Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-22T17:47:46.740Z Has data issue: false hasContentIssue false
  • English
  • Français

Reproductive effects of endocrine disrupting chemicals, bisphenol-A and 17β-oestradiol, on Cerastoderma edule from south-west England: field study and laboratory exposure

Published online by Cambridge University Press:  11 April 2016

Amy L. Lusher Open the ORCID record for Amy L. Lusher [Opens in a new window] ,
Nick Pope  and
Richard D. Handy
Amy L. Lusher*
Affiliation:
The Marine Biological Association of the United Kingdom, Citadel Hill, Plymouth PL1 2PB, UK
Nick Pope
Affiliation:
The Marine Biological Association of the United Kingdom, Citadel Hill, Plymouth PL1 2PB, UK
Richard D. Handy
Affiliation:
School of Biomedical and Biological Sciences, Plymouth University, Drake Circus, Plymouth PL4 8AA, UK
*
Correspondence should be addressed to:A. Lusher, The Marine Biological Association of the United Kingdom, Citadel Hill, Plymouth PL1 2PB, UK email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Endocrine disruption has rarely been reported in field populations of the edible cockle and the context with the general health of the shellfish is unclear. This study examined the reproductive state of two Cerastoderma edule populations over a 6-month period to assess their reproductive condition, the incidence of intersex and presence of parasitic infection. A further seven native sites from south-west England were examined during the peak reproductive season to identify the presence of intersex within the region. Laboratory exposures of organisms collected from field populations showed a significantly female-biased sex ratio compared with controls when exposed to the endocrine disrupting chemicals, bisphenol-A (nominal concentration: 0.1 µg L−1) and 17β-oestradiol (nominal concentration: 0.1 µg L−1), but none of the chemical exposures induced intersex. Intersex was revealed in seven out of the nine native populations of C. edule sampled at peak reproductive season. The highest incidence and most severe case of intersex were reported at Lower Anderton on the River Tamer which also had a significantly female-biased sex ratio. Additionally, the dominant trematode family was the Bucephalaidae. Parasitic infection influences the maturity of C. edule by lowering both mean gonad index and condition index. These results suggest that endocrine disrupting chemicals could be contributing factors towards the development of intersex in C. edule.

Keywords

Gametogenesismortalityparasitesoestrogen mimicsE2BPA
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Issue 2 , March 2017 , pp. 347 - 357
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aarab, N., Lemaire-Gony, S., Unruh, E., Hansen, P.D., Larsen, B.K., Andersen, O.K. and Narbonne, J.F. (2006) Preliminary study of responses in mussel (Mytilus edulis) exposed to bisphenol A, diallyl phthalate and tetrabromodiphenyl ether. Aquatic Toxicology 78 (S-1), S86–S92.CrossRefGoogle ScholarPubMed
Azevedo, C., Conchas, R.F. and Montes, J. (2003) Description of Haplosporidium edule n. sp. (Phylum Haplosporidia), a parasite of Cerastoderma edule (Mollusca, Bivalvia) with complex spore ornamentation. European Journal of Protistology 39, 161–167.CrossRefGoogle Scholar
Bauer, B., Fioroni, P., Ide, I., Liebe, S., Oehlmann, J., Stroben, E. and Watermann, B. (1995) TBT effects on the female genital system of Littorina littorea: a possible indicator of tributyltin pollution. Hydrobiologia 309, 15–27.Google Scholar
Boyden, C.R. (1971) A comparative study of the reproductive cycles of the cockles Cerastoderma edule and C. glaucum . Journal of the Marine Biological Association of the United Kingdom 51, 605–622. doi: 10.1017/S0025315400014995.CrossRefGoogle Scholar
Bryan, G.W., Gibbs, P.E., Burt, G.R. and Hummerstone, L.G. (1987) The effects of tributyltin (TBT) accumulation on adult dog-whelks, Nucella lapillus: long-term field and laboratory experiments. Journal of the Marine Biological Association of the United Kingdom 67, 525–544.Google Scholar
Burdon, D., Callaway, R., Elliott, M., Smith, T. and Wither, A. (2014) Mass mortalities in bivalve populations: a review of the edible cockle Cerastoderma edule (L.). Estuarine, Coastal and Shelf Science. doi: 10.1016/j.ecss.2014.04.011.Google Scholar
Chesman, B.S. and Langston, W.J. (2006) Intersex in the clam Scrobicularia plana: a sign of endocrine disruption in estuaries? Biology Letters 22, 420–422.Google Scholar
De Montaudouin, X., Thieltges, D.W., Gam, M., Krakau, M., Pina, S., Bazairi, H., Dabouineau, L., Russell-Pinto, F. and Jensen, K.T. (2009) Digenean trematode species in the cockle Cerastoderma edule: identification key and distribution along the north-eastern Atlantic shoreline. Journal of the Marine Biological Association of the United Kingdom 89, 543–556.CrossRefGoogle Scholar
Derbali, A., Jarboui, O. and Ghorbel, M. (2009) Reproductive biology of the cockle Cerastoderma glaucum (Mollusca: Bivalvia). Ciencias Marinas 35, 141–152.CrossRefGoogle Scholar
Desbrow, C., Routledge, E., Sheehan, D., Waldock, M. and Sumpter, J. (1996) The identification and assessment of oestrogenic substances in sewage treatment works effluents. Bristol: Environmental Agency, 76 pp.Google Scholar
Environment Agency (EA) (2009) River Basin Management Plan, South West River Basin District Main Document. 77 pp. Available at http://www.environment-agency.gov.uk/research/planning/125027.aspx (Accessed 5 July 2012).Google Scholar
Gosling, E. (2003) Bivalve molluscs: biology, ecology and culture. Oxford: Blackwell Publishing, p. 146.Google Scholar
Gravato, C., Guimarães, L., Santos, J., Faria, M., Alves, A. and Guilhermino, L. (2010) Comparative study about the effects of pollution on glass and yellow eels (Anguilla anguilla) from the estuaries of Minho, Lima and Douro Rivers (NW Portugal). Ecotoxicology and Environmental Safety 73, 524–533.Google Scholar
Hancock, D.A. and Franklin, A. (1972) Seasonal changes in the condition of the edible cockle (Cardium edule L.). Journal of Applied Ecology 9, 567–579.Google Scholar
Handy, R.D., Runnalls, T. and Russell, P.M. (2002) Histopathologic biomarkers in three spined sticklebacks, Gasterosteus aculeatus, from several rivers in Southern England that meet the freshwater fisheries directive. Ecotoxicology 11, 467–479.Google Scholar
Heemken, O.P., Reincke, H., Stachel, B. and Theobald, N. (2001) The occurrence of xenoestrogens in the Ebe river and the North Sea. Chemosphere 45, 245–259.CrossRefGoogle Scholar
Hutchinson, T.H. (2002) Reproductive and developmental effects of endocrine disruptors in invertebrates: in vitro and in vivo approaches. Toxicology Letters 131, 75–81.Google Scholar
James, B.L. and Bowers, E.A. (1967) Reproduction in the daughter sporocyst of Cercaria bucephalopsis haimeana (Lacaze-Duthiers, 1854) (Bucephalidae) and Cercaria dichotoma Lebour, 1911 (non Müller) (Gymnophallidae). Parasitology 57, 607–625.Google Scholar
Johnstone, J. (1899) Cardium. Number II. Liverpool, UK: Liverpool Marine Biology Committee Memoirs.Google Scholar
Lai, K.M., Scrimshaw, M.D. and Lester, J.N. (2002) Predication of the bioaccumulation factors and body burden of natural and synthetic estrogens in aquatic organisms in the river systems. Science of the Total Environment 289, 159–168.Google Scholar
Langston, W.J., Burt, G.R. and Chesman, B.S. (2007) Feminisation of male clams Scrobicularia plana from estuaries in South West UK and its induction by endocrine-disrupting chemicals. Marine Ecology Progress Series 333, 173–184.Google Scholar
Liu, R., Zhou, J.L. and Wilding, A. (2004) Microwave-assisted extraction followed by gas chromatography–mass spectrometry for the determination of endocrine disrupting chemicals in river sediments. Journal of Chromatography A, 1038, 19–26.Google Scholar
Luckenbach, M.W., deFur, P., Kellogg, M.L. and Van Veld, P. (2010) Potential effects of endocrine disrupting compounds on bivalve population in Chesapeake Bay: a review of current knowledge and assessment of research needs. CRC Publication No. 10–170. Edgewater, MD: Chesapeake Research Consortium, 32 pp.Google Scholar
Marcogliese, D.J. and Pietrock, M. (2011) Combined effects of parasites and contaminants on animal health: parasites do matter. Trends in Parasitology 27, 123–130.Google Scholar
Marin, M.G., Rigato, S., Ricciardi, R. and Matozzo, V. (2008) Lethal and estrogenic effects of 4-nonylphenol in the cockle Cerastoderma glaucum . Marine Pollution Bulletin 57, 552–558.CrossRefGoogle ScholarPubMed
Matozzo, V., Rova, G., Ricciardi, F. and Marin, M.G. (2008) Immunotoxicity of the xenoestrogen 4-nonylphenol to the cockle Cerastoderma glaucum . Marine Pollution Bulletin 57, 453–459.Google Scholar
Morgan, E., O'Riordan, R.M., Kelly, T.C. and Culloty, S.C. (2012) Influence of disseminated neoplasia, trematode infection and gametogenesis on surfacing and mortality in the cockle Cerastoderma edule . Diseases of Aquatic Organisms 98, 73–84.Google Scholar
Mouritsen, K.N. and Poulin, R. (2002) Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101–S117.Google Scholar
Navarro, E., Iglesias, J.I.P. and Larrañaga, A. (1989) Interannual variation in the reproductive cycle and biochemical composition of the cockle Cerastoderma edule from Mundaca Estuary (Biscay, North Spain). Marine Biology 101, 501–511.Google Scholar
Newell, R.I.E. and Bayne, B.L. (1980) Seasonal changes in the physiology, reproductive condition and carbohydrate content of the cockle Cardium (=Cerastoderma) edule (Bivalvia: Cardiidae). Marine Biology 56, 11–19.Google Scholar
Nice, H.E., Morritt, D., Crane, M. and Thorndyke, M. (2003) Long-term and transgenerational effects of nonylphenol exposure at a key stage in the development of Crassostrea gigas. Possible endocrine disruption? Marine Ecology Progress Series 256, 293–300.Google Scholar
Oehlmann, J., Schulte-Oehlmann, U., Kloas, W., Jagnvtsch, O., Lutz, M., Kusk, K.O., Wollenberger, L., Santos, E.M., Paull, G.C., Van Look, K.J.W. and Tyler, C.R. (2009) A critical analysis of the biological impacts of plasticisers on wildlife. Philosophical Transactions of the Royal Society B – Biological Sciences 364, 2047–2062.CrossRefGoogle ScholarPubMed
Oehlmann, J., Schulte-Oehlmann, U., Tillmann, M. and 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.Google Scholar
Pike, A.W. and Burt, M.D.B. (1981) Paravortex karlingi sp. nov. from Cerastoderma edule L., in Britain. Hydrobiologia 84, 23–30.Google Scholar
Seed, R. and Brown, R.A. (1977) A comparison of the reproductive cycles of Modiolus modiolus (L.), Cerastoderma (=Cardium) edule (L.), and Mytilus edulis L. in Strangford Lough, Northern Ireland. Oecologia 30, 173–188.Google Scholar
Sheir, S.K., Handy, R.D. and Henry, T.B. (2013) Effect of pollution history on immunological responses and organ histology in the marine mussel Mytilus edulis exposed to cadmium. Archives of Environmental Contamination and Toxicology 64, 701–716.Google Scholar
Sokolova, I.M., Sokolov, E.P. and Ponnappa, K.M. (2005) Cadmium exposure affects mitochondrial bioenergetics and gene expression of key mitochondrial proteins in the eastern oyster Crassostrea virginica Gmelin (Bivalvia: Ostreidea). Aquatic Toxicology 73, 242–255.CrossRefGoogle Scholar
Staples, C.A., Dome, P.B., Klecka, G.M., Oblock, S.T. and Harris, L.R. (1998) A review of the environmental fate, effects, and exposures of bisphenol A. Chemosphere 36, 2149–2173.Google Scholar
Timmermans, B.M.H., Hummel, H. and Bogaards, R.H. (1996) The effect of polluted sediment on the gonadal development and embryogenesis of bivalves. Science of the Total Environment 187, 23–236.Google Scholar
Western Channel Observatory (2012) Meteorological station data. Available at http://www.westernchannelobservatory.org.uk/pml_weather_station/index.php (Accessed 10 August 2012).Google Scholar
Zhou, J., Zhu, X. and Zhong-Hua, C. (2009) Endocrine disruptors: an overview and discussion on issues surrounding their impact on marine animals. Journal of Marine Animals and their Ecology 2, 7–17.Google Scholar
Zwarts, L. (1991) Seasonal variation in body weight of the bivalves Macoma balthica, Scrobicularia plana, Mya arenaria and Cerastoderma edule in the Dutch Wadden sea. Netherland Journal of Sea Research 28, 231–245.Google Scholar
Supplementary material: File

Lusher supplementary material

Figure A and Table A

Download Lusher supplementary material(File)
File 5.8 MB