Climate change and pollution speed declines in zebrafish populations

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 11, 2015, Pages E1237-E1246

  Brown, A Ross ^a,b   Owen, Stewart F ^a   Peters, James ^a   Zhang, Yong ^a   Soffker, Marta ^b,c   Paull, Gregory C ^b   Hosken, David J ^b   Abdul Wahab, M ^d   Tyler, Charles R ^b  

^a ASTRAZENECA   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c CENTRE FOR ENVIRONMENT   (United Kingdom)

^d BANGLADESH AGRICULTURAL UNIVERSITY   (Bangladesh)

Author keywords

Additive; Interaction; Population; Stressors; Viability

Indexed keywords

AROMATASE; CLOTRIMAZOLE; WATER;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CLIMATE CHANGE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DEVELOPMENTAL TOXICITY; ENVIRONMENTAL EXPOSURE; ESTROGEN SYNTHESIS; FEMALE; GROWTH RATE; HIGH TEMPERATURE; INBRED STRAIN; MALE; NONHUMAN; OUTBRED STRAIN; POLLUTION; POPULATION GROWTH; POPULATION MODEL; POPULATION RISK; PRIORITY JOURNAL; SEX RATIO; SEXUAL DEVELOPMENT; WATER QUALITY; WATER TEMPERATURE; ZEBRA FISH; ANALYSIS; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; DRUG EFFECTS; GERM CELL; GONAD; GROWTH, DEVELOPMENT AND AGING; INBREEDING; POPULATION DYNAMICS; TEMPERATURE; TIME FACTOR;

DANIO RERIO; VERTEBRATA;

ANIMALS; CLIMATE CHANGE; CLOTRIMAZOLE; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL POLLUTION; FEMALE; GERM CELLS; GONADS; INBREEDING; MALE; MODELS, BIOLOGICAL; POPULATION DYNAMICS; TEMPERATURE; TIME FACTORS; ZEBRAFISH;

EID: 84925321721     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1416269112     Document Type: Article

References (95)

1. United Nations Environment Programme (2012) Biodiversity. Global Environment Outlook Report GEO-5. Available at www.unep.org/geo/geo5.asp. Accessed November 16, 2014.
2. Bates BC, Kundzewicz ZW, Wu S, Palutikof JP (2008) Climate Change and Water. Technical Paper of the Intergovernmental Panel on Climate Change (IPCC Secretariat, Geneva).
3. Vörösmarty CJ, et al. (2010) Global threats to human water security and river biodiversity. Nature 467(7315):555-561.
4. Holmstrup M, et al. (2010) Interactions between effects of environmental chemicals and natural stressors: A review. Sci Total Environ 408(18):3746-3762.
5. Hallare AV, Schirling M, Luckenbach T, Köhler H-R, Triebskorn R (2005) Combined effects of temperature and cadmium on developmental parameters and biomarker responses in zebrafish (Danio rerio) embryos. J Therm Biol 30(1):7-17.
6. Quinn AL (2007) The Impacts of Agricultural Chemicals and Temperature on the Physiological Stress Response in Fish (University of Lethbridge, Leithbridge, AB, Canada).
7. Sih A, Bell AM, Kerby JL (2004) Two stressors are far deadlier than one. Trends Ecol Evol 19(6):274-276.
8. Bancroft BA, Baker NJ, Blaustein AR (2008) A meta-analysis of the effects of ultraviolet B radiation and its synergistic interactions with pH, contaminants, and disease on amphibian survival. Conserv Biol 22(4):987-996.
9. Gibbons JW, et al. (2000) The global decline of reptiles, déjà vu amphibians. Bioscience 50(8):653-666.
10. Willingham EJ (2005) The effects of atrazine and temperature on turtle hatchling size and sex ratios. Front Ecol Environ 3(6):309-313.
11. Moe SJ, et al. (2013) Combined and interactive effects of global climate change and toxicants on populations and communities. Environ Toxicol Chem 32(1):49-61.
12. Gergs A, Zenker A, Grimm V, Preuss TG (2013) Chemical and natural stressors combined: From cryptic effects to population extinction. Sci Rep 3:2036.
13. Lande R, Shannon S (1996) The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50(1):434-437.
14. Reed DH, Lowe EH, Briscoe DA, Frankham R (2003) Fitness and adaptation in a novel environment: Effect of inbreeding, prior environment, and lineage. Evolution 57(8):1822-1828.
15. Kamel SJ, Mrosovsky N (2006) Deforestation: Risk of sex ratio distortion in hawksbill sea turtles. Ecol Appl 16(3):923-931.
16. Hawkes LA, Broderick AC, Godfrey MH, Godley BJ (2007) Investigating the potential impacts of climate change on a marine turtle population. Glob Change Biol 13(5):923-932.
17. Head G, May RM, Pendleton L (1987) Environmental determination of sex in the reptiles. Nature 329(6136):198-199.
18. Pieau C, Dorizzi M, Richard-Mercier N (1999) Temperature-dependent sex determination and gonadal differentiation in reptiles. Cell Mol Life Sci 55(6-7):887-900.
19. Wapstra E, et al. (2009) Climate effects on offspring sex ratio in a viviparous lizard. J Anim Ecol 78(1):84-90.
20. Warner RR (1997) Sperm allocation in coral reef fish, strategies for coping with demands on sperm production. Bioscience 47(9):561-564.
21. Ospina-Alvarez N, Piferrer F (2008) Temperature-dependent sex determination in fish revisited: Prevalence, a single sex ratio response pattern, and possible effects of climate change. PLoS ONE 3(7):e2837.
22. Eggert C (2004) Sex determination: The amphibian models. Reprod Nutr Dev 44(6):539-549.
23. Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21(6):296-302.
24. Rankin DJ, Kokko H (2007) Do males matter? The role of males in population dynamics. Oikos 116(2):335-348.
25. Baroiller JF, D'Cotta H, Saillant E (2009) Environmental effects on fish sex determination and differentiation. Sex Dev 3(2-3):118-135.
26. Delvin RH, Nagahama Y (2002) Sex determination and sex differentiation in fish: An overview of genetic, physiological and environmental influences. Aquaculture 208(3-4):191-364.
27. Kohno S, Guillette LJ (2013) Endocrine disruption and reptiles: Using the unique attributes of temperature-dependent sex determination to assess impacts. Endocrine Disrupters: Hazard Testing and Assessment Methods, ed Matthiessen P (Wiley, Hoboken, NJ), pp 245-271.
28. Orton F, Tyler CR (2014) Do hormone-modulating chemicals impact on reproduction and development of wild amphibians? Biol Rev Camb Philos Soc, 10.1111/brv.12147.
29. Hamlin HJ, Guillette LJ, Jr (2010) Birth defects in wildlife: The role of environmental contaminants as inducers of reproductive and developmental dysfunction. Syst Biol Reprod Med 56(2):113-121.
30. Harris CA, et al. (2011) The consequences of feminization in breeding groups of wild fish. Environ Health Perspect 119(3):306-311.
31. Kidd KA, et al. (2007) Collapse of a fish population after exposure to a synthetic estrogen. Proc Natl Acad Sci USA 104(21):8897-8901.
32. Brook BW, Tonkyn DW, O'Grady JJ, Frankham R (2002) Contribution of inbreeding to extinction risk in threatened species. Conserv Ecol 6(1):16.
33. Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10(11):783-796.
34. Roff DA (2002) Inbreeding depression: Tests of the overdominance and partial dominance hypotheses. Evolution 56(4):768-775.
35. Wright LI, Tregenza T, Hosken DJ (2008) Inbreeding, inbreeding depression and extinction. Conserv Genet 9(4):833-843.
36. Spitsbergen JM, Kent ML (2003) The state of the art of the zebrafish model for toxicology and toxicologic pathology research - Advantages and current limitations. Toxicol Pathol 31(Suppl):62-87.
37. Rubinstein AL (2006) Zebrafish assays for drug toxicity screening. Expert Opin Drug Metab Toxicol 2(2):231-240.
38. Spence R, Gerlach G, Lawrence C, Smith C (2008) The behaviour and ecology of the zebrafish, Danio rerio. Biol Rev Camb Philos Soc 83(1):13-34.
39. Uchida D, Yamashita M, Kitano T, Iguchi T (2004) An aromatase inhibitor or high water temperature induce oocyte apoptosis and depletion of P450 aromatase activity in the gonads of genetic female zebrafish during sex-reversal. Comp Biochem Physiol A Mol Integr Physiol 137(1):11-20.
40. Brown AR, et al. (2011) Are toxicological responses in laboratory (inbred) zebrafish representative of those in outbred (wild) populations? A case study with an endocrine disrupting chemical. Environ Sci Technol 45(9):4166-4172.
41. Guiguen Y, Fostier A, Piferrer F, Chang C-F (2010) Ovarian aromatase and estrogens: A pivotal role for gonadal sex differentiation and sex change in fish. Gen Comp Endocrinol 165(3):352-366.
42. Navarro-Martín L, et al. (2011) DNA methylation of the gonadal aromatase (cyp19a) promoter is involved in temperature-dependent sex ratio shifts in the European sea bass. PLoS Genet 7(12):e1002447.
43. Falconer DS, Mackay TFC (1996) Introduction to Quantitative Genetics (Longman, New York), 4th Ed.
44. Morton NE, Crow JF, Muller HJ (1956) An estimate of the mutational damage in man from data on consanguineous marriages. Proc Natl Acad Sci USA 42(11):855-863.
45. Lawrence C, Ebersole JP, Kesseli RV (2008) Rapid growth and out-crossing promote female development in zebrafish (Danio rerio). Environ Biol Fishes 81(2):239-246.
46. Uusi-Heikkilä S, Wolter C, Meinelt T, Arlinghaus R (2010) Size-dependent reproductive success of wild zebrafish Danio rerio in the laboratory. J Fish Biol 77(3):552-569.
47. Reed DH, O'Grady JJ, Brook BW, Ballou JD, Frankham R (2003) Estimates of minimum viable population sizes for vertebrates and factors influencing those estimates. Biol Conserv 113(1):23-34.
48. Beverton RJH, Holt SJ (1957) On the Dynamics of Exploited Fish Populations, Fishery Investigations Series II (Ministry of Agriculture, Fisheries, and Food, HMSO, London), Vol XIX.
49. Hazlerigg CRE, Tyler CR, Lorenzen K, Wheeler JR, Thorbek P (2014) Population relevance of toxicant mediated changes in sex ratio in fish: An assessment using an individual-based zebrafish (Danio rerio) model. Ecol Modell 280(2014):76-88.
50. Intergovernmental Panel on Climate Change (2013) Summary for policymakers. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, eds Stocker TF, et al. (Cambridge Univ Press, Cambridge, UK).
51. United Nations Environment Programme, World Health Organization (2013) State of the Science of Endocrine Disrupting Chemicals - 2012: An Assessment of the State of the Science of Endocrine Disruptors Prepared by a Group of Experts for the United Nations Environment Programme and World Health Organization, eds Bergman Å, Heindel JJ, Jobling S, Kidd KA, Zoeller RT (UNEP/WHO, Geneva).
52. Jobling S, et al. (2002) Wild intersex roach (Rutilus rutilus) have reduced fertility. Biol Reprod 67(2):515-524.
53. Orlando EF, et al. (2004) Endocrine-disrupting effects of cattle feedlot effluent on an aquatic sentinel species, the fathead minnow. Environ Health Perspect 112(3):353-358.
54. Kortenkamp A (2007) Ten years of mixing cocktails: A review of combination effects of endocrine-disrupting chemicals. Environ Health Perspect 115(1, Suppl 1):98-105.
55. Oslo Paris Commission (2013) OSPAR Background Document on Clotrimazole 2013 update (London).
56. Hinfray N, Porcher J-M, Brion F (2006) Inhibition of rainbow trout (Oncorhynchus mykiss) P450 aromatase activities in brain and ovarian microsomes by various environmental substances. Comp Biochem Physiol C Toxicol Pharmacol 144(3):252-262.
57. Kahle M, Buerge IJ, Hauser A, Müller MD, Poiger T (2008) Azole fungicides: Occurrence and fate in wastewater and surface waters. Environ Sci Technol 42(19):7193-7200.
58. Macikova P, Groh KJ, Ammann AA, Schirmer K, Suter MJ-F (2014) Endocrine disrupting compounds affecting corticosteroid signaling pathways in czech and swiss waters: Potential impact on fish. Environ Sci Technol 48(21):12902-12911.
59. Roberts PH, Thomas KV (2006) The occurrence of selected pharmaceuticals in wastewater effluent and surface waters of the lower Tyne catchment. Sci Total Environ 356(1-3):143-153.
60. Berenzen N, et al. (2005) A comparison of predicted and measured levels of runoff-related pesticide concentrations in small lowland streams on a landscape level. Chemosphere 58(5):683-691.
61. Jacobsen NW, Halling-Sørensen B, Birkved FK (2008) Inhibition of human aromatase complex (CYP19) by antiepileptic drugs. Toxicol In Vitro 22(1):146-153.
62. Hazlerigg CRE (2012) Fish population ecology and ecological risk assessment. PhD thesis (University of Exeter, Exeter, UK). Available at ethos.bl.uk/OrderDetails.do?uin=uk.bl.ethos.555911. Accessed November 16, 2014.
63. Ropelewski CF, Halpert MS (1987) Global and regional scale precipitation patterns associated with the El Niño/Southern Oscillation. Monthly Weather Review 115(8):1606-1626.
64. Erikstad KE, Moum T, Bustnes JO, Reiertsen TK (2011) High levels of organochlorines may affect hatching sex ratio and hatchling body mass in arctic glaucous gulls. Funct Ecol 25(1):289-296.
65. Parker GA (1992) The evolution of sexual size dimorphism in fish. J Fish Biol 41(sB):1-20.
66. von Hofsten J, Olsson P-E (2005) Zebrafish sex determination and differentiation: Involvement of FTZ-F1 genes. Reprod Biol Endocrinol 3:63.
67. Bradley KM, et al. (2011) An SNP-based linkage map for zebrafish reveals sex determination. G3 (Bethesda) 1(1):3-9.
68. Wilson CA, et al. (2014) Wild sex in zebrafish: Loss of the natural sex determinant in domesticated strains. Genetics 198(3):1291-1308.
69. Anderson JL, et al. (2012) Multiple sex-associated regions and a putative sex chromosome in zebrafish revealed by RAD mapping and population genomics. PLoS ONE 7(7):e40701.
70. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308(5730):1912-1915.
71. Foden WB, et al. (2013) Identifying the world's most climate change vulnerable species: A systematic trait-based assessment of all birds, amphibians and corals. PLoS ONE 8(6):e65427.
72. Rice WR, Chippindale AK (2001) Sexual recombination and the power of natural selection. Science 294(5542):555-559.
73. Colegrave N (2002) Sex releases the speed limit on evolution. Nature 420(6916):664-666.
74. Becks L, Agrawal AF (2012) The evolution of sex is favoured during adaptation to new environments. PLoS Biol 10(5):e1001317.
75. Roze D (2012) Disentangling the benefits of sex. PLoS Biol 10(5):e1001321.
76. Tucker JK, Dolan CR, Lamer JT, Dustman EA (2008) Climatic warming, sex ratios and red-eared sliders (Trachemys scripta elegans) in Illinois. Chelonian Conserv Biol 7(1):60-69.
77. Conover DO, Voorhees DAV, Ehtisham A (1992) Sex ratio selection and changes in environmental sex determination in laboratory populations of Menidia menidia. Evolution 46(6):1722-1730.
78. Le Page Y, et al. (2010) Aromatase, brain sexualization and plasticity: The fish paradigm. Eur J Neurosci 32(12):2105-2115.
79. Fenske M, Segner H (2004) Aromatase modulation alters gonadal differentiation in developing zebrafish (Danio rerio). Aquat Toxicol 67(2):105-126.
80. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421(6918):37-42.
81. Rodrigues AD, Gibson GG, Ioannides C, Parke DV (1987) Interactions of imidazole antifungal agents with purified cytochrome P-450 proteins. Biochem Pharmacol 36(24):4277-4281.
82. Rupa Kumar KR, et al. (2006) High-resolution climate change scenarios for India for the 21st century. Curr Sci 90(3):334-345.
83. Bickley LK, et al. (2013) Interactive effects of inbreeding and endocrine disruption on reproduction in a model laboratory fish. Evol Appl 6(2):279-289.
84. Organisation for Economic Cooperation and Development (2011) OECD Guideline for Testing of Chemicals, Guideline 234: Fish, Sexual Development Test (OECD, Paris).
85. Bolger T, Connolly P (1989) The selection of suitable indices for the measurement and analysis of fish condition. J Fish Biol 34(2):171-182.
86. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671-675.
87. Neuheimer AB, Taggart CT (2007) The growing degree day and fish size at age: The overlooked metric. Can J Fish Aquat Sci 64(2):375-385.
88. Maack G, Segner H (2003) Morphological development of the gonads in zebrafish. J Fish Biol 62(4):895-906.
89. Miller PS, Lacy RC (2005) VORTEX: A Stochastic Simulation of the Extinction Process. Version 9.50 User's Manual [Conservation Breeding Specialist Group (SSC/IUCN), Apple Valley, MN].
90. Shaffer ML (1981) Minimum population sizes for species conservation. Bioscience 31(2):131-134.
91. Lacy RC, Borbat M, Pollak JP (2005) VORTEX: A Stochastic Simulation of the Extinction Process. Version 9.50 (Chicago Zoological Society, Brookfield, IL).
92. Hazlerigg CRE, Lorenzen K, Thorbek P, Wheeler JR, Tyler CR (2012) Density dependent processes in the life history of fishes: Evidence from laboratory populations of zebrafish Danio rerio. PLoS ONE 7(5):e37550.
93. Uusi-Heikkilä S, Kuparinen A, Wolter C, Meinelt T, O'Toole AC, Arlinghaus R (2011) Experimental assessment of the probabilistic maturation reaction norm: Condition matters. Proc Royal Soc Lond B Biol Sci 278(1706):709-717.
94. McCune AR, et al. (2002) A low genomic number of recessive lethals in natural populations of bluefin killifish and zebrafish. Science 296(5577):2398-2401.
95. McCune AR, Houle D, McMillan K, Annable R, Kondrashov AS (2004) Two classes of deleterious recessive alleles in a natural population of zebrafish, Danio rerio. Proc Biol Sci 271(1552):2025-2033.