Research Article Received: 29 September 2011 Revised: 30 June 2012 Accepted article published: 3 August 2012 Published online in Wiley Online Library: 28 August 2012 (wileyonlinelibrary.com) DOI 10.1002/ps.3394 Imidacloprid as a contact arrestant for larvae of the European chafer, Amphimallon majale Gengping Zhu,a,b∗ Matthew J Petersen,b Guoqing Liuc and Daniel C Peckb,d Abstract BACKGROUND: Manipulative studies of the behavioral response of soil-dwelling insects to insecticides and other antagonists are stymied by the difficulties of observing and interpreting interactions played out below ground. Six experiments were carried out using X-ray radiography to quantify the movement of the European chafer, Amphimallon majale (Razoumowsky), larvae in response to imidacloprid and how this was affected by host plant cues and cold temperature. RESULTS: The movement of third instars was arrested in imidacloprid-treated soil at ≥0.6 ppm concentration. At ≥0.8 ppm, the arrestant effect of imidacloprid was stronger than the attraction cue posed by germinating grass seed. There was a less disruptive effect on dispersal distance in vertical versus lateral panels. In vertical panels, there was a less disruptive effect on downward movement under a cold temperature treatment that simulated overwintering conditions. CONCLUSION: Larvae of A. majale do not remotely detect imidacloprid in the soil; they neither evade contact, nor are repelled after contact. Imidacloprid thereby acts as a contact arrestant to disrupt grub movement. This finding might help to explain the synergistic effect of imidacloprid in combination with other biological agents for white grub control, and its effects on grub overwintering behavior. c 2012 Society of Chemical Industry Keywords: white grub; European chafer; Amphimallon majale; movement arrestant; imidacloprid; sublethal effect; X-ray radiography 1 INTRODUCTION the outcome of insecticidal interventions against a suite of The interrelated factors that influence insecticidal activity in the root-feeding and soil-inhabiting insect pest complexes that are of soil include chemistry and formulation of the active ingredient, global agricultural and economic concern. A better understanding soil and climatic conditions, susceptibility and behavior of the of how insecticides influence the sublethal behavior of soil insects target species and insect developmental stage.1 Additionally, the will lead to improved soil insect management via better targeting, presence of both synthetic insecticides and biological control greater efficacy and novel application approaches. agents can significantly influence the behavior of taxa from Imidacloprid is a versatile insecticide that is used for systemic fo- major soil insect pest complexes. Understanding how insecticides liar and soil drench applications and as seed dressing, film coating, and neurotoxicants modify insect behaviors, including mating, pelleting and multilayer coating, allowing for relatively safe and 11,12 host-finding and feeding, may offer new avenues for effective efficacious protection of young plants against insect attack. pest management.2 Among soil-inhabiting arthropod pests, It has a relatively broad spectrum of activity and a long-lasting repellence behavior has been widely tested and is highly relevant effect against early insect developmental stages. Sublethal ef- to insect susceptibility and control product efficacy.3–10 Larvae fects after exposure to imidacloprid have been documented for of the wireworms (Coleoptera: Elateridae) Agriotes obscurus L. several insect pests. Disruption of host evaluation behavior was 13 and Limonius canus (LeConte) were repelled by tefluthrin-treated observed in Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae). seeds after feeding for ≤15mininsoilmicrocosms.4,5 Larvae In choice tests, adult B. tabaci and alate morphs of Myzus per- of the weevil (Coleoptera: Curculionidae) Otiorhynchus sulcatus sicae (Sulzer) (Hemiptera: Aphididae) preferred untreated leaves (F.) were significantly deterred by bifenthrin absence of the host plant Picea abies L. Karst. (Pinales: Pinaceae).6 The mole ∗ crickets (Orthoptera: Gryllotalpidae) Scapteriscus borellii Giglio-Tos Correspondence to: Gengping Zhu, College of Environmental Science and and Scapteriscus vicinus Scudder modified their movement Engineering, Nankai University, Tianjin 300071, China. E-mail: [email protected] in response to Metarhizium anisopliae (Metchnikoff) Sorokin (Hypocreales: Clavacipitaceae) and Beauveria bassiana (Balsamo) a College of Environmental Science and Engineering, Nankai University, Tianjin, Vuillemin (Hypocreales: Clavacipitaceae), ultimately reducing China 7,8 their exposure to the entomopathogenic fungi. Among white b Department of Entomology, New York State Agricultural Experiment Station, grubs (Coleoptera: Scarabaeidae), the larvae of Popillia japonica Cornell University, Geneva, NY, USA Newman (Japanese beetle) avoid soil that contains mycelial 9,10 c College of Life Sciences, Nankai University, Tianjin, China particles of M. anisopliae. This suggests that detection of 483 and orientation to soil-borne antagonists are likely to influence d EntomoTech Fundamentals, Geneva, NY, USA Pest Manag Sci 2013; 69: 483–492 www.soci.org c 2012 Society of Chemical Industry www.soci.org G Zhu et al. over systemically treated leaves.14,15 Antifeedant effects were documented in M. persicae.15–17 Reduced fecundity was docu- mented in Diaphorina citri Kuwayama (Hemiptera: Psyllidae),18 Ceutorhynchus obstrictus (Marsham) (Coleoptera: Curculionidae)19 and Nilaparvata lugens (Stål) (Hemiptera: Delphacidae).20 With regard to white grubs, recent studies have shown an impact of imidacloprid on oviposition behavior,21 increased suscepti- bility to infection by entomopathogens22–25 and greater over- wintering mortality of larvae.26 While the alteration of insect behavior after exposure to imidacloprid has been demonstrated for white grubs, repellence behavior has yet to be thoroughly examined under controlled conditions. Because of imidaclo- prid’s widespread use in turf environments, understanding and exploiting potential insect behavioral modifications, such as re- pellence behavior, could be important for management of soil insects, particularly those displaying low susceptibility to contact insecticides. Since its first North American detection in 1940,27 Amphimallon majale (Razoumowsky) (Coleoptera: Scarabaeidae) has become a dominant white grub pest of turfgrass in many areas of Figure 1. Diagrams of the PVC pipe and Plexiglas panel microcosms. New York State. Elsewhere it has caused problems in other (A) PVC pipe with treated soil (106 g, left) and untreated soil (144 g, right); 28 29 evasion before contact with the treated zone would be evidence of remote nursery crops and in winter wheat. The species occurs from repellence; evasion upon contact would be evidence of contact repellence. the northeast United States west to Michigan, with a disjunct (B) Plexiglas panel in a horizontal (left) and vertical (right) position; the five population now established in British Columbia.30 Compared circles indicate grub placement sites. with the three other major species of turf-infesting white grubs in the northeast United States, Asiatic garden beetle [Maladera castanea (Arrow)], Japanese beetle and oriental beetle [Anomala 2 EXPERIMENTAL METHODS 2.1 Source of insects orientalis (Waterhouse)], control of A. majale hasproventobe difficult as it is less susceptible to insecticidal controls31 and to Third-instar A. majale collected from three field sites in New York State were used to conduct all laboratory experiments. Grubs environmental stressors such as drought.32 Behavior modifications were collected on 19 October 2009 in Fulton (Battle Island Golf due to insecticide exposure may help to explain the decreased Course, Oswego County), on 27 October 2009 in Victor (Parkview ability for control of A. majale. Fairways Golf Course, Ontario County) and on 9 November 2009 in To gain a better understanding of the nature of imidacloprid’s Rochester (Park Point at RIT, Monroe County). Larvae were held in sublethal effects on A. majale larval behavior, a series of soil, with a piece of sod from the collection site included as a food experiments was conducted with different combinations of ◦ source, at 4.4 C until 24 h before the start of experiments when antagonists and agonists, namely soil-incorporated imidacloprid ◦ they were transferred to 23 C. and germinating grass seed. Third-instar A. majale were chosen for the following studies not only because of the species’ pest status but also because the developmental stage can be 2.2 Radiographic imaging maintained in the laboratory for several months and is the Non-destructiveradiographicimagesofinsectswithinmicrocosms target of curative control in the field. The first objective of were made with a Faxitron X-ray cabinet (Model 43855B; Hewlett- this study was to determine (1) whether larvae could detect Packard, Palo Alto, CA). This system has been widely used in soil and orient away from imidacloprid, with two kinds of repellence insect behavior studies.7,9,10,32 The voltage was set at 74 kVp. being considered: evading imidacloprid before contact with the A digital X-ray scanner system (Model EZ400; NTB Eletronische treated zone, or evasion upon contact with the insecticides. The Geraete GmbH, Dickel, Germany) was used to capture, read and former would be evidence of remote repellence, while the latter manipulate the images. would be evidence of contact