Feeding behavior and hormoligosis associated with imidacloprid resistance in Asian citrus psyllid,Diaphorina citri

Xue Dong Chen , Justin George , Lauren M. Diepenbrock , Hunter Gossett , Guoping Liu , Jawwad A. Qureshi , Lukasz L. Stelinski

Insect Science ›› 2024, Vol. 31 ›› Issue (4) : 1211 -1221.

PDF
Insect Science ›› 2024, Vol. 31 ›› Issue (4) : 1211 -1221. DOI: 10.1002/1744-7917.13293
ORIGINAL ARTICLE

Feeding behavior and hormoligosis associated with imidacloprid resistance in Asian citrus psyllid,Diaphorina citri

Author information +
History +
PDF

Abstract

Imidacloprid is a neonicotinoid insecticide used for managing the Asian citrus psyllid,Diaphorina citri Kuwayama, which serves as vector of phytopathogens causing citrus greening. However, development of resistance to neonicotinoids among populations of D. citri has coincided with occasional control failures in the field. The objectives of this research were to (1) survey current levels of imidacloprid resistance in Florida citrus; (2) compare feeding behavior between imidacloprid-resistant and susceptible D. citri using electrical penetration graph recordings, and (3) investigate the possible amplification of insecticide hormoligosis associated with resistance. Field surveys confirmed that the susceptibility of D. citri populations to imidacloprid has decreased in commercial Florida citrus groves compared with a laboratory-susceptible population. Following 12 generations of selection, resistance to imidacloprid increased by 438 fold compared with the susceptible strain. Imidacloprid-susceptible D. citri feeding on citrus exhibited significantly more bouts associated with intercellular pathway (C), phloem penetration (D), phloem salivation (E1), and nonprobing (Np) activities than imidacloprid-resistant counterparts. However, there were no differences observed in the frequency or duration of phloem ingestion or xylem feeding between susceptible and resistant D. citri. There was no statistical difference in fecundity between resistant and susceptible strains. However, the fecundity of imidacloprid-susceptible female D. citri treated with a sublethal concentration of imidacloprid (LC25) increased significantly compared with controls, while such hormoligosis was less pronounced among imidacloprid-resistant psyllids. Our results suggest that imidacloprid-resistant psyllids may cease feeding sooner than susceptible counterparts following sublethal exposure to this insecticide, indicative of a behavioral resistance mechanism.

Keywords

artificial selection / electrical penetration graph / feeding behavior / hormoligosis / insecticide resistance / sublethal exposure

Cite this article

Download citation ▾
Xue Dong Chen, Justin George, Lauren M. Diepenbrock, Hunter Gossett, Guoping Liu, Jawwad A. Qureshi, Lukasz L. Stelinski. Feeding behavior and hormoligosis associated with imidacloprid resistance in Asian citrus psyllid,Diaphorina citri. Insect Science, 2024, 31(4): 1211-1221 DOI:10.1002/1744-7917.13293

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Abbott, W.S. (1925) A method for computing the effectiveness of an insecticide. Journal of Economic Entomology,18,265–267.

[2]

Afzal, M.B.S.,Shad, S.A.,Abbas, N.,Ayyaz, M. and Walker, W.B. (2015) Cross-resistance, the stability of acetamiprid resistance and its effect on the biological parameters of cotton mealybug,Phenacoccus solenopsis (Homoptera: Pseudococcidae), in Pakistan. Pest Management Science,71,151–158.

[3]

Backus, E.A.,Cervantes, F.A.,Guedes, R.N.C.,Li, A.Y. and Wayadande, A.C. (2019) AC–DC electropenetrography for in-depth studies of feeding and oviposition behaviors. Annals of Entomological Society of America,112,236–248.

[4]

Backus, E.A.,Cline, A.R.,Ellerseick, M.R. and Serrano, M.S. (2007) Behaviour: Lygus hesperus (Hemiptera: Miridae) feeding on cotton: new methods and parameters for analysis of nonsequential electrical penetration graph data. Annals of Entomological Society of America,100,296–310.

[5]

Boina, D.R. and Bloomquist, J.R. (2015) Chemical control of the Asian citrus psyllid and of huanglongbing disease in citrus. Pest Management Science,71,808–823.

[6]

Boina, D.R.,Onagbola, E.O.,Salyani, M. and Stelinski, L.L. (2009) Antifeedant and sublethal effects of imidacloprid on Asian citrus psyllid,Diaphorina citri. Pest Management Science,65,870–877.

[7]

Boina, D.R.,Rogers, M.E.,Wang, N. and Stelinski, L.L. (2010) Effect of pyriproxyfen, a juvenile hormone mimic, on egg hatch, nymph development, adult emergence and reproduction of the Asian citrus psyllid,Diaphorina citri Kuwayama. Pest Management Science,66,349–357.

[8]

Bonani, J.P.,Fereres, A.,Garzo, E.,Miranda, M.P.,Appezzato-Da-Gloria, B. and Lopes, J.R.S. (2010) Characterization of electrical penetration graphs of the Asian citrus psyllid,Diaphorina citri, in sweet orange seedlings. Entomologia Experimentalis et Applicata,134,35–49.

[9]

Bove, J.M. (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology,88,7–37.

[10]

Chen, X.D.,Ebert, T.A.,Pelz-Stelinski, K.S. and Stelinski, L.L. (2020) Fitness costs associated with thiamethoxam and imidacloprid resistance in three field populations of Diaphorina citri (Hemiptera: Liviidae) from Florida. Bulletin of Entomological Research,110,512–520.

[11]

Chen, X.D.,Gill, T.A.,Ashfaq, M.,Pelz-Stelinski, K.S. and Stelinski, L.L. (2018) Resistance to commonly used insecticides in Asian citrus psyllid: stability and relationship to gene expression. Journal of Applied Entomology,142,967–977.

[12]

Chen, X.D.,Neupane, S.,Gossett, H.,Pelz-Stelinski, K.S. and Stelinski, L.L. (2021) Insecticide rotation scheme restores insecticide susceptibility in thiamethoxam-resistant field populations of Asian citrus psyllid,Diaphorina citri Kuwayama (Hemiptera: Liviidae), in Florida. Pest Management Science,77,464–473.

[13]

Chen, X.D.,Qureshi, J.A. and Stelinski, L.L. (2022a) Monitoring of Diaphorina citri populations from Florida reveals reduced susceptibility to cyantraniliprole and thiamethoxam. Journal of Applied Entomology,6,725–733.

[14]

Chen, X.D.,Seo, M. and Stelinski, L.L. (2017) Behavioral and hormetic effects of the butenolide insecticide, flupyradifurone, on Asian citrus psyllid,Diaphorina citri. Crop Protection,98,102–107.

[15]

Chen, X.D.,Stockton, D.,Gossett, H.,Qureshi, J.A.,Ibanez, F.,Pelz-Stelinski, K.S. et al. (2022b) Comparisons of economic thresholds for Asian citrus psyllid management suggest a revised approach to reduce management costs and improve yield. Frontiers in Sustainable Food Systems,6,948278.

[16]

Civolani, S.,Cassanelli, S.,Chicca, M.,Rison, J.L.,Bassi, A.,Alvarez, J.M. et al. (2014) An EPG study of the probing behavior of adult Bemisia tabaci biotype Q (Hemiptera: Aleyrodidae) following exposure to cyantraniliprole. Journal of Economic Entomology,107,910–919.

[17]

Costa, R.R.,Moraes, J.C. and DaCosta, R.R. (2011) Feeding behaviour of the greenbug Schizaphis graminum on wheat plants treated with imidacloprid and/or silicon. Journal of Applied Entomology,135,115–120.

[18]

Cui, L.,Sun, L.,Shao, X.,Cao, Y.,Yang, D.,Li, Z. and Yuan, H. (2010). Systemic action of novel neonicotinoid insecticide IPP-10 and its effect on the feeding behaviour of Rhopalosiphum padi on wheat. Pest Management Science,66,779–785.

[19]

Curtin, T.J. and Jones, J.C. (1961). The mechanism of ovulation and oviposition in Aedes aegypti. Annals of the Entomological Society of America,54,298–313.

[20]

Cutler, G.C. (2013) Insects, insecticides and hormesis: evidence and considerations for study. Dose-Response,11,154–177.

[21]

Desneux, N.,Decourtye, A. and Delpuech, J.M. (2007) The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology,52,81–106.

[22]

Dittrich, V.,Streibert, P. and Bathe, P.A. (1974). An old case reopended: mite stimulation by insecticide residues. Environmental Entomology,3,534–540.

[23]

Ebert, T.A.,Backus, E.A.,Shugart, H.J. and Rogers, M.E. (2018) Behavioral plasticity in probing by Diaphorina citri (Hemiptera, Liviidae): ingestion from phloem versus xylem is influenced by leaf age and surface. Journal of Insect Behavior,31,119–137.

[24]

Fujiwara, Y.,Takahashi, T.,Yoshioka, T. and Nakasuji, F. (2002) Changes in egg size of the diamondback moth Plutella xylostella (Lepidoptera: Yponomeutidae) treated with fenvalerate at sublethal doses and viability of the eggs. Applied Entomology and Zoology,37,103–109.

[25]

George, J.,Ammar, E.D.,Hall, D.G. and Lapointe, S.L. (2017) Sclerenchymatous ring as a barrier to phloem feeding by Asian citrus psyllid: evidence from electrical penetration graph and visualization of stylet pathways. PLoS ONE,12,e0173520.

[26]

George, J.,Kanissery, R.,Ammar, E.D.,Cabral, I.,Markle, L.T.,Patt, J.M. et al. (2020) Feeding behavior of Asian citrus psyllid [Diaphorina citri (Hemiptera: Liviidae)] nymphs and adults on common weeds occurring in cultivated citrus described using electrical penetration graph recordings. Insects,11,48.

[27]

George, J.,Shi, Q.,Stelinski, L.L.,Stover, E. and Lapointe, S.L. (2019) Host selection, oviposition and feeding by a phytopathogen vector,Diaphorina citri (Hemiptera: Liviidae), modulated by plant exposure to formic acid. Frontiers in Ecology and Evolution,7,78.

[28]

Grafton-Cardwell, E.E.,Stelinski, L.L. and Stansly, P.A. (2013) Biology and management of Asian citrus psyllid, vector of the huanglongbing pathogens. Annual Review of Entomology,58,413–432.

[29]

Hamilton, R. and Schal, C. (1990). Sublethal effects of chlorpyrifos-methyl on reproduction in female German Cockroaches (Dictyoptera: Blattellidae). Journal of Economic Entomology,83,441–443.

[30]

He, L.,Xue, C.H.,Wang, J.J.,Li, M.,Lu, W.C. and Zhao, Z.M. (2009) Resistance selection and biochemical mechanism of resistance to two Acaricides in Tetranychus cinnabarinus (Boiduval). Pesticide Biochemistry and Physiology,93,47–52.

[31]

Kanga, L.H.B.,Eason, J.,Haseeb, M.,Qureshi, J. and Stansly, P. (2016) Monitoring for insecticide resistance in Asian citrus psyllid (Hemiptera: Psyllidae) populations in Florida. Journal of Economic Entomology,109,832–836.

[32]

Kuang, Y.,Xiong, Y.,Chen, X.D. and Yu, X. (2022) Antennae-abundant expression of candidate cytochrome P450 genes associated with odorant degradation in the Asian citrus psyllid,Diaphorina citri. Frontiers in Physiology,13,1004192.

[33]

Kuenen, D.J. (1958). Influences of sublethal doses of DDT upon the multiplication of Sitophilus granarius (Coleopt. Curculionidae). Entomologia Experimentalis et Applicata,1,147–152.

[34]

Lai, T. and Su, J. (2011). Assessment of resistance risk in Spodoptera exigua (Hubner) (Lepidoptera: Noctuidae) to chlorantraniliprole. Pest Management Science,67,1468–1472.

[35]

Langdon, K.W.,Schumann, R.,Stelinski, L.L. and Rogers, M.E. (2018) Spatial and temporal distribution of soil-applied neonicotinoids in citrus tree foliage. Journal of Economic Entomology,111,1788–1798.

[36]

Lowery, T. and Sears, M.K. (1986). Effect of exposure to the insecticide azinphosmethyl on reproduction of green peach aphid (Homoptera: Aphididae). Journal of Economic Entomology,79,1534–1538.

[37]

Luckey, T.D. (1963). Germfree life and Gnotobiology. Boca Raton,CRC Press.

[38]

Luckey, T.D. (1968). Insecticide Hormoligosis. Journal of Economic Entomology,61,7–12.

[39]

Luo, X.,Yen, A.L.,Powell, K.S.,Wu, F.,Wang, Y.,Zeng, L. et al. (2015) Feeding behavior of Diaphorina citri (Hemiptera: Liviidae) and its acquisition of “Candidatus Liberibacter asiaticus” on huanglongbing-infected Citrus reticulata leaves of several maturity stages. Florida Entomologist,98,186–192.

[40]

Nauen, R. (1995) Behaviour modifying effects of low systemic concentrations of imidacloprid on Myzus persicae with special reference to an antifeeding response. Pesticide Science,44,145–153.

[41]

O’Hara, F.M.,Liu, Z.,Davis, J.A. and Swale, D.R. (2023) Catalyzing systemic movement of inward rectifier potassium channel inhibitors for antifeedant activity against the cotton aphid,Aphis gossypii (Glover). Pest Management Science,79,194–205.

[42]

Prado, E. and Tjallingii, W.F. (1994). Aphid activities during sieve element puncture. Entomologia Experimentalis et Applicata,72,157–165.

[43]

Ripper, W.E. (1956). Effect of pesticides on balance of arthropod populations. Annual Review of Entomology,1,303–438.

[44]

Roan, C.C. and Hopkins, T.L. (1961). Mode of action of insecticide. Annual Review of Entomology,6,333–346.

[45]

Saryazdi, G.A.,Hejazi, M.J.,Rashidi, M.R. and Ferguson, S. (2014) Incidence and characterization of resistance to fenpropathrin in some Liriomyza sativae (Diptera: Agromyzidae) populations in Iran. Journal of Economic Entomology,107,1908–1915.

[46]

Sivasupramaniam, S. and Watson, T.F. (2000) Selection for fenpropathrin and fenpropathrin+acephate resistance in the silverleaf whitefly (Homoptera: Aleyrodidae). Journal of Economic Entomology,93,949–954.

[47]

Stark, J.D.,Chen, X.D. and Johnson, C.S. (2012) Effects of herbicides on Behr’s metalmark butterfly, a surrogate species for the endangered butterfly, Lange’s metalmark. Environmental Pollution,164,24–27.

[48]

Tiwari, S.,Mann, R.S.,Rogers, M.E. and Stelinski, L.L. (2011) Insecticide resistance in field populations of Asian citrus psyllid in Florida. Pest Management Science,67,1258–1268.

[49]

Wu, Q.,Zhang, G.,Chen, Y.,Yu, J.L.,Zhou, Y.K.,Shu, Z.L. et al. (2021) Seed dressing with triflumezopyrim controls brown planthopper populations by inhibiting feeding behavior, fecundity and enhancing rice plant resistance. Pest Management Science,77,2870–2886.

[50]

Zanardi, O.Z.,Bordini, G.P.,Franco, A.A.,de Morais, M.R. and Yamamoto, P.T. (2018) Spraying pyrethroid and neonicotinoid insecticides can induce outbreaks of Panonychus citri (Trombidiformes: Tetranychidae) in citrus groves. Experimental and Applied Acarology,76,339–354.

[51]

Zhu, J.,Sun, W.Q.,Li, Y.,Ge, L.Q.,Yang, G.Q.,Xu, J.X. et al. (2020) Effects of a novel mesoionic insecticide, triflumezopyrim, on the feeding behavior of rice planthoppers,Nilaparvata lugens and Sogatella furcifera (Hemiptera: Delphacidae). Journal of Integrative Agriculture,19,2488–2499.

RIGHTS & PERMISSIONS

2023 The Authors. Insect Science published by John Wiley & Sons Australia, Ltd on behalf of Institute of Zoology, Chinese Academy of Sciences.

AI Summary AI Mindmap
PDF

267

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/