Effects of sewage effluent remediation on body size, somatic RNA: DNA ratio, and markers of chemical exposure in three-spined sticklebacks

Environment International

Volumn 37, Issue 1, 2011, Pages 158-169

  Pottinger, Tom G ^a   Cook, Alastair ^b   Jürgens, Monika D ^a   Rhodes, Glenn ^a   Katsiadaki, Ioanna ^b   Balaam, Jan L ^b   Smith, Andrew J ^b   Matthiessen, Peter ^a,c  

^a CENTRE FOR ECOLOGY AND HYDROLOGY   (United Kingdom)

^b CENTRE FOR ENVIRONMENT   (United Kingdom)

^c Old School House   (United Kingdom)

Author keywords

CYP1A; EROD; Pollution; Remediation; RNA:DNA ratio; Sewage; Stickleback; Waste water treatment

Indexed keywords

ACTIVATED CARBON; ACTIVATED CARBON TREATMENT; CARBON; DNA; EFFLUENT TREATMENT; EFFLUENTS; FISHERIES; IMPURITIES; NUCLEIC ACIDS; POLLUTION; REMEDIATION; RIVER POLLUTION; RIVERS; RNA; SEWAGE; URBAN GROWTH; WASTE TREATMENT; WASTEWATER; WASTEWATER TREATMENT; WATER POLLUTION; WATER RESOURCES; WATER TREATMENT;

CYP1A; EROD; GRANULAR ACTIVATED CARBONS; RNA:DNA RATIOS; SECONDARY-TREATED SEWAGE; SPECIFIC GROWTH RATE; STICKLEBACK; THREE-SPINED STICKLEBACKS;

FISH;

ACTIVATED CARBON; CYTOCHROME P450 1A; DNA; ETHOXYRESORUFIN DEETHYLASE; RIVER WATER; RNA;

BODY SIZE; DNA; EFFLUENT; FINFISH; GROWTH RATE; NUTRIENT UPTAKE; POLLUTION EXPOSURE; POPULATION SIZE; REMEDIATION; RNA; SPAWNING POPULATION; WASTE TREATMENT; WASTEWATER;

ARTICLE; BODY MASS; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; FISH; GROWTH RATE; NONHUMAN; NUTRIENT CONTENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEWAGE EFFLUENT; STICKLEBACKS; WASTE WATER MANAGEMENT; WATER QUALITY; WATER TEMPERATURE; WINTER;

ENGLAND; RAY RIVER; UNITED KINGDOM;

GASTEROSTEUS ACULEATUS;

EID: 78349307875     PISSN: 01604120     EISSN: 18736750     Source Type: Journal    
DOI: 10.1016/j.envint.2010.08.012     Document Type: Article

References (59)

1. Ali M., Wootton R.J. Do random fluctuations in the intervals between feeding affect growth rate in juvenile three-spined sticklebacks?. J Fish Biol 1998, 53:1006-1014.
2. Ali M., Wootton R.J. Correlates of growth in juvenile three-spined sticklebacks: potential predictors of growth rates in natural populations. Ecol Freshw Fish 2003, 12:87-92.
3. Allen J.R.M., Wootton R.J. Age, growth and rate of food consumption in an upland population of the three-spined stickleback, Gasterosteus aculeatus L. J Fish Biol 1982, 21:95-105.
4. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
5. Alvarez M.D., Fuiman L.A. Environmental levels of atrazine and its degradation products impair survival skills and growth of red drum larvae. Aquat Toxicol 2005, 74:229-241.
6. Amara R., Selleslagh J., Billon G., Minier C. Growth and condition of 0-group European flounder, Platichthys flesus as indicator of estuarine habitat quality. Hydrobiologia 2009, 627:87-98.
7. Arnold K.E., Adam A., Orr K.J., Griffiths R., Barber I. Sex-specific survival and parasitism in three-spined sticklebacks: seasonal patterns revealed by molecular analysis. J Fish Biol 2003, 63:1046-1050.
8. Balaam J.L., Grover D., Johnson A.C., Jürgens M., Readman J., Smith A.J., White S., Williams R., Zhou J.L. The use of modelling to predict levels of estrogens in a river catchment: How does modelled data compare with chemical analysis and in vitro yeast assay results?. Sci Tot Environ 2010, 408:4826-4832.
9. Boxall A.B.A., Maltby L. The effects of motorway runoff on freshwater ecosystems: 3. Toxicant confirmation. Arch Environ Contam Toxicol 1997, 33:9-16.
10. Buckley L., Caldarone E., Ong T.-L. RNA-DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes. Hydrobiologia 1999, 401:265-277.
11. Chellappa S., Huntingford F.A., Strang R.H.C., Thomson R.Y. Annual variation in energy reserves in male three-spined stickleback, Gasterosteus aculeatus L. (Pisces, Gasterosteidae). J Fish Biol 1989, 35:275-286.
12. Chícharo M.A., Chícharo L. RNA:DNA ratio and other nucleic acid derived indices in marine ecology. Int J Mol Sci 2008, 9:1453-1471.
13. Clavero M., Pou-Rovira Q., Zamora L. Biology and habitat use of three-spined stickleback (Gasterosteus aculeatus) in intermittent Mediterranean streams. Ecol Freshw Fish 2009, 18:550-559.
14. Clemmesen C. The effect of food availability, age or size on the RNA/DNA ratio of individually measured herring larvae: laboratory calibration. Mar Biol 1994, 118:377-382.
15. Devlin R.H., Nagahama Y. Sex determination and sex differentiation in fish: an overview of genetic, physiological, and environmental influences. Aquaculture 2002, 208:191-364.
16. Filby A.L., Tyler C.R. Appropriate 'housekeeping' genes for use in expression profiling the effects of environmental estrogens in fish. BMC Mol Biol 2007, 8. article number 10.
17. Friberg N., Dybkjær J.B., Olafsson J.S., Gislason G.M., Larsen S.E., Lauridsen T.L. Relationships between structure and function in streams contrasting in temperature. Freshw Biol 2009, 54:2051-2068.
18. Geoghegan F., Katsiadaki I., Williams T.D., Chipman J.K. A cDNA microarray for the three-spined stickleback, Gasterosteus aculeatus L., and analysis of the interactive effects of oestradiol and dibenzanthracene exposures. J Fish Biol 2008, 72:2133-2153.
19. Gewurtz S.B., Lazar R., Haffner G.D. Comparison of polycyclic aromatic hydrocarbon and polychlorinated biphenyl dynamics in benthic invertebrates of Lake Erie, USA. Environ Toxicol Chem 2000, 19:2943-2950.
20. Gorokhova E., Kyle M. Analysis of nucleic acids in Daphnia: development of methods and ontogenetic variations in RNA-DNA content. J Plankton Res 2002, 24:511-522.
21. Graham C.T., Harrod C. Implications of climate change for the fishes of the British Isles. J Fish Biol 2009, 74:1143-1205.
22. Gücker B., Brauns M., Pusch M.T. Effects of wastewater treatment plant discharge on ecosystem structure and function of lowland streams. J. N. Am. Benthol. Soc. 2006, 25:313-329.
23. Hahlbeck E., Griffiths R., Bengtsson B.-E. The juvenile three-spined stickleback (Gasterosteus aculeatus L.) as a model organism for endocrine disruption I. Sexual differentiation. Aquat Toxicol 2004, 70:287-310.
24. Hodson P.V., Efler S., Wilson J.Y., El-Shaarawi A., Maj M., Williams T.G. Measuring the potency of pulp mill effluents for induction of hepatic mixed-function oxygenase activity in fish. J Toxicol Environ Health 1996, 49:83-110.
25. Huntingford F.A., Ruiz-Gomez M.L. Three-spined sticklebacks Gasterosteus aculeatus as a model for exploring behavioural biology. J Fish Biol 2009, 75:1943-1976.
26. Huo C.X., Hickey P. EDC demonstration programme in the UK-Anglian Water's approach. Environ Technol 2007, 28:731-741.
27. Katsiadaki I., Scott A.P., Mayer I. The potential of the three-spined stickleback (Gasterosteus aculeatus L.) as a combined biomarker for oestrogens and androgens in European waters. Mar Environ Res 2002, 54:725-728.
28. Kim S.D., Cho J., Kim I.S., Vanderford B.J., Snyder S.A. Occurrence and removal of pharmaceuticals and endocrine disruptors in South Korean surface, drinking, and waste waters. Water Res 2007, 41:1013-1021.
29. Kynard B.E. Breeding behaviour of a lacustrine population of threespine sticklebacks (Gasterosteus aculeatus L.). Behaviour 1978, 67:178-207.
30. Logan D.T. Perspective on ecotoxicology of PAHs to fish. Hum Ecol Risk Assess 2007, 13:302-316.
31. Lorenzen A., Kennedy S.W. A fluorescence-based protein assay for use with a microplate reader. Anal Biochem 1993, 214:346-348.
32. Ma T., Wan X., Huang Q., Wang Z., Liu J. Biomarker responses and reproductive toxicity of the effluent from a Chinese large sewage treatment plant in Japanese medaka (Oryzias latipes). Chemosphere 2005, 59:281-288.
33. Mann R.H.K. The populations, growth and production of fish in four small streams in southern England. J Anim Ecol 1971, 40:155-190.
34. UK Hydrometric Register, Hydrological Data Series 2008, Centre for Ecology and Hydrology, 210 pp. T.J. Marsh, J. Hannaford (Eds.).
35. McArdle M., Elskus A., McElroy A., Larsen B., Benson W., Schlenk D. Estrogenic and CYP1A response of mummichogs and sunshine bass to sewage effluent. Mar Environ Res 2000, 50:175-179.
36. Meriläinen P., Oikari A. Uptake of organic xenobiotics by benthic invertebrates from sediment contaminated by the pulp and paper industry. Water Res 2008, 42:1715-1725.
37. Mori S. The breeding system of the three-spined stickleback, Gasterosteus aculeatus (Forma leiura) with reference to spatial and temporal patterns of nesting activity. Behaviour 1993, 126:97-124.
38. O'Hara K., Penczak T. Production of the three-spined stickleback, Gasterosteus aculeatus L., in the River Weaver, England. Freshw Biol 1987, 18:353-360.
39. Poizat G., Rosecchi E., Crivelli A.J. Life-history variation within a three-spined stickleback population in the Camargue. J Fish Biol 2002, 60:1296-1307.
40. Pottinger T.G., Carrick T.R., Yeomans W.E. The three-spined stickleback as an environmental sentinel: effects of stressors on whole-body physiological indices. J Fish Biol 2002, 61:207-229.
41. Poulin R., FitzGerald G.J. Early life histories of three sympatric sticklebacks in a salt-marsh. J Fish Biol 1989, 34:207-221.
42. Rice C.A., Myers M.S., Willis M.L., French B.L., Casillas E. From sediment bioassay to fish biomarker-connecting the dots using simple trophic relationships. Mar Environ Res 2000, 50:527-533.
43. Richard P., Bergeron J.-P., Boulhic M., Galois R., Person-Le Ruyet J. Effect of starvation on RNA, DNA and protein content of laboratory-reared larvae and juveniles of Solea solea. Mar Ecol Prog Ser 1991, 72:69-77.
44. Sanchez W., Aït-Aïssa S., Palluel O., Ditche J.-M., Porcher J.-M. Preliminary investigation of multi-biomarker responses in three-spined stickleback (Gasterosteus aculeatus L.) sampled in contaminated streams. Ecotoxicology 2007, 16:279-287.
45. Sanchez W., Katsiadaki I., Piccini B., Ditche J.-M., Porcher J.-M. Biomarker responses in wild three-spined stickleback (Gasterosteus aculeatus L.) as a useful tool for freshwater biomonitoring: a multiparametric approach. Environ Int 2008, 34:490-498.
46. Sanchez W., Piccini B., Ditche J.-M., Porcher J.-M. Assessment of seasonal variability of biomarkers in three-spined stickleback (Gasterosteus aculeatus L.) from a low contaminated stream: implication for environmental biomonitoring. Environ Int 2008, 34:791-798.
47. Snyder S.A., Adham S., Redding A.M., Cannon F.S., DeCarolis J., Oppenheimer J., et al. Role of membranes and activated carbon in the removal of endocrine disruptors and pharmaceuticals. Desalination 2007, 212:156-181.
48. Ternes T.A., Meisenheimer M., Mcdowell D., Brauch H.J., Brigitte H.G., Preuss G., et al. Removal of pharmaceuticals during drinking water treatment. Environ Sci Technol 2002, 36:3855-3863.
49. UKWIR. Endocrine Disrupting Chemicals National Demonstration Programme: Assessment of the Performance of WwTW in Removing Oestrogenic Substances (09/TX/04/16). London, UK; UKWIR; 2009 [ISBN 1 84057 525 5].
50. Wartman C.A., Hogan N.S., Hewitt L.M., McMaster M.E., Landman M.J., Taylor S., et al. Androgenic effects of a Canadian bleached kraft pulp and paper effluent as assessed using threespine stickleback (Gasterosteus aculeatus). Aquat Toxicol 2009, 92:131-139.
51. Whyte J.J., Jung R.E., Schmitt C.J., Tillitt D.E. Ethoxyresorufin-O-deethylase (EROD) activity in fish as a biomarker of chemical exposure. Crit Rev Toxicol 2000, 30:347-570.
52. Williams T.D., Wu H., Santos E.M., Ball J., Katsiadaki I., Brown M.M., et al. Hepatic transcriptomic and metabolomic responses in the stickleback (Gasterosteus aculeatus) exposed to environmentally relevant concentrations of dibenzanthracene. Environ Sci Technol 2009, 43:6341-6348.
53. Wootton R.J. A functional biology of sticklebacks 1984, Croom Helm, London.
54. Wootton R.J. Over-wintering growth and losses in a small population of the threespine stickleback, Gasterosteus aculeatus (L.), in mid-Wales. Ecol Freshw Fish 2007, 16:476-481.
55. Wootton R.J., Smith C. A long-term study of a short-lived fish: the demography of Gasterosteus aculeatus. Behaviour 2000, 137:981-997.
56. Wright H.A., Wootton R.J., Barber I. Interpopulation variation in early growth of threespine sticklebacks (Gasterosteus aculeatus) under laboratory conditions. Can J Fish Aquat Sci 2004, 61:1832-1838.
57. Wu R.S.S., Zhou B.S., Randall D.J., Woo N.Y.S., Lam P.K.S. Aquatic hypoxia is an endocrine disruptor and impairs fish reproduction. Environ Sci Technol 2003, 37:1137-1141.
58. Young W.F., Whitehouse P., Johnson I., Sorokin N. Proposed predicted-no-effect-concentrations (PNECs) for natural and synthetic steroid oestrogens in surface waters. Environment Agency R&D Technical Report P2-T04/1 2004, 172.
59. Zhou B.S., Wu R.S.S., Randall D.J., Lam P.K.S. Bioenergetics and RNA/DNA ratios in the common carp (Cyprinus carpio) under hypoxia. J Comp Physiol B 2001, 171:49-57.