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Influence of Dissolved Oxygen Conditions on Toxicity of Ammonium Nitrate to Larval Natterjack Toads

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Abstract

Temporary ponds, where many amphibians from temperate regions breed, show an annual cycle with a maximum water volume in spring followed by a progressive desiccation throughout late spring and summer. This desiccation leads to a decrease in dissolved oxygen and an increase in nitrogen levels, which can additionally increase because of anthropogenic sources such as chemical fertilizers. We analyzed the toxicity posed by environmentally relevant levels of a common nitrogenous fertilizer, ammonium nitrate, at different conditions of oxygen availability to Bufo calamita tadpoles, which typically develop in ephemeral ponds. Ammonium nitrate (90.3 mg N–NO3NH4/l) and hypoxic conditions (initial dissolved oxygen 4.53 ± 0.40 mg/l) caused significant lethal effects after 7 and 12 days of exposure, respectively. At the end of experiment (16 days), mortality rates were 32.5 % in individuals exposed to the fertilizer and 15 % in those growing under hypoxic conditions. When both stressors were combined, they showed an additive effect on tadpole survival. Malformations, such as oedemas and spinal curvatures, and locomotory abnormalities, were detected after 12 days of experiment in >90 % of individuals exposed to 45.2 mg N–NO3NH4/l under hypoxic conditions, whereas none of these stressors by separate related to abnormality rates >35 %. Delayed development was also observed in tadpoles exposed to ammonium nitrate with hypoxia affecting developmental rate only after 12 days of exposure. The results are discussed in terms of potential mechanisms linking negative effects of both factors as well as in terms of potential alterations of the ecological plasticity that often allows amphibians to survive in unpredictable environments.

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References

  • Allan GL, Maguire GB, Hopkins SJ (1990) Acute and chronic toxicity of ammonia to juvenile Metapenaeus macleayi and Penaeus monodon and the influence of low dissolved-oxygen levels. Bull Environ Contam Toxicol 92:277–288

    Google Scholar 

  • Allran JW, Karasov WH (2001) Effects of atrazine on embryos, larvae, and adults of anuran amphibians. Environ Toxicol Chem 20:769–775

    Article  CAS  Google Scholar 

  • Baker NJ, Bancroft BA, Garcia TS (2013) A meta-analysis of the effects of pesticides and fertilizers on survival and growth of amphibians. Sci Total Environ 449:150–156

    Article  CAS  Google Scholar 

  • Beebee TJC (1983) The natterjack toad. Oxford University Press, Oxford

    Google Scholar 

  • Blaustein AR, Wildy EL, Belden LK, Hatch A (2001) Influence of abiotic and biotic factors on amphibians in ephemeral ponds with special reference to long-toed salamanders (Ambystoma macrodactylum). Isr J Zool 47:333–345

    Article  Google Scholar 

  • Boutilier RG, Stiffler DF, Toews DP (1992) Exchange of respiratory gases, ions, and water in amphibious and aquatic amphibians. In: Feder ME, Burggren WW (eds) Environmental physiology of amphibians. University of Chicago Press, Chicago, pp 81–124

    Google Scholar 

  • Branch LC, Taylor DH (1977) Physiological and behavioral responses of larval spotted salamanders (Ambystoma maculatum) to various concentrations of oxygen. Comp Biochem Physiol A 58:269–274

    Article  Google Scholar 

  • Burgett AA, Wright CD, Smith GR, Fortune DT, Johnson SL (2007) Impact of ammonium nitrate on wood frog (Rana sylvatica) tadpoles: effects on survivorship and behavior. Herpetol Conserv Biol 2:29–34

    Google Scholar 

  • de Wijer P, Watt PJ, Oldham RS (2003) Amphibian decline and aquatic pollution: effects of nitrogenous fertiliser on survival and development of larvae of the frog Rana temporaria. Appl Herpetol 1:3–12

    Article  Google Scholar 

  • Dejours P, Armand J, Beekenkamp H (1989) Action de la pression partielle d’oxygene sur la toxicite de l’ammoniac chez deux amphibiens, Xenopus laevis et Pleurodeles waltl. C R Seances Acad Sci III 309:191–196

    CAS  Google Scholar 

  • Duellman WE, Trueb L (1994) Biology of amphibians. John Hopkins University Press, Baltimore

    Google Scholar 

  • 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 20:1246–1257

    Article  CAS  Google Scholar 

  • Feder ME (1981) Effect of body size, trophic state, time of day, and experimental stress on oxygen-consumption of anuran larvae: an experimental assessment and evaluation of the literature. Comp Biochem Physiol A 70:497–508

    Article  Google Scholar 

  • Feder ME (1982) Effect of developmental stage and body size on oxygen consumption of anuran larvae: a reappraisal. J Exp Zool 220:33–42

    Article  Google Scholar 

  • Feder ME (1983) Responses to acute hypoxia in larvae of the frog Rana berlandieri. J Exp Biol 104:79–95

    Google Scholar 

  • 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 29:59–73

    Google Scholar 

  • Gomez-Mestre I (2014) Sapo corredor—Epidalea calamita. In: Salvador A, Martínez-Solano I (eds) Enciclopedia virtual de los vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid. Available at: http://www.vertebradosibericos.org. Accessed 11 Dec 2014

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Griffis-Kyle KL, Ritchie ME (2007) Amphibian survival, growth and development in response to mineral nitrogen exposure and predator cues in the field: an experimental approach. Oecologia 152:633–642

    Article  Google Scholar 

  • Hecnar SJ (1995) Acute and chronic toxicity of ammonium-nitrate fertilizer to amphibians from southern Ontario. Environ Toxicol Chem 14:2131–2137

    Article  CAS  Google Scholar 

  • Hochachka PW, Lutz PL (2001) Mechanism, origin, and evolution of anoxia tolerance in animals. Comp Biochem Physiol B 130:435–459

    Article  CAS  Google Scholar 

  • Huey DW, Beitinger TL (1980a) Hematological responses of larval Rana catesbiana to sublethal nitrite exposures. Bull Environ Contam Toxicol 25:574–577

    Article  CAS  Google Scholar 

  • Huey DW, Beitinger TL (1980b) Toxicity of nitrite to larvae of the salamander Ambystoma texanum. Bull Environ Contam Toxicol 25:909–912

    Article  CAS  Google Scholar 

  • Jofre MB, Karasov WH (1999) Direct effect of ammonia on three species of North American anuran amphibians. Environ Toxicol Chem 18:1806–1812

    Article  CAS  Google Scholar 

  • Jofré MB, Rosenshield ML, Karasov WH (2000) Effects of PCB 126 and ammonia, alone and in combination, on green frog (Rana clamitans) and leopard frog (R. pipiens) hatching success, development, and metamorphosis. J Iowa Acad Sci 107:113–122

    Google Scholar 

  • Johnson CJ, Bonrud PA, Dosch TL, Kilness AW, Senger KA, Busch DC et al (1987) Fatal outcome of methemoglobinemia in an infant. J Am Med Assoc 257:2796–2797

    Article  CAS  Google Scholar 

  • Krishnamurthy SV, Smith GR (2010) Growth, abnormalities, and mortality of tadpoles of American toad exposed to combinations of malathion and nitrate. Environ Toxicol Chem 29:2777–2782

    Article  CAS  Google Scholar 

  • Krishnamurthy SV, Smith GR (2011) Combined effects of malathion and nitrate on early growth, abnormalities, and mortality of wood frog (Rana sylvatica) tadpoles. Ecotoxicology 20:1361–1367

    Article  CAS  Google Scholar 

  • Kross BC, Ayebo AD, Fuortes LJ (1992) Methemoglobinemia: nitrate toxicity in rural America. Am Fam Phys 46:183–188

    CAS  Google Scholar 

  • Lajmanovich RC, Izaguirre MF, Casco VH (1998) Paraquat tolerance and alteration of internal gill structure of Scinax nasica tadpoles (Anura: Hylidae). Arch Environ Contam Toxicol 34:364–369

    Article  CAS  Google Scholar 

  • Marco A, Blaustein AR (1999) The effects of nitrite on behavior and metamorphosis in cascades frogs (Rana cascadae). Environ Toxicol Chem 18:946–949

    Article  CAS  Google Scholar 

  • Marco A, Ortiz-Santaliestra ME (2009) Pollution: impact of reactive nitrogen on amphibians (nitrogen pollution). In: Heatwole H, Wilkinson JW (eds) Amphibian biology, vol 8., Amphibian decline: diseases, parasites, maladies and pollutionSurrey Beattie & Sons, Baulkham Hills, pp 3145–3185

    Google Scholar 

  • Mead R (1988) The design of experiments. Cambridge University Press, Cambridge

    Google Scholar 

  • Oldham RS, Latham DM, Hilton-Brown D, Towns M, Cooke AS, Burn A (1997) The effect of ammonium nitrate fertiliser on frog (Rana temporaria) survival. Agric Ecosyst Environ 61:69–74

    Article  CAS  Google Scholar 

  • Ortiz ME, Marco A, Saiz N, Lizana M (2004) Impact of ammonium nitrate on growth and survival of six European amphibians. Arch Environ Contam Toxicol 47:234–239

    Article  CAS  Google Scholar 

  • Ortiz-Santaliestra ME, Marco A, Fernández MJ, Lizana M (2006) Influence of developmental stage on sensitivity to ammonium nitrate of aquatic stages of amphibians. Environ Toxicol Chem 25:105–111

    Article  CAS  Google Scholar 

  • Ortiz-Santaliestra ME, Fernández-Benéitez MJ, Lizana M, Marco A (2010) Adaptation to osmotic stress provides protection against ammonium nitrate in Pelophylax perezi embryos. Environ Pollut 158:934–940

    Article  CAS  Google Scholar 

  • Ortiz-Santaliestra ME, Fernández-Benéitez MJ, Lizana M, Marco A (2011) Responses of toad tadpoles to ammonium nitrate fertilizer and predatory stress: differences between populations on a local scale. Environ Toxicol Chem 30:1440–1446

    Article  CAS  Google Scholar 

  • Ortiz-Santaliestra ME, Fernández-Benéitez MJ, Marco A (2012) Density effects on ammonium nitrate toxicity on amphibians. Survival, growth and cannibalism. Aquat Toxicol 110–111:170–176

    Article  Google Scholar 

  • Rice TM, Blackstone BJ, Nixdorf WL, Taylor DH (1999) Exposure to lead induces hypoxia-like responses in bullfrog larvae (Rana catesbeiana). Environ Toxicol Chem 18:2283–2288

    Article  CAS  Google Scholar 

  • Smith GR, Dibble CJ, Terlecky AJ, Dayer CB, Burner AB, Ogle ME (2013) Effects of invasive Western mosquitofish and ammonium nitrate on green frog tadpoles. Copeia 2013:248–253

    Article  Google Scholar 

  • Tejedo M, Reques R (1994) Plasticity in metamorphic traits of natterjack tadpoles: the interactive effects of density and pond duration. Oikos 71:295–304

    Article  Google Scholar 

  • Ultsch GR, Bradford DF, Freda J (1999) Physiology. Coping with the environment. In: McDiarmid RW, Altig R (eds) Tadpoles. The biology of anuran larvae. The University of Chicago Press, Chicago, pp 189–214

  • Ultsch GR, Reese SA, Stewart ER (2004) Physiology of hibernation in Rana pipiens: metabolic rate, critical oxygen tension, and the effects of hypoxia on several plasma variables. J Exp Zool A Ecol Genet Physiol 301:169–176

    Google Scholar 

  • UNIDO-IFDC (United Nations Industrial Development Organization-International Fertilizer Development Center) (1998) Fertilizer manual. Kluwer Academic, Dordrecht

    Google Scholar 

  • United States Environmental Protection Agency (1986) Quality criteria for water. Report EPA 440/5-86-001. USEPA, Washington

  • Vitousek PM, Aber J, Howarth RW, Likens GE, Matson PA, Schindler DW et al (1997) Human alteration of the global nitrogen cycle: causes and consequences. Iss Ecol 1:1–16

    Google Scholar 

  • Wassersug RJ, Seibert EA (1975) Behavioral responses of amphibian larvae to variation in dissolved-oxygen. Copeia 1975:87–103

    Article  Google Scholar 

  • Werner EE, Glennemeier KS (1999) Influence of forest canopy cover on the breeding pond distributions of several amphibian species. Copeia 1999:1–12

    Article  Google Scholar 

  • West NH, Burggren WW (1982) Gill and lung ventilatory responses to steady-state aquatic hypoxia and hyperoxia in the bullfrog tadpole. Respir Physiol 47:165–176

    Article  CAS  Google Scholar 

  • Xu Q, Oldham RS (1997) Lethal and sublethal effects of nitrogen fertilizer ammonium nitrate on common toad (Bufo bufo) tadpoles. Arch Environ Contam Toxicol 32:298–303

    Article  CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. Institute for Environmental Sciences, University of Koblenz-Landau, Fortstrasse 7, 76829, Landau, Germany

    Manuel E. Ortiz-Santaliestra

  2. Estación Biológica de Doñana (CSIC), Av. Américo Vespucio s/n, 41092, Sevilla, Spain

    Adolfo Marco

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  1. Manuel E. Ortiz-Santaliestra
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  2. Adolfo Marco
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Correspondence to Manuel E. Ortiz-Santaliestra.

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Ortiz-Santaliestra, M.E., Marco, A. Influence of Dissolved Oxygen Conditions on Toxicity of Ammonium Nitrate to Larval Natterjack Toads. Arch Environ Contam Toxicol 69, 95–103 (2015). https://doi.org/10.1007/s00244-014-0126-3

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  • DOI: https://doi.org/10.1007/s00244-014-0126-3

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