Abstract
Due to expected changes in climate, it is predicted that disease-carrying mosquitoes will expand their geographical range, resulting in increased use of insect growth regulators (IGRs) to face their proliferation. Among IGRs, pyriproxyfen (PXF) is widely used and has been shown to prevent larvae from developing into adults, rendering them unable to reproduce. However, because of the similarity of crustacean and insect endocrine systems, PXF could also impact aquatic crustaceans. In addition, when spreading in the environment, PXF is found in a mixture with other pollutants such as metallic trace elements, which could alter its effect. Consequently, the present work was devoted to analysing the effects of PXF on the methylfarnesoate (MF) hormonal pathway of the freshwater amphipod Gammarus pulex, as well as its combined binary effects with cadmium (Cd), by measuring MF concentration, as well as the relative transcriptional expression of the farnesoic acid O-methyltransferase (FAMeT) (enzyme limiting the MF production), the methoprene-tolerant receptor (Met), and the broad-complex (BrC) as a transcription factor. Results revealed that single exposures to PXF or Cd have mainly overexpressed FAMeT, Met, and BrC but did not significantly affect MF concentration. Conversely, the mixture exposures seemed to suppress these effects and even achieve antagonistic effects. This work confirmed that PXF single exposure could impact non-target organisms such as amphipods through changes in hormonal pathways of MF. In the same way, it highlighted that Cd could also impair the endocrine system of exposed organisms. However, antagonistic effects have been observed in exposure to mixtures, suggesting different long-term consequences on the growth of amphipods under realistic exposure conditions.
Similar content being viewed by others
References
Abidi S, Abbaci K, Geffard O, Boumaiza M, Dumet A, Garric J, Mondy N (2016) Impact of cadmium on the ecdysteroids production in Gammarus fossarum. Ecotoxicology 25:80–887
Bellini R, Zeller H, Van Bortel W (2014) A review of the vector management methods to prevent and control outbreaks of West Nile virus infection and the challenge for Europe. Parasite Vector 7:323
Biswas R, Laufer H (2015) Feedback regulation of methylfarnesoate synthesis by mandibular organs of the crayfish. IJANS 4(2):17–24
Bodnaryk RP (1986) Feedback inhibition of ecdysone production by 20-hydroxyecdysone during pupal—adult metamorphosis of Mamestra configurata wlk. Arch Insect Biochem 3(1):53–60
Buaklin A, Sittikankaew K, Khamnamtong B, Menasveta P, Klinbunga S (2013) Characterization and expression analysis of the broad-complex (Br-c) gene of the giant tiger shrimp Penaeus monodon. Comp Biochem Phys B 164(4):280–289
Charles JP, Iwema T, Epa VC, Takaki K, Rynes J, Jindra M (2011) Ligand-binding properties of a juvenile hormone receptor, Methoprene-tolerant. P Natl Acad Sci USA 108(52):21128–21133
Devillers J (2020) Fate and ecotoxicological effects of pyriproxyfen in aquatic ecosystems. Environ Sci Pollut Res
European Commission (1998) Directive 98/8/EC of the European parliament and of the council of 16 February 1998 concerning the placing of biocidal products on the market
European Commission (2013) Commission Directive 2013/5/EU of 14 February 2013 amending directive 98/8/EC of the European Parliament and of the council to include pyriproxyfen as an active substance in annex I therero
Ginjupalli GK, Baldwin WS (2013) The time- and age-dependent effects of the juvenile hormone analog pesticide, pyriproxyfen on Daphnia magna reproduction. Chemosphere 92(9):1260–1266
Gismondi E (2018) Identification of molt-inhibiting hormone and ecdysteroid receptor cDNA sequences in Gammarus pulex, and variations after endocrine disruptor exposures. Ecotox Environ Safe 158:9–17
Gismondi E, Cossu-Leguille C, Beisel JN (2013) Do male and female gammarids defend themselves differently during chemical stress? Aquat Toxicol 140:432–438
Gismondi E, Fivet A, Joaquim-Justo C (2017) Effects of cyproterone acetate and vertically transmitted microsporidia parasite on Gammarus pulex sperm production. Envir Sci Pollut R 24(29):23417–23421
Gismondi E, Joaquim-Justo C (2019) Relative expression of three key genes involved in the hormonal cycle of the freshwater amphipod, Gammarus pulex. J Exp Zool Part A
Gismondi E, Thomé JP (2016) Transcriptome of the freshwater amphipod Gammarus pulex hepatopancreas. Genoms Data 8:91–92
Gismondi E, Thomé JP, Urien N, Uher E, Baiwir D, Mazzucchelli G, de Pauw E, Fechner LC, Lebrun JD (2017) Ecotoxicoproteomic assessment of the functional alterations caused by chronic metallic exposures in gammarids. Environ Pollut 225:428–438
Goodman WG, Cusson M (2012) The juvenile hormones. In: Gilbert LI (ed) Insect endocrinology. Elsevier, Amsterdam, pp 310–365
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-UK 8(1):3793
Helvig C, Koener JF, Unnithan GC, Feyereisen R (2004) CYP15A1, the cytochrome P450 that catalyzes epoxidation of methyl farnesoate to juvenile hormone III in cockroach corpora allata. P Natl Acad Sci USA 101(12):4024–4029
Homola E, Chang ES (1997) Methyl farnesoate: crustacean juvenile hormone in search of functions. Comp Biochem Phys B 117(3):347–356
Hopkins PM (1992) Hormonal control of the molt cycle in the fiddler crab Uca pugilator. Am Zool 32(3):450–458
Hui JHL, Hayward A, Bendena WG, Takahashi T, Tobe SS (2010) Evolution and functional divergence of enzymes involved in sesquiterpenoid hormone biosynthesis in crustaceans and insects. Peptides 31(3):451–455
Hui JHL, Tobe SS, Chan S-M (2008) Characterization of the putative farnesoic acid O-methyltransferase (LvFAMeT) cDNA from white shrimp, Litopenaeus vannamei: evidence for its role in molting. Peptides 29(2):252–260
Hyde CJ, Elizur A, Ventura T (2019) The crustacean ecdysone cassette: a gatekeeper for molt and metamorphosis. J Steroid Biochem Mol Biol 185:172–183
Hyne RV (2011) Review of the reproductive biology of amphipods and their endocrine regulation: identification of mechanistic pathways for reproductive toxicants. Environ Toxicol Chem 30(12):2647–2657
Invest JF, Lucas JR (2008) Pyriproxyfen as a mosquito larvicide. Proc international conference on urban pests, Budapest
Ishaaya I, Horowitz AR (1995) Pyriproxyfen, a novel insect growth regulator for controlling whiteflies: mechanisms and resistance management. Pestic Sci 43(3):227–232
Jindra M, Bittova L (2020) The juvenile hormone receptor as a target of juvenoid “insect growth regulators” Arch Insect Biochem, 103(3)
Kayukawa T, Minakuchi C, Namiki T, Togawa T, Yoshiyama M, Kamimura M, Mita K, Imanishi S, Kiuchi M, Ishikawa Y, Shinoda T (2012) Transcriptional regulation of juvenile hormone-mediated induction of Krüppel homolog 1, a repressor of insect metamorphosis. Proc Natl Acad Sci U S A 109:11729–11734
Kayukawa T, Nagamine K, Ito Y, Nishita Y, Ishikawa Y, Shinoda T (2016) Krüppel Homolog 1 inhibits insect metamorphosis via direct transcriptional repression of Broad-Complex, a pupal specifier gene. J Biol Chem 291:1751–1762
Konopova B, Jindra M (2008) Broad-Complex acts downstream of Met in juvenile hormone signaling to coordinate primitive holometabolan metamorphosis. Development 135(3):559–568
Kraemer MUG, Reiner RC, Brady OJ, Messina JP, Gilbert M, Pigott DM et al (2019) Past and future spread of the arbovirus vectors Aedes aegypti and Aedes albopictus. Nat Microbiol 4(5):854–863
Kunz PY, Kienle C, Gerhardt A (2010) Gammarus spp. in aquatic ecotoxicology and water quality assessment: toward integrated multilevel tests (pp. 1–76)
Laufer H, Demir N, Pan X, Stuart JD, Ahl JSB (2005) Methyl farnesoate controls adult male morphogenesis in the crayfish, Procambarus clarkii. J Insect Physiol 51(4):379–384
LeBlanc GA, Wang YH, Holmes CN, Kwon G, Medlock EK (2013) A transgenerational endocrine signaling pathway in crustacea. PLoS One 8(4):e61715
Lebrun JD, Geffard O, Urien N, François A, Uher E, Fechner LC (2015) Seasonal variability and inter-species comparison of metal bioaccumulation in caged gammarids under urban diffuse contamination gradient: implications for biomonitoring investigations. Sci Total Environ 511:501–508
Liu X, Nie S, Yu Q, Wang X, Huang D, Xie M (2017) Downregulation of steroid hormone receptor expression and activation of cell signal transduction pathways induced by a chiral nonylphenol isomer in mouse sertoli TM4 cells. Environ Toxicol 32(2):469–476
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408
Lozano J, Belles X (2014) Role of Methoprene-tolerant (Met) in adult morphogenesis and in adult ecdysis of Blattella germanica. PLoS One 9(7):e103614
Meng QW, Xu QY, Deng P, Fu KY, Guo WC, Li GQ (2018) Involvement of methoprene-tolerant (Met) in the determination of the final body size in Leptinotarsa decemlineata (Say) larvae. Insect biochem molec 97:1–9
Miyakawa H, Sato T, Song Y, Tollefsen KE, Iguchi T (2018) Ecdysteroid and juvenile hormone biosynthesis, receptors and their signaling in the freshwater microcrustacean Daphnia. J Steroid Biochem, Elsevier Ltd
Miyakawa H, Toyota K, Hirakawa I, Ogino Y, Miyagawa S, Oda S, Tatarazako N, Miura T, Colbourne JK, Iguchi T (2013) A mutation in the receptor Methoprene-tolerant alters juvenile hormone response in insects and crustaceans. Nat Commun 4(1):1856
Montes R, Rodil R, Neuparth T, Santos MM, Cela R, Quintana JB (2017) A simple and sensitive approach to quantify methyl farnesoate in whole arthropods by matrix-solid phase dispersion and gas chromatography–mass spectrometry. J Chromatogr A 1508:158–162
Mu X, Leblanc GA (2004) Cross communication between signaling pathways: juvenoid hormones modulate ecdysteroid activity in a crustacean. J Exp Zool 301A(10):793–801
Nagaraju GPC (2011) Reproductive regulators in decapod crustaceans: an overview. J Exp Biol 214:3–16
Naylor C, Maltby L, Calow P (1989) Scope for growth in Gammarus pulex, a freshwater benthic detritivore. Hydrobiologia 188–189(1):517–523
Nørgaard KB, Cedergreen N (2010) Pesticide cocktails can interact synergistically on aquatic crustaceans. Environ Sci Pollut Res 17(4):957–967
Olmstead AW, LeBlanc GA (2003) Insecticidal juvenile hormone analogs stimulate the production of male offspring in the crustacean Daphnia magna. Environ Health Persp 111(7):919–924
Owen SC, Doak AK, Ganesh AN, Nedyalkova L, McLaughlin CK, Shoichet BK, Shoichet MS (2014) Colloidal drug formulations can explain “bell-shaped” concentration–response curves. ACS Chem Biol 9(3):777–784
Pecasse F, Beck Y, Ruiz C, Richards G (2000) Krüppel-homolog, a stage-specific modulator of the prepupal ecdysone response, is essential for Drosophila metamorphosis. Dev Biol 221(2000):53–67
Qu Z, Bendena WG, Tobe SS, Hui JHL (2018) Juvenile hormone and sesquiterpenoids in arthropods: biosynthesis, signaling, and role of MicroRNA. J Steroid Biochem 184:69–76
Rani A, Kumar A, Lal A, Pant M (2014) Cellular mechanisms of cadmium-induced toxicity: a review. Int J Environ Heal R 24(4):378–399
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(5):1768–1776
Serafini M (2001) Pyriproxyfen – registration of a major change of label for Esteem_ 3/01. In: Division of solid & hazardous materials, P.P.R.S. (Ed.). New York State Department of Environmental Conservation, New York
Shinoda T (2016). Methyl farnesoate. Handbook of Hormones, 566-e100–3
Sihunincha M, Zamora-Perea E, Orellana-Rios W, Stancil JD, Lopez-Sifuentes V, Vidal-Oré C, Devine GJ (2005) Potential use of pyriproxyfen for control of Aedes aegypti (Diptera: Culicidae) in Iquitos, Peru. J Med Entomol 42(4):620–630
Subramoniam T (2000) Crustacean ecdysteriods in reproduction and embryogenesis. Comp Biochem Phys C 125(2):135–156
Sullivan JJ, Goh KS (2008) Environmental fate and properties of pyriproxyfen. J Pestic Sci 33(4):339–350
Tamone SL, Chang ES (1993) Methyl farnesoate stimulates ecdysteroid secretion from Y-organs in vitro. Gen Comp Endocr 89:425–432
Trevisan M, Leroy D, Decloux N, Thomé JP, Compère P (2014) Moult-related changes in the integument, midgut, and digestive gland in the freshwater amphipod Gammarus pulex. J Crustacean Biol 34(5):539–551
Tuberty SR, McKenney CL (2005) Ecdysteroid responses of estuarine crustaceans exposed through complete larval development to juvenile hormone agonist insecticides. Integr Comp Biol 45(1):106–117
Vellinger C, Gismondi E, Felten V, Rousselle P, Mehennaoui K, Parant M, Usseglio-Polatera P (2013) Single and combined effects of cadmium and arsenate in Gammarus pulex (Crustacea, Amphipoda): understanding the links between physiological and behavioural responses. Aquat Toxicol 140:106–116
Vellinger C, Parant M, Rousselle P, Usseglio-Polatera P (2012) Antagonistic toxicity of arsenate and cadmium in a freshwater amphipod (Gammarus pulex). Ecotoxicology 21(7):1817–1827
Wang Y, Chen C, Qian Y, Zhao X, Wang Q, Kong X (2015) Toxicity of mixtures of λ-cyhalothrin, imidacloprid and cadmium on the earthworm Eisenia fetida by combination index (CI)-isobologram method. Ecotox Environ Safe 111:242–247
Wang C, Yang Y, Wu N, Gao M, Tan Y (2019) Combined toxicity of pyrethroid insecticides and heavy metals: a review. Environ Chem Lett 17:1693–1706
Watanabe B (2015) Structure-activity relationship studies of insect and plant steroid hormones. J Pestic Sci 40(3):146–151
Wilder MN, Okada S, Fusetani N, Aida K (1995) Hemolymph profiles of juvenoid substances in the giant freshwater prawn, Macrobrachium rosenbergii in relation to reproduction and molting. Fish Sci 61:175–176
Wilson TG (2004) The molecular site of action of juvenile hormone and juvenile hormone insecticides during metamorphosis: how these compounds kill insects. J Insect Physiol 50(2–3):111–121
World Health Organization (2006) Pesticides and their application: for the control of vectors and pests of public health importance (sixth edition). World Health Organization, Geneva, 114 pp.
Zhou X, Riddiford LM (2002) Broad specifies pupal development and mediates the ‘status quo’ action of juvenile hormone on the pupal-adult transformation in Drosophila and Manduca. Development 129(9):2259–2269
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible Editor: Cinta Porte
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
Jaegers, J., Gismondi, E. Gammarid exposure to pyriproxyfen and/or cadmium: what effects on the methylfarnesoate signalling pathway?. Environ Sci Pollut Res 27, 31330–31338 (2020). https://doi.org/10.1007/s11356-020-09419-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-09419-3