Tribolium castaneum: A Model for Investigating the Mode of Action of Insecticides and Mechanisms of Resistance

Author(s): Janin Rösner, Benedikt Wellmeyer, Hans Merzendorfer*

Journal Name: Current Pharmaceutical Design

Volume 26 , Issue 29 , 2020


Become EABM
Become Reviewer
Call for Editor

Abstract:

The red flour beetle, Tribolium castaneum, is a worldwide insect pest of stored products, particularly food grains, and a powerful model organism for developmental, physiological and applied entomological research on coleopteran species. Among coleopterans, T. castaneum has the most fully sequenced and annotated genome and consequently provides the most advanced genetic model of a coleopteran pest. The beetle is also easy to culture and has a short generation time. Research on this beetle is further assisted by the availability of expressed sequence tags and transcriptomic data. Most importantly, it exhibits a very robust response to systemic RNA interference (RNAi), and a database of RNAi phenotypes (iBeetle) is available. Finally, classical transposonbased techniques together with CRISPR/Cas-mediated gene knockout and genome editing allow the creation of transgenic lines. As T. castaneum develops resistance rapidly to many classes of insecticides including organophosphates, methyl carbamates, pyrethroids, neonicotinoids and insect growth regulators such as chitin synthesis inhibitors, it is further a suitable test system for studying resistance mechanisms. In this review, we will summarize recent advances in research focusing on the mode of action of insecticides and mechanisms of resistance identified using T. castaneum as a pest model.

Keywords: ABC transporter, detoxification, efflux transporters, insecticide, metabolic resistance, pest model, target site resistance, Tribolium castaneum.

[1]
Pimentel D. Natural resources and an optimum human population. Earth Isl J 1994; 9: 26-7.
[http://dx.doi.org/10.1007/BF02208317]
[2]
Kendall HW, Pimentel D. Constraints on the expansion of the global food-supply. Ambio 1994; 23: 198-205.
[3]
Phillips TW, Throne JE. Biorational approaches to managing stored-product insects. Annu Rev Entomol 2010; 55: 375-97.
[http://dx.doi.org/10.1146/annurev.ento.54.110807.090451] [PMID: 19737083]
[4]
Bebber DP, Holmes T, Gurr SJ. The global spread of crop pests and pathogens. Glob Ecol Biogeogr 2014; 23: 1398-407.
[http://dx.doi.org/10.1111/geb.12214]
[5]
Lorenzen MD, Kimzey T, Shippy TD, Brown SJ, Denell RE, Beeman RW. piggyBac-based insertional mutagenesis in Tribolium castaneum using donor/helper hybrids. Insect Mol Biol 2007; 16(3): 265-75.
[http://dx.doi.org/10.1111/j.1365-2583.2007.00727.x] [PMID: 17316329]
[6]
Pavlopoulos A, Berghammer AJ, Averof M, Klingler M. Efficient transformation of the beetle Tribolium castaneum using the Minos transposable element: quantitative and qualitative analysis of genomic integration events. Genetics 2004; 167(2): 737-46.
[http://dx.doi.org/10.1534/genetics.103.023085] [PMID: 15238525]
[7]
Farnworth MS, Eckermann KN, Ahmed HMM, Mühlen DS, He B, Bucher G. The red flour beetle as model for comparative neural development: Genome editing to mark neural cells in Tribolium brain development. Methods Mol Biol 2020; 2047: 191-217.
[http://dx.doi.org/10.1007/978-1-4939-9732-9_11] [PMID: 31552656]
[8]
Gilles AF, Schinko JB, Averof M. Efficient CRISPR-mediated gene targeting and transgene replacement in the beetle Tribolium castaneum. Development 2015; 142(16): 2832-9.
[http://dx.doi.org/10.1242/dev.125054] [PMID: 26160901]
[9]
Richards S, Gibbs RA, Weinstock GM, et al. Tribolium Genome Sequencing Consortium. The genome of the model beetle and pest Tribolium castaneum. Nature 2008; 452(7190): 949-55.
[http://dx.doi.org/10.1038/nature06784] [PMID: 18362917]
[10]
Dönitz J, Schmitt-Engel C, Grossmann D, et al. iBeetle-Base: a database for RNAi phenotypes in the red flour beetle Tribolium castaneum. Nucleic Acids Res 2015; 43(Database issue): D720-5.
[http://dx.doi.org/10.1093/nar/gku1054] [PMID: 25378303]
[11]
Linz DM, Clark-Hachtel CM, Borràs-Castells F, Tomoyasu Y. Larval RNA interference in the red flour beetle, Tribolium castaneum. J Vis Exp 2014; (92): e52059
[http://dx.doi.org/10.3791/52059] [PMID: 25350485]
[12]
Schmitt-Engel C, Schultheis D, Schwirz J, et al. The iBeetle large-scale RNAi screen reveals gene functions for insect development and physiology. Nat Commun 2015; 6: 7822.
[http://dx.doi.org/10.1038/ncomms8822] [PMID: 26215380]
[13]
Dönitz J, Gerischer L, Hahnke S, Pfeiffer S, Bucher G. Expanded and updated data and a query pipeline for iBeetle-Base. Nucleic Acids Res 2018; 46(D1): D831-5.
[http://dx.doi.org/10.1093/nar/gkx984] [PMID: 29069517]
[14]
Beeman RW, Friesen KS, Denell RE. Maternal-effect selfish genes in flour beetles. Science 1992; 256(5053): 89-92.
[http://dx.doi.org/10.1126/science.1566060] [PMID: 1566060]
[15]
Hurst LD. scat+ is a selfish gene analogous to Medea of Tribolium castaneum. Cell 1993; 75(3): 407-8.
[http://dx.doi.org/10.1016/0092-8674(93)90375-Z] [PMID: 8221883]
[16]
Peters LL, Barker JE. Novel inheritance of the murine severe combined anemia and thrombocytopenia (Scat) phenotype. Cell 1993; 74(1): 135-42.
[http://dx.doi.org/10.1016/0092-8674(93)90301-6] [PMID: 8334700]
[17]
Muthukrishnan S, Merzendorfer H, Arakane Y, Yang Q. Chitin organizing and modifying enzymes and proteins involved in remodeling of the insect cuticle. Adv Exp Med Biol 2019; 1142: 83-114.
[http://dx.doi.org/10.1007/978-981-13-7318-3_5] [PMID: 31102243]
[18]
Agrawal S, Kelkenberg M, Begum K, et al. Two essential peritrophic matrix proteins mediate matrix barrier functions in the insect midgut. Insect Biochem Mol Biol 2014; 49: 24-34.
[http://dx.doi.org/10.1016/j.ibmb.2014.03.009] [PMID: 24680676]
[19]
Kelkenberg M, Odman-Naresh J, Muthukrishnan S, Merzendorfer H. Chitin is a necessary component to maintain the barrier function of the peritrophic matrix in the insect midgut. Insect Biochem Mol Biol 2015; 56: 21-8.
[http://dx.doi.org/10.1016/j.ibmb.2014.11.005] [PMID: 25449129]
[20]
Schröder R, Beermann A, Wittkopp N, Lutz R. From development to biodiversity-Tribolium castaneum, an insect model organism for short germband development. Dev Genes Evol 2008; 218(3-4): 119-26.
[http://dx.doi.org/10.1007/s00427-008-0214-3] [PMID: 18392874]
[21]
Benton MA. A revised understanding of Tribolium morphogenesis further reconciles short and long germ development. PLoS Biol 2018; 16(7) e2005093
[http://dx.doi.org/10.1371/journal.pbio.2005093] [PMID: 29969459]
[22]
Altincicek B, Knorr E, Vilcinskas A. Beetle immunity: Identification of immune-inducible genes from the model insect Tribolium castaneum. Dev Comp Immunol 2008; 32(5): 585-95.
[http://dx.doi.org/10.1016/j.dci.2007.09.005] [PMID: 17981328]
[23]
Altincicek B, Elashry A, Guz N, Grundler FM, Vilcinskas A, Dehne HW. Next generation sequencing based transcriptome analysis of septic-injury responsive genes in the beetle Tribolium castaneum. PLoS One 2013; 8(1) e52004
[http://dx.doi.org/10.1371/journal.pone.0052004] [PMID: 23326321]
[24]
Bingsohn L, Knorr E, Billion A, Narva KE, Vilcinskas A. Knockdown of genes in the Toll pathway reveals new lethal RNA interference targets for insect pest control. Insect Mol Biol 2017; 26(1): 92-102.
[http://dx.doi.org/10.1111/imb.12273] [PMID: 27862545]
[25]
Blum M. Chemical defenses of arthropods. NewYork: Academic Press 1981.
[26]
Howard RW, Jurenka RA, Blomquist GJ. Prostaglandin synthetase inhibitors in the defensive secretion of the red flour beetle Tribolium castaneum (Herbst) (Coleoptera:Tenebrionidae). Insect Biochem 1986; 16: 757-60.
[http://dx.doi.org/10.1016/0020-1790(86)90111-3]
[27]
Brandt A, Joop G, Vilcinskas A. Tribolium castaneum as a whole-animal screening system for the detection and characterization of neuroprotective substances. Arch Insect Biochem Physiol 2019; 100(3) e21532
[http://dx.doi.org/10.1002/arch.21532] [PMID: 30653719]
[28]
Prendeville HR, Stevens L. Microbe inhibition by Tribolium flour beetles varies with beetle species, strain, sex, and microbe group. J Chem Ecol 2002; 28(6): 1183-90.
[http://dx.doi.org/10.1023/A:1016281600915] [PMID: 12184396]
[29]
Vilcinskas A, Mukherjee K, Vogel H. Expansion of the antimicrobial peptide repertoire in the invasive ladybird Harmonia axyridis. Proc Biol Sci 2013; 280(1750) 20122113
[http://dx.doi.org/10.1098/rspb.2012.2113] [PMID: 23173204]
[30]
Tonk M, Knorr E, Cabezas-Cruz A, Valdés JJ, Kollewe C, Vilcinskas A. Tribolium castaneum defensins are primarily active against Gram-positive bacteria. J Invertebr Pathol 2015; 132: 208-15.
[http://dx.doi.org/10.1016/j.jip.2015.10.009] [PMID: 26522790]
[31]
Bingsohn L, Knorr E, Vilcinskas A. The model beetle Tribolium castaneum can be used as an early warning system for transgenerational epigenetic side effects caused by pharmaceuticals. Comp Biochem Physiol C Toxicol Pharmacol 2016; 185-186: 57-64.
[http://dx.doi.org/10.1016/j.cbpc.2016.03.002] [PMID: 26972758]
[32]
Mahroof RM, Hagstrum DW. Biology, behavior, and ecology of pests in processed commodities Stored product protection. Kansas State University, Manhattan, KS 2012; pp. 45-61.
[33]
Beeman RW, Stuart JJ, Denell RE, McGaughey WH, Dover BA. Tribolium as a model insect for study of resistance mechanisms.Molecular Mechanisms of Insecticide Resistance. ACS 1992; 202-8.
[34]
Arthur FH. Grain protectants: Current status and prospects for the future. J Stored Prod Res 1996; 32: 293-302.
[http://dx.doi.org/10.1016/S0022-474X(96)00033-1]
[35]
Oppert B, Morgan TD, Kramer KJ. Efficacy of Bacillus thuringiensis Cry3Aa protoxin and protease inhibitors against coleopteran storage pests. Pest Manag Sci 2011; 67(5): 568-73.
[http://dx.doi.org/10.1002/ps.2099] [PMID: 21268232]
[36]
Walski T, Van Damme EJ, Smagghe G. Penetration through the peritrophic matrix is a key to lectin toxicity against Tribolium castaneum. J Insect Physiol 2014; 70: 94-101.
[http://dx.doi.org/10.1016/j.jinsphys.2014.09.004] [PMID: 25240534]
[37]
Casida JE, Durkin KA. Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol 2013; 58: 99-117.
[http://dx.doi.org/10.1146/annurev-ento-120811-153645] [PMID: 23317040]
[38]
Usherwood PNR. Insect glutamate receptors. Adv Insect Physiol 1994; 24: 309-41.
[http://dx.doi.org/10.1016/S0065-2806(08)60086-7]
[39]
Fukuto TR. Mechanism of action of organophosphorus and carbamate insecticides. Environ Health Perspect 1990; 87: 245-54.
[http://dx.doi.org/10.1289/ehp.9087245] [PMID: 2176588]
[40]
Flessel P, Quintana PJE, Hooper K. Genetic toxicity of malathion: a review. Environ Mol Mutagen 1993; 22(1): 7-17.
[http://dx.doi.org/10.1002/em.2850220104] [PMID: 8339727]
[41]
Strong RG, Sbur DE, Partida GJ. The toxicity and residual effectiveness of malathion and diazinon used for protection of stored wheat. J Econ Entomol 1967; 60: 500-5.
[http://dx.doi.org/10.1093/jee/60.2.500]
[42]
Parkin EA. A provisonal assessment of malathion for stored-product insect control. J Sci Fd Agric 1958; 370-5.
[43]
Haliscak JP, Beeman RW. Status of malathion resistance in five genera of beetles infesting farm-stored corn, wheat and oats in the United States. J Econ Entomol 1983; 76: 717-22.
[http://dx.doi.org/10.1093/jee/76.4.717]
[44]
Daft JL. Fumigants and related chemicals in foods: review of residue findings, contamination sources, and analytical methods. Sci Total Environ 1991; 100(Spec No): 501-18.
[http://dx.doi.org/10.1016/0048-9697(91)90390-Z] [PMID: 2063187]
[45]
Al-Hakkak ZS, Al-Azzawi MJ, Al-Adhamy BW, Khalil SA. Inhibitory action of phosphine on acetylcholinesterase of Ephestia cautella (Lepidoptera: Pyralidae). J Stored Prod Res 1989; 25: 171-4.
[http://dx.doi.org/10.1016/0022-474X(89)90039-8]
[46]
Nath NS, Bhattacharya I, Tuck AG, Schlipalius DI, Ebert PR. Mechanisms of phosphine toxicity. J Toxicol 2011. 2011494168
[http://dx.doi.org/10.1155/2011/494168] [PMID: 21776261]
[47]
Bond EJ, Robinson JR, Buckland CT. Toxic action of phosphine - Absorption and symptoms of poisoning in insects. J Stored Prod Res 1969; 5: 289-92.
[http://dx.doi.org/10.1016/0022-474X(69)90002-2]
[48]
Valmas N, Zuryn S, Ebert PR. Mitochondrial uncouplers act synergistically with the fumigant phosphine to disrupt mitochondrial membrane potential and cause cell death. Toxicology 2008; 252(1-3): 33-9.
[http://dx.doi.org/10.1016/j.tox.2008.07.060] [PMID: 18755236]
[49]
Winks RG. The toxicity of phosphine to adults of Tribolium castaneum (Herbst) - Time as a dosage factor. J Stored Prod Res 1984; 20: 45-56.
[http://dx.doi.org/10.1016/0022-474X(84)90035-3]
[50]
Winks RG. The toxicity of phosphine to adults of Tribolium castaneum (Herbst): Phosphine-induced narcosis. J Stored Prod Res 1985; 21: 25-9.
[http://dx.doi.org/10.1016/0022-474X(85)90056-6]
[51]
Manivannan S. Toxicity of phosphine on the developmental stages of rust-red flour beetle, Tribolium castaneum Herbst over a range of concentrations and exposures. J Food Sci Technol 2015; 52(10): 6810-5.
[http://dx.doi.org/10.1007/s13197-015-1799-y] [PMID: 26396434]
[52]
Rajendran S. Inhibition of hatching of Tribolium castaneum by phosphine. J Stored Prod Res 2000; 36: 101-6.
[http://dx.doi.org/10.1016/S0022-474X(99)00038-7]
[53]
Grenier S, Grenier A-M. Fenoxycarb, a fairly new insect growth regulator: review of its effects on insects. Ann Appl Biol 1993; 122: 369-403.
[http://dx.doi.org/10.1111/j.1744-7348.1993.tb04042.x]
[54]
Thind BB, Edwards JP. Laboratory evaluation of the juvenile hormone analogue fenoxycarb against some insecticide-susceptible and resistant stored products beetles. J Stored Prod Res 1986; 22: 235-41.
[http://dx.doi.org/10.1016/0022-474X(86)90016-0]
[55]
Cogburn RR. Fenoxycarb as a long-term protectant for stored rough rice. J Econ Entomol 1988; 81: 722-6.
[http://dx.doi.org/10.1093/jee/81.2.722]
[56]
Ihara M, Matsuda K. Neonicotinoids: molecular mechanisms of action, insights into resistance and impact on pollinators. Curr Opin Insect Sci 2018; 30: 86-92.
[http://dx.doi.org/10.1016/j.cois.2018.09.009] [PMID: 30553491]
[57]
Wood TJ, Goulson D. The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013. Environ Sci Pollut Res Int 2017; 24(21): 17285-325.
[http://dx.doi.org/10.1007/s11356-017-9240-x] [PMID: 28593544]
[58]
Buckingham S, Lapied B, Corronc H, Sattelle F. Imidacloprid actions on insect neuronal acetylcholine receptors. J Exp Biol 1997; 200(Pt 21): 2685-92.
[PMID: 9326496]
[59]
Daglish GJ, Nayak MK. Potential of the neonicotinoid imidacloprid and the oxadiazine indoxacarb for controlling five coleopteran pests of stored grain. Insect Sci 2012; 19: 96-101.
[http://dx.doi.org/10.1111/j.1744-7917.2011.01430.x]
[60]
Athanassiou CG, Kavallieratos NG, Arthur FH, Throne JE. Efficacy of a combination of beta-cyfluthrin and imidacloprid and beta-cyfluthrin alone for control of stored-product insects on concrete. J Econ Entomol 2013; 106(2): 1064-70.
[http://dx.doi.org/10.1603/EC12406] [PMID: 23786102]
[61]
Ma C, Zhang Y, Sun J, et al. Impact of acute oral exposure to thiamethoxam on the homing, flight, learning acquisition and short-term retention of Apis cerana. Pest Manag Sci 2019; 75(11): 2975-80.
[http://dx.doi.org/10.1002/ps.5411] [PMID: 30884080]
[62]
Coulon M, Schurr F, Martel AC, et al. Influence of chronic exposure to thiamethoxam and chronic bee paralysis virus on winter honey bees. PLoS One 2019; 14(8) e0220703
[http://dx.doi.org/10.1371/journal.pone.0220703] [PMID: 31415597]
[63]
Tesovnik T, Zorc M, Ristanić M, et al. Exposure of honey bee larvae to thiamethoxam and its interaction with Nosema ceranae infection in adult honey bees. Environ Pollut 2020. 256113443
[http://dx.doi.org/10.1016/j.envpol.2019.113443] [PMID: 31733951]
[64]
Arthur FH, Yue SS, Wilde GE. Susceptibility of stored-product beetles on wheat and maize treated with thiamethoxam: Effects of concentration, exposure interval, and temperature. J Stored Prod Res 2004; 40: 527-46.
[http://dx.doi.org/10.1016/j.jspr.2003.08.001]
[65]
Hertlein MB, Thompson GD, Subramanyam B, Athanassiou CG. Spinosad: A new natural product for stored grain protection. J Stored Prod Res 2011; 47: 131-46.
[http://dx.doi.org/10.1016/j.jspr.2011.01.004]
[66]
Cleveland CB, Mayes MA, Cryer SA. An ecological risk assessment for spinosad use on cotton. Pest Manag Sci 2002; 58(1): 70-84.
[http://dx.doi.org/10.1002/ps.424] [PMID: 11838288]
[67]
Flinn PW, Subramanyam B, Arthur FH. Comparison of aeration and spinosad for suppressing insects in stored wheat. J Econ Entomol 2004; 97(4): 1465-73.
[http://dx.doi.org/10.1093/jee/97.4.1465] [PMID: 15384362]
[68]
Huang F, Subramanyam B, Toews MD. Susceptibility of laboratory and field strains of four stored-product insect species to spinosad. J Econ Entomol 2004; 97(6): 2154-9.
[http://dx.doi.org/10.1093/jee/97.6.2154] [PMID: 15666777]
[69]
Narahashi T. Mode of action of pyrethroids. Bull World Health Organ 1971; 44(1-3): 337-45.
[PMID: 5315351]
[70]
Hirano M. Characteristics of pyrethroids for insect pest control in agriculture. Pestic Sci 1989; 27: 353-60.
[http://dx.doi.org/10.1002/ps.2780270404]
[71]
Mujeeb KA, Shakoori AR. Toxicity of synthetic pyrethroid, fury, against different developmental stages of three strains of Tribolium castaneum (Herbst.). Pak J Zool 2007; 39: 361-6.
[72]
Kavallieratos NG, Athanassiou CG, Arthur FH. Effectiveness of insecticide-incorporated bags to control stored-product beetles. J Stored Prod Res 2017; 70: 18-24.
[http://dx.doi.org/10.1016/j.jspr.2016.11.001]
[73]
Paudyal S, Opit GP, Arthur FH, Bingham GV, Gautam SG. Contact Toxicity of deltamethrin against Tribolium castaneum (Coleoptera: Tenebrionidae), Sitophilus oryzae (Coleoptera: Curculionidae), and Rhyzopertha dominica (Coleoptera: Bostrichidae) adults. J Econ Entomol 2016; 109(4): 1936-42.
[http://dx.doi.org/10.1093/jee/tow107] [PMID: 27270576]
[74]
Scheff DS, Arthur FH. Fecundity of Tribolium castaneum and Tribolium confusum adults after exposure to deltamethrin packaging. J Pest Sci 2018; 91: 717-25.
[http://dx.doi.org/10.1007/s10340-017-0923-3]
[75]
Morrison WR III, Wilkins RV, Gerken AR, et al. Mobility of adult Tribolium castaneum (Coleoptera: Tenebrionidae) and Rhyzopertha dominica (Coleoptera: Bostrichidae) after exposure to long-lasting insecticide-incorporated netting. J Econ Entomol 2018; 111(5): 2443-53.
[http://dx.doi.org/10.1093/jee/toy173] [PMID: 29982560]
[76]
Toews MD, Campbell JF, Arthur FH, West M. Monitoring Tribolium castaneum (Coleoptera: Tenebrionidae) in pilot-scale warehouses treated with residual applications of (S)-hydroprene and cyfluthrin. J Econ Entomol 2005; 98(4): 1391-8.
[http://dx.doi.org/10.1603/0022-0493-98.4.1391] [PMID: 16156595]
[77]
Toews MD, Arthur FH, Campbell JF. Monitoring Tribolium castaneum (Herbst) in pilot-scale warehouses treated with beta-cyfluthrin: are residual insecticides and trapping compatible? Bull Entomol Res 2009; 99(2): 121-9.
[http://dx.doi.org/10.1017/S0007485308006172] [PMID: 18947447]
[78]
Arthur FH, Starkus LA, Mckay T. Effects of flour and milling debris on efficacy of beta-cyfluthrin for control of Tribolium castaneum (Coleoptera: Tenebrionidae). J Econ Entomol 2015; 108(2): 811-25.
[http://dx.doi.org/10.1093/jee/tov015] [PMID: 26470194]
[79]
Buckingham SD, Biggin PC, Sattelle BM, Brown LA, Sattelle DB. Insect GABA receptors: splicing, editing, and targeting by antiparasitics and insecticides. Mol Pharmacol 2005; 68(4): 942-51.
[http://dx.doi.org/10.1124/mol.105.015313] [PMID: 16027231]
[80]
Hosie AM, Baylis HA, Buckingham SD, Sattelle DB. Actions of the insecticide fipronil, on dieldrin-sensitive and- resistant GABA receptors of Drosophila melanogaster. Br J Pharmacol 1995; 115(6): 909-12.
[http://dx.doi.org/10.1111/j.1476-5381.1995.tb15896.x] [PMID: 7582519]
[81]
Raymond V, Sattelle DB, Lapied B. Co-existence in DUM neurones of two GluCl channels that differ in their picrotoxin sensitivity. Neuroreport 2000; 11(12): 2695-701.
[http://dx.doi.org/10.1097/00001756-200008210-00018] [PMID: 10976946]
[82]
Ffrench constant RH, Rocheleau TA, Steichen JC, Chalmers AE. A point mutation in a Drosophila GABA receptor confers insecticide resistance. Nature 1993; 363: 449-51.
[http://dx.doi.org/10.1038/363449a0]
[83]
Kavallieratos NG, Athanassiou CG, Vayias BJ, Betsi PCC. Insecticidal efficacy of fipronil against four stored-product insect pests: influence of commodity, dose, exposure interval, relative humidity and temperature. Pest Manag Sci 2010; 66(6): 640-9.
[http://dx.doi.org/10.1002/ps.1923] [PMID: 20205233]
[84]
Oberlander H, Silhacek DL. Insect Growth regulatorsAlternatives to pesticides in stored-product IPM. Norwell, MA: Kluwer Academic Publishers 2000; pp. 147-63.
[http://dx.doi.org/10.1007/978-1-4615-4353-4_6]
[85]
Oberlander H, Silhacek DL, Shaaya E, Ishaaya I. Current status and future perspectives of the use of insect growth regulators for the control of stored product insects. J Stored Prod Res 1997; 33: 1-6.
[http://dx.doi.org/10.1016/S0022-474X(96)00047-1]
[86]
Riddiford LM. Cellular and molecular actions of juvenile hormone I. General considerations and premetamorphic actions. Adv Insect Physiol 1994; 24: 211-74.
[http://dx.doi.org/10.1016/S0065-2806(08)60084-3]
[87]
Jindra M, Bellés X, Shinoda T. Molecular basis of juvenile hormone signaling. Curr Opin Insect Sci 2015; 11: 39-46.
[http://dx.doi.org/10.1016/j.cois.2015.08.004] [PMID: 28285758]
[88]
Jindra M, Palli SR, Riddiford LM. The juvenile hormone signaling pathway in insect development. Annu Rev Entomol 2013; 58: 181-204.
[http://dx.doi.org/10.1146/annurev-ento-120811-153700] [PMID: 22994547]
[89]
Jacob M, Prabhu VKK. Effect of two juvenile hormone analogues on embryonic morphogenesis, histogenesis, endocrines and cuticulogenesis of Dysdercus cingulatus Fabr. (Heteroptera: Pyrrhocoridae). Prof Anim Sci 1988; 97: 55-65.
[http://dx.doi.org/10.1007/BF03179511]
[90]
Sláma K. Insect juvenile hormone analogues. Annu Rev Biochem 1971; 40: 1079-102.
[http://dx.doi.org/10.1146/annurev.bi.40.070171.005243] [PMID: 4941234]
[91]
Henrick CA, Staal GB, Siddall JB. Alkyl 3,7,11-trimethyl-2,4-dodecadienoates, a new class of potent insect growth regulators with juvenile hormone activity. J Agric Food Chem 1973; 21(3): 354-9.
[http://dx.doi.org/10.1021/jf60187a043] [PMID: 4708794]
[92]
Liu SS, Arthur FH, VanGundy D, Phillips TW. Combination of methoprene and controlled aeration to manage insects in stored wheat. Insects 2016; 7(2) E25
[http://dx.doi.org/10.3390/insects7020025] [PMID: 27322331]
[93]
Arthur FH, Liu S, Zhao B, Phillips TW. Residual efficacy of pyriproxyfen and hydroprene applied to wood, metal and concrete for control of stored-product insects. Pest Manag Sci 2009; 65(7): 791-7.
[http://dx.doi.org/10.1002/ps.1756] [PMID: 19360716]
[94]
Kavallieratos NG, Athanassiou CG, Vayias BJ, Tomanović Z. Efficacy of insect growth regulators as grain protectants against two stored-product pests in wheat and maize. J Food Prot 2012; 75(5): 942-50.
[http://dx.doi.org/10.4315/0362-028X.JFP-11-397] [PMID: 22564945]
[95]
Kostyukovsky M, Chen B, Atsmi S, Shaaya E. Biological activity of two juvenoids and two ecdysteroids against three stored product insects. Insect Biochem Mol Biol 2000; 30(8-9): 891-7.
[http://dx.doi.org/10.1016/S0965-1748(00)00063-1] [PMID: 10876135]
[96]
Wijayaratne LKW, Fields PG, Arthur FH. Effect of methoprene on the progeny production of Tribolium castaneum (Coleoptera: Tenebrionidae). Pest Manag Sci 2012; 68(2): 217-24.
[http://dx.doi.org/10.1002/ps.2247] [PMID: 21770015]
[97]
Konopova B, Jindra M. Juvenile hormone resistance gene Methoprene-tolerant controls entry into metamorphosis in the beetle Tribolium castaneum. Proc Natl Acad Sci USA 2007; 104(25): 10488-93.
[http://dx.doi.org/10.1073/pnas.0703719104] [PMID: 17537916]
[98]
Parthasarathy R, Palli SR. Molecular analysis of juvenile hormone analog action in controlling the metamorphosis of the red flour beetle, Tribolium castaneum. Arch Insect Biochem Physiol 2009; 70(1): 57-70.
[http://dx.doi.org/10.1002/arch.20288] [PMID: 19072925]
[99]
Riddiford LM, Cherbas P, Truman JW. Ecdysone receptors and their biological actions. Vitam Horm 2000; 60: 1-73.
[http://dx.doi.org/10.1016/S0083-6729(00)60016-X] [PMID: 11037621]
[100]
Ishaaya I, Yablonski S, Horowitz AR. Comparative toxicity of 2 ecdysteroid agonists, RH-2485 and RH-5992, on susceptible and pyrethroid-resistant strains of the egyptian cotton leafworm, Spodoptera littoralis. Phytoparasitica 1995; 23: 139-45.
[http://dx.doi.org/10.1007/BF02980973]
[101]
Wing HA, Aller HE. Ecdysteroid agonists as novel insect regulatorsPesticides and alternatives. Amsterdam: Elsevier 1990; pp. 251-7.
[102]
Ali Q. ul Hasan M, Sagheer M, Saleem S, Faisal M, Naeem A, Iqbal J. Screening of seven insect growth regulators for their anti-insect activity against the larvae of Trogoderma Granarium (Everts) and Tribolium castaneum (Herbst). Pak J Agric Sci 2017; 54: 589-95.
[http://dx.doi.org/10.21162/PAKJAS/17.5088]
[103]
Ishaaya I, Casida JE. Dietary Th 6040 alters composition and enzyme-activity of housefly larval cuticle. Pestic Biochem Physiol 1974; 4: 484-90.
[http://dx.doi.org/10.1016/0048-3575(74)90073-X]
[104]
Merzendorfer H. Chitin synthesis inhibitors: old molecules and new developments. Insect Sci 2013; 20(2): 121-38.
[http://dx.doi.org/10.1111/j.1744-7917.2012.01535.x] [PMID: 23955853]
[105]
van Daalen JJ, Meltzer J, Mulder R, Wellinga K. A selective insecticide with a novel mode of action. Naturwissenschaften 1972; 59(7): 312-3.
[http://dx.doi.org/10.1007/BF00593360] [PMID: 5080920]
[106]
Merzendorfer H, Kim HS, Chaudhari SS, et al. Genomic and proteomic studies on the effects of the insect growth regulator diflubenzuron in the model beetle species Tribolium castaneum. Insect Biochem Mol Biol 2012; 42(4): 264-76.
[http://dx.doi.org/10.1016/j.ibmb.2011.12.008] [PMID: 22212827]
[107]
Clarke L, Temple GHR, Vincent JFV. The effects of a chitin inhibitor-dimilin- on the production of peritrophic membrane in the locust, Locusta migratoria. J Insect Physiol 1977; 23(2): 241-6.
[http://dx.doi.org/10.1016/0022-1910(77)90037-3] [PMID: 323371]
[108]
Champ BR. Insecticide resistance in Australian Tribolium castaneum (Herbst) (Coleoptera, Tenebrionidae) - II: Malathion resistance in eastern Australia. J Stored Prod Res 1970; 6: 111-31.
[http://dx.doi.org/10.1016/0022-474X(70)90001-9]
[109]
Collins JP. A new resistance to pyrethroids in Tribolium castaneum. Pestic Sci 1989; 28: 101-15.
[http://dx.doi.org/10.1002/ps.2780280112]
[110]
Speirs RD, Redlinger LM, Boles HP. Malathion resistance in the red flour beetle. J Econ Entomol 1967; 60: 1373-4.
[http://dx.doi.org/10.1093/jee/60.5.1373]
[111]
Speirs RD, Redlinger LM, Jones R. DDT-resistant red flour beetles from a Georgia peanut sheller. J Econ Entomol 1971; 64(5): 1328-9.
[http://dx.doi.org/10.1093/jee/64.5.1328] [PMID: 5122365]
[112]
Zettler JL, Arthur FH. Dose-response tests on red flour beetle and confused flour beetle (coleoptera: Tenebrionidae) collected from flour mills in the United States. J Econ Entomol 1997; 90: 1157-62.
[http://dx.doi.org/10.1093/jee/90.5.1157]
[113]
Bond EJ. Increased tolerance to ethylene dibromide in field population of Tribolium castaneum (Herbst). J Stored Prod Res 1973; 9: 61-3.
[http://dx.doi.org/10.1016/0022-474X(73)90040-4]
[114]
Whalon ME, Mota-Sanchez D, Hollingworth R, Duynslager L. Arthropod resistance database 2012.Available at:. https://www.pesticideresistance.org/
[115]
Feyereisen R. Molecular biology of insecticide resistance. Toxicol Lett 1995; 82-83: 83-90.
[http://dx.doi.org/10.1016/0378-4274(95)03470-6] [PMID: 8597150]
[116]
Balabanidou V, Grigoraki L, Vontas J. Insect cuticle: a critical determinant of insecticide resistance. Curr Opin Insect Sci 2018; 27: 68-74.
[http://dx.doi.org/10.1016/j.cois.2018.03.001] [PMID: 30025637]
[117]
Arakane Y, Muthukrishnan S, Beeman RW, Kanost MR, Kramer KJ. Laccase 2 is the phenoloxidase gene required for beetle cuticle tanning. Proc Natl Acad Sci USA 2005; 102(32): 11337-42.
[http://dx.doi.org/10.1073/pnas.0504982102] [PMID: 16076951]
[118]
Julio AH, Gigliolli AA, Cardoso KA, et al. Multiple resistance to pirimiphos-methyl and bifenthrin in Tribolium castaneum involves the activity of lipases, esterases, and laccase2. Comp Biochem Physiol C Toxicol Pharmacol 2017; 195: 27-43.
[http://dx.doi.org/10.1016/j.cbpc.2017.01.011] [PMID: 28163254]
[119]
Jacomb F, Marsh J, Holman L. Sexual selection expedites the evolution of pesticide resistance. Evolution 2016; 70(12): 2746-51.
[http://dx.doi.org/10.1111/evo.13074] [PMID: 27677862]
[120]
Andreev D, Kreitman M, Phillips TW, Beeman RW. ffrench-Constant RH. Multiple origins of cyclodiene insecticide resistance in Tribolium castaneum (Coleoptera: Tenebrionidae). J Mol Evol 1999; 48(5): 615-24.
[http://dx.doi.org/10.1007/PL00006504] [PMID: 10198127]
[121]
Schlipalius DI, Valmas N, Tuck AG, et al. A core metabolic enzyme mediates resistance to phosphine gas. Science 2012; 338(6108): 807-10.
[http://dx.doi.org/10.1126/science.1224951] [PMID: 23139334]
[122]
Oppert B, Guedes RN, Aikins MJ, et al. Genes related to mitochondrial functions are differentially expressed in phosphine-resistant and -susceptible Tribolium castaneum. BMC Genomics 2015; 16: 968.
[http://dx.doi.org/10.1186/s12864-015-2121-0] [PMID: 26582239]
[123]
Erdman HE. Effects of x-radiation and the insecticide DDT on mortality and reproduction of flour beetles, Tribolium confusum and T. castaneum, with a genetic interpretation for DDT resistance. Ann Entomol Soc Am 1970; 63(1): 191-7.
[http://dx.doi.org/10.1093/aesa/63.1.191] [PMID: 5415594]
[124]
Davies TG, Field LM, Usherwood PN, Williamson MS. DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 2007; 59(3): 151-62.
[http://dx.doi.org/10.1080/15216540701352042] [PMID: 17487686]
[125]
Li X, Schuler MA, Berenbaum MR. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol 2007; 52: 231-53.
[http://dx.doi.org/10.1146/annurev.ento.51.110104.151104] [PMID: 16925478]
[126]
Liska DJ. The detoxification enzyme systems. Altern Med Rev 1998; 3(3): 187-98.
[PMID: 9630736]
[127]
Omiecinski CJ, Vanden Heuvel JP, Perdew GH, Peters JM. Xenobiotic metabolism, disposition, and regulation by receptors: from biochemical phenomenon to predictors of major toxicities. Toxicol Sci 2011; 120(Suppl. 1): S49-75.
[http://dx.doi.org/10.1093/toxsci/kfq338] [PMID: 21059794]
[128]
Heidel-Fischer HM, Vogel H. Molecular mechanisms of insect adaptation to plant secondary compounds. Curr Opin Insect Sci 2015; 8: 8-14.
[http://dx.doi.org/10.1016/j.cois.2015.02.004]
[129]
Merzendorfer H. ABC Transporters and their role in protecting insects from pesticides and their metabolites.Target receptors in the control of insect pests: Part II Elsevier. Oxford 2014; pp. 1-73.
[http://dx.doi.org/10.1016/B978-0-12-417010-0.00001-X]
[130]
Wool D, Noiman S, Manheim O, Cohen E. Malathion resistance in Tribolium strains and their hybrids: inheritance patterns and possible enzymatic mechanisms (Coleoptera, Tenebrionidae). Biochem Genet 1982; 20(7-8): 621-36.
[http://dx.doi.org/10.1007/BF00483961] [PMID: 7138493]
[131]
Yu SJ. Detoxification mechanisms in insectsEncyclopedia of entomology. Dordrecht: Springer 2008.
[132]
Hu HX, Zhou D, Ma L, Shen B, Sun Y, Zhu CL. Lipase is associated with deltamethrin resistance in Culex pipiens pallens. Parasitol Res 2019.
[http://dx.doi.org/10.1007/s00436-019-06489-2] [PMID: 31760499]
[133]
Araújo RA, Guedes RN, Oliveira MG, Ferreira GH. Enhanced activity of carbohydrate- and lipid-metabolizing enzymes in insecticide-resistant populations of the maize weevil, Sitophilus zeamais. Bull Entomol Res 2008; 98(4): 417-24.
[http://dx.doi.org/10.1017/S0007485308005737] [PMID: 18279568]
[134]
Song X, Qi X, Hao B, Qu Y. Studies of substrate specificities of lipases from different sources. Eur J Lipid Sci Technol 2008; 110: 1095-101.
[http://dx.doi.org/10.1002/ejlt.200800073]
[135]
Zhu F, Moural TW, Shah K, Palli SR. Integrated analysis of cytochrome P450 gene superfamily in the red flour beetle, Tribolium castaneum. BMC Genomics 2013; 14: 174.
[http://dx.doi.org/10.1186/1471-2164-14-174] [PMID: 23497158]
[136]
Zhu F, Parthasarathy R, Bai H, et al. A brain-specific cytochrome P450 responsible for the majority of deltamethrin resistance in the QTC279 strain of Tribolium castaneum. Proc Natl Acad Sci USA 2010; 107(19): 8557-62.
[http://dx.doi.org/10.1073/pnas.1000059107] [PMID: 20410462]
[137]
Kalsi M, Palli SR. Transcription factors, CncC and Maf, regulate expression of CYP6BQ genes responsible for deltamethrin resistance in Tribolium castaneum. Insect Biochem Mol Biol 2015; 65: 47-56.
[http://dx.doi.org/10.1016/j.ibmb.2015.08.002] [PMID: 26255690]
[138]
Liang X, Xiao D, He Y, Yao J, Zhu G, Zhu KY. Insecticide-mediated up-regulation of cytochrome P450 genes in the red flour beetle (Tribolium castaneum). Int J Mol Sci 2015; 16(1): 2078-98.
[http://dx.doi.org/10.3390/ijms16012078] [PMID: 25607733]
[139]
Xiong W, Gao S, Mao J, et al. CYP4BN6 and CYP6BQ11 mediate insecticide susceptibility and their expression is regulated by Latrophilin in Tribolium castaneum. Pest Manag Sci 2019; 75(10): 2744-55.
[http://dx.doi.org/10.1002/ps.5384] [PMID: 30788896]
[140]
Haubruge E, Amichot M, Cuany A, Berge JB, Arnaud L. Purification and characterization of a carboxylesterase involved in malathion-specific resistance from Tribolium castaneum (Coleoptera: Tenebrionidae). Insect Biochem Mol Biol 2002; 32(9): 1181-90.
[http://dx.doi.org/10.1016/S0965-1748(02)00054-1] [PMID: 12213253]
[141]
Yu SJ. The Toxicology and biochemistry of insecticides. London, England: CRC Press, Llc 2008.
[142]
Enayati AA, Ranson H, Hemingway J. Insect glutathione transferases and insecticide resistance. Insect Mol Biol 2005; 14(1): 3-8.
[http://dx.doi.org/10.1111/j.1365-2583.2004.00529.x] [PMID: 15663770]
[143]
Shi H, Pei L, Gu S, et al. Glutathione S-transferase (GST) genes in the red flour beetle, Tribolium castaneum, and comparative analysis with five additional insects. Genomics 2012; 100(5): 327-35.
[http://dx.doi.org/10.1016/j.ygeno.2012.07.010] [PMID: 22824654]
[144]
Pajaro-Castro N, Caballero-Gallardo K, Olivero-Verbel J. Toxicity of naphthalene and benzene on Tribollium castaneum Herbst. Int J Environ Res Public Health 2017; 14(6): 14.
[http://dx.doi.org/10.3390/ijerph14060667] [PMID: 28635673]
[145]
Plavšin I, Stašková T, Šerý M, Smýkal V, Hackenberger BK, Kodrík D. Hormonal enhancement of insecticide efficacy in Tribolium castaneum: oxidative stress and metabolic aspects. Comp Biochem Physiol C Toxicol Pharmacol 2015; 170: 19-27.
[http://dx.doi.org/10.1016/j.cbpc.2015.01.005] [PMID: 25661030]
[146]
Chen X, Xiong W, Li C, et al. Comparative RNA-sequencing profiling reveals novel Delta-class glutathione S-transferases relative genes expression patterns in Tribolium castaneum. Gene 2016; 593(1): 13-20.
[http://dx.doi.org/10.1016/j.gene.2016.08.013] [PMID: 27511373]
[147]
Ahn SJ, Vogel H, Heckel DG. Comparative analysis of the UDP-glycosyltransferase multigene family in insects. Insect Biochem Mol Biol 2012; 42(2): 133-47.
[http://dx.doi.org/10.1016/j.ibmb.2011.11.006] [PMID: 22155036]
[148]
Nho CW, Jeffery E. The synergistic upregulation of phase II detoxification enzymes by glucosinolate breakdown products in cruciferous vegetables. Toxicol Appl Pharmacol 2001; 174(2): 146-52.
[http://dx.doi.org/10.1006/taap.2001.9207] [PMID: 11446830]
[149]
Dermauw W, Van Leeuwen T. The ABC gene family in arthropods: comparative genomics and role in insecticide transport and resistance. Insect Biochem Mol Biol 2014; 45: 89-110.
[http://dx.doi.org/10.1016/j.ibmb.2013.11.001] [PMID: 24291285]
[150]
Kennedy CT. K Xenobiotic Protection/resistance mechanisms in organisms. New York: Springer 2013.
[http://dx.doi.org/10.1007/978-1-4614-5764-0_23]
[151]
Broehan G, Kroeger T, Lorenzen M, Merzendorfer H. Functional analysis of the ATP-binding cassette (ABC) transporter gene family of Tribolium castaneum. BMC Genomics 2013; 14: 6.
[http://dx.doi.org/10.1186/1471-2164-14-6] [PMID: 23324493]
[152]
Kalsi M, Palli SR. Cap n collar transcription factor regulates multiple genes coding for proteins involved in insecticide detoxification in the red flour beetle, Tribolium castaneum. Insect Biochem Mol Biol 2017; 90: 43-52.
[http://dx.doi.org/10.1016/j.ibmb.2017.09.009] [PMID: 28951207]
[153]
Rösner J, Merzendorfer H. Transcriptional plasticity of different ABC transporter genes from Tribolium castaneum contributes to diflubenzuron resistance. Insect Biochem Mol Biol 2020. 116103282
[http://dx.doi.org/10.1016/j.ibmb.2019.103282] [PMID: 31740345]
[154]
Daglish GJ, Wallbank BE, Nayak MK. Synergized bifenthrin plus chlorpyrifos-methyl for control of beetles and psocids in sorghum in Australia. J Econ Entomol 2003; 96(2): 525-32.
[http://dx.doi.org/10.1093/jee/96.2.525] [PMID: 14994824]
[155]
Khalequzzaman M, Nahar J. Toxicity of nine insecticides to adult Tribolium castaneum (Herbst). J Biol Sci 2001; 1
[http://dx.doi.org/10.3923/jbs.2001.1043.1045]
[156]
Shi N, Sengupta GC, Satpathy BN. Toxicity of some insecticides to the red flour beetle, Tribolium castaneum. J Econ Entomol 1961; 54: 437-9.
[http://dx.doi.org/10.1093/jee/54.3.437]
[157]
Bengston M, Connell M, Davies RAH, et al. Fenitrothion plus (1R)-phenothrin, and pirimiphos-methyl plus carbaryl, as grain protectant combinations for wheat. Pestic Sci 1980; 11: 471-82.
[http://dx.doi.org/10.1002/ps.2780110505]
[158]
Parkin EA. A provisional assessment of malathion for stored-product insect control. J Sci Food Agric 1958; 9: 370-5.
[http://dx.doi.org/10.1002/jsfa.2740090609]
[159]
Rajendran S, Muthu M. The toxic action of phosphine in combination with some alkyl halide fumigants and carbon dioxide against the eggs of Tribolium castaneum Herbst (Coleoptera: Tenebrionidae). J Stored Prod Res 1989; 25: 225-30.
[http://dx.doi.org/10.1016/0022-474X(89)90028-3]
[160]
Khan MA. Effectiveness of insecticides and repellents on stored product insect pests. Anz. Schädl.kd. Pflanzenschutz Umweltschutz 1983; 56: 25-9.
[http://dx.doi.org/10.1007/BF01905984]
[161]
Huang F, Subramanyam B. Management of five stored-product insects in wheat with pirimiphos-methyl and pirimiphos-methyl plus synergized pyrethrins. Pest Manag Sci 2005; 61(4): 356-62.
[http://dx.doi.org/10.1002/ps.968] [PMID: 15751013]
[162]
Cogburn RR. Fenoxycarb as a long-term protectant for stored rough rice. J Econ Entomol 81: 722-6.
[http://dx.doi.org/10.1093/jee/81.2.722]
[163]
Arthur FH, Yue B, Wilde GE. Susceptibility of stored-product beetles on wheat and maize treated with thiamethoxam: effects of concentration, exposure interval, and temperature. J Stored Prod Res 2004 2004; v. 40(no.5): 527-46.
[164]
Fang L, Subramanyam B, Arthur FH. Effectiveness of spinosad on four classes of wheat against five stored-product insects. J Econ Entomol 2002; 95(3): 640-50.
[http://dx.doi.org/10.1603/0022-0493-95.3.640] [PMID: 12076013]
[165]
Hertlein MB, Mavrotas C, Jousseaume C, et al. A review of spinosad as a natural product for larval mosquito control. J Am Mosq Control Assoc 2010; 26(1): 67-87.
[http://dx.doi.org/10.2987/09-5936.1] [PMID: 20402353]
[166]
Lloyd CJ. The toxicity of pyrethrins and five synthetic pyrethroids, to Tribolium castaneum (Herbst), and susceptible and pyrethrin-resistant Sitophilus granarius (L.). J Stored Prod Res 1973; 9: 77-92.
[http://dx.doi.org/10.1016/0022-474X(73)90014-3]
[167]
Silveira RD, Faroni LR, Pimentel MA, Peternelli LA, Zocolo G. [Biological efficacy and persistence of biphenthrin sprayed on maize at different grain temperatures]. Neotrop Entomol 2006; 35(2): 264-8.
[http://dx.doi.org/10.1590/S1519-566X2006000200017] [PMID: 17348140]
[168]
Zaka SM, Iqbal N, Saeed Q, et al. Toxic effects of some insecticides, herbicides, and plant essential oils against Tribolium confusum Jacquelin du val (Insecta: Coleoptera: Tenebrionidae). Saudi J Biol Sci 2019; 26(7): 1767-71.
[http://dx.doi.org/10.1016/j.sjbs.2018.05.012] [PMID: 31762656]
[169]
Kharel K, Arthur FH, Zhu KY, Campbell JF, Subramanyam B. Evaluation of synergized pyrethrin aerosol for control of Tribolium castaneum and Tribolium confusum (Coleoptera: Tenebrionidae). J Econ Entomol 2014; 107(1): 462-8.
[http://dx.doi.org/10.1603/EC13355] [PMID: 24665733]
[170]
Iordanou NT, Watters FL. Temperature Effects on the toxicity of five insecticides against five species of stored-product insects. J Econ Entomol 1969; 62: 130-5.
[http://dx.doi.org/10.1093/jee/62.1.130]
[171]
Ishaaya I, Ascher KRS. Effect of diflubenzuron on growth and carbohydrate hydrolases of Tribolium castaneum. Phytoparasitica 1977; 5: 149-58.
[http://dx.doi.org/10.1007/BF02980348]
[172]
Jagadeesan R, Nayak MK, Pavic H, Chandra K, Collins PJ. Susceptibility to sulfuryl fluoride and lack of cross-resistance to phosphine in developmental stages of the red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae). Pest Manag Sci 2015; 71(10): 1379-86.
[http://dx.doi.org/10.1002/ps.3940] [PMID: 25382378]
[173]
Gao S, Xiong W, Wei L, et al. Transcriptome profiling analysis reveals the role of latrophilin in controlling development, reproduction and insecticide susceptibility in Tribolium castaneum. Genetica 2018; 146(3): 287-302.
[http://dx.doi.org/10.1007/s10709-018-0020-4] [PMID: 29797154]
[174]
Sehgal B, Subramanyam B, Arthur FH, Gill BS. Variation in susceptibility of laboratory and field strains of three stored-grain insect species to β-cyfluthrin and chlorpyrifos-methyl plus deltamethrin applied to concrete surfaces. Pest Manag Sci 2014; 70(4): 576-87.
[http://dx.doi.org/10.1002/ps.3580] [PMID: 23674499]
[175]
Ishaaya IYSAK, Casida JE. Pyrethroid synergism and prevention of emergence in Tribolium castaneum and Musca dornestica vicina by the insect growth regulator. Phytoparasitica 1984.
[176]
Ishaaya I, Elsner A, Acher S, Casida JE. Synthetic pyrethroids: toxicity and synergism on dietary exposure of Tribolium castaneum (Herbst) larvae. Pestic Sci 1983; 14: 367-72.
[http://dx.doi.org/10.1002/ps.2780140405]
[177]
Singh S, Prakash S. Development of resistance in Tribolium castaneum, Herbst (Coleoptera: Tenebrionidae) towards deltamethrin in laboratory. Intl J Sci Res Publ 2013; 3: 146-50.
[178]
Dyte CE. The spread of insecticide resistance in Tribolium castaneum (Herbst) (Coleoptera, Tenebrionidae). J Stored Prod Res 1970; 6: 255-61.
[http://dx.doi.org/10.1016/0022-474X(70)90015-9]
[179]
Opit GP, Phillips TW, Aikins MJ, Hasan MM. Phosphine resistance in Tribolium castaneum and Rhyzopertha dominica from stored wheat in Oklahoma. J Econ Entomol 2012; 105(4): 1107-14.
[http://dx.doi.org/10.1603/EC12064] [PMID: 22928286]
[180]
Sehgal B, Subramanyam B, Arthur FH, Gill BS. Variation in susceptibility of field strains of three stored grain insect species to spinosad and chlorpyrifos-methyl plus deltamethrin on hard red winter wheat. J Econ Entomol 2013; 106(4): 1911-9.
[http://dx.doi.org/10.1603/EC13083] [PMID: 24020310]
[181]
Awan DA, Saleem MA, Nadeem MS, Shakoori AR. Toxicological and biochemical studies on spinosad and synergism with piperonyl butoxide in susceptible and resistant strains of Tribolium castaneum. Pak J Zool 2012; 44: 649-62.


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 26
ISSUE: 29
Year: 2020
Published on: 03 September, 2020
Page: [3554 - 3568]
Pages: 15
DOI: 10.2174/1381612826666200513113140
Price: $65

Article Metrics

PDF: 32
HTML: 5