A meta-analysis of the effects of ultraviolet B radiation and its synergistic interactions with pH, contaminants, and disease on amphibian survival

Conservation Biology

Volumn 22, Issue 4, 2008, Pages 987-996

  Bancroft, Betsy A ^a,b   Baker, Nick J ^a   Blaustein, Andrew R ^a  

^a OREGON STATE UNIVERSITY   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Anura; Caudata; Life history stage; Meta analysis; Synergistic; UVB radiation

Indexed keywords

BIODIVERSITY; CONSERVATION PLANNING; DAMAGE; DISEASE; ENVIRONMENTAL STRESS; HABITAT LOSS; HUMAN ACTIVITY; INTRODUCED SPECIES; LARVA; LIFE HISTORY; META-ANALYSIS; PH; POLLUTION EFFECT; POPULATION DECLINE; SURVIVAL; SYNERGISM; ULTRAVIOLET B RADIATION;

AMPHIBIA; ANIMAL; ANIMAL EMBRYO; ARTICLE; DRUG EFFECT; LARVA; META ANALYSIS; PH; PHYSIOLOGY; RADIATION EXPOSURE; SPECIES EXTINCTION; ULTRAVIOLET RADIATION; WATER POLLUTANT;

AMPHIBIA; ANIMALS; EMBRYO, NONMAMMALIAN; EXTINCTION, BIOLOGICAL; HYDROGEN-ION CONCENTRATION; LARVA; ULTRAVIOLET RAYS; WATER POLLUTANTS, CHEMICAL;

AMPHIBIA; ANURA; AVES; CAUDATA; MAMMALIA; SALAMANDROIDEA;

EID: 48749108798     PISSN: 08888892     EISSN: 15231739     Source Type: Journal    
DOI: 10.1111/j.1523-1739.2008.00966.x     Document Type: Article

References (83)

1. Adams, D. C., J. Gurevitch, and M. S. Rosenberg. 1997. Resampling tests for meta-analysis of ecological data. Ecology 78 : 1277 1283.
2. Allen, C. D., M. Savage, D. A. Falk, K. F. Suckling, T. W. Swetnam, T. Schulke, P. B. Stacey, P. Morgan, M. Hoffman, and J. T. Klingel. 2002. Ecological restoration of Southwestern ponderosa pine ecosystems: a broad perspective. Ecological Applications 12 : 1418 1433.
3. Ankley, G. T., J. E. Tietge, D. L. DeFoe, K. M. Jensen, G. W. Holocombe, E. J. Durhan, and S. A. Diamond. 1998. Effects of ultraviolet light and methoprene on survival and development of Rana pipiens. Environmental Toxicology and Chemistry 17 : 2530 2542.
4. Ankley, G. T., J. E. Tietge, G. W. Holocombe, D. L. DeFoe, S. A. Diamond, K. M. Jensen, and S. J. Degitz. 2000. Effects of laboratory ultraviolet radiation and natural sunlight on survival and development of Rana pipiens. Canadian Journal of Zoology 78 : 1092 1100.
5. Ankley, G. T., S. A. Diamond, J. E. Tietge, G. W. Holocombe, K. M. Jensen, D. L. DeFoe, and R. Peterson. 2002. Assessment of the risk of solar ultraviolet radiation to amphibians: I. Dose-dependent induction of hind limb malformations in the northern leopard frog (Rana pipiens). Environmental Science Technology 36 : 2853 2858.
6. Bancroft, B. A., N. J. Baker, and A. R. Blaustein. 2007. The effects of UVB radiation in marine and freshwater organisms: a synthesis through meta-analysis. Ecology Letters 10 : 332 345.
7. Bancroft, B. A., N. J. Baker, C. L. Searle, T. S. Garcia, and A. R. Blaustein. 2008. Larval amphibians seek warm temperatures and do not avoid harmful UVB radiation. Behavioral Ecology. DOI :.
8. Baud, D. R., and M. L. Beck. 2005. Interactive effects of UV-B and copper on spring peeper tadpoles (Pseudacris crucifer). Southeastern Naturalist 4 : 15 22.
9. Belden, L. K., E. L. Wildy, and A. R. Blaustein. 2000. Growth, survival and behaviour of larval long-toed salamanders (Ambystoma macrodactylum) exposed to ambient levels of UV-B radiation. Journal of Zoology, London 251 : 473 479.
10. Belden, L. K., I. T. Moore, R. T. Mason, J. C. Wingfield, and A. R. Blaustein. 2003. Survival, the hormonal stress response and UV-B avoidance in Cascades frog tadpoles (Rana cascadae) exposed to UV-B radiation. Functional Ecology 17 : 409 416.
11. Blaustein, A. R., and L. K. Belden. 2003. Amphibian defenses against ultraviolet-B radiation. Evolution & Development 5 : 89 97.
12. Blaustein, A. R., and J. M. Kiesecker. 2002. Complexity in conservation: lessons from the global decline of amphibian populations. Ecology Letters 5 : 597 608.
13. Blaustein, A. R., P. D. Hoffman, D. G. Hokit, J. M. Kiesecker, S. C. Walls, and J. B. Hays. 1994. UV repair and resistance to solar UV-B in amphibian eggs: A link to population declines? Proceedings of the National Academy of Sciences of the United States of America 91 : 1791 1795.
14. Blaustein, A. R., P. D. Hoffman, J. M. Kiesecker, and J. B. Hays. 1996. DNA repair activity and resistance to solar UV-B radiation in eggs of the red-legged frog. Conservation Biology 10 : 1398 1402.
15. Blaustein, A. R., J. M. Kiesecker, D. P. Chivers, D. G. Hokit, A. Marco, L. K. Belden, and A. C. Hatch. 1998. Effects of ultraviolet radiation on amphibians: field experiments. American Zoologist 38 : 799 812.
16. Blaustein, A. R., L. K. Belden, A. C. Hatch, L. B. Kats, P. D. Hoffman, J. B. Hays, A. Marco, D. P. Chivers, and J. M. Kiesecker. 2001. Ultraviolet radiation and amphibians. Pages 63 79 in C. S. Cockell and A. R. Blaustein, editors. Ecosystems, evolution, and ultraviolet radiation. Springer-Verlag, New York.
17. Blaustein, A. R., J. M. Romansic, J. M. Kiesecker, and A. C. Hatch. 2003. Ultraviolet radiation, toxic chemicals and amphibian population declines. Diversity and Distributions 9 : 123 140.
18. Borer, E. T., E. W. Seabloom, J. B. Shurin, K. E. Anderson, C. A. Blanchette, B. Broitman, S. D. Cooper, and B. S. Halpern. 2005. What determines the strength of a trophic cascade? Ecology 86 : 528 537.
19. Borer, E. T., B. S. Halpern, and E. W. Seabloom. 2006. Asymmetry in community regulation: effects of predators and productivity. Ecology 87 : 2813 2820.
20. Bothwell, M. L., D. M. J. Sherbort, and C. M. Pallock. 1994. Ecosystem response to solar ultraviolet-B radiation: influence of trophic level interactions. Science 265 : 97 100.
21. Bruner, M. A., P. A. Shipman, M. Rao, and J. M. Bantle. 2002. Developmental effects of ambient UV-B light and landfill leachate in Rana blairi and Hyla chrysoscelis. Ecotoxicology and Environmental Safety 53 : 73 80.
22. Caldwell, M. M., L. O. Björn, J. F. Bornman, S. D. Flint, G. Kulandaivelu, A. H. Teramura, and M. Tevini. 1998. Effects of increased solar ultraviolet radiation on terrestrial ecosystems. Journal of Photochemistry and Photobiology B 46 : 40 52.
23. Christensen, M. R., M. D. Graham, R. D. Vinebrook, D. L. Findlay, M. J. Paterson, and M. A. Turner. 2006. Multiple anthropogenic stressors cause ecological surprises in boreal lakes. Global Change Biology 12 : 2316 2322.
24. Collins, J. P., and A. Storfer. 2003. Global amphibian declines: sorting the hypotheses. Diversity and Distributions 9 : 89 98.
25. Diamond, S. A., et al. 2005. Estimated ultraviolet radiation doses in wetlands in six national parks. Ecosystems 8 : 462 477.
26. Dupré, R. K., and J. W. Petranka. 1985. Ontogeny of temperature selection in larval amphibians. Copeia 1985 : 462 467.
27. Epel, D., K. Hernela, M. Schick, and C. Patton. 1999. Development in the floating world: defenses of eggs and embryos against damage from UV radiation. American Zoologist 39 : 271 278.
28. Feder, M. E. 1999. Organismal, ecological, and evolutionary aspects of heat-shock proteins and the stress response: established conclusions and unresolved issues. American Zoologist 39 : 857 864.
29. Fleeger, J. W., K. R. Carman, and R. M. Nisbet. 2003. Indirect effects of contaminants in aquatic ecosystems. The Science of the Total Environment 317 : 207 233.
30. Garcia, T. S., J. Stacy, and A. Sih. 2004. Larval salamander response to UV radiation and predation risk: color change and microhabitat use. Ecological Applications 14 : 1055 1064.
31. Gergel, S. E., S. R. Carpenter, and E. H. Stanley. 2005. Do dams and levees impact nitrogen cycling? Simulating the effects of flood alterations on floodplain denitrification. Global Change Biology 11 : 1352 1367.
32. Gurevitch, J., and L. V. Hedges. 1999. Statistical issues in ecological meta-analyses. Ecology 80 : 1142 1149.
33. Gurevitch, J., J. A. Morrson, and L. V. Hedges. 2000. The interaction between competition and predation: a meta-analysis of field experiments. The American Naturalist 155 : 435 453.
34. Häkkinen, J., S. Pasanen, and J. V. K. Kukkonen. 2001. The effects of solar UV-B radiation on embryonic mortality and development in three boreal anurans (Rana temporaria, Rana arvalis, and Bufo bufo). Chemosphere 44 : 441 446.
35. Hatch, A. C., and A. R. Blaustein. 2002. Combined effects of UV-B, nitrate, and low pH reduce survival and activity level of larval Cascades frogs (Rana cascadae). Archives of Environmental Contamination and Toxicology 39 : 494 499.
36. Hatch, A. C., and A. R. Blaustein. 2003. Combined effects of UV-B radiation and nitrate fertilizer on larval amphibians. Ecological Applications 13 : 1083 1093.
37. Hawkes, C. V., and J. J. Sullivan. 2001. The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82 : 2045 2058.
38. Hedges, L. V., J. Gurevitch, and P. S. Curtis. 1999. The meta-analysis of response ratios in experimental ecology. Ecology 80 : 1150 1156.
39. Hutchison, V. H., and R. K. Dupré. 1992. Thermoregulation. Pages 206 249 in M. E. Feder and W. W. Burggren, editors. Environmental physiology of the Amphibia. The University of Chicago Press, Chicago.
40. Hutchison, V. H., and J. D. Maness. 1979. The role of behavior in temperature acclimation and tolerance in ectotherms. American Zoologist 19 : 367 384.
41. IPCC (Intergovernmental Panel on Climate Change). 2007. Climate change 2007: the physical basis. Contribution of Working Group 1 to the Fourth assessment report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland. Available from http://www.ipcc.ch/SPM2feb07.pdf (accessed April 2007).
42. Jablonski, N. J. 1998. Ultraviolet light-induced neural tube defects in amphibian larvae and their implications for the evolution of melanized pigmentation and declines of amphibian populations. Journal of Herpetology 32 : 455 457.
43. Jones, R. B. 1998. TechDig 2.0 Software. The WinSite Group, Bloomington, Indiana. Available from http://www.winsite.com/bin/Info?500000016137 (accessed April 2007).
44. Keen, W. H., and E. E. Schroeder. 1975. Temperature selection and tolerance in three species of Ambystoma larvae. Copeia 1975 : 523 530.
45. Kerr, J. B., and C. T. McElroy. 1993. Evidence for large upward trends of ultraviolet-B radiation linked to ozone depletion. Science 262 : 1032 1034.
46. Kiesecker, J. M., and A. R. Blaustein. 1995. Synergism between UV-B radiation and a pathogen magnifies amphibian embryo mortality in nature. Proceedings of the National Academy of Sciences of the United States of America 92 : 11049 11052.
47. Kiesecker, J. M., L. K. Belden, and A. R. Blaustein. 2001. Complex causes of amphibian population declines. Nature 410 : 681 684.
48. Koponen, P. S., and J. V. K. Kukkonen. 2002. Effects of bisphenol A and artificial UVB radiation on the early development of Rana temporaria. Journal of Toxicology and Environmental Health, Part A 65 : 947 959.
49. Lee, R. E., C.-P. Chen, and D. L. Denlinger. 1987. A rapid cold-hardening process in insects. Science 238 : 1415 1417.
50. Lesser, M. P., S. L. Turtle, J. H. Farrell, and C. W. Walker. 2001. Exposure to ultraviolet radiation (290-400 nm) causes oxidative stress, DNA damage, and expression of p53/p73 in laboratory experiments on embryos of the spotted salamander, Ambystoma maculatum. Physiological and Biochemical Zoology 74 : 733 741.
51. Licht, L. E. 2003. Shedding light on ultraviolet radiation and amphibian embryos. BioScience 53 : 551 561.
52. Long, L. E., L. S. Saylor, and M. E. Soulé. 1995. A pH/UV-B synergism in amphibians. Conservation Biology 9 : 1301 1303.
53. Lucas, E. A., and W. A. Reynolds. 1967. Temperature selection by amphibian larvae. Physiological Zoology 40 : 159 171.
54. Madronich, S., R. L. McKenzie, L. O. Björn, and M. M. Caldwell. 1998. Changes in biologically active ultraviolet radiation reaching the Earth's surface. Journal of Photochemistry and Photobiology B 46 : 5 19.
55. Marinone, M. C., S. M. Marque, D. A. Suárez, M. d. C. Diéguez, P. Pérez, P. De Los Ríos, D. Soto, and H. E. Zagarese. 2006. UV radiation as a potential driving force for zooplankton community structure in Patagonian lakes. Photochemistry and Photobiology 82 : 962 971.
56. Mendelson III., J. R., et al. 2006. Confronting amphibian declines and extinctions. Science 313 : 48.
57. Merilä, J., A. Laurila, and M. Pahkala. 2000. Effects of ambient UV-B radiation on early development of the common frog (Rana temporaria) embryos in the subarctic. Annales Zoologici Fennici 37 : 51 58.
58. Mostajir, B., S. Demers, S. de Mora, C. Belzile, J.-P. Chanut, M. Gosselin, S. Roy, P. Z. Villegas, J. Fauchot, and J. Bouchard. 1999. Experimental test of the effect of ultraviolet-B radiation in a planktonic community. Limnology and Oceanography 44 : 586 596.
59. Nagl, A. M., and R. Hofer. 1997. Effects of ultraviolet radiation on early larval stages of the Alpine newt, Triturus alpestris, under natural and laboratory conditions. Oecologia 110 : 514 519.
60. Nobel, P. S. 1982. Low-temperature tolerance and cold hardening of cacti. Ecology 63 : 1650 1656.
61. O'Hara, R. K. 1981. Habitat selection behavior in three species of anuran larvae: environmental cues, ontogeny, and adaptive significance. PhD thesis. Oregon State University, Corvallis, Oregon.
62. Osenberg, C. W., O. Sarnelle, and S. D. Cooper. 1997. Effect size in ecological experiments: the application of biological models in meta-analysis. The American Naturalist 150 : 798 812.
63. Pahkala, M., A. Laurila, L. O. Björn, and J. Merilä. 2001. Effects of ultraviolet-B radiation and pH on early development of the moor frog Rana arvalis. Journal of Applied Ecology 38 : 628 636.
64. Pahkala, M., K. Räsänen, A. Laurila, U. Johanson, L. O. Björn, and J. Merilä. 2002. Lethal and sublethal effects of a UV-B/pH synergism on common frog embryos. Conservation Biology 16 : 1063 1073.
65. Palen, W. J., C. E. Williamson, and A. A. Clauser. 2005. Impact of UV-B exposure on amphibian embryos: linking species physiology and oviposition behaviour. Proceedings of the Royal Society B 272 : 1227 1234.
66. Parmesan, C., and G. Yohe. 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421 : 37 42.
67. Root, T. L., J. T. Price, K. R. Hall, S. H. Schneider, C. Rosenzweig, and J. A. Pounds. 2003. Fingerprints of global warming on wild animals and plants. Nature 421 : 57 60.
68. Rosenberg, M. S., D. C. Adams, and J. Gurevitch. 2000. MetaWin: statistical software for meta-analysis. Version 2.0. Sinauer Associates, Sunderland, Massachusetts.
69. Rosenthal, R. 1979. The "file drawer problem" and tolerance for null results. Psychology Bulletin 86 : 638 641.
70. Sakai, A. K., et al. 2001. The population biology of invasive species. Annual Reviews in Ecology and Systematics 32 : 305 332.
71. Sancar, A., and G. B. Sancar. 1988. DNA repair enzymes. Annual Review of Biochemistry 57 : 29 67.
72. Shurin, J. B., E. T. Borer, E. W. Seabloom, K. Anderson, B. Broitman, S. D. Cooper, and B. S. Halpern. 2002. A cross-ecosystem comparison of the strength of trophic cascades. Ecology Letters 5 : 785 791.
73. Sih, A., A. M. Bell, and J. L. Kerby. 2004. Two stressors are far deadlier than one. Trends in Ecology & Evolution 19 : 274 276.
74. Smith, M. A., M. Berrill, and C. M. Kapron. 2002. Photolyase activity of the embryo and the ultraviolet absorbance of embryo jelly for several Ontario amphibian species. Canadian Journal of Zoology 80 : 1109 1116.
75. Solomon, S. 1999. Stratospheric ozone depletion: a review of concepts and history. Reviews of Geophysics 37 : 275 316.
76. Starnes, S. M., C. A. Kennedy, and J. W. Petranka. 2000. Sensitivity of embryos of Southern Appalachian amphibians to ambient solar UV-B radiation. Conservation Biology 14 : 277 282.
77. Stuart, S. N., J. S. Chanson, N. A. Cox, B. E. Young, A. S. L. Rodrigues, D. L. Fischman, and R. W. Waller. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306 : 1783 1786.
78. Tevini, M., editor. 1993. UV-B radiation and ozone depletion: effects on humans, animals, plants, microorganisms, and materials. Lewis Publishers, Boca Raton, Florida.
79. van de Mortel, T. F., and W. A. Buttemer. 1998. Avoidance of ultraviolet-B radiation in frogs and tadpoles of the species Litoria aurea, L. dentata, and L. peronii. Proceedings of the Linnean Society of New South Wales 119 : 173 179.
80. Vonesh, J. R., and O. De la Cruz. 2002. Complex life cycles and density dependence: assessing the contribution of egg mortality to amphibian declines. Oecologia 133 : 325 333.
81. Wahl, M., et al. 2004. UV effects that come and go: a global comparison of marine benthic community level impacts. Global Change Biology 10 : 1962 1972.
82. Wollmuth, L. P., L. I. Crawshaw, R. B. Forbes, and D. A. Grahn. 1987. Temperature selection during development in a montane anuran species, Rana cascadae. Physiological Zoology 60 : 472 480.
83. Zaga, A., E. E. Little, C. F. Rabeni, and M. R. Ellersieck. 1998. Photoenhanced toxicity of a carbamate insecticide to early life stage anuran amphibians. Environmental Toxicology and Chemistry 17 : 2543 2553.