Effects of insecticides, fipronil and imidacloprid, on the growth, survival, and behavior of brown shrimp Farfantepenaeus aztecus

English version

Autoři: Ali Abdulameer Al-Badran ^aff001; Masami Fujiwara ^aff001; Miguel A. Mora ^aff001
Působiště autorů: Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, Texas, United States of America ^aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223641

Souhrn

Increased use of pesticide is causing detrimental effects on non-target species worldwide. In this study, we examined the lethal and sub-lethal effects of fipronil and imidacloprid, two commonly used insecticides, on juvenile brown shrimp (Farfantepenaeus aztecus), one of the most commercially and ecologically important species in the United States. The effects of six concentrations of fipronil (0.0, 0.005, 0.01, 0.1, 1.0, and 3.0 μg/L) and six concentrations of imidacloprid (0.0, 0.5, 1.0, 15.0, 34.5, 320.0 μg/L) were tested in a laboratory. We examined five different endpoints: growth, moulting interval, survivorship, behavioral change, and body color change. Growth of shrimp was reduced significantly under higher concentrations of both insecticides. Under fipronil exposure, shrimp in control showed the shortest inter-moult interval (7.57 ± 2.17 day) compared with other treatments; similarly, in the imidacloprid experiment, moulting increased from 8.43 ± 2.52 day in control to 11.95 ± 4.9 day in 0.5 μg/L treatment. Higher concentrations of fipronil (1.0 and 3.0 μg/L) showed a 0.0% survival rate compared with 100% survival in the control and 0.005 μg/L treatment. Under imidacloprid, survivorship decreased from 100% in the control to 33.33% in the 320.0 μg/L treatment. The 96-h LC₅₀ of fipronil was 0.12 μg/L, which makes brown shrimp one of the most sensitive invertebrates to the pesticide. Changes in behavior and body color were observed under both insecticides after different durations of exposures depending on concentrations. We conclude that, at the corresponding EPA benchmark concentrations, fipronil had more lethal effects than imidacloprid, and imidacloprid had more sub-lethal effects than fipronil. Both effects are of serious concern, and we suggest monitoring is necessary in estuaries.

Klíčová slova:

Invertebrates – Shrimp – Water quality – Weight gain – Insecticides – Molting – Pesticides – Pest control

Zdroje

1. Oerke EC, Dehne HW. Safeguarding production—losses in major crops and the role of crop protection. Crop Protection. 2004;23(4):275–85.

2. Hayasaka D, Korenaga T, Suzuki K, Saito F, Sanchez-Bayo F, Goka K. Cumulative ecological impacts of two successive annual treatments of imidacloprid and fipronil on aquatic communities of paddy mesocosms. Ecotoxicol Environ Saf. 2012;80:355–62. doi: 10.1016/j.ecoenv.2012.04.004 22521688.

3. Elliott R, Barnes JM. Organophosphorus Insecticides for the Control of Mosquitos in Nigeria. Trials with Fenthion and Malathion Conducted by the WHO Insecticide Testing Unit in 1960–61. Bull Org mond Sante. 1963;28:35–54.

4. Aktar MW, Sengupta D, Chowdhury A. Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol. 2009 Mar;2(1):1–12. doi: 10.2478/v10102-009-0001-7 21217838.

5. Drees BM. How to Select, Apply, and Develop Insecticides for Imported Fire Ant Control. Texas A&M AgriLife Extension Service. 2014:8 p.

6. Clasen B, Loro VL, Cattaneo R, Moraes B, Lopes T, de Avila LA, et al. Effects of the commercial formulation containing fipronil on the non-target organism Cyprinus carpio: implications for rice-fish cultivation. Ecotoxicol Environ Saf. 2012 Mar;77:45–51. 22078114.

7. Roessink I, Merga LB, Zweers HJ, Van den Brink PJ. The neonicotinoid imidacloprid shows high chronic toxicity to mayfly nymphs. Environ Toxicol Chem. 2013;32(5):1096–100. doi: 10.1002/etc.2201 23444274.

8. Goulson D. REVIEW: An overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology. 2013;50(4):977–87.

9. Krupke CH, Long EY. Intersections between neonicotinoid seed treatments and honey bees. Curr Opin Insect Sci. 2015;10:8–13. doi: 10.1016/j.cois.2015.04.005 29588017

10. Pritchard JB. Aquatic toxicology: past, present, and prospects. Environ Health Perspect. 1993;100:249–57. doi: 10.1289/ehp.93100249 8354173

11. Laboy-Nieves EN, Schaffner FC, Abdelhadi AH, Goosen MFA. Environmental Management, Sustainable Development and Human Health. London, UK: CRC Press/Balkema; 2009.

12. Hayasaka D, Korenaga T, Sanchez-Bayo F, Goka K. Differences in ecological impacts of systemic insecticides with different physicochemical properties on biocenosis of experimental paddy fields. Ecotoxicology. 2012 Jan;21(1):191–201. doi: 10.1007/s10646-011-0778-y 21877228.

13. Shaw JR, Pfrender ME, Eads BD, Klaper R, Callaghan A, Sibly RM, et al. Daphnia as an emerging model for toxicological genomics. Adv Exp Biol. 2008;2:165–328.

14. Abbott LC. Selecting optimal animal models to investigate environmental toxicology. Poult Fish Wildl Sci. 2013;1.

15. Dai YJ, Jia YF, Chen N, Bian WP, Li QK, Ma YB, et al. Zebrafish as a model system to study toxicology. Environ Toxicol Chem. 2014 Jan;33(1):11–7. doi: 10.1002/etc.2406 24307630.

16. Ditty JG. Young of Litopenaeus setiferus, Farfantepenaeus aztecus and F. duorarum (Decapoda: Penaeidae): a re-assessment of characters for species discrimination and their variability. J Crustac Biol. 2011;31(3):458–67.

17. Montero JT, Chesney TA, Bauer JR, Froeschke JT, Graham J. Brown shrimp (Farfantepenaeus aztecus) density distribution in the Northern Gulf of Mexico: an approach using boosted regression trees. Fish Oceanogr. 2016;25(3):337–48.

18. NMFS. Commercial fisheries statistics. National Marine Fisheries Service. https://www.st.nmfs.noaa.gov/commercial-fisheries/commercial-landings/annual-landings-with-group-subtotals/index (Accessed: 5th July 2018). 2017.

19. Sheridan PF, Ray SM. Report of the workshop on the ecological interactions between shrimp and bottomfishes, April 1980. National Marine Fisheries Service (NMFS). Southeast Fisheries Center. Galveston, TX; 1981.

20. Fujiwara M, Zhou C, Acres C, Martinez-Andrade F. Interaction between Penaeid Shrimp and Fish Populations in the Gulf of Mexico: Importance of Shrimp as Forage Species. PloS one. 2016;11(11):e0166479. doi: 10.1371/journal.pone.0166479 27832213.

21. Chandler GT, CARY TL, Volz DC, Walse SS, Ferry JL, KLOSTERHAUS SL. Fipronil Effects on Estuarine Copepod (Amphiascus Tenuiremis) Development, Fertility, and Reproduction: A Rapid Life-Cycle Assay in 96-Well Microplate Format. Environmental Toxicology and Chemistry. 2004;23(1):117–24. doi: 10.1897/03-124 14768875

22. Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, et al. Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res Int. 2015;22(1):68–102. doi: 10.1007/s11356-014-3471-x 25223353

23. Simon-Delso N, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Chagnon M, Downs C, et al. Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environ Sci Pollut Res (). 2015;22:5–34.

24. Gunasekara AS, Truong T, Goh KS, Spurlock F, Tjeerdema RS. Environmental fate and toxicology of fipronil. Journal of Pesticide Science. 2007;32(3):189–99.

25. Mortensen SR, Holmsen JD, Weltje L. Fipronil should not be categorized as a "systemic insecticide": a reply to Gibbons et al. (2015). Environmental science and pollution research international. 2015 Nov;22(21):17253–4. doi: 10.1007/s11356-015-4719-9 26002371.

26. Overmyer JP, Mason BN, Armbrust KL. Acute toxicity of imidacloprid and fipronil to a nontarget aquatic insect, Simulium vittatum Zetterstedt cytospecies IS-7. Bull Environ Contam Toxicol. 2005;74(5):872–9. doi: 10.1007/s00128-005-0662-7 16097320

27. USEPA. New pesticide fact sheet: fipronil. United States Environmental Protection Agency. Office of Prevention, Pesticides and Toxic Substances. Washington DC. USA; 1996.

28. Raby M, Zhao X, Hao C, Poirier DG, Sibley PK. Chronic effects of an environmentally-relevant, short-term neonicotinoid insecticide pulse on four aquatic invertebrates. The Science of the total environment. 2018 Oct 15;639:1543–52. doi: 10.1016/j.scitotenv.2018.05.259 29929317.

29. Tisler T, Jemec A, Mozetic B, Trebse P. Hazard identification of imidacloprid to aquatic environment. Chemosphere. 2009;76(7):907–14. doi: 10.1016/j.chemosphere.2009.05.002 19505710.

30. Van Dijk TC, Van Staalduinen MA, Van der Sluijs JP. Macro-invertebrate decline in surface water polluted with imidacloprid. PloS one. 2013;8(5):e62374. doi: 10.1371/journal.pone.0062374 23650513.

31. McMahen RL, Strynar MJ, McMillan L, DeRose E, Lindstrom AB. Comparison of fipronil sources in North Carolina surface water and identification of a novel fipronil transformation product in recycled wastewater. The Science of the total environment. 2016 Nov 1;569–570:880–7. doi: 10.1016/j.scitotenv.2016.05.085 27378152.

32. Mize SV, Porter SD, Demcheck DK. Influence of fipronil compounds and rice-cultivation land-use intensity on macroinvertebrate communities in streams of southwestern Louisiana, USA. Environmental pollution. 2008 Mar;152(2):491–503. doi: 10.1016/j.envpol.2007.03.021 17706328.

33. Gan J, Bondarenko S, Oki L, Haver D, Li JX. Occurrence of fipronil and its biologically active derivatives in urban residential runoff. Environ Sci Technol. 2012;46(3):1489–95. doi: 10.1021/es202904x 22242791.

34. Ensminger MP, Budd R, Kelley KC, Goh KS. Pesticide occurrence and aquatic benchmark exceedances in urban surface waters and sediments in three urban areas of California, USA, 2008–2011. Environmental monitoring and assessment. 2013 May;185(5):3697–710. doi: 10.1007/s10661-012-2821-8 22899460.

35. Ruby A. Review of pyrethroid, fipronil and toxicity monitoring data from california urban watersheds. California Stormwater Quality Association (CASQA). 2013:90 p.

36. Jemec A, Tisler T, Drobne D, Sepcic K, Fournier D, Trebse P. Comparative toxicity of imidacloprid, of its commercial liquid formulation and of diazinon to a non-target arthropod, the microcrustacean Daphnia magna. Chemosphere. 2007;68(8):1408–18. doi: 10.1016/j.chemosphere.2007.04.015 17524455.

37. Main AR, Headley JV, Peru KM, Michel NL, Cessna AJ, Morrissey CA. Widespread use and frequent detection of neonicotinoid insecticides in wetlands of Canada’s Prairie Pothole Region. PloS one. 2014;9(3):e92821. doi: 10.1371/journal.pone.0092821 24671127.

38. Hook SE, Doan H, Gonzago D, Musson D, Du J, Kookana R, et al. The impacts of modern-use pesticides on shrimp aquaculture: An assessment for north eastern Australia. Ecotoxicol Environ Saf. 2018 Feb;148:770–80. doi: 10.1016/j.ecoenv.2017.11.028 29190596.

39. USEPA. Aquatic life benchmarks for pesticide registration Washington, DC. https://www.epa.gov/pesticide-science-and-assessing-pesticide-risks/aquatic-life-benchmarks-and-ecological-risk: Environmental Protection Agency; 2017 [cited 2018. https://www.epa.gov/pesticide-science-and-assessingpesticide-risks/aquatic-life-benchmarks-and-ecological-risk.

40. Sneck-Fahrer DA, East JW. Water-quality, sediment-quality, stream-habitat, and biological data for Mustang Bayou near Houston, Texas, 2004–05. U.S. Geological Survey, Interior USDot; 2007.

41. Al-Badran AA, Fujiwara M, Gatlin III DM, Mora MA. Lethal and sub-lethal effects of the insecticide fipronil on juvenile brown shrimp Farfantepenaeus aztecus. Scientific Reports. 2018.

42. Lovell T. Nutrition and Feeding of Fish. 2nd ed. New York, USA: Springer Science+Business Media, LLC; 1998.

43. Kollman W, Randall S. Interim Report of the Pesticide Chemistry Database. Environmental Protection Agency. Department of Pesticide Regulation. 1020 N Street, Sacramento, California. 95814–5604. EH 95–04. 45 p; 1995.

44. Lamers M, Anyusheva M, La N, Nguyen VV, Streck T. Pesticide Pollution in Surface- and Groundwater by Paddy Rice Cultivation: A Case Study from Northern Vietnam. CLEAN—Soil, Air, Water. 2011;39(4):356–61.

45. Greenberg L, Rust MK, Klotz JH, Haver D, Kabashima JN, Bondarenko S, et al. Impact of ant control technologies on insecticide runoff and efficacy. Pest Manag Sci. 2010;66(9):980–7. doi: 10.1002/ps.1970 20730990.

46. Starner K, Goh KS. Detections of the neonicotinoid insecticide imidacloprid in surface waters of three agricultural regions of California, USA, 2010–2011. Bull Environ Contam Toxicol. 2012 Mar;88(3):316–21. doi: 10.1007/s00128-011-0515-5 22228315.

47. USGS. Fipronil and degradation products in the rice-producing areas of the mermentau river basin, Louisiana, February–September 2000. Fact Sheet FS-010-03. US Geological Survey (USGS). 2003:6 p.

48. Wirth EF, Pennington PL, Lawton JC, DeLorenzo ME, Bearden D, Shaddrix B, et al. The effects of the contemporary-use insecticide (fipronil) in an estuarine mesocosm. Environ Pollut. 2004 Oct;131(3):365–71. doi: 10.1016/j.envpol.2004.03.012 15261399.

49. Fossen M. Environmental Fate of Imidacloprid. Environmental Monitoring. Department of Pesticide Regulation. 1001 I Street. Sacramento, CA 95812–4015. 16 p; 2006.

50. Gilliom RJ, Barbash JE, Crawford CG, Hamilton MC, Martin BT, Nakagaki N, et al. The Quality of Our Nation’s Waters—Pesticides in the Nation’s Streams and Ground Water, 1992–2001. U.S. Geological Survey Circular 1291. 2006:172 p.

51. USEPA. Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. United States Environmental Protection Agency. Office of Water. Washington DC. USA; 2002.

52. Shan Z, Wang L, Cai D, Gong R, Zhu Z, Yu F. Impact of fipronil on crustacean aquatic organisms in a paddy field-fishpond ecosystem. Bull Environ Contam Toxicol. 2003;70(4):746–52. doi: 10.1007/s00128-003-0046-9 12677386.

53. USEPA. Fipronil environmental fate and ecological effects assessment and characterization for section 18 registration of in-furrow applications to rutabaga and turnips. United States Environmental Protection Agency. Environmental Fate and Effects Division. 72 p (Washington DC. USA). 2007.

54. JMP. JMP® Pro. V. 13.1.0. SAS Institute Inc. Cary, North Carolina, U.S.A. 2016.

55. Lassuy DR. Species profiles: Life histories and environmental requirements (Gulf of Mexico), brown shrimp. U.S. Fish and Wildlife Service. Coastal Engineering Research Center. 1983:15 P.

56. Mensah PK, Palmer CG, Muller WJ. Lipid peroxidation in the freshwater shrimp Caridina nilotica as a biomarker of Roundup((R)) herbicide pollution of freshwater systems in South Africa. Water Sci Technol. 2012;65(9):1660–6. doi: 10.2166/wst.2012.060 22508130.

57. Rozas LP, Minello TJ, Miles MS. Effect of deepwater horizon oil on growth rates of juvenile penaeid shrimps. Estuar Coast. 2014;37:1403–14.

58. Stoughton SJ, Liber K, Culp J, Cessna A. Acute and chronic toxicity of imidacloprid to the aquatic invertebrates Chironomus tentans and Hyalella azteca under constant- and pulse-exposure conditions. Arch Environ Contam Toxicol. 2008 May;54(4):662–73. doi: 10.1007/s00244-007-9073-6 18214581.

59. Azevedo-Pereira HMVS, Lemos MFL, Soares AMVM. Behaviour and Growth of Chironomus riparius Meigen (Diptera: Chironomidae) under Imidacloprid Pulse and Constant Exposure Scenarios. Water, Air, & Soil Pollution. 2011;219(1–4):215–24.

60. Goff AD, Saranjampour P, Ryan LM, Hladik ML, Covi JA, Armbrust KL, et al. The effects of fipronil and the photodegradation product fipronil desulfinyl on growth and gene expression in juvenile blue crabs, Callinectes sapidus, at different salinities. Aquat Toxicol. 2017;186:96–104. doi: 10.1016/j.aquatox.2017.02.027 28282622.

61. Frontera JL, Vatnick I, Chaulet A, Rodriguez EM. Effects of glyphosate and polyoxyethylenamine on growth and energetic reserves in the freshwater crayfish Cherax quadricarinatus (Decapoda, Parastacidae). Arch Environ Contam Toxicol. 2011;61(4):590–8. doi: 10.1007/s00244-011-9661-3 21424220.

62. Gauquelin F, Cuzon G, Gaxiola G, Rosas C, Arena L, Bureau DP, et al. Effect of dietary protein level on growth and energy utilization by Litopenaeus stylirostris under laboratory conditions. Aquaculture. 2007;271(1–4):439–48.

63. Ecobichon DJ. Toxic effects of pesticides. In: Klaassen CD, editor. Casarett & Doull’s Toxicology: The Basic Science of Poisons. New York: McGraw-Hill; 1996. p. 782.

64. Morrissey CA, Mineau P, Devries JH, Sanchez-Bayo F, Liess M, Cavallaro MC, et al. Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: a review. Environ Int. 2015 Jan;74:291–303. doi: 10.1016/j.envint.2014.10.024 25454246.

65. Hasenbein S, Lawler SP, Geist J, Connon RE. The use of growth and behavioral endpoints to assess the effects of pesticide mixtures upon aquatic organisms. Ecotoxicology. 2015;24(4):746–59. doi: 10.1007/s10646-015-1420-1 25630500.

66. Minello TJ, Zimmerman RJ, Martinez EX. Mortality of Young Brown Shrimp Penaeus aztecus in Estuarine Nurseries. Transactions of the American Fisheries Society. 1989;118(6):693–708.

67. Baker R, Fujiwara M, Minello TJ. Juvenile growth and mortality effects on white shrimp Litopenaeus setiferus population dynamics in the northern Gulf of Mexico. Fisheries Research. 2014;155:74–82.

68. Lachaise F, Le Roux A, Hubert M, Lafont R. The molting gland of crustaceans: localization, activity, and endocrine control (Review). J Crustac Biol. 1993;13(2):198–234.

69. OECD. Detaild review paper on aquatic Arthropods in life cycle and two-generation toxicity tests. Organisation for Economic Co-operation and Development. 2005 (50):135 p.

70. Volz DC, Wirth EF, Fulton MH, Scott GI, Strozier E, Block DS, et al. Effects of fipronil and chlorpyrifos on endocrine-related endpoints in female grass shrimp (Palaemonetes pugio). Bull Environ Contam Toxicol. 2003;71(3):497–503. doi: 10.1007/s00128-003-8920-z 14567575

71. Baines D, Wilton E, Pawluk A, de Gorter M, Chomistek N. Neonicotinoids act like endocrine disrupting chemicals in newly-emerged bees and winter bees. Sci Rep. 2017 Sep 8;7(1):10979. doi: 10.1038/s41598-017-10489-6 28887455.

72. Key PB, Chung KW, Opatkiewicz AD, Wirth EF, Fulton MH. Toxicity of the insecticides fipronil and endosulfan to selected life stages of the grass shrimp (Palaemonetes pugio). Bull Environ Contam Toxicol. 2003;70(3):533–40. doi: 10.1007/s00128-003-0019-z 12592529.

73. Overmyer JP, Rouse DR, Avants JK, Garrison AW, DeLorenzo ME, Chung KW, et al. Toxicity of fipronil and its enantiomers to marine and freshwater non-targets. J Environ Sci Health, Part B. 2007;42(5):471–80.

74. Chaton PF, Ravanel P, Tissut M, Meyran JC. Toxicity and bioaccumulation of fipronil in the nontarget Arthropodan fauna associated with subalpine mosquito breeding sites. Ecotoxicol Environ Saf. 2002;52:8–12. doi: 10.1006/eesa.2002.2166 12051802

75. Leo JP, Minello TJ, Grant WE. Assessing Variability in Juvenile Brown Shrimp Growth Rates in Small Marsh Ponds: An Exercise in Model Evaluation and Improvement. Marine and Coastal Fisheries. 2018;10(3):347–56.

76. Adamack AT, Stow CA, Mason DM, Rozas LP, Minello TJ. Predicting the effects of freshwater diversions on juvenile brown shrimp growth and production: a Bayesian-based approach. Marine Ecology Progress Series. 2012;444:155–73.

77. Zein-Eldin ZP, Aldrich DV. Growth and Survival of Postlarval Penaeus aztecus under Controlled Conditions of Temperature and Salinity. Biological Bulletin. 1965;129(1):199–216.

78. Russo R, Becker JM, Liess M. Sequential exposure to low levels of pesticides and temperature stress increase toxicological sensitivity of crustaceans. The Science of the total environment. 2018 Jan 1;610–611:563–9. doi: 10.1016/j.scitotenv.2017.08.073 28822923.

79. Willming MM, Qin G, Maul JD. Effects of environmentally realistic daily temperature variation on pesticide toxicity to aquatic invertebrates. Environ Toxicol Chem. 2013 Dec;32(12):2738–45. doi: 10.1002/etc.2354 23955707.

80. Tu HT, Silvestre F, Phuong NT, Kestemont P. Effects of pesticides and antibiotics on penaeid shrimp with special emphases on behavioral and biomarker responses. Environ Toxicol Chem. 2010 Apr;29(4):929–38. doi: 10.1002/etc.99 20821523.

81. Raley-Susman KM. Like a Canary in the coal mine: behavioral change as an early warning sign of neurotoxicological damage. In: Soloneski S, editor. Pesticides—Toxic Aspects inTech; 2014. p. 29 p.

82. Stratman KN, Wilson PC, Overholt WA, Cuda JP, Netherland MD. Toxicity of fipronil to the midge, Cricotopus lebetis Sublette. J Toxicol Environ Health, Part A. 2013;76(12):716–22. doi: 10.1080/15287394.2013.802266 23980838.

83. Roque A, Abad S, Betancourt-Lozano M, de la Parra LM, Baird D, Guerra-Flores AL, et al. Evaluation of the susceptibility of the cultured shrimp Litopenaeus vannamei to vibriosis when orally exposed to the insecticide methyl parathion. Chemosphere. 2005;60(1):126–34. doi: 10.1016/j.chemosphere.2005.01.008 15910911.

84. Martinez A, Romero Y, Castillo T, Mascaro M, Lopez-Rull I, Simoes N, et al. The effect of copper on the color of shrimps: redder is not always healthier. PloS one. 2014;9(9):e107673. doi: 10.1371/journal.pone.0107673 25229639.

85. O’Halloran MJ. Color control in shrimp. In: Goldman CA, editor. Tested Studies for Laboratory Teaching. 111990. p. 15–26.

86. Fernlund P, Josefsson L. Crustacean color-change hormone: amino acid sequence and chemical synthesis. Science. 1972;177(4044):173–5. doi: 10.1126/science.177.4044.173 5041363

87. Fingerman M, Jackson NC, Nagabhushanam R. Hormonally-regulated functions in crustaceans as biomarkers of environmental pollution (Review). Comp Biochem Physiol Part C. 1998;120:343–50.

Effects of insecticides, fipronil and imidacloprid, on the growth, survival, and behavior of brown shrimp Farfantepenaeus aztecus

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