Journal of Economic Entomology Advance Access published July 3, 2015 ECOTOXICOLOGY Lethal and Sublethal Impacts of Acaricides on Tamarixia radiata (Hemiptera: Eulophidae), an Important Ectoparasitoid of Diaphorina citri (Hemiptera: Liviidae) A. C. S. LIRA,1 O. Z. ZANARDI,2 V. H. BELOTI,2 G. P. BORDINI,2 P. T. YAMAMOTO,2,3 J. R. P. PARRA,2 1 AND G. A. CARVALHO J. Econ. Entomol. 1–11 (2015); DOI: 10.1093/jee/tov189 ABSTRACT The use of synthetic acaricides for management of pest mites may alter the efficacy of the ectoparasitoid Tamarixia radiata (Waterston) in biological control of Diaphorina citri Kuwayama, the vector of the bacteria associated with huanglongbing (HLB) in citrus orchards. We evaluated the toxicity of 16 acaricides that are recommended for the control of citrus-pest mites to T. radiata. Acrinathrin, bifenthrin, carbosulfan, and fenpropathrin caused high acute toxicity and were considered harmful (mor- tality >77%) to T. radiata. Abamectin, diflubenzuron, etoxazole, fenbutatin oxide, fenpyroximate, flufe- noxuron, hexythiazox, propargite, spirodiclofen, and sulfur caused low acute toxicity and affected the par- asitism rate and emergence rate of adults (F1 generation), and were considered slightly harmful to T. radiata. Dicofol and pyridaben did not affect the survival and action of the ectoparasitoid, and were considered harmless. In addition to its acute toxicity, carbosulfan caused mortality higher than 25% for >30 d after application, and was considered persistent. Acrinathrin, bifenthrin, fenpropathrin, fenpyroxi- mate, propargite, and sulfur caused mortalities over 25% until 24 d after application and were considered moderately persistent; abamectin was slightly persistent, and fenbutatin oxide was short lived. Our re- sults suggest that most acaricides used to control pest mites in citrus affect the density and efficacy of T. radiata in the biological control of D. citri. However, further evaluations are needed in order to deter- mine the effect of these products on this ectoparasitoid under field conditions. KEY WORDS biological control, acaricide, mortality, parasitism rate, emergence rate Huanglongbing (HLB) is among the most important Therefore, conservation and augmentation of biologi- and destructive citrus diseases worldwide (Bove´2006, cal control agents are important strategies to reduce Grafton-Cardwell et al. 2013). In Brazil, HLB is pre- population levels of pests and the impacts caused by sent in 6.9% of cultivated citrus trees (200 million overuse of insecticides in citrus orchards. Among the trees) in the state of Sa˜o Paulo, the main citrus-produc- natural enemies, the ectoparasitoid wasp Tamarixia ing region of the country (Fundecitrus 2013). Given radiata (Waterston) (Hemiptera: Eulophidae) has the absence of a cure, HLB is managed by planting shown great potential for use in pest management pro- healthy seedlings, reducing inoculum by eliminating grams to control D. citri (Pluke et al. 2008, Qureshi symptomatic trees, and mainly, control of the insect et al. 2009, Hall and Nguyen 2010, Williams et al. vector, the Asian citrus psyllid Diaphorina citri 2013). T. radiata is a specialized ectoparasitoid, devel- Kuwayama (Hemiptera: Liviidae). Currently, in Brazil, oping preferentially in third- to fifth-instar D. citri growers are spraying insecticides (organophosphates, nymphs (Skelley and Hoy 2004, Hall et al. 2013). In pyrethroids, and neonicotinoids) from 18 to 25 times Brazil, this ectoparasitoid was found in 2006 in the mu- annually, to control D. citri (Belasque Jr. et al. 2010). nicipality of Piracicaba, Sa˜o Paulo, and is currently pre- Despite their high efficacy, these products may alter sent in most citrus-producing regions of the country the balance between pests and their natural enemies, (Paiva and Parra 2012). It can be mass-reared in the causing outbreaks of secondary pests, resurgence of tar- laboratory for inundative release in field conditions, get pests, and selection of resistant populations (Yama- and rapidly suppresses populations of D. citri (Chen moto and Bassanezi 2003, Tiwari et al. 2011, Guedes and Stansly 2014). In recent years, successive releases and Cutler 2013). of T. radiata have been conducted in areas of HLB management programs, as well as in areas with orange jasmine [Murraya paniculata (L.) Jack (Rutaceae)] in- fested with D. citri nymphs or in areas next to commer- 1 Department of Entomology, Federal University of Lavras cial orchards, where the ectoparasitoid is multiplying (UFLA), 37200-000, Lavras, MG, Brazil. (Parra et al. 2010). In Sa˜o Paulo state, early estimates 2 Department of Entomology and Acarology, College of Agriculture “Luiz de Queiroz”/University of Sa˜o Paulo (ESALQ/USP), 13418-900, of parasitism rates ranged from 27.5 to 80% (Go´mez- Piracicaba, SP, Brazil. Torres et al. 2006, Parra et al. 2010). However, with in- 3 Corresponding author, e-mail: [email protected]. creased use of chemical pesticides for control of the VC The Authors 2015. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please email: [email protected] 2JOURNAL OF ECONOMIC ENTOMOLOGY vector D. citri, parasitism rates were reduced to below Pesticides. Sixteen commercial acaricides registered 25.7% (Paiva and Parra 2012). for the control of pest mites (especially B. phoenicis In addition to D. citri, the flat mite Brevipalpus and P. oleivora) in citrus orchards were evaluated on phoenicis (Geijskes) (Acari: Tenuipalpidae), vector of T. radiata. All compounds were tested without adjuvant the Citrus Leprosis Virus (CiLV), and the citrus rust at the label rates recommended by the Brazilian Minis- mite Phyllocoptruta oleivora (Ashmead) (Acari: Eryo- try of Agriculture, Livestock and Food Supply (MAPA; phyidae) are considered key pests of this crop (Oliveira Agrofit 2014). The acaricides and concentrations (g a.i. and Pattaro 2008). Although less important, mites of literÀ1) used in the bioassays are described in Table 1. the family Tetranychidae, especially the citrus red mite Bioassays. All laboratory bioassays were conducted Panonychus citri (McGregor) and the Texas citrus mite in a climate-controlled room (25 6 2C, 70 6 10% RH, Eutetranychus banksi (McGregor), also require control and a photoperiod of 14:10 [L:D] h), using a fully because of the continual population outbreaks observed randomized design. after successive applications of insecticides to control Bioassay 1: Acute Toxicity of Acaricides to D. citri (Yamamoto and Zanardi 2013). This increased T. radiata Adults. To assess the acute toxicity of acari- use of acaricides can alter biological and behavioral pa- cides to T. radiata adults, leaf discs (3.3 cm in diameter) rameters of the ectoparasitoid T. radiata and affect the of Valencia sweet orange [Citrus sinensis (L.) Osbeck action of this natural enemy in controlling D. citri. (Rutaceae)] were initially sprayed with 2 ml of solution, Some studies have demonstrated the acute and residual in a Potter tower (Burkard Scientific, Uxbridge, United toxicity of certain acaricides to T. radiata (Cocco and Kingdom) adjusted to a pressure of 0.7 kg cmÀ2, result- Hoy 2008, Hall and Nguyen 2010, Lira et al. 2014), but ing in a fresh dry deposition of 1.8 6 0.1 mg cmÀ2, none has examined the sublethal effects of acaricides according to the criteria established by the Pesticides on its biological parameters and parasitism efficiency. and Beneficial Organisms Working Group of the Inter- Knowledge of sublethal effects contributes to the un- national Organization for Biological Control of Noxious derstanding of the impacts of pesticides on natural ene- Animals and Plants, West Palearctic Regional Section mies (Desneux et al. 2007). This information is (IOBC/WPRS) for studies of pesticide toxicity to natu- important for the development of management strate- ral enemies (Van de Veire et al. 2002). Distilled water gies aimed at the conservation and augmentation of bi- was used as a control treatment. ological control agents, and also to guarantee the After the treatments were sprayed, the discs were success of integrated pest management (IPM) pro- kept in a climate-controlled room for 3 h to allow the grams in citrus. Considering the importance of T. radi- residues to dry. Then, the discs were placed in individ- ata as a biological control agent of D. citri,thisstudy ual Petri dishes (3.5 cm in diameter by 0.7 cm in assessed the lethal and sublethal impacts of 16 acari- height) containing a 2-mm layer of agar: water (2.5% cides that are recommended for the control of citrus w/v)andusedasanexperimentalunit.Next,10parasi- mites, on this ectoparasitoid. toid adults (5 females and 5 males) up to 24 h old were anesthetized with CO2 for 5 s and placed in each exper- imental unit. The experimental units were sealed with Materials and Methods voile fabric to allow gas exchange and prevent the accu- Rearing of T. radiate. The culture was established mulation of excess moisture. A honey droplet (1 from adults collected in citrus orchards in the munici- mm3) was placed on the voile to serve as food for the pality of Piracicaba, Sa˜o Paulo, Brazil. The insect popu- parasitoids during the assay period. For each treatment, lations were maintained at the Insect Biology five repetitions were used. Laboratory of the Department of Entomology and The number of alive and dead insects was recorded Acarology of the “Luiz de Queiroz” College of Agricul- 24 h after exposure to the residues. Moribund parasi- ture, University of Sa˜o Paulo (ESALQ/USP), Piraci- toids and those that did not react to the touch of a fine caba, Sa˜o Paulo, Brazil. The culture was maintained in brush were considered dead. The acute toxicity (mor- a climate-controlled room (25 6 2C, 70 6 10% relative tality) of each acaricide was calculated using the for- humidity [RH], and a photoperiod of 14:10 [L:D] h). mula of Abbott (1925). Based on mortality data (M), For the rearing we used seedlings of orange jasmine the acaricides were classified according to the criteria (M.