Acute Toxicity and Sublethal Effects of Fenpyroximate to ... - BioOne

ECOTOXICOLOGY

Acute Toxicity and Sublethal Effects of Fenpyroximate to Amblyseius swirskii (Acari: Phytoseiidae) L. LOPEZ,1,2 H. A. SMITH,1 M. A. HOY,3 AND J. R. BLOOMQUIST4

J. Econ. Entomol. 108(3): 1047–1053 (2015); DOI: 10.1093/jee/tov033

ABSTRACT Knowledge about the effects of pesticides on biological control agents is required in order to successfully implement integrated pest management programs. The predatory mite Amblyseius swirskii Athias-Henriot has been used to control thrips, whiteflies, and broad mites in vegetable production; however, effects of fenpyroximate, an acaricide and insecticide used in vegetable crops, on A. swirskii have not been evaluated. The effect of four residual concentrations of fenpyroximate on A. swirskii females was measured under laboratory conditions including its effect on their fecundity and larval survival. Fresh residues of fenpyroximate were significantly toxic to adult females and larvae. Mortality increased and fecundity decreased as the concentration (0.026–0.208 ml/50 ml of water) and time after treatment (24–120 h) increased. Fifty percent of the larvae survived on the two lower concentrations (0.026 and 0.052 ml/50 ml of water) after 120 h. KEY WORDS acaricide, insecticide, predatory mite, residual concentration, side effect Major pest species are developing resistance to a broad spectrum of plant protection products (Jensen 2000, Emden et al. 2004, Hoy 2011, Haddi et al. 2012). This problem is often exacerbated by intensive and inappropriate insecticide applications. Alternative pest management techniques such as biological control (the use of parasites, predators, or pathogens) are promising components to many essential integrated pest management (IPM) programs and can help reduce the need for chemical pesticides (Nauen et al. 2001, Hamedi et al. 2010). Total abandonment of chemical inputs in a short period of time is often not feasible because the sole use of biological control may not maintain crop pests below the economic injury level (Hamedi et al. 2010, Hoy 2011). Creating better conditions for natural enemies, reducing pesticide applications, and mitigating the development of insecticide resistance are key goals of IPM programs (Irigaray et al. 2007, Amor et al. 2012). The two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), is an important pest of numerous fruit and vegetable crops (Nauen et al. 2001, Hoy 2011). Resistance has been reported to a wide variety of compounds from different classes of pesticides including organophosphates, avermectins, pyrethroids, carbamates, and METI-(mitochondrial electron transport inhibitors) acaricides (Nauen et al. 2001, Gorman

1 Gulf Coast Research and Education Center, University of Florida, 14625 County Rd., 672, Wimauma, FL 33598. 2 Corresponding author, e-mail: [email protected]. 3 Entomology and Nematology Department, University of Florida, Gainesville, FL 32611. 4 Entomology and Nematology Department, Emerging Pathogens Institute, 2055 Mowry Rd., University of Florida, Gainesville, FL 32611.

et al. 2002, Van Leeuwen et al. 2009, Hoy 2011). These chemicals also have undesired effects on nontarget organisms. The absence of control of two-spotted spider mites by natural enemies due to their death by pesticides can cause increases in their populations (Attia et al. 2013). Chemical control of other major pests, such as whiteflies (Hemiptera: Aleyrodidae) and thrips (Thysanoptera), has also been problematic due to rapid resistance development (Jensen 2000, Emden et al. 2004). Some neonicotinoids, insect growth regulators such as pyriproxyfen, and tetronic acids such as spiromesifen, have limited efficacy against certain strains of Bemisia tabaci Gennadius and Trialeurodes vaporariorum Westwood (Hemiptera: Aleyrodidae), respectively, because of the development of resistance (Gorman et al. 2002, Horowitz et al. 2004, Nauen and Denholm 2005, Karatolos et al. 2012). Similarly, the western flower thrips, Frankliniella occidentalis Pergande (Thysanoptera: Thripidae), is no longer effectively controlled by synthetic spinosyns and pyrethroids in some areas due to strains developing resistance (Jensen 2000, Bielza et al. 2007). The predatory mite Amblyseius swirskii AthiasHenriot (Acari: Phytoseiidae) has been used to control thrips, whiteflies, and broad mites (Polyphagotarsonemus latus Banks) in the field and in greenhouses and semiprotected vegetable production (Van Driesche et al. 2006, Messelink et al. 2010, Xu and Enkegaard 2010, Calvo et al. 2011, Colomer et al. 2011, Kutuk and Yigit 2011, Amor et al. 2012, Xiao et al. 2012). A. swirskii is not commonly used to control T. urticae because this species is not successful at reducing the pest population without chemical applications. However, A. swirskii has reduced populations of this phytophagous mite when alternative prey such as western flower

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thrips, sweetpotato whiteflies, or both, were present (Messelink et al. 2010, Xu and Enkegaard 2010). Fenpyroximate (Portal) is a pyrazole acaricide and insecticide with selective activity against important phytophagous mites in the families Tetranychidae, Eriophyiidae, and Tarsonemidae (Lummen 1998, Dekeyser 2005, Cloyd et al. 2010). It is a METI-acaricide at Complex I (Lummen 1998, Dekeyser 2005, Irigaray et al. 2007, Shiraishi et al. 2012). After spraying this acaricide, oxygen consumption and ATP production in the pest decline, causing knock down and paralysis (Lummen 1998). It is active against all stages of agriculturally important mites, showing higher efficacy against larvae than against other life stages (Dekeyser 2005). It has been registered to control major mite pests (twospotted spider mite, broad mite, citrus red mite [Panonychus citri McGregor] and European red mite [Panonychus ulmi Koch]), and is commonly used in vegetable production (Kim et al. 2006, Cloyd et al. 2010, Nichino America Inc 2012). In bioassays conducted using fenpyroximate, acute toxicity and sublethal effects have been evaluated for phytoseiid species such as Amblyseius andersoni Chant, A. stipulatus Athias-Henriot, Neoseiulus (¼Amblyseius) womersleyi Schicha (Kim and Paik 1996, Park et al. 2011), Metaseiulus occidentalis (Nesbitt) (Irigaray et al. 2007), Neoseiulus californicus McGregor (Meyer et al. 2009), Phytoseius plumifer Canestrini & Fanzago (Nadimi et al. 2009, Hamedi et al. 2010), Phytoseiulus macropilis Banks (Veronez et al. 2012), and Phytoseiulus persimilis Athias-Henriot (Irigaray et al. 2007, Nadimi et al. 2011, Park et al. 2011). Nadimi et al. (2009) found that sublethal concentrations of fenpyroximate did not affect phytoseiid egg hatchability but showed high toxicity to adults of P. plumifer when exposed to fresh residues. In another study, fenpyroximate showed high toxicity to adults of M. occidentalis and decreased fecundity (Irigaray et al. 2007). On the other hand, Van de Veire and collaborators (2001) reported that residual concentrations of fenpyroximate were harmless to A. californicus. Similarly, Park et al. (2011) argued that fenpyroximate is a compatible compound for the augmentative release of N. womersleyi, but should not be used where P. persimilis is present. The inconsistency of these findings is likely due to assessment of different phytoseiid species as well as variables such as type of food supplied, sex, and age of the mites tested. Moreover, the estimated lethal doses or concentrations during acute and sublethal toxicity tests may only be a part of the deleterious pesticide effects. Other sublethal effects such as learning performance, behavior, and physiology should be measured as well (Desneux et al. 2007). Phytoseiid species need to be examined independently to determine their compatibility with plant-protection products in IPM programs (Nadimi et al. 2009). Because applications of fenpyroximate and releases of A. swirskii are pest management techniques used in fruit and vegetable production in Florida (Colomer et al. 2011, Park et al. 2011, Santos and Vallad 2014), it is relevant to consider the effects of fenpyroximate on A. swirskii. Evaluations of the side effects of other

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acaricides on the performance of this predator have been made (Colomer et al. 2011, Gradish et al. 2011, Amor et al. 2012, BioBest 2013); however, the effects of fenpyroximate on A. swirskii have not been evaluated. Such information may be used to determine the compatibility of this acaricide with A. swirskii in IPM programs (Hamedi et al. 2010). The overall goal of this study was to evaluate the acute toxicity of four residual concentrations of the acaricide and insecticide fenpyroximate (Portal) on survival of A. swirskii females and the sublethal effects on their fecundity as well as on the survival of their progeny.

Materials and Methods Colony Tested. A. swirskii individuals were purchased from BioBest Biological Systems (Ontario, Canada), and the colony was started in November 2012 at the University of Florida’s Department of Entomology and Nematology, Gainesville, FL (25 6 2 C, 40 6 20% relative humidity (RH), and a photoperiod of 16:8 [L:D] h). Rearing was conducted on a waxed-paper arena resting on wet cotton in plastic trays. Small tufts of cotton fibers were added to provide shelter for oviposition. A colony of two-spotted spider mites was maintained in a greenhouse on pinto bean plants (Phaseolus vulgaris L., Fabaceae) to serve as prey for A. swirskii. It was selected to serve as prey for A. swirskii due to the two-spotted spider mite’s ability to grow rapidly in horticultural crops and the ease with which this species can be mass reared and handled under laboratory conditions (Hoy and Ouyang 1986, Hoy 2011). Insecticide and Miticide. Fenpyroximate (Portal) was obtained from Nichino America, Inc. as an emulsifiable concentrate (EC) formulation with 5% active ingredient (AI). The full rate was prepared based on the average rate used by bell pepper growers in Florida (2.4 liter/568 liter of water per ha) or 0.208 ml formulated product/50 ml of water (Nichino America, Inc. 2012; Santos and Vallad 2014). Rates 1-, 0.5-, 0.25-, and 0.125-fold of the proposed average field rate in bell peppers were tested (0.208 ml EC/50 ml of water, 0.104 ml EC/50 ml of water, 0.052 ml EC/50 ml of water, and 0.026 ml EC/50 ml of water, respectively). Distilled water was sprayed as the control. All tests were conducted using freshly prepared solutions in distilled water at 25 6 2 C, 35 6 20% RH. Solutions were agitated for a few seconds then sprayed on detached pepper leaves (12 6 6 1 cm) for about 5 s using an aerosol spray system (Crown Spra-Tool, 0.20 L, Aervoe Industries, Inc., Gardnerville, NV), covering the whole surface of the leaf but avoiding run off. Bioassay. For each concentration, five leaf discs (2.1 cm diameter) were cut from the sprayed pepper leaves after drying for approximately 1.5 h. Discs were placed bottom side up on water-soaked cotton in petri dishes (14 cm diameter; Hoy and Ouyang 1986). Five gravid A. swirskii females (5 d old) were placed on each disc, 25 females per concentration, using four concentrations and 25 for the control. The experiment was replicated four times with 125 females tested for

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LOPEZ ET AL.: EFFECT OF FENPYROXIMATE ON A. swirskii

each replication, for a total of 500 mites tested. Each disc had sufficient space for A. swirskii individuals and an ample amount of all stages of T. urticae was provided daily as prey. All replicates were conducted at 25 6 2 C, 40 6 20% RH, and a photoperiod of 16:8 (L:D) h and were set up at 1700 hours. Mites were checked on a daily basis for 5 d (total ¼ 120 h), and the criterion for survival was the ability to walk after being touched gently with a fine sable-hair brush. Immobilized, obviously dead, and run-off (escaped to the cotton surrounding the discs) mites were considered dead. Female and larval mortality were recorded following the criterion for survival mentioned above. Fecundity was measured as the number of eggs found daily, and no eggs were removed in order to allow their development to larvae. Statistical Analysis. Female mortality was analyzed using a two-way analysis of variance (ANOVA), followed by Tukey’s mean separation test when indicated (Statistica 7.0; StatSoft 1995). A probit analysis was conducted (SAS Institute 2011) to calculate lethal concentration indices (LC50 and LC90) for the two lower rates and lethal time indices (LT50 and LT90) for 24 and 48 h after treatment. Abbott’s formula (Yu 2008) was used to correct mortality data used in the probit analysis. The accumulated number of eggs (fecundity) over the 120 h was recorded. The daily fecundity (number of eggs laid each day) was calculated by subtracting the fecundity from each day minus the fecundity from the previous day (fecundity at 48 h ¼ accumulated fecundity at 48 – fecundity at 24 h, etc.). Fecundity data (number of eggs laid) per day and per concentration (including the control) were analyzed using oneway ANOVA, followed by Tukey’s mean separation test when appropriate (Statistica 7.0; StatSoft 1995). Larval mortality was analyzed using Multiple Pairwise Fisher’s Exact Test (SAS Institute 2011), and the Dunn–Sidak adjustment was performed using the P values obtained from the test. Pearson’s correlation index (r) was calculated to estimate the relation between adult mortality, fecundity, and larval mortality with the doses assessed (Microsoft Excel 2011).

Results Adult Mortality. Fresh residues of fenpyroximate (Portal) were significantly toxic to adult A. swirskii females (Fig. 1). Mortality of the females increased as the concentration of the insecticide and time after treatment increased, showing a positive relationship with both variables (r ¼ 0.76 and r ¼ 0.95, respectively). Control mortality reached a maximum of 1.5 (6%) dead females after 120 h (Fig. 1). Each concentration showed significantly different mortality rates compared with the control treatment over time, and differences between concentrations were identified as well (F4, 20 ¼ 2.86; P < 0.001). There was a slight, but not significant, grouping tendency of the registered mortality on the two lower and the two higher acaricide concentrations. The 0.125 - and 0.25-fold field rates were toxic for an average of 8 and 9 (50%) mites, respectively, after the same time period (Fig. 1). All calculated indices of lethality gave small numerical values (Table 1), reflecting the high level of toxicity of this acaricide to A. swirskii females. The LC50 value was between the 0.25 and 0.5 rates (0.052 and 0.104 ml/50 ml of water) after 24 h, whereas the estimated LC50 value 48 h after treatment was below the 0.125 concentration (0.026 ml/50 ml water). The estimated LC90 value after 24 h (0.745 ml EC/50 ml water) was above the highest concentration tested (0.208 ml EC/50 ml water). At 48 h posttreatment, the estimated LC90 fell between the two higher concentrations tested (0.104 and 0.208 ml EC/50 ml water). The LT50 calculations for the two lower concentrations showed that 50% of the mites died before the second day of treatment. According to these results, 90% mortality (LC90) was achieved because mites in the lower rates were exposed to more than twice the estimated LC50 values (Table 1). Fecundity. Residual concentrations of fenpyroximate had a significant effect on the number of eggs laid by A. swirskii females (F4, 20 ¼ 2.86; P < 0.001). Fecundity decreased substantially as the concentration of fenpyroximate increased (r ¼ 0.91). All residual concentrations resulted in significantly different fecundities compared with the control (Fig. 2A). Females in the control treatment laid 5 times more eggs compared with females from both the lowest and highest concentrations (0.125- and 1-fold of the field rate, respectively). The number of eggs recorded in all treatments decreased after 72 h due to hatching of eggs and their development to larvae (Fig. 2B). Similarly, fecundity decreased significantly as time increased (r ¼ 0.93). There were significant differences in fecundity recorded 24, 48, and 72 h after treatment (F3, 12 ¼ 9.71, P < 0.001; F3, 12 ¼ 9.63, P < 0.002; and F3, 12 ¼ 3.8, P < 0.04, respectively). No significant differences were found between fecundity recorded from the fenpyroximate rates assessed at 96 and 120 h. Larval Mortality. Larvae of A. swirskii from eggs deposited by treated females were negatively affected by all residual concentrations of fenpyroximate compared with control larvae (df ¼ 4; P < 0.001; Fig. 3). Larval mortality increased as the concentration of acaricide and time after treatment increased, showing a positive correlation with both variables (r ¼ 0.9 and r ¼ 0.87, respectively). No significant differences were identified by comparing mortality rates between pairs of concentrations (Fig. 3). Discussion The present study is the first assessment of acute toxicity and sublethal effects of fenpyroximate to A. swirskii under laboratory conditions. The results demonstrated that fresh residues of this acaricide strongly affect adult females of A. swirskii, causing immobilization and death even at one-eighth the average field rate used by vegetable producers in Florida (Nichino America Inc. 2012, Santos and Vallad 2014).

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Fig. 1. Mean (6 SE) number of A. swirskii females killed by residual concentrations of fenpyroximate at 0 -, 0.125-, 0.25-, 0.5-, and 1-fold the average field rate for peppers in Florida (total ¼ 500, 25 females per concentration, four concentrations and the control with four replications). A two-way ANOVA and Tukey’s mean separation test was performed to compare female mortality between days evaluated within each concentration. Letters above columns represent differences among days sampled for each of the concentrations evaluated. Table 1. Probit analysis for the concentration- and time-mortality response of A. swirskii females to fenpyroximate tested at 25 6 2 C, 40 6 20% RH, and a photoperiod of 16:8 (L:D) h n

Slope 6 SE Index of toxicitya

100 2.22 6 0.33 LC50 (24 h) 0.077 LC90 (24 h) 0.745 100 2.57 6 0.39 LC50 (48 h) 0.025 LC90 (48 h) 0.178 100 5.06 6 0.48 LT50 (0.125) 39.3 LT90 (0.125) 106.6 100 5.92 6 0.55 LT50 (0.25) 33.1 LT90 (0.25) 77.8

95% Confidence limits

v2

0.061–0.096 0.428–1.990 0.016–0.032 0.127–0.315 34.5–43.7 92.2–129.8 29.1–36.8 68.7–91.4

45.19 42.17 107.98 114.55

a Lethal concentration indices (LC50 and LC90) were estimated for the two lower concentration rates: 0.25 - (0.052 ml EC/50 ml of water) and 0.125-fold (0.026 ml EC/50 ml of water) of the average field rate in bell peppers. Lethal time indices (LT50 and LT90) were calculated for 24 and 48 h after treatment.

The toxic effect of fenpyroximate to A. swirskii females was greatest during the first 48 h of treatment. This is consistent with the interaction observed between residual concentration and time after treatment, where at higher concentrations and shorter periods of time the toxic effect of the acaricide is greater. Both adult and larval mortality rates showed a positive correlation with the residual concentrations tested. However, residues of the acaricide had a stronger effect on newly hatched larvae (r ¼ 0.9) in comparison with adult females (r ¼ 0.76). This effect is explained by the higher survival capacity of females. Their greater size and weight in comparison with males, larvae, protonymphs, or deutonymphs make them less susceptible to chemical intoxication (Kim et al. 2006). Additionally, it is known that fenpyroximate is more toxic to mite larvae because the decline in oxygen consumption and ATP production (MET inhibition) causes disruption of molting (Lummen 1998). Kim and collaborators (2006) showed similar effects for P. plumifer. Their bioassays demonstrated high toxicity of fenpyroximate to developmental stages of this phytoseiid compared with other

acaricides with the same mode of action, such as pyridaben. Under laboratory conditions, the estimated median lethal concentration (LC50) is widely used to evaluate the level of toxicity of plant-protection products to different arthropod pests (Throne et al. 1995, Yu 2008). However, 50% control is inadequate for field production and most growers require 90% suppression (Emden et al. 2004, Yu 2008, Hoy 2011). Therefore, to approximate levels of toxicity measured under artificial conditions to agricultural crops (e.g., open field or protected agriculture), the estimated values of LC90 are considered. By contrast, when side effects of pesticides are evaluated on beneficial arthropods in laboratory conditions, LC50 values represent concentrations that may not suppress populations of natural enemies (Yu 2008). In this study, the estimated values of LC50 demonstrated that even one-eighth of the field rate (0.025 ml EC/50 ml water) killed half of A. swirskii females after 48 h. The estimated LC90 value was close to the highest concentration evaluated (0.178 ml EC/50 ml water). Based on these results, it may be inferred that the average field rate used by fruit and vegetable producers in Florida (0.208 ml EC/50 ml water) may kill 90% of A. swirskii individuals if they are present on crops where fenpyroximate has been sprayed and complete coverage is achieved. Nevertheless, results obtained from semiartificial conditions are not necessarily translated into effects in crop fields (Yu 2008, Hoy 2011). Environmental factors such as sunlight, temperature, wind, and rain affect the degree of degradation and coverage of the acaricide. Also, characteristics of the crop, such as the irrigation system (overhead vs. drip) and behavior of natural enemies, may affect the degree of toxicity of fenpyroximate toxicity in the field, thus making it difficult to relate laboratory estimations to field conditions (Hoy and Ouyang 1986, Colomer et al. 2011, Hoy 2011).

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Fig. 2. Effects of fenpyroximate on A. swirskii female fecundity. (A) Mean ( 6 SE) number of eggs laid per female of A. swirskii exposed to fresh residues of fenpyroximate at 0-, 0.125-, 0.25-, 0.5-, and 1-fold of the average field rate 120 h after treatment. Data were compared using a one-way ANOVA. Differences identified using a Tukey’s mean separation test are represented by lowercase letters above columns. (B) Mean ( 6 SE) number of eggs laid per A. swirskii female after 24, 48, 72, 96, or 120 h after treatment at each concentration.

The numbers of A. swirskii eggs declined 72 h after initiated the experiment due to the development of eggs to larvae. Hamedi and Fathipour (2006) showed similar results for P. plumifer exposed to fenpyroximate. This compound had minimal effect on egg hatchability of P. plumifer. Similarly, the reduction in egg numbers of P. plumifer females was only related to development of eggs into larvae. Amor et al. (2012) carried out laboratory and field trials to assess the toxicity of emamectin benzoate to A. swirskii. Their results contrasted with other studies that showed high toxicity of emamectin benzoate to A. swirskii females under laboratory conditions. A thorough evaluation of pesticide side effects should go through a multistep approach, including the assessment of the population dynamics of the organism and its ecosystem services (Desneux et al. 2006, Biondi et al. 2013). The purpose of conducting different forms of assessments (laboratory bioassays

and field trials) is not to contradict the results of other evaluations, but to create complementary knowledge that facilitates the understanding of insecticide toxicity in agricultural settings. At the end of the bioassay, no A. swirskii larvae survived on the highest concentration tested and only 9% survived at the 0.5-fold rate (Fig. 3). On the other hand, >50% of larvae survived after 120 h at the 0.125 - and 0.25-fold rates (Fig. 3). These survivors molted to protonymphs and were observed to be active and feeding only at the lowest concentration of residue. Assuming that all larvae that survived to the end of the bioassay had the capacity to molt into adults and reproduce normally, it can be inferred that populations of A. swirskii may recover from fenpyroximate applications. However, field studies are needed to confirm if A. swirskii populations may recover from fenpyroximate applications.

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Fig. 3. Percentage mortality of A. swirskii larvae exposed to fresh residues of fenpyroximate at the conclusion of the evaluation period (120 h). The overall P value from Fisher’s exact test (P < 0.05) was 0.0111, df ¼ 3 (the control was excluded from the analysis). The Dunn–Sidak adjustment was performed using the P values from the multiple pairwise Fisher’s exact test. Adjusted P values are shown above columns.

Phytoseiid mortality is closely related to the quantity and quality of food (Yu 2008, Messelink et al. 2010, Hoy 2011). During the bioassay, A. swirskii females and immatures were supplied with an abundant quantity of food. Nevertheless, survival capacity of A. swirskii may have been affected by the nutritional value of T. urticae. Thus, evaluations using different prey (whiteflies, thrips, broad mites) are recommended. Further studies, including evaluation of sublethal effects and population dynamics under semifield and field conditions, are required to clarify the level of compatibility of fenpyroximate to this phytoseiid species in vegetable production. Acknowledgments We thank Haleigh Ray and Aaron Pomerantz for their constructive comments on early drafts, Godfrey Maina for assistance in rearing the mites, Nick Larson for assistance with running the bioassays, and James Colee and Emmanuel A. Torres Quezada for their assistance in the statistical analyses. This research was supported in part by the University of Florida’s Gulf Coast Research and Education Research, Dean’s Matching Assistantship Program for stipend and tuition support.

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