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Responses to nitrate pollution, warming and density in common frog tadpoles (Rana temporaria)

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Amphibians face a variety of anthropogenic environmental perturbations that could act alone or in combination to influence population size. We investigated interactive effects of warming conditions, a moderate pulse of nitrogen pollution, and conspecific density on larvae of the common frog, Rana temporaria. The 16-day experiment had a 2 × 2 × 2 factorial design implemented in 80-l outdoor mesocosms. High density and warm temperature both resulted in reduced activity and visibility; tadpoles grew and developed more quickly at low density and high temperature. The high-nitrogen treatment did not influence behavior, growth, or development rate. We attribute this to several realistic features of our study, including a pulsed treatment application and natural denitrification within the mesocosms. There was only a single interaction among the three factors: higher temperature exacerbated density-dependence in growth rate. These results illustrate that climate warming may benefit temperate amphibians, although the benefits may be counteracted by enhanced larval crowding.

Affiliations: 1: 1Institute of Evolutionary Biology and Environmental Studies, University of Zurich, CH-8057 Zurich, Switzerland

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1. Álvarez D. , Nicieza A.G. (2002): "Effects of temperature and food quality on anuran larval growth and metamorphosis". Funct. Ecol. Vol 16: 640-648.
2. Angilletta M.J. Jr. (2009): Thermal Adaptation. A Theoretical and Empirical Synthesis. Oxford University Press Inc., New York.
3. Baayen R.H. , Davidson D.J. , Bates D.M. (2008): "Mixed effects modeling with crossed random effects for subjects and items". J. Mem. Lang. Vol 59: 390-412.
4. Baker L.F. , Mudge J.F. , Houlahan J.E. , Thompson D.G. , Kidd K.A. (2014): "The direct and indirect effects of a glyphosate-based herbicide and nutrients on Chironomidae (Diptera) emerging from small wetlands". Env. Tox. Chem. Vol 33: 2076-2085.
5. Baker N.J. , Bancroft B.A. , Garcia T.S. (2013): "A meta-analysis of the effects of pesticides and fertilizers on survival and growth of amphibians". Sci. Total Environ. Vol 449: 150-156.
6. Bernardo E. , Henzy A. , Milinichik M. , Morrison L. , Russell T. (2011): "Effects of temperature on feeding rate of larval two-lined salamanders (Eurycea bislineata)". J. Ecol. Res. Vol 13: 39-43.
7. Bernhardt E.S. , Hall R.O. Jr. , Likens G.E. (2002): "Whole-system estimates of nitrification and nitrate uptake in streams of the Hubbard Brook Experimental Forest". Ecosystems Vol 5: 419-430.
8. Berven K.A. (1990): "Factors affecting population fluctuations in larval and adult stages of the wood frog (Rana sylvatica)". Ecology Vol 71: 1599-1608.
9. Boone M.D. , Bridges C.M. (1999): "The effect of the temperature on the potency of carbaryl for survival of tadpoles of the green frog (Rana clamitans)". Environ. Toxicol. Chem. Vol 18: 1482-1484.
10. Boone M.D. , Semlitsch R.D. (2001): "Interactions of an insecticide with larval density and predation in experimental amphibian communities". Conserv. Biol. Vol 15: 228-238.
11. Boone M.D. , Semlitsch R.D. , Little E.E. , Doyle M.C. (2007): "Multiple stressors in amphibian communities: effects of chemical contamination, bullfrogs, and fish". Ecol. Appl. Vol 17: 291-301.[0291:MSIACE]2.0.CO;2
12. Bridges C.M. , Semlitsch R.D. (2000): "Variation in pesticide tolerance of tadpoles among and within species of Ranidae and patterns of amphibian decline". Conserv. Biol. Vol 14: 1490-1499.
13. Camargo J.A. , Alonso A. (2006): "Ecological and toxicological effects of inorganic nitrogen pollution in aquatic ecosystems: a global assessment". Environ. Int. Vol 32: 831-849.
14. Camargo J.A. , Alonso A. , Salamanca A. (2005): "Nitrate toxicity to aquatic animals: a review with new data for freshwater invertebrates". Chemosphere Vol 58: 1255-1267.
15. Carey C. , Alexander M.A. (2003): "Climate change and amphibian declines: is there a link?" Divers. Distrib. Vol 9: 111-121.
16. Castano B. , Miely S. , Smith G.R. , Rettig J.E. (2010): "Interactive effects of food availability and temperature on wood frogs (Rana sylvatica) tadpoles". Herpetol. J. Vol 20: 209-211.
17. DeNicola D.M. (1996): "Periphyton responses to temperature at different ecological levels". In: Algal Ecology: Freshwater Benthic Ecosystems, p.  150-183. Stevenson R.J. , Bothwell M.L. , Lowe R.L. , Eds, Academic Press, San Diego, California, USA.
18. Denöel M. , D’Hooghe B. , Ficetola G.F. , Brasseur C. , De Puaw E. , Thomé J.P. , Kestemont P. (2012): "Using sets of behavioral biomarkers to assess short-term effects of pesticide: a study case with endosulfan on frog tadpoles". Ecotoxicology Vol 21: 1240-1250.
19. Deutsch C.A. , Tewksbury J.J. , Huey R.B. , Sheldon K.S. , Ghalambor C.K. , Haak D.C. , Martin P.R. (2008): "Impacts of climate warming on terrestrial ectotherms across latitude". P. Natl. Acad. Sci. Vol 105: 6668-6672.
20. Distel C.A. , Boone M.D. (2009): "Effects of aquatic exposure to the insecticide carbaryl and density on aquatic and terrestrial growth and survival in American toads". Environ. Toxicol. Chem. Vol 28: 1963-1969.
21. Distel C.A. , Boone M.D. (2010): "Effects of aquatic exposure to the insecticide carbaryl are species-specific across life-stages and mediated by heterospecific competitors in anurans". Funct. Ecol. Vol 24: 1342-1352.
22. Duarte H. , Tejedo M. , Katzenberger M. , Marangoni F. , Baldo D. , Beltrán J.F. , Martí D.A. , Richter-Boix A. , González-Voyer A. (2012): "Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities". Global Change Biol. Vol 18: 412-421.
23. Edge C. , Thompson D. , Hao C. , Houlahan J. (2014): "The response of amphibian larvae to exposure to a glyphosate-based herbicide (Roundup WeatherMax) and nutrient enrichment in an ecosystem experiment". Ecotox. Env. Safety Vol 109: 124-132.
24. Egea-Serrano A. , Tejedo M. (2014): "Contrasting effects of nitrogenous pollution on fitness and swimming performance of Iberian waterfrog, Pelophylax perezi (Seoane, 1885), larvae in mesocosms and field enclosures". Aquat. Toxicol. Vol 146: 144-153.
25. Egea-Serrano A. , Tejedo M. , Torralva M. (2009): "Populational divergence in the impact of three nitrogenous compounds and their combination on larvae of the frog Pelophylax perezi (Seoane, 1885)". Chemosphere Vol 76: 869-877.
26. Egea-Serrano A. , Tejedo M. , Torralva M. (2011): "Behavioral responses of the Iberian waterfrog, Pelophylax perezi (Seoane, 1885), to three nitrogenous compounds in laboratory conditions". Ecotoxicology Vol 20: 1246-1257.
27. Egea-Serrano A. , Relyea R. , Tejedo M. , Torralva M. (2012): "Understanding of the impact of chemicals on amphibians. A meta-analytic review". Ecol. Evol. Vol 2: 1382-1397.
28. Fernández-Aláez M. , Fernández-Aláez C. (2010): "Effects of the intense summer desiccation and the autumn filling on the water chemistry in some Mediterranean ponds". Limnetica Vol 29: 59-74.
29. Fertiliser Manufacturer’s Association, Ministry of Agriculture, Fisheries and Food, Scottish Office of Agriculture and Fisheries Department (1993): The British Survey of Fertiliser Practice: Fertiliser Use on Farm Crops 1992. HMSO, London, UK.
30. Galloy V. , Denöel M. (2010): "Detrimental effects of temperature increase on the fitness of an amphibian (Lissotriton helveticus)". Acta Oecologica Vol 36: 179-183.
31. Ghalambor C.K. , McKay J.K. , Carroll S.P. , Reznick D.N. (2007): "Adaptive versus non adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments". Funct. Ecol. Vol 21: 394-407.
32. Goldman J.C. , Carpenter E.J. (1974): "A kinetic approach to the effect of temperature on algal growth". Limnol. Oceanogr. Vol 19: 756-766.
33. Gosner K.L. (1960): "A simplified table for staging anuran embryos and larvae with notes on identification". Herpetologica Vol 16: 183-190.
34. Govindirajulu P.P. , Anholt B.R. (2006): "Interaction between biotic and abiotic factors determines tadpole survival rate under natural conditions". Ecoscience Vol 13: 413-421.
35. Griffis-Kyle K.L. , Ritchie M.E. (2007): "Amphibian survival, growth and development in response to mineral nitrogen exposure and predator cues in the field: an experimental approach". Oecologia Vol 152: 633-642.
36. Hatch A.C. , Blaustein A.R. (2003): "Combined effects of UV-V radiation and nitrate fertilizer on larval amphibians". Ecol. Appl. Vol 13: 1083-1093.[1083:CEOURA]2.0.CO;2
37. Hoffman A.A. , Parsons P.A. (1991): Evolutionary Genetics and Environmental Stress. Oxford Scientific, Oxford.
38. Johansson M. , Räsänen K. , Merilä J. (2001): "Comparison of nitrate tolerance between different populations of the common frog, Rana temporaria ". Aquat. Toxicol. Vol 54: 1-14.
39. Karraker N.E. , Gibbs J.P. , Vonesh J.R. (2008): "Impact of road deicing salt on the demography of vernal pool-breeding amphibians". Ecol. Appl. Vol 18: 724-734.
40. Kemp M.J. , Dodds W.K. (2002): "The influence of ammonium, nitrate, and dissolved oxgen concentrations on uptake, nitrification and denitrification rates associated with prairie stream substrata". Limnol. Oceanogr. Vol 47: 1380-1393.
41. Lanctot C. , Robertson C. , Navarro-Martin L. , Edge C. , Melvin S.D. , Houlahan J. , Trudeau V.L. (2013): "Effects of the glyphosate-based herbicide Roundup WeatherMax on metamorphosis of wood frogs (Lithobates sylvaticus) in natural wetlands". Aquat. Toxicol. Vol 140-141: 48-57.
42. Laugen A.T. , Laurila A. , Rasanen K. , Merila J. (2003): "Latitudinal countergradient variation in the common frog (Rana temporaria) development rates: evidence for local adaptation". J. Evol. Biol. Vol 16: 996-1005.
43. Lindgren B. , Laurila A. (2005): "Proximate causes of adaptive growth rates: growth efficiency variation among latitudinal populations of Rana temporaria ". J. Evol. Biol. Vol 18: 820-828.
44. Mann R.M. , Hyne R.V. , Choung C.B. , Wilson S.P. (2009): "Amphibians and agricultural chemicals: review of the risks in a complex environment". Env. Poll. Vol 157: 2903-2927.
45. Marco A. , Blaustein A.R. (1999): "The effect of nitrite on behavior and metamorphosis in Cascades frogs (Rana cascadae)". Environ. Toxicol. Chem. Vol 18: 946-949.
46. Marco A. , Ortiz-Santaliestra M.E. (2009): "Impact of reactive nitrogen on amphibians". In: Amphibian Decline: Diseases, Parasites, Maladies and Pollution, Amphibian Biology, Vol. 8, p.  3145-3185. Heatwole H. , Wilkinson J.W. , Eds, Surrey Beatty & Sons, Baulkham Hills, New South Wales, Australia.
47. Massal L.R. , Snodgrass J.W. , Casey R.E. (2007): "Nitrogen pollution of stormwater ponds: potential for toxic effects on amphibian embryos and larvae". Appl. Herpetol. Vol 4: 19-29.
48. Meehl G.A. , Stocker T.F. , Collins W.D. , Friedlingstein P. , Gaye A.T. , Gregory J.M. , Kitoh A. , Knutti R. , Murphy J.M. , Noda A. , Raper S.C.B. , Watterson I.G. , Weaver A.J. , Zhao Z.-C. (2007): "Global climate projections". In: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, p.  747-845. Solomon S. , Qin D. , Manning M. , Chen Z. , Marquis M. , Averyt K.B. , Tignor M. , Miller H.L. , Eds, Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA.
49. Merchán D. , Otero N. , Soler A. , Caupasé J. (2014): "Main sources and processes affecting dissolved sulphates and nitrates in a small irrigated basin (Lerma basin, Zaragoza, Spain): isotopic characterization". Agri. Ecosyst. Environ. Vol 195: 127-138.
50. Mills N.E. , Semlitsch R.D. (2004): "Competition and predation mediate the indirect effects of an insecticide on southern leopard frogs". Ecol. Appl. Vol 14: 1041-1054.
51. Newman R.A. (1998): "Ecological constraints on amphibian metamorphosis: interactions of temperature and larval density with responses to changing food level". Oecologia Vol 115: 9-16.
52. O’Regan S.M. , Palen W.J. , Anderson S.C. (2014): "Climate warming mediates negative impacts of rapid pond drying for three amphibian species". Ecology Vol 95: 845-855.
53. Orizaola G. , Laurila A. (2009): "Microgeographic variation in temperature-induced plasticity in an isolated amphibian metapopulation". Evol. Ecol. Vol 23: 979-991.
54. Oromi N. , Sanuy D. , Vilches M. (2009): "Effects of nitrate and ammonium on larvae of Rana temporaria from the Pyrenees". Bull. Env. Cont. Tox. Vol 82: 534-537.
55. Ortiz-Santaliestra M.E. , Marco A. , Fernandez M.J. , Lizana M. (2006): "Influence of developmental stage on sensitivity to ammonium nitrate of aquatic stages of amphibians". Env. Tox. Chem. Vol 25: 105-111.
56. Ortiz-Santaliestra M.E. , Fernández-Benéitez M.J. , Lizana M. , Marco A. (2010): "Adaptation to osmotic stress provides protection against ammonium nitrate in Pelophylax perezi embryos". Environ. Pollut. Vol 158: 934-940.
57. Ortiz-Santaliestra M.E. , Fernández-Benéitez M.J. , Marco A. (2012): "Density effects on ammonium nitrate toxicity on amphibians. Survival, growth and cannibalism". Aquat. Toxicol. Vol 110-111: 170-176.
58. Peltzer P.M. , Lajmanovich R.C. , Attademo A.M. , Beltzer A.H. (2006): "Diversity of anurans across agricultural ponds in Argentina". Biodivers. Conserv. Vol 15: 3499-3513.
59. Sahuquillo M. , Miracle M.E. , Morata S.M. , Vicente E. (2012): "Nutrient dynamics in water and sediment of Mediterranean ponds across a wide hydroperiod gradient". Limnologica Vol 42: 282-292.
60. Sanuy D. , Oromí N. , Galofré A. (2008): "Effects of temperature on embryonic and larval development and growth in the natterjack toad (Bufo calamita) in a semi-arid zone". Anim. Biod. Cons. Vol 31: 41-46.
61. Secondi J. , Hinot E. , Djalout Z. , Sourice S. , Jadas-Hécart A. (2009): "Realistic nitrate concentration alters the expression of sexual traits and olfactory male attractiveness in newts". Funct. Ecol. Vol 23: 800-808.
62. Smith D.C. (1987): "Adult recruitment in chorus frogs: effects of size and date at metamorphosis". Ecology Vol 68: 344-350.
63. Smith D.C. , Van Buskirk J. (1995): "Phenotypic design, plasticity, and ecological performance in two tadpole species". Am. Nat. Vol 145: 211-233.
64. Smith R.L. , Böhlke J.K. , Repert D.A. , Hart C.P. (2009): "Nitrification and denitrification in a midwestern stream containing high nitrate: in situ assessment using tracers in domed-shape incubation chambers". Biogeochemistry Vol 96: 189-208.
65. Sparling D.W. , Linder G. , Bishop C.A. , Krest S.K. (2010): Ecotoxicology of Amphibians and Reptiles, 2nd Edition. CRC Press, Taylor & Francis Group, Boca Ratón, FL.
66. Steinwascher K. (1978): "Interference and exploitation competition among tadpoles of Rana utricularia ". Ecology Vol 59: 1039-1046.
67. Stoks R. , Swillen I. , De Block M. (2012): "Behaviour and physiology shape the growth accelerations associated with predation risk, high temperatures and southern latitudes in Ischnura damselfly larvae". J. Anim. Ecol. Vol 81: 1034-1040.
68. Tan C.O. (2002): The roles of hydrology and nutrients in alternative equilibrium of two shallow lakes of Anatolia. Lake Eymir and Lake Mogan: using monitoring and modelling approaches. M.Sc. Thesis, Middle East Technical University, Ankara, Turkey.
69. Tejedo M. , Reques R. (1994): "Plasticity in metamorphic traits of natterjack tadpoles: the interactive effect of density and pond duration". Oikos Vol 71: 295-304.
70. Thomas M.K. , Kremer C.T. , Klausmeier C.A. , Litchman E. (2012): "A global pattern of thermal adaptation in marine phytoplankton". Science Vol 338: 1085-1088.
71. Van Buskirk J. (2005): "Local and landscape influence on amphibian occurrence and abundance". Ecology Vol 86: 1936-1947.
72. Van Buskirk J. , Yurewicz K.L. (1998): "Effects of predators on prey growth rate: relative contributions of thinning and reduced activity". Oikos Vol 82: 20-28.
73. Warkentin K.M. (1992): "Effects of temperature and illumination on feeding rates of green frog tadpoles (Rana clamitans)". Copeia Vol 1992: 725-730.
74. Wexler S.K. , Hiscock K.M. , Dennis P.F. (2012): "Microbial and hydrological influences on nitrate isotopic composition in an agricultural lowland catchment". J. Hydrol. Vol 468-469: 85-93.
75. Wilbur H.M. (1977a): "Interactions of food level and population density in Rana sylvatica ". Ecology Vol 58: 206-209.
76. Wilbur H.M. (1977b): "Density-dependent aspects of growth and metamorphosis in Bufo americanus ". Ecology Vol 58: 196-200.
77. Winkler J.D. , Forte G. (2011): "The effects of road salt on larval life history traits and behavior in Rana temporaria ". Amphibia-Reptilia Vol 32: 527-532.

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