Attractive Toxic Sugar Bait (ATSB) For Control of Mosquitoes and Its Impact on Non-Target Organisms: A Review

Jodi M Fiorenzano, Philip G Koehler, Rui-De Xue, Jodi M Fiorenzano, Philip G Koehler, Rui-De Xue

Abstract

Mosquito abatement programs contend with mosquito-borne diseases, insecticidal resistance, and environmental impacts to non-target organisms. However, chemical resources are limited to a few chemical classes with similar modes of action, which has led to insecticide resistance in mosquito populations. To develop a new tool for mosquito abatement programs that control mosquitoes while combating the issues of insecticidal resistance, and has low impacts of non-target organisms, novel methods of mosquito control, such as attractive toxic sugar baits (ATSBs), are being developed. Whereas insect baiting to dissuade a behavior, or induce mortality, is not a novel concept, as it was first introduced in writings from 77 AD, mosquito baiting through toxic sugar baits (TSBs) had been quickly developing over the last 60 years. This review addresses the current body of research of ATSB by providing an overview of active ingredients (toxins) include in TSBs, attractants combined in ATSB, lethal effects on mosquito adults and larvae, impact on non-target insects, and prospects for the use of ATSB.

Keywords: attractive toxic sugar baits; mosquito control; sugar feeding.

Conflict of interest statement

The authors declare no conflict of interest.

References

    1. World Health Organization . A Global Brief on Vector-Borne Diseases. World Health Organization; Geneva, Switzerland: 2014.
    1. American Mosquito Control Association . Best Management Practices for Integrated Mosquito Management. American Mosquito Control Association; Mount Laurel, NJ, USA: 2009.
    1. World Health Organization . Handbook for Integrated Vector Management. World Health Organization; Geneva, Switzerland: 2012.
    1. World Health Organization . Global Plan for Insecticide Resistance Management in Malaria Vectors. World Health Organization; Geneva, Switzerland: 2012.
    1. Dethier V.G. Chemical Insect Attractants and Repellents. Maple Press Company; York, PA, USA: 1947.
    1. Foster W.A. Mosquito sugar feeding and reproductive energetics. Annu. Rev. Entomol. 1995;40:443–474. doi: 10.1146/annurev.en.40.010195.002303.
    1. Schlein Y., Müller G.C. An approach to mosquito control: Using the dominant attraction of flowering Tamarix jordanis trees against Culex pipiens. J. Med. Entomol. 2008;45:384–390. doi: 10.1093/jmedent/45.3.384.
    1. Müller G.C., Kravchenko V.D., Schlein Y. Decline of Anopheles sergentii and Aedes caspius populations following presentations of attractive toxic (spinosad) sugar bait stations in oasis. J. Am. Mosq. Control Assoc. 2008;24:147–149. doi: 10.2987/8756-971X(2008)24[147:DOASAA];2.
    1. Müller G.C., Beier J.C., Traore S.F., Toure M.B., Traore M.M., Bah S., Doumbia S., Schlein Y. Successful field trial of attractive toxic sugar bait (ATSB) plant-spraying methods against malaria vectors in the Anopheles gambiae complex in Mali, West Africa. Malar. J. 2010;9:210.
    1. Lewis D.J., Domoney C.R. Sugar meals in Phlebotominae and Simuliidae (Diptera) Proc. R. Entomol. Soc. Ser. A Gen. Entomol. 1966;41:175–179. doi: 10.1111/j.1365-3032.1966.tb00340.x.
    1. Mascari T.M., Foil L.D. Laboratory evaluation of insecticide-treated sugar baits for control of Phlebotomine sand flies (Diptera: Psychodidae) J. Am. Mosq. Control Assoc. 2010;26:398–402. doi: 10.2987/10-6017.1.
    1. Schlein Y., Müller G.C. Experimental control of Phlebotomus papatasi by spraying attractive toxic sugar bait (ATSB) on vegetation. Trans. R. Soc. Trop. Med. Hyg. 2010;104:766–771. doi: 10.1016/j.trstmh.2010.08.014.
    1. Müller G.C., Revay E.E., Beier J.C. Simplified and improved monitoring traps for sampling sand flies. J. Vector Ecol. 2011;36:454–457. doi: 10.1111/j.1948-7134.2011.00188.x.
    1. Xue R.D., Kline D.L., Ali A., Barnard D.R. Application of boric acid baits to plant foliage for adult mosquito control. J. Am. Mosq. Control Assoc. 2006;22:497–500. doi: 10.2987/8756-971X(2006)22[497:AOBABT];2.
    1. Allan S.A. Susceptibility of adult mosquitoes to insecticides in aqueous sucrose baits. J. Vector Ecol. 2011;36:59–67. doi: 10.1111/j.1948-7134.2011.00141.x.
    1. Clements A.N. The Biology of Mosquitoes. CABI Publishing; London, UK: 1999. Volume 2: Sensory Reception and Behavior.
    1. Lea A.O. Sugar-baited insecticide residues against mosquitoes. Mosq. News. 1965;25:65–66.
    1. Schlein Y., Pener H. Bait-fed Culex pipiens carry the larvicide Bacillus sphaericus to larval habitats. Med. Vet. Entomol. 1990;4:283–288. doi: 10.1111/j.1365-2915.1990.tb00441.x.
    1. Xue R.D., Barnard D.R. Boric acid bait kills adult mosquitoes (Diptera: Culicidae) J. Econ. Entomol. 2003;96:1559–1562. doi: 10.1093/jee/96.5.1559.
    1. Insecticide Resistance Action Committee Mode of Action Labeling of Insecticides. [(accessed on 16 December 2016)]; Available online: .
    1. Ali A., Xue R.D., Barnard D.R. Effects of sublethal exposure to boric acid sugar bait on adult survival, host-seeking, blood feeding behavior, and reproduction of Stegomyia albopictus. J. Am. Mosq. Control Assoc. 2006;22:464–468. doi: 10.2987/8756-971X(2006)22[464:EOSETB];2.
    1. Lindh J.M., Terenius O., Eriksson-Gonzales K., Knols B.G.J., Faye I. Re-introducing bacteria in mosquitoes—A method for determination of mosquito feeding preferences based on colored sugar solutions. Acta Trop. 2006;99:173–183. doi: 10.1016/j.actatropica.2006.07.008.
    1. Shin E., Park C., Ahn Y.-J., Lee D.-K., Chang. K.-S. Insecticidal and repellent activities of insecticide-sucrose solutions to Culex pipiens molestus (Diptera: Culicidae) under laboratory and field conditions. Pest Manag. Sci. 2011;67:665–671. doi: 10.1002/ps.2106.
    1. Coy M.R., Sanscrainte N.D., Chalaire K.C., Inberg A., Maayan I., Glick E., Paldi N., Becnel J.J. Gene silencing in adult Aedes aegypti mosquitoes through oral delivery of double-stranded RNA. J. Appl. Entomol. 2012;136:741–748. doi: 10.1111/j.1439-0418.2012.01713.x.
    1. Schlein Y., Müller G.C. Diurnal resting behavior of adult Culex pipiens in arid habitat in Israel and possible control measures with toxic sugar baits. Acta Trop. 2012;124:48–53. doi: 10.1016/j.actatropica.2012.06.007.
    1. Fulcher A., Scott J.M., Qualls W.A., Müller G.C., Xue R.D. Attractive toxic sugar bait mixed with pyriproxyfen sprayed on plants against adult larval Aedes albopictus (Diptera: Culicidae) J. Med. Entomol. 2014;51:896–899. doi: 10.1603/ME13243.
    1. Hossain T.T., Fulcher A., Davidson C., Beier J.C., Xue R.D. Evaluation of boric acid sprayed on plants against salt marsh mosquitoes, Aedes taeniorhynchus (Diptera: Culicidae) Fla. Entomol. 2014;97:1865–1868. doi: 10.1653/024.097.0469.
    1. Bidlingmayer W.I., Hem D.G. Sugar feeding by Florida mosquitoes. Mosq. News. 1973;33:535–538.
    1. Heil M. Nectar: Generation, regulation and ecological functions. Trends Plant Sci. 2011;16:191–200. doi: 10.1016/j.tplants.2011.01.003.
    1. Knab F. Mosquitoes as flower visitors. JNY Entomol. Soc. 1907;15:215–219.
    1. Müller G.C., Schlein Y. Sugar questing mosquitoes in arid areas gather on scarce blossoms that can be used for control. Int. J. Parasitol. 2006;36:1077–1080.
    1. Theobald F.V. A Monograph of the Culicidae or Mosquitoes. Volume 1 Clowes & Sons; London, UK: 1901.
    1. Joseph S.R. Fruit feeding of mosquitoes in nature. Proc. Annu. Meet. N.J. Mosq. Exterm. Assoc. 1970;57:125–131.
    1. Müller G.C., Beier J.C., Traore S.F., Toure M.B., Traore M.M., Bah S., Doumbia S., Schlein Y. Field experiments of Anopheles gambiae attraction to local fruits/seedpods and flowering plants in Mali to optimize strategies for malaria vector control in Africa using attractive toxic sugar bait methods. Malar. J. 2010;9:262.
    1. Müller G.C., Xue R.D., Schlein Y. Differential attraction of Aedes albopictus in the field to flowers, fruits, and honeydew. Acta Trop. 2011;118:45–49. doi: 10.1016/j.actatropica.2011.01.009.
    1. Xue R.D., Ali A., Kline D.L., Barnard D.R. Field evaluation of boric acid-and fipronil-based bait stations against adult mosquitoes. J. Am. Mosq. Control Assoc. 2008;25:415–418. doi: 10.2987/5683.1.
    1. Beier J.C., Müller G.C., Gu W., Arheart K.L., Schlein Y. Attractive toxic sugar bait (ATSB) methods decimate populations of Anopheles malaria vectors in arid environments regardless of the local availability of favored sugar-source blossoms. Malar. J. 2012;11:31. doi: 10.1186/1475-2875-11-31.
    1. Qualls W.A., Müller G.C., Revay E.E., Allan S.A., Arheart K.L., Beier J.C., Smith M.L., Scott J.M., Kravchenko V.D., Hausmann A., et al. Evaluation of attractive toxic sugar bait (ATSB)-barrier for control of vector and nuisance mosquitoes and its effect on non-target organisms in sub-tropical environments in Florida. Acta Trop. 2014;131:104–110. doi: 10.1016/j.actatropica.2013.12.004.
    1. Jiang Y., Mulla M.S. Susceptibility of the adult eye gnat Liohippelates collusor (Diptera: Chloropidae) to neonicotinoids and spinosad insecticides. J. Vector Ecol. 2006;31:65–70. doi: 10.3376/1081-1710(2006)31[65:SOTAEG];2.
    1. Müller G.C., Junnila A., Schlein Y. Effective control of adult Culex pipiens by spraying an attractive toxic sugar bait in the vegetation near larval habitats. J. Med. Entomol. 2010;47:63–66. doi: 10.1093/jmedent/47.1.63.
    1. Müller G.C., Schlein Y. Efficacy of toxic sugar baits against cistern-dwelling Anopheles claviger. Trans. R. Soc. Trop. Med. 2008;102:147–149. doi: 10.1016/j.trstmh.2008.01.008.
    1. Müller G.C., Junnila A., Qualls W.A., Revay E.E., Kline D.L., Allan S.A., Schlein Y., Xue R.D. Control of Culex quinquefasciatus in a storm drain system in Florida using attractive toxic sugar bait. Med. Vet. Entomol. 2010;24:346–351.
    1. Qualls W.A., Xue R.D., Revay E.E., Allan S.A., Müller G.C. Implications for operational control of adult mosquito production in cisterns and wells in St. Augustine, FL using attractive sugar baits. Acta Trop. 2012;124:158–161. doi: 10.1016/j.actatropica.2012.07.004.
    1. Revay E.E., Müller G.C., Qualls W.A., Kline D.L., Naranjo D.P., Arheart K.L., Kravchenko V.D., Yfremova Z., Hausmann A., Beier J.C., et al. Control of Aedes albopictus with attractive toxic sugar baits (ATSB) and potential impact on non-target organisms in St. Augustine, Florida. Parasitol. Res. 2014;113:73–79. doi: 10.1007/s00436-013-3628-4.
    1. Qualls W.A., Müller G.C., Traore S.F., Traore M.M., Arheart K.L., Doumbia S., Schlein Y., Kravchenko V.D., Xue R.D., Beier J.C. Indoor use of attractive toxic sugar bait (ATSB) to effectively control malaria vectors in Mali, West Africa. Malar. J. 2015;14:301. doi: 10.1186/s12936-015-0819-8.
    1. Naranjo D.P., Qualls W.A., Müller G.C., Samson D.M., Roque D., Alimi T., Arheart K., Beier J.C., Xue R.D. Evaluation of boric acid baits against Aedes albopictus (Diptera: Culicidae) in tropical environments. Parasitol. Res. 2013;112:1583–1587. doi: 10.1007/s00436-013-3312-8.
    1. Stewart Z.P., Oxborough R.M., Tungu P.K., Kirby M.J., Rowland M.W., Irish S.R. Indoor applications of attractive toxic sugar bait (ATSB) in combination with mosquito nets for control of pyrethroid-resistant mosquitoes. PLoS ONE. 2013;8:e84168. doi: 10.1371/journal.pone.0084168.
    1. Junnila A., Revay E.E., Müller G.C., Kravchenko Y., Qualls W.A., Xue R.D., Allan S.A., Beier J.C., Schlein Y. Efficacy of attractive toxic sugar bait (ATSB) against Aedes albopictus with garlic oil encapsulated in beta-cyclodextrin as the active ingredient. Acta Trop. 2015;152:195–200. doi: 10.1016/j.actatropica.2015.09.006.
    1. Revay E.E., Schlein Y., Tsabari O., Kravchenko V., Qualls W.A., Xue R.D., Beier J.C., Traore S.F., Doumbia S., Hausmann A., et al. Formulation of attractive toxic sugar bait (ATSB) with safe EPA-exempt substance significantly diminishes the Anopheles sergentii population in a desert oasis. Acta Trop. 2015;150:29–34. doi: 10.1016/j.actatropica.2015.06.018.
    1. Schlein Y., Müller G.C. Decrease of larval and subsequent adult Anopheles sergentii populations following feeding of adult mosquitoes from Bacillus sphaericus- containing attractive sugar baits. Parasit. Vectors. 2015;8:244. doi: 10.1186/s13071-015-0845-y.
    1. Khallaayoune K., Qualls W.A., Revay E.E., Allan S.A., Arheart K.L., Kravchenko V.D., Xue R.D., Schlein Y., Beier J.C., Müller G.C. Attractive toxic sugar baits: Control of mosquitoes with the low-risk active ingredient dinotefuran and potential impacts on non-target organisms in Morocco. Environ. Entomol. 2013;42:1040–1045. doi: 10.1603/EN13119.
    1. Florida Coordinating Council on Mosquito Control . Florida Mosquito Control: The State Mission as Defined by Mosquito Controllers, Regulators, and Environmental Managers. Florida Coordinating Council on Mosquito Control, University of Florida; Gainesville, FL, USA: 1998.
    1. Rose R.I. Pesticides and public health: Integrated methods of mosquito management. Emerg. Infect. Dis. 2001;7:17–23. doi: 10.3201/eid0701.010103.

Source: PubMed

Sponsors en medewerkers

Medische omstandigheden

Geneesmiddelinterventies

3
Abonneren