Edited by Nancy Knowlton, Smithsonian Institution, Washington, DC, and approved January 26, 2015 (received for review August 26, 2014)
Climate change impacts on wildlife populations are likely to be accentuated by pollution. Small (inbred) populations may be more vulnerable to these effects, but empirical data supporting these hypotheses are lacking. We present the first substantial empirical evidence, to our knowledge, for interactive effects on population viability of elevated temperature (climate); an endocrine disrupting chemical, clotrimazole (pollution); and inbreeding. Using the zebrafish (Danio rerio) as a model, we show these three factors interact to skew population sex ratios toward males and that this interaction can lead to increased risk of extinction. Our results suggest that climate change and pollution impacts are likely to pose significant extinction risks for small, endangered populations exhibiting environmental sex determination and/or differentiation.
Endocrine disrupting chemicals (EDCs) are potent environmental contaminants, and their effects on wildlife populations could be exacerbated by climate change, especially in species with environmental sex determination. Endangered species may be particularly at risk because inbreeding depression and stochastic fluctuations in male and female numbers are often observed in the small populations that typify these taxa. Here, we assessed the interactive effects of water temperature and EDC exposure on sexual development and population viability of inbred and outbred zebrafish (Danio rerio). Water temperatures adopted were 28 °C (current ambient mean spawning temperature) and 33 °C (projected for the year 2100). The EDC selected was clotrimazole (at 2 μg/L and 10 μg/L), a widely used antifungal chemical that inhibits a key steroidogenic enzyme [cytochrome P450(CYP19) aromatase] required for estrogen synthesis in vertebrates. Elevated water temperature and clotrimazole exposure independently induced male-skewed sex ratios, and the effects of clotrimazole were greater at the higher temperature. Male sex ratio skews also occurred for the lower clotrimazole exposure concentration at the higher water temperature in inbred fish but not in outbred fish. Population viability analysis showed that population growth rates declined sharply in response to male skews and declines for inbred populations occurred at lower male skews than for outbred populations. These results indicate that elevated temperature associated with climate change can amplify the effects of EDCs and these effects are likely to be most acute in small, inbred populations exhibiting environmental sex determination and/or differentiation.
Author contributions: A.R.B., D.J.H., and C.R.T. designed research; A.R.B., S.F.O., J.P., Y.Z., and G.C.P. performed research; G.C.P. and M.A.W. contributed new reagents/analytic tools; A.R.B., M.S., and D.J.H. analyzed data; and A.R.B., S.F.O., M.S., D.J.H., and C.R.T. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1416269112/-/DCSupplemental.
Freely available online through the PNAS open access option.
Edited by Nancy Knowlton, Smithsonian Institution, Washington, DC, and approved January 26, 2015 (received for review August 26, 2014)
Climate change impacts on wildlife populations are likely to be accentuated by pollution. Small (inbred) populations may be more vulnerable to these effects, but empirical data supporting these hypotheses are lacking. We present the first substantial empirical evidence, to our knowledge, for interactive effects on population viability of elevated temperature (climate); an endocrine disrupting chemical, clotrimazole (pollution); and inbreeding. Using the zebrafish (Danio rerio) as a model, we show these three factors interact to skew population sex ratios toward males and that this interaction can lead to increased risk of extinction. Our results suggest that climate change and pollution impacts are likely to pose significant extinction risks for small, endangered populations exhibiting environmental sex determination and/or differentiation.
Endocrine disrupting chemicals (EDCs) are potent environmental contaminants, and their effects on wildlife populations could be exacerbated by climate change, especially in species with environmental sex determination. Endangered species may be particularly at risk because inbreeding depression and stochastic fluctuations in male and female numbers are often observed in the small populations that typify these taxa. Here, we assessed the interactive effects of water temperature and EDC exposure on sexual development and population viability of inbred and outbred zebrafish (Danio rerio). Water temperatures adopted were 28 °C (current ambient mean spawning temperature) and 33 °C (projected for the year 2100). The EDC selected was clotrimazole (at 2 μg/L and 10 μg/L), a widely used antifungal chemical that inhibits a key steroidogenic enzyme [cytochrome P450(CYP19) aromatase] required for estrogen synthesis in vertebrates. Elevated water temperature and clotrimazole exposure independently induced male-skewed sex ratios, and the effects of clotrimazole were greater at the higher temperature. Male sex ratio skews also occurred for the lower clotrimazole exposure concentration at the higher water temperature in inbred fish but not in outbred fish. Population viability analysis showed that population growth rates declined sharply in response to male skews and declines for inbred populations occurred at lower male skews than for outbred populations. These results indicate that elevated temperature associated with climate change can amplify the effects of EDCs and these effects are likely to be most acute in small, inbred populations exhibiting environmental sex determination and/or differentiation.
Author contributions: A.R.B., D.J.H., and C.R.T. designed research; A.R.B., S.F.O., J.P., Y.Z., and G.C.P. performed research; G.C.P. and M.A.W. contributed new reagents/analytic tools; A.R.B., M.S., and D.J.H. analyzed data; and A.R.B., S.F.O., M.S., D.J.H., and C.R.T. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1416269112/-/DCSupplemental.
Freely available online through the PNAS open access option.
