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Toxicity and risk of permethrin and naled to non-target insectsafter adult mosquito management Jerome J. Schleier III • Robert K. D. Peterson Accepted: 14 April 2010Ó Springer Science+Business Media, LLC 2010 We derived laboratory LC50 values, assessed and naled most likely will not result in population impacts non-target insect risks, and conducted a field bioassay for on medium- to large-bodied insects.
ultra-low-volume (ULV) aerosol applications of insecti-cides used to manage adult mosquitoes. The house cricket, Indicator species  LC50  Mosquito control  Acheta domesticus (L.), was used as an indicator species Organophosphate  Pyrethroid for medium- to large-bodied ground dwelling insects. The24-h LC50 values for PermanoneÒ (formulated product ofpermethrin), Permanone ? piperonyl technical grade permethrin, and technical grade permeth-rin ? PBO ranged from 0.052 to 0.9 lg/cm2. The 24 h West Nile virus (WNV), a mosquito-borne arbovirus, has LC50 for technical grade naled and TrumpetÒ (formulated become endemic to North America and disease cases occur product of naled) were 0.038 and 0.44 lg/cm2, respec- throughout the virus transmission season. Since the arrival tively. The synergist ratio was 2.65 for Permanone ? PBO of WNV, more areas of the country have experienced and 1.57 for technical grade permethrin ? PBO. The tox- icity of technical grade permethrin was about 10-fold (ULV) aerosol applications of insecticides are used to greater than Permanone. A risk assessment using modeled manage high densities of adult mosquitoes and are the estimated environmental concentrations resulted in risk minimum effective volume of insecticide that is used as an quotients (RQ) that exceeded regulatory levels of concern, outdoor space spray. Currently, adult mosquito management but when compared to field-derived actual environmental utilizes pyrethroids and pyrethrins ((Z)-(S)-2-methyl-4-oxo- concentrations RQs did not exceed a regulatory level of concern, except in the case of technical grade naled. These results were expected because higher tiered risk assess- with piperonyl butoxide (PBO; 5-[2-(2-butoxyethoxy)eth- ments using field-verified data generally lead to lower risk estimates. Field bioassays using caged crickets showed no phate insecticides (Rose ).
significant mortality for permethrin or naled after a single The insecticides commonly used for mosquito man- truck-mounted ULV application. The results of the risk agement are highly toxic to non-target organisms like assessment using actual environmental concentrations are aquatic and terrestrial invertebrates and aquatic vertebrates, supported by the field bioassays and suggest that a single and there have been concerns about the effect of ULV ULV application of synergized or unsynergized permethrin applications on these organisms (Amweg et al. Daviset al. ; Paul and Simonin Paul et al. ;Schleier III et al. Weston et al. Pyrethrins, J. J. Schleier III (&)  R. K. D. Peterson pyrethroids, and organophosphate ULV insecticide sprays Department of Land Resources and Environmental Sciences, have had detrimental effects on non-target organisms like Montana State University, 334 Leon Johnson Hall, Bozeman, honey bees (Caron Hester et al. Pankiw and MT 59717-3120, USAe-mail: [email protected] Jay Womeldorf et al. ; Zhong et al. J. J. Schleier III, R. K. D. Peterson Aerial applications of ULV malathion (O,O-dimethyl di- from lower to higher tiered assessments for non-target thiophosphate of diethyl mercaptosuccinate) significantly organisms (Giddings et al. Peterson ; Schleier decreased populations of certain Hymenoptera (Hill et al.
III et al. Therefore we compared estimated envi- ). However, the aerial applications did not signifi- ronmental concentrations to actual environmental concen- cantly affect Hemiptera, Coleoptera, and Diptera (exclud- trations to demonstrate the change in risk when higher ing Culicidae) populations (Hill et al. ).
tiered assessments are performed.
Materials and methods impact on aquatic macroinvertebrates and Gambusia affinis(Baird and Girard) when used above wetlands, but did have Laboratory bioassay a significant impact on small flying insects (Jensen et al.
). Flying insect populations, though, recovered within 48 h after the initial application. Aerial ULV applications SD = 51.71 mg) were obtained from Big Apple Herpeto- with pyrethrins and PBO had no significant impact on caged logical (Hauppauge, NY, USA) for both the laboratory and medium- to large-bodied insects within the spray zone, but field experiments. House crickets were chosen for the lab researchers observed an impact on smaller-bodied insects and field experiments because they are considered to be (Boyce et al. ). Davis et al. (found that the one of the best indicators of environmental pollution exposures to mammals, birds, and aquatic vertebrates and because they are more susceptible than other species of invertebrates most likely would not result in risks that invertebrates (Antwi and Peterson ; Bass ; Brie- exceed regulatory levels of concern after truck-mounted ger et al. ; Harris ; Hoffmann et al. Tietze ULV applications. Davis and Peterson ) demonstrated that there was little to no significant impact on aquatic and Technical grade permethrin (98% purity) and synergist terrestrial invertebrates after single and multiple applica- PBO (98.2% purity) were obtained from Sigma-Aldrich tions of permethrin or d-phenothrin (3-(phenoxy)phenyl] (St. Louis, MO, USA), PermanoneÒ 10% emulsified concentrate (EC) (permethrin) was obtained from Bayer propane-1-carboxylate) used for adult mosquito manage- Environmental Science (Research Triangle Park, NC, ment. Lawler et al. (found that the use of ULV USA), TrumpetÒ EC (naled; 1,2-dibromo-2,2-dichloroeth- pyrethrins synergized with PBO did not cause significant yl dimethyl phosphate) was obtained from the AMVAC mortality of the aquatic invertebrates, Daphnia magna Corporation (Los Angeles, CA, USA), and technical grade Straus and Callibaetis californicus Banks. However, truck- naled (98.2% purity) was obtained from Chem Service mounted ULV applications of malathion have been shown (West Chester, PA, USA). Gas chromatograph analysis of to have a significant effect on house crickets, Acheta Permanone and Trumpet showed that the percent active domesticus Linnaeus in a peridomestic setting (Tietze et al.
ingredient in the formulations is 10.05 and 78%, respec- ), causing 12.5–48.7% mortality, depending on the tively. Stock solutions for technical grade permethrin, location in residential yards.
technical grade permethrin ? PBO (1:1 technical grade There have been few studies examining the effects of permethrin/PBO), Permanone, Permanone ? PBO (1:1 truck-mounted ULV applications on non-target ground Permanone/PBO), Trumpet, and technical grade naled dwelling organisms. In addition, there are few data on non- were prepared for each experiment in high pressure liquid target arthropods with respect to toxicity and risks associ- chromatography acetone (99.7% purity; EMD Chemicals, ated with insecticides used for adult mosquito management.
Gibbstown, NJ, USA). Concentrations of Permanone were Therefore, the objectives of our study were to determine the based on 0.84 kg/l, the amount of permethrin in the for- susceptibility of house crickets to permethrin and naled, and mulation. Concentrations of Trumpet were based on perform an ecological risk assessment using the house 1.29 kg/l, the amount of naled in the formulation.
cricket as a surrogate for medium- to large-bodied ground The LC50 was determined under laboratory conditions dwelling arthropods. In addition to the toxicity testing and using methods similar to those of Snodgrass ) and risk assessment, caged crickets were placed in the field to Antwi and Peterson ). Acetone solutions of the dif- determine if the insecticide applications caused significant ferent active ingredients listed above were applied in 20-ml glass scintillation vials with a total inside surface area of Despite the well known approaches in risk assessment of 40.26 cm2 (Thermo Fisher Scientific Inc., Waltham, MA, tiers, recursiveness, and refinement (NRC ; SETAC USA). A 0.5-ml aliquot of test solution was dispensed into ), surprisingly few studies have been conducted and individual glass vials. Acetone was used as the control.
published that quantitatively characterize the change in risk Vials were placed on hot dog rollers (model HDR-565, The Toxicity and risk of permethrin and naled to non-target insects Helman Group, Ltd., Oxnard, CA, USA) and rotated Significant differences (p B 0.05) between permethrin and mechanically so that the acetone dried and the insecticide naled LC50 estimates were determined by the LC50 ratio was uniformly coated in the vial. One insect was placed in test of Wheeler et al. ).
each vial and covered with a perforated cap, without diet.
Treated vials were placed on large plastic trays and left on the laboratory bench (21.28 ± 0.04°C, photoperiod of 16:8[L:D] h). Mortality was assessed at 24 h, and insects that The study occurred in conjunction with the Cascade did not move when stimulated with forceps were consid- County Weed and Mosquito Control District outside ered dead. All combinations of permethrin were run at the of Cascade (N47°13.4890, W111°42.0400), and Ulm same time so that differences between the treatments and (N47°25.4020, W111°29.7670), MT, USA during the sum- times could be analyzed.
mers of 2007 and 2008, respectively. In 2007 only Trumpet To establish the concentration-mortality relationships (formulated product of naled) was applied, while in 2008 the experiments were performed four times so that dose– both Permanone and Trumpet were applied. Each insecti- response curves could be produced. The experimental cidal product was applied once per year in late July or early design for the permethrin experiments was a complete August (Schleier III and Peterson ). A truck was randomized block with eight vials (individuals) per con- equipped with a Bison (VecTec Inc., Orlando, FL, USA) centration, 12 concentrations (blocks), and four treatments ULV generator. Permanone 10% EC was mixed 1:1 with (technical grade, technical grade ? PBO, Permanone, and BVA oil (BVA Inc. Wixom, MI, USA) and was applied at Permanone ? PBO). The experimental design for the the maximum application rate of 7.85 g active ingredient naled experiments was a complete randomized block with (ai)/ha with a flow rate of 205 ml/min. Trumpet was eight vials (individuals) per concentration, 12 concentra- applied undiluted at the maximum application rate of tions (blocks), and two treatments (technical grade naled 22.42 g ai/ha with a flow rate of 44.36 ml/min. Schleier III and Trumpet).
and Peterson (provide further information on the To establish the concentration-mortality relationships for Permanone and Permanone mixed with PBO, insects Approximately 15 adults were placed in a 25-cm 9 were exposed to 12 concentrations with 32 individuals 25-cm 9 8-cm mesh wire screen cage. One cage of exposed at each concentration: 0, 0.026, 0.078, 0.13, 0.16, crickets was placed on the ground 25, 50, and 75 m from 0.19, 0.26, 0.65, 0.78, 1.04, 1.3, and 2.6 lg/cm2. To the spray truck. There were three sample replicates with establish the concentration-mortality relationships for 200 m buffer zones between replicates. Three cages of technical grade permethrin and technical grade permethrin crickets were placed in a control area located where no mixed with PBO, insects were exposed to 12 concentra- spraying or drift could occur, but were subjected to the tions with 32 individuals exposed at each concentration: 0, same meteorological conditions as the residue samples.
0.015, 0.031, 0.037, 0.07, 0.093, 0.12, 0.16, 0.19, 0.23, Cricket mortality was assessed 2 h after application 0.31, and 0.78 lg/cm2. Concentration-mortality relation- because of low overnight temperatures. BoxCox transfor- ships were established for technical grade naled and mations were run on mortality to determine the correct Trumpet using 12 concentrations with 32 individuals transformation. Analysis of variance (a = 0.05) was run on exposed at each concentration: 0, 0.0078, 0.016, 0.0548, mortalities that were transformed by ln(y ? 1) to deter- 0.078, 0.12, 0.2, 0.24, 0.32, 0.39, 0.79, and 1.59 lg/cm2.
mine differences between crickets in the treated and controlareas.
Non-target insect risk assessment Abbott's formula was used to correct for control mortality(Abbott Perry et al. ). Synergist ratios were Ecological risk assessment can be described in quantitative calculated by dividing the unsynergized LC50 by the syn- terms as a function of toxicity and exposure (NRC ; ergized LC50 (Casabe et al. Data were analyzed USEPA The LC50 values at 24 h were compared using Statistical Analysis System 9.1 (SAS Institute, Cary, with the actual environmental concentrations (AEC) mea- NC, USA) and dose-mortality regressions were estimated sured by Schleier III and Peterson (and estimated by probit analysis (PROC PROBIT). However, for Per- environmental concentrations (EEC) from the industrial manone the poor fit of the model was accounted for by source complex dispersion model version 3 (ISCST3; multiplying the variances by a heterogeneity factor (v2/k - 2), where k is the number of concentrations to been used to estimate the ground deposition concentrations account for extra-binomial variations that causes poor fit of insecticides after ULV applications in previous risk (Hoekstra Robertson et al. Williams assessments (Davis et al. Macedo et al. ; J. J. Schleier III, R. K. D. Peterson Peterson et al. ; Schleier III et al. , and has in Table . There was generally a good fit to the model been shown to be a sufficiently conservative model for assumptions. Technical grade permethrin alone and syn- conducting lower tiered risk assessments (Schleier III and ergized was significantly more toxic than the permethrin in Permanone alone and synergized. The addition of PBO did Peterson et al. (and Davis et al. ) contain not significantly increase the toxicity of Permanone or more information on the ISCST3 modeling assumptions, technical grade permethrin. The 24 h LC50 values for which are briefly reviewed here. The assumptions included: Permanone, Permanone ? PBO, technical grade permeth- (a) permethrin had a 24-h half-life in the air and naled had rin, and technical grade permethrin ? PBO ranged from a 18-h half-life; (b) the insecticides were applied at the 0.052 to 0.9 lg/cm2 (Table ). The synergist ratio of Per- maximum application rate as stated on each label; (c) all of manone ? PBO and technical grade permethrin ? PBO the insecticides were susceptible to the same weather was 2.65 and 1.57, respectively. The 24 h LC50 for conditions using standardized weather data from Salem, technical grade naled and Trumpet were 0.038 and Massachusetts, USA, from the year 1988; (d) all spray 0.44 lg/cm2, respectively.
events occurred at 2100 h; (e) each spray was released at1.5 m; and (f) deposition concentrations were estimated 25 m from the spray source.
Actual environmental concentrations of permethrin and There was no significant difference in mortality between naled were measured by Schleier III and Peterson ( crickets in the control and treated areas for the Permanone The applications took place in open fields with no vege- (F = 0.08, p = 0.78) and naled spray events (F = 1, tation taller than 20 cm, to represent a worst-case assess- p = 0.33). During the 2007 naled application, average ment of ground deposition. Within each study site, surface mortality was 18% in the treated area and 10% in the control residue samples were taken. Three replicates with 200 m area. During the 2008 permethrin application, average buffer zones between replicates were used. The collection mortality was 5% in the treated area and 6% in the control of surface residues at ground level were performed using area. During the 2008 naled application, average mortality 10 cm 9 10 cm (100 cm2) cotton dosimeters pinned to a was 1% in the treated area and 3% in the control area.
piece of cardboard at 25 m from the spray truck and werecollected 1 h after application.
The average deposition concentrations 25 m from the spray truck for permethrin estimated by ISCST3 and AECs Environmental concentrations estimated by ISCST3 resul- were 0.18 and 0.0024 lg/cm2, respectively. The average ted in RQs that exceeded the LOC for Permanone ? PBO, deposition concentrations 25 m from the spray truck of technical grade permethrin, technical grade permeth- naled estimated by ISCST3 and AECs were 0.34 and rin ? PBO, technical grade naled, and Trumpet, but Per- 0.036 lg/cm2, respectively.
manone alone did not exceed the RQ LOC (Table Risk We used the risk quotient (RQ) method for estimating quotients using the EECs exceeded the RQ LOC, which risk, which is calculated by dividing the deposition con- were about 10- to 100-fold greater than the RQs using centration by the LC50. Estimated RQs typically are com- AECs (Table The RQ for technical grade naled pared to a RQ level of concern (LOC) which is set by the exceeded the RQ LOC when using AECs (Table ).
United States Environmental Protection Agency (USEPA)or another regulatory agency to determine if regulatoryaction is needed. The RQ LOC used for our assessment was 0.5 (USEPA An RQ C 0.5 means the esti-mated exposure is C50% of the LC50. To assess the change When examining the risks of insecticides to non-target in risk when higher tiered risk assessments are performed arthropods, it is important to consider the AECs of insec- we compare the RQ for the AECs and EECs.
ticides and the toxicity of the formulated products. In theirecological risk assessment, Davis et al. () used theconservative model ISCST3 to estimate concentrations of mosquito insecticides that would be deposited on theground. The concentrations estimated by ISCST3 were 75 and 9.5 times greater for permethrin and naled than theAECs used in this study, respectively (Schleier III and The LC50 values for Permanone, Permanone ? PBO, Peterson ). The RQs for synergized Permanone, syn- technical grade permethrin, technical grade permeth- ergized and unsynergized technical grade permethrin, rin ? PBO, technical grade naled, and Trumpet are given technical grade naled, and Trumpet exceeded the RQ LOC Toxicity and risk of permethrin and naled to non-target insects Table 1 The 24 h lethal concentrations that kill 50% of a population (LC50) for house crickets treated with PermanoneÒ (formulated product ofpermethrin), Permanone and piperonyl butoxide (PBO), technical permethrin, technical permethrin and PBO, technical naled, TrumpetÒ(formulated product of naled) Technical permethrin Technical permethrin ? PBO a Standard errorb 95% confidence interval for the LC50c Degrees of freedomd Piperonyl butoxide Table 2 Risk quotients (deposition concentration/LC50) for the insecticide was coated on the inside of glass vials so that actual environmental concentration (AEC) from Schleier III and the house crickets were in constant contact with the Peterson () and estimated environmental concentrations modeled insecticide. However, in the field non-target organisms with ISCST3b for PermanoneÒ (formulated product of permethrin),Permanone ? piperonyl butoxide (PBO), technical grade permethrin, most likely are not in constant contact with the insecticide.
technical grade permethrin ? PBO, technical grade naled, and In addition, house crickets have been shown to be more TrumpetÒ (formulated product of naled) at 24 h sensitive to pyrethroid insecticides than smaller non-target organisms such as adult convergent lady beetles, Hippod-amia convergens (Gue´rin-Me´neville) (Antwi and Peterson The toxicity of technical grade permethrin was about Technical grade permethrin 10-fold greater than Permanone. Previous studies have Technical grade permethrin ? PBO shown that the cis-isomer of permethrin is more toxic than Technical grade naled the trans-isomer (Alzogaray et al. ). However, the increased toxicity of the technical grade cannot be a Piperonyl butoxide explained by this fact because technical grade permethrin b The industrial source complex dispersion model version 3 contained 26.4% cis-isomer, while the Permanone formu-lation contained 35%. Stevens et al. (found that when compared to the EECs of ISCST3. However, when technical grade organophosphates have a higher toxicity the AECs were used, the RQs for all insecticide combi- than the formulated products. Paul et al. (and Coats nations were below the RQ LOC, except for technical and O'Donnell-Jeffery ) found that technical-grade grade naled.
pyrethroids can be two to nine times more toxic than the There have been few studies examining the change in formulated product to fish. The increased toxicity of risk as more refined risk assessments are performed. Not technical grade permethrin could be due to a more rapid surprisingly, our estimates of risks for non-target ground penetration through the cuticle because high boiling point dwelling arthropods using AECs were lower than the risks oils and emulsifiers like those in Permanone can slow the using EECs. These results are expected because higher penetration of pyrethroid insecticides (Coats and O'Don- tiered risk assessments using field verified data generally nell-Jeffery ; Matsumura Pree et al. ).
lead to lower risk estimates which has been observed for The toxicity of permethrin to house crickets is similar to aerial applications of ULV insecticides (Schleier III et al.
that of adult tarnished plant bugs, Lygus lineolaris (Palisot ). Our results were supported by the field bioassay de Beauvois), green stink bugs, Acrosternum hilare (Say), showing no significant difference in mortality between and southern green stink bugs, Nezara viridula (L.), using crickets in the control and treated areas for either the methods similar to our study (Snodgrass ; Snodgrass Permanone or Trumpet treatments.
et al. The LC50 values for technical grade per- Although we used AECs to estimate risks, the RQs most methrin ? PBO were similar to technical grade resmethrin likely still overestimate the risks to non-target ground dwelling insects. For example, to derive the LC J. J. Schleier III, R. K. D. Peterson d-phenothrin synergized with PBO (Antwi and Peterson Amweg EL, Weston DP, You J, Lydy MJ (2006) Pyrethroid insecticides and sediment toxicity in urban creeks from Califor-nia and Tennessee. Environ Sci Technol 40:1700–1706 Piperonyl butoxide is commonly used with pyrethroids Antwi FB, Peterson RKD (2009) Toxicity to non-target insects after for mosquito management because it can suppress or delay exposure to d-phenothrin and resmethrin. Pest Manag Sci the onset of resistance to pyrethroids and pyrethrins as well as reduce the concentration needed to have a lethal effect Bass EL (1986) Use of the cricket Acheta domestica L. as a bioassay organism for the toxic extract from Gonyaulax monilata (Farnham ; Xu et al. ). The results of our study (dinophyceae). J Phycol 22:546–548 showed a synergist ratio of 1.57 to 2.65, which is similar to Boyce WM, Lawler SP, Schultz JM, McCauley SJ, Kimsey LS, previous studies (De Vries and Georghiou ; Gist and Niemela MK, Nielsen CF, Reisen WK (2007) Nontarget effects Pless ; Pree et al. ).
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