Flupyradifurone'nun subletal dozlarının Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae)'nin yaşam çizelgesi ve esteraz enzimi üzerine etkisi
Year 2024,
Volume: 48 Issue: 2, 155 - 166, 12.07.2024
Nazlı Gürbüz
,
Gizem Berber Tortop
,
Ali Kemal Birgücü
,
Sibel Yorulmaz
Abstract
Bu çalışmanın amacı, flupyradifurone etken maddesinin iki farklı subletal dozunun (LC10 ve LC30) Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae)’nin yaşam çizelgesi ve esteraz enzimi üzerine etkisini belirlemektir. Denemeler, 2022 yılında Isparta Uygulamalı Bilimler Üniversitesi laboratuvar ve iklim odalarında 1 kontrol+ 2 sublethal doz olacak şekilde yürütülmüştür. Yaşam çizelgesi için kontrol, LC10 ve LC30 dozları sırasıyla 30, 25 ve 30 tekerrür olarak kurulmuştur. Flupyradifurone’nun LC10 konsantrasyonuna maruz kalan M. persicae erginlerinin dişi ömrü ve toplam yaşam süreleri önemli ölçüde kısalmıştır. Günlük ve toplam yavru sayıları hem LC10 hem de LC30 konsantrasyonlarında azalmıştır. Ayrıca yaprakbiti üzerindeki bu olumsuz etkiler daha düşük bir kalıtsal üreme yeteneği (r), net üreme gücü (R0), içsel artış oranı (λ) ve üreme oranları (F) olarak ortaya çıkmıştır. Elde edilen verilere göre, flupyradifurone’nun M. persicae’nin popülasyon büyümesini baskıladığı görülmektedir. Pestisit detoksifikasyonunda rol alan esteraz enzim aktivitesinin flupyradifurone'nun iki farklı subletal dozları uygulanmış ve uygulanmamış (kontrol) popülasyonlarında değişmediği belirlenmiştir. Çalışmanın, flupyradifurone’nun yaprakbiti performansı üzerindeki letal ve subletal etkilerinin anlaşılmasını kolaylaştırdığı düşünülmektedir.
Supporting Institution
TUBITAK (The Scientific and Technological Research Council of Türkiye)
Project Number
2209-A University Students Research Projects Support Programme.
Thanks
This study was financially supported by the TUBITAK (The Scientific and Technological Research Council of Türkiye), 2209-A University Students Research Projects Support Programme.
References
- Akca, I., T. Ayvaz, E. Yazici, C. L. Smith & H. Chi, 2015. Demography and population projection of Aphis fabae (Hemiptera: Aphididae): with additional comments on life table research criteria. Journal of Economic Entomology, 108 (4): 1466-1478.
- Akköprü, E. P., R. Atlıhan, H. Okut & H. Chi, 2015. Demographic assessment of plant cultivar resistance to insect pests: a case study of the dusky-veined walnut aphid (Hemiptera: Callaphididae) on five walnut cultivars. Journal of Economic Entomology, 108 (2): 378-387.
- Barbosa, P. R., J. P. Michaud, C. L. Bain & J. B. Torres, 2017. Toxicity of three aphicides to the generalist predators Chrysoperla carnea (Neuroptera: Chrysopidae) and Orius insidiosus (Hemiptera: Anthocoridae). Ecotoxicology, 26 (5): 589-599.
- Bass, C. & L. M. Field, 2011. Gene amplification and insecticide resistance. Pest Management Science, 67 (8): 886-890.
- Bass, C., A. M. Puinean, C. T. Zimmer, I. Denholm, L. M. Field, S. P. Foster, O. Gutbrod, R. Nauen, R. Slater, M. S. Williamson, 2014. The evolution of insecticide resistance in the peach potato aphid. Myzus persicae. Insect Biochemistry and Molecular Biology, 51: 41-51.
- Biondi, A., V. Mommaerts, G. Smagghe, E. Vinuela, L. Zappalà & N. Desneux, 2012. The non-target impact of spinosyns on beneficial arthropods. Pest Management Science. 68 (12): 1523-1536.
- Blackman, R. L. & V. F. Eastop, 2023. Aphids on the world's plants an online identification and information guide. (Web page: http://www.aphidsonworldsplants.info) (Date accessed: July 2023).
- Bonmatin, J. M., I. Moineau, R. Charvet, M. E. Colin, C. Fleche, & E. R. Bengsch, 2005. “Behaviour of Imidacloprid in Fields: Toxicity for Honey Bees, 483-494”. In: Environmental Chemistry (Eds. E. Lichtfouse, J. Schwarzbauer & D. Robert). Springer, Berlin, Germany, 780 pp.
- Boukhris-Bouhachem, S., I. Ben Fekih, S. Nahdi & R. Souissi, 2017. Capacity assessment of Myzus persicae, Aphis gossypii and Aphis spiraecola (Hemiptera: Aphididae) to acquire and retain PVYNTN in Tunisia. Arthropod-Plant Interactions, 11 (5): 669-674.
- Cai, H., L. Yang, Z. Zuo, W. Liao & Z. Yang, 2021. Resistance status of Myzus persicae to pesticide and its relationship with enzymes. Agronomy Journal, 113 (2): 806-819.
- Calabrese, E. J. & L. A. Baldwin, 2003. Hormesis: the dose-response revolution. Annual Review of Pharmacology and Toxicology, 43 (1): 175-197.
- Chen, X. D., M. Seo & L. L. Stelinski, 2017. Behavioral and hormetic effects of the butenolide insecticide, flupyradifurone, on Asian citrus psyllid, Diaphorina citri. Crop Protection, 98: 102-107.
- Chen, X., K. Ma, F. Li, P. Liang, Y. Liu, T. Guo, D. Song, N. Desneux & X. Gao, 2016. Sublethal and transgenerational effects of sulfoxaflor on the biological traits of the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae). Ecotoxicology, 25: 1841-1848.
- Chi, H., A. Kavousi, G. Gharekhani, R. Atlihan, M. S. Özgökçe, A. Güncan, A. Gökçe, C. L. Smith, G. Benelli, R. N. C. Guedes, M. Amir-Maaf, J. Shirazi, R. Taghizadeh, M. Maroufpoor, Y. Y. Xu, F. Q. Zheng, B. H. Ye, Z. Z. Chen, M. S. You, J. W. Fu, J. Y. Li, M. Z. Shi, Z. Q. Hu, C. Y. Zheng, L. Luo, Z. L. Yuan, L. S. Zang, Y. M. Chen, S. J. Tuan, Y.Y. Lin, H. H. Wang, T. Gotoh, M. S. Ullah, C. Botto-Mahan, S. De Bona, P. Bussaman, R. M. Gabre, P. Saska, M. I. Schneider, F. Ullah & N. Desneux, 2023. Advances in theory, data analysis, and application of the age-stage, two-sex life table for demographic research, biological control, and pest management. Entomologia Generalis, 43 (4): 705-35.
- Chi, H., M. You, R. Atlıhan, C. L. Smith, A. Kavousi, M. S. Özgökçe, A. Güncan, S. J. Tuan, J. W. Fu, Y. Y. Xu, F. Q. Zheng, B. H. Ye, D. Chu, Y. Yu, G. Gharekhani, P. Saska, T. Gotoh, M. I. Schneider, P. Bussaman, A. Gökçe & T. X. Liu, 2020. Age-Stage, two-sex life table: an introduction to theory, data analysis, and application. Entomologia Generalis, 40 (2): 103-124.
- Cohen, E., 2006. Pesticide-mediated homeostatic modulation in arthropods. Pesticide Biochemistry and Physiology, 85 (1): 21-27.
- Colares, F., J. P. Michaud, C. L. Bain & J. B. Torres, 2017. Relative toxicity of two aphicides to Hippodamia convergens (Coleoptera: Coccinellidae): implications for integrated management of sugarcane aphid, Melanaphis sacchari (Hemiptera: Aphididae). Journal of Economic Entomology, 110 (1): 52-58.
- De França, S. M., M. O. Breda, D. R. Barbosa, A. M. Araujo & C. A. Guedes, 2017. “The Sublethal Effects of Insecticides in Insects, 23-29”. In: Biological Control of Pest and Vector Insects (Eds. V. D. C. Shields). BoD-Books on Demand, London, UK, 360 pp.
- Desneux, N., A. Decourtye & J. M. Delpuech, 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52: 81-106.
- Desneux, N., X. Fauvergue, F. X. Dechaume-Moncharmont, L. Kerhoas, Y. Ballanger & L. Kaiser, 2005. Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. Journal of Economic Entomology, 98 (1): 9-17.
- Devine, G. J., Z. K. Harling, A. W. Scarr & A. L. Devonshire, 1996. Lethal and sublethal effects of imidacloprid on nicotine-tolerant Myzus nicotianae and Myzus persicae. Pesticide Science, 48 (1): 57-62.
- Devonshire, A. L., 1975. Studies of the acetylcholinesterase from houseflies (Musca domestica L.) resistant and susceptible to organophosphorus insecticides. Biochemical Journal, 149 (2): 463-469.
- Devonshire, A. L., G. J. Devine & G. D. Moores, 1992. Comparison of microplate esterase assays and immunoassay for identifying insecticide resistant variants of Myzus persicae (Homoptera: Aphididae). Bulletin of Entomological Research, 82 (4): 459-463.
- Efron, B & R. Tibshirani, 1993. An Introduction to the Bootstrap. CRC Press, New York, 914 pp.
- Erol, A. B., Ş. Arzuman, İ. Özdemir & İ. Karaca, 2018. Aphid species (Hemiptera: Aphididae) determined on the campus of Isparta province, Turkey. Süleyman Demirel University Journal of Natural and Applied Sciences, 22 (2): 1045-1053.
- Field, L. M., A. L. Devonshire & B. G. Forde, 1988. Molecular evidence that insecticide resistance in peach-potato aphids (Myzus persicae Sulz.) results from amplification of an esterase gene. Biochemical Journal, 251 (1): 309-312.
- Foster, S. P., I. Denholm & A. L. Devonshire, 2000. The ups and downs of insecticide resistance in peach-potato aphids (Myzus persicae) in the UK. Crop Protection, 19 (8-10): 873-879.
- Fouad, E. A., S. A. El-Sherif & E. S. M. Mokbel, 2022. Flupyradifurone induces transgenerational hormesis effects in the cowpea aphid, Aphis craccivora. Ecotoxicology, 31 (6): 909-918.
- Gao, X. W., B. Z. Zheng & B. J. Cao, 1992. Reisitance in Myzus persicae to organophosohorus and carbamate insecticides in China. Journal of Plant Protection, 19 (4): 365-371
- Guo, L., N. Desneux, S. Sonoda, P. Liang, P. Han & X. W. Gao, 2013. Sublethal and transgenerational effects of chlorantraniliprole on biological traits of the diamondback moth, Plutella xylostella L. Crop Protection, 48: 29-34.
- Han, W., S. Zhang, F. Shen, M. Liu, C. Ren & X. Gao, 2012. Residual toxicity and sublethal effects of chlorantraniliprole on Plutella xylostella (Lepidoptera: Plutellidae). Pest Management Science, 68 (8): 1184-1190.
- He, Y. X., J. W. Zhao, Y. Zheng, Q. Y. Weng, A. Biondi, N. Desneux & K. M. Wu, 2013. Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. International Journal of Biological Sciences, 9 (3): 246-255.
- Hosseini, S., H. Abbasipour, A. Askarianzadeh & A. Noroozi, 2020. Sublethal effects of flupyradifurone insecticide on the life table parameters of the mustard aphid, Lipaphis erysimi (Kalt). Plant Pests Research, 10 (1): 55-68.
- Huang, Y. B. & H. Chi, 2012. Assessing the application of the jackknife and bootstrap techniques to the estimation of the variability of the net reproductive rate and gross reproductive rate: a case study in Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). Journal of Agriculture & Forestry, 61 (1): 37-45.
- Jeschke, P., R. Nauen, O. Gutbrod, M. E. Beck, S. Matthiesen, M. Haas & R. Velten, 2015. Flupyradifurone (SivantoTM) and its novel butenolide pharmacophore: Structural considerations. Pesticide Biochemistry and Physiology, 121: 31-38.
- Joseph, S. V. & M. Bolda, 2016. Efficacy of insecticides against Lygus hesperus Knight (Hemiptera: Miridae) in the California’s Central Coast strawberry. International Journal of Fruit Science, 16 (sup1): 178-187.
- Lashkari, M. R., A. Sahragard & M. Ghadamyari, 2007. Sublethal effects of imidacloprid and pymetrozine on population growth parameters of cabbage aphid, Brevicoryne brassicae on rapeseed, Brassica napus L. Insect Science, 14 (3): 207-212.
- Lee, C. Y., 2000. Sublethal effects of insecticides on longevity, fecundity and behaviour of insect pests: a review. Journal of Bioscience, 11 (1): 107-112.
- LeOra Software, 1994. Polo-PC: Probit and Logit Analysis. Berkeley, CA: LeOra Software.
- Liang, P. Z., K. S. Ma, X. W. Chen, C. Y. Tang, J. Xia, H. Chi & X. W. Gao, 2019. Toxicity and sublethal effects of flupyradifurone, a novel butenolide insecticide, on the development and fecundity of Aphis gossypii (Hemiptera: Aphididae). Journal of Economic Entomology, 112 (2): 852-858.
- Liu, X., Z. Fu, Y. Zhu, X. Gao, T.-X. Liu & P. Liang, 2022. Sublethal and transgenerational effects of afidopyropen on biological traits of the green peach aphid Myzus persicae (Sluzer). Pesticide Biochemistry and Physiology, 180: 104981 (1-8).
- Liu, Y., Y. Lu, K. Wu, K. A. Wyckhuys & F. Xue, 2008. Lethal and sublethal effects of endosulfan on Apolygus lucorum (Hemiptera: Miridae). Journal of Economic Entomology, 101 (6): 1805-1810.
- Lodos, N., 1986. Entomology of Türkiye II: General Applied and Faunistic. Ege University Faculty of Agriculture Publications, No: 429, İzmir, 580 pp (in Turkish).
- Luckey, T. D., 1968. Insecticide hormoligosis. Journal of Economic Entomology, 61 (1): 7-12.
- Montella, I. R., R. Schama & D. Valle, 2012. The classification of esterases: an important gene family involved in insecticide resistance-A review. Memorias do Instituto Oswaldo Cruz, 107 (4): 437-449.
- Nauen, R., P. Jeschke, R. Velten, M. E. Beck, U. Ebbinghaus-Kintscher, W. Thielert, K. Wölfel, M. Haas, K. Kunz & G. Raupach, 2015. Flupyradifurone: a brief profile of a new butenolide insecticide. Pest Management Science, 71 (6): 850-862.
- Şenol, Ö., H. A. Beğen, G. Görür & E. Demirtaş, 2015. New additions and invasive aphids for Turkey’s aphidofauna (Hemiptera: Aphidoidea). Turkish Journal of Zoology, 39 (1): 39-45.
- Sial, M. U., Z. Zhao, L. Zhang, Y. Zhang, L. Mao & H. Jiang, 2018. Evaluation of Insecticides induced hormesis on the demographic parameters of Myzus persicae and expression changes of metabolic resistance detoxification genes. Scientific Reports, 8 (1): 16601.
- Smith, H. A. & M. C. Giurcanu, 2013. Residual effects of new insecticides on egg and nymph densities of Bemisia tabaci (Hemiptera: Aleyrodidae). Florida Entomologist, 96 (2): 504-511.
- Sohrabi, F., P. Shishehbor, M. Saber & M. S. Mosaddegh, 2011. Lethal and sublethal effects of buprofezin and imidacloprid on Bemisia tabaci (Hemiptera: Aleyrodidae). Crop Protection, 30 (9): 1190-1195.
- Song, S. S., H. K. Oh & N. Motoyama, 1995. Insecticide resistance mechanism in the spiraea aphid, Aphis citricola (van der Goot). Korean Journal Applied Entomology, 34 (2): 89-94.
- Tan, Y., A. Biondi, N. Desneux & X. W. Gao, 2012. Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-Dür). Ecotoxicology, 21: 1989-1997.
- Tang, Q., K. Ma, H. Chi, Y. Hou & X. Gao, 2019. Transgenerational hormetic effects of sublethal dose of flupyradifurone on the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). PloS One, 14 (1): e0208058.
- Tukey, J. W., 1949. Comparing individual means in the analysis of variance. Biometrics, 5 (2): 99-114.
- van Emden, H. F., 2007. “Integrated Pest Management and Introduction to IPM Case Studies, 537-548”. In: Aphids as Crop Pests (Eds. H.F. van Emden & R. Harrington). CABI: Wallingford, UK, 717 pp.
- Wang, X. Y., Z. Q. Yang, Z. R. Shen, J. Lu & W. B. Xu, 2008. Sublethal effects of selected insecticides on fecundity and wing dimorphism of green peach aphid (Hom., Aphididae). Journal of applied entomology, 132 (2): 135-142.
- Wei M., H. Chi, Y. Guo, X. Li, L. Zhao & R. Ma, 2020. Demography of Cacopsylla chinensis (Hemiptera: Psyllidae) reared on four cultivars of Pyrus bretschneideri (Rosales: Rosaceae) and P. communis pears with estimations of confidence intervals of specific life table statistics. Journal of Economic Entomology, 113 (5): 2343-2353.
- Wei, X., Y. Pan, X. Xin, C. Zheng, X. Gao, J. Xi & Q. Shang, 2017. Cross-resistance pattern and basis of resistance in a thiamethoxam-resistant strain of Aphis gossypii Glover. Pesticide Biochemistry and Physiology, 138: 91-96.
- Zeng, X., Y. He, J. Wu, Y. Tang, J. Gu, W. Ding & Y. Zhang, 2016. Sublethal effects of cyantraniliprole and imidacloprid on feeding behavior and life table parameters of Myzus persicae (Hemiptera: Aphididae). Journal of Economic Entomology, 109 (4): 1595-1602.
The effect of sublethal doses of flupyradifurone on the life table and esterase enzyme of Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae)
Year 2024,
Volume: 48 Issue: 2, 155 - 166, 12.07.2024
Nazlı Gürbüz
,
Gizem Berber Tortop
,
Ali Kemal Birgücü
,
Sibel Yorulmaz
Abstract
The aim of this study was to determine the effect of two different sublethal doses (LC10 and LC30) of flupyradifurone on the life table and esterase enzyme of Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae). The experiments were conducted in 2022 in Isparta University of Applied Sciences laboratory and climate rooms in 2022 as 1 control + 2 sublethal doses. For the life table, control, LC10 and LC30 doses were established as 30, 25 and 30 replications, respectively. Female and total lifespan of M. persicae adults exposed to LC10 concentrations of flupyradifurone were significantly shortened. Daily and total numbers of the offsprings decreased at both LC10 and LC30 concentrations. Furthermore, these negative effects on the aphid were revealed as a lower intrinsic rate of increase (r), net reproductive rate (R0), finite rate of increase (λ) and fecundity (F). Based on the obtained data, flupyradifurone seems to suppress the population growth of M. persicae. It was determined that esterase enzyme activity involved in pesticide detoxification did not change in populations exposed to two different sublethal doses of flupyradifurone and unexposed (control). It is thought that this study facilitates the understanding of the lethal and sublethal effects of flupyradifurone on aphid performance.
Supporting Institution
TUBITAK (The Scientific and Technological Research Council of Türkiye)
Project Number
2209-A University Students Research Projects Support Programme.
Thanks
This study was financially supported by the TUBITAK (The Scientific and Technological Research Council of Türkiye), 2209-A University Students Research Projects Support Programme.
References
- Akca, I., T. Ayvaz, E. Yazici, C. L. Smith & H. Chi, 2015. Demography and population projection of Aphis fabae (Hemiptera: Aphididae): with additional comments on life table research criteria. Journal of Economic Entomology, 108 (4): 1466-1478.
- Akköprü, E. P., R. Atlıhan, H. Okut & H. Chi, 2015. Demographic assessment of plant cultivar resistance to insect pests: a case study of the dusky-veined walnut aphid (Hemiptera: Callaphididae) on five walnut cultivars. Journal of Economic Entomology, 108 (2): 378-387.
- Barbosa, P. R., J. P. Michaud, C. L. Bain & J. B. Torres, 2017. Toxicity of three aphicides to the generalist predators Chrysoperla carnea (Neuroptera: Chrysopidae) and Orius insidiosus (Hemiptera: Anthocoridae). Ecotoxicology, 26 (5): 589-599.
- Bass, C. & L. M. Field, 2011. Gene amplification and insecticide resistance. Pest Management Science, 67 (8): 886-890.
- Bass, C., A. M. Puinean, C. T. Zimmer, I. Denholm, L. M. Field, S. P. Foster, O. Gutbrod, R. Nauen, R. Slater, M. S. Williamson, 2014. The evolution of insecticide resistance in the peach potato aphid. Myzus persicae. Insect Biochemistry and Molecular Biology, 51: 41-51.
- Biondi, A., V. Mommaerts, G. Smagghe, E. Vinuela, L. Zappalà & N. Desneux, 2012. The non-target impact of spinosyns on beneficial arthropods. Pest Management Science. 68 (12): 1523-1536.
- Blackman, R. L. & V. F. Eastop, 2023. Aphids on the world's plants an online identification and information guide. (Web page: http://www.aphidsonworldsplants.info) (Date accessed: July 2023).
- Bonmatin, J. M., I. Moineau, R. Charvet, M. E. Colin, C. Fleche, & E. R. Bengsch, 2005. “Behaviour of Imidacloprid in Fields: Toxicity for Honey Bees, 483-494”. In: Environmental Chemistry (Eds. E. Lichtfouse, J. Schwarzbauer & D. Robert). Springer, Berlin, Germany, 780 pp.
- Boukhris-Bouhachem, S., I. Ben Fekih, S. Nahdi & R. Souissi, 2017. Capacity assessment of Myzus persicae, Aphis gossypii and Aphis spiraecola (Hemiptera: Aphididae) to acquire and retain PVYNTN in Tunisia. Arthropod-Plant Interactions, 11 (5): 669-674.
- Cai, H., L. Yang, Z. Zuo, W. Liao & Z. Yang, 2021. Resistance status of Myzus persicae to pesticide and its relationship with enzymes. Agronomy Journal, 113 (2): 806-819.
- Calabrese, E. J. & L. A. Baldwin, 2003. Hormesis: the dose-response revolution. Annual Review of Pharmacology and Toxicology, 43 (1): 175-197.
- Chen, X. D., M. Seo & L. L. Stelinski, 2017. Behavioral and hormetic effects of the butenolide insecticide, flupyradifurone, on Asian citrus psyllid, Diaphorina citri. Crop Protection, 98: 102-107.
- Chen, X., K. Ma, F. Li, P. Liang, Y. Liu, T. Guo, D. Song, N. Desneux & X. Gao, 2016. Sublethal and transgenerational effects of sulfoxaflor on the biological traits of the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae). Ecotoxicology, 25: 1841-1848.
- Chi, H., A. Kavousi, G. Gharekhani, R. Atlihan, M. S. Özgökçe, A. Güncan, A. Gökçe, C. L. Smith, G. Benelli, R. N. C. Guedes, M. Amir-Maaf, J. Shirazi, R. Taghizadeh, M. Maroufpoor, Y. Y. Xu, F. Q. Zheng, B. H. Ye, Z. Z. Chen, M. S. You, J. W. Fu, J. Y. Li, M. Z. Shi, Z. Q. Hu, C. Y. Zheng, L. Luo, Z. L. Yuan, L. S. Zang, Y. M. Chen, S. J. Tuan, Y.Y. Lin, H. H. Wang, T. Gotoh, M. S. Ullah, C. Botto-Mahan, S. De Bona, P. Bussaman, R. M. Gabre, P. Saska, M. I. Schneider, F. Ullah & N. Desneux, 2023. Advances in theory, data analysis, and application of the age-stage, two-sex life table for demographic research, biological control, and pest management. Entomologia Generalis, 43 (4): 705-35.
- Chi, H., M. You, R. Atlıhan, C. L. Smith, A. Kavousi, M. S. Özgökçe, A. Güncan, S. J. Tuan, J. W. Fu, Y. Y. Xu, F. Q. Zheng, B. H. Ye, D. Chu, Y. Yu, G. Gharekhani, P. Saska, T. Gotoh, M. I. Schneider, P. Bussaman, A. Gökçe & T. X. Liu, 2020. Age-Stage, two-sex life table: an introduction to theory, data analysis, and application. Entomologia Generalis, 40 (2): 103-124.
- Cohen, E., 2006. Pesticide-mediated homeostatic modulation in arthropods. Pesticide Biochemistry and Physiology, 85 (1): 21-27.
- Colares, F., J. P. Michaud, C. L. Bain & J. B. Torres, 2017. Relative toxicity of two aphicides to Hippodamia convergens (Coleoptera: Coccinellidae): implications for integrated management of sugarcane aphid, Melanaphis sacchari (Hemiptera: Aphididae). Journal of Economic Entomology, 110 (1): 52-58.
- De França, S. M., M. O. Breda, D. R. Barbosa, A. M. Araujo & C. A. Guedes, 2017. “The Sublethal Effects of Insecticides in Insects, 23-29”. In: Biological Control of Pest and Vector Insects (Eds. V. D. C. Shields). BoD-Books on Demand, London, UK, 360 pp.
- Desneux, N., A. Decourtye & J. M. Delpuech, 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52: 81-106.
- Desneux, N., X. Fauvergue, F. X. Dechaume-Moncharmont, L. Kerhoas, Y. Ballanger & L. Kaiser, 2005. Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. Journal of Economic Entomology, 98 (1): 9-17.
- Devine, G. J., Z. K. Harling, A. W. Scarr & A. L. Devonshire, 1996. Lethal and sublethal effects of imidacloprid on nicotine-tolerant Myzus nicotianae and Myzus persicae. Pesticide Science, 48 (1): 57-62.
- Devonshire, A. L., 1975. Studies of the acetylcholinesterase from houseflies (Musca domestica L.) resistant and susceptible to organophosphorus insecticides. Biochemical Journal, 149 (2): 463-469.
- Devonshire, A. L., G. J. Devine & G. D. Moores, 1992. Comparison of microplate esterase assays and immunoassay for identifying insecticide resistant variants of Myzus persicae (Homoptera: Aphididae). Bulletin of Entomological Research, 82 (4): 459-463.
- Efron, B & R. Tibshirani, 1993. An Introduction to the Bootstrap. CRC Press, New York, 914 pp.
- Erol, A. B., Ş. Arzuman, İ. Özdemir & İ. Karaca, 2018. Aphid species (Hemiptera: Aphididae) determined on the campus of Isparta province, Turkey. Süleyman Demirel University Journal of Natural and Applied Sciences, 22 (2): 1045-1053.
- Field, L. M., A. L. Devonshire & B. G. Forde, 1988. Molecular evidence that insecticide resistance in peach-potato aphids (Myzus persicae Sulz.) results from amplification of an esterase gene. Biochemical Journal, 251 (1): 309-312.
- Foster, S. P., I. Denholm & A. L. Devonshire, 2000. The ups and downs of insecticide resistance in peach-potato aphids (Myzus persicae) in the UK. Crop Protection, 19 (8-10): 873-879.
- Fouad, E. A., S. A. El-Sherif & E. S. M. Mokbel, 2022. Flupyradifurone induces transgenerational hormesis effects in the cowpea aphid, Aphis craccivora. Ecotoxicology, 31 (6): 909-918.
- Gao, X. W., B. Z. Zheng & B. J. Cao, 1992. Reisitance in Myzus persicae to organophosohorus and carbamate insecticides in China. Journal of Plant Protection, 19 (4): 365-371
- Guo, L., N. Desneux, S. Sonoda, P. Liang, P. Han & X. W. Gao, 2013. Sublethal and transgenerational effects of chlorantraniliprole on biological traits of the diamondback moth, Plutella xylostella L. Crop Protection, 48: 29-34.
- Han, W., S. Zhang, F. Shen, M. Liu, C. Ren & X. Gao, 2012. Residual toxicity and sublethal effects of chlorantraniliprole on Plutella xylostella (Lepidoptera: Plutellidae). Pest Management Science, 68 (8): 1184-1190.
- He, Y. X., J. W. Zhao, Y. Zheng, Q. Y. Weng, A. Biondi, N. Desneux & K. M. Wu, 2013. Assessment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. International Journal of Biological Sciences, 9 (3): 246-255.
- Hosseini, S., H. Abbasipour, A. Askarianzadeh & A. Noroozi, 2020. Sublethal effects of flupyradifurone insecticide on the life table parameters of the mustard aphid, Lipaphis erysimi (Kalt). Plant Pests Research, 10 (1): 55-68.
- Huang, Y. B. & H. Chi, 2012. Assessing the application of the jackknife and bootstrap techniques to the estimation of the variability of the net reproductive rate and gross reproductive rate: a case study in Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). Journal of Agriculture & Forestry, 61 (1): 37-45.
- Jeschke, P., R. Nauen, O. Gutbrod, M. E. Beck, S. Matthiesen, M. Haas & R. Velten, 2015. Flupyradifurone (SivantoTM) and its novel butenolide pharmacophore: Structural considerations. Pesticide Biochemistry and Physiology, 121: 31-38.
- Joseph, S. V. & M. Bolda, 2016. Efficacy of insecticides against Lygus hesperus Knight (Hemiptera: Miridae) in the California’s Central Coast strawberry. International Journal of Fruit Science, 16 (sup1): 178-187.
- Lashkari, M. R., A. Sahragard & M. Ghadamyari, 2007. Sublethal effects of imidacloprid and pymetrozine on population growth parameters of cabbage aphid, Brevicoryne brassicae on rapeseed, Brassica napus L. Insect Science, 14 (3): 207-212.
- Lee, C. Y., 2000. Sublethal effects of insecticides on longevity, fecundity and behaviour of insect pests: a review. Journal of Bioscience, 11 (1): 107-112.
- LeOra Software, 1994. Polo-PC: Probit and Logit Analysis. Berkeley, CA: LeOra Software.
- Liang, P. Z., K. S. Ma, X. W. Chen, C. Y. Tang, J. Xia, H. Chi & X. W. Gao, 2019. Toxicity and sublethal effects of flupyradifurone, a novel butenolide insecticide, on the development and fecundity of Aphis gossypii (Hemiptera: Aphididae). Journal of Economic Entomology, 112 (2): 852-858.
- Liu, X., Z. Fu, Y. Zhu, X. Gao, T.-X. Liu & P. Liang, 2022. Sublethal and transgenerational effects of afidopyropen on biological traits of the green peach aphid Myzus persicae (Sluzer). Pesticide Biochemistry and Physiology, 180: 104981 (1-8).
- Liu, Y., Y. Lu, K. Wu, K. A. Wyckhuys & F. Xue, 2008. Lethal and sublethal effects of endosulfan on Apolygus lucorum (Hemiptera: Miridae). Journal of Economic Entomology, 101 (6): 1805-1810.
- Lodos, N., 1986. Entomology of Türkiye II: General Applied and Faunistic. Ege University Faculty of Agriculture Publications, No: 429, İzmir, 580 pp (in Turkish).
- Luckey, T. D., 1968. Insecticide hormoligosis. Journal of Economic Entomology, 61 (1): 7-12.
- Montella, I. R., R. Schama & D. Valle, 2012. The classification of esterases: an important gene family involved in insecticide resistance-A review. Memorias do Instituto Oswaldo Cruz, 107 (4): 437-449.
- Nauen, R., P. Jeschke, R. Velten, M. E. Beck, U. Ebbinghaus-Kintscher, W. Thielert, K. Wölfel, M. Haas, K. Kunz & G. Raupach, 2015. Flupyradifurone: a brief profile of a new butenolide insecticide. Pest Management Science, 71 (6): 850-862.
- Şenol, Ö., H. A. Beğen, G. Görür & E. Demirtaş, 2015. New additions and invasive aphids for Turkey’s aphidofauna (Hemiptera: Aphidoidea). Turkish Journal of Zoology, 39 (1): 39-45.
- Sial, M. U., Z. Zhao, L. Zhang, Y. Zhang, L. Mao & H. Jiang, 2018. Evaluation of Insecticides induced hormesis on the demographic parameters of Myzus persicae and expression changes of metabolic resistance detoxification genes. Scientific Reports, 8 (1): 16601.
- Smith, H. A. & M. C. Giurcanu, 2013. Residual effects of new insecticides on egg and nymph densities of Bemisia tabaci (Hemiptera: Aleyrodidae). Florida Entomologist, 96 (2): 504-511.
- Sohrabi, F., P. Shishehbor, M. Saber & M. S. Mosaddegh, 2011. Lethal and sublethal effects of buprofezin and imidacloprid on Bemisia tabaci (Hemiptera: Aleyrodidae). Crop Protection, 30 (9): 1190-1195.
- Song, S. S., H. K. Oh & N. Motoyama, 1995. Insecticide resistance mechanism in the spiraea aphid, Aphis citricola (van der Goot). Korean Journal Applied Entomology, 34 (2): 89-94.
- Tan, Y., A. Biondi, N. Desneux & X. W. Gao, 2012. Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-Dür). Ecotoxicology, 21: 1989-1997.
- Tang, Q., K. Ma, H. Chi, Y. Hou & X. Gao, 2019. Transgenerational hormetic effects of sublethal dose of flupyradifurone on the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). PloS One, 14 (1): e0208058.
- Tukey, J. W., 1949. Comparing individual means in the analysis of variance. Biometrics, 5 (2): 99-114.
- van Emden, H. F., 2007. “Integrated Pest Management and Introduction to IPM Case Studies, 537-548”. In: Aphids as Crop Pests (Eds. H.F. van Emden & R. Harrington). CABI: Wallingford, UK, 717 pp.
- Wang, X. Y., Z. Q. Yang, Z. R. Shen, J. Lu & W. B. Xu, 2008. Sublethal effects of selected insecticides on fecundity and wing dimorphism of green peach aphid (Hom., Aphididae). Journal of applied entomology, 132 (2): 135-142.
- Wei M., H. Chi, Y. Guo, X. Li, L. Zhao & R. Ma, 2020. Demography of Cacopsylla chinensis (Hemiptera: Psyllidae) reared on four cultivars of Pyrus bretschneideri (Rosales: Rosaceae) and P. communis pears with estimations of confidence intervals of specific life table statistics. Journal of Economic Entomology, 113 (5): 2343-2353.
- Wei, X., Y. Pan, X. Xin, C. Zheng, X. Gao, J. Xi & Q. Shang, 2017. Cross-resistance pattern and basis of resistance in a thiamethoxam-resistant strain of Aphis gossypii Glover. Pesticide Biochemistry and Physiology, 138: 91-96.
- Zeng, X., Y. He, J. Wu, Y. Tang, J. Gu, W. Ding & Y. Zhang, 2016. Sublethal effects of cyantraniliprole and imidacloprid on feeding behavior and life table parameters of Myzus persicae (Hemiptera: Aphididae). Journal of Economic Entomology, 109 (4): 1595-1602.