Anti-Varroa Efficiency of Coumaphos and Its Influence on Oxidative Stress and Survival of Honey Bees

1. Hung KLJ, Kingston JM, Albrecht M, Holway DA, Kohn JR: The worldwide importance of honey bees as pollinators in natural habitats. P Roy Soc B: Biol Sci 2018, 285.10.1098/rspb.2017.2140578419529321298Search in Google Scholar

2. Ramsey SD, Ochoa R, Bauchan G, Gulbronson C, Mowery JD, Cohen A, Lim D, Joklik J, Cicero JM, Ellis JD, Hawthorne D, vanEngelsdorp D: Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. P Natl Acad Sci USA 2019, 116:1792-1801.10.1073/pnas.1818371116635871330647116Search in Google Scholar

3. De Jong D, Morse RA, Eickwort GC: Mite pests of honeybees. Ann Rev Entomol 2003, 27:229-252.10.1146/annurev.en.27.010182.001305Search in Google Scholar

4. Gajic B, Radulovic Z, Stevanovic J, Kulisic Z, Vucicevic M, Simeunovic P, Stanimirovic Z: Variability of the honey bee mite Varroa destructor in Serbia, based on mtDNA analysis. Exp Appl Acarol 2013, 61: 97-105.10.1007/s10493-013-9683-923471517Search in Google Scholar

5. Gajić B, Stevanovic J, Radulović Ž, Kulišić Z, Vejnović B, Glavinić U, Stanimirović Z: Haplotype identification and detection of mitochondrial DNA heteroplasmy in Varroa destructor mites using ARMS and PCR–RFLP methods. Exp Appl Acarol 2016, 70: 287–297.10.1007/s10493-016-0086-627631761Search in Google Scholar

6. Glavinic U, Stevanovic J, Gajic B, Simeunovic P, Djuric S, Vejnovic B, Stanimirovic Z. Nosema ceranae DNA in honey bee haemolymph and honey bee mite Varroa destructor. Acta Vet-Beograd 2014, 64:349-357.10.2478/acve-2014-0033Search in Google Scholar

7. Simeunovic P, Stevanovic J, Vidanovic D, Nisavic J, Radovic D, Stanisic Lj, Stanimirovic Z: A survey of deformed wing virus and acute bee paralysis virus in honey bee colonies from Serbia using real-time RT-PCR. Acta Vet-Beograd 2014, 64:81-92.10.2478/acve-2014-0009Search in Google Scholar

8. Bernardi S, Venturino E: Viral epidemiology of the adult Apis mellifera infested by the Varroa destructor mite. Heliyon 2016, 2:e00101.10.1016/j.heliyon.2016.e00101494622027441276Search in Google Scholar

9. Stanimirovic Z, Glavinic U, Lakic N, Radovic D, Ristanic M, Taric E, Stevanovic J: Efficacy of plant-derived formulation “Argus Ras” in Varroa destructor control. Acta Vet-Beograd 2017, 67:191-200.10.1515/acve-2017-0017Search in Google Scholar

10. Cirkovic D, Stevanovic J, Glavinic U, Aleksic N, Djuric S, Aleksic J, Stanimirovic Z: Honey bee viruses in Serbian colonies of different strength. PeerJ 2018, 6:e5887.10.7717/peerj.5887624034030479890Search in Google Scholar

11. Stanimirovic Z, Glavinic U, Ristanic M, Aleksic N, Jovanovic N, Vejnovic B, Stevanović J: Looking for the causes of and solutions to the issue of honey bee colony losses. Acta Vet-Beograd 2019, 69: 1-31.10.2478/acve-2019-0001Search in Google Scholar

12. Stokes BA, Yadav S, Shokal U, Smith LC, Eleftherianos I: Bacterial and fungal pattern recognition receptors in homologous innate signaling pathways of insects and mammals. Front Microbiol 2015, 6:19.10.3389/fmicb.2015.00019430918525674081Search in Google Scholar

13. Harwood G, Amdam G, Freitak D: The role of vitellogenin in the transfer of immune elicitors from gut to hypopharyngeal glands in honey bees (Apis mellifera). J Insect Physiol 2019, 112:90-100.10.1016/j.jinsphys.2018.12.00630578811Search in Google Scholar

14. Rosenkranz P, Aumeier P, Ziegelmann B: Biology and control of Varroa destructor. J Invertebr Pathol 2010, 103: S96-S119.10.1016/j.jip.2009.07.01619909970Search in Google Scholar

15. Stanimirovic Z, Stevanovic J, Jovanovic S, Andjelkovic M: Evaluation of genotoxic effects of Apitol® (cymiazole hydrochloride) in vitro by 4 measurement of sister chromatid exchange. Mutat Res-Gen Tox En 2005, 588:152-157.10.1016/j.mrgentox.2005.10.00316309949Search in Google Scholar

16. Boecking O, Spivak M: Behavioral defenses of honey bees against Varroa jacobsoni Oud. Apidologie 1999, 30:141-158.10.1051/apido:19990205Search in Google Scholar

17. Stanimirovic Z, Pejovic D, Stevanovic J, Vucinic M, Mirilovic M: Investigations of hygienic behaviour and disease resistance in organic beekeeping of two honeybee ecogeographic varieties from Serbia. Acta Vet-Beograd 2002, 52:169-180.10.2298/AVB0203169SSearch in Google Scholar

18. Le Conte Y, Alaux C, Martin JF, Harbo JR, Harris JW, Dantec C, Séverac D, Cros-Arteil S, Navajas M: Social immunity in honeybees (Apis mellifera): transcriptome analysis of varroa-hygienic behaviour. Insect Mol Biol 2011, 20:399-408.10.1111/j.1365-2583.2011.01074.x21435061Search in Google Scholar

19. Stevanovic J, Stanimirovic Z, Lakic N, Djelic N, Radovic I: Stimulating effect of sugar dusting on honey bee grooming behaviour. Entomol Exp Appl 2012, 143:23-30.10.1111/j.1570-7458.2012.01231.xSearch in Google Scholar

20. Mondet F, Alaux C, Severac D, Rohmer M, Mercer AR, Le Conte Y: Antennae hold a key to Varroa-sensitive hygiene behaviour in honey bees. Sci Rep 2015, 5:10454.10.1038/srep10454444111526000641Search in Google Scholar

21. Ravindran R, Jyothimol G, Amithamol KK, Sunil AR, Chandrasekhar L, Lenka DR, Amritha A, Sreelekha K, Sathish N, Udayan D, Krishna TPA, Divya MT, Juliet S, Kumar KGA, Nair SN, Ghosh S: In vitro efficacy of amitraz, coumaphos, deltamethrin and lindane against engorged female Rhipicephalus (Boophilus) annulatus and Haemaphysalis bispinosa ticks. Exp Appl Acarol 2018, 75:241-253.10.1007/s10493-018-0262-y29737450Search in Google Scholar

22. Ola-Davies OE, Azeez OI, Oyagbemi AA, Abatan MO: Acute coumaphos organophosphate exposure in the domestic dogs: Its implication on haematology and liver functions. Int J Vet Sci Med 2018, 6:103-112.10.1016/j.ijvsm.2018.04.004614925630255086Search in Google Scholar

23. Bajuk BP, Babnik K, Snoj T, Milčinski L, Ocepek MP, Škof M, Jenčič V, Filazi A, Štajnbaher D, Kobal S: Coumaphos residues in honey, bee brood, and beeswax after Varroa treatment. Apidologie 2017, 48:588-598.10.1007/s13592-017-0501-ySearch in Google Scholar

24. Chakrabarti P, Rana S, Sarkar S, Smith B, Basu P: Pesticide-induced oxidative stress in laboratory and field populations of native honey bees along intensive agricultural landscapes in two Eastern Indian states. Apidologie 2015, 46:107-129.10.1007/s13592-014-0308-zSearch in Google Scholar

25. Balieira KVB, Mazzo M, Bizerra PFV, Guimarães ARDJS, Nicodemo D, Mingatto FE: Imidacloprid-induced oxidative stress in honey bees and the antioxidant action of caffeine. Apidologie 2018, 49:562-572.10.1007/s13592-018-0583-1Search in Google Scholar

26. Gregorc A, Alburaki M, Rinderer N, Sampson B., Knight PR, Karim S, Adamczyk J: Effects of coumaphos and imidacloprid on honey bee (Hymenoptera: Apidae) lifespan and antioxidant gene regulations in laboratory experiments. Sci Rep 2018, 8:15003.10.1038/s41598-018-33348-4617741030301926Search in Google Scholar

27. Nikolić VT, Purać J, Orčić S, Kojić D, Vujanović D, Stanimirović Z, Gržetić I, Ilijević K, Šikoparija B, Blagojević PD: Environmental effects on superoxide dismutase and catalase activity and expression in honey bee. Arch Insect Biochem Physiol 2015, 90:181-194.10.1002/arch.2125326314562Search in Google Scholar

28. Glavinic U: The effects of various antimicrobials and supplements on the expression of immune-related genes, oxidative stress and survival of honey bee Apis mellifera infected with microsporidium Nosema ceranae. PhD Thesis, University of Belgrade 2019.Search in Google Scholar

29. Stevanovic J, Stanimirovic Z, Simeunovic P, Lakic N, Radovic I, Sokovic M, Van Griensven JLD: The effect of Agaricus brasiliensis extract supplementation on honey bee colonies. An Acad Bras Cienc 2018, 90: 219-229.10.1590/0001-376520182015018229424386Search in Google Scholar

30. ОIЕ: Manual of Diagnostic Tests and Vaccines for Terrestrial Animals, 2013 [http://www.oie.int/en/international-standard-setting/terrestrial-manual/access-online/].Search in Google Scholar

31. Goodwin M, Van Eaton C: Control of Varroa. A guide for New Zealand beekeepers. New Zealand Ministry of Agriculture and Forestry; 2001:37-38.Search in Google Scholar

32. EMA – European Medicines Agency, EMA/CVMP/EWP/459883/2008, Committee for Medicinal Products for Veterinary Use (CVMP), Guideline on veterinary medicinal products controlling Varroa destructor parasitosis in bees (2010). https://www.ema.europa.eu/en/documents/scientific-guideline/guideline-veterinary-medicinal-products-controlling-varroa-destructor-parasitosis-bees_en.pdfSearch in Google Scholar

33. Human H, Brodschneider R, Dietemann V, Dively G, Ellis JD, Forsgren E: Miscellaneous standard methods for Apis mellifera research. J Apicult Res 2013, 52:1-53.10.3896/IBRA.1.52.4.10Search in Google Scholar

34. Nikolić T, Purać J, Orčić S, Kojić D, Vujanović D, Stanimirović Z, Gržetić I, Ilijević K, Šikoparija B, Blagojević D: Environmental effects on superoxide dismutase and catalase activity and expression in honey bee. Arch Insect Biochem Physiol 2015, 90:181-194.10.1002/arch.21253Search in Google Scholar

35. Orcic S, Nikolic T, Purac J, Sikoparija B, Blagojević D, Vukasinovic E, Plavsa N, Stevanovic J, Kojic D: Mullin Seasonal variations in the activity of selected antioxidant enzymes and malondialdehyde level in worker honey bees. Entomol Exp Appl 2017, 165:120-128.10.1111/eea.12633Search in Google Scholar

36. Kojic DK, Purac JS, Nikolic TV, Orcic SM, Vujanovic D, Ilijevic K, Vukasinovic EL, Blagojevic DP: Oxidative stress and the activity of antioxidative defense enzymes in overwintering honey bees. Entomol Gen 2019, 39:33-44.10.1127/entomologia/2019/0743Search in Google Scholar

37. Gregorc and Planinc (2012) Use of thymol formulations, amitraz and oxalic acid for the control of the varroa mite in honey bee (Apis mellifera carnica) colonies. J Apic Sci, 56:61-69.10.2478/v10289-012-0024-8Search in Google Scholar

38. Spreacifico M, Eordegh FR, BernardinelliI, Colombo M: First detection of strains of Varroa destructor resistant to coumaphos. Results of laboratory tests and field trials. Apidologie 2001, 32:49–55.10.1051/apido:2001110Search in Google Scholar

39. Elzen PJ, Westervelt D: Detection of coumaphos resistance in Varroa destructor in Florida. Am Bee J 2002, 142:291-292.Search in Google Scholar

40. Medici SK, Maggi MD, Sarlo EG, Ruffinengo S, Marioli JM, Eguaras MJ: The presence of synthetic acaricides in beeswax and its influence on the development of resistance in Varroa destructor. J Apicult Res 2016, 54:267–274.10.1080/00218839.2016.1145407Search in Google Scholar

41. Mitton GA, Szawarski N, Ramos F, Fuselli S, Meroi Arcerito FR, Javier Eguaras M, Ruffinengo SR, Matías Daniel Maggi: (2018) Varroa destructor: when reversion to coumaphos resistance does not happen, J Apicult Res 2018, 57:536-540.10.1080/00218839.2018.1475038Search in Google Scholar

42. vanEngelsdorp, Meixner MD: A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J Invertebr Pathol 2010, 103:S80-S95.10.1016/j.jip.2009.06.01119909973Search in Google Scholar

43. Smodis Skerl I, Gregorc A: Heat shock proteins and cell death in situ localisation in hypopharyngeal glands of honeybee (Apis mellifera carnica) workers after imidacloprid or coumaphos treatment. Apidologie 2010, 41:73–86.10.1051/apido/2009051Search in Google Scholar

44. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, vanEngelsdorp D, Pettis JS: High levels of miticides and agrochemicals in North American apiaries: Implications for honey bee health. PLoS ONE 2010, 5:e9754.10.1371/journal.pone.0009754284163620333298Search in Google Scholar

45. Gregorc A: A clinical case of honey bee intoxication after using coumaphos strips against Varroa destructor. J Apicult Res 2012, 51:142-143.10.3896/IBRA.1.51.1.19Search in Google Scholar

46. Dahlgren L, Johnson RM, Siegfried BD, Ellis MD: Comparative toxicity of acaricides to honey bee (Hymenoptera: Apidae) workers and queens. J Econ Entom 2012, 105:1895-190210.1603/EC1217523356051Search in Google Scholar

47. Johnson RM, Dahlgren L, Siegfried BD, Ellis MD: Effect of in-hive miticides on drone honey bee survival and sperm viability. J Apicult Res 2013, 52: 88-95.10.3896/IBRA.1.52.2.18Search in Google Scholar

48. Johnson RM, Dahlgren L, Siegfried BD, Ellis MD: Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PloS One 2013, 8:e54092.10.1371/journal.pone.0054092355850223382869Search in Google Scholar

49. Williamson SM, Right GA: Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J Exp Biol 2013, 216:1799-1807.10.1242/jeb.083931364180523393272Search in Google Scholar

50. Cizelj I, Glavan G, Božič J, Oven I, Mrak V, Narat M: Prochloraz and coumaphos induce different gene expression patterns in three developmental stages of the Carniolan honey bee (Apis mellifera carnica Pollmann). Pestic Biochem Physiol 2016, 128:68-75.10.1016/j.pestbp.2015.09.01526969442Search in Google Scholar

51. Sanchez-Bayo I, Goka K: (2016) Impacts of Pesticides on honey bees. In: Chambo, ED. (ed.) Beekeeping and bee conservation – advances in research. Rijeka, Croatia: In Tech; 2016, 77-97.10.5772/62487Search in Google Scholar

52. Dai P, Jack CJ, Mortensen AN, Bustamante TA, Ellis JD: (2018) Chronic toxicity of amitraz, coumaphos and fluvalinate to Apis mellifera L. larvae reared in vitro. Sci Rep 2018, 8:5635.10.1038/s41598-018-24045-3588478429618776Search in Google Scholar

53. Balieira KVB, Mazzo M, Bizerra PFV, Guimarães ARDJS., Nicodemo D, Mingatto FE: Imidacloprid-induced oxidative stress in honey bees and the antioxidant action of caffeine. Apidologie 2018, 49:562-57210.1007/s13592-018-0583-1Search in Google Scholar

54. Morimoto T, Kojima Y, Toki T, Komeda Y, Yoshiyama M, Kimura K, Nirasawa K, Kadowaki T: The habitat disruption induces immune-suppression and oxidative stress in honey bees. Ecol Evol 2011, 1:201-217.10.1002/ece3.21328730022393496Search in Google Scholar

55. Simone-Finstrom M, Li-Byarlay H, Huang MH, Strand MK, Rueppell O, Tarpy DR: Migratory menagment and enviromental conditions affect lifespan and oxidative stress in honey bees. Sci Rep 2016, 6:32023.10.1038/srep32023499552127554200Search in Google Scholar

56. Margotta JW, Roberts SP, Elekonich MM: Effects of flight activity and age on oxidative damage in the honey bee, Apis mellifera. J Exp Biol 2018, 221:14.10.1242/jeb.18322829724776Search in Google Scholar

57. Vilić M, Gajger IT, Tucak P, Stambuk A, Šrut M, Klobučar GIV, Malarić K, Žaja ŽI, Pavelić A, Manger M, Tkalec M: Effects of short-term exposure to mobile phone radiofrequency (900 MHz) on the oxidative response and genotoxicity in honey bee larvae. J Apicult Res 2017, 56:430-438.10.1080/00218839.2017.1329798Search in Google Scholar

58. Li-Byarlay H, Huang MH, Simone-Finstrom M, Strand MK, Tarpy DR, Rueppell O: Honey bee (Apis mellifera) drones survive oxidative stress due to increased tolerance instead of avoidance or repair of oxidative damage. Exp Gerontol 2016, 83:15-21.10.1016/j.exger.2016.07.003500719927422326Search in Google Scholar

59. Premrov Bajuk B, Babnik K, Snoj T, Milčinski L, Ocepek MP, Škof M, Jenčič V, Filazi A, Štajnbaher D, Kobal S: Coumaphos residues in honey, bee brood, and beeswax after Varroa treatment. Apidologie 2017, 48:588-598.10.1007/s13592-017-0501-ySearch in Google Scholar