Implications of persistent exposure to treated wastewater effluent for breeding in wild roach (Rutilus rutilus) populations

Environmental Science and Technology

Volumn 45, Issue 4, 2011, Pages 1673-1679

  Lange, Anke ^a   Paull, Gregory C ^a   Hamilton, Patrick B ^a   Iguchi, Taisen ^b,c   Tyler, Charles R ^a  

^a UNIVERSITY OF EXETER   (United Kingdom)

^b NATIONAL INSTITUTE FOR BASIC BIOLOGY   (Japan)

^c GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BREEDING POPULATIONS; CHRONIC EXPOSURE; EFFLUENT DISCHARGE; ENDOCRINE DISRUPTING CHEMICALS; FISH POPULATIONS; IMPACT ASSESSMENTS; LONG TERM EXPOSURE; MICROSATELLITES; NEW DIMENSIONS; POPULATION-LEVEL EFFECTS; RUTILUS RUTILUS; SEXUAL MATURITY; TREATED WASTEWATER; WASTEWATER EFFLUENTS; WASTEWATER TREATMENT WORKS;

ECOLOGY; EFFLUENT TREATMENT; FISH; FISHERIES; WASTEWATER; WASTEWATER TREATMENT;

EFFLUENTS;

ESTRONE; MICROSATELLITE DNA; ENDOCRINE DISRUPTOR; WASTE WATER; WATER POLLUTANT;

BREEDING POPULATION; CHEMICAL POLLUTANT; CYPRINID; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; GENETIC MARKER; POLLUTION EXPOSURE; SEX REVERSAL; SEXUAL MATURITY; WASTE TREATMENT; WASTEWATER;

ARTICLE; BREEDING; CONTROLLED STUDY; DILUTION; EFFLUENT; EXPOSURE; FEMALE; FISH; MALE; NONHUMAN; OVARY; PARENTHOOD; PHENOTYPE; POPULATION; PROGENY; REPRODUCTION; RUTILUS RUTILUS; SEX TRANSFORMATION; SEXUAL MATURITY; TESTIS; WASTE WATER MANAGEMENT; ANIMAL; CYPRINIFORMES; DRUG EFFECTS; PHYSIOLOGY; RIVER; SEXUAL MATURATION; TOXICITY; WASTE WATER; WATER POLLUTANT;

UNITED KINGDOM;

RUTILUS RUTILUS;

ANIMALS; BREEDING; CYPRINIDAE; ENDOCRINE DISRUPTORS; ESTRONE; FEMALE; MALE; OVARY; RIVERS; SEXUAL MATURATION; WASTE WATER; WATER POLLUTANTS, CHEMICAL;

EID: 79951603215     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es103232q     Document Type: Article

References (37)

1. Hotchkiss, A. K.; Rider, C. V.; Blystone, C. R.; Wilson, V. S.; Hartig, P. C.; Ankley, G. T.; Foster, P. M.; Gray, C. L.; Gray, L. E. Fifteen years after "Wingspread"-Environmental endocrine disrupters and human and wildlife health: Where we are today and where we need to go Toxicol. Sci. 2008, 105, 235-259
2. Jobling, S.; Nolan, M.; Tyler, C. R.; Brighty, G.; Sumpter, J. P. Widespread sexual disruption in wild fish Environ. Sci. Technol. 1998, 32, 2498-2506 (Pubitemid 28420276)
3. Scholz, S.; Kluver, N. Effects of endocrine disrupters on sexual, gonadal development in fish Sex. Dev. 2009, 3, 136-151
4. Jobling, S.; Coey, S.; Whitmore, J. G.; Kime, D. E.; Van Look, K. J. W.; McAllister, B. G.; Beresford, N.; Henshaw, A. C.; Brighty, G.; Tyler, C. R.; Sumpter, J. P. Wild intersex roach (Rutilus rutilus) have reduced fertility Biol. Reprod. 2002, 67, 515-524 (Pubitemid 34803938)
5. Diniz, M. S.; Peres, I.; Magalhaes-Antoine, I.; Falla, J.; Pihan, J. C. Estrogenic effects in crucian carp (Carassius carassius) exposed to treated sewage effluent Ecotox. Environ. Safe 2005, 62, 427-435 (Pubitemid 41427147)
6. Diniz, M. S.; Peres, I.; Pihan, J. C. Comparative study of the estrogenic responses of mirror carp (Cyprinus carpio) exposed to treated municipal sewage effluent (Lisbon) during two periods in different seasons Sci. Total Environ. 2005, 349, 129-139 (Pubitemid 41421070)
7. Rodgers-Gray, T. P.; Jobling, S.; Kelly, C.; Morris, S.; Brighty, G.; Waldock, M. J.; Sumpter, J. P.; Tyler, C. R. Exposure of juvenile roach (Rutilus rutilus) to treated sewage effluent induces dose-dependent and persistent disruption in gonadal duct development Environ. Sci. Technol. 2001, 35, 462-470 (Pubitemid 32125951)
8. Lange, A.; Paull, G. C.; Coe, T. S.; Katsu, Y.; Urushitani, H.; Iguchi, T.; Tyler, C. R. Sexual reprogramming and estrogenic sensitization in wild fish exposed to ethinylestradiol Environ. Sci. Technol. 2009, 43, 1219-1225
9. Wedekind, C. Lek-like spawning behaviour and different female mate preferences in roach (Rutilus rutilus) Behaviour 1996, 133, 681-695
10. Jacob, A.; Evanno, G.; Renai, E.; Sermier, R.; Wedekind, C. Male body size and breeding tubercles are both linked to intrasexual dominance and reproductive success in the minnow Anim. Behav. 2009, 77, 823-829
11. Kortet, R.; Vainikka, A.; Rantala, M. J.; Jokinen, I.; Taskinen, J. Sexual ornamentation, androgens and papillomatosis in male roach (Rutilus rutilus) Evol. Ecol. Res. 2003, 5, 411-419 (Pubitemid 38681692)
12. Larsen, M. G.; Hansen, K. B.; Henriksen, P. G.; Baatrup, E. Male zebrafish (Danio rerio) courtship behaviour resists the feminising effects of 17α-ethinyloestradiol-morphological sexual characteristics do not Aquat. Toxicol. 2008, 87, 234-244
13. Martinovic, D.; Hogarth, W. T.; Jones, R. E.; Sorensen, P. W. Environmental estrogens suppress hormones, behavior, and reproductive fitness in male fathead minnows Environ. Toxicol. Chem. 2007, 26, 271-278 (Pubitemid 46191368)
14. Coe, T. S.; Hamilton, P. B.; Hodgson, D.; Paull, G. C.; Tyler, C. R. Parentage outcomes in response to estrogen exposure are modified by social grouping in zebrafish Environ. Sci. Technol. 2009, 43, 8400-8405
15. Grist, E. P. M.; Wells, N. C.; Whitehouse, P.; Brighty, G.; Crane, M. Estimating the effects of 17α-ethinylestradiol on populations of the fathead minnow Pimephales promelas: Are conventional toxicological endpoints adequate? Environ. Sci. Technol. 2003, 37, 1609-1616 (Pubitemid 36438162)
16. Meng, Y. B.; Lin, B. L.; Tominaga, M.; Nakanishi, J. Simulation of the population-level effects of 4-nonylphenol on wild Japanese medaka (Oryzias latipes) Ecol. Modell. 2006, 197, 350-360 (Pubitemid 44108398)
17. Miller, D. H.; Ankley, G. T. Modeling impacts on populations: fathead minnow (Pimephales promelas) exposure to the endocrine disruptor 17β-trenbolone as a case study Ecotox. Environ. Safe 2004, 59, 1-9 (Pubitemid 39295221)
18. Raimondo, S.; Hemmer, B. L.; Goodman, L. R.; Cripe, G. M. Multigenerational exposure of the estuarine sheepshead minnow (Cyprinodon variegatus) to 17β-estradiol. II. Population-level effects through two life cycles Environ. Toxicol. Chem. 2009, 28, 2409-2415
19. An, W.; Hu, J. Y.; Giesy, J. P.; Yang, M. Extinction risk of exploited wild roach (Rutilus rutilus) populations due to chemical feminization Environ. Sci. Technol. 2009, 43, 7895-7901
20. Cotton, S.; Wedekind, C. Population consequences of environmental sex reversal Conserv. Biol. 2009, 23, 196-206
21. Paull, G. C.; Lange, A.; Henshaw, A. C.; Tyler, C. R. Ontogeny of sexual development in the roach (Rutilus rutilus) and its interrelationships with growth and age J. Morphol. 2008, 269, 884-895
22. Liney, K. E.; Jobling, S.; Shears, J. A.; Simpson, P.; Tyler, C. R. Assessing the sensitivity of different life stages for sexual disruption in roach (Rutilus rutilus) exposed to effluents from wastewater treatment works Environ. Health Perspect. 2005, 113, 1299-1307 (Pubitemid 41511983)
23. Rodgers-Gray, T. P.; Jobling, S.; Morris, S.; Kelly, C.; Kirby, S.; Janbakhsh, A.; Harries, J. E.; Waldock, M. J.; Sumpter, J. P.; Tyler, C. R. Long-term temporal changes in the estrogenic composition of treated sewage effluent and its biological effects on fish Environ. Sci. Technol. 2000, 34, 1521-1528 (Pubitemid 30217479)
24. Routledge, E. J.; Sumpter, J. P. Estrogenic activity of surfactants and some of their degradation products assessed using a recombinant yeast screen Environ. Toxicol. Chem. 1996, 15, 241-248 (Pubitemid 26069072)
25. Environment Agency. Biological effect measures in fish-application to treated sewage effluent; Bristol, UK, 2007; p 36.
26. Thorpe, K. L.; Maack, G.; Benstead, R.; Tyler, C. R. Estrogenic wastewater treatment works effluents reduce egg production in fish Environ. Sci. Technol. 2009, 43, 2976-2982
27. Jobling, S.; Williams, R.; Johnson, A.; Taylor, A.; Gross-Sorokin, M.; Nolan, M.; Tyler, C. R.; van Aerle, R.; Santos, E.; Brighty, G. Predicted exposures to steroid estrogens in U.K. rivers correlate with widespread sexual disruption in wild fish populations Environ. Health Perspect. 2006, 114, 32-39
28. Tyler, C. R.; Jobling, S. Roach, sex, and gender-bending chemicals: The feminization of wild fish in English rivers Bioscience 2008, 58, 1051-1059
29. Jobling, S.; Beresford, N.; Nolan, M.; Rodgers-Gray, T.; Brighty, G. C.; Sumpter, J. P.; Tyler, C. R. Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents Biol. Reprod. 2002, 66, 272-281 (Pubitemid 34101823)
30. Vøllestad, L. A.; L'Abée-Lund, J. H. Reproductive biology of stream-spawning roach, Rutilus rutilus Environ. Biol. Fishes 1987, 18, 219-227
31. Environment Agency. The identification of oestrogenic effects in wild fish-Phase II. R&D Technical Report W2-014/TR; Bristol, UK, 2002; p 102.
32. Miranda, A. C. L.; Bazzoli, N.; Rizzo, E.; Sato, Y. Ovarian follicular atresia in two teleost species: a histological and ultrastructural study Tissue Cell 1999, 31, 480-488 (Pubitemid 29531290)
33. Jacob, A.; Nussle, S.; Britschgi, A.; Evanno, G.; Muller, R.; Wedekind, C. Male dominance linked to size and age, but not to 'good genes' in brown trout (Salmo trutta) BMC Evol. Biol. 2007, 7
34. Kidd, K. A.; Blanchfield, P. J.; Mills, K. H.; Palace, V. P.; Evans, R. E.; Lazorchak, J. M.; Flick, R. W. Collapse of a fish population after exposure to a synthetic estrogen Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 8897-8901 (Pubitemid 47175408)
35. Vos, J. G.; Dybing, E.; Greim, H. A.; Ladefoged, O.; Lambre, C.; Tarazona, J. V.; Brandt, I.; Vethaak, A. D. Health effects of endocrine-disrupting chemicals on wildlife, with special reference to the European situation Crit. Rev. Toxicol. 2000, 30, 71-133 (Pubitemid 30090598)
36. Bickham, J. W.; Sandhu, S.; Hebert, P. D. N.; Chikhi, L.; Athwal, R. Effects of chemical contaminants an genetic diversity in natural populations: implications for biomonitoring and ecotoxicology Mutat. Res.-Rev. Mutat. Res. 2000, 463, 33-51 (Pubitemid 30326799)
37. Vaha, J. P.; Erkinaro, J.; Niemela, E. Primmer, C.R. Life-history and habitat features influence the within-river genetic structure of Atlantic salmon Mol. Ecol. 2007, 16, 2638-2654 (Pubitemid 47012148)