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Facultative nitrogen fixation by canopy legumes in a lowland tropical forest

  • Ecosystem ecology - Original Paper
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Abstract

Symbiotic dinitrogen (N2) fixation is often invoked to explain the N richness of tropical forests as ostensibly N2-fixing trees can be a major component of the community. Such arguments assume N2 fixers are fixing N when present. However, in laboratory experiments, legumes consistently reduce N2 fixation in response to increased soil N availability. These contrasting views of N2 fixation as either obligate or facultative have drastically different implications for the N cycle of tropical forests. We tested these models by directly measuring N2-fixing root nodules and nitrogenase activity of individual canopy-dominant legume trees (Inga sp.) across several lowland forest types. Fixation was substantial in disturbed forests and some gaps but near zero in the high N soils of mature forest. Our findings suggest that canopy legumes closely regulate N2 fixation, leading to large variations in N inputs across the landscape, and low symbiotic fixation in mature forests despite abundant legumes.

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References

  • Aber J et al (1998) Nitrogen saturation in temperate forest ecosystems—hypotheses revisited. Bioscience 48:921–934

    Article  Google Scholar 

  • Ågren GI, Bosatta E (1988) Nitrogen saturation of terrestrial ecosystems. Environ Pollut 54:185–197

    Article  PubMed  Google Scholar 

  • Alpkem (1992) Ammonia in seawater. In: Document No. 000674. Alpkem, Wilsonville

  • Anderson MD, Ruess RW, Uliassi DD, Mitchell JS (2004) Estimating N2 fixation in two species of Alnus in interior Alaska using acetylene reduction and 15N2 uptake. Ecoscience 11:102–112

    Google Scholar 

  • Barron AR (2007) Patterns and controls on nitrogen fixation in a lowland tropical rain forest, Panama. PhD thesis, Princeton University, Princeton

  • Barron AR, Wurzburger N, Bellinger JP, Wright SJ, Kraepiel AML, Hedin LO (2009) Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat Geosci 2:42–45

    Article  CAS  Google Scholar 

  • Bergersen FJ (1970) Quantitative relationship between nitrogen fixation and acetylene-reduction assay. Aust J Biol Sci 23:1015

    CAS  Google Scholar 

  • Binkley D (1992) Mixtures of nitrogen2-fixing and non-nitrogen2-fixing tree species. In: Cannell M, Malcolm D, Robertson PA (eds) Ecology of mixed species stands. Blackwell, Oxford, pp 99–123

    Google Scholar 

  • Boddey RM, Peoples MB, Palmer B, Dart PJ (2000) Use of the N-15 natural abundance technique to quantify biological nitrogen fixation by woody perennials. Nutr Cycl Agroecosyst 57:235–270

    Article  Google Scholar 

  • Braman RS, Hendrix SA (1989) Nanogram nitrite and nitrate determination in environmental and biological-materials by vanadium(III) reduction with chemi-luminescence detection. Anal Chem 61:2715–2718

    Article  CAS  PubMed  Google Scholar 

  • Bruijnzeel LA (1991) Nutrient input output budgets of tropical forest ecosystems—a review. J Trop Ecol 7:1–24

    Article  Google Scholar 

  • Cavalier J (1992) Fine root biomass and soil properties in a semi-deciduous and a lower montane rain forest in Panama. Plant Soil 142:187–201

    Article  Google Scholar 

  • Cleveland CC et al (1999) Global patterns of terrestrial biological nitrogen (N-2) fixation in natural ecosystems. Glob Biogeochem Cycles 13:623–645

    Article  CAS  Google Scholar 

  • Davidson EA et al (2007) Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447:995

    Article  CAS  PubMed  Google Scholar 

  • de Faria SM, de Lima HC (1998) Additional studies of the nodulation status of legume species in Brazil. Plant Soil 200:185–192

    Article  Google Scholar 

  • Denslow JS, Guzman S (2000) Variation in stand structure, light and seedling abundance across a tropical moist forest chronosequence, Panama. J Veg Sci 11:201–212

    Article  Google Scholar 

  • Forrester DI, Bauhus J, Cowie AL, Vanclay JK (2006) Mixed-species plantations of Eucalyptus with nitrogen-fixing trees: a review. For Ecol Manage 233:211–230

    Article  Google Scholar 

  • Fujikake H, Yashima H, Sato T, Ohtake N, Sueyoshi K, Ohyama T (2002) Rapid and reversible nitrate inhibition of nodule growth and N-2 fixation activity in soybean (Glycine max (L.) Merr.). Soil Sci Plant Nutr 48:211–217

    CAS  Google Scholar 

  • Gehring C, Vlek PLG (2004) Limitations of the N-15 natural abundance method for estimating biological nitrogen fixation in Amazonian forest legumes. Basic Appl Ecol 5:567–580

    Article  CAS  Google Scholar 

  • Gentry AH (1988) Changes in plant community diversity and floristic composition on environmental and geographical gradients. Ann Mo Bot Gard 75:1–34

    Article  Google Scholar 

  • Gerber S, Hedin LO, Oppenheimer M, Pacala SW, Shevliakova E (2010) Nitrogen cycling and feedbacks in a global dynamic land model. Glob Biogeochem Cycles 24:GB1001

    Article  Google Scholar 

  • Gutschick VP (1981) Evolved strategies in nitrogen acquisition by plants. Am Nat 118:607–637

    Article  CAS  Google Scholar 

  • Harms KE, Condit R, Hubbell SP, Foster RB (2001) Habitat associations of trees and shrubs in a 50-ha neotropical plot. J Ecol 89:947–959

    Article  Google Scholar 

  • Hartwig UA (1998) The regulation of symbiotic N2 fixation: a conceptual model of N feedback from the ecosystem to the gene expression level. Perspect Plant Ecol Evol Syst 1:92–120

    Article  Google Scholar 

  • Hedin LO, Vitousek PM, Matson PA (2003) Pathways and implications of nutrient losses during four million years of tropical forest ecosystem development. Ecology 84:2231–2255

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Hilborn R, Mangel M (1997) The ecological detective. Princeton University Press, Princeton

    Google Scholar 

  • Högberg P, Alexander IJ (1995) Roles of root symbioses in african woodland and forest—evidence from N-15 abundance and foliar analysis. J Ecol 83:217–224

    Article  Google Scholar 

  • Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330

    Article  CAS  PubMed  Google Scholar 

  • Ingestad T (1980) Growth, nutrition, and nitrogen-fixation in Grey Alder at varied rate of nitrogen addition. Physiol Plant 50:353–364

    Article  CAS  Google Scholar 

  • Jenny H (1950) Causes of the high nitrogen and organic matter content of certain tropical forest soils. Soil Sci 69:63–69

    Article  CAS  Google Scholar 

  • John R et al (2007) Soil nutrients influence spatial distributions of tropical tree species. Proc Natl Acad Sci USA 104:864–869

    Article  CAS  PubMed  Google Scholar 

  • Kern J, Darwich A, Furch K, Junk WJ (1996) Seasonal denitrification in flooded and exposed sediments from the Amazon floodplain at Lago Camaleão. Microb Ecol 32:47–57

    Article  PubMed  Google Scholar 

  • Koponen P, Nygren P, Domenach AM, Le Roux C, Saur E, Roggy JC (2003) Nodulation and dinitrogen fixation of legume trees in a tropical freshwater swamp forest in French Guiana. J Trop Ecol 19:655–666

    Article  Google Scholar 

  • Kreibich H, Kern J, de Camargo PB, Moreira MZ, Victoria RL, Werner D (2006) Estimation of symbiotic N2 fixation in an Amazon floodplain forest. Oecologia (Berl) 147:359–368

    Article  Google Scholar 

  • McHargue LA (1999) Factors affecting the nodulation and growth of tropical woody legume seedlings. PhD dissertation, Florida International University, Miami

  • McKey D (1994) Legumes and nitrogen: the evolutionary ecology of a nitrogen demanding lifestyle. In: Sprent JI, McKey D (eds) Advances in legume systematics 5: the nitrogen factor. Royal Botanic Garden, Kew, pp 211–228

    Google Scholar 

  • Menge DNL, Hedin LO (2009) Nitrogen fixation in different biogeochemical niches along a 120,000-year chronosequence in New Zealand. Ecology 90:2190–2220

    Article  PubMed  Google Scholar 

  • Menge DNL, Levin SA, Hedin LO (2009) Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences. Am Nat 174:465–477

    Article  PubMed  Google Scholar 

  • Minchin FR, Witty JF, Sheehy JE, Muller M (1983) A major error in the acetylene reduction assay: decreases in nodular nitrogenase activity under assay conditions. J Exp Bot 34:641–649

    Article  CAS  Google Scholar 

  • Moriera FMS, Franco AA (1994) Rhizobia-host interactions in tropical ecosystems in Brazil. In: Sprent JI, McKey D (eds) Advances in legume systematics. Part 5. The nitrogen factor, vol 5. Royal Botanic Gardens, Kew, pp 63–74

    Google Scholar 

  • Moriera FMS, Da Silva MF, De Faria SM (1992) Occurence of nodulation in legume species in the Amazon region of Brazil. New Phytol 121

  • Neill C, Piccolo MC, Cerri CC, Steudler PA, Melilo JA (2006) Soil solution nitrogen losses during clearing of lowland Amazon forest for pasture. Plant Soil 281:233–245

    Article  CAS  Google Scholar 

  • Pastor J, Binkley D (1998) Nitrogen fixation and the mass balances of carbon and nitrogen in ecosystems. Biogeochemistry 43:63–78

    Article  Google Scholar 

  • Pearson HL, Vitousek PM (2001) Stand dynamics, nitrogen accumulation, and symbiotic nitrogen fixation in regenerating stands of Acacia koa. Ecol Appl 11:1381–1394

    Article  Google Scholar 

  • Pons TL, Perreijn K, van Kessel C, Werger MJA (2006) Symbiotic nitrogen fixation in a tropical rainforest: N-15 natural abundance measurements supported by experimental isotopic enrichment. New Phytol 173:154–167

    Article  Google Scholar 

  • Roskoski JP, Van Kessel C (1985) Annual, seasonal and diel variation in nitrogen-fixing activity by Inga jinicuil, a tropical leguminous tree. Oikos 44:306–312

    Article  Google Scholar 

  • Saur E, Bonheme I, Nygren P, Imbert D (1998) Nodulation of Pterocarpus officinalis in the swamp forest of Guadeloupe (Lesser Antilles). J Trop Ecol 14:761–770

    Article  Google Scholar 

  • Sprent JI (2005) Nodulated legume trees. In: Werner D, Newton WE (eds) Nitrogen fixation in agriculture, forestry and the environment. Springer, Netherlands, pp 113–141

    Chapter  Google Scholar 

  • Sprent JI (2009) Legume nodulation. Wiley-Blackwell, United Kingdom, 200 pp

  • Sylvester-Bradley R, De Oliveira LA, Filho JAD, Stjohn TV (1980) Nodulation of legumes, nitrogenase activity of roots and occurrence of nitrogen-fixing Azospirillum sp. in representative soils of central Amazonia. Agro-Ecosystems 6:249–266

    Article  Google Scholar 

  • Van Kessel C, Burris RH (1983) Effect of H-2 evolution on N-15(2) fixation, C2H2 reduction and relative efficiency of leguminous symbionts. Physiol Plant 59:329–334

    Article  Google Scholar 

  • Visser S, Leenders J (2001) The recovery of mineralization in gaps of different size. In: Van Dam O (ed) Forest filled with gaps: effects of gap size on water and nutrient cycling in tropical rain forest. Tropenbos-Guyana Program, Georgetown, pp 149–160

    Google Scholar 

  • Vitousek PM, Field CB (1999) Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46:179–202

    CAS  Google Scholar 

  • Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167

    Article  Google Scholar 

  • Vitousek PM et al (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45

    Article  Google Scholar 

  • Walter CA, Bien A (1989) Aerial root-nodules in the tropical legume, Pentaclethra macroloba. Oecologia 80:27–31

    Article  Google Scholar 

  • Wieder RK, Wright SJ (1995) Tropical forest litter dynamics and dry season irrigation on Barro-Colorado Island, Panama. Ecology 76:1971–1979

    Article  Google Scholar 

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Acknowledgments

We thank S. Pacala for assistance with MLE calculations, J. Dushoff for assistance with other statistics, S.J. Wright for advice and the STRI staff for logistical assistance, the Coley-Kursar lab for assistance with plant identification and L. Stanley, B. Kennedy, E. Dettweiler-Robinson and L. Bennett for assistance in the field. D. Menge and D. Sigman provided helpful comments on early drafts of this manuscript. This work was supported by an NSF-GRF, EPA STAR and STRI-PDF to A.R.B. and grants from the A.W. Mellon Foundation and the NSF (DEB-0614116) to L.O.H.

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Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, Princeton University, Guyot Hall, Princeton, NJ, 08544, USA

    Alexander R. Barron & Lars O. Hedin

  2. Computational Ecology and Environmental Science Group, Microsoft Research, 7 JJ Thomson Avenue, Cambridge, CB3 0FP, UK

    Drew W. Purves

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  1. Alexander R. Barron
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  2. Drew W. Purves
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Correspondence to Alexander R. Barron.

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Communicated by Alan Knapp.

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Barron, A.R., Purves, D.W. & Hedin, L.O. Facultative nitrogen fixation by canopy legumes in a lowland tropical forest. Oecologia 165, 511–520 (2011). https://doi.org/10.1007/s00442-010-1838-3

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