, Volume 21, Issue 5, pp 901–912 | Cite as

Modest Gaseous Nitrogen Losses Point to Conservative Nitrogen Cycling in a Lowland Tropical Forest Watershed

  • Fiona M. SoperEmail author
  • Phillip G. Taylor
  • William R. Wieder
  • Samantha R. Weintraub
  • Cory C. Cleveland
  • Stephen Porder
  • Alan R. Townsend


Primary tropical rainforests are generally considered to be relatively nitrogen (N) rich, with characteristically large hydrologic and gaseous losses of inorganic N. However, emerging evidence suggests that some tropical ecosystems can exhibit tight N cycling, with low biologically available losses. In this study, we combined isotopic data with a well-characterized watershed N mass balance to close the N budget and characterize gaseous N losses at the ecosystem scale in a lowland tropical rainforest on the Osa Peninsula in southwestern Costa Rica. We measured δ15N and δ18O of nitrate (NO3 ) in precipitation, surface, shallow and deep soil lysimeters and stream water biweekly for 1 year. Enrichment of both isotopes indicates that denitrification occurs predominantly as NO3 moves from surface soil down to 15 cm depth or laterally to stream water, with little further processing in deeper soil. Two different isotopic modeling approaches suggested that the gaseous fraction comprises 14 or 32% of total N loss (2.7 or 7.5 kg N ha−1 y−1), though estimates are sensitive to selection of isotopic fractionation values. Gas loss estimates using the mass balance approach (3.2 kg N ha−1 y−1) fall within this range and include N2O losses of 0.9 kg N ha−1 y−1. Overall, gaseous and soluble hydrologic N losses comprise a modest proportion (~ 25%) of the total N inputs to this ecosystem. By contrast, relatively large, episodic hydrologic losses of non-biologically available particulate N balance the majority of N inputs and may contribute to maintaining conservative N cycling in this lowland tropical forest. Similar patterns of N cycling may occur in other tropical forests with similar state factor combinations—high rainfall, steep topography, relatively fertile soils—such as the western arc of the Amazon Basin and much of IndoMalaysia, but this hypothesis remains untested.


denitrification nitrogen cycle nitrous oxide δ15δ18NO3 tropical forest 



We thank W. Combronero-Castro for his invaluable assistance with fieldwork in Costa Rica. We thank M. Jimenez and the late H. Michaud of the Drake Bay Wilderness Camp for providing field access and logistical support and we also thank F. Campos Rivera, the Organizaciόn para Estudios Tropicales (OET) and the Ministerio de Ambiente y Energia (MINAE) for assisting with research permits and logistics in Costa Rica. This study was supported by a National Science Foundation GK-12 fellowship, the Andrew Mellon Foundation and an NSF DEB Award (# 0919080) to CC and NSF DEB Award (# 0918387) to SP.

Supplementary material

10021_2017_193_MOESM1_ESM.docx (109 kb)
Supplementary material 1 (DOCX 109 kb)


  1. Alvarez-Clare S, Mack MC. 2011. Influence of precipitation on soil and foliar nutrients across nine Costa Rican forests. Biotropica 43:433–41.CrossRefGoogle Scholar
  2. Asner GP, Martin RE, Tupayachi R, Anderson CB, Sinca F, Carranza-Jiménez L, Martinez P. 2014. Amazonian functional diversity from forest canopy chemical assembly. Proc Natl Acad Sci USA 111:5604–9.CrossRefPubMedGoogle Scholar
  3. Bai E, Houlton BZ. 2009. Coupled isotopic and process-based modeling of gaseous nitrogen losses from tropical rain forests. Global Biogeochem Cycles 23:GB2011. doi: 10.1029/2008GB003361.CrossRefGoogle Scholar
  4. Bai E, Houlton BZ, Wang YP. 2012. Isotopic identification of nitrogen hotspots across natural terrestrial ecosystems. Biogeosciences 9:3287–304.CrossRefGoogle Scholar
  5. Balzotti CS, Asner GP, Taylor PG, Cleveland CC, Cole R, Martin RE, Nasto MK, Osborne BB, Porder S, Townsend AR. 2016. Environmental controls on canopy foliar nitrogen distributions in a neotropical lowland forest. Ecol Appl 26:2451–64.CrossRefGoogle Scholar
  6. Brookshire ENJ, Thomas SA. 2013. Ecosystem consequences of tree monodominance for nitrogen cycling in lowland tropical forest. PLoS ONE 8:e70491–7.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Brookshire ENJ, Gerber S, Menge DNL, Hedin LO. 2011. Large losses of inorganic nitrogen from tropical rainforests suggest a lack of nitrogen limitation. Ecol Lett 15:9–16.CrossRefPubMedGoogle Scholar
  8. Buchs DM, Baumgartner PO, Baumgartner-Mora C, Bandini AM, Jackett S-J, Diserens M-O, Stucki J. 2009. Late Cretaceous to Miocene seamount accretion and mélange formation in the Osa and Burica Peninsulas (Southern Costa Rica): episodic growth of a convergent margin. Geol Soc Lon Spec Publ 328:411–56.CrossRefGoogle Scholar
  9. Casciotti K, Sigman D, Hastings M, Bohlke J, Hilkert A. 2002. Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method. Anal Chem 74:4905–12.CrossRefPubMedGoogle Scholar
  10. Chestnut TJ, Zarin DJ, Mcdowell WH, Keller M. 1999. A nitrogen budget for late-successional hillslope tabonuco forest, Puerto Rico. Biogeochemistry 46:85–108.Google Scholar
  11. Cleveland CC, Townsend AR. 2006. Nutrient additions to a tropical rain forest drive substantial soil carbon dioxide losses to the atmosphere. Proc Natl Acad Sci USA 103:10316–21.CrossRefPubMedGoogle Scholar
  12. Cleveland CC, Townsend AR, Schimel D, Fisher H, Howarth RW, Hedin L, Perakis S, Latty E, Von Fischer J, Elseroad A. 1999. Global patterns of terrestrial biological nitrogen (N2) fixation in natural ecosystems. Glob Biogeochem Cycles 13:623–45.CrossRefGoogle Scholar
  13. Craine JM, Brookshire ENJ, Cramer MD, Hasselquist NJ, Koba K, Marin-Spiotta E, Wang L. 2015. Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant Soil 396:1–26.CrossRefGoogle Scholar
  14. 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 USA 112:1470–4.CrossRefPubMedGoogle Scholar
  15. Fisher JB, Malhi Y, Torres IC, Metcalfe DB, van de Weg MJ, Meir P, Silva-Espejo JE, Huasco WH. 2012. Nutrient limitation in rainforests and cloud forests along a 3,000-m elevation gradient in the Peruvian Andes. Oecologia 172:889–902.CrossRefPubMedGoogle Scholar
  16. Garcia Montiel DC, Steudler PA, Piccolo MC, Melillo JM, Neill C, Cerri CC. 2001. Controls on soil nitrogen oxide emissions from forest and pastures in the Brazilian Amazon. Glob Biogeochem Cycles 15:1021–30.CrossRefGoogle Scholar
  17. Groffman P, Altabet M, Böhlke J, Butterbach-Bahl K, David M, Firestone MK, Giblin A, Kana T, Nielsen L, Voytek M. 2006. Methods for measuring denitrification: diverse approaches to a difficult problem. Ecol Appl 16:2091–122.CrossRefPubMedGoogle Scholar
  18. Hall SJ, Silver WL. 2015. Reducing conditions, reactive metals, and their interactions can explain spatial patterns of surface soil carbon in a humid tropical forest. Biogeochemistry 125:149–65.CrossRefGoogle Scholar
  19. Hall SJ, Weintraub SR, Bowling DR. 2016. Scale-dependent linkages between nitrate isotopes and denitrification in surface soils: implications for isotope measurements and models. Oecologia 181:1221–31.CrossRefPubMedGoogle Scholar
  20. Harrington RA, Fownes JH, Vitousek PM. 2001. Production and resource use efficiencies in N- and P-limited tropical forests: a comparison of responses to long-term fertilization. Ecosystems 4:646–57.CrossRefGoogle Scholar
  21. Hedin L, Vitousek P. 2003. Nutrient losses over four million years of tropical forest development. Ecology 84:2231–55.CrossRefGoogle Scholar
  22. Hedin L, Brookshire E, Menge D, Barron A. 2009. The nitrogen paradox in tropical forest ecosystems. Annu Rev Ecol Syst 40:613–35.CrossRefGoogle Scholar
  23. Hofhansl F, Wanek W, Drage S, Huber W, Weissenhofer A, Richter A. 2010. Topography strongly affects atmospheric deposition and canopy exchange processes in different types of wet lowland rainforest, Southwest Costa Rica. Biogeochemistry 106:371–96.CrossRefGoogle Scholar
  24. Holtgrieve G, Jewett PK, Matson PA. 2006. Variations in soil N cycling and trace gas emissions in wet tropical forests. Oecologia 146:584–94.CrossRefPubMedGoogle Scholar
  25. Houlton BZ, Sigman DM, Hedin LO. 2006. Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc Natl Acad Sci USA 103:8745–50.CrossRefPubMedGoogle Scholar
  26. Houlton BZ, Bai E. 2009. Imprint of denitrifying bacteria on the global terrestrial biosphere. Proc Natl Acad Sci USA 106:21713–16.CrossRefPubMedGoogle Scholar
  27. Højberg O, Revsbech NP, Tiedje JM. 1994. Denitrification in soil aggregates analyzed with microsensors for nitrous oxide and oxygen. Soil Sci Soc Am J 58:1691–8.CrossRefGoogle Scholar
  28. Ishizuka S, Tsuruta H, Murdiyarso D. 2002. An intensive field study on CO2, CH4, and N2O emissions from soils at four land-use types in Sumatra. Indonesia. Glob Biogeochem Cycles 16:22.Google Scholar
  29. Jenny H. 1941. Factors of soil formation: a system of quantitative pedology. New York: McGraw-Hill.Google Scholar
  30. Kaspari M, Garcia MN, Harms KE, Santana M, Wright SJ, Yavitt JB. 2008. Multiple nutrients limit litterfall and decomposition in a tropical forest. Ecol Lett 11:35–43.PubMedGoogle Scholar
  31. Kaspari M, Powers JS. 2016. Biogeochemistry and geographical ecology: embracing all twenty-five elements required to build organisms. Am Nat 188:S62–73.CrossRefPubMedGoogle Scholar
  32. Kendall C, Elliott EM, Wankel SD. 2007. Tracing anthropogenic inputs of nitrogen to ecosystems. In: Michener R, Lajtha K, Eds. Stable isotopes in ecology and environmental science. Malden: Blackwell Publishing. p 375–449.CrossRefGoogle Scholar
  33. Koehler B, Corre MD, Veldkamp E, Wullaert H, Wright SJ. 2009. Immediate and long-term nitrogen oxide emissions from tropical forest soils exposed to elevated nitrogen input. Glob Change Biol 15:2049–66.CrossRefGoogle Scholar
  34. Liptzin D, Silver WL. 2015. Spatial patterns in oxygen and redox sensitive biogeochemistry in tropical forest soils. Ecosphere 6:11–14.CrossRefGoogle Scholar
  35. Mariotti A, Germon JC, Hubert P, Kaiser P, Letolle R, Tardieux A, Tardieux P. 1981. Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant Soil 62:413–30.CrossRefGoogle Scholar
  36. Menge D, DeNoyer JL, Lichstein J. 2010. Phylogenetic constraints do not explain the rarity of nitrogen-fixing trees in late-successional temperate forests. PLoS ONE 5:e12056.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Michalski G, Scott Z, Kabiling M, Thiemens MH. 2003. First measurements and modeling of Δ17O in atmospheric nitrate. Geophys Res Lett 30:1–4.Google Scholar
  38. Nardoto GB, Ometto GPHB, 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
  39. Osborne BB, Nasto MK, Asner GP, Balzotti CS, Cleveland CC, Sullivan BW, Taylor PG, Townsend AR, Porder S. 2017. Climate, topography, and canopy chemistry exert hierarchical control over soil N cycling in a Neotropical lowland forest. Ecosystems 20:1089–103.CrossRefGoogle Scholar
  40. Pérez T, Garcia-Montiel D, Trumbore S, Tyler S, de Camargo P, Moreira M, Piccolo M, Cerri C. 2006. Nitrous oxide nitrification and denitrification 15N enrichment factors from Amazon forest soils. Ecol Appl 16:2153–67.CrossRefPubMedGoogle Scholar
  41. Porder S, Asner GP, Vitousek PM. 2005a. Ground-based and remotely sensed nutrient availability across a tropical landscape. Proc Natl Acad Sci USA 102:10909–12.CrossRefPubMedGoogle Scholar
  42. Porder S, Paytan A, Vitousek PM. 2005b. Erosion and landscape development affect plant nutrient status in the Hawaiian Islands. Oecologia 142:440–9.CrossRefPubMedGoogle Scholar
  43. Posada JM, Schuur EA. 2011. Relationships among precipitation regime, nutrient availability, and carbon turnover in tropical rain forests. Oecologia 165:783–95.CrossRefPubMedGoogle Scholar
  44. Reed SC, Cleveland CC, Townsend AR. 2007. Controls over leaf litter and soil nitrogen fixation in two lowland tropical rain forests. Biotropica 39:585–92.CrossRefGoogle Scholar
  45. Reed SC, Townsend AR, Davidson EA, Cleveland CC. 2012. Stoichiometric patterns in foliar nutrient resorption across multiple scales. New Phytol 196:173–80.CrossRefPubMedGoogle Scholar
  46. Rose LA, Sebestyen SD, Elliott EM, Koba K. 2015. Drivers of atmospheric nitrate processing and export in forested catchments. Water Resour Res 51:1333–52.CrossRefGoogle Scholar
  47. Russell AE, Raich JW. 2012. Rapidly growing tropical trees mobilize remarkable amounts of nitrogen, in ways that differ surprisingly among species. Proc Natl Acad Sci USA 109:10398–402.CrossRefPubMedGoogle Scholar
  48. Schuur EA. 2003. Productivity and global climate revisited: the sensitivity of tropical forest growth to precipitation. Ecology 84:1165–70.CrossRefGoogle Scholar
  49. Schuur EA, Matson PM. 2001. Net primary productivity and nutrient cycling across a mesic to wet precipitation gradient in Hawaiian montane forest. Oecologia 128:431–42.CrossRefPubMedGoogle Scholar
  50. Schwendenmann L, Veldkamp E. 2005. The role of dissolved organic carbon, dissolved organic nitrogen, and dissolved inorganic nitrogen in a tropical wet forest ecosystem. Ecosystems 8:339–51.CrossRefGoogle Scholar
  51. Sigman D, Casciotti K, Andreani M, Barford C, Galanter M, Böhlke J. 2001. A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal Chem 73:4145–53.CrossRefPubMedGoogle Scholar
  52. Silver WL, Lugo AE, Keller M. 1999. Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils. Biogeochemistry 44:301–28.Google Scholar
  53. Sotta ED, Corre MD, Veldkamp E. 2008. Differing N status and N retention processes of soils under old-growth lowland forest in Eastern Amazonia, Caxiuanã, Brazil. Soil Biol Biogeochem 40:740–50.CrossRefGoogle Scholar
  54. Sullivan BW, Smith WK, Townsend AR, Nasto MK, Reed SC, Chazdon RL, Cleveland CC. 2014. Spatially robust estimates of biological nitrogen (N) fixation imply substantial human alteration of the tropical N cycle. Proc Natl Acad Sci USA 111:8101–6.CrossRefPubMedGoogle Scholar
  55. Taylor PG, Wieder WR, Weintraub S, Cohen S, Cleveland CC, Townsend AR. 2015a. Organic forms dominate hydrologic nitrogen export from a lowland tropical watershed. Ecology 96:1229–41.CrossRefPubMedGoogle Scholar
  56. Taylor PG, Cleveland CC, Wieder WR, Sullivan BW, Doughty CE, Dobrowski SZ, Townsend AR. 2015b. Temperature and rainfall interact to control carbon cycling in tropical forests. Ecol Lett 20:779–88.CrossRefPubMedGoogle Scholar
  57. Templer P, Silver W, Pett-Ridge J, DeAngelis KM. 2008. Plant and microbial controls on nitrogen retention and loss in a humid tropical forest. Ecology 89:3030–40.CrossRefGoogle Scholar
  58. Townsend A, Cleveland CC, Asner G. 2007. Controls over foliar N: p ratios in tropical rain forests. Ecology 88:107–18.CrossRefPubMedGoogle Scholar
  59. Townsend A, Asner G, Cleveland CC. 2008. The biogeochemical heterogeneity of tropical forests. Trends Ecol Evol 23:424–31.CrossRefPubMedGoogle Scholar
  60. Uehara G, Gillman GP. 1981. The mineralogy, chemistry, and physics of tropical soils with variable charge clays. Westview Press.Google Scholar
  61. Vitousek PM. 1997. Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75.CrossRefGoogle Scholar
  62. Vitousek PM. 1984. Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285–98.CrossRefGoogle Scholar
  63. Vitousek PW, Porder S, Houlton BZ, Chadwick OA. 2010. Terrestrial phosphorus limitation: mechanisms, implications, and nitrogen–phosphorus interactions. Ecol Appl 20:5–15.CrossRefPubMedGoogle Scholar
  64. Wanek W, Drage S, Hinko N, Hofhansl F. 2008. Primary production and nutrient cycling in lowland rainforests of the Golfo Dulce region. In: Weissenhofer A, Huber W, Mayer V, Pamperl S, Weber A, Aubrecht G, Eds. Natural and cultural history of the Golfo Dulce Region, Costa Rica. Oberösterreichisches Landesmuseum, Biologiezentrum. pp 155–177.Google Scholar
  65. Weintraub S, Cole J, Schmitt CG, All JD. 2016. Climatic controls on the isotopic composition and availability of soil nitrogen across mountainous tropical forest. Ecosphere 7(8):e01412. doi: 10.1002/ecs2.1412.CrossRefGoogle Scholar
  66. Weintraub SR, Taylor PG, Porder S, Cleveland CC, Asner GP, Townsend AR. 2015. Topographic controls on soil nitrogen availability in a lowland tropical forest. Ecology 96:1561–74.CrossRefGoogle Scholar
  67. Wieder WR, Cleveland CC, Townsend AR. 2009. Controls over leaf litter decomposition in wet tropical forests. Ecology 90:3333–41.CrossRefPubMedGoogle Scholar
  68. Wieder WR, Cleveland CC, Townsend AR. 2011. Throughfall exclusion and leaf litter addition drive higher rates of soil nitrous oxide emissions from a lowland wet tropical forest. Glob Change Biol 17:3195–207.CrossRefGoogle Scholar
  69. Wieder WR, Cleveland CC, Taylor PG, Nemergut DR, Hinckley E-L, Philippot L, Bru D, Weintraub SR, Martin M, Townsend AR. 2013. Experimental removal and addition of leaf litter inputs reduces nitrate production and loss in a lowland tropical forest. Biogeochemistry 113:629–42.CrossRefGoogle Scholar
  70. Wright SJ, Yavitt JB, Wurzburger N, Turner BL, Tanner EVJ, Sayer EJ, Santiago LS, Kaspari M, Hedin LO, Harms KE, Garcia MN, Corre MD. 2011. Potassium, phosphorus, or nitrogen limit root allocation, tree growth, or litter production in a lowland tropical forest. Ecology 92:1616–25.CrossRefPubMedGoogle Scholar
  71. Yang WH, Weber KA, Silver WL. 2012. Nitrogen loss from soil through anaerobic ammonium oxidation coupled to iron reduction. Nat Geosci 5:538–41.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Fiona M. Soper
    • 1
    Email author
  • Phillip G. Taylor
    • 2
  • William R. Wieder
    • 3
  • Samantha R. Weintraub
    • 4
  • Cory C. Cleveland
    • 1
  • Stephen Porder
    • 5
  • Alan R. Townsend
    • 2
  1. 1.Department of Ecosystem and Conservation SciencesUniversity of MontanaMissoulaUSA
  2. 2.The Institute of Artic and Alpine ResearchUniversity of ColoradoBoulderUSA
  3. 3.Climate and Global Dynamics LaboratoryNational Center for Atmospheric ResearchBoulderUSA
  4. 4.National Ecological Observatory NetworkBoulderUSA
  5. 5.Department of Ecology and Evolutionary BiologyBrown UniversityProvidenceUSA

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