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
Ågren GI, Bosatta E (1988) Nitrogen saturation of terrestrial ecosystems. Environ Pollut 54:185–197
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
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
Bergersen FJ (1970) Quantitative relationship between nitrogen fixation and acetylene-reduction assay. Aust J Biol Sci 23:1015
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
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
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
Bruijnzeel LA (1991) Nutrient input output budgets of tropical forest ecosystems—a review. J Trop Ecol 7:1–24
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
Cleveland CC et al (1999) Global patterns of terrestrial biological nitrogen (N-2) fixation in natural ecosystems. Glob Biogeochem Cycles 13:623–645
Davidson EA et al (2007) Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447:995
de Faria SM, de Lima HC (1998) Additional studies of the nodulation status of legume species in Brazil. Plant Soil 200:185–192
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
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
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
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
Gentry AH (1988) Changes in plant community diversity and floristic composition on environmental and geographical gradients. Ann Mo Bot Gard 75:1–34
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
Gutschick VP (1981) Evolved strategies in nitrogen acquisition by plants. Am Nat 118:607–637
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
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
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
Hedin LO, Brookshire ENJ, Menge DNL, Barron AR (2009) The nitrogen paradox in tropical forest ecosystems. Annu Rev Ecol Evol Syst 40:613–635
Hilborn R, Mangel M (1997) The ecological detective. Princeton University Press, Princeton
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
Houlton BZ, Wang YP, Vitousek PM, Field CB (2008) A unifying framework for dinitrogen fixation in the terrestrial biosphere. Nature 454:327–330
Ingestad T (1980) Growth, nutrition, and nitrogen-fixation in Grey Alder at varied rate of nitrogen addition. Physiol Plant 50:353–364
Jenny H (1950) Causes of the high nitrogen and organic matter content of certain tropical forest soils. Soil Sci 69:63–69
John R et al (2007) Soil nutrients influence spatial distributions of tropical tree species. Proc Natl Acad Sci USA 104:864–869
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
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
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
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
Menge DNL, Hedin LO (2009) Nitrogen fixation in different biogeochemical niches along a 120,000-year chronosequence in New Zealand. Ecology 90:2190–2220
Menge DNL, Levin SA, Hedin LO (2009) Facultative versus obligate nitrogen fixation strategies and their ecosystem consequences. Am Nat 174:465–477
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
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
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
Pastor J, Binkley D (1998) Nitrogen fixation and the mass balances of carbon and nitrogen in ecosystems. Biogeochemistry 43:63–78
Pearson HL, Vitousek PM (2001) Stand dynamics, nitrogen accumulation, and symbiotic nitrogen fixation in regenerating stands of Acacia koa. Ecol Appl 11:1381–1394
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
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
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
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
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
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
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
Vitousek PM, Field CB (1999) Ecosystem constraints to symbiotic nitrogen fixers: a simple model and its implications. Biogeochemistry 46:179–202
Vitousek PM, Sanford RL (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167
Vitousek PM et al (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–45
Walter CA, Bien A (1989) Aerial root-nodules in the tropical legume, Pentaclethra macroloba. Oecologia 80:27–31
Wieder RK, Wright SJ (1995) Tropical forest litter dynamics and dry season irrigation on Barro-Colorado Island, Panama. Ecology 76:1971–1979
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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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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DOI: https://doi.org/10.1007/s00442-010-1838-3