Sublethal Effects on Stored-Product Insects

Fundamentals of Stored-Product Entomology book on pages 244-245 has a table with sublethal effects of 20 pesticides on reproduction, mating, light response, development, tolerance, respiration, resistance or repellency for one or more of 11 species of stored-product insects as reported in 30 studies.

The following 178 papers examine the effects of sublethal doses of pesticides on 38 stored product insect species. Fifteen of these species were the subject of 5 or more papers, i.e., Tribolium casteneum (33), Sitophilus zeamais (22), Rhyzopertha dominica (18), Sitophilus oryzae (17), Tribolium confusum (16), Sitophilus granarius (14), Oryzaephilus surinamensis (11), Callosobruchus maculatus (9), Habrobracon hebetor (9), Plodia interpunctella (8), Tenebrio molitor (8), Trogoderma granarium (7), Corcyra cephalonica (6), Drosophila melanogaster (6) and Cadra cautella (5).

In the 177 papers cited here, insect responses to sublethal doses include 75 reproduction + 12 oviposition + 9 population increase + 6 longevity + 2 mating + 1 functional response + 1 sex pheromone = 106; 17 repellent + 15 mobility + 6 dispersion + 2 preference + 1 photic = 41; 18 development + 1 drinking + 14 feeding + 10 biochemical + 8 respiration = 51.

Sublethal effects are described in the papers cited here for phosphine (17), malathion (13), deltamethrin (13), carbon dioxide (9), pyrethrum (9), essential oils (8), DDT (7), methyl bromide (7), plant extracts (7), neem (6), permethrin (6), spinosad (6), cypermethrin (5), ethylene dibromide (5), modified atmospheres (5), pirimiphos-methyl (5) and 70 other pesticides that are each covered in fewer than 5 papers.

Guedes et al. (2011) reviewed current knowledge sublethal effects of pesticides on stored product insects and future needs. Beneficial or stimulatory effects of sublethal doses (hormesis) are discussed. Bond and Upitis (1973) and Hobbs and Bond (1989) looked at effect of repeated sublethal doses of phosphine on Sitophilus granarius, Tenebroides mauritanicus, Tribolium castaneum, Tribolium confusum. Khan and Selman (1988) looked at the effect sublethal exposure of Tribolium castaneum larvae on subsequent adults.

Considering the sublethal effects of pesticides may be important in doing cost-benefit analysis. There are additional benefits which are often overlooked such as delayed development, reduced reproduction and slower population growth which add no cost. Effectiveness of pesticides may be reduced by the pesticide avoidance behavior of insects and hormesis.

Abedi, Zahra. Moosa Saber, Gholamhossein Gharekhani1, Ali Mehrvar, Vahid Mahdavi. 2012. Effects of azadirachtin, cypermethrin, methoxyfenozide and pyridalil on functional response of Habrobracon hebetor Say (Hym.: Braconidae). Journal of Plant Protection Research 52(3): 353-358.

Adedire, C.O. and Lajide, L. 1999. Toxicity and oviposition deterrence of some plant extracts on cowpea storage bruchid, Callosobruchus maculatus Fabricius. Journal of Plant Diseases and Protection 106: 647-653.

Adeyemi, H. M. M. and D. A. Adebote. 2010. A Comparative study of the antifeedant effect of Bobgunnia madagascariensis (Desv.) J.H. Kirkbr & Wiersema. (Caesalpiniaceae) plant extracts with a standard storage pesticide. Electronic Journal of Environmental, Agricultural and Food Chemistry 9: 1559-1566. Tribolium casteneum, feeding

Adler, C. 1992. Vertical dispersion of adult Sitophilus granarius (L.) (Coleoptera: Curculionidae) in a wheat column flushed with modified atmospheres. J. Stored Prod. Res. 28: 201-209.

Ahmadi, M. and S. Moharramipour. 2011. Antifeedant Effects of Gamma Radiation and Rosmarinus Officinalis to Larval Stage of Tribolium castaneum (Col: Tenebrionidae). Intern. J. Artif. Organs 34: 667-667. feeding, plant extracts

Akrami, H., S. Moharramipour and S. Imani. 2011. Efficacy of Mentha longifolia and Thymus kotschyanus essential oils on nutrition indices and oviposition deterrence of Tribolium castaneum. IOBC/wprs Bulletin 69: 263-269. feeding

Al-Hakkak, Z., A. Murad and A. Hussain. 1985. Phosphine-Induced Sterility in Ephestia cautella (Lepidoptera, Pyralidae). J. Stored Prod. Res. 21: 119-121. reproduction

Ali, N. S., S. S. Ali and A. R. Shakoori. 2011. Effects of Sublethal Doses of Talstar on biochemical Components of Malathion-Resistant and -Susceptible Adults of Rhyzopertha dominica. Pak. J. Zool. 43: 879-887.

Ali, N. S., S. S. Ali and A. R. Shakoori. 2013. Effects of sublethal doses of malathion on biochemical components of malathion-resistant and-susceptible adults of Rhyzopertha dominica. Pakistan J. Zool. 45: 203-212.

Ali, N. S., S. S. Ali and A. R. Shakoori. 2014. Biochemical Response of Malathion-Resistant and-Susceptible Adults of Rhyzopertha dominica to the Sublethal Doses of Deltamethrin. Pakistan J. Zool. 42: 853-861.

Ara, N., M. Hossain and S. Parween. 2013. Preference between dimilin-treated and untreated food media by Tribolium castaneum (Herbst) larvae. Bangladesh Entomological Society 23: 21-27.

Arif, S., Naqvi, S. N. H., Rajput, T., Younus, M. F. and Arif, I. 2012. Effect of Acorus calamus, Biosal® and deltamethrin on fecundity of Callosobruchus analis. FUUAST Journal of Biology, 2(1): 131-133. reproduction

Arif, Samina, Naqvi, S. N. U. H., Raza, A., Tabassum, S. and Fatima, N. 2015. Fecundity effect of Biosal against Callosobruchus analis (Fabricius, 1781). International Journal of Fauna and Biological Studies 2 (2): 34-37. reproduction

Armstrong, K. F. and A. B. Bonner. 1985. Investigation of a permethrin-induced antifeedant effect in Drosophila melanogaster: an ethological approach.  Pestic. Sci. 16: 641-650. feeding

Arthur, F. H. 2012. Lethal and sub-lethal effects from short-term exposure of Rhyzopetha dominica on wheat treated with Storicide II ®. J. Pest Sci. 85: 261-265. reproduction

Asadi, Mohammad, Gadir Nouri-Ganbalani, Hooshang Rafiee-Dastjerdi, Mahdi Hassanpour and Bahram Naseri. 2018. The Effects of Rosmarinus officinalis L. and Salvia officinalis L.(Lamiaceae) Essential Oils on Demographic Parameters of Habrobracon hebetor Say (Hym.: Braconidae) on Ephestia kuehniella Zeller (Lep.: Pyralidae) Larvae. Journal of Essential Oil Bearing Plants 21(3): 713-731. population

Ascher, K., M. Eliyahu, E. Glotter, A. Goldman, I. Kirson, A. Abraham, M. Jacobson and H. Schmutterer. 1987. The Antifeedant Effect of some New Withanolides on 3 Insect Species, Spodoptera littoralis, Epilachna varivestis and Tribolium cstaneum. Phytoparasitica 15: 15-29. feeding, plant extracts

Bang, Y. H. and H. S. Telford. 1966. Effect of sublethal doses of fumigants on stored grain insects. Washington Agric. Exp. Sta. Techn. Bull. 50. Oryzaephilus surinamensis, Rhyzopertha dominica, Tribolium castaneum, Tribolium confusum, Trogoderma variabile, respiration, carbon tetrachloride, chloropicrin, ethylene dibromide, ethylene dichloride, hydrogen cyanide, methyl bromide, phosphine

Barlow, C. A. 1968. Changes in the photic reaction due to DDT in the granary weevil, Sitophilus granarius (L.) (Coleoptera: Curculionidae). Can. J. Zool. 46: 35-40.

Barson, G., D. Fleming and E. Allan. 1992. Laboratory assessment of the behavioral-responses of residual populations of Oryzaephilus surinamensis (L) (Coleoptera, Silvanidae) to the contact insecticide pirimiphos-methyl by linear logistic modeling. J. Stored Prod. Res. 28: 161-170. repellent

Beckel, H., I. Lorini and S. M. N. Lazzari. 2005. Repellency of deltamethrin against resistant and susceptibile insects of strains of Rhyzopertha dominica (F.) (Coleoptera, Bostrichidae) in stored wheat. Revista Brasileira de Entomologia 49(4): 572-574.

Bell, C. H. 1986. The response of insects to fumigant concentration gradients. p. 316-326. in: Proc. 4th Intern. Work. Conf. Stored-Prod. Prot. E. Donahaye and S. Navarro, Eds. Wallach Press, Jerusalem. Cryptolestes ferrugineus, Oryzaephilus surinamensis, SitophiIus granarius, Tribolium castaneum, mobility, methyl bromide, phosphine

Benezet, H. J. 1984. Survival of consecutive generations of cigarette beetles reared on media containing less than 1 ppm methoprene. p. 217-221. In R. B. Mills, V. F. Wright, J. R. Pedersen, W. H. McGaughey, R. W. Beeman, K. J. Kramer, R. D. Speirs and C. L. Storey (eds.) Proceedings of the 3rd International Working Conference on Stored-Product Entomology, 23-28 October, 1983, Manhattan, Kansas. Lasioderma serricorne, population

Benezet, H. J. and C. W. Helms. 1985. Reproductive potential of cigarette beetle population exposed to methoprene. Tobacco Sci. 29: 14-15. Lasioderma serricorne

Boles, H. P. 1971. Ovipositional responses of the rice weevil, Sitophilus oryzae (L.), treated with synergized pyrethrins. J. Kansas Entomol. Soc. 44: 70-75.

Boles, H. P. 1974. The effect of sublethal dosages of pyrethrins on the mating efficiency of the rice weevil, Sitophilus oryzae (L.) (Coleoptera: Curculionidae). J. Kansas Entomol. Soc. 47: 444-451.

Bond. E. J. and Upitis. E. 1973. Response of three insects to sublethal doses of phosphine. J. stored Prod. Res. 8: 307-313. Sitophilus granarius,Tenebroides mauritanicus, Tribolium confusum

Boots, M. and M. Begon. 1994. Resource Limitation and the Lethal and Sublethal Effects of a Viral Pathogen in the Indian Meal Moth, Plodia interpunctella. Ecol. Entomol. 19: 319-326. feeding

Bouchard, Brenda L. and Thomas G. Wilson. 1987. Effects of sublethal doses of methoprene on reproduction and longevity of Drosophila melanogaster (Diptera: Drosophilidae). Journal of economic entomology 80(2): 317-321.

Brady, U. E. and Finley, L. H. 1969. Behavioral response of bidrin-treated male Indian-meal moths to the female sex pheromone J. Econ. Entomol. 62: 1117-1118. Plodia interpunctella

Braga, L.S., Corrêa, A.S., Pereira, E.J.G. and Guedes, R.N.C. 2011. Face or flee? Fenitrothion resistance and behavioral response in populations of the maize weevil, Sitophilus zeamais. Journal of Stored Products Research 47: 161–167. repellent

Brudnaya, A. A., A. N. Chudinova and N. I. Anoskina. 1966. The effect of sublethal doses of toxic chemicals upon pests of stored products. Entomologicheskoe Obozrenie/ Entomological Review 45: 83-94. (in Russian with English summary) Sitophilus granarius, reproduction, chlorpicrin, methyl bromide, metallilchloride

Carlson, S. D. 1968. Respiration of confused flour beetle adults in CO2 or N2 and after sublethal fumigation. J. Econ. Entomol. 61: 125-131. Tribolium confusum, modified atmosphere

Celestino, Daiane, Guilherme I. Braoios, Rodrigo S. Ramos, Lessando M. Gontijo and Raul Narciso C. Guedes. 2014. Azadirachtin-mediated reproductive response of the predatory pirate bug Blaptostethus pallescens. BioControl 59(6): 697-705.

Chadwick, P. R. 1962. Studies on the sub-lethal effects of pyrethrins on the grain weevil, Calandra oryzae L. Pyrethrum Post 7: 11-15, 48. Sitophilus oryzae, reproduction

Chiam, W., Y. Huang, S. Chen and S. Ho. 1999. Toxic and antifeedant effects of allyl disulfide on Tribolium castaneum (Coleoptera : Tenebrionidae) and Sitophilus zeamais (Coleoptera : Curculionidae). J. Econ. Entomol. 92: 239-245. feeding

Cline, L. D., Zettler, J. L., McDonald, L. L. and Highland, H. A. 1984. Continuous exposure to sublethal doses of synergized pyrethrins: Effects on resistance and repellency in Tribolium confusum (Coleoptera: Tenebrionidae). J. Econ. Entomol. 77: 1189-1193.

Collins, P. J., Sinclair, E. R., Howitt, C. J. and Haddrell, R. L. 1988. Dispersion of grain beetles (Coleoptera) in grain partially treated with insecticide. J. Econ. Entomol. 81: 1810-1815. Rhyzopertha dominica, Sitophilus oryzae, Tribolium castaneum, bioresmethrin, carbaryl, fenitrothion

Corrêa, A. S., E. M. G. Cordeiro, L. S. Braga, E. J. G. Peireira and R. N. C. Guedes. 2010. Physiological and behavioral resistance to esfenvalerate + fenitrothion in populations of the maize weevil, Sitophilus zeamais, pp. 851-857. In M. O. Carvalho, P. G. Fields, C. S. Adler, F. H. Arthur, C. G. Athanassiou, J. F. Campbell, F. Fleurat-Lessard, P. W. Flinn, R. J. Hodges, A. A. Isikber, S. Navarro, R. T. Noyes, J. Riudavets, K. K. Sinha, G. R. Thorpe, B. H. Timlick, P. Trematerra and N. D. G. White (eds.), Proceedings of the 10th International Working Conference on Stored Product Protection, 27 June-2 July 2010, Estoril, Portugal. Julius Kühn-Institut, Berlin, Germany. mobility, population

Cox P. D., D. A. Fleming, J. E. Atkinson, K. L. Bannon and J. M. Whitefield. 1997. The effect of behavior on the survival of Cryptolestes ferrugineus in an insecticide-treated laboratory environment. Journal of Stored Products Research 33: 257–269. mobility, fenitrothion, malathion

Dawson, C. 1995. The effect of carbon dioxide induced anaethesia on fecundity of Callosobruchus maculatus (Coleoptera: Bruchidae). J. stored Prod. Res. 31: 49-54. reproduction

Dutt, N. and Roy, D. 1984. Effect of sublethal dosages of insecticide on the population dynamics of pulse beetle, Callosobruchus chinensis L. Sci. Cult. 50: 167-170. diazinon, dimethoate, fenitrothion, fenthion, methyl demeton

El-Lakwah, F. A. et al. 1991. Effect of the sublethal dose of phosphine on the biological characteristics of the survivors of the flour mite Acarus Siro L. Egyptian J. Appl. Sci. 6 (10): 285-291.

El-Nahal, A. K. M., and El Halfawy, M. A. 1973. The effect of sublethal doses of carbon disulfide on the biology of Tribolium confusum (Duv.), Sitophilus oryzae (L.) and Sitophilus granarius (L.) (Coleoptera). Bull. Entomol. Soc. Egypt Econ. Ser. 7: 201-211. development, reproduction

El-Nahal, A. K. M., and El Halfawy, M. A. 1973. The effects of sublethal doses of methyl bromide on the biology of the confused flour beetle, Tribolium confusum (Duv.) (Coleoptera: Tenebrionidae). Bull. Entomol. Soc. Egypt Econ. Ser. 7: 123-132. development, reproduction

El-Nahal, A. K. M., and El Halfawy, M. A. 1973. The effects of sublethal treatments with pyrethrins and certain dusts on some biological aspects of Sitophilus oryzae L. and S. granarius L. (Coleoptera). Bull. Entomol. Soc. Egypt Econ. Ser. 7: 253-260. reproduction

El-Nahal, A. K. M., G. H. Schmidt and E. M. Risha. 1994. Influence of vapours of Acorus calamus L. oil on the reproductivity of some stored produt Coleoptera. Pak. J. Entomol., Karachi 9: 21-27.

Emekci M, Navarro S, Donahaye E, Rindner M, Azrieli, A. 2004. Respiration of Rhyzopertha dominica (F.) at reduced oxygen concentrations. Journal of Stored Products Research 40: 27–38.

Faragalla, A., M. Ibrahim and S. Mostafa. 1985. Reproductive Inhibition of F1 Progeny of some Stored Grain Pests (Tenebrionidae, Bostrichidae) Fed on Grains Treated with the Antimoulting Inhibitor Dimilin. Zeitschrift Fur Angewandte Entomologie-Journal of Applied Entomology 100: 57-62. Latheticus oryzae, Rhyzopertha dominica, Tribolium castaneum, Tribolium confusum

Flaherty, B. R., Press, J. W. and Lum, P. T. M. 1973. Fecundity of Plodia interpunctella (Hübner) adults after exposure to sublethal dosages of carbon dioxide. J. Ga. Entomol. Soc. 8: 141-145. reproduction

Fondacaro, Joseph D., and Andrew Butz. 1970. Circadian rhythm of locomotor activity and susceptibility to methyl parathion of adult Tenebrio molitor (Coleoptera: Tenebrionidae). Annals of the Entomological Society of America 63(4): 952-955. mobility

Freitas, Rita Cristina P., Lêda Rita D’Antonino Faroni, Khalid Haddi, Luis O. Viteri Jumbo and Eugênio E. Oliveira. 2016. Allyl isothiocyanate actions on populations of Sitophilus zeamais resistant to phosphine: Toxicity, emergence inhibition and repellency. J. Stored Prod. Res. 69: 257-264. development

Grosch, D. S. 1975. Reproductive performance of Bracon hebetor after sublethal doses of carbaryl.  J. Econ. Entomol. 68: 659-662

Guedes R. N. C., J. F. Campbell, F. H. Arthur, G. P. Opit, K.Y. Zhu and J. E. Throne. 2008. Acute lethal and behavioral sublethal responses of two stored-product psocids to surface insecticides. Pest Management Science 64: 1314–1322. Liposcelis bostrychophila, Liposcelis entomophila, mobility, β-cyfluthrin, chlorfenapyr, pyrethrins

Guedes N. M. P., R. N. C. Guedes, G. H. Ferreira and L. B. Silva. 2009. Flight take-off and walking behavior of insecticide-susceptible and –resistant strains of Sitophilus zeamais exposed to deltamethrin. Bulletin of Entomological Research 99: 393–400. mobility

Guedes, R. N. C., N. M. P. Guedes, and C. A. Rosi-Denadai. 2011. Sub-lethal effects of insecticides on stored-product insects: current knowledge and future needs, Stewart Postharvest Review 7(3): 1-5 doi: 10.2212/spr.2011.3.5 ed.

Guedes, N. M. P., R. N. C. Guedes, L. B. Silva, and E. M. G. Cordeiro. 2009. Deltamethrin-induced feeding plasticity in pyrethroid-susceptible and -resistant strains of the maize weevil, Sitophilus zeamais. J. Appl. Entomol. 133: 524-532.

Guedes, N.M.P., L.B. Silva, R.N.C. Guedes. 2006. Deltamethrin-induced behavioral responses of pyrethroid-resistant and -susceptible populations of the maize weevil (Sitophilus zeamais) p. 299-305. In Lorini, I.; Bacaltchuk, B.; Beckel, H.; Deckers, D.; Sundfeld, E.; dos Santos, J.P.; Biagi, J.D.; Celaro, J.C.; Faroni, L.R.D’A.; Bortolini, L.de O.F.; Sartori, M.R.; Elias, M.C.; Guedes, R.N.C.; da Fonseca, R.G.; Scusse, V.M. (Eds.), Proceedings of the 9th International Working Conference on Stored Product Protection, 15-18 October 2006, Campinas, Sao Paulo, Brazil. Brazilian Post-harvest Association – ABRAPOS, Passo Fundo, RS, Brazil. repellent

Guedes NMP, Tolledo J, Corrêa AS and Guedes RNC. 2010. Insecticide induced hormesis in an insecticide-resistant strain of the maize weevil, Sitophilus zeamais. Journal of Applied Entomology 134: 142–148. reproduction, deltamethrin

Guedes, Raul Narciso C., Mayra Velez and Spencer S. Walse 2018. Spinosad-induced stress on the maize weevil Sitophilus zeamais p. 759-768. In C.S. Adler, G. Opit, B. Fürstenau, C. Müller-Blenkle, P. Kern, F.H. Arthur, C.G. Athanassiou, R. Bartosik, J. Campbell, M.O. Carvalho, W. Chayaprasert, P. Fields, Z. Li, D. Maier, M. Nayak, E. Nukenine, D. Obeng-Ofori, T. Phillips, J. Riudavets, J. Throne, M. Schöller, V. Stejskal, H. Talwana, B. Timlick, P. Trematerra eds. Proceedings of the12th International Working Conference on Stored Product Protection (IWCSPP) in Berlin, Germany, October 7-11, 2018. walking, feeding, drinking, mating behavior,  deltamethrin, spinosad

Haddi, K., L. P. Mendonça, M. F. Dos Santos, R. N. C. Guedes, and E. E. Oliveira. 2015. Metabolic and Behavioral Mechanisms of Indoxacarb Resistance in Sitophilus zeamais (Coleoptera: Curculionidae). J. Econ. Entomol. 108: 362-369. biochemical, repellent

Haddi, K., E. E. Oliveira, L. R. A. Faroni, D. C. Guedes and N. N. S. Miranda. 2015 Sublethal Exposure to Clove and Cinnamon Essential Oils Induces Hormetic-Like Responses and Disturbs Behavioral and Respiratory Responses in Sitophilus zeamais (Coleoptera: Curculionidae). J. Econ. Entomol. 108: 2815-2822. mobility

Harein, Phillip K. 1960. Effect of ronnel upon the adult rice weevil, Sitophilus oryza. J. Econ. Entomol. 53(3): 372-375. reproduction

Herrick, Glenn W., and William R. Horsfall. 1931. The reproductivity of the bean weevil (Mylabris obtectus Say) as affected by the vapor of ethylene oxide. J. Econ. Entomol. 24(5): 1084-1086. Acanthoscelides obtectus

Hobbs, S., and E. Bond. 1989. Response of Tribolium castaneum (Herbst) (Coleoptera, Tenebrionidae) to Sublethal Treatments with Phosphine. J. Stored Prod. Res. 25: 137-146.

Hodges, R. J., and Meik, J. 1986. Lethal and sublethal effects of permethrin on Tanzanian strains of Tribolium castaneum (Herbst), Gnatocerus maxillosus (F.), Sitophilus oryzae (L.) and Sitophilus zeamais Motschulsky. Insect Sci. Appl. 7: 533-537. repellent, reproduction

Howe, R. W. and B. D. Hole 1967. Predicting the dosage of fumigant needed to eradicate insect pests from stored products. J. Appl. Ecol. 4: 337-351. Sitophilus granarius, longevity, reproduction, methyl bromide

Izakmehri, Khadijeh, Moosa Saber, Ali Mehrvar, Mohammad Bagher Hassanpouraghdam and Samad Vojoudi. 2013. Lethal and sublethal effects of essential oils from Eucalyptus camaldulensis and Heracleum persicum against the adults of Callosobruchus maculatus. Journal of Insect Science 13(152): 1-10. 2013 doi: http://dx.doi.org/10.1673/031.013.15201. longevity, reproduction

Jacob, P. and A. Qamar. 2013. Reproductive impairment and lethal effects of selected combinations of some essential oils against the rice moth, Corcyra cecphalonica. European Journal of Experimental Biology 3: 409-415.

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Kroschel, Jurgen and Octavio Zegarra 2013. Attract-and-kill as a new strategy for the management of the potato tuber moths Phthorimaea operculella (Zeller) and Symmetrischema tangolias (Gyen) in potato: evaluation of its efficacy under potato field and storage conditions. Pest Manag. Sci.  69(11): 1205-1215. repellent, cyfluthrin

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Laudani, H. & Swank, G.R. (1954) A laboratory apparatus for determining repellency of pyrethrum when applied to grain. Journal of Economic Entomology 47: 1104–1107. Attagenus unicolor, Lasioderma serricorne, Lophocateres pusillus, Oryzaephilus surinamensis, Rhyzopertha dominica, Sitophilus, Tribolium castaneum

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