Abstract
Pyriproxyfen is an insect growth regulator acting as larvicide against a large spectrum of public health insect pests, especially dipterans. It is also widely used in agriculture and horticulture for the control of many insect species. Disrupting the endocrine system by mimicking the activity of the juvenile hormone, pyriproxyfen interferes with metamorphosis in insects and prevents them from reaching maturity and reproducing. Because the aquatic ecosystems can be directly or indirectly contaminated by pyriproxyfen, the goal of this study was to establish the aquatic ecotoxicological profile of pyriproxyfen and to identify the gaps that need to be filled. Pyriproxyfen is photodegraded quickly in water. In the absence of organic matter, its persistence in aerobic water media is also limited especially with high temperature and sunlight. Analysis of the laboratory and in situ results for more than 60 aquatic algae, plants, invertebrates, and vertebrates shows that the toxicity of pyriproxyfen is highly variable including within a same taxonomical group. Abiotic and biotic factors can highly influence the toxicity of the molecule. Pyriproxyfen disrupts the development of numerous species and adversely impacts various physiological events. It can also disturb the behavior of the organisms such as their predatory and swimming performances. Although some experimental studies focus on the environmental fate of pyriproxyfen metabolites, those dealing with their aquatic ecotoxicity assessment are scarce. In the same way, the limited number of studies dealing with the search of pyriproxyfen residues in lake, river, and other natural aquatic media does not include the identification of the metabolites.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdu U, Barki A, Karplus I, Barel S, Takac P, Yehezkel G, Laufer H, Sagi A (2001) Physiological effects of methyl farnesoate and pyriproxyfen on wintering female crayfish, Cherax quadricarinatus. Aquaculture 202:163–175. https://doi.org/10.1016/S0044-8486(01)00596-8
AFSSET (2007) La lutte antivectorielle dans le cadre de l’épidémie de chikungunya sur l’île de la Réunion. Évaluation des risques et de l’efficacité des produits larvicides. Maisons-Alfort, Paris
Ali A, Nayar JK, Xue RD (1995) Comparative toxicity of selected larvicides and insect growth regulators to a Florida laboratory population of Aedes albopictus. J Am Mosq Control Assoc 11:72–76
Ali A, Chowdhury MA, Hossain ML, Mahmud UA, Habiba DB, Aslam AFM (1999) Laboratory evaluation of selected larvicides and insect growth regulators against field-collected Culex quinquefasciatus larvae from urban Dhaka, Bangladesh. J Am Mosq Control Assoc 15:43–47
Araújo MC, Assis CRD, Silva KCC, Souza KS, Azevedo RS, Alves MHME, Silva LC, Silva VL, Adam ML, Carvalho Junior LB, Souza Bezerra R, Oliveira MBM (2018) Characterization of brain acetylcholinesterase of bentonic fish Hoplosternum littorale: perspectives of application in pesticides and metal ions biomonitoring. Aquat Toxicol 205:213–226. https://doi.org/10.1016/j.aquatox.2018.10.017
Azevedo-Linhares M, Souza ATC, Lenz CA, Leite NF, Brito IA, Folle NMT, Garcia JE, Filipak Neto F, Oliveira Ribeiro CA (2018) Microcystin and pyriproxyfen are toxic to early stages of development in Rhamdia quelen: an experimental and modelling study. Ecotoxicol Environ Saf 166:311–319. https://doi.org/10.1016/j.ecoenv.2018.09.064
Belenguer V, Martinez-Capel F, Masiá A, Picó Y (2014) Patterns of presence and concentration of pesticides in fish and waters of the Júcar River (Eastern Spain). J Hazard Mater 265:271–279. https://doi.org/10.1016/j.jhazmat.2013.11.016
Biale H, Geden CJ, Chiel E (2017) Effects of pyriproxyfen on wild populations of the housefly, Musca domestica, and compatibility with its principal parasitoids. Pest Manag Sci 73:2456–2464. https://doi.org/10.1002/ps.4638
Brown MD, Thomas D, Watson K, Greenwood JG, Kay BH (1996) Acute toxicity of selected pesticides to the estuarine shrimp Leander tenuicornis (Decapoda: Palaemonidae). J Am Mosq Control Assoc 12:721–724
Brown MD, Thomas D, Kay BH (1998) Acute toxicity of selected pesticides to the Pacific blue-eye, Pseudomugil signifer (Pisces). J Am Mosq Control Assoc 14:463–466
Brown MD, Carter J, Thomas D, Purdie DM, Kay BH (2002) Pulse-exposure effects of selected insecticides to juvenile Australian crimson-spotted rainbowfish (Melanotaenia duboulayi). J Econ Entomol 95:294–298. https://doi.org/10.1603/0022-0493-95.2.294
Caixeta ES, Silva CF, Santos VS, Olegário de Campos Júnior E, Pereira BB (2016) Ecotoxicological assessment of pyriproxyfen under environmentally realistic exposure conditions of integrated vector management for Aedes aegypti control in Brazil. J Toxicol Environ Health A 79:799–803. https://doi.org/10.1080/15287394.2016.1191400
Campo J, Masiá A, Blasco C, Picó Y (2013) Occurrence and removal efficiency of pesticides in sewage treatment plants of four Mediterranean River Basins. J Hazard Mater 263(Pt 1):146–157. https://doi.org/10.1016/j.jhazmat.2013.09.061
Ccanccapa A, Masiá A, Navarro-Ortega A, Picó Y, Barceló D (2016a) Pesticides in the Ebro River basin: occurrence and risk assessment. Environ Pollut 211:414–424. https://doi.org/10.1016/j.envpol.2015.12.059
Ccanccapa A, Masiá A, Andreu V, Picó Y (2016b) Spatio-temporal patterns of pesticide residues in the Turia and Júcar Rivers (Spain). Sci Total Environ 540:200–210. https://doi.org/10.1016/j.scitotenv.2015.06.063
Darriet F, Corbel V (2006) Laboratory evaluation of pyriproxyfen and spinosad, alone and in combination, against Aedes aegypti larvae. J Med Entomol 43:1190–1194
Devillers J (1988) Acute toxicity of cresols, xylenols, and trimethylphenols to Daphnia magna Straus 1820. Sci Total Environ 76:79–83. https://doi.org/10.1016/0048-9697(88)90286-0
Devillers J (2009) Endocrine disruption modeling. CRC Press, Boca Raton
Devillers J (2013) Juvenile hormones and juvenoids: a historical survey. In: Devillers J (ed) Juvenile hormones and juvenoids. Modeling biological effects and environmental fate. CRC Press, Boca Raton, pp 1–14
Devillers J, Chambon P (1988) A methodological framework for the early detection of drinking water pollutants. Chemosphere 17:1647–1654. https://doi.org/10.1016/0045-6535(88)90093-8
Devillers J, Doré JC, Guyot M, Poroikov V, Gloriozova T, Lagunin A, Filimonov D (2007) Prediction of biological activity profiles of cyanobacterial secondary metabolites. SAR QSAR Environ Res 18:629–643. https://doi.org/10.1080/10629360701698704
Devillers J, Devillers H, Decourtye A, Fourrier J, Aupinel P, Fortini D (2014) Agent-based modeling of the long term effects of pyriproxyfen on honey bee population. In: Devillers J (ed) In silico bees. CRC Press, Boca Raton, pp 179–208
Devine GJ, Perea EZ, Killeen GF, Stancil JD, Clark SJ, Morrison AC (2009) Using adult mosquitoes to transfer insecticides to Aedes aegypti larval habitats. Proc Natl Acad Sci U S A 106:11530–11534. https://doi.org/10.1073/pnas.0901369106
EC (2012) Directive 98/8/EC concerning the placing of biocidal products on the market. Inclusion of active substances in Annex I to Directive 98/8/EC. Assessment Report Pyriproxyfen Product-type 18 (insecticides, acaricides and products to control other arthropods), 21 September 2012, Annex I - The Netherlands. http://dissemination.echa.europa.eu/Biocides/ActiveSubstances/0061-18/0061-18_Assessment_Report.pdf
EFSA (2019) Conclusion on the peer review of the pesticide risk assessment of the active substance pyriproxyfen. Appendix EFSA J 17(6):5732. https://doi.org/10.2903/j.efsa.2019.5732
Eliahu M, Blumberg D, Horowitz AR, Ishaaya I (2007) Effect of pyriproxyfen on developing stages and embryogenesis of California red scale (CRS), Aonidiella aurantii. Pest Manag Sci 63:743–746. https://doi.org/10.1002/ps.1369
El-Shazly MM, Refaie BM (2002) Larvicidal effect of the juvenile hormone mimic pyriproxyfen on Culex pipiens. J Am Mosq Control Assoc 18:321–328
EPA (1996) https://archive.epa.gov/pesticides/chemicalsearch/chemical/foia/web/pdf/129032/129032-040.pdf
Estrada JG, Mulla MS (1986) Evaluation of two new insect growth regulators against mosquitoes in the laboratory. J Am Mosq Control Assoc 2:57–60
FAO, Joint Meeting Pesticide Residues, PYRIPROXYFEN (1999). http://www.fao.org/fileadmin/templates/agphome/documents/Pests_Pesticides/JMPR/Evaluation99/25Pyriproxyfen.pdf
Faraji A, Unlu I (2016) The eye of the tiger, the thrill of the fight: effective larval and adult control measures against the Asian tiger mosquito, Aedes albopictus (Diptera: Culicidae), in North America. J Med Entomol 53:1029–1047. https://doi.org/10.1093/jme/tjw096
Fuertes I, Jordão R, Piña B, Barata C (2019) Time-dependent transcriptomic responses of Daphnia magna exposed to metabolic disruptors that enhanced storage lipid accumulation. Environ Pollut 249:99–108. https://doi.org/10.1016/j.envpol.2019.02.102
Ginjupalli GK, Baldwin WS (2013) The time- and age-dependent effects of the juvenile hormone analog pesticide, pyriproxyfen on Daphnia magna reproduction. Chemosphere 92:1260–1266. https://doi.org/10.1016/j.chemosphere.2013.04.061
Gómez A, Seccacini E, Zerba E, Licastro S (2011) Comparison of the insecticide susceptibilities of laboratory strains of Aedes aegypti and Aedes albopictus. Mem Inst Oswaldo Cruz Rio de Janeiro 106:993–996. https://doi.org/10.1590/S0074-02762011000800015
Gouveia D, Bonneton F, Almunia C, Armengaud J, Quéau H, Degli-Esposti D, Geffard O, Chaumot A (2018) Identification, expression, and endocrine-disruption of three ecdysone-responsive genes in the sentinel species Gammarus fossarum. Sci Rep 8(1):3793. https://doi.org/10.1038/s41598-018-22235-7
Guyot M, Doré JC, Devillers J (2004) Typology of secondary cyanobacterial metabolites from minimum spanning tree analysis. SAR QSAR Environ Res 15:101–114. https://doi.org/10.1080/10629360410001665866
Hwang JS (2009) Eradication of Solenopsis invicta by pyriproxyfen at the Shihmen Reservoir in northern Taiwan. Insect Sci 16:493–501. https://doi.org/10.1111/j.1744-7917.2009.01279.x
Isayama S, Tsuda N (2008) Development of a novel formulation: Pluto® MC to control mulberry scale on tea. Sumitomo Kagaku 2:1–12
Itoh T (1994) Utilization of bloodfed females of Aedes aegypti as a vehicle for the transfer of the insect growth regulator pyriproxyfen to larval habitats. Trop Med 36:243–248
Itoh T, Kawada H, Abe A, Eshita Y, Rongsriyam Y, Igarashi A (1994) Utilization of bloodfed females of Aedes aegypti as a vehicle for the transfer of the insect growth regulator pyriproxyfen to larval habitats. J Am Mosq Control Assoc 10:344–347
Jobling S, Casey D, Rodgers-Gray T, Oehlmann J, Schulte-Oehlmann U, Pawlowski S, Baunbeck T, Turner AP, Tyler CR (2003) Comparative responses of molluscs and fish to environmental estrogens and an estrogenic effluent. Aquat Toxicol 65:205–220. https://doi.org/10.1016/S0166-445X(03)00134-6
Jordão R, Garreta E, Campos B, Lemos MF, Soares AM, Tauler R, Barata C (2016) Compounds altering fat storage in Daphnia magna. Sci Total Environ 545-546:127–136. https://doi.org/10.1016/j.scitotenv.2015.12.097
Kakiichi N, Kitamikado A, Sasamori T, Tanaka Y, Ishiwata Y, Sakurai A, Shimizu K, Kamata SI (1996) Toxicity of several insecticides against ciliate Colpoda aspera. Anim Sci Technol 67:844–850. https://doi.org/10.2508/chikusan.67.844
Kalogridi EC, Christophoridis C, Bizani E, Drimaropoulou G, Fytianos K (2014) Part I: temporal and spatial distribution of multiclass pesticide residues in lake waters of Northern Greece: application of an optimized SPE-UPLC-MS/MS pretreatment and analytical method. Environ Sci Pollut Res Int 21:7239–7251. https://doi.org/10.1007/s11356-014-2793-z
Kawada H, Dohara K, Shinjo G (1988) Laboratory and field evaluation of an insect growth regulator, 4-phenoxyphenyl (RS)-2-(2-pyridyloxy)propyl ether, as a mosquito larvicide. Jpn J Sanit Zool 39:339–346. https://doi.org/10.7601/mez.39.339
Kawada H, Shono Y, Ito T, Abe Y (1993) Laboratory evaluation of insect growth regulators against several species of anopheline mosquitoes. Jpn J Sanit Zool 44:349–353. https://doi.org/10.7601/mez.44.349
Kiware SS, Corliss G, Merrill S, Lwetoijera DW, Devine G, Majambere S, Killeen GF (2015) Predicting scenarios for successful autodissemination of pyriproxyfen by malaria vectors from their resting sites to aquatic habitats; description and simulation analysis of a field-parameterizable model. PLoS One 10(7):e0131835. https://doi.org/10.1371/journal.pone.0131835
Kodaka R, Swales SE, Lewis C, Katagi T (2011) Effect of illumination on degradation of pyriproxyfen in water-sediment system. J Pestic Sci 36:33–40. https://doi.org/10.1584/jpestics.G10-56
Lajmanovich RC, Peltzer PM, Martinuzzi CS, Attademo AM, Bassó A, Colussi C (2019) Insecticide pyriproxyfen (Dragón®) damage biotransformation, thyroid hormones, heart rate, and swimming performance of Odontophrynus americanus tadpoles. Chemosphere 220:714–722. https://doi.org/10.1016/j.chemosphere.2018.12.181
Legrand E, Boulangé-Lecomte C, Restoux G, Trémolet G, Duflot A, Forget-Leray J (2017) Individual and mixture acute toxicity of model pesticides chlordecone and pyriproxyfen in the estuarine copepod Eurytemora affinis. Environ Sci Pollut Res Int 24:5976–5984. https://doi.org/10.1007/s11356-016-8294-5
Linton S, Barrow L, Davies C, Harman L (2009) Potential endocrine disruption of ovary synthesis in the Christmas Island red crab Gecarcoidea natalis by the insecticide pyriproxyfen. Comp Biochem Physiol A Mol Integr Physiol 154:289–297. https://doi.org/10.1016/j.cbpa.2009.02.024
Maharajan K, Muthulakshmi S, Nataraj B, Ramesh M, Kadirvelu K (2018) Toxicity assessment of pyriproxyfen in vertebrate model zebrafish embryos (Danio rerio): a multi biomarker study. Aquat Toxicol 196:132–145. https://doi.org/10.1016/j.aquatox.2018.01.010
Maoz D, Ward T, Samuel M, Mueller P, Runge-Ranzinger S, Toledo J, Boyce R, Velayudhan R, Horstick O (2017) Community effectiveness of pyriproxyfen as a dengue vector control method: a systematic review. PLoS Negl Trop Dis 11(7):e0005651. https://doi.org/10.1371/journal.pntd.0005651
Masiá A, Campo J, Navarro-Ortega A, Barceló D, Picó Y (2015) Pesticide monitoring in the basin of Llobregat River (Catalonia, Spain) and comparison with historical data. Sci Total Environ 503-504:58–68. https://doi.org/10.1016/j.scitotenv.2014.06.095
Matsumoto T, Ikuno E, Itoi S, Sugita H (2008) Chemical sensitivity of the male daphnid, Daphnia magna, induced by exposure to juvenile hormone and its analogs. Chemosphere 72:451–456. https://doi.org/10.1016/j.chemosphere.2008.02.016
Mikhali AC (2015) Effects of insect growth regulator pyriproxyfen on dragonfly nymphs as predators of Anopheles mosquitoes at Mahanga, Vihiga County, Kenya. Degree of Master of Science (Agricultural Entomology) in the School of Pure and Applied Sciences of Kenyatta University, p 56
Miyamoto J, Hirano H, Takimoto Y, Hatakoshi M (1993) Insect growth regulators for pest control, with emphasis on juvenile hormone analogs. Present status and future prospect. In: Duke SO, Menn JJ, Plimmer JR (eds) Pest control with enhanced environmental safety, ACS Syposium series 524. American Chemical Society, Washington DC, pp 144–168
Miyamoto M, Tanaka H, Katagu T (2008) Ecotoxicological risk assessment of pesticides in aquatic ecosystem. Sumitomo Kagaku, R&D Report Sumitomo Chemical Co., Ltd. vol. 2008-I, p 18
Mu X, Leblanc GA (2004) Cross communication between signaling pathways: juvenoid hormones modulate ecdysteroid activity in a crustacean. J Exp Zool A Comp Exp Biol 301:793–801. https://doi.org/10.1002/jez.a.104
Mulla MS, Darwazeh HA, Kennedy B, Dawson DM (1986) Evaluation of new insect growth regulators against mosquitoes with notes on nontarget organisms. J Am Mosq Control Assoc 2:314–320
Mulligan FS 3rd, Schaefer CH (1990) Efficacy of a juvenile hormone mimic, pyriproxyfen (S-31183), for mosquito control in dairy wastewater lagoons. J Am Mosq Control Assoc 6:89–92
Oda S, Tatarazako N, Watanabe H, Morita M, Iguchi T (2006) Genetic differences in the production of male neonates in Daphnia magna exposed to juvenile hormone analogs. Chemosphere 63:1477–1484. https://doi.org/10.1016/j.chemosphere.2005.09.026
Oehlmann J, Schulte-Oehlmann U, Tillmann M, Markert B (2000) Effects of endocrine disruptors on prosobranch snails (Mollusca: Gastropoda) in the laboratory. Part I: bisphenol A and octylphenol as xeno-estrogens. Ecotoxicology 9:383–397. https://doi.org/10.1023/A:1008972518019
Ohashi K (2017) Control of mosquito larvae in catch basins using pyriproxyfen and the mechanism underlying residual efficacy. Med Entomol Zool 68:127–135. https://doi.org/10.7601/mez.68.127
Olmstead AW, LeBlanc GA (2003) Insecticidal juvenile hormone analogs stimulate the production of male offspring in the crustacean Daphnia magna. Environ Health Perspect 111:919–924. https://doi.org/10.1289/ehp.5982
Olmstead AW, LeBlanc GA (2007) The environmental-endocrine basis of gynandromorphism (intersex) in a crustacean. Int J Biol Sci 3:77–84. https://doi.org/10.7150/ijbs.3.77
Ose K, Miyamoto M, Fujisawa T, Katagi T (2017) Bioconcentration and metabolism of pyriproxyfen in tadpoles of African clawed frogs, Xenopus laevis. J Agric Food Chem 65:9980–9986. https://doi.org/10.1021/acs.jafc.7b04184
Ose K, Yamada F, Ohara A, Suzuki N, Fukuda T, Miyamoto M, Sumida K (2019) A microarray-based comparative analysis of gene expression profiles in thyroid glands in amphibian metamorphosis: differences in effects between chemical exposure and food restriction. J Appl Toxicol 39:1030–1042. https://doi.org/10.1002/jat.3791
Park YK, Oh JA, You AS, Park SJ, Jo YM, Lee JB, Kim CS (2017) Acute toxicity of pesticides to carp (Cyprinus carpio) and changes of toxicity to the exposure time. Korean J Pestic Sci 21:453–492. https://doi.org/10.7585/kjps.2017.21.4.453
Qureshi MS, Midmore DJ, Syeda SS, Reid DJ (2009) Pyriproxyfen controls silverleaf whitefly, Bemisia tabaci (Gennadius), biotype B (Homoptera: Aleyrodidae) (SLW) better than buprofezin in bitter melons Momordica charantia L. (Cucurbitaceae). Aust J Entomol 48:60–64. https://doi.org/10.1111/j.1440-6055.2008.00684.x
Ritchie SA, Paton C, Buhagiar T, Webb GA, Jovic V (2013) Residual treatment of Aedes aegypti (Diptera: Culicidae) in containers using pyriproxyfen slow-release granules (Sumilarv 0.5G). J Med Entomol 50:1169–1172. https://doi.org/10.1603/ME13043
Ross DH, Pennington RG, Cruthers LR, Slone RL (1997) Efficacy of a permethrin and pyriproxyfen product for control of fleas, ticks and mosquitoes on dogs. Canine Pract 22:53–58
Saltzmann KA, Saltzmann KD, Neal JJ, Scharf ME, Bennett GW (2006) Effects of the juvenile hormone analog pyriproxyfen on German cockroach, Blattella germanica (L.), tergal gland development and production of tergal gland secretion proteins. Arch Insect Biochem Physiol 63:15–23. https://doi.org/10.1002/arch.20137
Schaefer CH, Miura T (1990) Chemical persistence and effects of S-31183, 2-[1-methyl-2-(4-phenoxyphenoxy)ethoxy]pyridine, on aquatic organisms in field tests. J Econ Entomol 83:1768–1776. https://doi.org/10.1093/jee/83.5.1768
Schaefer CH, Miura T, Dupras EF Jr, Mulligan FS 3rd, Wilder WH (1988) Efficacy, nontarget effects, and chemical persistence of S-31183, a promising mosquito (Diptera: Culicidae) control agent. J Econ Entomol 81:1648–1655. https://doi.org/10.1093/jee/81.6.1648
Schaefer CH, Dupras EF Jr, Mulligan FS 3rd (1991) Studies on the environmental persistence of S-31183 (pyriproxyfen): adsorption onto organic matter and potential for leaching through soil. Ecotoxicol Environ Saf 21:207–214. https://doi.org/10.1016/0147-6513(91)90022-H
Silva Alves PE, Oliveira MDDA, Marcos de Almeida P, Martins FA, Amélia de Carvalho Melo Cavalcante A, de Jesus Aguiar Dos Santos Andrade T, Feitosa CM, Rai M, Campinho Dos Reis A, Soares da Costa J Jr (2019) Determination by chromatography and cytotoxotoxic and oxidative effects of pyriproxyfen and pyridalyl. Chemosphere 224:398–406. https://doi.org/10.1016/j.chemosphere.2019.02.037
Spirhanzlova P, Le Mevel S, Wejaphikul K, Mughal B, Gothie JD, Sebillot A, Butruille L, Leemans M, Visser T, Remaud S, Fini JB, Demeneix B (2018) The pyriproxyfen metabolite 4′OH- pyriproxyfen disrupts thyroid hormone signaling and enhances Musashi-1 levels in neuroprogenitors. bioRxiv. https://doi.org/10.1101/352088
Stanneck D, Larsen KS, Mencke N (2002) An evaluation of the effects of pyriproxyfen on eggs and adults of the cat flea, Ctenocephalides felis felis (Siphonaptera: Pulicidae). Irish Vet J 55:383–387
Sullivan JJ, Goh KS (2008) Environmental fate and properties of pyriproxyfen. J Pestic Sci 33:339–350. https://doi.org/10.1584/jpestics.R08-02
Suman DS, Wang Y, Dong L, Gaugler R (2013) Effects of larval habitat substrate on pyriproxyfen efficacy against Aedes albopictus (Diptera: Culicidae). J Med Entomol 50:1261–1266. https://doi.org/10.1603/ME13068
Takagi M, Tsuda Y, Wada Y (1995) Laboratory evaluation of a juvenile hormone mimic, pyriproxyfen, against Chironomus fusciceps (diptera: chironomidae). J Am Mosq Control Assoc 11:474–475
Tassou KT, Schulz R (2009) Effects of the insect growth regulator pyriproxyfen in a two-generation test with Chironomus riparius. Ecotoxicol Environ Saf 72:1058–1062. https://doi.org/10.1016/j.ecoenv.2009.02.001
Tassou KT, Schulz R (2012) Combined effects of temperature and pyriproxyfen stress in a full life-cycle test with Chironomus riparius (Insecta). Environ Toxicol Chem 31:2384–2390. https://doi.org/10.1002/etc.1969
Tatarazako N, Oda S, Watanabe H, Morita M, Iguchi T (2003) Juvenile hormone agonists affect the occurrence of male Daphnia. Chemosphere 53:827–833. https://doi.org/10.1016/S0045-6535(03)00761-6
Tokishita S, Kato Y, Kobayashi T, Nakamura S, Ohta T, Yamagata H (2006) Organization and repression by juvenile hormone of a vitellogenin gene cluster in the crustacean, Daphnia magna. Biochem Biophys Res Commun 345:362–370. https://doi.org/10.1016/j.bbrc.2006.04.102
Trapp J, Armengaud J, Pible O, Gaillard JC, Abbaci K, Habtoul Y, Chaumot A, Geffard O (2015) Proteomic investigation of male Gammarus fossarum, a freshwater crustacean, in response to endocrine disruptors. J Proteome Res 14:292–303. https://doi.org/10.1021/pr500984z
Trapp J, Gouveia D, Almunia C, Pible O, Degli Esposti D, Gaillard J-C, Chaumot A, Geffard O, Armengaud J (2018) Digging deeper into the pyriproxyfen-response of the amphipod Gammarus fossarum with a next-generation ultra-high-field orbitrap analyser: new perspectives for environmental toxicoproteomics. Front Environ Sci 6:54. https://doi.org/10.3389/fenvs.2018.00054
Trayler KM, Davis JA (1996) Sensitivity of Daphnia carinata sensu lato to the insect growth regulator, pyriproxyfen. Ecotoxicol Environ Saf 33:154–156. https://doi.org/10.1006/eesa.1996.0019
Trayler KM, Pinder AM, David JA (1994) Evaluation of the juvenile hormone mimic pyriproxyfen (S-31183) against nuisance Chironomids (Diptera:Chironomidae), with particular emphasis on Polypedilum nubifer (Skuse). J Aust Entomol Soc 3:127–130. https://doi.org/10.1111/j.1440-6055.1994.tb00937.x
Truong L, Gonnerman G, Simonich MT, Tanguay RL (2016) Assessment of the developmental and neurotoxicity of the mosquito control larvicide, pyriproxyfen, using embryonic zebrafish. Environ Pollut 218:1089–1093. https://doi.org/10.1016/j.envpol.2016.08.061
Tuberty SR, McKenney CL Jr (2005) Ecdysteroid responses of estuarine crustaceans exposed through complete larval development to juvenile hormone agonist insecticides. Integr Comp Biol 45:106–117. https://doi.org/10.1093/icb/45.1.106
Unlu I, Suman DS, Wang Y, Klingler K, Faraji A, Gaugler R (2017) Effectiveness of autodissemination stations containing pyriproxyfen in reducing immature Aedes albopictus populations. Parasit Vectors 10(1):139. https://doi.org/10.1186/s13071-017-2034-7
Vandekerkhove J, Rossetti G, Mezquita F (2007) Pyriproxyfen, a juvenoid hormone analog, does not induce male production in parthenogenetic lineages of Eucypris virens (Crustacea: Ostracoda). J Limnol 66:60–63. https://doi.org/10.4081/jlimnol.2007.60
Vieira Santos VS, Caixeta ES, Campos Júnior EO, Pereira BB (2017) Ecotoxicological effects of larvicide used in the control of Aedes aegypti on nontarget organisms: redefining the use of pyriproxyfen. J Toxicol Environ Health A 80:155–160. https://doi.org/10.1080/15287394.2016.1266721
Wang HY, Olmstead AW, Li H, Leblanc GA (2005a) The screening of chemicals for juvenoid-related endocrine activity using the water flea Daphnia magna. Aquat Toxicol 74:193–204. https://doi.org/10.1016/j.aquatox.2005.05.010
Wang S, Phong TV, Tuno N, Kawada H, Takagi M (2005b) Sensitivity of the larvivorous copepod species, Mesocyclops pehpeiensis and Megacyclops viridis, to the insect growth regulator, pyriproxyfen. J Am Mosq Control Assoc 21:483–488. https://doi.org/10.2987/8756-971X(2006)21[483:SOTLCS]2.0.CO;2
Webb G, Miller P, Peters B, Keats A, Winner S (2011) Efficacy, environmental persistence and non-target impacts of pyriproxyfen use against Aedes vigilax in Australia. In: Robinson WH, de Carvalho Campos AE (eds) Proc Seventh Int Conf Urban Pests. Instituto Biológico, Săo Paulo, pp 151–157
WHO (2006a) Pesticides and their application for the control of vectors and pests of public health importance, 6th ed. Geneva, World Health Organization, Department of Control of Neglected Tropical Diseases, Pesticide Evaluation Scheme (WHO/CDS/NTD/WHOPES/GCDPP/2006.1. http://whqlibdoc.who.int/hq/2006/WHO_CDS_NTD_WHOPES_GCDPP_2006.1_eng.pdf)
WHO (2006b) WHO specifications and evaluations for public health pesticides: pyriproxyfen, 4-phenoxyphenyl (RS)-2-(2-pyridyloxy)propyl ether, 2006. WHO Press, World Health Organization, Geneva
Yapabandara AM, Curtis CF (2002) Laboratory and field comparisons of pyriproxyfen, polystyrene beads and other larvicidal methods against malaria vectors in Sri Lanka. Acta Trop 81:211–223. https://doi.org/10.1016/S0001-706X(01)00208-X
Acknowledgments
This work was supported by the AUTODIS program (Convention 18C08).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that he has no conflict of interest.
Additional information
Responsible editor: Philippe Garrigues
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Devillers, J. Fate and ecotoxicological effects of pyriproxyfen in aquatic ecosystems. Environ Sci Pollut Res 27, 16052–16068 (2020). https://doi.org/10.1007/s11356-020-08345-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-08345-8