Abstract
Natural resource managers are concerned about the impacts of aerial ultra-low volume spray (ULV) of insecticides for mosquito control (i.e., mosquito adulticides) and seek science-driven management recommendations that reduce risk but allow vector control for nearby human populations. Managers at the National Key Deer Refuge (Florida Keys, FL) are concerned for ULV effects upon conservation efforts for imperiled butterflies (Florida leafwing [Anaea troglodyta floridalis] and Bartram’s hairstreak [Strymon acis bartrami] butterflies). No-spray zones were designated for protection of those butterflies, but their effectiveness for mitigation is unclear. To address this uncertainty, cholinesterase activity (ChE) and mortality were monitored for caged butterflies gulf fritillary [Agraulis vanilla] and great southern white [Ascia monuste]) deployed on the Refuge during three aerial ULV applications of the insecticide naled. Residue samplers also were deployed to estimate butterfly exposure. Spray efficacy against mosquitoes was assessed by deploying caged mosquitoes at the same locations as the butterflies. Average naled residue levels on filter paper samplers in the target area (1882–2898 µg/m2) was significantly greater than in the no-spray zone (9–1562 µg/m2). Differences between the no-spray zone and target area for butterfly mortality and ChE were inconsistent. Average mortality was significantly lower, and average ChE was significantly higher in the no-spray zone for larvae of one species but not for larvae of the other species. Mosquito mortality did not differ significantly between the two areas. Data from the present study reflect the inconsistent effectiveness of no-spray zones on the Refuge using standard methods employed at the time by the vector control agency in the Florida Keys and possibly by other vector control agencies in similar coastal environments. Furthermore, these findings helped to guide the design and to improve the conservation value of future no-spray zone delineations while allowing for treatment in areas where mosquito control is necessary for vector-borne disease reduction.
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References
Bargar TA (2012a) The relationship between total cholinesterase activity and mortality in four butterfly species. Environ Toxicol Chem 31:2124–2129. https://doi.org/10.1002/etc.1927
Bargar TA (2012b) Risk assessment for adult butterflies exposed to the mosquito control pesticide naled. Environ Toxicol Chem 31:885–891. https://doi.org/10.1002/etc.1757
Bargar TA, Sowers A, Anderson CR (2020) Cholinesterase inhibition in butterflies on the National Key Deer Refuge following aerial application of a mosquito control pesticide: U.S. Geological Survey data release. https://doi.org/10.5066/F74X55ZP
Brewer SK, Little EE, DeLonay AJ, Beauvais SL, Jones SB, Ellersieck MR (2001) Behavioral dysfunctions correlate to altered physiology in rainbow trout (Oncoryncus mykiss) exposed to cholinesterase-inhibiting chemicals. Arch Environ Contam Toxicol 40:70–76. https://doi.org/10.1007/s002440010149
Colovic MB, Krstic DZ, Lazarevic-Pasti TD, Bondzic AM, Vasic VM (2013) Acetylcholinesterase inhibitors: pharmacology and toxicology. Curr Neuropharmacol 11:315–335
Coluzzi M (1964) Maintenance of laboratory colonies of Anopheles mosquitos. B World Health Organ 31:441–443
Cooper NL, Bidwell JR (2006) Cholinesterase inhibition and impacts on behavior of the Asian clam, Corbicula fluminea, after exposure to an organophosphate insecticide. Aquat Toxicol 76:258–267. https://doi.org/10.1016/j.aquatox.2005.09.012
Coppage DL, Matthews E (1975) Brain-acetylcholinesterase inhibition in a marine teleost during lethal and sublethal exposures to 1,2-dibromo-2,2-dichloroethyl dimethyl phosphate (naled) in seawater. Toxicol Appl Pharmacol 31:128–133. https://doi.org/10.1016/0041-008X(75)90060-5
Day KE, Scott IM (1990) Use of acetylcholinesterase activity to detect sublethal toxicity in stream invertebrates exposed to low concentrations of organophosphate insecticides. Aquat Toxicol 18:101–114. https://doi.org/10.1016/0166-445X(90)90021-G
Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
Fildes K, Astheimer LB, Story P, Buttemer WA, Hooper MJ (2006) Cholinesterase response in native birds exposed to fenitrothion during locust control operations in eastern Australia. Environ Toxicol Chem 25:2964–2970. https://doi.org/10.1897/05-585r.1
Fukuto TR (1990) Mechanism of action of organophosphorus and carbamate insecticides. Environ Health Perspect 87:245–254
Goldstein MI, Lacher TE Jr, Zaccagnini ME, Parker ML, Hooper MJ (1999) Monitoring and assessment of Swainson’s hawks in Argentina following restrictions on monocrotophos use, 1996–1997. Ecotoxicology 8:215–224. https://doi.org/10.1023/A:1026448415467
Harburguer L, Seccacini E, Licastro S, Zerba E, Masuh H (2012) Droplet size and efficacy of an adulticide-larvicide ultralow-volume formulation on Aedes aegypti using different solvents and spray application methods. Pest Manag Sci 68:137–141. https://doi.org/10.1002/ps.2237
Hill EF (1988) Brain cholinesterase activity of apparently normal wild birds. J Wildlife Dis 24:51–61. https://doi.org/10.7589/0090-3558-24.1.51
Hilz E, Vermeer AWP (2013) Spray drift review: the extent to which a formulation can contribute to spray drift reduction. Crop Prot 44:75–83. https://doi.org/10.1016/j.cropro.2012.10.020
Hoang TC, Rand GM (2015) Mosquito control insecticides: a probabilistic ecological risk assessment on drift exposures of naled, dichlorvos (naled metabolite) and permethrin to adult butterflies. Sci Total Environ 502:252–265. https://doi.org/10.1016/j.scitotenv.2014.09.027
Hoang TC, Pryor RL, Rand GM, Frakes RA (2011) Use of butterflies as nontarget insect test species and the acute toxicity and hazard of mosquito control insecticides. Environ Toxicol Chem 30:997–1005. https://doi.org/10.1002/etc.462
Hooper MJ, Detrich PJ, Weisskopf CP, Wilson BW (1989) Organophosphorous insecticide exposure in hawks inhabiting orchards during winter dormant-spraying. B Environ Contamin Tox 42:651–659. https://doi.org/10.1007/bf01700383
Kumar A, Chapman JC (1998) Profenofos toxicity to the eastern rainbow fish (Melanotaenia duboulayi). Environ Toxicol Chem 17:1799–1806. https://doi.org/10.1002/etc.5620170920
Lothrop H, Lothrop B, Palmer M, Wheeler S, Gutierrez A, Miller P, Gomsi D, Reisen WK (2007) Evaluation of pyrethrin aerial ultra-low volume applications for adult Culex tarsalis control in the desert environments of the Coachella Valley, Riverside County, California. J Am Mosquito Control Assoc 23:405–419. https://doi.org/10.2987/5623.1
Ludke JL, Hill EF, Dieter MP (1975) Cholinesterase (ChE) response and related mortality among birds fed ChE inhibitors. Arch Environ Contam Toxicol 3:1–21. https://doi.org/10.1007/BF02221128
Martinez-Haro M, Vinuela J, Mateo R (2007) Exposure of birds to cholinesterase-inhibiting pesticides following a forest application for tick control. Environ Toxicol Pharmacol 23:347–349. https://doi.org/10.1016/j.etap.2006.11.011
Maul JD, Farris JL (2005) Monitoring exposure of northern cardinals, Cardinalis, to cholinesterase-inhibiting pesticides: enzyme activity, reactivations, and indicators of environmental stress. Environ Toxicol Chem 24:1721–1730. https://doi.org/10.1897/04-385r.1
Mazur A, Bodansky O (1946) The mechanism of in vitro and in vivo inhibition of cholinesterase activity by di-isopropyl fluorosphate. J Biol Chem 163:261–276
Morgan MJ, Fancey LL, Kiceniuk JW (1990) Response and recovery of brain acetylcholinesterase activity in Atlantic salmon (Salmo salar) exposed to fenitrothion. Can J Fish Aquat Sci 47:1652–1654. https://doi.org/10.1139/f90-188
Salvato MH (2001) Influence of mosquito control chemicals on butterflies (Nymphalidae, Lycaenidae, Hesperiidae) of the Lower Florida Keys. J Lepid Soc 55:8–14
Sugiura M, Horibe Y, Kawada H, Takagi M (2011) Effect of different droplet size on the knockdown efficacy of directly sprayed insecticides. Pest Manag Sci 67:1115–1123. https://doi.org/10.1002/ps.2157
Teske ME, Thistle HW, Mickle RE (2000) Modeling finer droplet aerial spray drift and deposition. Appl Eng Agric 16:351–357. https://doi.org/10.13031/2013.5216
Tietze NS, Shaffer KR, Hester PG (1996) Half-life of naled under three test scenarios. J Am Mosquito Control Assoc 12:251–254
USEPA (2006) Interim reregistration eligibility decision for naled. EPA-738-R-02-008. Prevention, Pesticides and Toxic Substances, Washington
USFWS (2014) Mosquito management plan Lower Florida Keys Wildlife Refuge Complex. U.S. Fish and Wildlife Service. https://www.fws.gov/nationalkeydeer/pdfs/20140310-MosquitoPlanEA.pdf. Accessed 8 May 2020
Varo I, Amat F, Navarro JC (2008) Acute toxicity of dichlorvos to Aphanius iberus (Cuvier & Valenciennes, 1846) and its anti-cholinesterase effects on this species. Aquat Toxicol 88:53–61. https://doi.org/10.1016/j.aquatox.2008.03.004
Weiss CM (1961) Physiological effect of organic phosphorous insecticides on several species of fish. Trans Am Fish Soc 90:143–152. https://doi.org/10.1577/1548-8659(1961)90%5b143:peoopi%5d2.0.co;2
Zhong H, Hribar LJ, Daniels JC, Feken MA, Brock C, Trager MD (2010) Aerial ultra-low-volume application of naled: impact on nontarget imperiled butterfly larvae (Cyclargus thomasi bethunebakeri) and efficacy against adult mosquitoes (Aedes taeniorhynchus). Environ Entomol 39:1961–1972. https://doi.org/10.1603/EN10089
Acknowledgments
This project would not have been possible without the assistance of Carla Wieser of the USGS and numerous biologists from the National Key Deer Wildlife Refuge and the Florida Keys Mosquito Control District. Drs. Harry Zhong and Richard Pierce provided analytical support for determination of pesticide residues. Many thanks to Shady Oak Butterfly Farm for providing, sometimes on short notice, all butterflies that were used during this project. Use of trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. Government.
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Bargar, T.A., Anderson, C. & Sowers, A. Mortality and Cholinesterase Inhibition in Butterflies Following Aerial Naled Applications for Mosquito Control on the National Key Deer Refuge. Arch Environ Contam Toxicol 79, 233–245 (2020). https://doi.org/10.1007/s00244-020-00745-8
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DOI: https://doi.org/10.1007/s00244-020-00745-8