance to pyre- Our results show a high susceptibility throids during their long-term use in pig of the field population to fipronil (RR = and calf barns in Nizhnaya Tavda village 0.80). In Russia insecticides containing was found in the local population of house fipronil are allowed in the form of gels flies, and a higher resistance was observed and poisoned baits (for example, to con- to the more effective preparations. In trol cockroaches), and therefore such 1999, RR to Butox (deltamethrin 5% EC) preparations are not applied to control the was 1600, Fastak (alpha-cypermethrin fly populations. This is probably the rea- 10% EC) – 1000, Arrivo (cypermethrin son why field populations of flies on 25% EC) – 800, Stomasanum (permethrin farms retain susceptibility to fipronil. 20% EC) – 200, Baversan (fenvalerate Given the high toxicity of fipronil for flies EC) – 50, mixtures of malathion and cy- and a high susceptibility of the field popu- permethrin – 200, permethrin with diazi- lation of flies to it, exploration and devel- non – 61 and chlorfenvinphos with al- opment of a suitable method of fipronil phamethrin – 45 (Pavlov et al., 2006). use to reduce the number of flies on live- The studied field house fly population stock breeding complexes is considered did not reveal resistance to thiamethoxam promising. It is important to consider the (RR = 1.12), despite the fact that neoni- world experience, indicating the possibil- cotinoid insecticides are quite common. ity of forming resistance to fipronil in Researchers from different countries house flies after its intensive use (Kris- noted the formation of resistance to tensen et al., 2004; Abbas et al., 2016). neonicotinoids in natural populations of Overall, the results suggest that the the house fly. For example, Kaufman et population of M. domestica on the live- al. (2010) reported the emergence of tol- stock farm in Chervishevo village, erant and resistant to imidacloprid house Tyumen municipal region, after many fly populations on Florida State dairy years of usage of pyrethroid insecticides farms. According to Khan et al. (2015), to control flies, retained susceptibility to the flies collected in different areas of permethrin and acquired tolerance or very Pakistan had different resistance to thia- low resistance to deltamethrin and cyper- methoxam: RR (at LC50 values) ranged methrin. It is necessary to restrict the use from 7.66 to 20.13. of pyrethroids to fly control. The monito- Another insecticide, to which the field ring of the susceptibility of field M. do- population of flies caught by us was also mestica populations to the conventional

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and new insecticides is important for more Musca, Sarcophaga, Calliphora, Fannia, effective of houseflies control on livestock Lucilia, Stomoxys) as vectors of patho- complexes. genic microorganisms. Parasitology Re- From practical point of view, in order search, 101, 243–246. to prevent the development of resistance, Kaufman, P. E., S. C. Nunez, R. S. Mann, C. it is important to use the rotation of insec- J. Geden & M. E. Scharf, 2010. Nicotinoid ticides with different modes of action, and pyrethroid insecticide resistance in houseflies (Diptera: Muscidae) collected taking into account the level of suscepti- from Florida dairies. Pest Management bility of the local population to the insec- Science, 66, 290–294. ticides used. The rotation scheme can be Khan, H. A., W. Akram & S. A. Shad, 2013. as follows: organophosphates – neonicoti- Resistance to conventional insecticides in noids – carbamates – neonicotinoids (Ro- Pakistani populations of Musca domestica slavtseva, 2011). According to our results, L. (Diptera: Muscidae): A potential ecto- the flies of field population are susceptible parasite of dairy animals. Ecotoxicology, to pyrroles (fipronil) and pyrazoles (chlor- 22, 522–527. fenapyr), therefore, the design of fipronil- Khan, H. A., W.Akram, J. Iqbal & U. Naeem- and chlorphenapyr-containing insecticidal Ullah, 2015. Thiamethoxam resistance in formulations for flies control and their the house fly, Musca domestica L.: Cur- inclusion in a system of integrated pest rent status, resistance selection, cross- management seems promising. resistance potential and possible bio- chemical mechanisms. PLoS One, 10, e0125850. REFERENCES Kristensen, M., J. B. Jespersen & M. Knorr, 2004. Cross-resistance potential of fipronil Abbas, N., S. Ali Shad, & M. Ismail, 2015. in Musca domestica. Pest Management Resistance to conventional and new insec- Science, 60, 894–900. ticides in house flies (Diptera: Muscidae) from poultry facilities in Punjab, Pakistan. Liu, N. & Yue, X., 2000. Insecticide resistance and cross-resistance in the house fly (Dip- Journal of Economic Entomology, 108, tera: Muscidae). Journal of Economic En- 826–833. tomology, 93, 1269–1275. Abbas, N., M. Ijaz, S. A. Shad & M. Binyameen, 2016. Assessment of resis- Marçon, P. C., G. D. Thomas, B. D. Siegfried, tance risk to fipronil and cross resistance J. B. Campbell & S. R. Skoda, 2003. Re- to other insecticides in the Musca domes- sistance status of house flies (Diptera: tica L. (Diptera: Muscidae). Veterinary Muscidae) from southeastern Nebraska beef cattle feedlots to selected insecticides. Parasitology, 223, 71–76. Journal of Economic Entomology, 96, Dremova, V. P., L. S. Putintseva & P. E., 1016–1020. Khodakov, 1999. Medical disinsection. Basic principles, means and methods. Vi- N'Guessan, R., P. Boko, A. Odjo, M. Akog- tar-Putived Publ., Ekaterinburg, Russia béto, A. Yates & M. Rowland, 2007. (RU). Chlorfenapyr: A pyrrole insecticide for the control of pyrethroid or DDT resistant Finney, D., 1971. A statistical treatment of the rd Anopheles gambiae (Diptera: Culicidae) sigmoid response curve, Probitanalysis, 3 mosquitoes. Acta Tropica, 102, 69–78. edn, Cambridge University Press, London. Pavlov, S. D., R. P. Pavlova, & S. M. Mavlju- Förster, M., S. Klimpel, H. Mehlhorn, K. tov, 2006. About resistance of insects of Sievert, S, Messler & K. Pfeffer, 2007. “gnus” complex and house fly to action of Pilot study on synanthropic flies (e.g. modern insecticides. In: Entomological re-

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tance in house flies from the United States: Dr. Silivanova Elena Anatolievna Resistance levels and frequency of pyre- All-Russian Scientific Research Institute of throid resistance alleles. Pesticide Bio- Veterinary Entomology and Arachnology, chemistry and Physiology, 107, 377–384. 625041, 2 Institutskaya str., Scott, J. G., W. C. Warren, L. W. Beukeboom, Tyumen, Russian Federation. D. Bopp, A. G. Clark, S. D. Giers, M. He- tel./fax: 8-10-3452-62-57-08, +79058204116; diger, A. K. Jones, S. Kasai, C. A. Leich- e-mail: [email protected] ter, M. Li, R. P. Meisel, P. Minx, T. D. Murphy, D. R. Nelson, W. R. Reid, F. D. Rinkevich, H. M. Robertson, T. B. Sack-

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