Maternal transfer of contaminants and reduced reproductive success of southern toads (Bufo [Anaxyrus] terrestris) exposed to coal combustion waste

Environmental Science and Technology

Volumn 47, Issue 6, 2013, Pages 2846-2853

  Metts, Brian S ^a   Buhlmann, Kurt A ^a   Tuberville, Tracey D ^a   Scott, David E ^a   Hopkins, William A ^b  

^a UNIVERSITY OF GEORGIA   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COAL COMBUSTION WASTES; CONCENTRATION-DEPENDENT; CONTAMINATED SITES; CU CONCENTRATIONS; ELEVATED CONCENTRATIONS; MATERNAL TRANSFER; REFERENCE SITES; REPRODUCTIVE SUCCESS;

BIOCHEMISTRY; LEAD; NICKEL; TISSUE;

CONTAMINATION;

ARSENIC; CADMIUM; COAL; COPPER; LEAD; MERCURY; NICKEL; SELENIUM; STRONTIUM; VANADIUM; ZINC;

BIOACCUMULATION; CLUTCH SIZE; COAL; FLOODPLAIN; POLLUTION EFFECT; POLLUTION EXPOSURE; REPRODUCTIVE SUCCESS; TOAD; TRACE ELEMENT; WASTE DISPOSAL;

ARTICLE; BUFO; BUFO TERRESTRIS; CLUTCH SIZE; COAL COMBUSTION WASTE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EGG; ENVIRONMENTAL EXPOSURE; FEMALE; HATCHLING; INDUSTRIAL WASTE; MOTHER; NONHUMAN; POLLUTANT; PROGENY; REPRODUCTIVE SUCCESS; REPRODUCTIVE TOXICITY; TISSUE LEVEL;

ANIMALS; ANURA; COAL; FEMALE; MATERNAL EXPOSURE; OVUM; REPRODUCTION; SOLID WASTE; TRACE ELEMENTS;

EID: 84875303426     PISSN: 0013936X     EISSN: 15205851     Source Type: Journal    
DOI: 10.1021/es303989u     Document Type: Article

References (72)

1. Linder, G.; Grillitsch, B. Ecotoxicology of metals. In Ecotoxicology of Amphibians and Reptiles; Sparling, D. W., Linder, G., Bishop, C. A., Eds.; SETAC Press: Pensacola, FL, 2000; pp 325-459.
2. Birge, W. J.; Westerman, A. G.; Spomberg, J. A. Comparative toxicology and risk assessment of amphibians. In Ecotoxicology of Amphibians and Reptiles; Sparling, D. W., Linder, G., Bishop, C. A., Eds.; SETAC Press: Pensacola, FL, 2000; pp 727-792.
3. Bernardo, J. Maternal effects in animal ecology Am. Zool. 1996, 36, 83-105
4. Hopkins, W. A.; DuRant, S. E.; Staub, B. P.; Rowe, C. L.; Jackson, B. P. Reproduction, embryonic development, and maternal transfer of contaminants in the amphibian Gastrophryne carolinensis Environ. Health Perspect. 2006, 114, 661-666
5. Kadokami, K.; Takeishi, M.; Kuramoto, M.; Ono, Y. Maternal transfer of organochlorine pesticides, polychlorinated dibenzo- p -dioxins, dibenzofurans, and coplanar polychlorinated biphenyls in frogs to their eggs Chemosphere 2004, 57, 383-389
6. Wu, J.-P.; Luo, X.-J.; Zhang, Y.; Chen, S.-J.; Mai, B.-X.; Guan, Y.-T.; Yang., Z.-Y. Residues of polybrominated diphenyl ethers in frogs (Rana limnocharis) from a contaminated site, South China: Tissue distribution, biomagnification, and maternal transfer Environ. Sci. Technol. 2009, 43, 5212-7
7. Bergeron, C. M.; Bodinof, C. M.; Unrine, J. M.; Hopkins, W. A. Bioaccumulation and maternal transfer of mercury and selenium in amphibians Environ. Toxicol. Chem. 2010, 29, 989-997
8. Kotyzova, D.; Sundeman, F. W. Maternal exposure to Cd (II) causes malformations of Xenopus laevis embryos Ann. Clin. Lab. Sci. 1998, 28, 224-235
9. Bergeron, C. M.; Hopkins, W. A.; Bodinof, C. M.; Budischak, S. A.; Wada, H.; Unrine, J. M. Counterbalancing effects of maternal mercury exposure during different stages of early ontogeny Sci. Total Environ. 2011, 409, 4746-4752
10. Bergeron, C. M.; Hopkins, W. A.; Todd, B. D.; Hepner, M. J.; Unrine, J. M. Interactive effects of maternal and dietary mercury exposure have latent and lethal consequences for amphibian larvae Environ. Sci. Technol. 2011, 43, 3781-3787
11. Collins, J. P.; Storfer, A. Global amphibian declines: Sorting the hypotheses Diversity Distributions 2003, 9, 89-98
12. Hoffmann, M.; Hilton-Taylor, C.; Angulo, A.; Böhm, M.; Brooks, T. M.; Butchart, S. H. M.; Carpenter, K. E. The impact of conservation on the status of the world's vertebrates Science 2010, 330, 1503-1509
13. Stuart, S. N.; Chanson, J. S.; Cox, N. A.; Young, B. E.; Rodriguez, A. S. L.; Fischman, D. L.; Waller, R. W. Status and trends of amphibian declines and extinctions worldwide Science 2004, 306, 1783-1786
14. Hof, C.; Araujo, M. B.; Jetz, W.; Rahbek, C. Additive threats from pathogens, climate and land-use change for global amphibian diversity Nature 2011, 480, 516-519
15. Voyles, J.; Young, S.; Berger, L.; Campbell, C.; Voyles, W. F.; Dinudom, A.; Cook, D.; Webb, R.; Alford, R. A.; Skerratt, L. F.; Speare, R. Pathogenesis of chytridiomycosis, a cause of catastrophic amphibian declines Science 2009, 326, 582-585
16. Energy Information Administration. EIA-767 Data Files: Annual Steam-Electric Plant Operation and Design Report; U.S. Department of Energy: Washington, DC, 2005.
17. Rowe, C. L.; Hopkins, W. A.; Congdon, J. D. Ecotoxicological implications of aquatic disposal of coal combustion residues in the United States: A review Environ. Monit. Assess. 2002, 80, 207-276
18. Hopkins, W. A.; Congdon, J. D.; Ray, J. K. Incidence and impact of axial malformations in larval bullfrogs (Rana catesbeiana) developing in sites polluted by a coal-burning power plant Environ. Toxicol. Chem. 2000, 19, 862-868
19. Raimondo, S. M.; Rowe, C. L. Exposure to coal ash impacts swimming performance and predator avoidance in larval bullfrogs (Rana catesbeiana) J. Herpetol. 1998, 32, 289-292
20. Rowe, C. L.; Kinney, O. M.; Fiori, A.; Congdon, J. D. Oral deformities in tadpoles (Rana catesbeiana) associated with coal ash deposition: Effects on grazing ability and growth Freshwater Biol. 1996, 36, 723-730
21. Rowe, C. L.; Hopkins, W. A.; Coffman, V. R. Failed recruitment of southern toads (Bufo terrestris) in a trace element-contaminated breeding habitat: direct and indirect effects that may lead to a local population sink Arch. Environ. Contam. Toxicol. 2001, 40, 399-405
22. Roe, J. H.; Hopkins, W. A.; DuRant, S. E.; Unrine, J. M. Effects of competition and coal-combustion wastes on recruitment and life history characteristics of salamanders in temporary wetlands Aquat. Toxicol. 2006, 79, 176-184
23. Snodgrass, J. W.; Hopkins, W. A.; Roe, J. H. Relationships among developmental stage, metamorphic timing, and concentrations of elements in bullfrogs (Rana catesbeiana) Environ. Toxicol. Chem. 2003, 22, 1597-1604
24. Snodgrass, J. W.; Hopkins, W. A.; Broughton, J.; Gwinn, D.; Baionno, J. A.; Burger, J. Species-specific responses of developing anurans to coal combustion wastes Aquat. Toxicol. 2004, 66, 171-182
25. Snodgrass, J. W.; Hopkins, W. A. Influence of larval period on responses of overwintering green frog (Rana clamitans) larvae exposed to contaminated sediments Environ. Toxicol. Chem. 2005, 24, 1508-1514
26. Metts, B. S.; Buhlmann, K. B.; Scott, D. E.; Tuberville, T. D.; Hopkins, W. A. Interactive effects of maternal and environmental exposure to coal combustion wastes decrease survival of larval southern toads (Bufo terrestris) Environ. Pollut. 2012, 164, 211-218
27. Rowe, C. L.; Hopkins, W. A. Anthropogenic activities producing sink habitats for amphibians in the local landscape: A case study of lethal and sublethal effects of coal combustion residues in the aquatic environment. In Amphibian Decline: An Integrated Analysis of Multiple Stressor Effects; Linder, G.; Krest, S. K.; Sparling, D. W., Eds.; SETAC Press: Pensacola, FL, 2003; pp 271-281.
28. Roe, J. H.; Hopkins, W. A.; Jackson, B. P. Species- and stage-specific differences in trace element tissue concentrations in amphibians: implications for the disposal of coal-combustion wastes Environ. Pollut. 2005, 136, 353-363
29. Bogert, C. M. A field study of homing in the Carolina toad Am. Mus. Novit. 1947, 1355, 24
30. Jensen, J. B. Southern toad Bufo (Anaxyrus) terrestris. In Amphibians and Reptiles of Georgia; Jensen, J. B.; Camp, C. D.; Gibbons, J. W.; Elliott, M. J., Eds.; University of Georgia Press: Athens, GA, 2008; pp 44-46.
31. U.S. EPA. Wastes from the Combustion of Fossil Fuels, EPA 530-R-99-010; U.S. Environmental Protection Agency: Washington, DC, 1999.
32. Sandhu, S. S.; Mills, G. L. Chapter 17. Mechanisms of mobilization and attenuation of inorganic contaminants in coal ash basins. In Emerging Technologies in Hazardous Waste Management; Tedder, D. W.; Pohland, F. G., Eds.; American Chemical Society: Washington, DC, 1991; pp 342-364.
33. Norton, D. M.; Mills, G. L. Polycyclic aromatic hydrocarbons in SRP aquatic systems derived from coal pile runoff. 193rd National Meeting; American Chemical Society: Washington, DC, 1987; pp 120-122.
34. Shorten, C. V.; Elzerman, A. W.; Mills, G. L. Methods for the determination of PAH desorption-kinetics in coal fines and coal contaminated sediments Chemosphere 1990, 20, 137-159
35. Sharitz, R. R. Carolina bay wetlands: Unique habitats of the Southeastern United States Wetlands 2003, 23, 550-562
36. Sharitz, R. R.; Gibbons, J. W. The Ecology of Southeastern Shrub Bogs (Pocosins) and Carolina Bays: A Community Profile. U.S. Fish and Wildlife Service, Division of Biological Services: Washington, DC, 1982.
37. Semlitsch, R. D.; McMillan, M. A. Breeding migrations, population size structure, and reproduction of the dwarf salamander, Eurycea quadridigitata, in South Carolina Brimleyana 1980, 3, 97-105
38. Pechmann, J. H. K.; Scott, D. E.; Semlitsch, R. D.; Caldwell, J. P.; Vitt, L. J.; Gibbons, J. W. Declining amphibian populations: The problem of separating human impacts from natural fluctuations Science 1991, 253, 892-895
39. Bantle, J. A.; Dumont, J.; Finch, R.; Linder, G. Atlas of Abnormalities: A Guide for the Performance of FETAX; Oklahoma State Publications: Stillwater, OK, 1991.
40. ASTM. Standard Guide for Conducting the Frog Embryo Teratogenesis Assay-Xenopus (FETAX). American Society for Testing and Materials: Philadelphia, PA, 1998.
41. Newman, M. C. Chapter 2: The measurement process. In Quantitative Ecotoxicology, 2 nd ed.; CRC Press: Boca Raton, FL, 2012; pp 27-76.
42. Kroll, K. J.; Doroshov, S. I. Vitellogenin: Potential vehicle for selenium in oocytes of the white sturgeon (Acipenser transmontanus). In Acipenser; Williot, P, Ed.; Cemagref Publishers: Montpellier, France, 1991; pp 99-106.
43. Ghosh, P.; Thomas, P. Binding of metals to red drum vitellogenin and incorporation into oocytes Mar. Environ. Res. 1995, 39, 165-168
44. Unrine, J. M.; Jackson, B. P.; Hopkins, W. A.; Romanek, C. Isolation and partial characterization of proteins involved in maternal transfer of selenium in the western fence lizard (Sceloporus occidentalis) Environ. Toxicol. Chem. 2006, 25, 1864-1867
45. Unrine, J. M.; Jackson, B. P.; Hopkins, W. A. Selenomethionine biotransformation and incorporation into proteins along a simulated terrestrial food chain Environ. Sci. Technol. 2007, 41, 3601-3606
46. Franson, J. C.; Pain, D. J. Lead in birds. In Environmental Contaminants in Biota: Interpreting Tissue Concentrations, 2 nd ed.; Beyer, W. N.; Meador, J. P., Eds.; CRC Press: Boca Raton, FL, 2011; pp 563-593.
47. ATSDR. Toxicological Profile for Lead (Update); U.S. Department of Health and Human Services: Atlanta, GA, 2007.
48. Goldstein, G. H. Evidence that lead acts as a calcium substitute in second messenger metabolism Neurotoxicology 1993, 14, 97-101
49. Fluck, R. A.; Miller, A. L.; Jaffe, L. F. Slow calcium waves accompany cytokinesis in medaka fish eggs J. Cell Biol. 1991, 115, 1259-1265
50. Rowe, C. L.; Kinney, O. M.; Congdon, J. D. Oral deformities in tadpoles of the bullfrog (Rana categsbeiana) caused by conditions in a polluted habitat Copeia 1998, 244-246
51. Rowe, C. L.; Kinney, O. M.; Nagle, R. D.; Congdon, J. D. Elevated maintenance costs in an anuran (Rana catesbeiana) exposed to a mixture of trace elements during the embryonic and early larval periods Physiol. Zool. 1998, 71, 27-35
52. Roe, J. H.; Hopkins, W. A.; Baionno, J. A.; Staub, B. P.; Rowe, C. L.; Jackson, B. P. Maternal transfer of selenium in Alligator mississippiensis nesting downstream from a coal-burning power plant Environ. Toxicol. Chem. 2004, 23, 1969-1972
53. Staub, B. P.; Hopkins, W. A.; Novak, J.; Congdon, J. D. Respiratory and reproductive characteristics of eastern mosquitofish (Gambusia holbrooki) inhabiting a coal ash settling basin Arch. Environ. Contam. Toxicol. 2004, 46, 96-101
54. Hopkins, W. A.; Mendonca, M. T.; Congdon, J. D. Increased circulating levels of testosterone and corticosterone in southern toads, Bufo terrestris, exposed to coal combustion waste Gen. Comp. Endrocrinol. 1997, 108, 237-246
55. Ward, C. K.; Appel, A. G.; Mendonca, M. T. Metabolic measures of male southern toads (Bufo terrestris) exposed to coal combustion waste Comparative Biochem. Physiol., Part A 2006, 143, 353-360
56. Chapman, P. Ecotoxicology of Selenium in the Aquatic Environment. SETAC Press: Pensacola, FL, 2010.
57. Gillespie, R. B.; Baumann, P. C. Effects of high tissue concentrations of selenium on reproduction in bluegills Trans. Am. Fish. Soc. 1986, 115, 208-213
58. Janz, D. M.; Brooks, M. L.; Chapman, P. M.; DeForest, D. K.; Gilron, G.; Hoff, D.; Hopkins, W. A.; McIntyre, D. O.; Mebane, C. A.; Palace, V. P.; Skorupa, J. P.; Wayland, M. Selenium toxicity to aquatic organisms. In Ecotoxicology of Selenium in the Aquatic Environment; Chapman, P., Ed.; SETAC Press: Pensacola, FL, 2010; pp 141-231.
59. Lemly, A. D. Selenium in aquatic organisms. In Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations; Beyer, W. N.; Heinz, G. H.; Redmon-Norwood, A. W., Eds.; Lewis Publishers: Boca Raton, FL, 1996; pp 427-445.
60. Ohlendorf, H. M. Ecotoxicology of selenium. In Handbook of Ecotoxicology; Hoffman, D. J.; Rattner, B. A.; Burton, G. A.; Cairns, J., Eds.; Lewis Publishers: Boca Raton, FL, 2003; 465-500.
61. Skorupa, J. P. Selenium poinsoning of fish and wildlife in nature: Lessons from twelve real-world examples. In Environmental Chemistry and Selenium; Frankenberger, W. T., Jr.; Engberg, R. A., Eds.; Marcel Dekker: New York, 1998; pp 315-354.
62. Young, T. F.; Finley, K.; Adams, W. F.; Besser, J.; Hopkins, W. A.; Jolley, D.; McNaughton, E.; Presser, T. S.; Shaw, D. P.; Unrine, J. M. Chapter 3. What you need to know about selenium. In Ecological Assessment of Selenium in the Aquatic Environment; Chapman, P. M.; Adams, W. J.; Brooks, M.; Delos, C. G.; Luoma, S. N.; Maher, W. A.; Ohlendorf, H. M.; Presser, T. S.; Shaw, P., Eds.; SETAC Press: Pensacola, FL, 2010; pp 7-45.
63. Heinz, G. H. Selenium in birds. In Environmental Contaminants in Wildlife: Interpreting Tissue Concentrations; Beyer, W. N.; Heinz, G. H.; Redmon-Norwood, A. W., Eds.; Lewis Press: Boca Raton, FL, 1996; pp 447-458.
64. Skorupa, J. P.; Ohlendorf, H. M. Contaminants in drainage water and avian risk thresholds. In The Economics and Management of Water and Drainage in Agriculture; Dinar, A.; Zilberman, D., Eds.; Kluwer Academic: Dordrecht, Netherlands, 1991; pp 345-368.
65. Fairbrother, A.; Brix, K. V.; Toll, J. E.; McKay, S.; Adams, W. J. Egg selenium concentrations as predictors of avian toxicity Hum. Ecol. Risk Assess. 1999, 5, 1229-1253
66. Bryan, A. L., Jr.; Hopkins, W. A.; Baionno, J. A.; Jackson, B. P. Maternal transfer of contaminants to eggs in common grackles (Quiscalus quiscala) nesting on coal fly ash basins Arch. Environ. Contam. Toxicol. 2003, 45, 273-277
67. Saino, N.; Romano, M.; Ferrari, R. P.; Martinelli, R.; Moller, A. P. Stressed mothers lay eggs with high corticosterone levels which produce low-quality offspring J. Exp. Zool. 2005, 303A, 998-1006
68. Willson, J. D.; Hopkins, W. A. Evaluating the effects of anthropogenic stressors on source-sink dynamics in pond-breeding amphibians. Conserv. Biol., 2013, in press.
69. Willson, J. D.; Hopkins, W. A.; Bergeron, C. M.; Todd, B. D. Making leaps in amphibian ecotoxicology: Translating individual-level effects of environmental contaminants to population viability Ecol. Appl. 2012, 22, 1791-1802
70. Vonesh, J. R.; De la Cruz, O. Complex life cycles and density-dependence: Population-level consequences of early mortality in amphibians Oecologia 2002, 133, 325-333
71. Taylor, B. E.; Scott, D. E.; Gibbons, J. W. Catastrophic reproductive failure, terrestrial survival, and persistence of the marbled salamander Conserv. Biol. 2006, 20, 792-801
72. Salice, C. J.; Rowe, C. L.; Pechmann, J. H. K.; Hopkins, W. A. Multiple stressors and complex life cycles: Insights from a population-level assessment of breeding site contamination and terrestrial habitat loss in an amphibian Environ. Toxicol. Chem. 2011, 30, 2874-2882