pp 1–19 | Cite as

Isotopic Evidence that Nitrogen Enrichment Intensifies Nitrogen Losses to the Atmosphere from Subtropical Mangroves

  • Carla R. G. ReisEmail author
  • Sasha C. Reed
  • Rafael S. Oliveira
  • Gabriela B. Nardoto


Nitrogen (N) enrichment can have large effects on mangroves’ capacity to provide critical ecosystem services by affecting fundamental functions such as N cycling and primary productivity. However, our understanding of excess N input effects on N cycling in mangroves remains quite limited. To advance our understanding of how N enrichment via water or air pollution affects mangroves, we evaluated whether increasing N inputs would decrease biological N fixation (BNF), but intensify N dynamics and N losses to the atmosphere in these systems. We measured N concentrations in sediment and vegetation, rates of BNF in sediment and litter, and net sediment ammonification and nitrification rates. We also evaluated long-term integrated N dynamics and N losses to the atmosphere using the natural abundance of N stable isotopes (δ15N) in the sediment–plant system and in estuarine water. We performed these analyses at non-N-enriched and N-enriched (that is, polluted) fringe and basin mangroves in southeastern Brazil. The δ15N in the sediment–plant system was higher at N-enriched than non-N-enriched fringe sites, indicating increased N losses to the atmosphere from N-enriched sites. However, N concentrations in sediment and vegetation were similar or lower at N-enriched relative to non-N-enriched sites. BNF and net ammonification and nitrification rates were also similar between N-enriched and non-N-enriched sites. Excess N inputs intensified N losses to the atmosphere from mangroves, but N pools, BNF, and net ammonification and nitrification rates were not affected by N enrichment, likely because excess N was quickly lost from the system by direct denitrification and volatilization.


biological nitrogen fixation denitrification nitrification nitrous oxide phosphorous stable isotopes 



CRGR was supported by the Rufford Foundation (Ref. 20243-1), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (Processes 1422671 and 88881.132767/2016-01), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (Process 141069/2016-3), and Idea Wild. SCR was supported by the US Geological Survey. We would like to thank the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio—Brazil) and the Instituto Florestal (Secretaria do Meio Ambiente, São Paulo, Brazil) for the permission to conduct this research in the Cananeia-Iguape-Peruibe Protection Area (Process 47365) and Cardoso Island State Park (Process 260108-012.547/2014), respectively. The authors are also thankful to Pedro Eisenlohr for providing statistical assistance, to Marília Cunha-Lignon for providing the shapefiles of mangrove forests area, and to João Souza for providing the map of the study area. We also thank Ariel Lugo, Maga Gei, and anonymous reviewers whose suggestions significantly improved the manuscript. The authors declare that they have no conflict of interest. Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the US Government.

Supplementary material

10021_2018_327_MOESM1_ESM.doc (59 kb)
Supplementary material 1 (DOC 59 kb)


  1. Adame MF, Fry B, Gamboa JN, Herrera-Silveira JA. 2015. Nutrient subsidies delivered by seabirds to mangrove islands. Mar Ecol Prog Ser 525:15–24.CrossRefGoogle Scholar
  2. Allen DE, Dalal RC, Rennenberg H, Meyer RL, Reeves S, Schmidt S. 2007. Spatial and temporal variation of nitrous oxide and methane flux between subtropical mangrove sediments and the atmosphere. Soil Biol Biochem 39:622–31.CrossRefGoogle Scholar
  3. Alongi DM. 2014. Carbon cycling and storage in mangrove forests. Ann Rev Mar Sci 6:195–219.
  4. Alongi DM, Christoffersen P, Tirendi F. 1993. The influence of forest type on microbial-nutrient relationships in tropical mangrove sediments. J Exp Mar Bio Ecol 171:201–23.CrossRefGoogle Scholar
  5. Alongi DM, Pfitzner J, Trott LA, Tirendi F, Dixon P, Klumpp DW. 2005. Rapid sediment accumulation and microbial mineralization in forests of the mangrove Kandelia candel in the Jiulongjiang Estuary, China. Estuar Coast Shelf Sci 63:605–18.CrossRefGoogle Scholar
  6. Alongi DM, Trott LA, Wattayakorn G, Clough BF. 2002. Below-ground nitrogen cycling in relation to net canopy production in mangrove forests of southern Thailand. Mar Biol 140:855–64.CrossRefGoogle Scholar
  7. Alvares CA, Stape JL, Sentelhas PC, De Moraes Gonçalves JL, Sparovek G. 2013. Köppen’s climate classification map for Brazil. Meteorol Zeitschrift 22:711–28.CrossRefGoogle Scholar
  8. Angiosperm Phylogeny Group III. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–21.CrossRefGoogle Scholar
  9. Bouyoucos GJ. 1932. Studies on the dispersion procedure used in the hydrometer method for making mechanical analysis of soil. Soil Sci 33:21–6.CrossRefGoogle Scholar
  10. Chen GC, Tam NFY, Ye Y. 2010. Summer fluxes of atmospheric greenhouse gases N2O, CH4 and CO2 from mangrove soil in South China. Sci Total Environ 408:2761–7. Scholar
  11. Compton JE, Harrison JA, Dennis RL, Greaver TL, Hill BH, Jordan SJ, Walker H, Campbell HV. 2011. Ecosystem services altered by human changes in the nitrogen cycle: A new perspective for US decision making. Ecol Lett 14:804–15.CrossRefGoogle Scholar
  12. Coplen TB, Qi H, Revesz K, Casciotti KL, Hannon JE. 2012. Determination of the δ15 N of nitrate in water; RSIL Lab Code 2899. In: Révész K, Coplen TB, editors. Methods of the Reston Stable Isotope Laboratory (slightly revised from 1.0 released in 2007): U.S. Geological Survey Techniques and Methods. p 35.Google Scholar
  13. Corredor JE, Morell JM, Bauza J. 1999. Atmospheric nitrous oxide fluxes from mangrove sediments. Mar Pollut Bull 38:473–8.CrossRefGoogle Scholar
  14. Costanzo SD, O’Donohue MJ, Dennison WC. 2003. Assessing the seasonal influence of sewage and agricultural nutrient inputs in a subtropical river estuary. Estuaries 26:857–65.CrossRefGoogle Scholar
  15. Costanzo SD, O’Donohue MJ, Dennison WC. 2004. Assessing the influence and distribution of shrimp pond effluent in a tidal mangrove creek in north-east Australia. Mar Pollut Bull 48:514–25.CrossRefGoogle Scholar
  16. Costanzo SD, O’Donohue MJ, Dennison WC, Loneragan NR, Thomas M. 2001. A new approach for detecting and mapping sewage impacts. Mar Pollut Bull 42:149–56.CrossRefGoogle Scholar
  17. Craine JM, Brookshire ENJ, Cramer MD, Hasselquist NJ, Koba K, Marin-Spiotta E, Wang L. 2015a. Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant Soil 396:1–26. Scholar
  18. Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TE, Hobbie EA, Kahmen A, MacK MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Peñuelas J, Reich PB, Schuur EAG, Stock WD, Templer PH, Virginia RA, Welker JM, Wright IJ. 2009. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol 183:980–92.CrossRefGoogle Scholar
  19. Craine JM, Elmore AJ, Wang L, Augusto L, Baisden WT, Brookshire ENJ, Cramer MD, Hasselquist NJ, Hobbie EA, Kahmen A, Koba K, Kranabetter JM, Mack MC, Marin-Spiotta E, Mayor JR, McLauchlan KK, Michelsen A, Nardoto GB, Oliveira RS, Perakis SS, Peri PL, Quesada CA, Richter A, Schipper LA, Stevenson BA, Turner BL, Viani RAG, Wanek W, Zeller B. 2015b. Convergence of soil nitrogen isotopes across global climate gradients. Sci Rep 5:1–8.Google Scholar
  20. Cunha-Lignon M, Almeida R, Lima NGB, Galvani E, Menghini RP, Coelho Jr. C, Schaeffer-Novelli Y. 2015. Monitoramento de manguezais: Abordagem integrada frente às alterações ambientais. In: Anais do VIII Congresso Brasileiro de Unidades de Conservação - trabalhos técnicos. pp 1–17.Google Scholar
  21. Cunha-Lignon M, Kampel M, Menghini RP, Novelli YS, Cintrón G, Guebas FD. 2011. Mangrove forests submitted to depositional processes and salinity variation investigated using satellite images and vegetation structure surveys. J Coast Res 1:344–8.Google Scholar
  22. Donato DC, Kauffman JB, Murdiyarso D, Kurnianto S, Stidham M, Kanninen M. 2011. Mangroves among the most carbon-rich forests in the tropics. Nat Geosci 4:293–7. Scholar
  23. de Lima NGB, Galvani E. 2013. Mangrove microclimate: A case study from southeastern Brazil. Earth Interact 17:1–16.CrossRefGoogle Scholar
  24. de Lima NGB, Galvani E, Falcão RM, Cunha-Lignon M. 2013. Air temperature and canopy cover of impacted and conserved mangrove ecosystems: a study of a subtropical estuary in Brazil. J Coast Res 165:1152–7. Scholar
  25. de Vries W, Goodale C, Erisman JW, Hettelingh J-P. 2014. Impacts of nitrogen deposition on ecosystem services in interaction with other nutrients, air pollutants and climate change. In: Sutton MA, Mason KE, Sheppard LJ, Sverdrup H, Haeuber R, Hicks WK, editors. Nitrogen Deposition, Critical Loads and Biodiversity. In: Proceedings of the International Nitrogen Initiative Workshop, linking experts of the Convention on Long-range Transboundary Air Pollution and the Convention on Biological Diversity. Dordrecht: Springer. pp 387–96.Google Scholar
  26. Eisenlohr PV. 2014. Persisting challenges in multiple models: A note on commonly unnoticed issues regarding collinearity and spatial structure of ecological data. Brazilian J Bot 37:365–71.CrossRefGoogle Scholar
  27. Ellison AM. 2002. Macroecology of mangroves: Large-scale patterns and processes in tropical coastal forests. Trees 16:181–94.CrossRefGoogle Scholar
  28. Elser JJ, Bracken MES, Cleland EE, Gruner DS, Harpole WS, Hillebrand H, Ngai JT, Seabloom EW, Shurin JB, Smith JE. 2007. Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol Lett 10:1135–42.CrossRefGoogle Scholar
  29. Empresa Brasileira de Pesquisa Agropecuária. 1997. Manual de métodos e análises de solo. 2nd edn. Rio de Janeiro: EMBRAPA.Google Scholar
  30. Empresa Brasileira de Pesquisa Agropecuária. 1999. Manual de análises químicas de solos, plantas e fertilizantes. 2nd edn. Brasília, DF: EMBRAPA.Google Scholar
  31. Empresa Brasileira de Pesquisa Agropecuária. 2000. Métodos de análises de tecidos vegetais utilizados na Embrapa Solos. Rio de Janeiro: EMBRAPA.Google Scholar
  32. Erisman JW, Galloway JN, Seitzinger S, Bleeker A, Dise NB, Roxana Petrescu AM, Leach AM, de Vries W. 2013. Consequences of human modification of the global nitrogen cycle. Philos Trans R Soc B 368:20130116.CrossRefGoogle Scholar
  33. Estrada GCD, Soares MLG, de Oliveira Chaves F, Cavalcanti VF. 2013. Analysis of the structural variability of mangrove forests through the physiographic types approach. Aquat Bot 111:135–43. Scholar
  34. Fang Y, Koba K, Makabe A, Takahashi C, Zhu W, Hayashi T, Hokari AA, Urakawa R, Bai E, Houlton BZ, Xi D, Zhang S, Matsushita K, Tu Y, Liu D, Zhu F, Wang Z, Zhou G, Chen D, Makita T, Toda H, Liu X, Chen Q, Zhang D, Li Y, Yoh M. 2015. Microbial denitrification dominates nitrate losses from forest ecosystems. Proc Natl Acad Sci 112:1470–4.
  35. Fernandes SO, Loka Bharathi PA, Bonin PC, Michotey VD. 2010. Denitrification: An important pathway for nitrous oxide production in tropical mangrove sediments (Goa, India). J Environ Qual 39:1507–16.
  36. Fogel ML, Wooller MJ, Cheeseman J, Smallwood BJ, Roberts Q, Romero I, Meyers MJ. 2008. Unusually negative nitrogen isotopic compositions (δ15 N) of mangroves and lichens in an oligotrophic, microbially-influenced ecosystem. Biogeosciences 5:1693–704.
  37. Fry B, Bern AL, Ross MS, Meeder JF. 2000. δ15 N Studies of nitrogen use by the red mangrove, Rhizophora mangle L. in South Florida. Estuar Coast Shelf Sci 50:291–6.
  38. Fry B, Cormier N. 2011. Chemical ecology of red mangroves, Rhizophora mangle, in the Hawaiian Islands. Pacific Sci 65:219–34.
  39. Fry B, Gace A, McClelland JW. 2003. Chemical indicators of anthropogenic nitrogen loading in four pacific estuaries. Pacific Sci 57:77–101.CrossRefGoogle Scholar
  40. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA. 2008. Transformation of the nitrogen cycle: Recent trends, questions, and potential solutions. Science 320:889–92.CrossRefGoogle Scholar
  41. Greweling T, Peech M. 1960. Chemical soil tests. Ithaca: Cornell University Agricultural Experiment Station, New York State College of Agriculture.Google Scholar
  42. Gritcan I, Duxbury M, Leuzinger S, Alfaro AC. 2016. Leaf stable isotope and nutrient status of temperate mangroves as ecological indicators to assess anthropogenic activity and recovery from eutrophication. Front Plant Sci 7:1–11.CrossRefGoogle Scholar
  43. Hannon JE, Böhlke JK. 2008. Determination of the δ(15 N/14 N) of ammonium (NH4 +) in water: RSIL Lab Code 2898. In: Révész K, Coplen TB, editors. Methods of the Reston Stable Isotope Laboratory: U.S. Geological Survey, Techniques and Methods. p 30.Google Scholar
  44. Hardy RWF, Holsten RD, Jackson EK, Burns RC. 1968. The acetylene-ethylene assay for N2 fixation: Laboratory and field evaluation. Plant Physiol 43:1185–207.
  45. Hicks BJ, Silvester WB. 1985. Nitrogen Fixation associated with the New Zealand mangrove (Avicennia marina (Forsk.) Vierh. var. resinifera (Forst. f.) Bakh.). Appl Environ Microbiol 49:955–9.
  46. Högberg P. 1997. Tansley Review No. 95 15 N natural abundance in soil—plant systems. New Phytol 137:179–203.CrossRefGoogle Scholar
  47. Holmes RM, McClelland JW, Sigman DM, Fry B, Peterson BJ. 1998. Measuring 15 N-NH4 in marine, estuarine, and freshwaters: An adaptation of the ammonia diffusion method for samples with low ammonium concentrations. Mar Chem 60:235–43.CrossRefGoogle Scholar
  48. Houlton BZ, Sigman DM, Hedin LO. 2006. Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc Natl Acad Sci 103:8745–50.
  49. Hutchison J, Manica A, Swetnam R, Balmford A, Spalding M. 2014. Predicting global patterns in mangrove forest biomass. Conserv Lett 7:233–40.CrossRefGoogle Scholar
  50. Huwaldt J, Steinhorst S. 2013. Plot digitizer.
  51. Instituto Brasileiro de Geografia e Estatística. 2010. Censo Demográfico.
  52. Instituto Brasileiro de Geografia Estatística. 2006. Censo agropecuário.
  53. Keller M, Veldkamp E, Weitz AM, Reiners WA. 1993. Effect of pasture age on soil trace-gas emissions from a deforested area of Costa Rica. Nature 365:244–6.CrossRefGoogle Scholar
  54. Kiese R, Hewett B, Graham A, Butterbach-Bahl K. 2003. Seasonal variability of N2O emissions and CH4 uptake by tropical rainforest soils of Queensland. Australia. Global Biogeochem Cycles 17:1043. Scholar
  55. Kottek M, Grieser J, Beck C, Rudolf B, Rubel F. 2006. World map of the Köppen-Geiger climate classification updated. Meteorol Zeitschrift 15:259–63.CrossRefGoogle Scholar
  56. Lee RY, Joye SB. 2006. Seasonal patterns of nitrogen fixation and denitrification in oceanic mangrove habitats. Mar Ecol Prog Ser 307:127–41.CrossRefGoogle Scholar
  57. McKee KL. 1995. Interspecific variation in growth, biomass partitioning, and defensive characteristics of neotropical mangrove seedlings: Response to light and nutrient availability. Am J Bot 82:299–307.CrossRefGoogle Scholar
  58. Mckee KL, Feller IC, Popp M, Wanek W. 2002. Mangrove isotopic (δ15 N and δ13C) fractionation across a nitrogen vs. phosphorus limitation gradient. Ecology 83:1065–75.Google Scholar
  59. Medeiros TCC, Sampaio EVSB. 2008. Allometry of aboveground biomasses in mangrove species in Itamaracá, Pernambuco, Brazil. Wetl Ecol Manag 16:323–30.CrossRefGoogle Scholar
  60. Medina E, Cuevas E, Lugo AE. 2010. Nutrient relations of dwarf Rhizophora mangle L. mangroves on peat in eastern Puerto Rico. Plant Ecol 207:13–24.CrossRefGoogle Scholar
  61. Medina E, Giarrizzo T, Menezes M, Carvalho-Lira M, Carvalho E, Peres A, Silva B, Vilhena R, Reise A, Braga F. 2001. Mangal communities of the”Salgado Paraense”: Ecological heterogeneity along the Braganca peninsula assessed through soil and leaf analyses. Amazoniana XVI:397–416.ça+peninsula+assessed+through+soil+and+leaf+analyses#0.
  62. Meier M. 1991. Nitratbestimmung in Boden-Proben (N-min-Methode). Berlin: LaborPraxis.Google Scholar
  63. Menezes MPM de, Berger U, Mehlig U. 2008. Mangrove vegetation in Amazonia: A review of studies from the coast of Pará and Maranhão States, north Brazil. Acta Amaz 38:403–20.
  64. Murdiyarso D, Purbopuspito J, Kauffman JB, Warren MW, Sasmito SD, Donato DC, Manuri S, Krisnawati H, Taberima S, Kurnianto S. 2015. The potential of Indonesian mangrove forests for global climate change mitigation. Nat Clim Chang 5:1089–92.CrossRefGoogle Scholar
  65. Nardoto GB, Ometto JPHB, Ehleringer JR, Higuchi N, Bustamante MMDC, Martinelli LA. 2008. Understanding the influences of spatial patterns on N availability within the Brazilian Amazon forest. Ecosystems 11:1234–46.CrossRefGoogle Scholar
  66. Niu S, Classen AT, Dukes JS, Kardol P, Liu L, Luo Y, Rustad L, Sun J, Tang J, Templer PH, Thomas RQ, Tian D, Vicca S, Wang YP, Xia J, Zaehle S. 2016. Global patterns and substrate-based mechanisms of the terrestrial nitrogen cycle. Ecol Lett 19:697–709.CrossRefGoogle Scholar
  67. Patrick WH Jr, Mahapatra IC. 1968. Transformation and availability to rice of nitrogen and phosphorous in waterlogged soils. Adv Agron 20:323–59.CrossRefGoogle Scholar
  68. Peel MC, Finlayson BL, McMahon TA. 2007. Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci Discuss 4:439–73.CrossRefGoogle Scholar
  69. Piccolo MC, Neill C, Cerri CC. 1994. Net nitrogen mineralization and net nitrification along a tropical forest-to-pasture chronosequence. Plant Soil 162:61–70.CrossRefGoogle Scholar
  70. Postgate JR. 1982. The fundamentals of nitrogen fixation. New York: Cambridge University Press.Google Scholar
  71. Potts M. 1984. Nitrogen fixation in mangrove forests. In: Por FD, Dor I, Eds. Hydrobiology of the mangal, the ecosystem of the mangrove forests Developments in hydrobiology. The Hague: Dr. W. Junk Publishers. p 155–62.Google Scholar
  72. R Core Team. 2014. R: A language and environment for statistical computing.
  73. Ray R, Majumder N, Das S, Chowdhury C, Jana TK. 2014. Biogeochemical cycle of nitrogen in a tropical mangrove ecosystem, east coast of India. Mar Chem 167:33–43. Scholar
  74. Reed SC, Cleveland CC, Townsend AR. 2011. Functional ecology of free-living nitrogen fixation: a contemporary perspective. Annu Rev Ecol Evol Syst 42:489–512.
  75. Reed SC, Townsend AR, Cleveland CC, Nemergut DR. 2010. Microbial community shifts influence patterns in tropical forest nitrogen fixation. Oecologia 164:521–31.CrossRefGoogle Scholar
  76. Reef R, Feller IC, Lovelock CE. 2010. Nutrition of mangroves. Tree Physiol 30:1148–60.CrossRefGoogle Scholar
  77. Reef R, Feller IC, Lovelock CE. 2014. Mammalian herbivores in Australia transport nutrients from terrestrial to marine ecosystems via mangroves. J Trop Ecol 30:179–88.
  78. Reis CRG, Nardoto GB, Oliveira RS. 2017a. Global overview on nitrogen dynamics in mangroves and consequences of increasing nitrogen availability for these systems. Plant Soil 410:1–19. Scholar
  79. Reis CRG, Nardoto GB, Rochelle ALC, Vieira SA, Oliveira RS. 2017b. Nitrogen dynamics in subtropical fringe and basin mangrove forests inferred from stable isotopes. Oecologia 183:841–8. Scholar
  80. Rivera-Monroy VH, Day JW, Twilley RR, Vera-Herrera F, Coronado-Molina C. 1995a. Flux of nitrogen and sediment in a fringe mangrove forest in terminos lagoon, Mexico. Estuar Coast Shelf Sci 40:139–60.CrossRefGoogle Scholar
  81. Rivera-monroy VH, Twilley RR. 1996. The relative role of denitrification and immobilization in the in mangrove fate of inorganic nitrogen sediments (Terminos Lagoon, Mexico). Limnol Oceanogr 41:284–96.CrossRefGoogle Scholar
  82. Rivera-Monroy VH, Twilley RR, Boustany RG, Day JW, Vera-Herrera F, Del Carmen Ramirez M. 1995b. Direct denitrification in mangrove sediments in Terminos Lagoon, Mexico. Mar Ecol Prog Ser 126:97–109.CrossRefGoogle Scholar
  83. Robinson D. 2001. δ15 N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153–62.CrossRefGoogle Scholar
  84. Romero IC, Jacobson M, Fuhrman JA, Fogel M, Capone DG. 2012. Long-term nitrogen and phosphorus fertilization effects on N2 fixation rates and nifH gene community patterns in mangrove sediments. Mar Ecol 33:117–27.CrossRefGoogle Scholar
  85. Schaeffer-Novelli Y, Cintrón G. 1986. Guia para estudo de áreas de manguezal. In: Estrutura, função e flora. São Paulo: Caribbean Ecological Research.Google Scholar
  86. Schaeffer-Novelli Y, Mesquita HDL, Cintrón-Molero G. 1990. The Cananeia Lagoon Estuarine System, São Paulo, Brazil. Estuaries 13:193–203.CrossRefGoogle Scholar
  87. Shiau Y, Lin M, Tan C, Tian G, Chiu C. 2017. Assessing N2 fixation in estuarine mangrove soils. Estuar Coast Shelf Sci 189:84–9.CrossRefGoogle Scholar
  88. Siegel S, Castellan NJ Jr. 1988. Nonparametric statistics for the behavioral sciences. 2nd edn. New York: MacGraw Hill.Google Scholar
  89. Sigman DM, Casciotti KL, Andreani M, Barford C, Galanter M, Böhlke JK. 2001. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal Chem 73:4145–53.CrossRefGoogle Scholar
  90. Silver WL, Neff J, Mcgroddy M, Veldkamp E, Keller M, Cosme R. 2000. Effects of soil texture on belowground carbon and nutrient storage in a lowland Amazonian Forest ecosystem. Ecosystems 3:193–209.CrossRefGoogle Scholar
  91. StatSoft I. 2011. STATISTICA (data analysis software system).
  92. Sutton MA, Mason KE, Sheppard LJ, Sverdrup H, Haeuber R, Hicks WK. 2014. Nitrogen deposition, critical loads and biodiversity. Dordrecht: Springer.CrossRefGoogle Scholar
  93. Thimdee W, Deein G, Thimdee W, Sangrungruang C, Matsunaga K. 2002. High %N and δ15 N values in mangrove leaves and sediments of a mangrove-fringed estuary, Thailand - Effects of shrimp pond effluents. Bull Soc Sea Water Sci Japan 56:166–73.Google Scholar
  94. Tognella MMP, Soares MLG, Cuevas E, Medina E. 2016. Heterogeneity of elemental composition and natural abundance of stables isotopes of C and N in soils and leaves of mangroves at their southernmost West Atlantic range. Brazilian J Biol 76:994–1003.
  95. Vitousek PM, Howarth RW. 1991. Nitrogen limitation on land and in the sea: How can it occur ? Biogeochemistry 13:87–115.CrossRefGoogle Scholar
  96. Whigham DF, Verhoeven JTA, Samarkin V, Megonigal PJ. 2009. Responses of Avicennia germinans (black mangrove) and the soil microbial community to nitrogen addition in a hypersaline wetland. Estuaries and Coasts 32:926–36.CrossRefGoogle Scholar
  97. Wolters J-W, Gillis LG, Bouma TJ, van Katwijk MM, Ziegler AD. 2016. Land Use Effects on Mangrove Nutrient Status in Phang Nga bay, Thailand. Lan Degrad Dev 76:68–76.CrossRefGoogle Scholar
  98. Wooller M, Smallwood B, Jacobson M, Fogel M. 2003a. Carbon and nitrogen stable isotopic variation in Laguncularia racemosa (L.) (white mangrove) from Florida and Belize: Implications for trophic level studies. Hydrobiologia 499:13–23.CrossRefGoogle Scholar
  99. Wooller M, Smallwood B, Scharler U, Jacobson M, Fogel M. 2003b. A taphonomic study of δ13C and δ15 N values in Rhizophora mangle leaves for a multi-proxy approach to mangrove palaeoecology. Org Geochem 34:1259–75.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature (This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply) 2019

Authors and Affiliations

  • Carla R. G. Reis
    • 1
  • Sasha C. Reed
    • 2
  • Rafael S. Oliveira
    • 3
  • Gabriela B. Nardoto
    • 1
  1. 1.Programa de Pós-Graduação em Ecologia, Instituto de Ciências Biológicas, Campus Darcy RibeiroUniversidade de BrasíliaBrasíliaBrazil
  2. 2.U.S. Geological Survey, Southwest Biological Science CenterMoabUSA
  3. 3.Departamento de Biologia VegetalUniversidade Estadual de CampinasCampinasBrazil

Personalised recommendations