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Monitoring for Resistance to Organophosphorus and Pyrethroid Insecticides in Varroa Mite Populations

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INSECTICIDE RESISTANCE AND RESISTANCE MANAGEMENT Monitoring for Resistance to Organophosphorus and Pyrethroid Insecticides in Varroa Mite Populations 1,2 3 1 4 LAMBERT H. B. KANGA, JOHN ADAMCZYK, KEITH MARSHALL, AND ROBERT COX J. Econ. Entomol. 103(5): 1797Ð1802 (2010); DOI: 10.1603/EC10064 ABSTRACT The occurrence of resistance in Varroa mite populations is a serious threat to the beekeeping industry and to crops that rely on the honey bee for pollination. Integrated pest management strategies for control of this pest include the judicious use of insecticides. To monitor Þeld populations of Varroa mite for insecticide resistance, a glass vial bioassay procedure was developed to use in the development of a resistance management strategy. Diagnostic concen- trations needed to separate susceptible genotypes from resistant individuals were determined for cypermethrin (0.1 ␮g per vial), ßuvalinate (5.0 ␮g per vial), malathion (0.01 ␮g per vial), coumaphos (10.0 ␮g per vial), diazinon (5.0 ␮g per vial), methomyl (0.5 ␮g per vial), propoxur (0.1 ␮g per vial), and endosulfan (2.5 ␮g per vial). Resistance to organophosphorus insecticides (malathion, coumaphos) and pyrethroids (cypermetrhrin, ßuvalinate) was widespread in both La Media Ranch, TX, and Wewahitchka, FL, from 2007 to 2009. There was no resistance to endosulfan, diazinon, methomyl, and propoxur in Þeld populations of Varroa mite in the two locations where resistance was monitored. The seasonal patterns of resistance in Wewahitchka were different from those of La Media Ranch. In the former location, the frequency of resistance to all insecticides tested decreased signiÞcantly from 2007 to 2009, whereas it increased in the latter location. Resistance levels were unstable, suggesting that resistance could be successfully managed. The results validate use of the glass vial bioassay to monitor for resistance in Varroa mite and provide the basis for the development of a resistance management strategy designed to extend the efÞcacy of all classes of insecticides used for control of Varroa mite. KEY WORDS Varroa destructor, Apis mellifera, monitoring insecticide resistance The honey bee, Apis mellifera L. is essential for honey States (Sanford et al. 1999), but some resistance has production and crop pollination (Ͼ130 agricultural already developed to this compound (Elzen and West- plants in the United States are pollinated by honey ervelt 2002). bees). The ectoparasitic mite Varroa destructor Selection for mite resistant honey bees has shown Anderson & Trueman is currently a serious worldwide some success (Rinderer et al. 2000, Spivak and Reuter threat to beekeeping (De Jong et al. 1982, Rosenkranz 2001). However, chemical treatments are still neces- et al. 2010). Without adequate control of Varroa mite sary to ensure colony survival within the breeding infestations, bee mortality approaches 100% in un- programs for strains resistant to Varroa in North Amer- treated colonies, which can perish within a few weeks. ica and Europe (Bu¨ chler 1994, Rinderer et al. 1997). A major chemical control strategy is the use of Chemical controls, such as ßumethrin, amitraz, plastic strips impregnated with the pyrethroid ßuvali- cymiazole, and bromopropylate, leave toxic residues nate (Apistan, Wellmark International, Bensenville, (Wallner 1999), and are difÞcult to register in North IL). Although Apistan strips have been very effective America because of safety concerns for public health in controlling mites (Ferrer-Dufol et al. 1991), resis- and the environment. Although entomopathogenic tance has developed in several mite populations (El- fungi (Metarhizium anisopliae and Hirsutella thomp- zen et al. 1998, Milani 1999). In addition, these prod- sonii ucts leave residues in wax and honey (Cabras et al. ) offer promising avenues for biological control of 1997, Wallner 1999). More recently, plastic strips Varroa mite (Kanga et al. 2002, 2003), the develop- coated with the organophosphate coumaphos ment of a sustainable pest management strategy will (CheckMite, Bayer Shawnee Mission, KS) have been require the judicious integration of other control mea- used under emergency registration in the United sures. In this study, we report on the selection of diag- 1 Center for Biological Control, Florida A&M University, Tallahas- nostic concentrations of insecticides for use in resis- see, FL 32307-4100. tance monitoring and present results on monitoring 2 Corresponding author, e-mail: [email protected]. 3 USDAÐARS, BeneÞcial Insects Research Unit, Weslaco, TX 78596. Varroa mite populations for resistance to several in- 4 USDAÐARS, Honey Bee Research Unit, Weslaco, TX 78596. secticides. 0022-0493/10/1797Ð1802$04.00/0 ᭧ 2010 Entomological Society of America 1798 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 103, no. 5 Table 1. Responses of susceptible (S-CA) and field-collected resistant (R-LMR) Varroa mite populations to different insecticides Na Ϯ b c Insecticide Strain Slope SE LC50 (95% CL) RR (95% CL) Pyrethroid Cypermethrin SCA 125 1.17 Ϯ 0.42 0.020 (0.001Ð0.066) R-LMR 130 1.68 Ϯ 0.68 0.090 (0.016Ð0.190) 4.5 (3.05Ð5.98) Fluvalinate S-CA 120 1.69 Ϯ 0.45 0.100 (0.030Ð0.290) R-LMR 145 2.25 Ϯ 0.44 0.260 (0.110Ð0.420) 2.6 (1.88Ð4.98) Organophosphate Malathion S-CA 165 4.47 Ϯ 1.85 0.003 (0.002Ð0.004) R-LMR 160 3.21 Ϯ 0.95 0.011 (0.004Ð0.020) 3.7 (2.24Ð5.26) Coumaphos S-CA 147 1.36 Ϯ 1.81 0.150 (0.001Ð0.042) R-LMR 153 1.11 Ϯ 0.37 2.150 (0.278Ð9.343) 14.3 (11.76Ð19.59) Diazinon S-CA 124 1.16 Ϯ 0.44 0.040 (0.001Ð0.219) R-LMR 118 0.99 Ϯ 0.41 0.050 (0.002Ð0.337) 1.3 (0.78Ð2.14) Carbamate Methomyl S-CA 98 3.43 Ϯ 1.13 0.002 (0.001Ð0.005) R-LMR 122 3.49 Ϯ 0.87 0.002 (0.001Ð0.004) 1.0 (0.32Ð1.35) Propoxur S-CA 92 1.83 Ϯ 0.63 0.002 (0.001Ð0.007) R-LMR 129 1.97 Ϯ 0.62 0.003 (0.001Ð0.011) 1.5 (0.77Ð2.46) Cyclodiene Endosulfan S-CA 109 1.95 Ϯ 0.51 0.023 (0.008Ð0.740) R-LMR 146 1.92 Ϯ 0.53 0.034 (0.007Ð0.152) 1.5 (0.96Ð2.88) a Number of mites tested. b Concentrations are expressed in micrograms per vial of the insecticide tested. c Resistance ratios (RR) calculated by dividing the LC50 for the R-LMR by the LC50 for the S-CA strain. Materials and Methods mites was determined 18 h after exposure. Mites that were unable to walk for a short distance (Ͼ5 mm) after Insecticides. All insecticides tested were technical gentle probing with a Þne brush were considered dead. grade samples (Ϸ98% purity) as supplied by the man- Diagnostic Concentrations for Resistance Monitor- ufacturers. We used the organophosphorodithionate ing. Susceptible and resistant mite populations were malathion, the organophosphorothioate coumaphos, exposed to insecticides to establish diagnostic concen- and the pyrethroids cypermethrin and ßuvalinate trations that were estimated from the concentrationÐ (Chemical Service, West Chester, PA) for resistance mortality responses. At that concentration, all suscepti- monitoring. Other technical grade insecticides tested ble individuals were killed and only resistant phenotypes included the cylodiene endosulfan, the organophos- survived (Kanga and Plapp 1995). Concentration-re- phorothiolate diazinon, the oxime carbamate metho- sponse regressions for each strain and each insecticide myl, and the aryl carbamate propoxur. These chemi- were calculated with seven concentrations of insecti- cals were purchased either from Sigma (St. Louis, cides (plus an acetone control), with eight to 10 repli- MO) or Aldrich (Milwaukee, WI). cates of two to three mites per vial. Mites. Female mites were collected from infested Monitoring for Resistance. Assessments of the lev- frames of sealed brood taken from honey bee colonies els of resistance in Þeld populations were conducted maintained in or nearby Weslaco, TX, and in Wewa- using techniques as described by Kanga et al. (1997) hitchka, FL. Susceptible mites (S-CA) were collected and Elzen et al. (1998, 2002). Varroa mites collected from an apiary located in Cactus Alley (Old Marine from the apiaries were brought to the laboratory and base) in Weslaco. This apiary has feral honey bee exposed to residues of insecticide in treated vials to colonies that have never been treated with pesticides. determine the frequencies of resistant phenotypes. The resistant mites (R-LMR) were Þeld collected indi- Between 75 and 112 mites were tested at each di- viduals from La Media Ranch (near Weslaco) where agnostic concentration during an experimental run. high levels of resistance were reported. Drone and Statistical Analyses. Concentration-mortality data worker brood cells were opened and adult female mites were analyzed by Probit analysis (Russell et al. 1977). were collected from larvae and pupae, by using a camelÕs- Data from multiple experiments were pooled. Differ- hair brush. The mites were placed into glass scintillation ences among populations in response to insecticides vials (20 ml) containing honey bee larvae as a food were considered not signiÞcant if the 95% conÞdence source before insecticide bioassays. limit (CL) of the resistance ratio at the LC bracketed Insecticide Bioassays. The procedure used in this 50 1.0 (Robertson and Preisler 1992). study was described by Kanga and Plapp (1995). In brief, 20-ml glass scintillation vials were treated with 0.5-ml solutions of insecticide in acetone. The vials Results were rolled until the acetone evaporated and the in- secticides were coated on the inner surfaces. Vials Laboratory Bioassays. Varroa mites displayed vary- treated with acetone only were used as controls. Two to ing levels of resistance within and between groups of three mites were placed in each vial and held at room insecticides tested (Table 1). The responses of S-CA temperature (27 Ϯ 1ЊC and 65% RH).
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    Environmental Health Criteria 63 ORGANOPHOSPHORUS INSECTICIDES: A GENERAL INTRODUCTION Please note that the layout and pagination of this web version are not identical with the printed version. Organophophorus insecticides: a general introduction (EHC 63, 1986) INTERNATIONAL PROGRAMME ON CHEMICAL SAFETY ENVIRONMENTAL HEALTH CRITERIA 63 ORGANOPHOSPHORUS INSECTICIDES: A GENERAL INTRODUCTION This report contains the collective views of an international group of experts and does not necessarily represent the decisions or the stated policy of the United Nations Environment Programme, the International Labour Organisation, or the World Health Organization. Published under the joint sponsorship of the United Nations Environment Programme, the International Labour Organisation, and the World Health Organization World Health Orgnization Geneva, 1986 The International Programme on Chemical Safety (IPCS) is a joint venture of the United Nations Environment Programme, the International Labour Organisation, and the World Health Organization. The main objective of the IPCS is to carry out and disseminate evaluations of the effects of chemicals on human health and the quality of the environment. Supporting activities include the development of epidemiological, experimental laboratory, and risk-assessment methods that could produce internationally comparable results, and the development of manpower in the field of toxicology. Other activities carried out by the IPCS include the development of know-how for coping with chemical accidents, coordination