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Effects of urea on behavior and functional traits of Asiatic toad (Bufo gargarizans) tadpoles

  • Tian Zhao
  • Xiaoyi Wang
  • Xungang Wang
  • Sishuo Wang
  • Youhua Chen
  • Jianping Jiang
Article

Abstract

As one of the important contributors of biodiversity, amphibian populations are declining worldwide. Numerous factors are involved in these declines, one of them being the use of fertilizers in agriculture. This is especially true for tadpoles which can live in the fertilizer-polluted farmland water bodies until metamorphosis. The present study aimed to assess the effects of urea (CH4N2O), as one of the most economical and effective fertilizers, on the anti-predator behavior and intraspecific functional trait variability of Asiatic toad (Bufo gargarizans) tadpoles. Based on published literatures and the field observation of urea concentrations in China, glass beakers with a gradient of urea concentrations (0, 200, 400, 600, and 1200 mg/L) were prepared, with 10 tadpoles placed in each glass beaker. Each treatment was replicated three times. Mosquito fish (Gambusia affinis) cues were used as the predator disturbance, and three main functional traits (body mass, trunk bending shape, and eye position) were selected. Our results revealed that tadpoles activity levels decreased when exposed to urea as well as to mosquito fish cues. However, urea exposure did not alter the anti-predator behaviors of tadpoles. Additionally, we found that increasing urea concentrations might modify some functional traits of tadpoles. Importantly, urea disturbance decreased tadpoles intraspecific functional trait variability. (Functional similarity increased between developmental stages.) Given that functional similarity between developmental stages could potentially increase intraspecific competition, urea could indirectly reduce tadpoles survival by decreasing intraspecific traits variability.

Keywords

Fertilizers Mosquito fish cues Activity levels Anti-predator behavior Functional traits Intraspecific trait variability 

Notes

Acknowledgements

We thank Dengwei Yang for his help during the experiments. We also thank Jianwei Guo for editing the English. We are grateful to the two anonymous reviewers for their constructive comments that improve the manuscript. This work is supported by the National Key Programme of Research and Development, Ministry of Science and Technology (2016YFC0503200), the National Natural Science Foundation of China (31700353), the State Key Laboratory of Integrated Management of Pest Insects and Rodents (Y752781603), the West Light Foundation of Chinese Academy of Sciences (2016XBZG_XBQNXZ_B_007), the Important Research Project of Chinese Academy of Sciences (KJZG-EW-L13), a CSC (China Scholarship Council) scholarship to ZT and an Innovative Practice Training Program for College Students of Chinese Academy of Sciences to WXy.

Supplementary material

10452_2018_9669_MOESM1_ESM.docx (46 kb)
Supplementary material 1 (DOCX 46 kb)

References

  1. Akin S, Winemiller KO (2008) Body size and trophic position in a temperate estuarine food web. Acta Oecol 33:144–153.  https://doi.org/10.1016/j.actao.2007.08.002 CrossRefGoogle Scholar
  2. Angelon KA, Petranka JW (2002) Chemicals of predatory mosquitofish (Gambusia affinis) influence selection of oviposition site by Culex mosquitoes. J Chem Ecol 28:797–806CrossRefPubMedGoogle Scholar
  3. Anholt B, Negovetic S, Rauter C, Som C (2005) Predator complement determines the relative success of tadpoles of the Rana esculenta complex. Evol Ecol Res 7:733–741Google Scholar
  4. Azizi E, Landberg T, Wassersug RJ (2007) Vertebral function during tadpole locomotion. Zoology 110:290–297.  https://doi.org/10.1016/j.zool.2007.02.002 CrossRefPubMedGoogle Scholar
  5. Beebee TJC, Griffiths RA (2005) The amphibian decline crisis: a watershed for conservation biology? Biol Conserv 125:271–285.  https://doi.org/10.1016/j.biocon.2005.04.009 CrossRefGoogle Scholar
  6. Burgett A, Wright C, Smith G, Fortune D (2007) Impact of ammonium nitrate on Wood Frog (Rana sylvatic) tadpoles: effects on survivorship and behavior. Herpetol Conserv Biol 2:29–34Google Scholar
  7. Casillas-Barragán I, Costa-Pereira R, Peixoto PEC (2016) Perceived predation risk decreases movement and increases aggregation of Amazon milk frog (Anura, Hylidae) tadpoles throughout ontogeny. Hydrobiologia 765:379–386.  https://doi.org/10.1007/s10750-015-2433-8 CrossRefGoogle Scholar
  8. Choudhury ATMA, Kennedy IR (2005) Nitrogen fertilizer losses from rice soils and control of environmental pollution problems. Commun Soil Sci Plant Anal 36:1625–1639.  https://doi.org/10.1081/CSS-200059104 CrossRefGoogle Scholar
  9. Crane AL, Demuth BS, Ferrari MCO (2017) Experience with predators shapes learning rules in larval amphibians. Behav Ecol 28:312–318.  https://doi.org/10.1093/beheco/arw161 CrossRefGoogle Scholar
  10. Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and if so, is it adaptive? A meta-analysis: invasive species have higher phenotypic plasticity. Ecol Lett 14:419–431.  https://doi.org/10.1111/j.1461-0248.2011.01596.x CrossRefPubMedGoogle Scholar
  11. Dayton GH, Fitzgerald LA (2001) Competition, predation, and the distributions of four desert anurans. Oecologia 129:430–435.  https://doi.org/10.1007/s004420100727 CrossRefPubMedGoogle Scholar
  12. Díaz S, Purvis A, Cornelissen JHC et al (2013) Functional traits, the phylogeny of function, and ecosystem service vulnerability. Ecol Evol 3:2958–2975.  https://doi.org/10.1002/ece3.601 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Edwards TM, McCoy KA, Barbeau T et al (2006) Environmental context determines nitrate toxicity in Southern toad (Bufo terrestris) tadpoles. Aquat Toxicol 78:50–58.  https://doi.org/10.1016/j.aquatox.2006.02.003 CrossRefPubMedGoogle Scholar
  14. Egea-Serrano A, Van Buskirk J (2016) Responses to nitrate pollution, warming and density in common frog tadpoles (Rana temporaria). Amphib-Reptil 37:45–54.  https://doi.org/10.1163/15685381-00003029 CrossRefGoogle Scholar
  15. Ferrari MCO, Chivers DP (2009) Temporal variability, threat sensitivity and conflicting information about the nature of risk: understanding the dynamics of tadpole antipredator behaviour. Anim Behav 78:11–16.  https://doi.org/10.1016/j.anbehav.2009.03.016 CrossRefGoogle Scholar
  16. Gallie JA, Mumme RL, Wissinger SA (2001) Experience has no effect on the development of chemosensory recognition of predators by tadpoles of the American toad, Bufo americanus. Herpetologica 57:376–383Google Scholar
  17. Glibert PM, Harrison J, Heil C, Seitzinger S (2006) Escalating worldwide use of urea: a global change contributing to coastal eutrophication. Biogeochemistry 77:441–463.  https://doi.org/10.1007/s10533-005-3070-5 CrossRefGoogle Scholar
  18. González-Suárez M, Bacher S, Jeschke JM (2015) Intraspecific trait variation is correlated with establishment success of alien mammals. Am Nat 185:737–746.  https://doi.org/10.1086/681105 CrossRefPubMedGoogle Scholar
  19. Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190Google Scholar
  20. Hamer A, Lane S, Mahony M (2002) The role of introduced mosquitofish (Gambusia holbrooki) in excluding the native green and golden bell frog (Litoria aurea) from original habitats in south-eastern Australia. Oecologia 132:445–452.  https://doi.org/10.1007/s00442-002-0968-7 CrossRefPubMedGoogle Scholar
  21. Hamer AJ, Makings JA, Lane SJ, Mahony MJ (2004) Amphibian decline and fertilizers used on agricultural land in south-eastern Australia. Agric Ecosyst Environ 102:299–305.  https://doi.org/10.1016/j.agee.2003.09.027 CrossRefGoogle Scholar
  22. Harris ML, Chora L, Bishop CA, Bogart JP (2000) Species-and age-related differences in susceptibility to pesticide exposure for two amphibians, Rana pipiens, and Bufo americanus. Bull Environ Contam Toxicol 64:263–270.  https://doi.org/10.1007/s001289910039 CrossRefPubMedGoogle Scholar
  23. Ilha P, Schiesari L (2014) Lethal and sublethal effects of inorganic nitrogen on gladiator frog tadpoles (Hypsiboas faber, Hylidae). Copeia 2014:221–230.  https://doi.org/10.1643/OT-13-117 CrossRefGoogle Scholar
  24. IUCN (2016) IUCN red list of threatened species. http://www.iucnredlist.org/initiatives/amphibians
  25. Ji X, Zheng S, Lu Y, Liao Y (2006) Dynamics of floodwater nitrogen and its runoff loss, urea and controlled release nitrogen fertilizer application regulation in rice. Sci Agric Sin 39:2521–2530 (in Chinese with English abstract) Google Scholar
  26. Jones DK, Relyea RA (2015) Here today, gone tomorrow: short-term retention of pesticide-induced tolerance in amphibians: inducible pesticide tolerance in gray treefrogs. Environ Toxicol Chem 34:2295–2301.  https://doi.org/10.1002/etc.3056 CrossRefPubMedGoogle Scholar
  27. Kruuk LEB, Gilchrist JS (1997) Mechanisms maintaining species differentiation: predator-mediated selection in a Bombina hybrid zone. Proc R Soc B Biol Sci 264:105–110.  https://doi.org/10.1098/rspb.1997.0016 CrossRefGoogle Scholar
  28. Laurila A (2000) Behavioural responses to predator chemical cues and local variation in antipredator performance in Rana temporaria tadpoles. Oikos 88:159–168.  https://doi.org/10.1034/j.1600-0706.2000.880118.x CrossRefGoogle Scholar
  29. Lawler SP, Dritz D, Strange T, Holyoak M (1999) Effects of introduced mosquitofish and bullfrogs on the threatened California red-legged frog. Conserv Biol 13:613–622.  https://doi.org/10.1046/j.1523-1739.1999.98075.x CrossRefGoogle Scholar
  30. Lefcort H (1996) Adaptive, chemically mediated fright response in tadpoles of the southern leopard frog, Rana utricularia. Copeia 1996:455–459.  https://doi.org/10.2307/1446864 CrossRefGoogle Scholar
  31. Marco A, Quilchano C, Blaustein AR (1999) Sensitivity to nitrate and nitrite in pond-breeding amphibians from the Pacific Northwest, USA. Environ Toxicol Chem 18:2836–2839.  https://doi.org/10.1002/etc.5620181225 CrossRefGoogle Scholar
  32. Marquis O, Saglio P, Neveu A (2004) Effects of predators and conspecific chemical cues on the swimming activity of Rana temporaria and Bufo bufo tadpoles. Arch Für Hydrobiol 160:153–170.  https://doi.org/10.1127/0003-9136/2004/0160-0153 CrossRefGoogle Scholar
  33. Medina MH, Correa JA, Barata C (2007) Micro-evolution due to pollution: possible consequences for ecosystem responses to toxic stress. Chemosphere 67:2105–2114.  https://doi.org/10.1016/j.chemosphere.2006.12.024 CrossRefPubMedGoogle Scholar
  34. Middlemis Maher J, Werner EE, Denver RJ (2013) Stress hormones mediate predator-induced phenotypic plasticity in amphibian tadpoles. Proc R Soc B Biol Sci 280:20123075–20123075.  https://doi.org/10.1098/rspb.2012.3075 CrossRefGoogle Scholar
  35. Mitchell RM, Bakker JD (2014) Quantifying and comparing intraspecific functional trait variability: a case study with Hypochaeris radicata. Funct Ecol 28:258–269.  https://doi.org/10.1111/1365-2435.12167 CrossRefGoogle Scholar
  36. Nyström P, Hansson J, Månsson J et al (2007) A documented amphibian decline over 40 years: possible causes and implications for species recovery. Biol Conserv 138:399–411.  https://doi.org/10.1016/j.biocon.2007.05.007 CrossRefGoogle Scholar
  37. 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.  https://doi.org/10.1002/etc.523 CrossRefGoogle Scholar
  38. R development Core Team (2011) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
  39. Relyea RA (2001) Morphological and behavioral plasticity of larval anurans in response to different predators. Ecology 82:523–540.  https://doi.org/10.1890/0012-9658(2001)082%5b0523:MABPOL%5d2.0.CO;2 CrossRefGoogle Scholar
  40. Relyea R, Hoverman J (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9:1157–1171.  https://doi.org/10.1111/j.1461-0248.2006.00966.x CrossRefPubMedGoogle Scholar
  41. Richards CL, Bossdorf O, Muth NZ et al (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9:981–993.  https://doi.org/10.1111/j.1461-0248.2006.00950.x CrossRefPubMedGoogle Scholar
  42. Rudolf VHW, Rasmussen NL (2013) Ontogenetic functional diversity: size structure of a keystone predator drives functioning of a complex ecosystem. Ecology 94:1046–1056.  https://doi.org/10.1890/12-0378.1 CrossRefPubMedGoogle Scholar
  43. Rudolf VHW, Van Allen BG (2017) Legacy effects of developmental stages determine the functional role of predators. Nat Ecol Evol 1:0038.  https://doi.org/10.1038/s41559-016-0038 CrossRefGoogle Scholar
  44. Schuytema GS, Nebeker AV (1999) Effects of ammonium nitrate, sodium nitrate, and urea on red-legged frogs, Pacific treefrogs, and African clawed frogs. Bull Environ Contam Toxicol 63:357–364.  https://doi.org/10.1007/s001289900988 CrossRefPubMedGoogle Scholar
  45. Smith GR (2001) Effects of acute exposure to a commercial formulation of glyphosate on the tadpoles of two species of anurans. Bull Environ Contam Toxicol 67:483–488.  https://doi.org/10.1007/s001280149 CrossRefPubMedGoogle Scholar
  46. Smith GR, Temple KG, Dingfelder HA, Vaala DA (2006) Effects of nitrate on the interactions of the tadpoles of two ranids (Rana clamitans and R. catesbeiana). Aquat Ecol 40:125–130.  https://doi.org/10.1007/s10452-005-9015-1 CrossRefGoogle Scholar
  47. Tilman D (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284.  https://doi.org/10.1126/science.1057544 CrossRefPubMedGoogle Scholar
  48. Tong D, Xu R (2012) Effects of urea and (NH4)2SO4 on nitrification and acidification of Ultisols from Southern China. J Environ Sci 24:682–689.  https://doi.org/10.1016/S1001-0742(11)60832-2 CrossRefGoogle Scholar
  49. Trenkel ME (2010) Slow-and controlled-release and stabilized fertilizers: an option for enhancing nutrient use efficiency in agriculture. IFA, International Fertilizer Industry Association, ParisGoogle Scholar
  50. Wang Q, Yang J, Chen J et al (2004) Dynamics of three kinds of nitrogen in surface water of rice field with an independent irrigation system. Chin J Appl Ecol 15:1182–1186 (in Chinese with English abstract) Google Scholar
  51. Wang X, Qiao B, Li S, Li J (2016) Using natural Chinese zeolite to remove ammonium from rainfall runoff following urea fertilization of a paddy rice field. Environ Sci Pollut Res 23:5342–5351.  https://doi.org/10.1007/s11356-015-5743-5 CrossRefGoogle Scholar
  52. White CR, Phillips NF, Seymour RS (2006) The scaling and temperature dependence of vertebrate metabolism. Biol Lett 2:125–127.  https://doi.org/10.1098/rsbl.2005.0378 CrossRefPubMedGoogle Scholar
  53. Winandy L, Denoël M (2013) Cues from introduced fish alter shelter use and feeding behaviour in adult alpine newts. Ethology 119:121–129.  https://doi.org/10.1111/eth.12043 CrossRefGoogle Scholar
  54. 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.  https://doi.org/10.1007/s002449900188 CrossRefPubMedGoogle Scholar
  55. Zhao T, Villéger S, Lek S, Cucherousset J (2014) High intraspecific variability in the functional niche of a predator is associated with ontogenetic shift and individual specialization. Ecol Evol 4:4649–4657.  https://doi.org/10.1002/ece3.1260 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Zhao T, Li C, Wang X et al (2017) Unraveling the relative contribution of inter- and intrapopulation functional variability in wild populations of a tadpole species. Ecol Evol 7:4726–4734.  https://doi.org/10.1002/ece3.3048 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.CAS Key Laboratory of Mountain Ecological Restoration and Bioresource Utilization and Ecological Restoration Biodiversity Conservation Key Laboratory of Sichuan Province, Chengdu Institute of BiologyChinese Academy of SciencesChengduChina
  2. 2.State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of ZoologyChinese Academy of SciencesBeijingChina
  3. 3.F. S Li Marine Science LaboratoryThe Chinese University of Hong KongShatinHong Kong

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