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Elevational differences in trait response to UV-B radiation by long-toed salamander populations

  • Behavioral ecology - Original research
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Abstract

Amphibian species capable of optimizing trait response to environmental stressors may develop complex strategies for defending against rapid environmental change. Trait responses may differ between populations, particularly if stressor strength varies across spatial or temporal gradients. Ultraviolet-B (UV-B) radiation is one such stressor that poses a significant threat to amphibian species. We examined the ability of long-toed salamanders (Ambystoma macrodactylum) at high- and low-elevation breeding sites to cooperatively employ behavioral and physiological trait responses to mediate UV-B damage. We performed a microhabitat survey to examine differences in oviposition behavior and UV-B conditions among breeding populations at high- (n = 3; >1,500 m) and low-elevation (n = 3; <100 m) sites. We found significant differences in oviposition behavior across populations, with females at high-elevation sites selecting oviposition substrates in UV-B protected microhabitats. We also collected eggs (n = 633) from each of the breeding sites for analysis of photolyase activity, a photoreactivating enzyme that repairs UV-B damage to the DNA, using a photoproduct immunoassay. Our results revealed no significant differences in photolyase activity between long-toed salamander populations at high and low elevations. For high-elevation salamander populations, relatively low physiological repair capabilities in embryos appear to be buffered by extensive behavioral modifications to reduce UV-B exposure and standardize developmental temperatures. This study provides valuable insight into environmental stress responses via the assessment of multiple traits in allowing sensitive species to persist in rapidly changing landscapes.

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References

  • Adams M, Hossack B, Knapp R, Corn P, Diamond S, Trenham P, Fagre D (2005) Distribution patterns of lentic-breeding amphibians in relation to ultraviolet radiation exposure in Western North America. Ecosystems 8:488–500. doi:10.1007/s10021-003-0033-3

    Article  Google Scholar 

  • Alton L, Wilson R, Franklin C (2010) Risk of predation enhances the lethal effects of UV-B in amphibians. Glob Change Biol 16:538–545. doi:10.1111/j.1365-2486.2009.02010.x

    Article  Google Scholar 

  • Bancroft B, Baker N, Blaustein A (2007) Effects of UVB radiation on marine and freshwater organisms: a synthesis through meta-analysis. Ecol Lett 10:332–345. doi:10.1111/j.1461-0248.2007.01022.x

    Article  PubMed  Google Scholar 

  • Bancroft BA, Baker NJ, Searle CA, Garcia TS, Blaustein AR (2008) Larval amphibians seek warm temperatures and do not avoid harmful UVB radiation. Behav Ecol 19(4):879–886. doi:10.1093/beheco/arn044

    Article  Google Scholar 

  • Belden L, Blaustein A (2002) Population differences in sensitivity to UV-B radiation in larval long-toed salamanders. Ecology 83(6):1586–1590. doi:10.1046/j.1523-1739.2002.t01-1-02109.x

    Article  Google Scholar 

  • Belden LK, Wildy EL, Blaustein AR (2000) Growth, survival, and behavior of larval long-toed salamanders (Ambystoma macrodactylum) exposed to ambient levels of UV-B radiation. J Zool 251:473–479. doi:10.1111/j.1469-7998.2000.tb00803.x

    Article  Google Scholar 

  • Blaustein AR, Bancroft BA (2007) Amphibian population declines: evolutionary considerations. Bioscience 57(5):437–444. doi:10.1641/B570517

    Article  Google Scholar 

  • Blaustein A, Belden L (2003) Amphibian defenses against ultraviolet-B radiation. Evol Devel 5(1):89–97. doi:10.1046/j.1525-142X.2003.03014.x

    Article  CAS  Google Scholar 

  • Blaustein AR, Hoffman PD, Hokit GD, Kiesecker JK, Walls SC, Hays JB (1994) UV repair and resistance to solar UV-B in amphibian eggs: a link to population declines? Proc Natl Acad Sci 91:1791–1795. doi:10.1073/pnas.91.5.1791

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Blaustein AR, Edmond B, Kiesecker JK, Beatty JJ, Hokit DG (1995) Ambient ultraviolet radiation causes mortality in salamander eggs. Ecol App 5(3):740–743. doi:10.2307/1941981

    Article  Google Scholar 

  • Blaustein AR, Hoffman PD, Kiesecker JM, Hays JB (1996) DNA repair and activity and resistance to solar UV-B radiation in eggs of the red-legged frog. Conserv Biol 10(5):1398–1402. doi:10.1046/j.1523-1739.1996.10051398.x

    Article  Google Scholar 

  • Blaustein A, Belden L, Olson D, Green D, Root T, Kiesecker J (2001) Amphibian breeding and climate change. Conserv Biol 15(6):1804–1809. doi:10.1046/j.1523-1739.2001.00307.x

    Article  Google Scholar 

  • Blumthaler M, Ambach W (1990) Indication of increasing solar ultraviolet-B radiation flux in alpine regions. Science 248(4952):206–208. doi:10.1126/science.2326634

    Article  CAS  PubMed  Google Scholar 

  • Both C, Artemyev AV, Blaauw B, Cowie RJ, Dekhuijzen AJ, Eeva T, Enemar A, Gustafsson L, Ivankina EV, Järvinen A, Metcalfe NB, Nyholm NE, Potti J, Ravussin PA, Sanz JJ, Silverin B, Slater FM, Sokolov LV, Török J, Winkel W, Wright J, Zang H, Visser ME (2004) Large-scale geographical variation confirms that climate change causes birds to lay earlier. Proc R Soc B 271:1657–1662

    Article  PubMed Central  PubMed  Google Scholar 

  • Brodie E III (1992) Correlational selection for color pattern and antipredator behavior in the garter snake Thamnophis ordinoides. Evolution 46(5):1284–1298

    Article  Google Scholar 

  • Caruso C, Maherali H, Mikulyuk A, Carlson K, Jackson R (2005) Genetic variance and covariance for physiological traits in Lobelia: are there constraints on adaptive evolution? Evolution 59(4):826–837. doi:10.1554/04-501

    PubMed  Google Scholar 

  • Croteau M, Davidson M, Lean DRS, Trudeau V (2008) Global increases in ultraviolet B radiation: potential impacts on amphibian development and metamorphosis. Physiol Biochem Zool 81(6):743–761. doi:10.1086/591949

    Article  CAS  PubMed  Google Scholar 

  • Crump D, Berrill M, Coulson D, Lean DRS, McGillivray L, Smith MA (1999) Sensitivity of amphibian embryos, tadpoles, and larvae to enhanced UV-B radiation in natural pond conditions. Can J Zool 77:1956–1966. doi:10.1139/cjz-77-12-1956

    Article  Google Scholar 

  • Curtis M, Hays J (2007) Tolerance of dividing cells to replication stress in UVB-irradiated Arabidopsis roots: requirements for DNA translesion polymerases eta and zeta. DNA Repair 6(9):1859–1872. doi:10.1016/j.dnarep.2007.03.004

    Article  Google Scholar 

  • Endler JA (1995) Multiple-trait coevolution and environmental gradients in guppies. Trends Ecol Evol 10(1):22–29. doi:10.1016/S0169-5347(00)88956-9

    Article  CAS  PubMed  Google Scholar 

  • Forister ML, Shapiro AM (2003) Climatic trends and advancing spring flight of butterflies in lowland California. Glob Change Biol 9:1130–1135

    Article  Google Scholar 

  • Friedberg EC, Walker GC, Siede W, Woods RD, Schultz RA, Ellenberger T (2006) DNA Repair and Mutagenesis, 2nd edn. American Society for Microbiology Press, Washington

    Google Scholar 

  • Garcia T, Paoletti D, Blaustein A (2009) Correlated trait response to multiple selection pressures in larval amphibians reveal conflict avoidance strategies. Freshwater Biol 54:1066–1077. doi:10.1111/j.1365-2427.2008.02154.x

    Article  Google Scholar 

  • Häder D, Kumar H, Smith R, Worrest R (2007) Effects of solar UV radiation on aquatic ecosystems and interactions with climate change. Photochem Photobiol Sci 6:267–285. doi:10.1039/b700020k

    Article  PubMed  Google Scholar 

  • Harper M, Peckarsky B (2006) Emergence cues of a mayfly in a high-altitude stream ecosystem: potential response to climate change. Ecol Appl 16(2):612–621

    Article  PubMed  Google Scholar 

  • Harrison RG (1969) Harrison stages and description of the normal development of the spotted salamander, Ambystoma punctatum (Linn.). In: Wilens S (ed) Organization and development of the embryo. Yale University, Hartford, pp 44–66

    Google Scholar 

  • Hoffman R, Larson G, Brokes B (2003) Habitat segregation of Ambystoma gracile and Ambystoma macrodactylum in mountain ponds and lakes, Mount Rainier National Park, Washington. USA. J Herpetol 37(1):24–34

    Article  Google Scholar 

  • Jones LC, Leonard WP, Olson DH (2005) Amphibians of the Pacific Northwest. Seattle Audubon Society, Seattle

    Google Scholar 

  • Kern M, Nassar A, Guzy J, Dorcas M (2013) Oviposition site selection by spotted salamandars (Ambystoma maculatum) in an isolated wetland. J Herpetol 47(3):445–449. doi:10.1670/11-179

    Article  Google Scholar 

  • Kiesecker J, Blaustein A, Belden L (2001) Complex causes of amphibian population declines. Nature 410(6829):681–684. doi:10.1038/35070552

    Article  CAS  PubMed  Google Scholar 

  • Killen SS, Marras S, Metcalfe NB, McKenzie DJ, Domenici P (2013) Environmental stressors alter relationships between physiology and behaviour. Trends Ecol Evol. doi:10.1016/j.tree.2013.05.005 (in press)

    PubMed  Google Scholar 

  • Lascoux M (1997) Unpredictability of correlated response to selection: linkage and initial frequency also matter. Evolution 51(5):1394–1400. doi:10.2307/2411191

    Article  Google Scholar 

  • Licht L (2003) Shedding light on ultraviolet radiation and amphibian embryos. Bioscience 53(6):551–561

    Article  Google Scholar 

  • Marco A, Lizana M, Alvarez A, Blaustein A (2001) Egg-wrapping behavior protects newt embryos from UV radiation. Anim Behav 61:639–644. doi:10.1006/anbe.2000.1632

    Article  Google Scholar 

  • Matsunaga T (2007) In vitro assays for evaluating the cellular responses to DNA damage induced by solar UV. AATEX 14:637–640

    Google Scholar 

  • Nussbaum RA, Brodie ED Jr, Storm RM (1983) Amphibians and reptiles of the Pacific Northwest. University of Idaho Press, Moscow

    Google Scholar 

  • Palen WJ, Schindler D (2010) Water clarity, maternal behavior, and physiology combine to eliminate UV radiation risk to amphibians in a montane landscape. Proc Natl Acad Sci 107(21):9701–9706. doi:10.1073/pnas.0912970107

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pandelova I, Hewitt SR, Hays JB (2005) Fluoroimaging-based immunoassay of DNA photoproducts in ultraviolet-B-irradiated tadpoles. Method Mol Biol 291(1):29–38. doi:10.1385/1-59259-840-4:029

    CAS  Google Scholar 

  • Pearl C, Adams M, Bury RB, Wente W, McCreary B (2009) Evaluating amphibian declines with site revisits and occupancy models: status of montane anurans in the Pacific Northwest USA. Diversity 1:166–181. doi:10.3390/d1020166

    Article  Google Scholar 

  • Perin S, Lean DRS (2004) The effects of ultraviolet-B radiation on freshwater ecosystems of the Arctic: influence from stratospheric ozone depletion and climate change. Environ Rev 12:1–70. doi:10.1139/A04-003

    Article  CAS  Google Scholar 

  • Petranka JW, Petranka JG (1981) On the evolution of nest site selection in the marbled salamander, Ambystoma opacum. Copeia 1981:387–391

    Article  Google Scholar 

  • Primack R, Ibáñez I, Higuchi H, Don Lee S, Miller-Rushing A, Wilson A, Silander J Jr (2009) Spatial and interspecific variability in phenological responses to warming temperatures. Biol Conserv 142:2569–2577

    Article  Google Scholar 

  • Refsnider J, Janzen F (2010) Putting eggs in one basket: ecological and evolutionary hypotheses for variation in oviposition-site choice. Annu Rev Ecol Evol S 41:39–57. doi:10.1146/annurev-ecolsys-102209-144712

    Article  Google Scholar 

  • Resetarits WJ, Wilbur HM (1989) Choice of oviposition site by Hyla chrysoscelis: role of predators and competitors. Ecology 70(1):220–228. doi:10.2307/1938428

    Article  Google Scholar 

  • Romano A, Forcina G, Barbanera F (2008) Breeding site selection by olfactory cues in the threatened northern spectacled salamander Salamandrina perspicillata (Savi 1821). Aquat Conserv 18(5):799–805. doi:10.1002/aqc.890

    Article  Google Scholar 

  • Sih A, Ferrari MCO, Harris DJ (2011) Evolution and behavioural responses to human-induced rapid environmental change. Evol Appl 4(2):367–387

    Article  PubMed Central  Google Scholar 

  • Sinha RP, Häder DP (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1:225–236. doi:10.1039/b201230h

    Article  CAS  PubMed  Google Scholar 

  • Smith MA, Berrill M, Kapron C (2002) Photolyase activity of the embryo and the ultraviolet absorbance of embryo jelly for several Ontario amphibian species. Can J Zool 80:1109–1116. doi:10.1139/Z02-093

    Article  CAS  Google Scholar 

  • Smithgill SJ, Berven KA (1979) Predicting amphibian metamorphosis. Am Nat 113(4):563–585. doi:10.1086/283413

    Article  Google Scholar 

  • Snodgrass JW, Forester DC, Lahti M, Lehman E (2007) Dusky salamander (Desmognathus fuscus) nest-site selection over multiple spatial scales. Herpetologica 63:441–449

    Article  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA, Young BE, Rodrigues ASL, Fischman DL, Waller RW (2004) Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786. doi:10.1126/science.1103538

    Article  CAS  PubMed  Google Scholar 

  • Thurman LL (2012) Elevational differences in UV-B response by the long-toed salamander (Ambystoma macrodactylum). Master thesis, Oregon State University, Corvallis, OR, USA

  • Todd B, Scott D, Pechmann J, Gibbons JW (2010) Climate change correlates with rapid delays and advancements in reproductive timing in an amphibian community. Proc R Soc B 278:2191–2197

    Article  PubMed Central  PubMed  Google Scholar 

  • van de Mortel T, Buttemer W, Hoffman P, Hays J, Blaustein A (1998) A comparison of photolyase activity in three Australian tree frogs. Oecologia 115:366–369. doi:10.1007/s004420050529

    Article  Google Scholar 

  • Vredenburg VT (2004) Reversing introduced species effects: experimental removal of introduced fish leads to rapid recovery of a declining frog. Proc Natl Acad Sci 101(20):7646–7650. doi:10.1073/pnas.0402321101

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wilbur HM, Collins JP (1973) Ecological aspects of amphibian metamorphosis. Science 182(4119):1305–1314. doi:10.1126/science.182.4119.1305

    Article  CAS  PubMed  Google Scholar 

  • Worley A, Houle D, Barrett S (2003) Consequences of hierarchical allocation for the evolution of life-history traits. Am Nat 161(1):153–167. doi:10.1086/345461

    Article  PubMed  Google Scholar 

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Acknowledgments

We would like to thank the John Hays Laboratory in the Department of Environmental and Molecular Toxicology at Oregon State University for their extensive assistance in the laboratory analysis portion of this project. We thank L. Ganio, K. Dugger, and J. Van Sickle for assistance with statistical analyses and the Willamette Valley National Wildlife Refuge Complex and US Forest Service for site access. We thank D.T. Thurman and S.K. McMurrain for their invaluable contributions. This study was funded by scholarship stipends from The Society for Northwestern Vertebrate Biology, Oregon State University Department of Fisheries and Wildlife, and Oregon State University College of Agricultural Sciences. Animals were collected under Oregon Department of Fisheries and Wildlife Scientific Taking Permit no. 078-10, US Fish and Wildlife Service Special Use Permit no. 13590-11-02, E.E. Wilson Management Area Special Use Permit no. 1513, and Oregon State University Animal Care and Use Protocol no. 3978.

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Authors and Affiliations

  1. Department of Fisheries and Wildlife, Oregon State University, Corvallis, USA

    Lindsey L. Thurman & Tiffany S. Garcia

  2. Department of Environmental and Molecular Toxicology, Oregon State University, Corvallis, USA

    Peter D. Hoffman

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  1. Lindsey L. Thurman
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  2. Tiffany S. Garcia
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  3. Peter D. Hoffman
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Correspondence to Lindsey L. Thurman.

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Communicated by Anssi Laurila.

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Thurman, L.L., Garcia, T.S. & Hoffman, P.D. Elevational differences in trait response to UV-B radiation by long-toed salamander populations. Oecologia 175, 835–845 (2014). https://doi.org/10.1007/s00442-014-2957-z

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