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Fitness costs associated with thiamethoxam and imidacloprid resistance in three field populations of Diaphorina citri (Hemiptera: Liviidae) from Florida

Published online by Cambridge University Press:  12 February 2020

Xue Dong Chen Open the ORCID record for Xue Dong Chen [Opens in a new window] ,
Timothy A. Ebert ,
Kirsten S. Pelz-Stelinski  and
Lukasz L. Stelinski
Xue Dong Chen
Affiliation:
Entomology and Nematology Department, University of Florida, Citrus Research and Education Center, 700 Experiment station Rd, Lake Alfred, FL, 33850, USA
Timothy A. Ebert
Affiliation:
Horticulture Department, University of Florida, Citrus Research and Education Center, 700 Experiment station, Lake Alfred, FL, 33850, USA
Kirsten S. Pelz-Stelinski
Affiliation:
Entomology and Nematology Department, University of Florida, Citrus Research and Education Center, 700 Experiment station Rd, Lake Alfred, FL, 33850, USA
Lukasz L. Stelinski*
Affiliation:
Entomology and Nematology Department, University of Florida, Citrus Research and Education Center, 700 Experiment station Rd, Lake Alfred, FL, 33850, USA
*
Author for correspondence: Lukasz L. Stelinski, Email: [email protected]
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Abstract

Insecticide resistance is an increasing problem in citrus production. The Asian citrus psyllid, Diaphornia citri Kuwayama, is recognized as one of the most important citrus pests worldwide and it has developed resistance in areas where insecticides have been overused. The development of insecticide resistance is often associated with fitness costs that only become apparent in the absence of selection pressure. Here, the fitness costs associated with resistance to thiamethoxam and imidacloprid were investigated in three agricultural populations of D. citri as compared with susceptible laboratory colonies. Results showed that all field populations had greater resistance than laboratory susceptible colonies. For both thiamethoxam and imidacloprid, a Candidatus Liberibacter asiaticus-positive (CLas+) colony was more susceptible than the CLas− colony. Resistance ratios ranged from 7.65–16.11 for imidacloprid and 26.79–49.09 for thiamethoxam in field populations as compared with a susceptible, CLas− laboratory strain. Among three resistant field populations, a significantly reduced net reproductive rate and finite rate of population increase were observed in a population from Lake Wales, FL as compared to both susceptible strains. The fecundity of field populations from Lake Wales, FL was statistically lower than both laboratory susceptible populations. Certain changes in morphological characteristics were observed among resistant, as compared, with susceptible strains. Our data suggest fitness disadvantages associated with insecticide resistance in D. citri are related to both development and reproduction. The lower fitness of D. citri populations that exhibit resistance to neonicotinoid insecticides should promote recovery of sensitivity when those populations are no longer exposed to thiamethoxam and/or imidacloprid in the field. The results are congruent with a strategy of insecticide rotation for resistance management.

Keywords

Candidatus Liberibacter asiaticuscitrus greeningDiaphornia citrifitness costsinsecticide resistance
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 110 , Issue 4 , August 2020 , pp. 512 - 520
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Copyright
Copyright © Cambridge University Press 2020

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References

Abbas, N, Shad, SA and Razaq, M (2012) Fitness cost, cross resistance and realized heritability of resistance to imidacloprid in Spodoptera litura (Lepidoptera: Noctuidae). Pesticide Biochemistry and Physiology 103, 181–188.CrossRefGoogle Scholar
Abbas, N, Shad, SA, Razaq, M, Waheed, A and Aslam, M (2014) Resistance of Spodoptera litura (Lepidoptera: Noctuidae) to profenofos: relative fitness and cross resistance. Crop Protection 58, 49–54.CrossRefGoogle Scholar
Abbas, N, Khan, H and Shad, SA (2015) Cross-resistance, stability, and fitness cost of resistance to imidacloprid in Musca domestica L., (Diptera: Muscidae). Parasitology Research 114, 247–255.CrossRefGoogle Scholar
Abbas, N, Shah, RM, Shad, SA and Azher, F (2016a) Dominant fitness costs of resistance to fipronil in Musca domestica Linnaeus (Diptera: Muscidae). Veterinary Parasitology 226, 78–82.CrossRefGoogle Scholar
Abbas, N, Shah, RM, Shad, SA, Iqbal, N and Razaq, M (2016b) Biological trait analysis and stability of lambda-cyhalothrin resistance in the house fly, Musca domestica L. (Diptera: Muscidae). Parasitology Research 115, 2073–2080.CrossRefGoogle Scholar
Abbott, WS (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265–267.CrossRefGoogle Scholar
Afzal, BMS, Shad, SA, Ayyaz, M and Walker, WB (2015) Cross-resistance, the stability of acetamiprid resistance and its effect on the biological parameters of cotton mealybug, Phenacoccus solenopsis (Homoptera: Pseudococcidae). Pest Management Science 71, 151–158.CrossRefGoogle Scholar
Alyokhin, A, Dively, G, Patterson, M, Castaldo, C, Rogers, D, Mahoney, M and Wollam, J (2007) Resistance and cross-resistance to imidacloprid and thiamethoxam in the Colorado potato beetle Leptinotarsa decemlineata. Pest Management Science 63, 32–41.CrossRefGoogle ScholarPubMed
Arnaud, L and Haubruge, E (2002) Insecticide resistance enhances male reproductive success in a beetle. Evolution 56, 2435–2444.CrossRefGoogle Scholar
Baguette, M and Schtickzelle, N (2006) Negative relationship between dispersal distance and demography in butterfly metapopulations. Ecology 87, 648–654.CrossRefGoogle ScholarPubMed
Baker, MB, Alyokhin, A, Porter, AH, Ferro, DN, Dastur, SR and Galal, N (2007) Persistence and inheritance of costs of resistance to imidacloprid in Colorado potato beetle. Journal of Economic Entomology 100, 1871–1879.CrossRefGoogle ScholarPubMed
Beanland, L, Hoy, CW, Miller, SA and Nault, LR (2000) Influence of aster yellows phytoplasma on the fitness of the aster leafhopper (Homoptera: Cicadellidae). Annals of the Entomological Society of America 93, 271–276.CrossRefGoogle Scholar
Bielza, P, Quinto, V, Gravalos, C, Abellan, J and Fernandez, E (2008) Lack of fitness costs of insecticide resistance in the western flower thrips (Thysanoptera: Thripidae). Journal of Economic Entomology 101, 499–503.CrossRefGoogle Scholar
Bilbo, TR, Reay-Jones, FPF, Reisig, DD and Greene, JK (2019) Susceptibility of corn earworm (Lepidoptera: Noctuidae) to Cry1A.105 and Cry2Ab2 in North and South Carolina. Journal of Economic Entomology 112, 1845–1857.CrossRefGoogle ScholarPubMed
Birch, LC (1948) The intrinsic rate of natural increase of an insect population. Journal of Animal Ecology 17, 15–26.CrossRefGoogle Scholar
Bourguet, D, Guillemaud, T, Chevillon, C and Raymond, M (2004) Fitness costs of insecticide resistance in natural breeding sites of the mosquito Culex pipiens. Evolution 58, 128–135.CrossRefGoogle ScholarPubMed
Bové, JM (2006) Huanglongbing: a destructive, newly-emerging, century-old disease of citrus. Journal of Plant Pathology 88, 7–37.Google Scholar
Cao, GC and Han, ZJ (2006) Tebufenozide resistance selected in Plutella xylostella and its cross-resistance and fitness cost. Pest management Science 62, 746–751.CrossRefGoogle ScholarPubMed
Chen, XD and Nakasuji, F (2004) Diminished egg size in fenvalerate resistant strains of the diamondback moth Plutella xylostella (Lepidoptera: Yponomeutidae). Applied Entomology and Zoology 39, 335–341.CrossRefGoogle Scholar
Chen, XD and Stelinski, LL (2017) Resistance management for Asian citrus psyllid, Diaphorina citri Kuwayama, in Florida. Insects 8, 130.Google ScholarPubMed
Chen, XD, Sanada-Morimura, S, Yanagi, SI and Nakasuji, F (2006) Rapid recovery of susceptibility under harsh environmental conditions in fenvalerate-resistant strains of the diamondback moth, Plutella xylostella (Lepidoptera: Yponomeutidae). Applied Entomology and Zoology 41, 641–650.CrossRefGoogle Scholar
Chen, XD, Seo, M and Stelinski, LL (2017) Behavioral and hormetic effects of the butenolide insecticide, flupyradifurone, on Asian citrus psyllid, Diaphorina citri. Crop Protection 98, 102–107.CrossRefGoogle Scholar
Chen, XD, Gill, AT, Ashfaq, M, Pelz-Stelinski, KS and Stelinski, LL (2018) Resistance to commonly used insecticides in Asian citrus psyllid: stability and relationship to gene expression. Journal of Applied Entomology 142, 967–977.CrossRefGoogle Scholar
Coustau, C, Chevillon, C and ffrench-Constant, R (2000) Resistance to xenobiotics and parasites: can we count the cost? Trends in Ecology and Evolution 15, 378–383.CrossRefGoogle ScholarPubMed
Denholm, I and Rowland, MW (1992) Tactics for managing pesticide resistance in arthropods: theory and practice. Annual Review of Entomology 37, 91–112.CrossRefGoogle ScholarPubMed
Ebbert, MA and Nault, LR (2001) Survival in Dalbulus Leafhopper vectors improves after exposure to maize stunting pathogens. Entomologia Experimentalis et Applicata 100, 311–324.CrossRefGoogle Scholar
Ejsmond, MJ, McNamara, JM, Søreide, J and Varpe, Ø (2018) Gradients of season length and mortality risk cause shifts in body size, reserves and reproductive strategies of determinate growers. Functional Ecology 32, 2395–2406.CrossRefGoogle Scholar
Elbert, A, Haas, M, Springer, B, Thielert, W and Nauen, R (2008) Applied aspects of neonicotinoid uses in crop protection. Pest Management Science 64, 1099–1105.CrossRefGoogle ScholarPubMed
Feng, YT, Wu, QJ, Xu, BY, Wang, SL, Chang, XL, Xie, W and Zhang, YJ (2009) Fitness costs and morphological change of laboratory-selected thiamethoxam resistance in the B-type Bemisia tabaci (Hemiptera: Aleyrodidae). Journal of Applied Entomology 133, 466–472.CrossRefGoogle Scholar
Finney, DJ (1971) Probit Analysis, 3rd Edn. Cambridge, USA: Cambridge University.Google Scholar
Fry, JD (1993) The “general vigor” problem: can antagonistic pleiotropy be detected when genetic covariances are positive? Evolution 47, 327–333.Google ScholarPubMed
Gottwald, TR (2010) Current epidemiological understanding of citrus huanglongbing. Annual Review of Phytopathology 48, 119–139.CrossRefGoogle ScholarPubMed
Grafton-Cardwell, EE, Stelinski, LL and Stansly, PA (2013) Biology and management of Asian citrus psyllid, vector of the Huanglongbing pathogens. Annual Review of Entomology 58, 413–432.CrossRefGoogle ScholarPubMed
Halbert, SE and Manjunath, KL (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Florida Entomologist 87, 330–353.CrossRefGoogle Scholar
Hall, DG, Shatters, RG, Carpenter, JE and Shapiro, JP (2010) Research toward an artificial diet for adult asian citrus psyllid. Annals of the Entomological Society of America 103, 611–617.CrossRefGoogle Scholar
Harshman, LG and Zera, AJ (2007) The cost of reproduction: the devil in the details. Trends in Ecology & Evolution 22, 80–86.CrossRefGoogle ScholarPubMed
Haubruge, E and Arnaud, L (2001) Fitness consequences of malathion-specific resistance in red flour beetle (Coleoptera: Tenebrionidae) and selection for resistance in the absence of malathion. Journal of Economic Entomology 94, 552–557.CrossRefGoogle ScholarPubMed
Hollingsworth, RG, Tabashnik, BE, Johnson, MW, Messing, RH and Ullman, DE (1997) Relationship between susceptibility to insecticides and fecundity across populations of cotton aphid (Homoptera: Aphididae). Journal of Economic Entomology 90, 55–58.CrossRefGoogle Scholar
Jeschke, P, Nauen, R, Schindler, M and Elbert, A (2011) Overview of the status and global strategy for neonicotinoids. Journal of Agricultural and Food Chemistry 59, 2897–2908.CrossRefGoogle ScholarPubMed
Kanga, LH, Eason, J, Haseeb, M, Qureshi, J and Stansly, PA (2016) Monitoring for insecticide resistance in asian citrus psyllid (Hemiptera: Psyllidae) populations in Florida. Journal of Economic Entomology 109, 832–836.CrossRefGoogle ScholarPubMed
Kilot, A and Ghanim, M (2012) Fitness costs associated with insecticide resistance. Pest Management Science 68, 1431–1437.CrossRefGoogle Scholar
Langdon, KW and Rogers, ME (2017) Neonicotinoid-induced mortality of Diaphorina citri (Hemiptera: Liviidae) is affected by route of exposure. Journal of Economic Entomology 110, 2229–2234.CrossRefGoogle ScholarPubMed
Langellotto, GA, Denno, RF and Ott, JR (2000) A trade-off between flight capability and reproduction in males of a wing-dimorphic insect. Ecology 81, 865–875.CrossRefGoogle Scholar
Lewis-Rosenblum, H, Martini, X, Tiwari, S and Stelinski, LL (2015) Seasonal movement patterns and long-range dispersal of Asian citrus psyllid in Florida citrus. Journal of Economic Entomology 108, 3–10.CrossRefGoogle ScholarPubMed
Li, W, Hartung, JS and Levy, L (2006) Quantitative real-time PCR for detection and identification of Candidatus Liberibacter species associated with huanglongbing. Journal of Microbiological Methods 66, 104–115.CrossRefGoogle ScholarPubMed
Liu, Z and Han, Z (2008) Fitness costs of laboratory-selected imidacloprid resistance in the brown planthopper, Nilaparvata lugens Stål. Pest management Science 62, 279–282.CrossRefGoogle Scholar
Nault, LR (1997) Arthropod transmission of plant viruses: a new synthesis. Annals of the Entomological Society of America 90, 521–541.CrossRefGoogle Scholar
Nicastro, RL, Sato, ME and da Silva, MZ (2010) Milbemectin resistance in Tetranychus urticae (Acari: Tetranychidae): selection, stability and cross-resistance to abamectin. Experimental and Applied Acarology 50, 231–241.CrossRefGoogle ScholarPubMed
Oliveira, EE, Pippow, A, Salgado, VL, Büschges, A, Schmidt, J and Kloppenburg, P (2010) Cholinergic currents in leg motoneurons of Carausius morosus. Journal of Neurophysiology 103, 2770–2782.CrossRefGoogle ScholarPubMed
Oliveira, EE, Schleicher, S, Buchges, A, Schmidt, J, Kloppenburg, P and Salgado, VL (2011) Desensitization of nicotinic acetylcholine receptors in central nervous system of the stickinsect (Carausius morosus) by imidacloprid and sulfoximine insecticides. Insect Biochemistry Molecular Biology 41, 872–880.CrossRefGoogle Scholar
Pelz-Stelinski, KS and Killiny, N (2016) Better together: association with Candidatus Liberibacter asiaticus increases the reproductive fitness of its insect vector, Diaphorina citri (Hemiptera: Liviidae). Annals of the Entomological Society of America 109, 371–376.CrossRefGoogle Scholar
Pelz-Stelinski, KS, Brlansky, RH, Ebert, TA and Rogers, ME (2010) Transmission of Candidatus Liberibacter asiaticus by the Asian citrus psyllid, Diaphorina citri. Journal of Economic Entomology 103, 1531–1541.CrossRefGoogle Scholar
Puinean, AM, Denholm, I, Millar, NS, Nauen, R and Williamson, MS (2010) Characterisation of imidacloprid resistance mechanisms in the brown planthopper, Nilaparvata lugens Stål. (Hemiptera: Delphacidae). Pesticide biochemistry and physiology 97, 129–132.CrossRefGoogle Scholar
Ribeiro, LM, Wanderley-Teixeira, V, Ferreira, HN, Teixeira, ÁAC and Siqueira, HAA (2014) Fitness costs associated with field-evolved resistance to chlorantraniliprole in Plutella xylostella (Lepidoptera: Plutellidae). Bulletin of Entomological Research 104, 88–96.CrossRefGoogle Scholar
Robertson, JL and Preisler, HK (1992) Pesticide Bioassays with Arthropods. Boca Raton FL: CRC Press.Google Scholar
SAS Institute (2002–2012) User's manual, version 9.4. SAS Institute, Cary, NC.Google Scholar
Salgado, VL (2016) Antagonist pharmacology of desensitizing and non-desensitizing nicotinic acetylcholine receptors in cockroach neurons. Neurotoxicology 56, 188–195.CrossRefGoogle ScholarPubMed
Salgado, VL and Saar, R (2004) Desensitizing and non-desensitizing subtypes of alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in cockroach neurons. Journal of Insect Physiology 50, 867–879.CrossRefGoogle ScholarPubMed
Sayyed, AH, Ahmad, M and Crickmore, N (2008) Fitness costs limit the development of resistance to indoxacarb and deltamethrin in Heliothis virescens (Lepidoptera: Noctuidae). Journal of Economic Entomology 101, 1927–1933.CrossRefGoogle Scholar
Stark, JD and Banks, JE (2003) Population-level effects of pesticides and other toxicants on arthropods. Annual Review of Entomology 48, 505–519.CrossRefGoogle ScholarPubMed
Stockton, DG, Pescitelli, LE, Ebert, TA, Martini, X and Stelinski, LL (2017) Induced preference improves offspring fitness in a phytopathogen vector. Environmental Entomology 46, 1090–1097.CrossRefGoogle Scholar
Tiwari, S, Lewis-Rosenblum, H, Pelz-Stelinski, KS and Stelinski, LL (2010) Incidence of Candidatus Liberibacter asiaticus infection in abandoned citrus occurring in proximity to commercially managed groves. Journal of Economic Entomology 103, 1972–1978.CrossRefGoogle ScholarPubMed
Tiwari, S, Killiny, N and Stelinski, LL (2013) Dynamic insecticide susceptibility changes in Florida populations of Diaphorina citri (Hemiptera: Psyllidae). Journal of Economic Entomology 106, 393–399.CrossRefGoogle Scholar
Tsai, JH and Liu, YH (2000) Biology of Diaphorina citri (Homoptera: Psyllidae) on four host plants. Journal of Economic Entomology 93, 1721–1725.CrossRefGoogle ScholarPubMed
Vázquez-García, M, Velázquez-Monreal, J, Manuel Medina-Urrutia, V, de Jesús Cruz-Vargas, C, Sandoval-Salazar, M, Virgen-Calleros, G and Pablo Torres-Morán, J (2013) Insecticide Resistance in Adult Diaphorina citri Kuwayama from Lime Orchards in Central West Mexico. Southwestern Entomologist 38, 579–596.CrossRefGoogle Scholar
Villa, SM, Evans, MD, Subhani, YK, Altuna, JC, Bush, SE and Clayton, DH (2018) Body size and fecundity are correlated in feather lice (Phthiraptera: Ischnocera): implications for Harrison's rule. Ecological Entomology 43, 394–396.CrossRefGoogle Scholar