Population relevance of toxicant mediated changes in sex ratio in fish: An assessment using an individual-based zebrafish (Danio rerio) model

Ecological Modelling

Volumn 280, Issue , 2014, Pages 76-88

  Hazlerigg, Charles R E ^a,b,c   Tyler, Charles R ^b   Lorenzen, Kai ^a,c   Wheeler, James R ^d   Thorbek, Pernille ^d  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c UNIVERSITY OF FLORIDA   (United States)

^d JEALOTT S HILL INTERNATIONAL RESEARCH CENTRE   (United Kingdom)

Author keywords

Density dependence; Ecological modelling; Ecological risk assessment; Endocrine disrupting chemicals; Fish ecology; Population regulation

Indexed keywords

ECOLOGY; FISH; RISK ASSESSMENT;

DENSITY DEPENDENCE; ECOLOGICAL MODELLING; ECOLOGICAL RISK ASSESSMENT; ENDOCRINE DISRUPTING CHEMICALS; FISH ECOLOGY; POPULATION REGULATION;

POPULATION STATISTICS;

ABUNDANCE; CONCENTRATION (COMPOSITION); CYPRINID; DENSITY DEPENDENCE; ECOLOGICAL MODELING; ECOTOXICOLOGY; ENDOCRINE DISRUPTOR; GROWTH RATE; INDIVIDUAL-BASED MODEL; MORTALITY; PHENOL; POLLUTION EFFECT; POLLUTION EXPOSURE; POPULATION MODELING; POPULATION REGULATION; REFUGIUM; RISK ASSESSMENT; SEX RATIO; WILD POPULATION;

BANGLADESH;

DANIO RERIO;

EID: 84897913373     PISSN: 03043800     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ecolmodel.2013.12.016     Document Type: Article

References (102)

1. An W., Hu J., 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.
2. Andersen L., Holbech H., Gessbo A., Norrgren L., Petersen G. Effects of exposure to 17 alpha-ethinylestradiol during early development on sexual differentiation and induction of vitellogenin in zebrafish (Danio rerio). Comp. Biochem. Physiol. C 2003, 134:365-374.
3. Balasubramani A., Pandian T.J. Endosulfan suppresses growth and reproduction in zebrafish. Curr. Sci. 2008, 94(7):883-890.
4. Baldwin D.H., Spromberg J.A., Collier T.K., Scholz N.L. A fish of many scales: extrapolating sublethal pesticide exposures to the productivity of wild salmon populations. Ecol. Appl. 2009, 19(8):2004-2015.
5. Science, Law, and Hudson River Power Plants. A Case Study in Environmental Impact Assessment. 1988, American Fisheries Society, Monograph 4. L.W. Barnthouse, R.J. Klauda, D.S. Vaughn, R.L. Kendall (Eds.).
6. Barnthouse L.W., Munns W.R., Sorensen M.T. Population-level Ecological Risk Assessment 2007, CRC Press, Boca Raton.
7. Bars R., Broeckaert F., Fegert I., Gross M., Hallmark N., Kedwards T., et al. Science based guidance for the assessment of endocrine disrupting properties of chemicals. Regul. Toxicol. Pharm. 2011, 59:37-46.
8. Bars R., Fegert I., Gross M., Lewis D., Weltje L., Weyer A., et al. Risk assessment of endocrine disrupting chemicals. Regul. Toxicol. Pharm. 2012, 64:143-154.
9. Beverton R.J.H., Holt S.J. On the Dynamics of Exploited Fish Populations 1957, Her Majesty's Stationery Office, London.
10. Brian J.V., Augley J.J., Brathwaite V.A. Endocrine disrupting effects on the nesting behaviour of male three-spined stickleback Gasterosteus aculeatus L. J. Fish Biol. 2006, 68(6):1883-1890.
11. Brion F., Tyler C.R., Palazzi X., Laillet B., Porcher J.M., Garric J., et al. Impacts of 17β-estradiol, including environmentally relevant concentrations, on reproduction after exposure during embryo-larval-, juvenile- and adult-life stages in zebrafish (Danio rerio). Aquat. Toxicol. 2004, 68:193-217.
12. Brown A.R., Hosken D.J., Balloux F., Bickley L.K., LePage G., Owen S.F., et al. Genetic variation, inbreeding and chemical exposure-combined effects in wildlife and critical considerations for ecotoxicology. Philos. Trans. R. Soc. B 2009, 364:3377-3390.
13. Caswell H. Matrix Population Models, Construction, Analysis and Interpretation 2001, Sinauer, Sunderland.
14. Christianson-Heiska I., Wahteristo P., Kastilan E.L., Bergelin E., Bylund G., Isomaa B. Effects of the wood extractive betulinol and 17β-oestradiol on reproduction in zebrafish, Danio rerio (Hamilton)-complications due to a bacterial infection. J. Fish Dis. 2004, 27:267-276.
15. Coe T.S., Hamilton P.B., Hodgson D., Paull G.C., Stevens J.R., Sumner K., et al. An environmental estrogen alters reproductive hierarchies, disrupting sexual selection in group-spawning fish. Environ. Sci. Technol. 2008, 42:5020-5025.
16. Cotton S., Wedekind C. Population consequences of environmental sex reversal. Conserv. Biol. 2008, 23(1):196-206.
17. Dyson E.A., Hurst G.D.D. Persistence of an extreme sex-ratio bias in a natural population. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:6520-6523.
18. Eaton R.C., Farley R.D. Spawning cycle and egg production of zebrafish, Brachydanio rerio, in the laboratory. Copeia 1974, 1:195-204.
19. European Food Safety Authority (EFSA) Scientific opinion on the development of specific protection goal options for environmental risk assessment of pesticides, in particular in relation to the revision of the Guidance Documents on Aquatic and Terrestrial Ecotoxicology (SANCO/3268/2001 and SANCO/10329/2002). EFSA J. 2010, 8(10):1821.
20. Einum S., Nislow K.H. Local-scale density-dependent survival of mobile organisms in continuous habitats: an experimental test using Atlantic salmon. Oecologia 2005, 143:203-210.
21. Elliott J.M. Quantitative Ecology and the Brown Trout 1994, Oxford University Press, Oxford.
22. Engeszer R., Patterson L., Rao A., Parichy D. Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 2007, 4(1):21-40.
23. Ensenbach U., Nagel R. Toxicity of binary chemical mixtures: effects on reproduction of zebrafish (Brachydanio rerio). Arch. Environ. Contam. Toxicol. 1997, 32:204-210.
24. EC European Commission Regulation No 1107/2009 of the European Parliament and of the council concerning the placing of plant protection products on the market. Off. J. Eur. Commun. L 2009, 309:1-50.
25. EC European Commission Regulation No 528/2012. Biocidal products. Off. J. Eur. Commun. L 2012, 167:1-123.
26. Fahraeus-Van Ree G.E., Payne J.F. Effect of toxaphene on reproduction of fish. Chemosphere 1997, 34(4):855-867.
27. Fenske M., Maack G., Schäfers C., Segner H. An environmentally relevant concentration of estrogen induces arrest of male gonad development in zebrafish, Danio rerio. Environ. Toxicol. Chem. 2005, 24(5):1088-1098.
28. Ferson S., Ginzburg L.R., Goldstein R.A. Inferring ecological risk from toxicity bioassays. Water Air Soil Pollut. 1996, 90:71-82.
29. Fleming I.A., Gross M.R. Breeding competition in a pacific salmon (Coho: Oncorhynchus kisutch): measures of natural and sexual selection. Evolution 1994, 48(3):637-657.
30. Forbes V.E., Calow P. Population growth rate as a basis for ecological risk assessment of toxic chemicals. Philos. Trans. R. Soc. Lond. B 2002, 357:1299-1306.
31. Forbes V.E., Calow P., Sibly R.M. The extrapolation problem and how population modelling can help. Environ. Toxicol. Chem. 2008, 27(10):1987-1994.
32. Forbes V.E., Calow P., Grimm V., Hayashi T., Jager T., Palmqvist A., et al. Integrating population modelling into ecological risk assessment. Integr. Environ. Assess. Manage. 2010, 6:191-193.
33. Galic N., Hommen U., Baveco J.M., van den Brink P.J. Potential application of population models in the European risk assessment of chemicals 2: review of models and their potential to address environmental protection aims. Integr. Environ. Assess. Manage. 2010, 6(3):338-360.
34. Gerlach G. Pheromonal regulation of reproductive success in female zebrafish: female suppression and male enhancement. Anim. Behav. 2006, 72:1119-1124.
35. Goodhead R.M., Tyler C.R. Endocrine-disrupting chemicals and their environmental impacts. Organic Pollutants 2009, CRC Press, Boca Raton. C.H. Walker (Ed.).
36. Grant A. Population consequences of chronic toxicity: incorporating density dependence into the analysis of life table response experiments. Ecol. Model. 1998, 105:325-335.
37. Gray M.A., Teather K.L., Metcalfe C.D. Reproductive success and behaviour of Japanese medaka (Oryzias latipes) exposed to 4-tert-octylphenol. Environ. Toxicol. Chem. 1999, 18(11):2587-2594.
38. Grimm V., Railsback F. Individual-Based Modelling and Ecology 2005, Princeton University Press, Princeton.
39. Grimm V., Berger U., Bastiansen F., Eliassen S., Ginot V., Giske J., et al. A standard protocol for describing individual-based and agent-based models. Ecol. Model. 2006, 198:115-126.
40. Grimm V., Berger U., DeAngelis D.L., Polhill J.G., Giske J., Railsback S.F. The ODD protocol: a review and first update. Ecol. Model. 2010, 221:2760-2768.
41. Gross T.S., Arnold B.S., Sepulveda M.S., McDonald K. Endocrine disrupting chemicals and endocrine active agents. Handbook of Ecotoxicology 2003, CRC Press, Boca Raton. D.J. Hoffman, B.A. Rattner, G.A. Burton, J. Cairns (Eds.).
42. Hazlerigg C.R.E. Fish Population Ecology and Ecological Risk Assessment 2012, (Ph.D. Thesis), (EThOS uk.bl.ethos.555911).
43. Hazlerigg C.R.E., Tyler C.R., Thorbek P., Wheeler J., Lorenzen K. Density-dependent processes in the life history of fishes: evidence from laboratory populations of zebrafish Danio rerio. PLoS ONE 2012, 7(5):e37550. 10.1371/journal.pone.0037550.
44. Hill R.L., Janz D.M. Developmental estrogenic exposure in zebrafish (Danio rerio): effects on sex ratio and breeding success. Aquat. Toxicol. 2003, 63:417-429.
45. Hill A.J., Teraoka H., Heideman W., Peterson R.E. Zebrafish as a model vertebrate for investigating chemical toxicity. Toxicol. Sci. 2005, 86(1):6-19.
46. Hommen U., Baveco J.M., Galic N., van den Brink P.J. Potential application of ecological models in the European Environmental Risk Assessment of chemicals 1: review of protection goals in EU directives and regulations. Integr. Environ. Assess. Manage. 2010, 6(3):325-337.
47. Hunka A.D., Meli M., Thit A., Palmqvist A., Thorbek P., Forbes V. Stakeholders' perspective on ecological modelling in environmental risk assessment of pesticides: challenges and opportunities. Risk Anal. 2012, 10.1111/j.1539-6924.2012.01835.x.
48. Hurley M.A., Matthiessen P., Pickering A.D. A model for environmental sex reversal in fish. J. Theor. Biol. 2004, 227(2):159-165.
49. Hutchinson T.H., Brown R., Brugger K.E., Campbell P.M., Holt M., Lange R., et al. Ecological risk assessment of endocrine disruptors. Environ. Health Perspect. 2000, 108(11):1007-1014.
50. Liew W.C., Bartfai R., Lim Z., Sreenivasan R., Siegfried K.R., Orban L. Polygenic sex determination system in zebrafish. PLoS ONE 2012, 7(4):e34397. 10.1371/journal.pone.0034397.
51. Lin L.L., Janz D.M. Effects of binary mixtures of xenoestrogens on gonadal development and reproduction in zebrafish. Aquat. Toxicol. 2006, 80:382-395.
52. Lin B.-L., Meng Y. Extrapolation of available acute and chronic toxicity test data to population-level effects for ecological risk management of chemicals. Environ. Toxicol. Chem. 2009, 28(7):1557-1566.
53. Lorenzen K. The relationship between body weight and natural mortality in juvenile and adult fish: a comparison of ecosystems and aquaculture. J. Fish Biol. 1996, 49:627-647.
54. Lorenzen K., Enberg K. Density-dependent growth as a key mechanism in the regulation of fish populations: evidence from among-population comparisons. Proc. R. Soc. Lond. B 2002, 269:49-54.
55. Luck G.W., Daily G.C., Ehrlich P.R. Population diversity and ecosystem services. Trends Ecol. Evol. 2003, 18(7):331-336.
56. Maack G., Segner H. Life-stage-dependent sensitivity of zebrafish (Danio rerio) to estrogen exposure. Comp. Biochem. Physiol. C 2004, 139:47-55.
57. Madenjian C.P., Carpenter S.R., Eck G.W., Miller M.A. Accumulation of PCBs by lake trout (Salvelinus namaycush): an individual-based model approach. Can. J. Fish. Aquat. Sci. 2011, 50(1):97-109.
58. McClure M.M., McIntyre P.B., McCune A.R. Notes on the natural diet and habitat of eight danionin fishes, including the zebrafish Danio rerio. J. Fish Biol. 2006, 69:553-570.
59. Meng Y.B., Lin B.-L., Tominaga M., Nakanishi J. Simulation of the population-level effects of 4-nonylphenol on the wild Japanese medaka (Oryzias latipes). Ecol. Model. 2006, 197:350-360.
60. Miller D.H., Ankley G.T. Modelling impacts on populations: fathead minnow (Pimephales promelas) exposure to the endocrine disruptor 17β-trenbolone as a case study. Ecotoxicol. Environ. Saf. 2004, 59:1-9.
61. Milner-Gulland E.J., Lhagvasuren B. Population dynamics of the Mongolian gazelle Procapra gutturosa: an historical analysis. J. Appl. Ecol. 1998, 35:240-251.
62. Myers R.A., Cadigan N.G. Density-dependent juvenile mortality in marine demersal fish. Can. J. Fish. Aquat. Sci. 1993, 50:1576-1590.
63. Nash J., Kime D., Van der Ven L., Wester P., Brion F., Maack G., et al. Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol cause reproductive failure in fish. Environ. Health Perspect. 2004, 112(17):1725-1733.
64. Nicholson A.J. The balance of animal populations. J. Anim. Ecol. 1933, 2:132-178.
65. Organisation for Economic Cooperation and Development (OECD), 2011a. http://www.oecd.org/env/chemicalsafetyandbiosafety/testingofchemicals/48478975.pdf.
66. Organisation for Economic Cooperation and Development (OECD), 2011b. http://www.oecd.org/env/chemicalsafetyandbiosafety/testingofchemicals/48479160.pdf.
67. Organisation for Economic Cooperation and Development (OECD), 2011c. http://www.oecd.org/env/chemicalsafetyandbiosafety/testingofchemicals/48479011.pdf.
68. OECD (Organisation for Economic Cooperation and Development) OECD 234. Fish Sexual Development Test 2011, 1-44. Organisation for Economic Co-operation and Development, Paris.
69. Olsen E.M., Helno M., Lilly G.R., Morgan M.J., Brattey J., Ernande B., et al. Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 2004, 428:932-935.
70. Ovidiu Vlad M. The optimal sex ratio for age-structured populations. Math. Biosci. 1989, 93:181-190.
71. Pastorok R.A., Bartell S.M., Ferson S., Ginzburg L.R. Ecological Modelling in Risk Assessment 2002, CRC Press, Boca Raton.
72. Paull G.C., Van Look K.J.W., Santos E.M., Filby A.L., Gray D.M., Nash J.P., et al. Variability in measures of reproductive success in laboratory-kept colonies of zebrafish and implications for studies addressing population-level effects of environmental chemicals. Aquat. Toxicol. 2008, 87:115-126.
73. Peterson I., Wroblewski J.S. Mortality rate of fish in the pelagic ecosystem. Can. J. Fish. Aquat. Sci. 1984, 41:1117-1120.
74. Preuss T.G., Hammers-Writz M., Hommen U., Rubach M.N., Ratte H.T. Development and validation of an individual based Daphnia magna population model: the influence of crowding on population dynamics. Ecol. Model. 2009, 220(3):310-329.
75. Purdom C.E., Hardiman P.A., Bye V.V.J., Eno N.C., Tyler C.R., Sumpter J.P. Estrogenic effects of effluents from sewage treatment works. Chem. Ecol. 1994, 8:275-285.
76. Pyron M. Female preferences and male-male interactions in zebrafish (Danio rerio). Can. J. Zool. 2003, 81:122-125.
77. Railsback S.F., Harvey B.C. Importance of fish behaviour in modelling conservation problems: food limitation as an example. J. Fish Biol. 2011, 79(6):1648-1662.
78. Ricker W.E. Computation and interpretations of biological statistics of fish populations. Bull. Fish. Res. Board. Can. 1975, 191:1-382.
79. Robinson C.D., Brown E., Craft J.A., Davies I.M., Moffat C.F. Effects of prolonged exposure to 4-tert-octylphenol on toxicity and indices of oestrogenic exposure in the sand goby (Pomatoschistus minutus, Pallas). Mar. Environ. Res. 2004, 58(1):19-38.
80. Rose K.A., Cowan J.H., Winemiller K.O., Myers R.A., Hilborn R. Compensatory density dependence in fish populations: importance, controversy, understanding and prognosis. Fish Fish. 2001, 2:293-327.
81. Schäfers C., Nagel R. Consequences of 3,4-dichloroaniline to guppy populations (Poecilia reticulata): computer simulation and experimental validation. Sci. Tot. Environ. 1993, (Suppl.):1471-1478.
82. Schäfers C., Teigeler M., Wenzel A., Maack G., Fenske M., Segner H. Concentration and time dependent effects of the synthetic estrogen, 17-ethinylestradiol, on reproductive capabilities of the zebrafish, Danio rerio. J. Toxicol. Environ. Health A 2007, 70:768-779.
83. Schiegg K., Walters J.R., Priddy J.A. Testing a spatially explicit, individual-based model of red-cockaded woodpecker population dynamics. Ecol. Appl. 2005, 15(5):1495-1503.
84. Schindler D.W. Replication versus realism: the need for ecosystem-scale experiments. Ecosystems 1998, 1:323-334.
85. Segner H. Zebrafish (Danio rerio) as a model organism for investigating endocrine disruption. Comp. Biochem. Physiol. 2008, 10.1016/j.cbpc.2008.10.099.
86. Segner H., Navas J.M., Schäfers C., Wenzel A. Potencies of estrogenic compounds in in vitro screening assays and in life cycle tests with zebrafish in vivo. Ecotoxicol. Environ. Saf. 2003, 54:315-322.
87. Senior A.M., Lim J.N., Nakagawa S. The fitness consequences of environmental sex reversal in fish: a quantitative review. Biol. Rev. 2012, 87(4):900-911.
88. Skinner A.M.J., Watt P.J. Strategic egg allocation in the zebrafish, Danio rerio. Behav. Ecol. 2007, 10.1093/beheco/arm059.
89. Spence R., Smith C. Male territoriality mediates density and sex ratio effects on oviposition in the zebrafish, Danio rerio. Anim. Behav. 2005, 69:1317-1323.
90. Spence R., Smith C. Mating preference of female zebrafish, Danio rerio, in relation to male dominance. Behav. Ecol. 2006, 10.1093/beheco/arl016.
91. Spence R., Fatema M.K., Ellis S., Ahmed Z.F., Smith C. Diet, growth and recruitment of wild zebrafish in Bangladesh. J. Fish Biol. 2007, 71:304-309.
92. Spence R., Gerlach G., Lawrence C., Smith C. The behaviour and ecology of the zebrafish, Danio rerio. Biol. Rev. 2007, 83:1-22.
93. Stelkens R.B., Wedekind C. Environmental sex reversal, Trojan sex genes and sex ratio adjustment: conditions and population consequences. Mol. Ecol. 2010, 19:627-646.
94. Thorbek P., Forbes V., Heimbach F., Hommen U., Thulke H.H., van den Brink P.J., et al. Ecological Models for Regulatory Risk Assessments of Pesticides: Developing a Strategy for the Future 2010, Society of Environmental Toxicology and Chemistry (SETAC)/CRC Press, Pensacola/Boca Raton, FL.
95. Turchin P. Quantitative Analysis of Movement: Measuring and Modelling Population Redistribution in Animals and Plants 1998, Sinauer Associates, Sunderland.
96. Uusi-Heikkila S., Wolter C., Meinelt T., Arlinghaus R. Size-dependent reproductive success of wild zebrafish Danio rerio in the laboratory. J. Fish Biol. 2010, 77:552-569.
97. Wenzel A., Schäfers C., Vollmer G., Michna H., Diel P. Research efforts towards the development and validation of a test method for the identification of endocrine disrupting chemicals. Fraunhofer 2001, B6-7920/98/000015.
98. Wheeler J., Green R., Weltje L. Developments on the regulation of endocrine disrupting substances in Europe-hazard, risk and the need for a scientific approach. Outlook Pest Manage. 2012, 23:85-91.
99. Whoriskey F.G., FitzGerald G.J. Ecology of the threespine stickleback on the breeding grounds. The Evolutionary Biology of the Threespine Stickleback 1994, 189-206. Oxford University Press, Oxford. M.A. Bell, S.A. Foster (Eds.).
100. Wilensky U. Netlogo 1999, Centre for Connected Learning and Computer-Based Modelling. Northwestern University, Evanston, IL. http://www.ccl.northwestern.edu/netlogo.
101. Wootton R.J. Ecology of Teleost Fishes 2002, Chapman and Hall, London. 3rd ed.
102. Zala S.M., Penn D.J. Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges. Anim. Behav. 2004, 68:649-664.