Sublethal effects of thiocyclam hydrogen oxalate and spiromesifen, on life history and population growth of Encarsia formosa (Hymenoptera: Aphelinidae)

Document Type : Complete paper

Authors

1 Department of Plant Protection, Faculty of Agriculture, Urmia University, Urmia, Iran

2 Plant Protection Research Department, Agricultural and Natural Resources Research Center, Urmia, Iran

Abstract

Encarsia formosa Gahan (Hymenoptera: Aphelinidae) is one of the most important endoparasitoids of the greenhouse whitefly, Trialeurodes vaporariorum, westwood (Hemiptera: Aleyrodidae). In this study, we investigated the sub-lethal effects (LC25) of two insecticides, thiocyclam hydrogen oxalate and spiromsifen, on the life table and population growth parameters of E. formosa under laboratory conditions. Bioassays were conducted by dipping bean leaves containing parasitized third instar nymphs of T. vaporariorum in the obtained LC25 concentrations of the two insecticides. The life table data were analyzed using the computer program TWOSEX–MSChart based on the age-stage, two-sex life table theory. The results showed that the shortest pre-adult period and the lowest survival rate were recorded in the F1 generation of parasitoides exposed to spiromsifen. Additionally, both thiocyclam hydrogen oxalate and spiromesifen reduced adult longevity, fecundity rate and reproductive days compared to the control group. However, using of sub-lethal concentration of spiromesifen negatively affeted on the population growth parameters (R0, r, and λ) of E. formosa, while thiocyclam hydrogen oxalate had no side effects on these parameters. The findings of this research suggest that thiocyclam hydrogen oxalate has the less harmful effect compared to spiromesifen on E. formosa, likely due to the biorational properties. This makes thiocyclam hydrogen oxalate a promising option for the management of T. vaporariorum. It would be better to evaluate complementary experiments in terms of its side effects against other natural enemis of greenhouse whitefly under greenhouse conditions.

Keywords

Main Subjects


Extended Abstract

Introduction

    Greenhouse whitefly, Trialeurodes vaporariorum, Westwood is one of the most important pests of vegetables, and ornamental plants. Usage of either biological agents or chemical control are considered in management of greenhouse whitefly. Therefore knowing the compatibility and effect of insecticides on biological agents is essential for the effective integration of chemical and biological control. For this reason, in this study, the lethal and sub-lethal effects (LC25) of two insecticides, thiocyclam hydrogen oxalate and spiromsifen were evaluated on life table and population growth parameters of Encarsia formosa Gahan (Hymenoptera: Aphelinidae), as one of the most important endoparasitoids of greenhouse whitefly under laboratory conditions. The lethal effects of insecticides lead to the death of the insect, while the sublethal effects may have different aspects. The sublethal effects of insecticides can reduce the performance of biological agents that play a key role in predicting the success of natural enemies in IPM programs.

Materials and Methods

    The colony of whitefly used in the experiment was collected on ornamental crops (vervain and hollyhocks). The whitefly population was reared on bean var. MINA in plastic pots (15 × 19 cm) under controlled greenhouse conditions (27 ± 2°C, 65% ± 10% RH, and a photoperiod of 16: 8 [L: D] h). It is worth mentioning that in order to equalize the bioassay test conditions with greenhouse and field conditions, the LC25 concentration obtained for T. vaporariorum was used in the tests related to the sublethal effects of parasitoid wasps.

The dipping method was used in bioassay and life table studies against parasitized of the third instar nymphs of the whitefly T. vaporariorum. The LC50 value of thiocyclam hydrogen oxalate and spiromsifen insecticides for parasitized third instar nymphs of the whitefly were 392.627 and 854.871 ppm, respectively after 24 hours. The LC25 concentrations (117.520 and 731.548 ppm) were used to estimate the sub-lethal effects of  thiocyclam hydrogen oxalate and spiromsifen on the biological parameters of parasitized third instar nymphs of the whitefly. The age stage, two-sex life table method was used to analyze the collected data. We used the bootstrap technique with 100,000 iterations to estimate the variance and standard errors of the biological and population parameters and used Sigma Plot software to draw graphs. The growth of the pest population in a period of 60 days was done using Timing-MsChart software.

 

Results

     According to the results, the shortest pre-adult period and the lowest survival rate were recorded in the F1 generation of E. formosa were exposed to spiromsifen. The adult lifespan/longevity was significantly different from the control by LC25 concentration of mentioned insecticides. The longest lifespan of adult parasitoid in control treatment was recorded as 21.0 days. Fecundity were significantly reduced in sublethal concentration of the insecticides compared to the control. The highest value of fecundity in control treatment was recorded 17.76 eggs per female and the lowest value in spiromesifen treatment was 3.38 eggs per female. The mean oviposition period of parasitoides decreased from 4.59 days in control to 3 and 1.92 days in LC25 concentration of thiocyclam hydrogen oxalate and spiromsifen insecticides respectively. Additionally, usage of sublethal concentration of spiromesifen had negatively effects on the population growth parameters (R0, r, and λ), but thiocyclam hydrogen oxalate had no side effects on population growth parameters of E. formosa. Also, the sublethal concentration of thiocyclam hydrogen oxalate and spiromsifen reduced the net reproductive rate (R0) from 15.1 nymphs per female in the control treatment to 7.3 and 2.2 nymphs in thiocyclam hydrogen oxalate and spiromsifen insecticides, respectively. The intrinsic rate of increase (r) was recorded 0.1410 (day-1) on control and 0.1260 and 0.0500 (day-1) on thiocyclam hydrogen oxalate and spiromsifen, respectively. The  finite rate of increase (λ) and gross reproductive rate (GRR), in spiromesifen treatment were also significantly lower than the control. The mean generation time (T) of treatment affected by LC25 concentration of insecticides reduced compared to the control treatment.

 

Discussion

    The findings of this research suggested that thiocyclam hydrogen oxalate was the less side effect compared to spiromesifen on E. formosa, likely due to the its biorational properties and this makes it as a promising option for the management of T. vaporariorum. Due to the broad-spectrum effects of thiocyclam hydrogen oxalate, it would be better to evaluate complementary experiments in terms of its side effects against other natural enemis of greenhouse whitefly under greenhouse conditions.

Abedi, Z., Saber, M., Gharekhani, G., Mehrvar, A. & Kamita, S.G. (2014). Lethal and sublethal effects of azadirachtin and cypermethrin on Habrobracon hebetor (Hymenoptera: Braconidae). Journal of Economic Entomology, 107(2), 638–645.
Arayal, J.E., Estay, P. & Araya, M.H. (2006). Short communication. Toxicity of abamectin, acetamiprid, imidacloprid, mineral oil and an industrial detergent with respect to Encarsia formosa (Gahan)parasitizing Trialeurodes vaporariorum Westwood nymphs. Spanish Journal of Agricultural Research, 1, 86-90.
Asadi, M., Rafiee–Dastjerdi, H., Nouri–Ganbalani, G., Naseri, B. & Hassanpour, M. (2019). Lethal and sublethal effects of five insecticides on the demography of a parasitoid wasp. International Journal of Pest Management, 65(4), 301–312.
Barati, R., Golmohammadi, Gh., Ghajarie, H., Zarabi, M. & Mansouri, R. (2013). The effects of some botanical insecticides and pymetrozine on life table parameters of silver leaf whitefly Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae). Pesticides and Phytomedicine, 28, 47-55.
Barati, R., Golmohammadi, Gh., Ghajarie, H., Zarabi, M. & Mansouri, R. (2014). Efficiency of some herbal pesticides on reproductive parameters of silverleaf whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Archives of Phytopathology and Plant Protection, 47, 212-221.
Bayram, A., Salerno, G., Onofri, A. & Conti, E. (2010), Sub–lethal effects of two pyrethroids on biological parameters and behavioral responses to host cues in the egg parasitoid Telenomus busseolae. Biological Control, 53(2), 153–160.
Beheshti, A. Imani, S., Zahdi, H., Tirgari, S., & Abdi Gudarzi, M. (2022). Investigation of the sublethal effects of the insecticides Apel, Abacmetin and Amidachloropride on the life span of different life stages of greenhouse whiteflies (Trialeurodes vaporariorum) (Hem.: Aleyrodidae) in laboratory conditions. Quarterly Entomological Research Specialty (scientific-research). 14(1): 27-31 (in Persian). Bielza, P., Fernández, E., Grávalos, C. & Izquierdo, J. (2009). Testing for non-target effects of spiromesifen on Eretmocerus mundus and Orius laevigatus under greenhouse conditions. Biological control, 54, 229-236.
Bigham, Z., Allahyari, H., Talebi Jahrami, K. & Hosseininaveh, V. (2021). Survey on different populations of Trialeurodes vaporariorum (Hem.: Aleyrodidae) resistance to imidacloprid and its effect on Encarsia formosa (Hym.: Aphelinidae) resistance. Plant Pest Research, 11 (3): 29-44 (in Persian).
Capinera, J. L. (2008) Greenhouse whitefly, Trialeurodes vaporariorum (westwood) (Hemiptera: Aleyrodidae). Encyclopedia of Entomology. Springer, Netherland, pp. 1723-1726.
Chi, H.  & Liu, H. (1985). Two new methods for the study of insect population ecology. Bulletin of the Institute of Zoology, Academia Sinica, 225-240.
Chi, H. (1988). Life-table analysis incorporating both sexes and variable development rates among individuals. Environmental Entomology, 17 (1), 26-34.
Chi, H. (2020a). TWOSEX-MSChart: a computer program for age stage, two-sex life table analysis. National Chung Hsing University, Taichung, Taiwan; available from http://140.120.197.173/ Ecology/Download/TWOSEX-MSChart.rar.
Chi, H. (2020b) TIMING-MSChart: a computer program for the population projection based on age-stage, two-sex life table. Taichung, Taiwan: National Chung Hsing University; Available from http://140.120.197.173/Ecology/Download/TimingMSChart.rar.
Chiasson, H., Vincent, C. & Bostanian, N.J. (2004). Insecticidal properties of a Chenopodium-based botanical. Journal of Economic Entomology, 97, 1378-1383.
Dadras, S., Mehrkhou, F., Atlihan, R. & Fourouzan, M. (2024).  The sublethal effects of thiamethoxam-lambda cyhalothrin on the life table parameters and the population prediction of greenhouse whitefly, Trialeurodes vaporariorum, and its parasitoid, Encarsia formosa, under laboratory conditions. Journal of Entomological Society of Iran, (In press).
De Cock, A., Ishaaya, I., Degheele, D., & Veierov, D. (1990). Vapor toxicity and concentration-dependent persistence of buprofezin applied to cotton foliage for controlling the sweetpotato whitefly (Homoptera: Aleyrodidae). Journal of Economic Entomology, 83 (4), 1254-1260. doi:10.1093/jee/83.4.1254
Desneux, N., Decourtye, A. & Delpuech, J.M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52: 81–106.
 Desneux, N., Denoyelle, R. & Kaiser, L. 2006. A multi–step bioassay to assess the effect of the deltamethrin on the parasitic wasp Aphidius ervi. Chemosphere, 65 (10): 1697–1706.
Drobnjaković, T. & Marčić, D. (2021). Effects of spirotetramat insecticide on life history traits and population growth of Encarsia formosa (Hymenoptera: Aphelinidae). Biocontrol Science and Technology, 31(6), 604-618. https://doi.org/10.1080/09583157.2021.1873248.
Drobnjaković, T., Marčić, D., Prijović, M. & Milenković, S. (2019). Toxic and sublethal effects of buprofezin on the whitefly parasitoid Encarsia formosa Gahan. Pesticidi i fitomedicina, 34(3-4): 201-209. https://doi.org/10.2298/PIF1904201D.
Drobnjakovic, T., Marcic, D., Prijovic, M., Peric, P., Milenkovic, S. and Boskovic, J. 2018. Sublethal effects of NeemAzal-T/S botanical insecticide on Dutch and Serbian populations of Encarsia formosa (Hymenoptera: Aphelinidae). Biocontrol Science and Technology, 28 (1): 1-19.
Drobnjaković, T., Marčić, D., Prijović, M., Perić, P., Milenković, S., and Bošković, J. 2016. Life history traits and population growth of Encarsia formosa Gahan (Hymenoptera: Aphelinidae) local population from Serbia. Entomology Generalis35, 281-295.
Drobnjaković, T., Marčić, D., Prijović, M., Perić, P., Milenković, S., and Bošković, J. )2018(. Sublethal effects of NeemAzal-T/S botanical insecticide on Dutch and Serbian populations of Encarsia formosa (Hymenoptera: Aphelinidae). Biocontrol Science and Technology28 (1): 1-19.
Ebneabbasi, S., Mehrkhou, F. & Fourouzan, M. (2023) Lethal and sublethal effects of thiocyclam hydrogen oxalate and flubendimide on the population growth parameters and population projection of Tuta absoluta (Lepidoptera: Gelechiidae). Journal of Entomological Society of Iran, 43 (3), 219-231. doi:  10.61186/JESI.44.2.71
Endo, S. & Tsurumachi, M. (2001). Insecticide susceptibility of the brown plant hopper and the whiteback plant hopper collected from Southeast Asia, Journal of Pesticide Science, 26 (1), 82-86.
Enkegaard, A., & Brǿdsgaard, H.F. (2006). Biocontrol in protected crops: is lack of biodiversity a limiting factor? In: J. Eilenberg and H.M.T. Hokkanen (eds.), An ecological and society approach to biological control (pp. 91-122). The Netherlands: Springer. doi: 10.1007/978-1-4020-4401-4
Fazeli Dinan, M., Talaei-Hassanloui, R., Allahyari, H., Kharazi Pakdel, A. & Goldansaz, S. H. 2012. The effect of the fungus Lecanicillium longisporum (Hypocreales: Clavicipitaceae) on the parameters of the life table of the parasitoid bee Encarsia formosa (Hymenoptera: Aphelinidae). Plant Pest Research, 2(2): 1-11 (in Persian)
Fernández, M., Medina, P., Fereres, A., Smagghe, G. & Vinuela, E. (2015). Are mummies and adults of Eretmocerus mundus (Hymenoptera: Aphelinidae) compatible with modern insecticides.  Ecotoxicology, 108(5): 2268-2277. doi:10.1093/jee/tov181
Fuladi, M., Golmohammadi, G. & Qajarieh, H. (2014). Review of the lethal and sublethal effects of azadirachtin, flunicamid, thiaclopride and thiocyclam on the parasitic bee Habrobracon hebetor. Journal of Biocontrol in Medicinal Plants, 3(1): 2423-5148.
Fuladi, M., Golmohammadi, G. H. & Ghajarieh, H. (2015). Lethal and sublethal effects of insecticides azadirachtin, flonicamid, thiacloprid and thiocyclam on parasitoide wasp Habrobracon hebetor. Biocontrol in Plant Protection, 3(1), 9-18. doi:  10.22092/BCPP.2015.103134
Galvan, T. L., Koch, R. L., & Hutchison, W. D. (2005). Effects of spinosad and indoxacarb on survival, development, and reproduction of the multicolored Asian lady beetle (Coleoptera: Coccinellidae). Biological Control, 34, 108-114. Doi: 10.1016/j.biocontrol.2005.04.005.
Greathead, D.J. (1995). Natural enemies in combination with pesticides for integrated pest management. In R. Reuveni (Ed.), Novel approaches to integrated pest management (pp. 183–197). Boca Raton, FL: CRC Press.
Guedes, R.N.C., Smagghe, G., Stark, J. D. & Desneux, N. (2016). Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annual Review of Entomology, 61, 43-62. doi: 10.1146/annurev-ento-010715-023646
Heidari, A., Moharramipour, S., Poormirza, A. A., & Talebi, A. A. (2006). Effects of buprofezin, pyriproxyfen and fenpropathrin on the reproductive parameters of Encarsia formosa (Hymenoptera: Aphelinidae)Journal of Entomological Society of Iran, 36 (2): 353 -361.
Hoseininaveh, V., Salehi, L., Ghadamyari, M. & Gholamzadeh, M. (2012). Effects of amitraz, buprofezin and propargite on some fitness parameters of the parasitoid Encarsia formosa (Hym.: Aphelinidae), using life table and IOBC methods. Journal of Entomological Society of Iran, 31(2), 1-14.
Hosseininia, A., Khanjani, M., Khobdel, M. & Javadi Khodri, S. (2016). Comparision the effectiveness of common oils and insecticidal compounds in controlling the greenhouse whitefly Trialeurodes vaporariorum (Westwood) (Hem.: Aleyrodidae) on rose and investigating their interaction. Iranian Plant Protection Research, 30 (4), 718-726 (in Persian)
Infante, F. (2000). Development and population growth rates of Prorops nasuta (Hym.: Bethylidae) at constant temperatures. Jourmnal of Applied Entomology, 124, 343-348.
Karatolos, N., Denholm, I., Williamson, M., Nauen, R. & Gorman, K. (2010). Incidence and characterization of resistance to neonicotinoid insecticides and pymetrozine in the greenhouse whitefly, Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae). Pest Management Science, 66, 1304-1307.
Majidpour M., Maroofpour N., Ghane-Jahromi M., & Guedes R.N.C. (2020). Thiacloprid+ deltamethrin on the life-table parameters of the cotton aphid, Aphis gossypii (Hemiptera: Aphididae), and the parasitoid, Aphidius flaviventris (Hymenoptera: Aphelinidae). Journal of economic entomology, 113, 2723-2731. https://doi.org/10.1093/jee/toaa214
Medeiros, G.F., Mendes, A., Castro, R.A., Baú, E.C., Nader, H.B. &  Dietrich, C.P. (2000). Distribution of sulfated glycosaminoglycans in the animal kingdom: widespread occurrence of heparin-like compounds in invertebrates. Biochimica et Biophysica Acta (BBA)-General Subjects, 1475 (3): 287-294. https://doi.org/10.1016/S0304-4165(00)00079-9
Mehdi Fuladi, M. Gul Mohammadi, G. & Hamid Qajareh, h. 2014. Investigating the lethal and sublethal effects of azadirachtin, flunicamide, thiacloprid and tiocyclam on the parasitic bee Habrobracon hebetor. The 3rd International Congress of Entomology of Iran, (220) (in Persian)
Nastri Nasrabadi, H. & Tabasian, H. (2021). Investigating the lethal and sublethal effect of palizin insecticide and salinity stress on Aphis gossypii in laboratory conditions. Applied Researches in Herbal Medicine, 10(4): 1-15 (in Persian).  https://doi.org/10.22034/arpp.2021.13483
Noorbakhsh, S. (2018). List of important pests, diseases, and weeds of major agricultural crops, pesticides and recommended methods for their control. Ministry of Agriculture Jihad and Plant Protection Organization. 209 p. (In Persian).
Oliveira, M. R.V.,  Amancio, M., Laumann, R. A., & de O. Gomes, L. (2003). Natural enemies of Bemisia tabaci (Gennadius) B biotype and Trialeurodes vaporariorum (Westwood) (Hemiptera: Aleyrodidae) in Brasília, Brazil. Neotropical Entomology, 32 (1): 151-154. https://doi.org/10.1590/S1519-566X2003000100023.
Papachristos, D.P. & Milonas, P.G. 2008. Adverse effects of soil applied insecticides on the predatory coccinellid Hippodamia undecimnotata (Coleoptera: Coccinellidae). Biological Control, 47(1), 77–81.
Pappari, S., Dousti, A., Fallahzadeh, M., Ullah, F., Desneux, N, & Saghaeim, N. (2022). Lethal and sublethal effects of commonly used insecticides on South American tomato pinworm, Tuta absoluta Meyrick and its parasitoid, Trichogramma brassicae Bezdenko. Research Square, 1-39.
Perera, P. A. (1982). Some effects of insecticide deposit pattern on the parasitism of Trialeurodes vaporariorum by Encarsia formosa. Annual Applied Biology, 101, 239-244.
Pilkington, L.J., Messelink, G., van Lenteren, Y.C., & Le Mottee, K. (2010). Protected Biological Control. Biological pest management in the greenhouse industry. Biological Control, 52(3), 216-220. doi: 10.1016/j.biocontrol.2009.05.022
Piri Ouchtape, M., Mehrkhou, F. & Foorouzan, M. (2024). Lethal and sub-lethal effects of Clothianidin and summer oil on the life table parameters and population trend of the cabbage aphid, Brevicoryne brassicae (Hem.: Aphididae). Plant Pest Research, 13 (4): 17-34.
Polaszek, A., Evans, G.A., & Bernett, F.D. (1992). Encarsia parasitoids of Bemisia tabaci (Hymenoptera: Aphelinidae, Homoptera: Aleyrodidae): a preliminary guide to identification. Bulletin of Entomological Research, 82(3), 375-392. doi:10.1017/S0007485300041171.
Qu, Y., Xiao, D., Li, J., Chen, Z., Biondi, A., Desneux, N., & Song, D. (2015). Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology24 (3): 479-487.
Rajaee, F. Ghane-Jahromi, M, Maroofpour, N. & Sedaratian-Jahromi, A. (2022). Sublethal effects of spiromesifen on life table traits of Tetranychus urticae (Acari: Tetranychidae) and Neoseiulus californicus (Acari: Phytoseiidae). Acarologia, 62 (3), 772-785.
Rakhshani, M.)2005(. Principle of agricultural toxicology (pesticides). Farhang Jame Press Center of Tehran, Iran, p. 100-374. (In Persian).
 Rashidi F. &   Nouri Ganbalani, G. (2018). Toxicity and sublethal effects of selected insecticides on life parameters of Encarsia formosa (Hymenoptera: Aphelinidae), a parasitoid of Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). Journal of Entomological Science, 53(4), 543-553.
Reshadat-Salvanagh, N. (2021). Survey on the sublethal effects of Flonicamid and Bino2 on the population growth prameters of Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). MSc thesis, Urmia University, 75 p.
Rezaei, N., Mossadegh, M.S., Kocheyli, F., Jahromi, K.T. & Kavousi, A.(2018). Sub–Lethal Effects of Thiamethoxam and Pirimicarb on Life–Table Parameters of Diaeretiella rapae (Hymenoptera: Braconidae), Parasitoid of Lipaphis erysimi (Hemiptera: Aphididae). International Journal of Agricultural and Biosystems Engineering, 12(10), 321–328.
Safavi, S.A. & Bakhshaei, M. (2017). Biological parameters of Trialeurodes vaporariorum (Hemiptera: Aleyrodidae) exposed to lethal and sublethal concentrations of Calypso®. Journal of Crop Protection, 6 (3): 341-351.
Saidi, Z. & Ziaei, M. 2017. The toxicity of Sivanto ® and Ebron Speed ® insecticides to control sugarcane whitefly, Nemaskellia andropogonis, (Hem.: Aleyrodidae) in laboratory conditions. Plant Pest Research, 8 (2): 53-65. (in Persian(
Sarbaz S., Goldasteh S., Zamani A.A., Solymannejadiyan E., & Vafaei Shoushtari R. (2017). Side effects of spiromesifen and spirodiclofen on life table parameters of the predatory mite, Neoseiulus californicus McGregor (Acari: Phytoseiidae). International Journal of Cardiology, 43, 380-386. https://doi.org/10.1080/01647954.2017.1325396
Sarmadi, S., Nouri–Gonbalani, G., Rafiee–Dastjerdi, H., Hassanpour, M. & Farshbaf–Pourabad, R. (2010). The effects of imidacloprid, indoxacarb and deltamethrin on some biological and demographic parameters of Habrobracon hebetor Say (Hymenoptera: Braconidae) in adult stage treatment. Munis Entomology and Zoology, 5, 646–651.
Schneider, M.I., Smagghe, G., Pineda, S. & Vinuela, E. (2004). Action of insect growth regulator insecticides and spinosad on life history parameters and absorption in third–instar larvae of the endoparasitoid Hyposoter didymator. Biological Control, 31(2), 189–198.
Sheikhigarjan, A. Najafi, H., Abbasi, Azimi, H. & Moradi, M. (2021). The chemical and organic pesticide guide of Iran. Rah Dan press, Tehran, Iran, p. 525.
Simmonds, M.S.J., Manlove, J.D., Blaney, W.M. & Khambay, B.P.S. (2002). Effects of selected botanical insecticides on the behaviour and mortality of the glasshouse whitefly Trialeurodes vaporariorum and the parasitoid Encarsia formosa. Entomologia Experimentalis et Applicata, 102(1), 39-47. https://doi.org/10.1046/j.1570-7458.2002.00923.x.
Smilanick, J.M., Zalom, F.G. & Ehler, L.E. (1996). Effect of Methamidophos Residue on the Pentatomid Egg Parasitoids Trissolcus basalis and T. utahensis (Hymenoptera: Scelionidae). Biological Control, 6(2), 193–201.
Sohrabi, F., Shishehbor, P., Saber, M. & Mosaddegh, M.S. (2012). Lethal and sublethal effects of buprofezin and imidacloprid on the whitefly parasitoid Encarsia inaron (Hymenoptera: Aphelinidae). Crop Protection, 32, 83-88.
Sohrabi, F., Shishehbor, P., Saber, M. & Mosaddegh, M.S. (2013). Lethal and sublethal effects of imidacloprid and buprofezin on the sweetpotato whitefly parasitoid Eretmocerus mundus (Hymenoptera: Aphelinidae). Crop Protection, 45, 98–103.
Southwood, T.R.E. & Henderson, P.A. (2009). Ecological methods. John Wiley & Sons.
Stark, J. D., Banks, J. E., & Acheampong, S. (2004). Estimating susceptibility of biological control agents to pesticides: Influence of life history strategies and population structure. Biological Control, 29, 392-398.
Stark, J. D., & Banks, J. E. (2003). Population–level effects of pesticides and other toxicants on arthropods. Annual Review of Entomology, 48 (1), 505–519.
Suh, C.P.C., Orr, D.B. & Van Duyn, J. W. (2000). Effect of insecticides on Trichogramma exiguum (Trichogrammatidae: Hymenoptera) preimaginal development and adult survival. Journal of Economic Entomology, 93(3), 577–583.
Talebi, K., Kavousi, A. & Sabahi, Q. (2008). Impacts of pesticides on arthropod biological control agents. Pest Technology, 2 (2): 87-97.
van Lenteren, J. C., & Martin, N. A. (2000). Biological control of whiteflies, p.202-214. In Albajes R, Gullino M, van Lenteren J C, Elad Y (eds) Integrated pest and disease management in greenhouse crops. Dordrecht, Kluwer Publishers, 568p.
Whalon, M. E., Mota-Sanchez, D., Hollingworth, R. M., & Duynslager, L. (2017). Arthropod pesticide resistance database. Retrieved May 20, 2017, from https://www.pesticideresistance. Com.
Zawrah, M. F. M., Masry, A. T. El., Noha, L., & Saleh, A. A. A. (2020). Efficiacy of certain insecticides against whitefly Bemisia tabaci (Genn.) infesting tomato plants and their associated predators. Plant Archives, 20 (2): 2221-2228.