A small increase in uv-b increases the susceptibility of tadpoles to predation

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1718, 2011, Pages 2575-2583

  Alton, Lesley A ^a   Wilson, Robbie S ^a   Franklin, Craig E ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Amphibian declines; Fitness consequences; Interactive effects; Predation; Sublethal effects; Ultraviolet B radiation

Indexed keywords

OZONE;

AMPHIBIAN; ATMOSPHERIC POLLUTION; CHEMICAL CUE; ENVIRONMENTAL STRESS; FITNESS; LARVA; LOCOMOTION; MORPHOLOGY; OZONE DEPLETION; POPULATION DECLINE; PREDATION RISK; RADIATION EXPOSURE; REPRODUCTIVE SUCCESS; SUBLETHAL EFFECT; SURVIVAL; ULTRAVIOLET B RADIATION;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; ASSOCIATION; FROGS AND TOADS; GROWTH, DEVELOPMENT AND AGING; LARVA; PALAEMONIDAE; PHYSIOLOGY; PREDATION; RADIATION EXPOSURE; SURVIVAL; ULTRAVIOLET RADIATION;

ANIMALS; ANURA; BEHAVIOR, ANIMAL; CUES; LARVA; OZONE; PALAEMONIDAE; PREDATORY BEHAVIOR; SURVIVAL ANALYSIS; ULTRAVIOLET RAYS;

AMPHIBIA; LIMNODYNASTES PERONII;

EID: 79960785523     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.2368     Document Type: Article

References (76)

1. IUCN. 2010 IUCN red list of threatened species. Version 2010.1. See http://www.iucnredlist.org (accessed on 23 June 2010).
2. Alford, R. A. & Richards, S. J. 1999 Global amphibian declines: a problem in applied ecology. Annu. Rev. Ecol. Syst. 30, 133-165. (doi:10.1146/annurev.ecolsys.30.1.133)
3. Farman, J. C., Gardiner, B. G. & Shanklin, J. D. 1985 Large losses of total ozone in Antarctica reveal seasonal ClOx/NOx interaction. Nature 315, 207-210. (doi:10. 1038/315207a0)
4. Stuart, S. N., Chanson, J. S., Cox, N. A., Young, B. E., Rodrigues, A. S. L., Fischman, D. L. & Waller, R. W. 2004 Status and trends of amphibian declines and extinctions worldwide. Science 306, 1783-1786. (doi:10.1126/ science.1103538)
5. WMO. 2007 Scientific assessment of ozone depletion: 2006, global ozone research and monitoring project-report No. 50. Geneva, Switzerland: World Meteorological Organization.
6. Blaustein, A. R., Belden, L. K., Hatch, A. C., Kats, L. B., Hoffman, P. D., Hays, J. B., Marco, A., Chivers, D. P. & Kiesecker, J. M. 2001 Ultraviolet radiation and amphibians. In Ecosystems, evolution, and ultraviolet radiation (eds C. S. Cockell & A. R. Blaustein), pp. 63-79. Berlin, Germany: Springer.
7. Croteau, M. C., Davidson, M. A., Lean, D. R. S. & Trudeau, V. L. 2008 Global increases in ultraviolet B radiation: potential impacts on amphibian development and metamorphosis. Physiol. Biochem. Zool. 81, 743-761. (doi:10.1086/591949)
8. Crump, D. 2001 The effects of UV-B radiation and endocrine- disrupting chemicals (EDCs) on the biology of amphibians. Environ. Rev. 9, 61-80. (doi:10.1139/ er-9-2-61)
9. Belden, L. K. & Blaustein, A. R. 2002 Exposure of redlegged frog embryos to ambient UV-B radiation in the field negatively affects larval growth and development. Oecologia 130, 551-554. (doi:10.1007/s00442-001- 0843-y)
10. Alton, L. A., Wilson, R. S. & Franklin, C. E. 2010 Risk of predation enhances the lethal effects of UV-B in amphibians. Global Change Biol. 16, 538-545. (doi:10. 1111/j.1365-2486.2009.02010.x)
11. Croteau, M. C., Martyniuk, C. J., Trudeau, V. L. & Lean, D. R. S. 2008 Chronic exposure of Rana pipiens tadpoles to UVB radiation and the estrogenic chemical 4-tert-octylphenol. J. Toxicol. Environ. Health Part A 71, 134-144. (doi:10.1080/15287390701613330)
12. Ankley, G. T., Tietge, J. E., Holcombe, G. W., DeFoe, D. L., Diamond, S. A., Jensen, K. M. & Degitz, S. J. 2000 Effects of laboratory ultraviolet radiation and natural sunlight on survival development of Rana pipiens. Can. J. Zool. 78, 1092-1100. (doi:10.1139/cjz- 78-6-1092)
13. Blaustein, A. R., Hoffman, P. D., Hokit, D. G., Kiesecker, J. M., Walls, S. C. & Hays, J. B. 1994 UV repair and resistance to solar UV-B in amphibian eggs: a link to population declines? Proc. Natl Acad. Sci. USA 91, 1791-1795. (doi:10.1073/pnas.91.5.1791)
14. Kats, L. B., Kiesecker, J. M., Chivers, D. P. & Blaustein, A. R. 2000 Effects of UV-B on antipredator behavior inthree species of amphibians. Ethology 106, 921-932. (doi:10.1046/j.1439-0310.2000.00608.x)
15. Kiesecker, J. M. & Blaustein, A. R. 1995 Synergism between UV-B radiation and a pathogen magnifies amphibian embryo mortality in nature. Proc. Natl Acad. Sci. USA 92, 11 049-11 052. (doi:10.1073/pnas.92.24. 11049)
16. van Uitregt, V. O., Wilson, R. S. & Franklin, C. E. 2007 Cooler temperatures increase sensitivity to ultraviolet B radiation in embryos and larvae of the frog Limnodynastes peronii. Global Change Biol. 13, 1114-1121. (doi:10. 1111/j.1365-2486.2007.01353.x)
17. Pahkala, M., Räsänen, K, Laurila, A, Johanson, U., Björn, L. O. & Merilä, J. 2002 Lethal and sublethal effects of UV-B/pH synergism on common frog embyros. Conserv. Biol. 16, 1063-1073. (doi:10.1046/j.1523- 1739.2002.00527.x)
18. Blaustein, A. R., Romansic, J. M., Kiesecker, J. M. & Hatch, A. C. 2003 Ultraviolet radiation, toxic chemicals and amphibian population declines. Divers. Distrib. 9, 123-140. (doi:10.1046/j.1472-4642.2003.00015.x)
19. Blaustein, A. R., Kiesecker, J. M., Chivers, D. P., Hokit, D. G., Marco, A., Belden, L. K. & Hatch, A. 1998 Effects of ultraviolet radiation on amphibians: field experiments. Am. Zool. 38, 799-812. (doi:10.1093/icb/ 38.6.799)
20. Bancroft, B. A., Baker, N. J. & Blaustein, A. R. 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, 987-996. (doi:10.1111/j.1523-1739.2008.00966.x)
21. Blaustein, A. R., Kiesecker, J. M., Chivers, D. P. & Anthony, R. G. 1997 Ambient UV-B radiation causes deformities in amphibian embryos. Proc. Natl Acad. Sci. USA 94, 13 735-13 737. (doi:10.1073/pnas.94.25. 13735)
22. Hays, J. B., Blaustein, A. R., Kiesecker, J. M., Hoffman, P. D., Pandelova, I., Coyle, D. & Richardson, T. 1996 Developmental response to amphibians to solar and artificial UVB sources: a comparative study. Photochem. Photobiol. 64, 449-456. (doi:10.1111/j.1751-1097. 1996.tb03090.x)
23. Fite, K. V., Blaustein, A. R., Bengston, L. & Hewitt, H. E. 1998 Evidence of retinal light damage in Rana cascadae: a declining amphibian species. Copeia 1998, 906-914. (doi:10.2307/1447337)
24. Flamarique, I. N., Ovaska, K. & Davis, T. M. 2000 UV-B induced damage to the skin and ocular system of amphibians. Biol. Bull. 199, 187-188. (doi:10.2307/1542889)
25. Kraft, P. G., Franklin, C. E. & Blows, M. W. 2006 Predator- induced phenotypic plasticity in tadpoles: extension or innovation. J. Evol. Biol. 19, 450-458. (doi:10.1111/j. 1420-9101.2005.01015.x)
26. Skelly, D. K. 1994 Activity level and susceptibility of anuran larvae to predation. Anim. Behav. 47, 465-468. (doi:10.1006/anbe.1994.1063)
27. Walker, J. A., Ghalambor, C. K., Griset, O. L., McKenney, D. & Reznick, D. N. 2005 Do faster starts increase the probability of evading predators? Funct. Ecol. 19, 808-815. (doi:10.1111/j.1365-2435.2005.01033.x)
28. Berven, K. A. 1990 Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica). Ecology 71, 1599-1608. (doi:10.2307/1938295)
29. Goater, C. P. 1994 Growth and survival of postmetamorphic toads: interactions among larval history, density, and parasitism. Ecology 75, 2264-2274. (doi:10.2307/1940882)
30. Scott, D. E. 1994 Effect of larval density on life history traits in Ambystoma opacum. Ecology 75, 1383-1396. (doi:10.2307/1937462)
31. Smith, D. C. 1987 Adult recruitment in chorus frogs: effects of size and date at metamorphosis. Ecology 68, 344-350. (doi:10.2307/1939265)
32. Pahkala, M., Merilä, J., Ots, I. & Laurila, A. 2003 Effects of ultraviolet-B radiation on metamorphic traits in the common frog Rana temporaria. J. Zool. 259, 57-62. (doi:10.1017/S0952836902002984)
33. Relyea, R. A. 2001 Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82, 523-540. (doi:10.1890/0012- 9658(2001)082[0523:MABPOL]2.0.CO;2)
34. Relyea, R. A. 2007 Getting out alive: how predators affect the decision to metamorphose. Oecologia 152, 389-400. (doi:10.1007/s00442-007-0675-5)
35. Sih, A. 1987 Predators and prey lifestyles: an evolutionary and ecological overview. In Predation: direct and indirect impacts on aquatic communities (eds W. C. Kerfoot & A. Sih). Hanover, Germany: University Press of New England.
36. Skelly, D. K. & Werner, E. E. 1990 Behavioral and lifehistorical changes responses of larval American toads to an odonate predator. Ecology 71, 2313-2322. (doi:10. 2307/1938642)
37. Chivers, D. P. & Smith, R. J. F. 1998 Chemical alarm signalling in aquatic predator-prey systems: a review and prospectus. Ecoscience 5, 338-352.
38. Lind, J. & Cresswell, W. 2005 Determining the fitness consequences of antipredation behavior. Behav. Ecol. 16, 945-956. (doi:10.1093/beheco/ari075)
39. Johnson, J. B., Burt, D. B. & DeWitt, T. J. 2008 Form, function, and fitness: pathways to survival. Evolution 62, 1243-1251. (doi:10.1111/j.1558-5646.2008.00343.x)
40. Bennett, A. F. & Huey, R. B. 1990 Studying the evolution of physiological performance. In Oxford surveys in evolutionary biology, vol. 7 (eds D. J. Futuyma & J. Antonovics), pp. 251-284. Oxford, UK: Oxford University Press.
41. Garland, T. J. & Losos, J. B. 1994 Ecological morphology of locomotor performance in squamate reptiles. In Ecological morphology: integrative organismal biology (eds P. C. Wainwright & S. M. Reilly), pp. 240-302. Chicago, IL: University of Chicago Press.
42. Artacho, P. & Nespolo, R. G. 2009 Natural selection reduces energy metabolism in the garden snail, Helix aspersa (Cornu aspersum). Evolution 63, 1044-1050. (doi:10.1111/j.1558-5646.2008.00603.x)
43. ARPANSA. 2010 UV-index summary for Brisbane 10th December 2005. See http://www.arpansa.gov.au/uvindex/historical/images/bri10122005.gif (accessed on 4 October 2010).
44. WHO. 2002 Global solar UV index: a practical guide. Geneva, Switzerland: World Health Organization.
45. ARPANSA. 2010 Monthly UV-index summaries for Brisbane. See http://www.arpansa.gov.au/uvindex/monthly/brimonthlysumm.htm (accessed on 4 October 2010).
46. McKinlay, A. F. & Diffey, B. L. 1987 A reference action spectrum for ultraviolet-induced erythema in skin. In Human exposure to ultraviolet radiation: risks and regulations (eds W. F. Passchier & B. F. M. Bosnjakovic), pp. 83-87. Amsterdam, The Netherlands: Elsevier.
47. Setlow, R. B. 1974 The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc. Natl Acad. Sci. USA 71, 3363-3366. (doi:10. 1073/pnas.71.9.3363)
48. McKenzie, R. L., Björn, L. O., Bais, A. & Ilyas, M. 2003 Changes in biologically active ultraviolet radiation reaching the Earth's surface. In Environmental effects of ozone depletion and its interactions with climate change: 2002 assessment, pp. 1-23. Nairobi, Kenya: United Nations Environment Programme.
49. Wardle, D. I., Kerr, J. B., McElroy, C. T. & Francis, D. R. 1997 Ozone science: a Canadian perspective on the changing ozone layer. Toronto, ON: Environment Canada.
50. Zerefos, C., Meleti, C., Balis, D., Tourpali, K. & Bais, A. F. 1998 Quasi-biennial and longer-term changes in clear-sky UV-B solar irradiance. Geophys. Res. Lett. 25, 4345-4348. (doi:10.1029/1998GL900160)
51. Blumthaler, M. & Webb, A. R. 2003 UVR climatology. In UV effects in aquatic organisms and ecosystems (eds E. R. Helbling & H. Zagarese), pp. 21-58. Cambridge, UK: Royal Society of Chemistry.
52. Udelhofen, P. M., Gies, P., Roy, C. & Randel, W. J. 1999 Surface UV radiation over Australia, 1979-1992: effects of ozone and cloud cover changes on variations of UV radiation. J. Geophys. Res. 104, 19 135-19 159. (doi:10. 1029/1999JD900306)
53. Gosner, K. L. 1960 A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16, 183-190.
54. Domenici, P. & Blake, R. W. 1997 The kinematics and performance of fish fast-start swimming. J. Exp. Biol. 200, 1165-1178.
55. von Seckendorf Hoff, K. & Wassersug, R. J. 2000 Tadpole locomotion: axial movement and tail functions in a largely vertebrateless vertebrate. Am. Zool. 40, 62-76. (doi:10.1093/icb/40.1.62)
56. Sokal, R. R. & Rohlf, F. J. 1995 Biometry: the principles and practices of statistics in biological research. New York, NY: W. H. Freeman and Co.
57. Quinn, G. P. & Keough, M. J. 2002 Experimental design and data analysis for biologists. Cambridge, UK: Cambridge University Press.
58. Romansic, J. M., Waggener, A. A., Bancroft, B. A. & Blaustein, A. R. 2009 Influence of ultraviolet-B radiation on growth, prevalence of deformities, and susceptibility to predation in Cascades frog (Rana cascadae) larvae. Hydrobiologia 624, 219-233. (doi:10.1007/s10750-009- 9703-2)
59. Warkentin, K. M. 1999 The development of behavioral defenses: a mechanistic analysis of vulnerability in redeyed tree frog hatchlings. Behav. Ecol. 10, 251-262. (doi:10.1093/beheco/10.3.251)
60. Formicki, G., Zamachowski, W. & Stawarz, R. 2003 Effect of UV-A and UV-B on oxygen consumption in common toad (Bufo bufo) tadpoles. J. Zool. 259, 317-326. (doi:10.1017/S0952836902003345)
61. Fischer, J. M., Fields, P. A., Pryzbylkowski, P. G., Nicolai, J. L. & Neale, P. J. 2006 Sublethal exposure to UV radiation affects respiration rates of the freshwater cladoceran Daphnia catawba. Photochem. Photobiol. 82, 547-550. (doi:10.1562/2005-08-30-RA-664)
62. Ylönen, O., Heikkilä, J. & Karjalainen, J. 2004 Metabolic depression in UV-B exposed larval coregonids. Ann. Zool. Fenn. 41, 577-585.
63. Capellán, E. & Nicieza, A. G. 2007 Trade-offs across life stages: does predator-induced hatching plasticity reduce anuran post-metamorphic performance? Evol. Ecol. 21, 445-458. (doi:10.1007/s10682-006-9133-9)
64. Anderson, A. L. & Brown, W. D. 2009 Plasticity of hatching in green frogs (Rana clamitans) to both egg and tadpole predators. Herpetologica 65, 207-213. (doi:10. 1655/08-016R1.1)
65. Warkentin, K. M. 1995 Adaptive plasticity in hatching age: a response to predation risk trade-offs. Proc. Natl Acad. Sci. USA 92, 3507-3510. (doi:10.1073/pnas.92.8.3507)
66. Chivers, D. P., Kiesecker, J. M., Marco, A., DeVito, J., Anderson, M. T. & Blaustein, A. R. 2001 Predatorinduced life history changes in amphibians: egg predation induces hatching. Oikos 92, 135-142. (doi:10.1034/j. 1600-0706.2001.920116.x)
67. Saenz, D., Johnson, J. B., Adams, C. K. & Dayton, G. H. 2003 Accelerated hatching of sourthern leopard frog (Rana sphenocephala) eggs in response to the presence of a crayfish (Procambarus nigrocinctus) predator. Copeia 2003, 646-649. (doi:10.1643/CE-02-172R1)
68. Laurila, A., Pakkasmaa, S., Crochet, P.-A. & Merilä, J. 2002 Predator-induced plasticity in early life history and morphology of two anuran amphibians. Oecologia 132, 524-530. (doi:10.1007/s00442-002-0984-7)
69. McCollum, S. A. & Leimberger, J. D. 1997 Predatorinduced morphological changes in an amphibian: predation by dragonflies affects tadpole shape and color. Oecologia 109, 615-621. (doi:10.1007/s004420050124)
70. Teplitsky, C., Plénet, S., Léna, J.-P., Mermet, N., Malet, E. & Joly, P. 2005 Escape behaviourand ultimate causes of specific induced defences in an anuran tadpole. J. Evol. Biol. 18, 180-190. (doi:10.1111/j.1420-9101.2004.00790.x)
71. Wilson, R. S., Kraft, P. G. & Van Damme, R. 2005 Predator- specific changes in morphology and swimming performance of larval Rana lessonae. Funct. Ecol. 19, 238-244. (doi:10.1111/j.1365-2435.2005.00958.x)
72. Van Buskirk, J., Anderwald, P., Lupold, S., Reinhardt, L. & Schuler, H. 2003 The lure effect, tadpole tail shape, and the target of dragonfly strikes. J. Herpetol. 37, 420-424. (doi:10.1670/0022-1511(2003)037[0420:TLETTS]2.0. CO;2)
73. Van Buskirk, J. & McCollum, S. A. 2000 Influence of tail shape on tadpole swimming performance. J. Exp. Biol. 203, 2149-2158.
74. Laurila, A., Crochet, P.-A. & Merilä, J. 2001 Predationinduced effects on hatchling morphology in the common frog (Rana temporaria). Can. J. Zool. 79, 926-930. (doi:10.1139/cjz-79-5-926)
75. Mandrillon, A.-L. & Saglio, P. 2009 Effects of single and combined embryonic exposures of herbicide and conspecific chemical alarm cues on hatching and larval traits in the common fog (Rana temporaria). Arch. Environ. Contam. Toxicol. 56, 566-576. (doi:10.1007/s00244-008-9196-4)
76. Kiesecker, J. M., Blaustein, A. R. & Belden, L. K. 2001 Complex causes of amphibian population declines. Nature 410, 681-684. (doi:10.1038/35070552)