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2 January 2019 Evaluating the Effect of Imidacloprid Administered in Artificial Diet on Feeding Behavior of Diaphorina citri (Hemiptera: Liviidae) Using Electropenetrography
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Abstract

The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae) is the vector of Candidatus Liberibacter asiaticus (CLas), the presumed cause of Huanglongbing (HLB) in citrus. Management strategies were developed in Florida that used soil-applied neonicotinoids to protect young trees. Despite the implementation of intense management programs, infection spread among the most intensively managed groves.We used electopenetrography to test five imidacloprid doses (0.55, 5.5, 55, 550, and 5,500 ppm) administered in artificial diet to approximate the dosage required to reduce feeding activity and prevent salivation/ingestion activity. We failed to detect a significant effect of 0.55 ppm imidacloprid on probing behavior, pathway, or salivation/ingestion activity when compared with the untreated control. We observed a significant reduction in the number of probes and the number of pathway with both 5.5 and 55 ppm imidacloprid. We detected a significant reduction in the number of salivation/ingestion events at both 5.5 ppm and 55 ppm imidacloprid (57 and 54 percent, respectively) compared with the untreated control, and a reduction in number of sustained (>600 s) salivation/ingestion at 55 ppm. While reductions in feeding activity were apparent at dosages of at least 5.5 ppm, we were unable to prevent salivation/ingestion with dosages as high as 5,500 ppm, which is greater than what is known to occur following application in the field. While soil-applied imidacloprid may slow the spread of CLas, our findings suggest that prevention of CLas inoculation in the field is unlikely. Management strategies must be refined to prevent the spread of HLB in Florida.

The Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Liviidae), was first detected in Florida in 1998 (Halbert and Manjunath 2004) and is known to transmit the phloem-limited proteobacterium, Candidatus Liberibacter asiaticus (CLas), the presumed cause of citrus greening disease, or Huanglongbing (HLB) (Halbert and Manjunath 2004, Bové 2006, Grafton-Cardwell et al. 2013). Huanglongbing was discovered in Florida in 2005 (Halbert 2005) and has since caused a significant decline in the state's citrus production (Hodges and Spreen 2015). Upon inoculation of CLas into plant phloem, the bacteria move downward into the roots where the root system is severely compromised (Trivedi et al. 2012). Consequently, the canopy is starved of vital nutrients resulting in dead limbs and leaf drop, reductions in fruit yield and quality, with eventual tree death (Halbert and Manjunath 2004, Bové 2006, Grafton-Cardwell et al. 2013). Following the discovery of HLB in Florida citrus, management strategies were quickly developed and focussed on tree health and vector management to aid in reducing the spread of the disease (Rogers 2008). Despite the implementation of intense management programs, virtually all D. citri are currently infected with CLas, and tree infection continues to spread among the most intensively managed groves (Rogers 2013, Coy and Stelinski 2015). We must evaluate current vector management practices to elucidate why spread of the pathogen continues in order to develop and deliver improved management tactics to growers.

Diaphorina citri are characterized as insects with high fecundity and rapid development, undergoing completion of the egg to adult life cycle in as little as 15 d during periods of optimal environmental conditions (Liu and Tsai 2000, Grafton-Cardwell et al. 2013). Adult D. citri are attracted to volatiles emitted by newly formed flush shoots where they lay up to 800 eggs per female (Patt and Setamou 2010). If egg lay occurs on CLas-infected host tissue, newly hatched nymphs feed on phloem sap and acquire CLas (Pelz-Stelinski et al. 2010). Acquisition efficiency is increased for nymphs developing on infected host tissue compared with D. citri acquiring the pathogen in the adult stage (Pelz-Stelinski et al. 2010). The resultant dispersal of infected adults causes a spread of the pathogen within and among groves.

Much of CLas vector management has maintained focus on young tree programs (Rogers 2008,2013). The key objective of the young tree management program is to maintain HLB-free trees until trees reach fruit-bearing age. Young trees flush asynchronously and frequently relative to mature trees in Florida (Hall and Albrigo 2007, Rogers 2012). Because adult D. citri seek young flush for egg lay or feeding, young trees are presumably at greatest risk of acquiring CLas (Stansly and Rogers 2006). Vector management programs in young trees advise an approximate 3wk alternation between soil-applied neonicotinoids and non-neonicotinoid foliar sprays aimed to maintain D. citri populations at low levels in young tree groves (Rogers 2012, Rogers et al. 2014). Neonicotinoids are a unique group of systemic insecticides that when applied to the soil are absorbed by the roots and transported through xylem vascular bundles to the foliage (Elbert et al. 2008). According to the Insecticide Resistance Action Committee (IRAC) neonicotinoids are within the insecticide subgroup 4A, and bind to the insect nicotinic acetylcholine receptor (nAChR) resulting in hyper-excitation, paralysis, and eventual death (IRAC 2017). Three neonicotinoid insecticides are currently labeled for use in nonbearing citrus in Florida: thiamethoxam (Platinum 75 SG—Syngenta Crop Protection, Inc., Greensboro, NC); imidacloprid (Admire Pro 4.6F—Bayer CropScience, Research Triangle Park, NC); and clothianidin (Belay 2.13 SC—Valent USA Corporation, Walnut Creek, CA). A number of studies have investigated the residual activity of neonicotinoids applied to the soil and reported between 6 and 11 wk control (Qureshi and Stansly 2007,2009; Ichinose et al. 2010; Setamou et al. 2010; Byrne et al. 2012; Rogers 2012). While factors such as tree size and application rate affect acute neonicotinoid leaf tissue residues (Langdon et al. 2018a), uneven insecticide distribution within a plant is likely to result in areas of sublethal concentrations within leaf tissue at any time following application to the soil (Boina et al. 2009, Rogers 2012).

Electropenetrography (EPG) is the only real-time method used to study and quantify specific feeding behaviors of piercing-sucking hemipterans (Janssen et al. 1989, Joost et al. 2006, Bonani et al. 2010, Cid and Fereres 2010, Butler et al. 2012, Jacobson and Kennedy 2014, Lucini et al. 2016) and rasping-sucking Thysanoptera (Joost and Riley 2005). An EPG monitor is used to identify specific waveforms associated with distinct feeding behaviors. Bonani et al. (2010) correlated repetitive waveforms for D. citri with six feeding behaviors including nonprobing (NP), pathway (C), xylem ingestion (G), phloem contact (D), phloem salivation (E1), and phloem ingestion (E2). Occurrence, frequency, and duration of specific waveforms can be used to study insect feeding behavior in re