Skip to main content
SpringerLink
Log in

Endocrine disruption in aquatic insects: a review

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

There is mounting evidence that a wide variety of compounds can have endocrine disrupting effects on humans and wildlife. However, investigations so far have focused primarily on exposure to human and other vertebrates, with invertebrate findings largely restricted to marine mollusks or to the ecdysteroid and juvenile hormone agonists as purposely synthesized endocrine disrupters for the pest management of insects. This article provides a brief description of the insect hormone system, a short sum-up of the relevant insect groups with aquatic life stages, and an overview of the additional evidence for endocrine disruption in aquatic insects from laboratory and field studies since 1999. In addition, the suitability of insects as sentinels for endocrine disrupting chemicals in aquatic ecosystems is discussed. Conclusions are drawn and research needs are defined.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Allan JD (1995) Stream ecology: structure and function of running waters. Chapman & Hall, New York

    Google Scholar 

  • Amrani L, Zerguine K, Farine J-P, Smagghe G, Soltani-Mazouni N (2004) Imidazole derivative KK-42 reduces ecdysteroid titers and interferes with reproductive processes in adult females of Tenebrio molitor. Pestic Biochem Physiol 88:163–172

    Article  CAS  Google Scholar 

  • ASTM (2006). Standard test methods for measuring the toxicity of sediment-associated contaminants with freshwater invertebrates. In: Annual book of standards, Volume 11.06. Philadelphia PA: ASTM.E1706–05

  • Atchley WR, Davis BL (1979) Chromosomal variability in the antarctic insect, Belgica antarctica (Diptera, Chironomidae). Ann Entomol Soc Am 72(2):246–252

    Google Scholar 

  • Baldwin WS, Graham SE, Shea D, Leblanc GA (1998) Altered metabolic elimination of testosterone and associated toxicity following exposure of Daphnia magna to nonylphenol polyethoxylate. Ecotox Environ Safe 39:104–111

    Article  CAS  Google Scholar 

  • Beckage NE, Marion KM, Walton WE, Wirth MC, Tan FF (2004) Comparitive larvicidal toxicities of three ecdysone agonists on the moquitos Aedes aegypti, Culex quinquefasciatus, and Anopheles gambiae. Arch Insect Biochem Physiol 57:111–122

    Article  CAS  Google Scholar 

  • Beeby A (2001) What do sentinels stand for? Environ Pollut 112:285–298

    Article  CAS  Google Scholar 

  • Belles X, Maestro JL (2005) Endocrine peptides and insect reproduction. Invertebr Reprod Dev 47:23–37

    CAS  Google Scholar 

  • Bonneton F, Zelus D, Iwema T, Robinson-Rechavi M, Laudet V (2003) Rapid divergence of the ecdysone receptor in Diptera and Lepidoptera suggests coevolution between EcR and Usp-RXR. Mol Biol Evol 20:541–555

    Article  CAS  Google Scholar 

  • Boudjelida H, Bouaziz A, Soin T, Smagghe G, Soltani N (2005) Effect of ecdysone agonist halofenozide against Culex pipiens. Pestic Biochem Physiol 83:115–123

    Article  CAS  Google Scholar 

  • Braeckman B, Simoens C, Rzeznik U, Raes H (1997) Effect of sublethal doses of cadmium, inorganic mercury and methylmercury on the cell morphology of an insect cell line (Aedes albopictus, C3/36). Cell Biol Int 12:823–832

    Article  Google Scholar 

  • Chapman PM (2000) Whole effluent toxicity testing – usefulness, level of protection and risk assessment. Environ Toxicol Chem 19:3–13

    Article  CAS  Google Scholar 

  • Cornel AJ, Stanich, MA Farley D, Mulligan FS, Byde G (2000) Methoprene tolerance in Aedes nigromaculis in Fresno County, California. J Am Mosq Control Assoc 16:223–228

    CAS  Google Scholar 

  • Cornel AJ, Stanich MA, McAbee RD, Mulligan FS (2002) High level methoprene resistance in the mosquito Ochleratus nigromaculis (Ludlow) in central California. Pest Manag Sci 58:791–798

    Article  CAS  Google Scholar 

  • deFur, P.L. Crane, M. Ingersoll, C.G., Tattersfield. L. (1999) Endocrine Disruption in Invertebrates: Endocrinology, Testing and Assessment. SETAC technical publication, Pensacola, Florida, pp 303

  • Dhadialla, T. S. Retnakaran, A and Smagghe, G. (2005) Insect growth and development disrupting insecticides. In: Comprehensive Insect Molecular Science (Gilbert, L.I., Kostas, I. and Gill, S.S., eds.). Pergamon Press, vol. 6:55–116

  • Dickman M, Rygiel G (1996) Chironomid larval deformity frequencies, mortality and diversity in heavy-metal contaminated sediments of a Canadian riverine wetland. Environ Int 22(6):693–703

    Article  CAS  Google Scholar 

  • Dinan L (1985) Ecdysteroid receptors in a tumorous blood cell line of Drosophila melanogaster. Arch Insect Biochem Physiol 2:295–317

    Article  CAS  Google Scholar 

  • Dinan L, Bourne P, Whiting P, Dhadialla TS, Hutchinson TH (2001). Screening of environmental contaminants for ecdysteroid agonist and antagonist activity using the Drosophila melanogaster B-II cell in vitro assay. Environ Toxicol Chem 20:2038–2046

    Article  CAS  Google Scholar 

  • Dubrovsky EB (2005) Hormonal cross talk in insect development. TRENDS in Endocrin Met 16:6–11

    Article  CAS  Google Scholar 

  • Fenner-Crisp PA, Maciorowski AF, Timm GE (2000) The endocrine disrupter screening program developed by the US Environmental Protection Agency. Ecotoxicology 9:85–91

    Article  CAS  Google Scholar 

  • Fescemeyer HW, Masler EP, Kelly TJ, Lusby WR (1995) Influence of development and prothoracicotropic hormone on the ecdysteroids produced in vitro by the prothoracic glands of female gypsy moth (Lymantria dispar) pupae and pharate adults. J Insect Physiol 41:489–500

    Article  Google Scholar 

  • Gäde Goldsworthy GJ (2003) Insect peptide hormones: a selective review of their physiology and potential application for pest control. Pest Manag Sci 59:1063–1075

    Article  CAS  Google Scholar 

  • Gäde G, Hoffmann KH, Spring JH (1997) Hormonal regulation in insects: facts, gaps, and future directions. Physiol Rev 77:963–1032

    Google Scholar 

  • Garcia ES, Luz N, Azambuja P, Rembold H (1990) Azadirachtin depresses the release of prothoracicotropic hormone in Rhodnius prolixus larvae: evidence from head transplantations. J Insect Physiol 36:679–682

    Article  CAS  Google Scholar 

  • Gilbert LI, Rybczinski R, Warren JT (2002) Control and biochemical nature of the ecdysteroidogenic pathway. Annu Rev Entomol 47:883–916

    Article  CAS  Google Scholar 

  • Hahn T, Liess M, Schulz R (2001) Effect of the hormone mimetic insecticide tebufenozide on Chironomus riparius larvae in two exposure setups. Ecotox Environ Safe 49:171–178

    Article  CAS  Google Scholar 

  • Hahn T, Schenk K, Schulz R (2002) Environmental chemicals with known endocrine potential affect yolk protein content in the aquatic insect Chironomus riparius. Environ Pollut 120:525–528

    CAS  Google Scholar 

  • Hahn T, Schulz R (2002) Ecdysteroid synthesis and imaginal disc development in the midge Chironomus riparius as biomarkers for endocrine effects of tributyltin. Environ Toxicol Chem 21:1052–1057

    Article  CAS  Google Scholar 

  • Henrich VC (2005) The Ecdysteroid Receptor. In: Comprehensive Molecular Insect Science (Gilbert L.I. Iatrou K. and Gill S.S., eds.) Pergamon Press, vol. 3:243–285

  • Huang ZW, Shi P, Dai JQ, Du JW (2004) Protein metabolism in Spodoptera litura (F.) is influenced by the botanical insecticide azadirachtin. Pestic Biochem Physiol 80:85–93

    Article  CAS  Google Scholar 

  • Huet MC (2000) OECD activity on endocrine disrupters test guidelines development. Ecotoxicology 9:77–84

    Article  CAS  Google Scholar 

  • Irato P, Santovito G, Cassini A, Piccinni E, Albergoni V (2003) Metal accumulation and binding protein induction in Mytilus galloprovencialis, Scapharca inaequivalis, and Tapes philippinarum from the lagoon of Venice. Arch Environ Contam Toxicol 44:476–484

    Article  CAS  Google Scholar 

  • Janssens de Bisthoven L, Timmermans KR, Ollevier F (1992) The concentration of cadmium, lead, copper and zinc in Chironomus gr. thummi larvae (Diptera, Chironomidae) with deformed versus normal menta. Hydrobiologia 239:141–149

    Article  Google Scholar 

  • Kreutzweiser DP, Gunn JM, Thompson DG, Pollard HG, Faber MJ (1998) Zooplankton community responses to a novel forest insecticide, tebufenozide (RH-5992), in littoral lake enclosures. Can J Fish Aquat Sci 55:639–648

    Article  Google Scholar 

  • Larsson DGJ, Adolfson-Erici M, Parkkonen J, Pettersson M, Berg AH, Olsson PE, Förlin L (1999) Ethynylestradiol – an undesired fish contraceptive?Aquat Toxicol 45:91–97

    Article  CAS  Google Scholar 

  • LeBlanc GA (2006) Crustacean endocrine toxicology: a review Ecotoxicology, DOI: 10.1007/s10646-006-0115-z

  • Li TR, White KP (2003) Tissue-specific gene expression and ecdysone-regulated genomic networks in Drosophila. Dev Cell 5:59–72

    Article  CAS  Google Scholar 

  • Licht O, Jungmann D, Ludwichowski K-U, Nagel R (2004) Long-term effects of fenoxycarb on two mayfly species in artificial indoor streams. Environ Toxicol Chem 58:246–255

    CAS  Google Scholar 

  • Meregalli G, Pluymers L, Ollevier F (2001) Induction of mouthpart deformities in Chironomus riparius larvae exposed to 4-n-nonylphenol. Environ Pollut 111:241–246

    Article  CAS  Google Scholar 

  • Meregalli G, Ollevier F (2001) Exposure of Chironomus riparius larvae to 17α-ethynylestradiol: Effects on survival and mouthpart deformities. Sci Total Environ 269:157–161

    Article  CAS  Google Scholar 

  • OECD (2004a) OECD Guidelines for the testing of chemicals, Sediment-water chironomid toxicity test using spiked sediment, OECD 218, adopted 13 April 2004

  • OECD (2004b). OECD Guidelines for the testing of chemicals, Sediment-water chironomid toxicity test using spiked water, OECD 219, adopted 13 April 2004

  • Oetken M, Bachmann J, Schulte-Oehlmann U, Oehlmann J (2004) Evidence for endocrine disruption in invertebrates. Int Rev Cytol 236:1–44

    Article  CAS  Google Scholar 

  • Okita RT, Okita JR (1992) Effects of diethylphthalate and other plasticizers on laurate hydroxylation in rat-liver microsomes. Pharm Res 9:1648–1653

    Article  CAS  Google Scholar 

  • Patlak M (1996) A testing deadline for endocrine disruptors: EPA scrambles to develop a screening program for these complex substances. Environ Sci Technol 30:A540-A544

    Google Scholar 

  • Quack S, Fretz A, Spindler-Barth M, Spindler-Barth KD (1995) Receptor affinities and biological responses of nonsteroidal agonists on the epithelial cell line from Chironomus tentans (Diptera, Chironomidae). Eur J Entomol 92:341–347

    CAS  Google Scholar 

  • Rasmussen JB (1984) Comparison of gut contents and assimilation efficiency of fourth instar of two coexisting chironomids, Chironomus riparius Meigen and Glyptopendipes paripes (Edwards). Can J Zool 62:1022–1026

    Article  Google Scholar 

  • Riddiford LM, Hiruma K, Zhou XF, Nelson CA (2003) Insights into the molecular basis of the hormonal control of molting and metamorphosis from Manduca sexta and Drosophila melanogaster. Insect Biochem Mol Biol 33:1327–1338

    Article  CAS  Google Scholar 

  • Santillo D, Stringer RL, Johnston PA, Tickner J (1998) The precautionary principle: protecting against failures of scientific method and risk assessment. Mar Pollut Bull 36:939–950

    Article  CAS  Google Scholar 

  • Schulz R, Dabrowski JM (2001) Combined effects of predatory fish and sublethal pesticide contamination on the behaviour and mortality of mayfly nymphs. Environ Toxicol Chem 20:2537–2543

    Article  CAS  Google Scholar 

  • Segner H, Caroll K, Fenske M, Janssen CR, Maack G, Pascoe D, Schäfers C, Vandenbergh GF, Watts M, Wenzel A (2003) Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project. Ecotox Environ Safe 54:302–314

    Article  CAS  Google Scholar 

  • Smagghe G, Braeckman BP, Huys N, Raes H (2003) Cultured mosquito cells Aedes albopictus C6/36 (Dip, Culicidae) responsive to 20-hydroxyecdysone and non-steroidal ecdysone agonists. J Appl Entomol 127:167–173

    Article  CAS  Google Scholar 

  • Smagghe G, Dhadialla TS, Lezzi M (2002) Comparative toxicity and ecdysone receptor affinity of non-steroidal ecdysone agonists and 20-hydroxyecdysone in Chironomus tentans. Insect Biochem Mol Biol 32:187–192

    Article  CAS  Google Scholar 

  • Spindler-Barth M, Junger E, Spindler KD (1992) Vesicle formation and ecdysteroid induced cellular differentiation in the epithelial cell line of Chironomus tentans. Tissue Cell 24:919–934

    Article  Google Scholar 

  • Spindler-Barth M, Quack S, Rauch P, Spindler KD (1997) Biological effects of muristerone A and turkesterone on the epithelial cell line from Chironomus tentans (Diptera: Chironomidae) and correlation with binding affinity to the ecdysteroid receptor. Eur J Entomol 94:161–166

    CAS  Google Scholar 

  • Staples CA, Dorn PB, Klecka GM, O’Block ST, Harris LR (1998) A review of the environmental fate, effects and exposures of bispenol A. Chemosphere 36:2149–2173

    Article  CAS  Google Scholar 

  • Swevers L, Kravariti L, Ciolfi S, Xenou-Kokoletsi M, Wong G, Ragousis N, Smagghe G, Nakagawa Y, Mazomenos V, Iatrou K (2003) A high-throughput screening system for fast detection of ecdysteroid mimetic and antagonistic substances using transformed Bombyx mori-derived cell lines. FASEB J 17:134–136

    Google Scholar 

  • Taenzler V, Bruns E, Dorgerloh M, Pfeifle V, Weltje L (2006) Chironomids: suitable test organisms for risk assessment investigations on the potential endocrine disrupting properties of pesticides. Ecotoxicology, DOI: 10.1007/s10646-006-0117-x

  • Trisyono A, Goodman CL, Grasela JJ, McIntosh AH, Chippendale GM (2000) Establishment and characterization of an Ostrinia nubilalis cell line, and its response to ecdysone agonists. In Vitro Cell Dev Biol-Anim 36:400–404

    Article  CAS  Google Scholar 

  • USEPA (2000). Methods for measuring the toxicity and bioaccumulation of sediment-associated contaminants with freshwater invertebrates, 2nd ed. Duluth MN and Washington DC: EPA 600/R-99/064

  • van der Geest HG, Greve GD, Boivin ME, Kraak MHS, van Gestel CAM (2000a) Mixture toxicity of copper and diazinon to larvae of the mayfly (Ephoron virgo) judging additivity at different effect levels. Environ Toxicol Chem 19:2900–2905

    Article  Google Scholar 

  • van der Geest HG, Greve GD, Kroon A, Kuijl S, Kraak MHS, Admiraal W (2000b) Sensitivity of characteric riverine insects, the caddisfly Cyrnus trimaculatus and the mayfly Ephoron virgo, to copper and diazinon. Environ Pollut 109:177–182

    Article  Google Scholar 

  • van der Geest HG, Soppe WJ, Greve GD, Kroon H, Kraak MHS (2002) Combined effects of lowered oxygen and toxicants (copper and diazinon) on the mayfly Ephoron virgo. Environ Toxicol Chem 21:431–436

    Article  Google Scholar 

  • Watts MM, Pascoe D, Carroll K (2001) Chronic exposure to 17α-ethynylestradiol and bisphenol A effects on development and reproduction in the freshwater invertebrate Chironomus riparius (Diptera: Chironomidae). Aquat Toxicol 55:113–124

    Article  CAS  Google Scholar 

  • Watts MM, Pascoe D, Caroll K (2003) Exposure to 17α-ethynylestradiol and bisphenol A – effects on larval moulting and mouthpart structure of Chironomus riparius. Ecotox Environ Safe 54:207–215

    Article  CAS  Google Scholar 

  • Wing KD (1988) RH-5849, a nonsteroidal ecdysone agonist: effects on a Drosophila cell line. Science 241:467–468

    Article  CAS  Google Scholar 

  • Wurtz J-M, Guillot B, Fagart J, Moras D, Tietjen K, Schindler M (2000). A new model for 20-hydroxyecdyson and dibenzoylhydrazine binding: a homology modeling and docking approach. Protein Sci 9:1073–1084

    Article  CAS  Google Scholar 

  • Yao T, Forman B, Jiang Z, Cherbas L, Chen J, McKeown M, Cherbas P, Evans R (1993) Functional ecdysone receptor is the product of EcR and Ultraspiracle genes. Nature 366:476–479

    Article  CAS  Google Scholar 

  • Yin CM, Zou BX, Jiang M, Li MF, Qin W, Potter TL, Stoffolano JG (1995) Identification of juvenile hormone III bisepoxide (JHB3), juvenile hormone III and methyl farnesoate secreted by the corpus allatum of Phormia regina (Meigen), in vitro and function of JHB3 either applied alone or as a part of a juvenoid blend. J Insect Physiol 41:473–479

    Article  CAS  Google Scholar 

  • Yin CM, Zou BX, Li MF, Stoffolano JG (1994) Discovery of a midgut peptide-hormone which activates the endocrine cascade leading to oogenesis in Phormia regina (Meigen). J Insect Physiol 40:283–292

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Agrozoology, Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Coupure links 653, B-9000, Ghent, Belgium

    Thomas Soin & Guy Smagghe

Authors
  1. Thomas Soin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guy Smagghe
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Thomas Soin.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Soin, T., Smagghe, G. Endocrine disruption in aquatic insects: a review. Ecotoxicology 16, 83–93 (2007). https://doi.org/10.1007/s10646-006-0118-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-006-0118-9

Keywords

Search

Navigation