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Relationships among precipitation regime, nutrient availability, and carbon turnover in tropical rain forests

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Abstract

The effect of high precipitation regime in tropical forests is poorly known despite indications of its potentially negative effects on nutrient availability and carbon (C) cycling. Our goal was to determine if there was an effect of high rainfall on nitrogen (N) and phosphorous (P) availability and indexes of C cycling in lowland tropical rain forests exposed to a broad range of mean annual precipitation (MAP). We predicted that C turnover time would increase with MAP while the availability of N and P would decrease. We studied seven Neotropical lowland forests covering a MAP range between 2,700 and 9,500 mm. We used radiocarbon (∆14C) from the atmosphere and respired from soil organic matter to estimate residence time of C in plants and soils. We also used C, N, and P concentrations and the stable isotope ratio of N (δ15N) in live and dead plant tissues and in soils as proxies for nutrient availability. Negative δ15N values indicated that the wettest forests had N cycles that did not exhibit isotope-fractionating losses and were potentially N-limited. Element ratios (N:P and C:P) in senescent leaves, litter, and live roots showed that P resorption increased considerably with MAP, which points towards increasing P-limitation under high MAP regimes. Soil C content increased with MAP but C turnover time only showed a weak relationship with MAP, probably due to variations in soil parent material and age along the MAP gradient. In contrast, comparing C turnover directly to nutrient availability showed strong relationships between C turnover time, N availability (δ15N), and P availability (N:P) in senescent leaves and litter. Thus, an effect of MAP on carbon cycling appeared to be indirectly mediated by nutrient availability. Our results suggest that soil nutrient availability plays a central role in the dynamic of C cycling in tropical rain forests.

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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 Cycles 17:31–32

    Article  Google Scholar 

  • Austin AT, Vitousek PM (1998) Nutrient dynamics on a precipitation gradient in Hawai’i. Oecologia 113:519–529

    Article  Google Scholar 

  • Bauer J, Williams PM, Druffel ERM (1992) Recovery of sub-milligram quantities of carbon dioxide from gas streams by molecular sieve for subsequent determination of isotopic natural abundance. Anal Chem 64:824–827

    Article  CAS  Google Scholar 

  • Bruijnzeel LA, Veneklaas EJ (1998) Climatic conditions and tropical, montane forest productivity: the fog has not lifted yet. Ecology 79:3–9

    Article  Google Scholar 

  • Bruno RD, Da Rocha HR, de Freitas HC, Goulden ML, Miller SD (2006) Soil moisture dynamics in an eastern Amazonian tropical forest. Hydrol Process 20:2477–2489

    Article  Google Scholar 

  • Christensen JH, Hewitson B, Busuioc A, Chen A, Gao X, Held I, Jones R, Kolli RK, Kwon W-T, Laprise R, Magaña Rueda V, Mearns L, Menéndez CG, Räisänen J, Rinke A, Sarr A, Whetton P (2007) Regional climate projections. In: Solomon S et al (eds) Climate change 2007: the physical science basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, pp 847–940

    Google Scholar 

  • Cisneros-Dozal LM, Trumbore S, Hanson PJ (2006) Partitioning sources of soil-respired CO2 and their seasonal variation using a unique radiocarbon tracer. Glob Change Biol 12:194–204

    Article  Google Scholar 

  • Clark DA, Clark DB (1994) Climate induced annual variation in canopy tree growth in a Costa Rican tropical rainforest. J Ecol 82:865–872

    Article  Google Scholar 

  • Clark DA, Piper SC, Keeling CD, Clark DB (2003) Tropical rain forest tree growth and atmospheric carbon dynamics linked to interannual temperature variation during 1984–2000. Proc Natl Acad Sci USA 100:5852–5857

    Article  CAS  PubMed  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 183:980–992

    Article  CAS  PubMed  Google Scholar 

  • Crawford RMM (1982) Physiological responses to flooding. In: Lange OL, Nobel PS, Osmond CB, Ziegler H (eds) Physiological plant ecology, vol 2. Springer, Berlin, pp 453–477

    Google Scholar 

  • Cuevas E, Medina E (1988) Nutrient dynamics within Amazonian forests. II. Fine root growth, nutrient availability and leaf litter decomposition. Oecologia 76:222–235

    Article  Google Scholar 

  • Davidson EA, de Carvalho CJR, Figueira AM, Ishida FY, Ometto J, Nardoto GB, Saba RT, Hayashi SN, Leal EC, Vieira ICG, Martinelli LA (2007) Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447:995–996

    Article  CAS  PubMed  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

    Article  PubMed  Google Scholar 

  • Feeley KJ, Joseph Wright S, Nur Supardi MN, Kassim AR, Davies SJ (2007) Decelerating growth in tropical forest trees. Ecol Lett 10:461–469

    Article  PubMed  Google Scholar 

  • Field CB, Behrenfeld MJ, Randerson JT, Falkowski P (1998) Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281:237–240

    Article  CAS  PubMed  Google Scholar 

  • Gale PM, Gilmour JT (1988) Net mineralization of carbon and nitrogen under aerobic and anaerobic conditions. Soil Sci Soc Am J 52:1006–1010

    Article  CAS  Google Scholar 

  • Grace J, Lloyd J, McIntyre J, Miranda A, Meir P, Miranda H, Moncrieff J, Massheder J, Wright I, Gash J (1995) Fluxes of carbon dioxide and water vapour over an undisturbed tropical forest in south-west Amazonia. Glob Clim Change 2:1–22

    Google Scholar 

  • Graham EA, Mulkey SS, Kitajima K, Phillips NG, Wright SJ (2003) Cloud cover limits net CO2 uptake and growth of a rainforest tree during tropical rainy seasons. Proc Natl Acad Sci USA 100:572–576

    Article  CAS  PubMed  Google Scholar 

  • Handley LL, Austin AT, Stewart GR, Robinson D, Scrimgeour CM, Raven JA, Heaton THE, Schmidt S (1999) The 15N natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Funct Plant Biol 26:185–199

    Google Scholar 

  • Hedin LO (2004) Global organization of terrestrial plant–nutrient interactions. Proc Natl Acad Sci USA 101:10849–10850

    Article  CAS  PubMed  Google Scholar 

  • Hobbie SE, Vitousek PM (2000) Nutrient limitation of decomposition in Hawaiian forests. Ecology 81:1867–1877

    Article  Google Scholar 

  • Hobbie SE, Schimel JP, Trumbore SE, Randerson JR (2000) Controls over carbon storage and turnover in high-latitude soils. Glob Change Biol 6:196–210

    Article  Google Scholar 

  • Högberg P (1990) Forests losing large quantities of nitrogen have elevated 15N:14N ratios. Oecologia 84:229–231

    Google Scholar 

  • Högberg P (1997) Tansley review no. 95 15N natural abundance in soil–plant systems. New Phytol 137:179–203

    Article  Google Scholar 

  • Högberg P, Nordgren A, Buchmann N, Taylor AFS, Ekblad A, Hogberg M, Nyberg G, Ottosson-Lofvenius M, Read DJ (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411:789–792

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Jenny H (1941) Factors of soil formation. McGraw-Hill, New York

    Google Scholar 

  • Jones JB, Case BW (1996) Soil testing and plant analysis no. 3. In: Sparks DL (ed) Methods of soil analysis part 3: chemical methods. Soil Science Society of America, Madison, pp 389–415

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  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 

  • Levin I, Hesshaimer V (2000) Radiocarbon—a unique tracer of global carbon cycle dynamics. Radiocarbon 42:69–80

    CAS  Google Scholar 

  • Mack MC, Schuur EAG, Bret-Harte MS, Shaver GR, Chapin III FS (2004) Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431:440–443

    Article  CAS  PubMed  Google Scholar 

  • Magnusson T (1992) Studies of the soil atmosphere and related physical site characteristics in mineral forest soils. J Soil Sci 43:767–790

    Article  CAS  Google Scholar 

  • Malhi Y, Phillips OL (2004) Tropical forests and global atmospheric change: a synthesis. Philos Trans R Soc Lond B 359:549–555

    Article  CAS  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

    CAS  Google Scholar 

  • McGroddy ME, Daufresne T, Hedin L (2004) Scaling of C:N:P stoichiometry in forests worldwide: implications of terrestrial redfield-type ratios. Ecology 85:2390–2401

    Article  Google Scholar 

  • Melillo JM, McGuire AD, Kicklighter DW, Moore B III, Vorosmarty CJ, Schloss AL (1993) Global climate change and terrestrial net primary production. Nature 363:234–240

    Article  CAS  Google Scholar 

  • Miller AJ, Schuur EAG, Chadwick OA (2001) Redox control of phosphorus pools in Hawaiian montane forest soils. Geoderma 102:219–237

    Article  CAS  Google Scholar 

  • Myneni RB, Yang W, Nemani RR, Huete AR, Dickinson RE, Knyazikhin Y, Didan K, Fu R, Negron Juarez RI, Saatchi SS, Hashimoto H, Ichii K, Shabanov NV, Tan B, Ratana P, Privette JL, Morisette JT, Vermote EF, Roy DP, Wolfe RE, Friedl MA, Running SW, Votava P, El-Saleous N, Devadiga S, Su Y, Salomonson VV (2007) Large seasonal swings in leaf area of Amazon rainforests. Proc Natl Acad Sci USA 104:4820–4823

    Article  CAS  PubMed  Google Scholar 

  • Nemani RR, Keeling CD, Hashimoto H, Jolly WM, Piper SC, Tucker CJ, Myneni RB, Running SW (2003) Climate-driven increases in global terrestrial net primary production from 1982 to 1999. Science 300:1560–1563

    Article  CAS  PubMed  Google Scholar 

  • Nepstad DC, Moutinho P, Dias MB, Davidson E, Cardinot G, Markewitz D, Figueiredo R, Vianna N, Chambers J, Ray D, Guerreiros JB, Lefebvre P, Sternberg L, Moreira M, Barros L, Ishida FY, Tohlver I, Belk E, Kalif K, Schwalbe K (2002) The effects of partial throughfall exclusion on canopy processes, aboveground production, and biogeochemistry of an Amazon forest. J Geophys Res-Atmos 107:8085

    Article  Google Scholar 

  • Nisbet TR, Mullins CE, Macleod DA (1989) The variation of soil-water regime, oxygen status and rooting pattern with soil type under sitka spruce. J Soil Sci 40:183–197

    Article  Google Scholar 

  • Ometto JPHB, Ehleringer JR, Domingues TF, Berry JA, Ishida FY, Mazzi E, Higuchi N, Flanagan LB, Nardoto GB, Martinelli LA (2006) The stable carbon and nitrogen isotopic composition of vegetation in tropical forests of the Amazon Basin, Brazil. Biogeochemistry 79:251–274

    Article  CAS  Google Scholar 

  • Pardo L, Templer P, Goodale C, Duke S, Groffman P, Adams M, Boeckx P, Boggs J, Campbell J, Colman B, Compton J, Emmett B, Gundersen P, Kjønaas J, Lovett G, Mack M, Magill A, Mbila M, Mitchell M, McGee G, McNulty S, Nadelhoffer K, Ollinger S, Ross D, Rueth H, Rustad L, Schaberg P, Schiff S, Schleppi P, Spoelstra J, Wessel W (2006) Regional assessment of N saturation using foliar and root δ15N. Biogeochemistry 80:143–171

    Article  Google Scholar 

  • Ponnamperuma FN (1972) The chemistry of submerged soils. Adv Agron 24:29–96

    Article  CAS  Google Scholar 

  • Post WM, Emanuel WR, Zinke PJ, Stangenberger AG (1982) Soil carbon pools and world life zones. Nature 298:156–159

    Article  CAS  Google Scholar 

  • Poveda G, Mesa OJ (2000) On the existence of Lloró (the rainest locality on Earth): enhanced ocean–land–atmosphere interaction by a low level jet. Geophys Res Lett 27:1675–1678

    Article  Google Scholar 

  • Radulovich R, Sollins P (1991) Nitrogen and phosphorus leaching in zero-tension drainage from a humid tropical soil. Biotropica 23:84–87

    Article  Google Scholar 

  • Richards JH, Caldwell MM (1987) Hydraulic lift: substantial nocturnal water transport between soil layers by Artemesia tridentata roots. Oecologia 73:486–489

    Article  Google Scholar 

  • Saleska SR, Miller SD, Matross DM, Goulden ML, Wofsy SC, da Rocha HR, de Camargo PB, Crill P, Daube BC, de Freitas HC, Hutyra L, Keller M, Kirchhoff V, Menton M, Munger JW, Pyle EH, Rice AH, Silva H (2003) Carbon in amazon forests: unexpected seasonal fluxes and disturbance-induced losses. Science 302:1554–1557

    Article  CAS  PubMed  Google Scholar 

  • Santiago LS, Kitajima K, Wright SJ, Mulkey SS (2004) Coordinated changes in photosynthesis, water relations and leaf nutritional traits of canopy trees along a precipitation gradient in lowland tropical forest. Oecologia 139:495–502

    Article  PubMed  Google Scholar 

  • Schuur EAG (2001) The effect of water on decomposition dynamics. Ecosystems 4:259–273

    Article  CAS  Google Scholar 

  • Schuur EAG (2003) Productivity and global climate revisted: the sensitivity of tropical forest growth to precipitation. Ecology 84:1165–1170

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Schuur EAG, Trumbore SE (2006) Partitioning sources of soil respiration in boreal black spruce forest using radiocarbon. Glob Change Biol 12:165–176

    Article  Google Scholar 

  • Schuur EAG, Chadwick OA, Matson PA (2001) Carbon cycling and soil carbon storage in mesic to wet Hawaiian montane forests. Ecology 82:3182–3196

    Article  Google Scholar 

  • Scott DF (1993) The hydrological effects of fire in South African mountain catchments. J Hydrol 150:409–432

    Article  Google Scholar 

  • Silver WL, Lugo AE, Keller M (1999) Soil oxygen availability and biogeochemistry along rainfall and topographic gradients in upland wet tropical forest soils. Biogeochemistry 44:301–328

    Google Scholar 

  • Stuiver M, Polach H (1977) Reporting of 14C data. Radiocarbon 19:355–363

    Google Scholar 

  • Tanner EVJ, Vitousek PM, Cuevas E (1998) Experimental investigation of nutrient limitation of forest growth on wet tropical mountains. Ecology 79:10–22

    Article  Google Scholar 

  • ter Steege H, Pitman NCA, Phillips OL, Chave J, Sabatier D, Duque A, Molino JF, Prévost MF, Spichiger R, Castellanos H, vH P, Vásquez R (2006) Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 443:444–447

    Article  CAS  PubMed  Google Scholar 

  • Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar N:P ratios in tropical forests. Ecology 88:107–118

    Article  PubMed  Google Scholar 

  • Trumbore S (2000) Age of soil organic matter and soil respiration: radiocarbon constraints on belowground C dynamics. Ecol Appl 10:399–411

    Article  Google Scholar 

  • Trumbore S (2009) Radiocarbon and soil carbon dynamics. Annu Rev Earth Planet Sci 37:47–66

    Article  CAS  Google Scholar 

  • Updegraff K, Pastor J, Bridgham SD, Johnston CA (1990) Environmental and substrate controls over carbon and nitrogen mineralization in northern wetlands. Ecol Appl 5:151–163

    Article  Google Scholar 

  • Vitousek PM (1982) Nutrient cycling and nutrient use efficiency. Am Nat 119:553–572

    Article  Google Scholar 

  • Vitousek PM (1984) Litterfall, nutrient cycling, and nutrient limitation in tropical forests. Ecology 65:285–298

    Article  CAS  Google Scholar 

  • Vitousek PM (2004) Nutrient cycling and limitation: Hawai’i as a model system. Princeton University Press, USA

    Google Scholar 

  • Vitousek PM, Farrington H (1997) Nutrient limitation and soil development: experimental test of a biogeochemical theory. Biogeochemistry 37:63–75

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Vogel JS (1992) A rapid method for preparation of biomedical targets for AMS. Radiocarbon 34:344–350

    Google Scholar 

  • Walker T, Syers J (1976) The fate of phosphorus during pedogenesis. Geoderma 15:1–19

    Article  CAS  Google Scholar 

  • Wright SJ, Carrasco C, Calderon O, Paton S (1999) The El Niño southern oscillation, variable fruit production, and famine in a tropical forest. Ecology 80:1632–1647

    Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas ML, Niinemets U, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was funded by a grant from the Andrew W. Mellon Foundation to E.A.G.S. We thank Alfredo Navas, Estebana Ortiz, Yan Ramos and Lou Santiago for their help in the field. We are grateful to Grace Crummer, Lauren Thorton, Kate Welch, Koushik Dutta and Melanie DesRochers for their help in different phases of this study. Jason Vogel gave valuable insights during the analysis of the data. We thank Deborah and David Clark (Organization for Tropical Studies, La Selva), Alicia Ríos and Yan Ramos (Universidad Tecnológica del Chocó), José Sinisterra (Ministerio de Ambiente, Vivienda y Desarrollo) and the Smithsonian Tropical Research Institute for logistical support. The meteorological data for Colombia were obtained from the Institute of Hidrology, Meteorology and Environmental Studies of Colombia (IDEAM) thanks to a cooperative agreement with the International Center for Physics (Convenio CIF-IDEAM). This study comply with the laws of the countries at the time in which sampling took place. This manuscript benefited from comments by Deborah Clark, Amy Austin and three anonymous reviewers.

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  1. Department of Biology, University of Florida, 220 Bartram Hall, Gainesville, FL, 32611-8526, USA

    Juan M. Posada & Edward A. G. Schuur

  2. Facultad de Ciencias Naturales y Matemáticas, Universidad del Rosario, Cr. 24 No. 63C-69, Bogotá, D.C., Colombia

    Juan M. Posada

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Correspondence to Edward A. G. Schuur.

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Communicated by Amy Austin.

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Posada, J.M., Schuur, E.A.G. Relationships among precipitation regime, nutrient availability, and carbon turnover in tropical rain forests. Oecologia 165, 783–795 (2011). https://doi.org/10.1007/s00442-010-1881-0

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