Mosquito larvicides derived from microbial organisms and insect growth regulators have been increasingly used to control mosquito larvae worldwide. Their relative target specificity, nontarget safety, and environmentally friendly profile have been well documented. The current chapter was intended to review and analyze the relevant information regarding resistance development and resistance management tactics. Bacillus thuringiensis israelensis de Bajac (B.t.i.) is a quick-acting and highly target-specific biopesticide against mosquitoes, blackflies, and other nematoceran species. Resistance development toward intact complementary toxin complex of B.t.i. was rare; however, low to high levels of resistance to individual toxins have occurred in laboratory mosquito populations. The toxins from bacterium Bacillus sphaericus Neide (recently renamed Lysinibacillus sphaericus Meyer and Neide) is another highly active larvicide against mosquitoes, toward which low to high levels of resistance have occurred in both laboratory and field mosquito populations. The Cyt1A toxin from B.t.i. and Mtx toxin from certain strains of B. sphaericus are the key components in resistance management to B.t.i. and B. sphaericus. The resistance management strategies have been well developed and implemented. Spinosad derived from Saccharopolyspora spinosa Mertz and Yao has been recently used for mosquito control; high levels of resistance and cross-resistance have occurred in laboratory mosquito populations and no management tactics have ever been developed. Methoprene has been used to control mosquitoes for decades, and low to high levels of resistance have been occasionally reported in both laboratory and field mosquito populations. Studies on mechanism and management of methoprene resistance are quite meager. Very little attention has been paid to the resistance management in mosquitoes to other insect growth regulators such as pyriproxyfen and diflubenzuron. The prevention of resistance and restoration of susceptibility in mosquitoes to these biorational larvicides are crucial to the success of sustainable integrated mosquito management.
- Microbial larvicides
- Insect growth regulators
- Mosquito control
- Resistance management
Mosquitoes and mosquito-borne diseases remain one of the leading public health concerns and socioeconomic burdens of mankind globally, particularly in tropical and subtropical regions. Nowadays, human and animal population movement, freight exchange, fast demographic growth, economic development, and subsequent environmental impact further elevate the scope and magnitude of the problem. Mosquito control is often the only or most effective way of the integrated management to combat mosquito-borne illnesses. Considering the strict governmental regulations, high environmental vulnerability, and increasing demand of mosquito control upon emergence, and spreading of mosquito-borne diseases, ecologically friendly management approaches based on microbial and insect growth regulator larvicides have been the great promise for their high activity and efficacy, target specificity, and environmental and nontarget safety profile. However, the development of resistance in the mosquito populations to these biorational larvicides has been reported since the past decades. In order to maintain the sustainability of mosquito control, susceptibility monitoring and resistance management tactics toward these available control tools must be developed and implemented.
Bacillus thuringiensis subsp israelensis ( B.t.i.)
2.1. Field occurrence
Generally, the risk of resistance development to wild-type
2.2. Laboratory studies
Multiple attempts to select resistance in laboratory colonies of
Exposures to individual toxins of
Cyt1A, a cytolytic endotoxin of
The high levels of resistance to CryIV in
It was discovered recently that the mosquitocidal toxins (Mtx) from some
The mosquitocidal activity of some strains of
3.1. Field occurrence
The earliest resistance in field populations was reported in
3.2. Laboratory studies
Furthermore, once mosquitoes develop resistance to a given strain of
3.3. Resistance mechanism
It is mostly believed that recessive genetic mechanism is involved in resistance to
3.4. Resistance management
Efforts were made to find practical strategies for controlling resistant mosquitoes and to prevent or delay the development of resistance in wild mosquito populations. In Nonthaburi Province, Thailand, the larvae of
3.5. Fitness cost of resistance
In a laboratory studies , the resistant strains showed some disadvantages such as lower fecundity and fertility, but higher survival rates were observed at the same time. The immature stages of the females from the resistant population developed slightly faster as compared with those of the susceptible strains, which could result in a shorter generation time. The similar findings are that the resistant colony showed lower fecundity and fertility and slower development than the susceptible colony . However, the opposite results were achieved in another study where the resistant colony did not display biological costs regarding fecundity, fertility, and pupal weight .
Spinosad, a biopesticide consisting of spinosyn A (C41H65NO10) and D (C42H67NO10), is produced by a naturally occurring, soil-dwelling bacterium,
5. Insect growth regulators
5.1. Juvenile hormone analogs (methoprene and pyriproxyfen)
Methoprene, hydroprene, kinoprene, and triprene were synthesized in 1960s. These insect growth regulators interrupt juvenile hormone balance during the transition from the late 4th instar larvae to pupae and adults. Most mortality occurs at pupal stage or incompletely emerged adults. Another juvenile hormone analog pyriproxyfen was synthesized in 1970s, the IRG activity of which is much higher than methoprene . The earliest experimental studies on potential of resistance development in mosquitoes to juvenile hormone analogs were in 1973 . The collective results indicated low risk of resistance development [82–86]. For example, the selection of
Data are meager with regard to resistance development in wild populations of mosquitoes.
5.2. Chitin synthesis inhibitor (diflubenzuron)
Diflubenzuron was synthesized in mid 1970s by Philips-Duphar B.V. This compound is a nonselective chitin synthesis inhibitor that interrupts formation of exoskeleton, interferes with integrity of cuticle, and causes leakage of body fluid and ultimately mortality of target organisms. Diflubenzuron acts on all stages of the mosquito life cycle, larval stages in particular, younger larvae show higher susceptibility. Up to date, studies on resistance management are limited to laboratory populations. For instance,
This chapter reviewed and analyzed historical data of resistance and resistance management in mosquitoes to biorational larvicides with microbial and IGR origins. Bacterial larvicide
There is no doubt about the consequence resulted from occurrence and spread of resistance, such as cost increase of control operations, outbreak of vector populations, and vector-borne diseases. On the other hand, there are some negative impacts of resistance development on mosquito biological fitness, such as shortened longevity and reduced fecundity [77, 78, 94], which may lower the vectorial capacity [95–97]. Therefore, evaluation on the exact impact of vector resistance to pesticides on the epidemiology of vector-borne diseases can be complicated. During the past decades, pesticide resistance development and spread promoted banning or limited applications of nonselective, long-lasting synthetic pesticides. At the same time, this situation also advanced toxicological studies and detection technology of resistance, as well as the research, development, and application of biorational pesticides, and other mosquito control techniques.
It must be emphasized that the occurrence of resistance to pesticides in mosquitoes has been on the rise, including cases to the biorational pesticides discussed in this chapter. For long-term benefits, susceptibility monitoring by standardized protocols must be implemented at the same time when a pesticide is introduced to the control operations. The collaboration among academic research, industrial development, and field application and evaluation is crucial to prolong the life and enhance efficacy of pesticides, as well as protect the environment and nontarget organisms.
The author is grateful to INTECH for the invitation to write this Chapter and its efforts and support to make the publication possible.
Roh JY, Choi JY, Li MS, Jin BR, Je YH. Bacillus thuringiensisas a specific, safe, and effective tool for insect pest control. J. Microbiol. Biotechnol. 2007; 17:547–559.
Goldberg LJ, Margalit JA. Bacterial spore demonstrating rapid larvicidal activity against Anopheles sergentii, Uranotaenia unguiculata, Culex univitattus, Aedes aegyptiand Culex pipiens.Mosq. News 1977; 37:355–358.
Margalit J, Dean D. The story of Bacillus thuringiensisvar. israelensis(B.t.i.). J. Am. Mosq. Control Assoc. 1985; 1:1–7.
Tabashnik BE. Evaluation of synergism among Bacillus thuringiensistoxins. Appl. Environ. Microbiol. 1992; 58:3343–3346.
Poncet S, Délécluse A, Klier A, Rapoport G. Evaluation of synergistic interactions among the CryIVA, CryIVB, and CryIVD toxic components of B. thuringiensis subsp. israelensiscrystals. J. Invertebr. Pathol. 1995; 66:131–135.
Crickmore N, Bone EJ, Williams JA, Ellar DJ. Contribution of the individual components of the δ-endotoxin crystal to the mosquitocidal activity of Bacillus thuringiensissubsp. israelensis. FEMS Microbiol. Lett. 1995; 131:249–254.
Wirth MC, Jiannino JJ, Federici BA, Walton WE. Synergy between toxins of Bacillus thuringiensissubsp. israelensisand Bacillus sphaericus. J. Med. Entomol. 2004; 41:935–41.
Gibbs KE, Brautigam FC, Stubbs CS, Zibilske LM. Experimental applications of B.t.i.for larval black fly control: persistence and downstream carry, efficacy, impact on non-target invertebrates and fish feeding. Maine Agricultural Experiments Station University of Maine. Tech. Bull. 123. October 1986. 25 pp.
Merritt RW, Walker ED, Wilzbach MA, Cummins KW, Morgan WT. A broad evaluation of B.t.i. for black fly (Diptera: Simuliidae) control in a Michigan river: efficacy, carry and nontarget effects on invertebrates and fish. J. Am. Mosq. Control Assoc. 1989; 5:397–415.
Ali A. Bacillus thuringiensisserovar. israelensis(ABG-6108) against chironomids and some non-target aquatic invertebrates. J. Invertebr. Pathol. 1980; 38:264–272.
Mulla MS, Chaney JD, Rodcharoen J. Control of nuisance midges (Diptera: Chironomidae) with the microbial larvicide Bacillus thuringiensisvar. israelensisin a man-made lake in Southern California. Bull. Soc. Vector Ecol. 1990; 15:176–184.
Rodcharoen J, Mulla MS, Chaney JD. Microbial larvicides for the control of nuisance aquatic midges (Diptera: Chironomidae) inhabiting mesocosms and man-made lakes in California. J. Am. Mosq. Control Assoc. 1991; 7:56–62.
Becker N, Ludwig M. Investigations on possible resistance in Aedes vexansfield populations after a 10-year application of Bacillus thuringiensis israelensis. J. Am. Mosq. Control Assoc 1993; 9:221–224.
Paul A, Harrington LC, Zhang L, Scott JG. Insecticide resistance in Culex pipiensin New York. J. Am. Mosq. Control Assoc. 2005; 21:305–309.
Vasquez MI, Violaris M, Hadjivassilis A, Wirth MC. Susceptibility of Culex pipiens(Diptera: Culicidae) field populations in Cyprus to conventional organic insecticides, Bacillus thuringiensissubsp. israelensis, and methoprene. J. Med. Entomol. 2009; 46:881–887.
Wirth MC, Ferrari JA, Georghiou GP. Baseline susceptibility to bacterial insecticides in populations of Culex pipienscomplex (Diptera: Culicidae) from California and from the Mediterranean Island of Cyprus. J. Med. Entomol. 2001; 94:920–928.
Vasquez-Gomez M. Investigations of the possibility of resistance to Bacillus thuringiensisser. H-14 in Culex quinquefasciatusthrough accelerated selection pressure in the laboratory. Riverside: University of California 1983.
Goldman I, Arnold J, Carlton BC. Selection for resistance to Bacillus thuringiensissubspecies israelensisin field and laboratory populations of the mosquito Aedes aegypti.J. Invertebr. Pathol. 1986; 47:317–24.
Saleh MS, El-Meniawi FA, Kelada NL, Zahran HM. Resistance development in mosquito larvae Culex pipiensto the bacterial agent Bacillus thuringiensisvar. israelensis. J. Appl. Entomol. 2003; 127:29–32.
Mittal P. Laboratory selection to investigate the development of resistance to Bacillus thuringiensisvar. israelensisH-14 in Culex quinquefasciatusSay (Diptera: Culicidae). Natl. Acad. Lett. India 2005; 28:281–283.
Tetreau G, Bayyareddy K, Jones CM, Stalinski R, Riaz, MA, Paris, M David, JP, Adang MJ, Després L. Larval midgut modifications associated with B.t.iresistance in the yellow fever mosquito using proteomic and transcriptomic approaches. BMC Genomics 2012; 13:248. doi:10.1186/1471-2164-13-248.
Tetreau G, Stalinski R, David JP, Després L. Monitoring resistance to Bacillus thuringiensissubsp. israelensisin the field by performing bioassays with each Cry toxin separately. Mem. Inst. Oswaldo Cruz. 2013; 108:894–900.
Georghiou GP, Wirth MC. Influence of exposure to single versus multiple toxins of Bacillus thuringiensisvar. israelensison the development of resistance in the mosquito Culex quinquefasciatus(Diptera: Culicidae). Appl. Environ. Microbiol. 1997; 63:1095–1101.
Wirth MC, Délécluse A, Walton WE. Laboratory selection for resistance to Bacillus thuringiensissubsp. jegathesanor a component toxin, Cry11B, in Culex quinquefasciatus(Diptera: Culicidae). J. Med. Entomol. 2004; 41:435–441.
Wirth MC, Georghiou GP. Cross-resistance among CryIV toxins of Bacillus thuringiensissubsp. israelensisin Culex quinquefasciatus(Diptera: Culicidae). J. Econ. Entomol. 1997; 90:1471–1477.
Wirth MC, Delécluse A, Federici BA, Walton WE. Variable cross resistance to Cry11B from Bacillus thuringiensissubsp. jegathesanin Culex quinquefasciatus(Diptera: Culicidae) resistant to single or multiple toxins from Bacillus thuringiensissubsp. israelensis.Appl. Environ. Microbiol. 1998; 64:4174–4179.
Wirth MC, Delécluse A, Walton WE. Lack of cross resistance to Cry19A from Bacillus thuringiensissubsp. jegathesanin Culex quinquefasciatus(Diptera: Culicidae) resistant to Cry toxins from Bacillus thuringiensissubsp. israelensis.Appl. Environ. Microbiol. 2001; 67:1956–1958.
Chueng, PYK, Buster D, Hammock BD. Lack of mosquitocidal activity by the cytolytic protein of the Bacillus thuringiensissubsp. israelensisparasporal crystal. Current Microbiol. 1987; 15:21–23.
Wirth MC, Georghiou GP, Federici BA. CytA enables CryIV endotoxins of Bacillus thuringiensisto overcome high levels of CryIV resistance in the mosquito, Culex quinquefasciatus. Proc. Natl. Acad. Sci. U.S.A. 1997; 94:10536–10540.
Wirth MC, Park HW, Walton WE, Federici BA. Cyt1A of Bacillus thuringiensisdelays resistance to Cry11A in the mosquito Culex quinquefasciatus. Appl. Environ. Microbiol. 2005; 71:185–189.
Pérez C, Fernandez LL, Sun J, Folch JL, Gill SS, Soberón M. Bacillus thuringiensissubsp. israelensisCyt1Aa synergizes Cry11Aa toxin by functioning as a membrane-bound receptor. Proc. Natl. Acad. Sci. 2005; 102:18303–18308.
Pérez C, Munoz-Garcia C, Portugal LC, Sanchez J, Gill SS, Soberón M, Bravo A. Bacillus thuringiensissubsp. israelensisCyt1Aa enhances activity of Cry11Aa toxin by facilitating the formation of a pre-pore oligomeric structure. Cell Microbiol. 2007; 9:2931–2937.
Wirth MC, Berry C, Walton WE, Federici BA. Mtx toxins from Lysinibacillus sphaericusenhance mosquitocidal cry-toxin activity and suppress cry-resistance in Culex quinquefasciatus. J. Invertebr. Pathol. 2014; 115:62–67.
Wirth MC. Mosquito resistance to bacterial larvicidal toxins. Open Toxinol. J. 2010; 3:126–140. doi: 10.2174/1875414701003010126].
Ahmed I, Yokota, A, Yamazoe, A, Fujiwara T. Proposal of Lysinibacillus boronitoleransgen. nov. sp. nov., and transfer of Bacillus fusiformisto Lysinibacillus fusiformiscomb. nov. and Bacillus sphaericus to Lysinibacillus sphaericuscomb. nov. Int. J. Syst. Evol. Microbiol. 2007; 57 (Pt 5):1117–1125.
Sinègre G, Babinot M, Quermel JM, Gavon B. First field occurrence of Culex pipiensresistance to Bacillus sphaericusin southern France: 1994. P17. Proceedings of the 8th European Meeting of Society for Vector Ecology, September 5–8, 1994; Barcelona, Spain. Society for Vector Ecology, Santa Ana, California, 1997.
Silva-Filha MH, Regis L, Nielsen-LeRoux C, Charles JF. Low level resistance to Bacillus sphaericusin a field-treated population of Culex quinquefasciatus(Diptera: Culicidae). J. Econ. Entomol. 1995; 88:525–530.
Rao DR, Mani TR, Rajendran R, Joseph AS, Gajanana A, Reuben R. Development of a high-level of resistance to Bacillus sphaericusin a field population of Culex quinquefasciatusfrom Kochi, India. J. Am. Mosq. Control Assoc. 1995; 11:1–5.
Adak T, Mittal PK, Raghavendra K, Subbaro SK, Ansari MA, Sharma VP. Resistance to Bacillus sphaericusin Culex quinquefasciatusSay 1823. Curr. Sci. 1995; 69:695–698.
Nielsen-LeRoux C, Pasquier F, Charles JF, Sinègre G, Gaven B, Pasteur N. Resistance to Bacillus sphaericusinvolves different mechanisms in Culex pipiens(Diptera: Culicidae) larvae. J. Med. Entomol. 1997; 34:321–327.
Yuan Z, Zhang Y, Cai Q, Liu EY. High-level field resistance to Bacillus sphaericusC3-41 in Culex quinquefasciatusfrom southern China. Biocon. Sci. Technol. 2000; 10:41–49.
Chevillon C, Bernard C, Marquine M, Pasteur N. Resistance to Bacillus sphaericusin Culex pipiens(Diptera: Culicidae): interaction between recessive mutants and evolution in southern France. J. Med. Entomol. 2001; 38:657–664.
Nielsen-LeRoux C, Pasteur N, Prètre J, Charles JF, Ben Sheik H, Chevillon C. High resistance to Bacillus sphaericusbinary toxin in Culex pipiens(Diptera: Culicidae): the complex situation of west Mediterranean countries. J. Med. Entomol. 2002; 39:729–735.
Mulla MS, Thavara U, Tawatsin A, Chomposri J, Su T. Emergence of resistance and resistance management in field populations of tropical Culex quinquefasciatusto the microbial control agent Bacillus sphaericus. J. Am. Mosq. Control Assoc. 2003; 19:39–46.
Su T, Mulla M S. Documentation of high level Bacillus sphaericus-resistance in tropical Culex quinquefasciatuspopulations from Thailand. J. Am. Mosq. Control Assoc. 2004; 20:405–411.
Su T, Soliman BA, Chaney JD, Mulla MS, Beehler JW. Susceptibility of Culexmosquitoes breeding in dairy ponds before and after treatment with Bacillus sphaericusformulation. Proc. Pap. Mosq. Vector Control Assoc. Calif 2001; 69:110–116.
Rodcharoen J, Mulla MS. Resistance development in Culex quinquefasciatus(Diptera: Culicidae) to Bacillus sphaericus. J. Econ. Entomol. 1994; 87:1133–1140.
Zahiri NS, Su T, Mulla MS. Strategies for the management of resistance in mosquito to the microbial control agent Bacillussphaericus.J. Med. Entomol. 2002; 39:513–520.
Zahiri NS, Mulla MS. Susceptibility profile of Culex quinquefasciatus(Diptera: Culicidae) to Bacillus sphaericuson selection with rotation and mixture of B. sphaericusand B. thuringiensis israelensis.J. Med. Entomol. 2003; 40:672–677.
Wirth MC, Georghiou GP, Malik JI, Hussain G. Laboratory selection for resistance to Bacillus sphaericusin Culex quinquefasciatus(Diptera: Culicidae) from California, USA. J. Med. Entomol. 2000; 37:534–540.
Pei G, Oliveira CMF, Yuan Z, Nielsen-LeRoux C, Silva-Filha MH, Yan J, Regis L. A strain of Bacillus sphaericuscauses slower development of resistance in Culex quinquefasciatus.Appl. Environ. Microbiol. 2002; 88:3003–3009.
Amorim LB, Oliveira CMF, Rios EM, Regis L, Silva-Filha MHNL. Development of Culex quinquefasciatusresistance to Bacillus sphaericusstrain IAB59 needs long term selection pressure. Biol. Control 2007; 42:155–160.
Amorim LB, de Barros RA, Chalegre KD, de Oliveira CM, Regis LN, Silva-Filha MH. Stability of Culex quinquefasciatusresistance to Bacillus sphaericusevaluated by molecular tools. Insect Biochem. Mol. Biol. 2010; 40:311–316. doi: 10.1016/j.ibmb.2010.02.002.
Poopathi S, Mani TR, Raghunatha D, Baskram G, Kabilan L. Cross-resistance to Bacillus sphaericusstrains in Culex quinquefasciatusresistant to B. sphaericus1593M. Southeast Asian J. Trop. Med. Public Health 1999; 30:478–481.
Rodcharoen J, Mulla MS. Cross-resistance to Bacillus sphaericusstrains in Culex quinquefasciatus.J. Am. Mosq. Control Assoc. 1996; 12:247–250.
Poopathi S, Kabilan L, Mani TR, Raghunatha RD, Baskaran G. Observation of low tolerance to Bacillus thuringiensisvar israelensisin Culex quinquefasciatusresistant to Bacillus sphaericus. Entomon. Ember. 2000; 25:201–208.
Yuan ZM, Pei GF, Regis L, Nielsen-LeRoux C, Cai QX. Cross resistance between strains of Bacillus sphaericusbut not B. thuringiensis israelensisin colonies of the mosquito Culex quinquefasciatus.Med. Vet. Entomol. 2003; 17:251–256.
Nielsen-LeRoux C, Rao D, Rodcharoen J, Carron A, Mani TR, Hamon S, Mulla MS .Various levels of cross-resistance to Bacillus sphaericusstrains in Culex pipiens(Diptera: Culicidae) colonies resistant to B. sphaericusstrain 2362. Appl. Environ. Microbiol. 2001; 67:5049–5054.
Oliveira CMF, Silva-Filha MH, Nielsen-LeRoux C, Pei G, Yuan Z, Regis L. Inheritance and mechanism of resistance to Bacillus sphaericusin Culex quinquefasciatus(Diptera: Culicidae) from China and Brazil. J. Med. Entomol. 2004; 41:58–64.
Darboux I, Charles JF, Pauchet Y, Warat S, Pauron D. Transposon mediated resistance to Bacillus sphaericusin a field-evolved population of Culex pipiens(Diptera: Culicidae). Cell Microbiol. 2007; 9: 2022–2029.
Darboux I, Pauchet Y, Castella C, Silva-Filha MH, Nielsen-LeRoux C, Charles JF, Pauron, D. Loss of the membrane anchor of the target receptor is a mechanism of bioinsecticide resistance. Proc. Natl. Acad. Sci. U.S.A. 2002; 99:5830–5835.
Nielsen-LeRoux C, Charles JF, Thièry I, Georghiou GP. Resistance in a laboratory population of Culex quinquefasciatus(Diptera: Culicidae) to Bacillus sphaericusbinary toxin is due to a change in the receptor on midgut brush-border membrane. Eur. J. Biochem. 1995; 228:206–210.
Romão TP, de Melo Chalegre KD, Key S, Ayres CF, Fontes de Oliveira CM, de-Melo-Neto OP, Silva-Filha MH. A second independent resistance mechanism to Bacillus sphaericusbinary toxin targets its α-glucosidase receptor in Culex quinquefasciatus.FEBS J. 2006; 273:1556–1568.
Chalegre KD, Romão TP, Amorim LB, Anastacio DB, de Barros RA, de Oliveira CM, Regis L, de-Melo-Neto OP, Silva-Filha MH. Detection of an allele conferring resistance to Bacillus sphaericusbinary toxin in Culex quinquefasciatuspopulations by molecular screening. Appl. Environ. Microbiol. 2009; 75:1044–1049.
Chalegre KD, Romão TP, Tavares DA, Santos EM, Ferreira LM, Oliveira CMF, de-Melo-Neto OP, Silva-Filha MHNL. Novel mutations associated with resistance to Bacillus sphaericusin a polymorphic region of the Culex quinquefasciatuscqm1 gene. Appl. Environ. Microbiol. 2012; 78:6321–6326. doi: 10.1128/AEM.01199-12.
Guo QY, Cai QX, Yan JP, Hu XM, Zheng DS, Yuan ZM. Single nucleotide deletion of cqm1 gene results in the development of resistance to Bacillus sphaericusin Culex quinquefasciatus. J. Insect Physiol. 2013; 59:967–973.
Rodcharoen J, Mulla MS. Comparative ingestion rates of Culex quinquefasciatus(Diptera: Culicidae) susceptible and resistant to Bacillus sphaericusJ. Invertebr. Pathol. 1995; 66:242–248.
Sun F, Yuan Z, Li T, Zhang Y, Yu J, Pang Y. Reduction of resistance of Culex pipienslarvae to the binary toxin from Bacillus sphaericusby coexpression of cry4Bafrom Bacillus thuringiensissubsp. israelensiswith the binary toxin. World J. Microbiol. Biotechnol. 2001; 17:385–389.
Wirth MC, Walton WE, Federici BA. Cyt1A from Bacillus thuringiensisrestores toxicity of Bacillus sphaericusagainst resistant Culex quinquefasciatus(Diptera: Culicidae). J. Med. Entomol. 2000; 37:401–407.
Wirth MC, Jiannino JA, Federici BA Walton WE. Evolution of resistance toward Bacillus sphaericusor a mixture of B. sphaericus+Cyt1A from Bacillus thuringiensis, in the mosquito, Culex quinquefasciatus(Diptera: Culicidae). J. Invertebr. Pathol .2005; 88:154–162.
Chenniappan K, Ayyadurai N. Synergistic activity of Cyt1A from Bacillus thuringiensissubsp. israelensiswith Bacillus sphaericusB101 H5a5b against Bacillus sphaericusB101 H5a5b-resistant strains of Anopheles stephensiListon (Diptera: Culicidae). Parasitol. Res. 2011; 110:381–388.
Park HW, Bideshi DK, Federici BA. Recombinant strain of Bacillus thuringiensisproducing Cyt1A, Cry11B, and the Bacillus sphaericusbinary toxin. Appl. Environ. Microbiol. 2003; 69:1331–1334.
Park HW, Bideshi DK, Wirth MC, Johnson JJ, Walton WE, Federici BA. Recombinant larvicidal bacteria with markedly improved efficacy against Culexvectors of West Nile virus. Am. J. Trop. Med. Hyg. 2005; 72:732–738.
Federici BA, Park HW, Bideshi DK, Wirth MC, Johnson JJ, Sakano Y, Tang M. Developing recombinant bacteria for control of mosquito larvae. J. Am. Mosq. Control Assoc. 2007; 23:S164–175.
Poopathi S, Mani TR, Raghunatha RD, Baskaran G, Kabilan L. Evaluation of synergistic interaction between Bacillus sphaericusand a neem based biopesticide against Culex quinquefasciatuslarvae susceptible to Bacillus sphaericus. 1593M. Insect Sci. Appl .2002; 22:303–306.
Wei S, Cai Q, Cai Y, Yuan Z. Lack of cross-resistance to Mtx1 from Bacillus sphaericusin B. sphaericus-resistant Culex quinquefasciatus(Diptera: Culicidae). Pest. Manag. Sci. 2007; 63:190–193.
Rodcharoen J, Mulla MS. Biological fitness of Culex quinquefasciatus(Diptera; Culicidae) susceptible and resistant to Bacillus sphaericus.J. Med. Entomol. 1997; 34:5–10.
Oliveira CMD, Costa Filho F, Beltran JFN, Silva-Filha MH, Regis L. Biological fitness of a Culex quinquefasciatuspopulation and its resistance to Bacillus sphaericus.J. Am. Mosq. Control Assoc. 2003; 19:125–129.
Su T, Cheng ML. Resistance development in Culex quinquefasciatusto spinosad: a preliminary report. J. Am. Mosq. Control Assoc. 2012; 28:263–267.
Su T, Cheng ML. Laboratory selection of resistance to spinosad in Culex quinquefasciatus(Diptera: Culicidae). J. Med. Entomol. 2014; 51:421–427.
Su T, Cheng ML. Cross resistances in spinosad – resistant Culex quinquefasciatus(Diptera: Culicidae). J. Med. Entomol. 2014; 51:428–435.
Schaefer CH, Wilder WH. Insect development inhibitors. 2. Effects on target mosquito species. J. Econ. Entomol. 1973; 66:913–916.
Brown TM, Brown AW. Experimental induction of resistance to a juvenile hormone mimic. J. Econ. Entomol. 1974; 67:799–801.
Georghiou GP, Lin CS, Pasternak ME. Assessment of potentiality of Culex tarsalisfor development of resistance to carbamate insecticides and insect growth regulator. Proc. Papers 42nd Ann. Conf. Calif. Mosq. Control Assoc. 1974; 42:117.
Brown TM, Devries DH, Brown AWA. 1978. Induction of resistance to insect growth regulators. J. Econ. Entomol. 1978; 71:223–229.
Amin AM, White GB. Resistance potential of Culex quinquefasciatusagainst the insect growth regulators methoprene and diflubenzuron. Ent. Exp. Appl. 1984; 36:69–76.
Brown TM, Hooper GHS. Metabolic detoxication as a mechanism of methoprene resistance in Culex pipiens pipiens. Pestic. Biochem. Physiol. 1979; 12:79–86.
Brown TM, Brown AWA. Accumulation and distribution of methoprene in resistance Culex pipiens pipienslarvae. Ent. Exp. Appl. 1980; 27:11–22.
Dame DA, Wichterman GJ, Hornby JA. Mosquito ( Aedes taeniorhynchus) resistance to methoprene in an isolated habitat. J. Am. Mosq. Control Assoc. 1998; 14:200–203.
Cornel AJ, Stanich MA, Farley D, Mulligan FS III, Byde G. Methoprene tolerance in Aedes nigromaculisin Fresno County, California. J. Am. Mosq. Control Assoc. 2000; 16:223–238.
Cornel AJ, M. Stanich A, McAbee RD, Mulligan FS III. High level methoprene resistance in the mosquito Ochlerotatus nigromaculis(Ludlow) in central California. Pest Manag. Sci. 2002; 58:791–798.
Schaefer CH, Mulligan FS III. 1991. Potential for resistance to pyriproxyfen: a promising new mosquito larvicide. J. Am. Mosq. Control Assoc. 1991; 7:409–411.
Walker AL, Wood RJ. Laboratory selected resistance to diflubenzuron in larvae of Aedes aegypti. Pesti. Sci, 1986; 17:495–502.
Ferrari JA, Georghiou GP. Effects of insecticidal selection and treatment on reproductive potential of resistant, susceptible, and heterozygous strains of the southern house mosquito. J. Econ. Entomol. 1981; 74: 323–327.
Rivero A, Vézilier J, Weill M, Read AF, Gandon S. Insecticide control of vector-borne diseases: when is insecticide resistance a problem? PLoS Pathog. 2010; 6(8): e1001000. doi:10.1371/journal.ppat.1001000.
Alout H, Ndam NT, Sandeu MM, Djégbe I, Chandre F, Dabiré RK, Djogbénou LS, Corbel V, Cohuet A. Insecticide resistance alleles affect vector competence of Anopheles gambiae s.s.for Plasmodium falciparumfield isolates. PLoS One. 2013; 8(5): e63849.
Liu R, Gourley SA. Resistance to larvicides in mosquito populations and how it could benefit malaria control. European J. Appl. Math. 2013; 24:415–436.