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Hormesis in the Brown Citrus Aphid, Toxoptera Citricida (Kirkaldy) (Hemiptera: Aphididae) Exposed to Sublethal Doses of Imidacloprid

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Hormesis in the Brown Citrus Aphid, Toxoptera Citricida (Kirkaldy) (Hemiptera: Aphididae) Exposed to Sublethal Doses of Imidacloprid Hormesis in the brown citrus aphid, Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae) exposed to sublethal doses of imidacloprid Xue Dong Chen1, Meeja Seo2, Timothy A. Ebert3, Muhammad Ashfaq4, Wenquan Qin5, and Lukasz L. Stelinski1,* Abstract The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), is a major pest that transmits phloem-limited, gram negative bacteria including ‘Candidatus’ liberibacter asiaticus (Clas), causing huanglongbing. Management of this pest relies primarily on insecticides, such as the neo- nicotinoid imidacloprid, that may affect secondary pests including the brown citrus aphid,Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae). Here, we report on direct toxicity and sublethal dose effects of imidacloprid on T. citricida nymphs and adults following direct contact and ingestion. We also examined transgenerational dose-response and hormetic effects following exposure of T. citricida to a sublethal concentration of imidacloprid. Toxicity of imidacloprid was similar for nymphs (0.6 ng per µL) and adults (1 ng per µL) at 72 h. Fecundity and finite rate of increase were greater for populations exposed to systemic and foliar treatments at a sublethal concentration (0.1 ng per µL) compared with untreated controls. Development times of first instar nymphs in the1 F generation and third instar nymphs in the 2F generation were significantly greater for individuals treated with the sublethal dose than an untreated control. Survival of second instar T. citricida on plants treated with a sublethal concentration also was significantly greater than controls. There also was a significant increase in fecundity of F1 and F2 individuals after sublethal treatment compared with controls. Our results indicated that a sublethal concentration of imidacloprid increased the reproductive performance and induced possible physiologically stimulative (hormetic) effects inT. citricida. Hormesis in secondary pests should be considered when developing a management program for patho- gen vectors such as D. citri. Key Words: secondary pests; stimulated reproduction; stress conditioning; toxicity; huanglongbing Resumen El psílido asiático de los cítricos, Diaphorina citri Kuwayama (Hemiptera: Liviidae), es una plaga importante que transmite bacterias gramnega- tivas limitadas por el floema, incluyendo Liberibacter asiaticus (Clas), Candidatus, causando la enfermedad huanglongbing. El manejo de esta plaga se basa principalmente en insecticidas, como el imidacloprid neonicotinoide, que puede afectar a las plagas secundarias, incluido el pulgón marrón de los cítricos, Toxoptera citricida (Kirkaldy) (Hemiptera: Aphididae). Aquí, informamos sobre la toxicidad directa y los efectos de la dosis subletal de imidacloprid en ninfas de T. citricida y adultos después del contacto directo y la ingestión. También examinamos la respuesta a la dosis transgeneracional y los efectos horméticos después de la exposición de T. citricida a una concentración subletal de imidacloprid. La toxicidad de imidacloprid fue similar para las ninfas (0.6 ng por µL) y adultos (1 ng por µL) a las 72 h. La fecundidad y la tasa finita de aumento fueron mayores para las poblaciones expuestas a tratamientos sistémicos y foliares a una concentración subletal (0.1 ng por µL) en comparación con los controles no tratados. Los tiempos de desarrollo de las ninfas de primer estadio en la generación F1 y las ninfas del tercer estadio en la generación F2 fueron significativamente mayores para los individuos tratados con la dosis subletal que un control no tratado. La sobrevivencia del segundo estadio de T. citricida en plantas tratadas con una concentración subletal también fue significativamente mayor que los controles. También hubo un aumento significativo en la fecundidad de los individuos F1 y F2 después del tratamiento subletal en comparación con los controles. Nuestros resultados indicaron que una concentración subletal de imidacloprid aumentó el rendimiento reproductivo e indujo posibles efectos fisiológicamente esti- mulantes (horméticos) en T. citricida. Se debe considerar la hormesis en plagas secundarias al desarrollar un programa de manejo para vectores de patógenos como D. citri. Palabras Claves: plagas secundarias; reproducción estimulada; acondicionamiento de estrés; toxicidad; huanglongbing 1Entomology and Nematology Department, University of Florida, Citrus Research and Education Center, 700 Experiment station Rd, Lake Alfred, Florida 33850, USA; E-mail: [email protected] (X. D. C.), [email protected] (L. L. S.) 2Department of Agro-food Safety and Crop Protection, National Institute of Agricultural Science, RDA, 166 Nongsaengmyeong-ro, Wanju-gun, Republic of Korea; E-mail: [email protected] (M. S.) 3Horticulture Department, University of Florida, Citrus Research and Education Center, 700 Experiment Station Road, Lake Alfred, Florida 33850, USA; E-mail: [email protected] (T. A. E.) 4Department of Entomology, University of Agriculture Faisalabad, University Main Road, Faisalabad 38000, Pakistan; E-mail: [email protected] (M. A.) 5South China Agricultural University, Guangzhou 510642, China; E-mail: [email protected] (W. Q.) *Corresponding author; E-mail: [email protected] 2020 — Florida Entomologist — Volume 103, No. 3 337 338 2020 — Florida Entomologist — Volume 103, No. 3 The brown citrus aphid, Toxoptera citricida (Kirkaldy) (Hemiptera: Various lethal and sublethal effects of imidacloprid have been Aphididae), is considered one of the most important vectors of citrus reported recently in several insects and mites such as a mirid bug, tristeza virus in citrus (Michaud 1998). This species transmits citrus Apolygus lucorum (Meyer-Dür) (Hemiptera: Miridae) (Tan et al. tristeza virus with high efficiency (Roistacher & Bar-Joseph 1987; 2012; Pan et al. 2014); tobacco whitefly, Bemisia tabaci (Gennadius) Bar-Joseph et al. 1989). Citrus tristeza virus is a phloem-limited clo- (Hemiptera: Aleyrodidae) (He et al. 2013); cotton aphid, Aphis gos- sterovirus and some strains can cause devastating losses in citrus, sypii Glover (Hemiptera: Aphididae) (Shi et al. 2011); green peach particularly in regions using a sour orange rootstock (Tsai & Wang aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae) (Ayyanath et 1999). Toxoptera citricida is found throughout Europe, Asia, Pacific Is- al. 2013); English grain aphid, Sitobion avenae (Fabricius) (Hemip- lands, Sub-Sahara Africa, and South America (Carver 1978). It spread tera: Aphididae) (Miao et al. 2013); and a predatory mite, Ambly- through Central America and the Caribbean islands during the late seius victoriensis (Womersley) (Acarina: Phytoseiidae) (James 1997). 1980s (Yokomi et al. 1994), and was first detected in southern Florida However, potential sublethal effects of imidacloprid onT. citricida are in 1996 (Halbert & Brown 1996) where it rapidly became distributed unknown. In Florida, we hypothesized that long-term use of imida- throughout the citrus producing regions of the state (Liu & Tsai 2002). cloprid to manage D. citri may have exposed T. citricida to sublethal In Florida groves, the brown citrus aphid is restricted to host plants concentrations, thus increasing population growth rates ofT. citricida in the Rutaceae family where it is responsible for the transmission in unpredictable ways depending on factors such as hormesis and of citrus tristeza virus to citrus trees (Brlansky et al. 2003; Halbert increased citrus tristeza virus infection. The goal of this investigation et al. 2004). Citrus tristeza virus causes stem-pitting, quick decline, was to quantify the sublethal effects of imidacloprid on T. citricida to and reduces productivity of infected trees. In the 1960s, sour orange facilitate inclusion of this phytopathogen vector into current citrus rootstock was planted widely in Florida citrus groves allowing citrus integrated pest management programs. tristeza virus to become widespread and remain endemic. Since then, sour orange rootstock has been identified as the most susceptible rootstock to citrus tristeza virus and has been replaced with more Materials and Methods tolerant alternatives (e.g., Carrizo and Swingle trifoliates, as well as others). Although the incidence of citrus decline has decreased, the viral population of citrus tristeza virus strain T36 is still endemic in INSECTS AND PLANTS Florida groves (Harper & Cowell 2016). This could lead to a resur- gence in citrus decline from citrus tristeza virus, because this disease Toxoptera citricida used in these experiments originated from a agent has not been eradicated (Shivankar et al. 2015). population maintained on ‎Mexican orange, Choisya ternata H.B.K. Neonicotinoid insecticides applied as foliar sprays and soil (Rutaceae), plants (Forest Farm, Williams, Oregon, USA) in a green- drenches have been used widely since the early 1990s for man- house facility at the University of Florida Citrus Research and Devel- agement of a broad spectrum of sucking insect pests (Nauen et al. opment Center, Lake Alfred, Florida, USA. This population has been 1998; Jeschke et al. 2011). Imidacloprid, for example, has been an reared in the laboratory without exposure to insecticides since Jun important insecticide for control of Asian citrus pdyllid, Diaphorina 2017. Aphids were reared on Choisya ternata (Rutaceae) and ‘Swingle citri Kuwayama (Hemiptera: Liviidae). This psyllid is the vector of citrumelo’ (Citrus paradisi Macf. × Poncirus trifoliata [L.] Raf.; both Ru- Candidatus liberibactor asiaticus, the putative
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