Skip to main content
Log in

Vitellogenin-like gene expression in freshwater amphipod Gammarus fossarum (Koch, 1835): functional characterization in females and potential for use as an endocrine disruption biomarker in males

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The induction of vitellogenin (Vtg) synthesis is widely accepted as a biomarker of estrogenic exposure in male and juvenile fish. Vtg synthesis has emerged as an interesting endpoint to assess endocrine disruptor (ED) effects in crustaceans. However, studies reporting induction of Vtg in male crustaceans are lacking. This study investigated the expression of the Vtg gene in a freshwater amphipod, Gammarus fossarum, using calibrated real-time reverse transcription polymerase chain reaction (real-time RT PCR). First, we described the basal pattern of expression in healthy male and female organisms at different reproductive moult stages, in order to validate the function of this gene. Females expressed from 200 to 700 times more Vtg transcripts than males, depending on the female reproductive stage. Females displayed significant elevation of Vtg mRNA levels at the end of the inter-moult phase and at the beginning of the pre-moult phase. Second, male gammarids were exposed to the estrogenic compound nonylphenol (NP) (0.05, 0.5, 5 and 50 μg L−1) and to the anti-androgen cyproterone (1, 10, 100 and 1000 μg L−1) for 2, 4, 8 and 16 days. Both chemicals altered the pattern of interindividual variability of Vtg gene expression in males with strong induction in some individuals. Finally, the impact of urban wastewater treatment plants (WWTP) on male Vtg gene expression was assessed in organisms transplanted in the field during in situ bioassay campaigns in three different watersheds. Induction of the Vtg mRNA level was observed in males transplanted downstream from WWTP effluent discharge in two of the three study sites.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • An L, Hu J, Zhang Z, Yang M (2006) Quantitative real-time RT-PCR for determination of vitellogenin mRNA in so-iuy mullet (Mugil soiuy). Anal Bioanal Chem 386:1995–2001

    Article  CAS  Google Scholar 

  • Ayaki T, Kawauchino Y, Nishimura C, Ishibashi H, Arizono K (2005) Sexual disruption in the freshwater crab (Geothelphusa dehaani). Integr Comp Biol 45(1):39–42

    Article  Google Scholar 

  • Baldwin WS, Milam DL, Leblanc GA (1995) Physiological and biochemical perturbations in Daphnia magna following exposure to the model environmental estrogen diethylstilbestrol. Environ Toxicol Chem 14(6):945–952

    CAS  Google Scholar 

  • Billinghurst Z, Clare AS, Matsumura K, Depledge MH (2000) Induction of cypris major protein in barnacle larvae by exposure to 4-n-nonylphenol and 17[beta]-oestradiol. Aquat Toxicol 47(3–4):203–212

    Article  CAS  Google Scholar 

  • Blackburn MA, Waldock MJ (1995) Concentrations of alkylphenols in rivers and estuaries in England and Wales. Water Res 29(7):1623–1629

    Article  CAS  Google Scholar 

  • Blanchet-Tournier M-F (1980) Mue et vitellogénèse chez le crustacé amphipode Orchestia gammarelus (PALLAS) : Controles endocries et interactions. Université Pierre et Marie Curie (Paris 6), Paris

  • Bosker T, Munkittrick KR, MacLatchy DL (2010) Challenges and opportunities with the use of biomarkers to predict reproductive impairment in fishes exposed to endocrine disrupting substances. Aquat Toxicol 100:9–16

    Article  CAS  Google Scholar 

  • Brown RJ, Conradi M, Depledge MH (1999) Long-term exposure to 4-nonylphenol affects sexual differentiation, growth of the amphipod Corophium volutator (Pallas, 1766). Sci Total Environ 233(1–3):77–88

    Article  CAS  Google Scholar 

  • Charniaux-Cotton H (1954) Découverte chez un Crustacé Amphipode (Orchestia gammarella) d’une glande endocrine responsable de la différenciation des caractères sexuels primères et secondères mâles. CR Acad Sc Paris 239:780–782

    CAS  Google Scholar 

  • Charniaux-Cotton H (1973) Description et contrôle de l’ovogénèse chez les Crustacés supérieurs. Ann Biol Anim Biochem Biophysiol 13(hors série):21–30

    Google Scholar 

  • Colborn T, Vom Saal FS, Soto AM (1993) Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 101:11–55

    Article  Google Scholar 

  • Dedourge-Geffard O, Palais F, Biagianti-Risbourg S, Geffard O, Geffard A (2009) Effects of metals on feeding rate and digestive enzymes in Gammarus fossarum: an in situ experiment. Chemosphere 11:1569–1576

    Article  Google Scholar 

  • deFur PL (2004) Use of invertebrates in testing for endocrine disruptors. Inst Lab Anim Res J 45(4):484–493

    CAS  Google Scholar 

  • deFur P, Crane M, Ingersoll C, Tattersfield L (1999) Endocrine disruption in invertebrates: endocrinology testing and assessment. SETAC Press, Pensacola

    Google Scholar 

  • Desbrow C, Routledge EJ, Brighty GC, Sumpter JP, Waldock MJ (1998) Identification of oestrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitro biological screening. Environ Sci Technol 32:1549–1558

    Article  CAS  Google Scholar 

  • Ford AT (2008) Can you feminise a crustacean? Aquat Toxicol 88(4):316–321

    Article  CAS  Google Scholar 

  • Ford AT, Fernandes TF, Rider SA, Read PA, Robinson CD, Davies IM (2004) Endocrine disruption in a marine amphipod? Field observations of intersexuality and de-masculinisation. Mar Environ Res 58(2–5):169–173

    Article  CAS  Google Scholar 

  • Friberg N, Andersen TH, Hansen HO, Iversen TM, Jacobsen D, Krojgaard L, Larsen SE (1994) The effect brown trout (Salmo trutta L.) on stream invertebrate drift, with specieal reference to Gammarus pulex (L.). Hydrobiologia 294:105–110

    Article  Google Scholar 

  • Gagné F, Blaise C (2004) Shell protein characteristics and vitellogenin-like proteins in brine shrimp Artemia franciscana exposed to municipal effluent and 20-hydroxyecdysone. Comp Biochem Physiol C 138(4):515–522

    Article  Google Scholar 

  • Gagné F, Blaise C, Pellerin J (2005) Altered exoskeleton composition and vitellogenesis in the crustacean Gammarus sp. collected at polluted sites in the Saguenay Fjord, Quebec, Canada. Environ Res 98(1):89–99

    Google Scholar 

  • García-Reyero N, Raldúa D, Quirós L, Llaveria G, Cerdà J, Barceló D, Grimalt JO, Piña B (2004) Use of vitellogenin mRNA as a biomarker for endocrine disruption in feral and cultured fish. Anal Bioanal Chem 378(3):670–675

    Article  Google Scholar 

  • Geffard O, Xuereb B, Chaumot A, Geffard A, Biagianti S, Noël C, Abbaci K, Garric J, Charmantier G, Charmantier-Daures M (2010) Ovarian cycle and embryonic development in Gammarus fossarum: application for reproductive toxicity assessment. Environ Toxicol Chem 29:2249–2259

    Article  CAS  Google Scholar 

  • Ghekiere A, Verslycke T, Fockedey N, Janssen CR (2006a) Non-target effects of the insecticide methoprene on molting in the estuarine crustacean Neomysis integer (Crustacea: Mysidacea). J Exp Mar Biol Ecol 332:226–234

    Article  CAS  Google Scholar 

  • Ghekiere A, Verslycke T, Janssen C (2006b) Effects of methoprene, nonylphenol, and estrone on the vitellogenesis of the mysid Neomysis integer. Gen Comp Endocrinol 147(2):190–195

    Article  CAS  Google Scholar 

  • Gross MY, Maycock DS, Thorndyke MC, Morritt D, Crane M (2001) Abnormalities in sexual development of the amphipod Gammarus pulex (L.) found below sewage treatment works. Environ Toxicol Chem 20(8):1792–1797

    Google Scholar 

  • Huang DJ, Chen HC (2004) Effects of chlordane and lindane on testosterone and vitellogenin levels in green neon shrimp (Neocaridina denticulata). Int J Toxicol 23(2):91–95

    Article  CAS  Google Scholar 

  • Huang D-J, Chen H-C, Wu J-P, Wang S-Y (2006) Reproduction obstacles for the female green neon shrimp (Neocaridina denticulata) after exposure to chlordane and lindane. Chemosphere 64(1):11–16

    Article  CAS  Google Scholar 

  • Jasmani S, Kawazoe I, Shih TW, Suzuki Y, Aida K (2000) Hemolymph vitellogenin levels during ovarian development in the kuruma prawn Penaeus japonicus. Fish Sci 66(3):535–539

    Article  CAS  Google Scholar 

  • Jasmani S, Ohira T, Jayasankar V, Tsutsui N, Aida K, Wilder MN (2004) Localization of vitellogenin mRNA expression and vitellogenin uptake during ovarian maturation in the giant freshwater prawn Macrobrachium rosenbergii. J Exp Zool A 301(4):334–343

    Google Scholar 

  • Jayasankar V, Tsutsui N, Jasmani S, Saido-Sakanaka H, Yang WJ, Okuno A, Hien TTT, Aida K, Wilder MN (2002) Dynamics of vitellogenin mRNA expression and changes in hemolymph vitellogenin levels during ovarian maturation in the giant freshwater prawn Macrobrachium rosenbergii. J Exp Zool 293(7):675–682

    Article  CAS  Google Scholar 

  • Jungmann D, Ladewig V, Ludwichowski K-U, Petzsch P, Nagel R (2004) Intersexuality in Gammarus fossarum KOCH—a common inducible phenomenon? Arch Hydrobiol 159(4):511–529

    Article  Google Scholar 

  • Kavlock RJ, Daston GP, DeRosa C, Fenner-Crisp P, Gray LE, Kaattari S, Lucier G, Luster M, Mac MJ, Maczka C, Miller R, Moore J, Rolland R, Scott G, Sheehan DM, Sinks T, Tilson HA (1996) Research needs for the risk assessment of health and environmental effects of endocrine disruptors: a report of the U.S. EPA-sponsored workshop. Environ Health Perspect 104:715–740

    Google Scholar 

  • Kidd KA, Blanchfield PJ, Mills KH, Palace VP, Evans RE, Lazorchack JM, Flick RW (2007) Collapse of a fish population after exposure to a synthetic estrogen. PNAS 104(21):8897–8901

    Article  CAS  Google Scholar 

  • Kiparissis Y, Metcalfe TL, Balch GC, Metcalfe CD (2003) Effects of the antiandrogens, vinclozolin and cyproterone acetate on gonadal development in the Japanese medaka (Oryzias latipes). Aquat Toxicol 63(4):391–403

    Article  CAS  Google Scholar 

  • Langston WJ, Burt GR, Chesman BS, Vane CH (2005) Partioning, bioavailability and effects of oestrogens and xeno-oestrogens in aquatic environment. J Mar Biol Assoc UK 85:1–31

    Article  CAS  Google Scholar 

  • Larkin P, Knoebl I, Denslow ND (2003) Differential gene expression analysis in fish exposed to endocrine disrupting compounds. Comp Biochem Physiol B 136(2):149–161

    Article  CAS  Google Scholar 

  • LeBlanc GA (2007) Crustacean endocrine toxicology: a review. Ecotoxicology 16(1):61–81

    Article  CAS  Google Scholar 

  • LeBlanc GA, Campbell P, den Besten P, Brown R, Chang E, Coats J, deFur P, Dhadialla T, Edwards J, Riddiford L, Simpson M, Snell T, Thorndyke M, Matsumura F (1999) The endocrinology of invertebrates. In: deFur P, Crane M, Ingersoll C, Tattersfield L (eds) Endocrine disruption in invertebrates: endocrinology, testing and assessment. SETAC Press, Pensacola, pp 23–106

  • Lee FY, Chang CF (1997) The concentrations of vitellogenin (vitellin) and protein in hemolymph, ovary and hepatopancreas in different ovarian stages of the freshwater prawn, Macrobrachium rosenbergii. Comp Biochem Physiol A 117(4):433–439

    Article  CAS  Google Scholar 

  • Lee K-W, Hwang D-S, Rhee J-S, Ki J-S, Park HG, Ryu JC, Raisuddin S, Lee J-S (2008) Molecular cloning, phylogenetic analysis and developmental expression of a vitellogenin (Vg) gene fron the intertidal copepod, Tigriopus japonicus. Comp Biochem Physiol B 150(4):395–402

    Article  Google Scholar 

  • 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 154(3):289–297

    Article  Google Scholar 

  • MacNeil C, Dick JTA, Bigsby E, Elwood RW, Montgomery WI, Gibbins CN, Kelly DW (2002) The validity of the Gammarus: Asellus ratio as an index of organic pollution: abiotic and biotic influences. Water Res 36:75–84

    Article  CAS  Google Scholar 

  • Maltby L, Clayton SA, Wood RM, McLoughlin N (2002) Evaluation of the Gammarus pulex in situ feeding assay as a biomonitor of water quality: robustness, responsiveness, and relevance. Environ Toxicol Chem 21(2):361–368

    CAS  Google Scholar 

  • Maltret-Geraudie P, Gerbron M, Minier C (2008) Estrogenic response of wild roach from the Seine River (France). Cybium 32(2):256–257

    Google Scholar 

  • Markey CM, Rubin BS, Soto AM, Sonnenschein C (2003) Endocrine disruptors: from Wingspread to environmental developmental biology. J Steroid Biochem 83:235–244

    Google Scholar 

  • Martin-Diaz M, Sales D, Del Valls TA (2004) Influence of salinity in hemolymph vitellogenin of the shore crab Carcinus maenas, to be use as a biomarker of contamination. Bull Environ Contam Toxicol 73:870–877

    Article  CAS  Google Scholar 

  • Matozzo V, Gagné F, Marin MG, Ricciardi F, Blaise C (2008) Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: a review. Environ Int 34(4):531–545

    Article  CAS  Google Scholar 

  • Matthiessen P (2003) Endocrine disruption in marine fish. Pure Appl Chem 75:2249–2261

    Article  CAS  Google Scholar 

  • Mazurová E, Hilscherová K, Triebskorn R, Köhler H-R, Maršálek B, Bláha L (2008) Endocrine regulation of the reproduction in crustaceans: identification of potential targets for toxicants and environmental contaminants. Biologia 63(2):139–150

    Article  Google Scholar 

  • Meusy J-J, Junera HYC (1974) Données sur la synthèse de la fraction protéique femelle chez Orchestia gammarella Palas (Crustacé Amphipode), au cours de l’intermue et chez les femelles en repos sexuel. CR Acad Sc Paris 279:587–590

    CAS  Google Scholar 

  • Moffat LT, May CL, Studer KE, Reckhow DA, Arcaro (2010) Effects of exposure water volume, depuration time, and feeding status on vitellogenin RNA induction in male madaka (Oryzias latipes) exposed to 17β-estradiol. Ecotoxicol Environ Saf 73:1835–1841

    Article  Google Scholar 

  • Moore CG, Stevenson JM (1991) The occurrence of intersexuality in harpacticoid copepods and its relationship with pollution. Mar Pollut Bull 22:72–74

    Article  Google Scholar 

  • Moore CG, Stevenson JM (1994) Intersexuality in benthic harpacticoid copepods in the Firth of Forth, Scotland. J Nat Hist 28:1213–1230

    Article  Google Scholar 

  • Nagabushanam R, Kulkarni GK (1981) Effect of exogenous testosterone on the androgenic gland and testis of a marine penaeid prawn, Parapenaeopsis hardwickii (Miers) (Crustacea, Decapoda, Penaeidae). Aquaculture 23:19–27

    Article  Google Scholar 

  • Nakamura A, Yasuda K, Adachi H, Sakurai Y, Ishii N, Goto S (1999) Vitellogenin-6 is a major carbonylated protein in aged nematode, Caenorhabditis elegans. Biochem Biophys Res Commun 264:580–583

    Article  CAS  Google Scholar 

  • Oberdorster E, Rice CD, Irwin LK (2000) Purification of vitellin from grass shrimp Palaemonetes pugio, generation of monoclonal antibodies, and validation for the detection of lipovitellin in Crustacea. Comp Biochem Physiol C 127(2):199–207

    CAS  Google Scholar 

  • Oetken M, Bachmann J, Schulte-Oehlmann U, Oehlmann J, Kwang WJ (2004) Evidence for endocrine disruption in invertebrates. In: International review of cytology, vol 236. Academic Press, pp 1–44

  • Okumura T, Aida K (2000a) Fluctuations in hemolymph ecdysteroid levels during the reproductive and non-reproductive molt cycles in the giant freshwater prawn Macrobrachium rosenbergii. Fish Sci 66(5):876–883

    Article  CAS  Google Scholar 

  • Okumura T, Aida K (2000b) Hemolymph vitellogenin levels and ovarian development during the reproductive and non reproductive molt cycles in the giant freshwater prawn Macrobrachium rosenbergii. Fish Sci 66(4):678–685

    Article  CAS  Google Scholar 

  • Okumura T, Yamano K, Sakiyama K (2007) Vitellogenin gene expression and hemolymph vitellogenin during vitellogenesis, final maturation, and oviposition in female kuruma prawn, Marsupenaeus japonicus. Comp Biochem Physiol A 147(4):1028–1037

    Article  Google Scholar 

  • Olmstead AW, LeBlanc GL (2001) Low exposure concentration effects of methoprene on endocrine-regulated processes in the Crustacean Daphnia magna. Toxicol Sci 62(2):268–273

    Article  CAS  Google Scholar 

  • Poynton HC, Varshavsky JR, Chang B, Cavigiolio G, Chan S, Holman PS, Loguinov AV, Bauer DJ, Komachi K, Theil EC, Perkins EJ, Hughes O, Vulpe CD (2007) Daphnia magna ecotoxicogenomics provides mechanistic insights into metal toxicity. Environ Sci Technol 41:1044–1050

    Article  CAS  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rinderhagen M, Ritterhoff J, Zauke G-P (2000) Crustaceans as bioindicators. In: Gerhardt A (ed) Biomonitoring of polluted warter—reviews on actual topics, environmental research forum, vol 9. Trans Tech Publications–Scitech Publications, Zürich, pp 161–194

    Google Scholar 

  • Sagi A, Khalaila I, Abdu U, Shoukrun R, Weil S (1999) A newly established ELISA showing the effect of androgenic gland on secondary-vitellogenic-specific protein in the hemolymph of the crayfish Cherax quadricarinatus. Gen Comp Endocrinol 115:37–45

    Article  CAS  Google Scholar 

  • Sanders MB, Billinghurst Z, Depledge MH, Clare AS (2005) Larval development and vitellin-like protein expression in Palaemon elegans larvae following xeno-oestrogen exposure. Integr Comp Biol 45(1):51–60

    Article  CAS  Google Scholar 

  • Sarojini S (1963) Comparison of the effects of androgenic hormone and testosterone propionate on the female ocypod crab. Curr Sci 32:411–412

    CAS  Google Scholar 

  • Schirling M, Jungmann D, Ladewig V, Nagel R, Triebskorn R, Köhler H-R (2005) Endocrine effects in Gammarus fossarum (Amphipoda): influence of wastewater effluents, temporal variability, and spatial aspects on natural populations. Arch Environ Contam Toxicol 49:53–61

    Article  CAS  Google Scholar 

  • Schirling M, Jungmann D, Ladewig V, Ludwichowski KU, Nagel R, Kohler HR, Triebskorn R (2006) Bisphenol A in artificial indoor streams: II. Stress response and gonad histology in Gammarus fossarum (Amphipoda). Ecotoxicology 15(2):143–156

    Google Scholar 

  • Seehuus SC, Norberg K, Gimsa U, Krekling T, Amdam GV (2006) Reproductive protein protects functionally sterile honey bee workers from oxidative stress. PNAS 103:962–967

    Article  CAS  Google Scholar 

  • Sharpe RL, MacLatchy DL, Courtenay SC, Van Der Kraak GJ (2004) Effects of a model androgen (methyl testosterone) and a model anti-androgen (cyproterone acetate) on reproductive endocrine endpoints in a short-term adult mummichog (Fundulus heteroclitus) bioassay. Aquat Toxicol 67(3):203–215

    Article  CAS  Google Scholar 

  • Shechter A, Aflalo ED, Davis C, Sagi A (2005) Expression of the reproductive female-specific vitellogenin gene in endocrinologically induced male and intersex Cherax quadricarinatus crayfish. Biol Reprod 73:72–79

    Article  CAS  Google Scholar 

  • Shi XD, Zhang SC, Pang QX (2006) Vitellogenin is a novel player in defense reactions. Fish Shellfish Immunol 20:769–772

    Article  CAS  Google Scholar 

  • Soares A, Guieysse B, Jefferson B, Cartmell E, Lester JN (2008) Nonylphenol in the environment: a critical review on occurrence, fate, toxicity and treatment in wastewaters. Environ Int 34(7):1033–1049

    Article  CAS  Google Scholar 

  • Subramoniam T (2000) Crustacean ecdysteriods in reproduction and embryogenesis. Comp Biochem Physiol C 125(2):135–156

    CAS  Google Scholar 

  • Suzuki S, Yamasaki K, Katakura Y (1990) Vitellogenin synthesis in andrectomized males of the terrestrial isopod, Armadillidium vulgare (Malacostracan Crustacea). Gen Comp Endocrinol 77(2):283–291

    Article  CAS  Google Scholar 

  • Tahara D, Suitoh K, Hattori H (2005) Hemolymph vitellogenin levels during final maturation and post-spawning in the female kuruma prawn, Marsupenaeus japonicus. Aquaculture 245(1–4):311–319

    Article  CAS  Google Scholar 

  • Takahashi T, Araki A, Nomura Y, Koga M, Arizono K (2000) The occurrence of dual-gender imposex in Japanese freshwater crab. J Health Sci 46(5):376–379

    CAS  Google Scholar 

  • Tiu SHK, Hui JHL, Mak ASC, He JG, Chan SM (2006) Equal contribution of hepatopancreas and ovary to the production of vitellogenin (PmVg1) transcripts in the tiger shrimp, Penaeus monodon. Aquaculture 254(1–4):666–674

    Article  CAS  Google Scholar 

  • Vandenbergh GF, Adriaens D, Verslycke T, Janssen CR (2003) Effects of 17[alpha]-ethinylestradiol on sexual development of the amphipod Hyalella azteca. Ecotoxicol Environ Saf 54(2):216–222

    Article  CAS  Google Scholar 

  • Volz DC, Chandler GT (2004) An enzyme-linked immunosobent assay for lipovitellin quantification in Copepods: a screening tool for endocrine toxicity. Environ Toxicol Chem 23(2):298–305

    Article  CAS  Google Scholar 

  • Volz DC, Wirth EF, Fulton MH, Scott GI, Strozier E, Block DS, Ferry JL, Walse SS, Chandler GT (2003) Effects of fipronil and chlorpyrifos on endocrine-related endpoints in female grass shrimp (Palaemonetes pugio). Bull Environ Contam Toxicol 71(3):497–503

    Article  CAS  Google Scholar 

  • Watts MM, Pascoe D, Carroll K (2001) Survival and precopulatory behaviour of Gammarus pulex (L.) exposed to two xenoestrogens. Water Res 35(10):2347–2352

    Google Scholar 

  • Welton JS (1979) Life-history and production of the amphipod Gammarus pulex in a Dorset chalk stream. Freshw Biol 9:263–285

    Article  Google Scholar 

  • Wollenberger L, Kusk KO (2006) Gonad histology of copepods exposed to (anti)androgens. In: Paper presented at the poster presented at controversies and solutions in environmental sciences; 16th annual meeting of the SETAC Europe, The Hague (Netherlands), 7–11 May 2006

  • Wouters R, Piguave X, Bastidas L, Calderon J, Sorgeloos P (2001) Ovarian maturation and haemolymphatic vitellogenin concentration of Pacific white shrimp Litopenaeus vannamei (Boone) fed increasing levels of total dietary lipids and HUFA. Aquac Res 32(7):573–582

    Article  CAS  Google Scholar 

  • Yang G, Kille P, Ford AT (2008) Infertility in a marine crustacean: have we been ignoring pollution impacts on male invertebrates? Aquat Toxicol 88:81–87

    Article  CAS  Google Scholar 

  • Zhang SC, Sun YN, Pang QX, Shi XD (2005) Hemagglutinating and antibacterial activities of vitellogenin. Fish Shellfish Immunol 19:93–95

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors wish to thank the French National Research Programs PNRPE (Convention n°CV05000088 and Convention n°0006942), ECCO (Convention n°06CV050) and ECOGER (Convention no. 20-2006), the Rhône-Méditerranée-Corse water agency, the Cluster Environnement Région Rhône-Alpes and the GIS Environalp for partial financial support. B. George and C. Moulin are acknowledged for their technical assistance. The authors also wish to thank the anonymous reviewers for providing very helpful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Olivier Geffard.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xuereb, B., Bezin, L., Chaumot, A. et al. Vitellogenin-like gene expression in freshwater amphipod Gammarus fossarum (Koch, 1835): functional characterization in females and potential for use as an endocrine disruption biomarker in males. Ecotoxicology 20, 1286–1299 (2011). https://doi.org/10.1007/s10646-011-0685-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-011-0685-2

Keywords

Navigation