Lethal time of insecticides on the predator mite Neoseiulus fallacis (Acari: Phytoseiidae) following topical exposure

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1 Lethal time of insecticides on the predator mite Neoseiulus fallacis (Acari: Phytoseiidae) following topical exposure Raja Z. Raja Jamil, 1 Christine Vandervoort, Larry J. Gut, Mark E. Whalon, John C. Wise 353 Abstract Neoseiulus fallacis (Garman) (Acari: Phytoseiidae) is an efficient predator of the European red mite (ERM) (Panonychus ulmi (Koch); Acari: Tetranychidae) in Michigan, United States of America apple orchards and an important part of integrated pest management. Four reduced-risk insecticides (acetamiprid, spinetoram, chlorantraniliprole, and novaluron) and two conventional insecticides (esfenvalerate and carbaryl) were tested against N. fallacis for topical toxicity effects. Bioassays using a Potter spray tower were conducted to measure the topical toxicity of compounds when applied at field rate concentrations to N. fallacis. Lethal time was measured for adult N. fallacis at 4, 24, 48, 72, and 96 hours after treatment. Carbaryl and esfenvalerate showed the highest levels of toxicity to adult N. fallacis with shortest lethal time values (LT 50 ) whereas the reduced risk insecticides novaluron, acetamiprid, spinetoram, and chlorantraniliprole were nontoxic. This study provides important information to apple growers regarding direct lethal effect of insecticides on predator mites and its implications to integrated mite management. Introduction Neoseiulus fallacis (Garman) (Acari: Phytoseiidae) is an important predacious mite in North American apple orchards and an efficient predator of the European red mite (ERM), Panonychus ulmi (Koch) (Acari: Tetranychidae), two-spotted spider mites (TSSM), Tetranychus urticae Koch (Acari: Tetranychidae), and other phytophagous mites. In the humid central and eastern regions of North America N. fallacis occurs on trees and lower vegetation, whereas in the drier western parts, N. fallacis usually inhabits low and sprawling plants, unless living on irrigated tree crops (Morris et al. 1996). In winter, N. fallacis finds shelter in the orchard ground cover and feeds upon overwintering two spotted spider mite (Croft 1990), apple rust mite Aculus schlectendali (Nalepa) (Acari: Eriophyidae), cyclamen mite Steneotarsonemus pallidus (Banks) (Acari: Tarsonemidae), and tomato russet mite Aculops lycopersici (Massee) (Acari: Eriophyidae) (Rincon Vitova Insectaries 2008). Efficacy of N. fallacis for biological control has been reported extensively. In western and eastern North America, N. fallacis is effective on pestmite populations on variety of crops including apple, strawberry, corn, soybean, sorghum, and hops (Croft and McGroarty 1977; Croft 1990; Morris et al. 1996). High population of P. ulmi and T. urticae negatively affect plant health, reducing fruit size, increasing the number of premature fruit and causing leaf bronzing (van de Vrie 1985). Received 16 February Accepted 23 July First published online 22 March R.Z. Raja Jamil, 1 J.C. Wise, Department of Entomology, Michigan State University, 206 Center for Integrated Plant Systems, 578 Wilson Road, East Lansing, Michigan, , United States of America C. Vandervoort, Pesticide Analytical Laboratory, Michigan State University, 206 Center for Integrated Plant Systems, 578 Wilson Road, East Lansing, Michigan, , United States of America L.J. Gut, Department of Entomology, Michigan State University, 106 Center for Integrated Plant Systems, 578 Wilson Road, East Lansing, Michigan, , United States of America M.E. Whalon, Department of Entomology, Michigan State University, B11 Center for Integrated Plant Systems, 578 Wilson Road, East Lansing, Michigan, , United States of America 1 Corresponding author ( rajajami@msu.edu). Subject editor: Keith Summerville doi: /tce Can. Entomol. 148: (2016)

2 354 Can. Entomol. Vol. 148, 2016 High ERM populations, relative to predator numbers indicate a low likelihood of control by N. fallacis, necessitating acaricide sprays. However, acaricide usage leads to lower farm profits along with development of resistance, thus is unfavourable to integrated mite management (Villanueva 1997). In regard to commercial apple production, the maintenance of ERM below economic thresholds is not 100% guaranteed with biological control alone. Successful management of mite pests must use the holistic approach of integrated pest management (IPM). One tool of IPM, the use of pesticides, plays an important role in achieving a marketable crop. Pesticides, however, must be used cautiously, not to interfere with beneficial arthropods behaviour or survival. Insecticides used to control arthropod pests may be toxic to N. fallacis, causing disruption to the successful application of integrated mite management through biological control. Apple orchards in the western and eastern Unites States of America have historically relied heavily on broad-spectrum synthetic insecticides such as organophosphates and carbamates (Jones et al. 2009). Enactment of Food Quality Protection Act led to the restrictions on the use of organophosphate and carbamate insecticides thus eliminating or restricting many of those insecticides important for apple production (United States Environmental Protection Agency 1996). As a result, newer pesticides with novel modes of action and fewer environmental effects have been introduced (Whalon et al. 1999; Agnello et al. 2009). However, growing evident has shown that these newer pesticides are not always compatible with the beneficial insects (Agnello et al. 2009; Wise and Whalon 2009) and predator mites (Villanueva and Walgenbach 2005; Bostanian et al. 2009; Lefebvre et al. 2012). Insecticide applications are sometimes followed by serious outbreaks, not of the pest against which they were applied, but of other phytophagous insects and mites which, prior to the treatment were in very small numbers too low to be of economic importance (Abivardi 2004). Pest resurgence occurrence after application of pesticides exhibiting different modes of action and under different climatic conditions indicates that chemical control in many cases upsets the population dynamics of the pests in question. Van de Vrie et al. (1972) reported that the outbreaks of P. ulmi in apple orchards have been attributed to the use of pesticides that suppress their natural enemies. The use of synthetic pyrethroid insecticides for example, has been implicated in the reduction of phytoseiid mite species on a number of fruit tree crops in different parts of the world (AliNiazee 1984). Synthetic pyrethroids such as permethrin and fluvalinate caused 100% mortality of females Phytoseiulus macropilis (Banks) (Acari: Phytoseiidae) after 72 hours exposure in the laboratory bioassay (Amin et al. 2009). As a result, synthetic pyrethroids have been eliminated from most IPM recommendations and are avoided in most apple production systems (Agnello et al. 2009; Wise et al. 2011). Organophosphate insecticides when first introduced were toxic to predaceous mites, but most species are now resistant to the Organophosphates used in apple production. Laboratory worse case studies have shown varying levels of direct toxicity of new reduced risk insecticides, including imidacloprid, acetamiprid, and spinosad to predacious mites (Bostonian et al. 2010). Despite past efforts to determine the effects of insecticides on predator mites, there is a gap in understanding the toxicity of several new insecticide classes, including diamides, insect growth regulators, and spinosyns, to predaceous mites in apple production systems. Bioassays that address toxicity, as well as the lethal time of new compounds, is needed to fully understand the potential impact of modern IPM programs on predator mite populations. The purpose of this study was to measure the toxicity effects of N. fallacis exposure to foliar applied insecticides belonging to several newer insecticide classes through direct exposure to spray droplets. Methods and materials Field sampling Neoseiulus fallacis were collected in an apple orchard, Malus domestica Borkhausen cultivar Red Delicious (Rosaceae), maintained free from insecticides within the Michigan State University Trevor Nichols Research Center (TNRC) in Fennville, Michigan, United States of America ( N, W). Field observations to determine the distribution of N. fallacis in the apple orchard were done prior to the beginning of

3 Raja Jamil et al. 355 the experiment. A high abundance of predator mites was observed in blocks that contained relatively high levels of grassy groundcover. Collections were done in the morning to ensure a high yield of healthy predator mites. In all, apple leaves were collected at random from the tree canopy. Individual leaves were placed in a brown paper bag and transported to the laboratory in a portable ice chest. Laboratory preparation Apple leaves were removed from the paper bag and held at room temperature for 10 minutes. Following this, leaves were passed through a mite brush machine and N. fallacis were collected in large size petri dishes (6-cm diameter). They were immediately transferred to small petri dishes (3 cm) that were sealed with a thin layer of Arabic gum to prevent predator mite escapes. Ten adults were placed in each petri dish, with a total of seven replicates of each treatment. The petri dishes were held overnight in a refrigerator at 5 C before conducted bioassays the following day. Bioassay On the following day, the predator mites in each petri dish (3 cm) were treated with 2 ml insecticide solution (field rate equivalent solution) at 20 psi using a Potter Spray Tower (Burkard Scientific, Uxbridge, United Kingdom (Potter 1952) and were allowed to dry between 2.0 and 2.5 hours before the bioassay. Sprays were made to the interior top and bottom of petri dishes. The control treatment consisted of predator mites sprayed with distilled water. Following exposure to the insecticides or control treatment, N. fallacis were hand transferred in group to clean petri dishes using a camel paint brush and stored at 26.8 C, 60% relative humidity, and photoperiod 16:8 light:dark hours in an incubator. Each of these clean petri dishes was laced with two nontreated leaf discs (2.4 cm) and two spotted spider mites as a food source. After 4, 24, 48, 72, and 96 hours the bioassays were evaluated. The numbers of living predator mites were recorded with mortality defined as the mites that were immobile after prodding with a camel hair brush. Chemical compounds Insecticides tested in the bioassay were esfenvalerate at ppm (Asana.66 EC, g active ingredient (AI)/ha in 935 L/ha diluent equivalent) (DuPont, Wilmington, Delaware, United States of America)), spinetoram at ppm (Delegate 25 WG, g AI/ha in 935 L/ha diluent equivalent) (Dow AgroSciences LLC, Indianapolis, Indiana, United States of America), novaluron at ppm (Rimon.83 EC, g AI/ha in 935 L/ha diluent equivalent) (Chemtura U.S.A. Corporation, Middlebury, Connecticut, United States of America), chlorantroniliprole at ppm (Altacor 35 WG, g AI/ha in 935 L/ha diluent equivalent) (DuPont, Wilmington, Delaware, United States of America), acetamiprid at ppm (Assail 30 SG, g AI/ha in 935 L/ha diluent equivalent) (UPI, King of Prussia, Pennsylvania, United States of America) and carbaryl at ppm (Sevin 4 EC XLR, g AI/ha in 935 L/ha diluent equivalent) (Bayer Corporation, Kansas City, Missouri, United States of America). Statistical analysis Adult mortality data were corrected for the check mortality using Abbott s formula (Abbott 1925). The percentage mortality was arcsine transformed before using analysis of variance (ANOVA) procedures. Treatments means were separated using LSD test at P = 0.05 (PROC GLM) (SAS Institute 2002). Tukey s honestly significant differences test was used for multiple comparisons. The probit analysis was performed to calculate the time (in hours) at which 50% of the mites were killed (LT 50 ), slope of the log time-probit line (± SE), the confidence interval and the fiducial limits. Results The results from the topical toxicity assay for six insecticides are presented in Figure 1 and Table 1. Predator mite adults exposed to 96-hour topical assays showed significantly higher levels of mortality from the carbaryl and esfenvalerate treatments as compared to the untreated control, whereas other compounds did not cause mortality different than the untreated control (F = 10.50, df = 6, P ) (Fig. 1). The time in hours at which 50% of the predator mites were killed by insecticides (LT 50 ) was calculated as a measure of toxicity from insecticides as exposure time increased. Carbaryl was

4 356 Can. Entomol. Vol. 148, 2016 significantly more toxic to adults of N. fallacis and corrected mortality (Abbott 1925) reached 88% within 96 hours from topical application (Fig. 1). The LT 50 of carbaryl was significantly lower as compared to the untreated with the most rapid lethal time LT 50 value of 4.14 hours (x ) (Table 1). Esfenvalerate was significantly toxic to N. fallacis adults with a mortality rate of 84% after 96 hours exposure to topical application. The LT 50 of esfenvalerate showed significantly shorter lethal time as compared to the untreated control with calculated value of hours (x ). Novaluron and acetamiprid were less toxic to predator mites with 13% and 28% of mortality within 96 hours. The lethal time of novaluron was calculated as LT 50 value of hours (x ), while acetamiprid had lethal activity at the calculated LT 50 value of Fig. 1. Mean (± SEM) survival of Neoseiulus fallacis on apple leaf discs following 96 hours exposure to different insecticides. Means with the same letter are not significantly different at α Mean separation calculated using the Tukey s honestly significant differences (HSD) test. Data shown are nontransformed means hours (x ) with overlapped 95% confidence interval. Chlorantraniliprole and spinetoram were the least toxic to N. fallacis adult with 31% and 16% of mortality within 96 hours, and the calculated lethal time showed the slowest lethal activity with LT 50 value of (x 2 = ) and hours (x 2 = ) respectively (Table 1). Discussion This study provides important new information about the direct lethal effects of insecticides to N. fallacis following topical sprays. Results varied quite dramatically from compounds to compound, with some showing relatively little effect while others having high lethality. Carbaryl was highly toxic to N. fallacis as a result of direct exposure to topical sprays. The LT 50 value of this carbamate insecticide showed the least time (in hours) needed to cause N. fallacis mortality. These results agree with those of Edward and Hodgson (1973) showing that carbamates were highly toxic to an important mite predator in citrus, Stethorus nigripes (Kapur) (Coleoptera: Coccinellidae). Similarly, a two-year field study by Walker and Aitken (1996) validated that carbaryl-elevated populations of citrus red mite, Panonychus citri (McGregor) (Acari: Tetranychidae), in California citrus. The toxicity of carbaryl against N. fallacis through direct sprays therefore is likely a primary contributor to any mite flaring associated with the application of this compound. The pyrethroid esfenvalerate also was highly toxic to the predator mite N. fallacis. From the LT 50 value, this compound showed the time it takes to kill 50% of the N. fallacis adult was four fold that of carbaryl, but fast-acting none-the-less. This result is in concordance with Rock (1979) Table 1. LT 50 values for N. fallacis mortality after 96 hours of topical exposure to a given treatment insecticide. Insecticide n Slope (+SE) LT 50 (h) 95% CI χ 2 UTC ( ) (87.62, ) < Carbaryl ( ) 4.14 (1.19, 7.81) < Esfenvalerate ( ) (11.76, 26.46) < Novaluron ( ) (61.40, ) < Acetamiprid ( ) (66.56, 163) < Chlorantraniliprole ( ) (55.08, 5687) Spinetoram ( ) (55.85, )

5 Raja Jamil et al. 357 and AliNiazee (1984) who documented mortality to predator mites, N. fallacis and Typhlodromus arboreus Chant (Acari: Phytoseiidae), after exposure to synthetic pyrethroids. Similarly, Cho et al. (1997) found high toxicity in a test of esfenvalerate against the insect predator, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae). Esfenvalerate, a voltage-dependent sodiumchannel agonist is generally is highly active on the nervous system of insects or arthropods (Royal Society of Chemistry 1994). Direct contact through exposure to spray droplets provides the most effective route of entry followed by consumption of spray droplets or dried residue (Kelly 2003). As evident in our study, topical spray exposure demonstrated high mortality to N. fallacis. Since this synthetic pyrethroid is toxic to the predator mite N. fallacis, the application of esfenvalerate would likely reduce the conservation of N. fallacis thus causing pest mite outbreaks. The insect growth regulator novaluron was relatively nontoxic to adult N. fallacis. The observed lethality time, LT 50 value of this compound was slightly shorter than that of the untreated control, but with substantial overlapping of the confidence intervals. The nontoxic effect of novaluron on phytoseiid mites, Galendromus occidentalis (Nesbitt) (Acari: Phytoseiidae) was also reported by Lefebvre et al. (2011). In addition, Amarasekare and Shearer (2013) observed low toxicity in the adult predatory mired bug, Deraeocoris brevis (Uhler) (Hemiptera: Miridae) after exposure in topical bioassays. The neonicotinoid acetamiprid was not toxic to N. fallacis. The observed lethality time, LT 50 value of this compound was slightly shorter than that of untreated control, but with substantial overlapping of the confidence intervals. Similar result was shown by Pozzebon et al. (2011) who studied the toxicity of thiamethoxam, another neonicotinoid, to Phytoseiulus persimilis (Athias-Henriot) through multiple routes of exposure, with topical exposure resulted in low mortality of predatory mites. They concluded that topical sprays of thiamethoxam might have resulted in less uptake by predatory mites, due to tarsal uptake being more prominent than integument absorption. In addition, the body surfaces of mites were relatively small as compared to the treated leaf and this also suggested the role of residual exposure was superior to the topical exposure (Pozzebon et al. 2011). In contrast, Bostanian et al. (2009, 2010) reported that acetamiprid was moderately to highly toxic to G. occidentalis and N. fallacis in worst-case exposure scenario. Acetamiprid, a first generation neonicotinoid developed by Aventis CropScience (now Bayer CropScience, Leverkusen, Germany) is more effective systemically after foliar application (Horowitz et al. 1998). Its low hydrophobicity contributes to its excellent systemic and translaminar activity. Studies by Stein-Dönecke et al. (1992) and Westwood et al. (1998) demonstrated that neonicotinoids are mainly acropetally transported in the xylem. Systemic insecticides can contaminate floral nectar when systemically distributed throughout the plant (Lord et al. 1968) and cause detrimental effects to parasitoids (Cate et al. 1972). In our study, the low incidence of N. fallacis mortality may be due to lack of exposure to treated plant material or through feeding on treated prey. The diamide chlorantraniliprole was relatively nontoxic to the predator mite N. fallacis. The observed lethality time, LT 50 value of this compound was similar to that of the untreated control, and with substantial overlapping of the confidence intervals. Acute mortality from chlorantraniliprole in topical assays has given diverging results. Amarasekare and Shearer (2013) found that chlorantraniliprole were highly toxic to two insect predators, green lacewings Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae) and C. johnsoni (Henry, Wells, and Pupedis), whereas slight toxicity was observed for G. occidentalis (Nesbitt) in a worst-case exposure scenario in the laboratory. The macrocyclic lactone spinosyn insecticide, spinetoram, was the least toxic to the adult predator mite N. fallacis when applied topically. There was no significant mortality in predator mite adults and the time taken to kill 50% of the adult population took substantially longer than that of chlorantraniliprole. Nasreen et al. (2003) reported that topical treatments had no significant lethal effect on the insect predator, Chrysoperla carnea, but 100% mortality occurred when adults ingested treated prey. Likewise, no effect on the predation index was observed following exposure of the predatory mite, Euseius tularensis Congdon

6 358 Can. Entomol. Vol. 148, 2016 (Acari: Phytoseiidae), to spinosad (Khan and Morse 2006), another spinosyn. In contrast, high mortality was observed for the predatory mirid bug, Pilophorus typicus Distant (Hemiptera: Miridae), following the exposure to low spinosad concentrations (Nakahira et al. 2010). Active through ingestion, the insecticidal action of spinetoram is from two spinosyns, factor J, XDE-175-J and factor L, XDE-175-L, which causes anomalies to insect nachr receptors. When ingested, these factors were broadly distributed in tissue, however, the highest concentrations were found in the gastrointestinal tract (Food and Agriculture Organization 2007). Acute mortality from spinosad and spinosyn on predatory mites from exposure to dried residue on leaves has been extensively reported in the past (Villanueva and Walgenbach 2005; Van Driesch et al. 2006; Olszak and Sekrecka 2008; Lefebvre et al. 2011; Rahman et al. 2011). Thus, topical exposure of spinetoram from direct sprays is not anticipated as the route contributing to toxicity of this predator or to subsequent mite flaring. In this study, effects attained by single exposure route, topical spray, varied depending on the insecticide. Conventional insecticides such carbamates and esfenvalerate were highly toxic and their applications in the field need to be carefully considered as to limit interference with the conservation of adult N. fallacis. The reduced risk insecticides novaluron, acetamiprid, spinetoram, and chlorantraniliprole were relatively harmless to predator mites from direct sprays, but impacts of residual exposure on sprayed plant materials must be considered before full integrated mite management recommendations can be made. Acknowledgements The authors thank Laura Lamb and Ryan VanDerPoppen for their technical assistance. This study was supported by Michigan Apple Committee and Trevor Nichol Research Center. References Abbott, W.S A method for computing the effectives of an insecticide. Journal of Economic Entomology, 18: Abivardi, C Pesticide hormoligosis. In Encyclopedia of entomology. Volume 3. Edited by J.L. Capinera. Kluwer Academic Press, Dordrecht, The Netherlands. Pp Agnello, A., Atanassov, A., Bergh, J.C., Biddinger, D.J., Gut, L.J., Haas, M.J., et al Reduced-risk pest management programs for eastern U.S. apple and peach orchards: a 4-year regional project. American Entomologist, 55: AliNiazee, M.T Effects of two synthetic pyrethroids on the predatory mite, Typhlodromus arboreus in the apple orchards of western Oregon. In Acarology. Volume 6(2). Edited by D.A. Griffiths and C.E. Bowman. Ellis Horwood, Chichester, United Kingdom. Pp Amarasekare, K.G. and Shearer, P.W Laboratory bioassays to estimate the lethal and sublethal effects of various insecticides and fungicides on Deraeocoris brevis (Hemiptera: Miridae). Journal of Economic Entomology, 106: Amin, M.M., Mizell, R.F., and Flowers, R.W Response of the predatory mite Phytoseiulus macropilis (Acari: Phytoseiidae) to pesticides and kairomones of three spider mite species (Acari: Tetranychidae), and non-prey food. Florida Entomologist, 92: Bostanian, N.J., Hardman, J.M., Thistlewood, H.M.A., and Racette, G Effects of six selected orchard insecticides on Neoseiulus fallacis (Acari: Phytoseiidae) in the laboratory. Pest Management Science, 66: Bostanian, N.J., Thistlewood, H.M.A., Hardman, J.M., Laurin, M.-C., and Racette, G Effect of seven new orchard pesticides on Galendromus occidentalis in laboratory studies. Pest Management Science, 65: Cate, J.R., Ridgway, R.L., and Lingren, P.D Effects of systemic insecticides applied to cotton on adults of an ichneumonid parasite Campoletis perdistinctus. Journal of Economic Entomology, 65: Cho, J., Hong, K.J., Yoo, J.K., Bang, J.R., and Lee, J.O Comparative toxicity of selected insecticides to Aphis citricola, Myzus malisuctus (Homoptera: Aphididae), and the predator Harmonia axyridis (Coleoptera: Coccinellidae). Journal of Economic Entomology, 90: Croft, B.A Arthropod biological control agents and pesticides. Wiley Intersci, New York, New York, United States of America. Croft, B.A. and McGroarty, D.L The role of Amblyseius fallacis in Michigan apple orchards. Research Report Michigan Agricultural Experiment Station, 33: Edwards, B.A.B. and Hodgson, P.J The toxicity of commonly used orchard chemicals to Stethorus nigripes (Coleoptera: Coccinellidae). Journal of the Australian Entomological Society, 12: Food and Agriculture Organization Spinetoram [online]. Available from templates/agphome/documents/pests_pesticides/ JMPR/Evaluation08/Spinetoram.pdf [accessed 23 September 2015].

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