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A Multimodal Attract-And-Kill Device for the Asian Citrus Psyllid Diaphorina Citri (Hemiptera: Liviidae)

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A Multimodal Attract-And-Kill Device for the Asian Citrus Psyllid Diaphorina Citri (Hemiptera: Liviidae) insects Article A Multimodal Attract-and-Kill Device for the Asian Citrus Psyllid Diaphorina citri (Hemiptera: Liviidae) Justin George 1,2, Stephen L. Lapointe 3, Larry T. Markle 2, Joseph M. Patt 2, Sandra A. Allan 4 , Mamoudou Setamou 5, Monique J. Rivera 6 , Jawwad A. Qureshi 7 and Lukasz L. Stelinski 1,* 1 Citrus Research and Education Center, Entomology and Nematology Department, University of Florida, 700 Experiment Station Rd., Lake Alfred, FL 33850, USA; [email protected] 2 United States Department of Agriculture, Agricultural Research Service, 2001 South Rock Road, Fort Pierce, FL 34945, USA; [email protected] (L.T.M.); [email protected] (J.M.P.) 3 18 Valle Vista Dr., Asheville, NC 28804, USA; [email protected] 4 Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), Agriculture Research Service (ARS), US Department of Agriculture (USDA), Gainesville, FL 32608, USA; [email protected] 5 Kingsville Citrus Center, Texas A&M University, 312 N. International Blvd, Weslaco, TX 78599, USA; [email protected] 6 Department of Entomology, University of California Riverside, Riverside, CA 92521, USA; [email protected] 7 Southwest Florida Research and Education Center, Institute of Food and Agricultural Sciences, University of Florida, Immokalee, FL 34142, USA; jawwadq@ufl.edu * Correspondence: stelinski@ufl.edu Received: 29 October 2020; Accepted: 3 December 2020; Published: 8 December 2020 Simple Summary: Control of Asian citrus psyllid (Diaphorina citri), a vector of Candidatus liberibacter asiaticus (CLas), contributes to management of citrus greening disease (huanglongbing). We developed two prototypes of a multimodal attract-and-kill (AK) device with specific elements of color, attractant, phagostimulant, ultraviolet (UV) reflectant, and toxicant. Key sensory stimuli comprising the AK ingredients were identified in our current and previous research studies and incorporated into a yellow, slow-release wax matrix (SPLAT). This formulation was applied directly to the surface of yellow cylinders, or to corrugated plastic cards housed within perforated cylinders. Psyllids landing on the devices attempted to feed from the wax matrix, became intoxicated, died, and fell from device surfaces. Our laboratory and field experiments showed that AK devices attracted and killed significantly more adult D. citri than ordinary yellow sticky cards and remained fully active over a period of 12 weeks. Effective use of attract-and-kill for management of D. citri could reduce need for broad-spectrum insecticide sprays and encourage biological control as part of an integrated approach to huanglongbing (HLB) management in citrus. Abstract: Phytophagous insects, including Asian citrus psyllids (Diaphorina citri Kuwayama), use multiple sensory modalities (vision, olfaction, and gustation,) to locate and accept host plants. We explored incorporation of several sensory cues into a multi-modal attract-and-kill device (AK device) using a three-dimensional shape to increase visibility, as well as elements of color, attractant, phagostimulant, UV reflectant, and toxicant. Attraction of adult D. citri to the device was mediated by a combination of a highly reflective yellow cylinder, a UV reflectant compound (magnesium oxide), and an odorant blend as a short-range attractant. The device surface was coated with a slow-release wax matrix (SPLAT™) augmented with a phagostimulant consisting of a 3-component blend (formic acid, acetic acid, and para-cymene) and an insecticide (β-cyfluthrin). Psyllids landing on the device attempted to feed from the wax matrix, became intoxicated, died, and fell from the device. The device remained fully active over a period of 12 weeks partly because dead psyllids or nontargets did not adhere to the surface as occurs on adhesive yellow sticky cards, the industry standard. Laboratory and field assays showed that the device attracted Insects 2020, 11, 870; doi:10.3390/insects11120870 www.mdpi.com/journal/insects Insects 2020, 11, 870 2 of 14 and killed significantly more adult D. citri than ordinary yellow sticky cards. This device or a future iteration based on the design elements of this device is expected to contribute to sustainable and environmentally appropriate management of D. citri by exploiting the psyllid’s innate behavioral responses to visual, olfactory, and gustatory stimuli. Keywords: Asian citrus psyllid; huanglongbing; attract-and-kill device; probing behavior; vision; olfaction; phagostimulant; UV reflectance 1. Introduction Citrus greening disease, also called huanglongbing (HLB), is devastating the citrus industry in Florida and worldwide resulting in unprecedented economic loss. Total citrus production in Florida, the state hardest hit by the disease, has declined by approximately 70% since the first detection of HLB in 2004 [1], largely, though not exclusively, due to the rapid spread of HLB to all citrus growing regions of the state. Asian citrus psyllid (Diaphorina citri Kuwayama) is the only known insect vector of Candidatus Liberibacter asiaticus (CLas), the causal pathogen of HLB [2,3]. Suppression of vector populations is considered essential to minimize primary spread to new plantings and secondary spread of the pathogen within established groves [4,5]. Conventional pest and disease management strategies, including intensive and regionally coordinated insecticide applications, have helped with suppression of this vector-pathogen complex; however, disease continues to spread. Recently, Chow et al. 2019 [6] reported suppression of D. citri with an ‘attract-and-kill’ (AK) device that combined visual cues with a pyrethroid toxicant (β-cyfluthrin). Building upon these results, we developed two AK device prototypes that incorporated multiple sensory cues known to affect host finding and probing behaviors of D. citri, viz. visual (color, UV reflectant), olfactory (scent lure), and gustatory (phagostimulant) cues. An advantage of AK devices is that they remain clear of insect cadavers, leaf material, or other debris while maintaining an effective kill rate of psyllids over several weeks in the field. In this study, we used a spreadable emulsified wax dyed with yellow color (‘SPLAT’ ISCA Technologies Inc., Riverside, CA, USA) as the primary carrier and emitter of the sensory stimuli and toxicant material in the AK device prototypes. SPLAT was designed as a slow-release medium for volatile compounds and numerous studies have used SPLAT as a carrier material to measure D. citri response to various types of test stimuli [7–10]. A coating of yellow SPLAT was applied to different parts of the AK device prototypes, depending on the prototype’s design (See Section2). Because D. citri relies on visual cues to locate its host plants [11–16], our AK device prototypes utilized visual stimuli as a primary attractant. Attraction of D. citri to wavelengths perceived as yellow or lime-green in the human visual spectrum has been well documented and is the basis for the use of the “yellow or lime-green” sticky trap for surveillance [11]. In field tests of multiple yellow reflective paints, we found that D. citri adults exhibited greater attraction to fluorescent yellow colors than to the bright yellow color used in standard sticky card traps [17]. Therefore, a fluorescent yellow color, shown to be the most attractive to D. citri in our earlier tests [17], was incorporated into the SPLAT matrix evaluated here. Paris et al. (2017) [16] demonstrated increased attraction of D. citri to yellow and green stimuli by incorporating UV reflectants compared with the same colors without UV. When we incorporated a non-toxic UV-reflective compound, magnesium oxide (MgO), into test mixtures of SPLAT, we observed a significant increase in probing by D. citri compared with formulations without this ingredient [18]. Based on these results, MgO was included in our SPLAT formulation to maximize both psyllid attraction to and probing on the device surface. In addition, our prototype AK devices had a cylindrical shape to provide a highly visible surface to nearby psyllids and an ample surface area for landing and probing (Figure1A,B). InsectsInsects 2020,2020 11, x, 11 , 870 3 of 143 of 14 Figure 1. Image of attract-and-kill (AK) device prototypes in the field with horizontal sticky trays Figureto capture1. Image dead of attract and moribund-and-kill (ADiaphorinaK) device citri.prototypes(A) Perforated in the field cylinder with horizontal AK device sticky with spreadabletrays to capture deademulsified and moribund wax dyedDiaphorina with citri. yellow (A) color Perforated (SPLAT) cylinder card inside. AK device SPLAT with with spreadable all the ingredientsemulsified wax was dyed withapplied yellow tocolor the (SPLAT) corrugated card plastic inside. card SPLAT (SPLAT with card) all insertedthe ingredients inside the was cylinder applied (B to) Solid the corrugated cylinder AK plastic carddevice. (SPLAT SPLAT card) inserted containing inside all the ingredients cylinder was(B) Solid applied cylinder to the AK aluminum device. SPLAT foil on containing outer surface all ofingredients the was yellowapplied cylinder. to the aluminum Attractant foil was on released outer surface from rubberof the yellow septa attached cylinder. to Attractant the top of was cylinders. released from rubber septa attached to the top of cylinders. Foliar volatiles also play a role in detection, location, and evaluation of potential host plants by D. citri [19–27]. George et al. [10] found that formic acid and acetic acid, produced as
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