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Nitrogen dynamics in subtropical fringe and basin mangrove forests inferred from stable isotopes

  • Ecosystem ecology – original research
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An Erratum to this article was published on 04 February 2017

Abstract

Mangroves exhibit low species richness compared to other tropical forests, but great structural and functional diversity. Aiming to contribute to a better understanding of the functioning of mangrove forests, we investigated nitrogen (N) dynamics in two physiographic types of mangroves (fringe and basin forests) in southeastern Brazil. Because fringe forests are under great influence of tidal flushing we hypothesized that these forests would exhibit higher N cycling rates in sediment and higher N losses to the atmosphere compared to basin forests. We quantified net N mineralization and nitrification rates in sediment and natural abundance of N stable isotopes (δ15N) in the sediment–plant–litter system. The fringe forest exhibited higher net N mineralization rates and δ15N in the sediment–plant–litter system, but net nitrification rates were similar to those of the basin forest. The results of the present study suggest that fringe forests exhibit higher N availability and N cycling in sediment compared to basin forests.

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References

  • Aburto-Oropeza O, Ezcurra E, Danemann G, Valdez V, Murray J, Sala E (2008) Mangroves in the gulf of California increase fishery yields. Proc Natl Acad Sci USA 105:10456–10459. doi:10.1073/pnas.0804601105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Almeida R (2005) Ecologia de manguezais: dinâmica da serapilheira e funcionamento do ecossistema, Ilha do Cardoso, Cananéia, São Paulo, Brasil. Ph.D. Thesis, Instituto Oceanográfico, Universidade de São Paulo, São Paulo, Brasil

  • Alongi DM (2014) Carbon cycling and storage in mangrove forests. Annu Rev Mar Sci 6:195–219. doi:10.1146/annurev-marine-010213-135020

    Article  Google Scholar 

  • Alongi DM, Boto KG, Robertson AI (1992) Nitrogen and phosphorus cycles. In: Robertson AI, Alongi DM (eds) Tropical mangrove ecosystems. American Geophysical Union, Washington, pp 251–292

    Chapter  Google Scholar 

  • Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linnean Soc 161:105–121. doi:10.1111/j.1095-8339.2009.00996.x

    Article  Google Scholar 

  • Coelho Jr. C (1998). Manguezal, desenvolvimento estrutural da cobertura vegetal ao longo de gradientes de inundação—Cananéia, Estado de São Paulo, Brasil. Master Thesis, Instituto Oceanográfico, Universidade de São Paulo, São Paulo, Brasil

  • Coelho Jr. C (2003) Ecologia de Manguezais: zonação e dinâmica da cobertura vegetal em gradientes ambientais, Cananéia, São Paulo, Brasil. Ph.D. Thesis, Instituto Oceanográfico, Universidade de São Paulo, São Paulo, Brasil

  • Chapin FS III, Matson PA, Vitousek PM (2011) Principles of terrestrial ecosystem ecology. Springer-Verlag, New York

    Book  Google Scholar 

  • Chen R, Twilley RR (1999) Patterns of mangrove forest structure and soil nutrient dynamics along the Shark River Estuary, Florida. Estuaries 22:955–970. doi:10.2307/1353075

    Article  Google Scholar 

  • 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 193:980–992. doi:10.1111/j.1469-8137.2009.02917.x

    Article  Google Scholar 

  • Crona BI, Rönnbäck P (2005) Use of replanted mangroves as nursery grounds by shrimp communities in Gazi Bay. Kenya Estuar Coast Shelf Sci 65:535–544. doi:10.1016/j.ecss.2005.07.001

    Article  Google Scholar 

  • Cunha-Lignon M, Coelho C Jr, Almeida R, Menghini RP, Schaeffer-Novelli Y, Cintrón G, Dahdouh-Guebas F (2011a) Characterization of mangrove forest types in view of conservation and management: a review of mangals at the Cananéia region, São Paulo State. Braz J Coast Res. 64:349–353

    Google Scholar 

  • Cunha-Lignon M, Kampel M, Menghini RP, Schaeffer-Novelli Y, Cintrón G, Dahdouh-Guebas F (2011b) Mangrove forests submitted to depositional processes and salinity variation investigated using satellite images and vegetation structure surveys. J Coast Res 64:344–348

    Google Scholar 

  • Duarte CM, Losada IJ, Hendriks IE, Mazarrasa I, Marbà N (2013) The role of coastal plant communities for climate change mitigation and adaptation. Nat Clim Change 3:961–968. doi:10.1038/nclimate1970

    Article  CAS  Google Scholar 

  • Ellison AM (2002) Macroecology of mangroves: large-scale patterns and processes in tropical coastal forests. Trees 16:181–194. doi:10.1007/s00468-001-0133-7

    Article  Google Scholar 

  • 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 10:1135–1142. doi:10.1111/j.1461-0248.2007.01113.x

    Article  PubMed  Google Scholar 

  • Empresa Brasileira de Pesquisas Agropecuárias (1997) Manual de métodos de análise de solos. Embrapa, Rio de Janeiro

    Google Scholar 

  • Empresa Brasileira de Pesquisas Agropecuárias (1999) Manual de análises químicas do solo, plantas e fertilizantes. Embrapa, Brasília

    Google Scholar 

  • Empresa Brasileira de Pesquisas Agropecuárias (2000) Métodos de análise de tecidos vegetais utilizados na Embrapa Solos. Embrapa, Rio de Janeiro

    Google Scholar 

  • Estrada GCD, Soares ML, Santos DMC, Fernandez V, Almeida PMM, Estevam MRM, Machado MRO (2014) Allometric models for aboveground biomass estimation of the mangrove Avicennia schaueriana. Hydrobiologia 734:171–185. doi:10.1007/s10750-014-1878-5

    Article  CAS  Google Scholar 

  • Fogel ML, Wooller MJ, Cheeseman J, Smallwood BJ, Roberts Q, Romero I, Meyers MJ (2008) Unusually negative nitrogen isotopic compositions (δ15N) of mangroves and lichens in an oligotrophic, microbially-influenced ecosystem. Biogeosciences 5:1693–1704. doi:10.5194/bg-5-1693-2008

    Article  CAS  Google Scholar 

  • Fry B, Bern AL, Ross MS, Meeder JF (2000) 15N Studies of nitrogen use by the red mangrove, Rhizophora mangle L. in South Florida. Estuar Coast Shelf Sci 50:291–296. doi:10.2984/65.2.219

    Article  CAS  Google Scholar 

  • Greweling T, Peech M (1960) Chemical soil tests. New York State College of Agriculture, New York

    Google Scholar 

  • Högberg P (1997) Tansley review no 95: 15N natural abundance in soil-plant systems. New Phytol 137:179–203. doi:10.1046/j.1469-8137.1997.00808.x

    Article  Google Scholar 

  • Ingram RL (1971) Sieve analysis. In: Carver RE (ed) Procedures in sedimentary petrology. Wiley Interscience, New York, pp 49–69

    Google Scholar 

  • Kjerfve B, Lacerda LD (1993) Mangroves of Brazil. In: Lacerda LD (ed) Conservation and sustainable utilization of mangrove forest in Latin America and Africa regions. Part I-Latin America. ITTO/ISME, Okinawa, pp 245–272

    Google Scholar 

  • Krishnan KP, LokaBharathi PA (2009) Organic carbon and iron modulate nitrification rates in mangrove swamps of Goa, south west coast of India. Estuar Coast Shelf Sci 84:419–426. doi:10.1016/j.ecss.2009.07.015

    Article  CAS  Google Scholar 

  • Kristensen E, Jensen MH, Banta GT, Hansen K, Holmer M, King GM (1998) Transformation and transport of inorganic nitrogen in sediments of a southeast Asian mangrove forest. Aquat Microb Ecol 15:165–175. doi:10.3354/ame015165

    Article  Google Scholar 

  • Lebauer DS, Treseder KK (2008) Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distributed. Ecology 89:371–379. doi:10.1890/06-2057.1

    Article  PubMed  Google Scholar 

  • Lugo AE, Medina E, Cuevas E, Cintrón G, Nieves ENL, Schaeffer-Novelli Y (2007) Ecophysiology of a mangrove forest in Jobos Bay, Puerto Rico. Caribb J Sci 43:200–219

    Article  Google Scholar 

  • Mckee KL, Feller IC, Poop M, Wanek W (2002) Mangrove isotopic δ15N and δ13C fractionation across a nitrogen vs. phosphorus limitation gradient. Ecology 83:1065–1075. doi:10.2307/3071914

    Google Scholar 

  • Medeiros TCC, Sampaio EVSB (2008) Allometry of aboveground biomasses in mangrove species in Itamaracá, Pernambuco. Braz Wetl Ecol Manag 16:323–330. doi:10.1007/s11273-007-9069-z

    Article  Google Scholar 

  • 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. doi:10.1007/s11258-009-9650-z

    Article  Google Scholar 

  • Meier M (1991) Nitratbestimmung in Boden-proben (N-min-method). Labor Praxis, Berlin

    Google Scholar 

  • Menezes MPM, 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. 38:403–420. doi:10.1590/S0044-59672008000300004

    Article  Google Scholar 

  • Morrell JM, Corredor JE (1993) Sediment nitrogen trapping in a mangrove lagoon. Estuar Coast Shelf Sci 37:203–212. doi:10.1006/ecss.1993.1051

    Article  Google Scholar 

  • Patrick WH Jr, Mahapatra IC (1968) Transformation and availability to rice of nitrogen and phosphorus in waterlogged soils. Adv Agron 20:323–359

    Article  CAS  Google Scholar 

  • 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. doi:10.1007/BF01416090

    Article  CAS  Google Scholar 

  • R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  • Reef R, Feller IC, Lovelock CE (2010) Nutrition of mangroves. Tree Physiol 30:1148–1160. doi:10.1093/treephys/tpq048

    Article  CAS  PubMed  Google Scholar 

  • Rivera-Monroy VH, Twilley RR (1996) The relative role of denitrification and immobilization in the fate of inorganic nitrogen in mangrove sediments (Terminos Lagoon, Mexico). Limnol Oceanogr 41:284–296. doi:10.4319/lo.1996.41.2.0284

    Article  CAS  Google Scholar 

  • Rivera-Monroy VH, Day JH, Twilley RR, Boustany RG, Day JW, Vera-Herrera F, del Carmen Ramirez M (1995a) Direct denitrification in mangrove sediments in Terminos Lagoon. Mex Mar Ecol Prog Ser. 126:97–109. doi:10.3354/meps126097

    Article  Google Scholar 

  • Rivera-Monroy VH, Day JH, Twilley RR, Vera-Herrera F, Coronado-Molina C (1995b) Flux of nitrogen and sediment in a fringe mangrove forest in Terminos Lagoon. Mex Estuar Coast Shelf Sci 40:139–160. doi:10.1016/S0272-7714(05)80002-2

    Article  CAS  Google Scholar 

  • Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153–162. doi:10.1016/S0169-5347(00)02098-X

    Article  CAS  PubMed  Google Scholar 

  • Schaeffer-Novelli Y, Cintrón-Molero G, Adaime RR, de Camargo TM (1990a) Variability of mangrove ecosystems along the Brazilian coast. Estuaries 13:204–218. doi:10.2307/1351590

    Article  Google Scholar 

  • Schaeffer-Novelli Y, Mesquita HSL, Cintrón-Molero G (1990b) The Cananéia Lagoon Estuarine System, São Paulo, Brazil. Estuaries 13:193–203. doi:10.2307/1351589

    Article  CAS  Google Scholar 

  • Schaeffer-Novelli Y, Cintrón-Molero G, Soares MLG, De-Rosa T (2000) Brazilian mangroves. Aquat. Ecosyst Health 3:561–570. doi:10.1080/14634980008650693

    Article  Google Scholar 

  • Siegel S, Castellan NJ Jr (1988) Nonparametric statistics for the behavioral sciences. MacGraw Hill, New York

    Google Scholar 

  • Spalding M, Kaimura M, Collins L (2010) World atlas of mangroves, 2nd edn. Earthscan, London

    Google Scholar 

  • Twilley RR (1988) Coupling of mangroves to the productivity of estuarine and coastal waters. In: Jansson BO (ed) Costal-offshore ecosystem interactions. Lecture Notes on Coastal and Estuarine Studies. Springer, Berlin, pp 155–180

    Google Scholar 

  • Twilley RW, Lugo AE, Patterson-Zucca C (1986) Litter production and turnover in basin mangrove forests in southwest Florida. Ecology 67:670–683. doi:10.2307/1937691

    Article  Google Scholar 

  • Wooller M, Smallwood B, Scharlerc U, Jacobsonb M, Fogel M (2003) A taphonomic study of 13C and 15N values in Rhizophora mangle leaves for a multi-proxy approach to mangrove palaeoecology. Org Geochem 34:1259–1275. doi:10.1016/S0146-6380(03)00116-5

    Article  CAS  Google Scholar 

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Acknowledgements

This study was supported by the Fundação de Amparo à Pesquisa no Estado de São Paulo (FAPESP) (Processo 2011/09613), and by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) by a fellowship grant for the first author. The authors are thankful to Marília Cunha-Lignon for kindly providing the shapefiles of mangrove forests area. Jim Hesson of AcademicEnglishSolutions.com revised the English.

Author contribution statement

CRGR, GBN, and RSO conceived the idea and field sampling design. All authors conducted fieldwork. CRGR and ALCR conducted laboratory and statistical analysis. All authors wrote the manuscript.

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Correspondence to Carla Roberta Gonçalves Reis.

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Communicated by Russell K. Monson.

An erratum to this article is available at http://dx.doi.org/10.1007/s00442-017-3819-2.

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Reis, C.R.G., Nardoto, G.B., Rochelle, A.L.C. et al. Nitrogen dynamics in subtropical fringe and basin mangrove forests inferred from stable isotopes. Oecologia 183, 841–848 (2017). https://doi.org/10.1007/s00442-016-3789-9

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