Skip to main content

Advertisement

Log in

Stable nitrogen isotope patterns of trees and soils altered by long-term nitrogen and phosphorus addition to a lowland tropical rainforest

  • Published:
Biogeochemistry Aims and scope Submit manuscript

Abstract

Foliar nitrogen (N) isotope ratios (δ15N) are used as a proxy for N-cycling processes, including the “openness” of the N cycle and the use of distinct N sources, but there is little experimental support for such proxies in lowland tropical forest. To address this, we examined the δ15N values of soluble soil N and canopy foliage of four tree species after 13 years of factorial N and P addition to a mature lowland rainforest. We hypothesized that N addition would lead to 15N-enriched soil N forms due to fractionating losses, whereas P addition would reduce N losses as the plants and microbes adjusted their stoichiometric demands. Chronic N addition increased the concentration and δ15N value of soil nitrate and δ15N in live and senesced leaves in two of four tree species, but did not affect ammonium or dissolved organic N. Phosphorus addition significantly increased foliar δ15N in one tree species and elicited significant N × P interactions in two others due to a reduction in foliar δ15N enrichment under N and P co-addition. Isotope mixing models indicated that three of four tree species increased their use of nitrate relative to ammonium following N addition, supporting the expectation that tropical trees use the most available form of mineral N. Previous observations that anthropogenic N deposition in this tropical region have led to increasing foliar δ15N values over decadal time-scales is now mechanistically linked to greater usage of 15N-enriched nitrate.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Amundson R, Austin AT, Schuur EAG, Yoo K, Matzek V, Kendall C, Uebersax A, Brenner D, Baisden WT (2003) Global patterns of the isotopic composition of soil and plant nitrogen. Glob Biogeochem Cycle 17:31

    Article  Google Scholar 

  • Andersen KA, Turner BL (2013) Preferences or plasticity in nitrogen acquisition by understory palms in a tropical montane forest? J Ecol 101:819–825

    Article  Google Scholar 

  • Ashton IW, Miller AE, Bowman WD, Suding KN (2008) Nitrogen preferences and plant–soil feedbacks as influenced by neighbors in the alpine tundra. Oecologia 156:625–636

    Article  Google Scholar 

  • Averil C, Finzi A (2011) Increasing plant use of organic nitrogen with elevation is reflected in nitrogen uptake rates and ecosystem δN15. Ecology 92:883–891

    Google Scholar 

  • Baayan RH, Davidson DJ, Bates DM (2008) Mixed-effects modeling with crossed random effects for subjects and items. J Mem Lang 59:390–412

    Article  Google Scholar 

  • Baayen RH (2011) languageR: Data sets and functions with “Analyzing Linguistic Data: A practical introduction to statistics”. R package version 14 http://CRAN.R-project.org/package=languageR

  • Bai E, Houlton BZ (2009) Coupled isotopic and process-based modeling of gaseous nitrogen losses from tropical rain forest. Global Biogeochem Cycle 23 (GB2011)

  • Bai E, Houlton BZ, Wang Y (2011) Isotopic identification of global nitrogen hotspots across natural terrestrial ecosystems. Biogeosci Discuss 8:12113–12152

    Article  Google Scholar 

  • Bassirirad H (2000) Kinetics of nutrient uptake by roots: responses to global change. New Phytol 147:155–169

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B (2012) lme4: Linear mixed-effects models using S4 classes. R package version 0.999999-0. http://CRANR-project.org/package=lme4

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens HH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  Google Scholar 

  • Bouwmeester RJB, Vlek PLG, Stumpe JM (1985) Effect of environmental factors on ammonia volatilization from a urea-fertilized soil. Soil Sci Soc Am J 49:376–381

    Article  Google Scholar 

  • Brookshire ENJ, Hedin LO, Newbold JD, Sigman DM, Jackson JK (2012) Sustained losses of bioavailable nitrogen from montane tropical forests. Nat Geosci 5:1–4

    Article  Google Scholar 

  • Cabrera ML, Beare MH (1993) Alkaline persulfate oxidation for determining total nitrogen in microbial biomass extracts. Soil Sci Soc Am J 57:1007–1012

    Article  Google Scholar 

  • Christianson CB, Baethgen WE, Carmona G, Howard RG (1993) Microsite reactions of urea-nbtpt fertilizer on the soil surface. Soil Biol Biochem 25:1107–1117

    Article  Google Scholar 

  • Corre MD, Veldkamp E, Arnold J, Wright SJ (2010) Impact of elevated N input on soil N cycling and losses in old-growth lowland and montane forests in Panama. Ecology 91:1715–1729

    Article  Google Scholar 

  • Davidson EA, Reis de Carvalho CJ, Figueira AM, Ishida FY, Ometto JPHB, Nardoto GB, Saba RT, Hayashi SN, Leal EC, Vieira ICG, Martinelli LA (2007) Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447:995–998

    Article  Google Scholar 

  • Dawson TE, Mambelli S, Plamboeck AH, Templer PH, Tu KP (2002) Stable isotopes in plant ecology. Annu Rev Ecol Syst 33:507–559

    Article  Google Scholar 

  • Dijkstra P, LaViolette CM, Coyle JS, Doucett RR, Schwartz E, Hart SC, Hungate BA (2008) 15N enrichment as an integrator of the effects of C and N on microbial metabolism and ecosystem function. Ecol Lett 11:1–9

    Article  Google Scholar 

  • Doyle A, Weintraub MN, Schimel JP (2004) Persulfate digestion and simultaneous colorimetric analysis of carbon and nitrogen in soil extracts. Soil Sci Soc Am J 68:669–676

    Article  Google Scholar 

  • Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends Plant Sci 6:121–126

    Article  Google Scholar 

  • Giblin AE, Nadelhoffer KJ, Shaver GR, Laundre J, McKerrow A (1991) Biogeochemical diversity along a topographic gradient in a tundra landscape. Ecol Monogr 61:415–436

    Article  Google Scholar 

  • Giblin AE, Laundre JA, Nadelhoffer KJ, Shaver GR (1994) Measuring nutrient availability in arctic soils using ion exchange resins: a field test. Soil Sci Soc Am J 58:1154–1162

    Article  Google Scholar 

  • Glass ADM, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi MY, Unkles SE, Vidmar JJ (2002) The regulation of nitrate and ammonium transport systems in plants. J Exp Bot 53:855–864

    Article  Google Scholar 

  • Guehl JM, Domenach AM, Bereau M, Barigah TS, Casabianca H, Ferhi A, Garbaye J (1998) Functional diversity in an Amazonian rainforest of French Guyana: a dual isotope approach (δ15N and δ13C). Oecologia 116:316–330

    Article  Google Scholar 

  • Hall SJ, Matson PA (2003) Nutrient status of tropical rain forests influences soil N dynamics after N additions. Ecol Monogr 73:107–129

    Article  Google Scholar 

  • Handley LL, Daft MJ, Wilson J, Scrimgeour CM, Ingleby K, Sattar MA (1993) Effects of the ecto-mycorrhizal and VA-mycorrhizal fungi Hydnagium carneum and Glomus clarum on the Delta-N-15 and Delta-C-13 values of Eucalyptus globulus and Ricinus communis. Plant Cell Environ 16:375–382

    Article  Google Scholar 

  • Harrison KA, Bol R, Bardgett RD (2007) Preferences for different nitrogen forms by coexisting plant species and soil microbes. Ecology 88:989–999

    Article  Google Scholar 

  • Hedin LO, Brookshire ENJ, Menge DNL, Barron AR (2009) The nitrogen paradox in tropical forest ecosystems. Annu Rev Ecol Syst 40:613–635

    Article  Google Scholar 

  • Hietz P, Dünisch O, Wanek W (2010) Long-term trends in nitrogen isotope composition and nitrogen concentration in Brazilian rainforest trees suggest changes in nitrogen cycle. Environ Sci Technol 44:1191–1196

    Article  Google Scholar 

  • Hietz P, Turner BL, Wanek W, Richter A, Nock CA, Wright SJ (2011) Long-term change in the nitrogen cycle of tropical forests. Science 334:664–666

    Article  Google Scholar 

  • Hobbie EA, Högberg P (2012) Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phyt 196:367–382

    Article  Google Scholar 

  • Hobbie EA, Ouimette AP (2009) Controls of nitrogen isotope patterns in soil profiles. Biogeochemistry 95:355–371

    Article  Google Scholar 

  • Hobbie EA, Jumpponen A, Trappe J (2005) Foliar and fungal 15N:14N ratios reflect development of mycorrhizae and nitrogen supply during primary succession: testing analytical models. Oecologia 146:258–268

    Article  Google Scholar 

  • Houlton BZ, Sigman DM, Hedin LO (2006) Isotopic evidence for large gaseous nitrogen losses from tropical rainforests. Proc Nat Acad Sci USA 103(23):8745–8750

    Article  Google Scholar 

  • Houlton BZ, Sigman DM, Schuur EAG, Hedin LO (2007) A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Nat Acad Sci USA 104:8902–8906

    Article  Google Scholar 

  • IAEA (2004) IAEA analytical quality control services reference materials catalouge 2004–2005. IAEA, Vienna

    Google Scholar 

  • Kahmen A, Wanek W, Buchmann N (2008) Foliar δ15N values characterize soil N cycling and reflect nitrate or ammonium preference of plants along a temperate grassland gradient. Oecologia 156:861–870

    Article  Google Scholar 

  • Khanif YM (1992) Ammonia volatilization from Malaysian soils following application of urea. Pertanika 15:115–120

    Google Scholar 

  • Killingbeck KT (1996) Nutrients in senesced leaves: keys to the search for potential resorption and resorption proficiency. Ecology 77:1716–1727

    Article  Google Scholar 

  • Knapp AN, Sigman DM, Lipschultz F (2005) N isotopic composition of dissolved organic nitrogen and nitrate at the Bermuda Atlantic Time-series Study site. Glob Biogeochem Cycle 19:GB1018

    Article  Google Scholar 

  • Koba K, Isobe K, Takebayashi Y, Fang YT, Sasaki Y, Saito W, Yoh M, Mo J, Liu L, Lu X, Zhang T, Zhang W, Senoo K (2010) δ15N of soil N and plants in a N-saturated, subtropical forest of southern China. Rapid Commun Mass Spectrom 24:2499–2506

    Article  Google Scholar 

  • 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 15:2049–2066

    Article  Google Scholar 

  • Koehler B, Corre MD, Steger K, Well R, Zehe E, Sueta JP, Veldkamp E (2012) An in-depth look into a tropical lowland forest soil: nitrogen-addition effects on the contents of N2O, CO2 and CH4 and N2O isotopic signatures down to 2-m depth. Biogeochemistry 111:695–713

    Article  Google Scholar 

  • Kramer MG, Sollins P, Sletten RS, Swart PK (2003) N isotope fractionation and measures of organic matter alteration during decomposition. Ecology 84:2021–2025

    Article  Google Scholar 

  • Lohse KA, Matson P (2005) Consequences of nitrogen additions for soil losses from wet tropical forests. Ecol Appl 15:1629–1648

    Article  Google Scholar 

  • Lu M, Yang Y, Luo Y, Fang C, Zhou X, Chen J, Yang X, Li B (2011) Responses of ecosystem nitrogen cycle to nitrogen addition: a meta-analysis. New Phyt 189:1040–1050

    Article  Google Scholar 

  • Marshal JD, Brooks JR, Lajtha K (2007) Sources of variation in the stable isotopic composition of plants. In: Michener R (ed) Stable isotopes in ecology and environmental science. Blackwell Publishing, USA, pp 22–60

    Chapter  Google Scholar 

  • Martinelli LA, Piccolo MC, Townsend AR, Vitousek PM, Cuevas E, McDowell W, Robertson GP, Santos OC, Treseder K (1999) Nitrogen stable isotopic composition of leaves and soil: tropical versus temperate forests. Biogeochemistry 46:45–65

    Google Scholar 

  • Mayor JR, Schuur EAG, Mack MC, Hollingsworth TN, Bååth E (2012) Nitrogen isotope patterns in Alaskan black spruce reflect organic nitrogen sources and the activity of ectomycorrhizal fungi. Ecosystems 15:819–831

    Google Scholar 

  • Mayor JR, Wright SJ, Turner BL (2014) Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest. J Ecology 102:36–44

    Article  Google Scholar 

  • Nadelhoffer K, Shaver G, Fry B, Giblin A, Johnson L, McKane R (1996) 15N natural abundances and N use by tundra plants. Oecologia 107:386–394

    Article  Google Scholar 

  • Niklas KJ, Owens T, Reich PB, Cobb ED (2005) Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecol Lett 8:636–642

    Article  Google Scholar 

  • Pardo LH, Nadelhoffer KJ (2010) Using nitrogen isotope ratios to assess terrestrial ecosystems at regional and global scales. In: West J, Bowen GJ, Dawson TE, Tu KP (eds) Isoscapes: understanding movement, pattern, and process on Earth through isotope mapping. Springer, New York

    Google Scholar 

  • Park S, Pérez T, Boering KA, Trumbore SE, Gil J, Marquina S, Tyler SC (2011) Can N2O stable isotopes and isotopomers be useful tools to characterize sources and microbial pathways of N2O production and consumption in tropical soils? Glob Biogeochem Cycle 25:GB1001

    Article  Google Scholar 

  • Pérez T, Trumbore SE, Tyler SC, Davidson EA, Keller M, de Camargo PB (2000) Isotopic variability of N2O emissions from tropical forest soils. Glob Biogeochem Cycle 14:525–535

    Article  Google Scholar 

  • Pérez T, Garcia-Montiel D, Trumbore S, Tyler S, Camargo P, Moreira M, Piccolo M, Cerri C (2006) Nitrous oxide nitrification and denitrification 15N enrichment factors from amazon forest soils. Ecol Appl 16:2153–2167

    Article  Google Scholar 

  • Phillips DL, Koch PL (2002) Incorporating concentration dependence in stable isotope mixing models. Oecologia 130:114–125

    Google Scholar 

  • Phillips DL, Newsome SD, Gregg JW (2005) Combining sources in stable isotope mixing models: alternative methods. Oecologia 144:520–527

    Article  Google Scholar 

  • Pörtl K, Zechmeister-Boltenstern S, Wanek W, Ambus P, Berger TW (2007) Natural 15N abundance of soil N pools and N2O reflect the nitrogen dynamics of forest soils. Plant Soil 295:79–94

    Article  Google Scholar 

  • Santiago LS, Wright SJ, Harms KE, Yavitt JB, Korine C, Garica MN, Turner BL (2012) Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. J Ecol 100:309–316

    Article  Google Scholar 

  • Schimann H, Pontona S, Hattenschwilerb S, Ferryc B, Lensib R, Domenacha A-M, Roggy J-C (2008) Differing nitrogen use strategies of two tropical rainforest late successional tree species in French Guiana: evidence from 15N natural abundance and microbial activities. Soil Biol Biochem 40:487–494

    Article  Google Scholar 

  • Schuur EAG, Matson PA (2001) Aboveground net primary productivity and nutrient cycling across a mesic to wet precipitation gradient in Hawaiian montane forest. Oecologia 128:431–442

    Article  Google Scholar 

  • Shearer G, Kohl DH (1986) N2 fixation in field settings, estimations based on natural 15N abundance. Aust J Plant Phys 13:699–757

    Google Scholar 

  • Sigman DM, Casciotti KL, Andreani M, Barford C, Galanter M, Bohlke JK (2001) A bacterial method for the nitrogen isotopic analysis of nitrate in seawater and freshwater. Anal Chem 73:4145–4153

    Article  Google Scholar 

  • Takebayashi Y, Koba K, Sasaki Y, Fang Y, Yoh M (2010) The natural abundance of 15N in plant and soil-available N indicates a shift of main plant N resources to NO3 from NH4 + along the N leaching gradient. Rapid Comm Mass Spectrom 24:1001–1008

    Article  Google Scholar 

  • Talbot JM, Treseder KK (2010) Controls over mycorrhizal uptake of organic nitrogen. Pedobiologia 53:169–179

    Article  Google Scholar 

  • Templer PH, Weathers KC (2011) Use of mixed ion exchange resin and the denitrifier method to determine isotopic values of nitrate in atmospheric deposition and canopy throughfall. Atmos Environ 45:2017–2020

    Article  Google Scholar 

  • Turner BL, Wright SJ (2014) The response of microbial biomass and hydrolytic enzymes to a decade of nitrogen, phosphorus, and potassium addition in a lowland tropical rain forest. Biogeochemistry 117:115–130

    Article  Google Scholar 

  • Turner BL, Yavitt JB, Harms KE, Garcia MN, Romero TE, Wright IJ (2013) Seasonal changes and treatment effects on soil inorganic nutrients following a decade of fertilizer addition in a lowland tropical forest. Soil Sci Soc Am J 17:1357–1369

    Article  Google Scholar 

  • Wang L, Macko SA (2011) Constrained preferences in nitrogen uptake across plant species and environments. Plant Cell Environ 34:525–534

    Article  Google Scholar 

  • Wang L, Shaner P-JL, Macko S (2007) Foliar δ15N patterns along successional gradients at plant community and species levels. Geophys Res Lett 34:L16403

    Google Scholar 

  • 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 92:1616–1625

    Article  Google Scholar 

  • Wunderlich A, Meckenstock RU, Einsiedl F (2013) A mixture of nitrite-oxidizing and denitrifying microorganisms affects the δ18O of dissolved nitrate during anaerobic microbial denitrification depending on the δ18O of ambient water. Geochim Cosmochim Ac 119:31–45

    Google Scholar 

  • Yavitt JB, Wright SJ (2001) Drought and irrigation effects on fine root dynamics in a tropical moist forest, Panama. Biotropica 33:421–434

    Article  Google Scholar 

  • Yavitt JB, Harms KE, Garcia MN, Wright SJ, He F, Mirabello MJ (2009) Spatial heterogeneity of soil chemical properties in a lowland tropical moist forest, Panama. Aust J Soil Res 47:674–687

    Article  Google Scholar 

  • Yavitt JB, Harms KE, Garcia MN, Marabello MJ, Wright SJ (2011) Soil fertility and fine root dynamics in response to 4 years of nutrient (N, P, K) fertilization in a lowland tropical moist forest, Panama. Aust Ecol 36:433–445

    Article  Google Scholar 

Download references

Acknowledgments

Support for J.M. was provided by the National Science Foundation’s International Research Fellowship Program (OISE-1012703) and in-kind support from the Smithsonian Tropical Research Institute’s Fellowship Program. We thank Julio Rodriquez, Dayana Agudo, Helene Mueller-Landau, Luis Ramos, Rueben Hernandez, Sarah Dale, and Tania Romero for their contributions, and the Republic of Panama for providing access to their natural resources for scientific research. We thank Grace Crummer, Jason Curtis, and Kathy Curtis for their contributions at the University of Florida. JM, BT, and JW designed the experiment and wrote the manuscript; TS contributed analytical ideas and logistical support, MB contributed a statistical method. The manuscript was improved due to the untiring efforts of three anonymous reviewers.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jordan R. Mayor.

Additional information

Responsible Editor: Jonathan Sanderman.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 491 kb)

Supplementary material 2 (CSV 4 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Mayor, J.R., Wright, S.J., Schuur, E.A.G. et al. Stable nitrogen isotope patterns of trees and soils altered by long-term nitrogen and phosphorus addition to a lowland tropical rainforest. Biogeochemistry 119, 293–306 (2014). https://doi.org/10.1007/s10533-014-9966-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-014-9966-1

Keywords

Navigation