Abstract
By analyzing 6,480 tree leaf samples from 57 sites within Brazilian biomes, we considered whether vegetation types in terrestrial ecosystems reflect biogeochemical diversity and whether they fit into a leaf economics spectrum (LES). To achieve this, we investigated the relations among leaf carbon (C) and nitrogen (N) concentrations, their isotope natural abundance and C:N ratio. In addition, we tested their correlations with mean annual temperature (MAT) and precipitation (MAP), as climatic factors. We found consistent differences in the C and N concentrations and their isotopic composition among the vegetation types. MAP is the main climatic driver of changes in N, C:N ratio, δ15N, and δ13C, correlating negatively with N and positively with C:N ratio. These relations show that these biomes follow an LES. The Caatinga had the highest δ15N values, suggesting that N residence time in soil is longer due to low leaching and plant uptake. We observed that MAP is not the only factor influencing δ13C values in different biomes; instead canopy effect probably explains the highest values observed in the Cerrado. Our results reinforce earlier findings that life diversity in the tropics reflects biogeochemistry diversity and leaf δ15N opens the possibility for investigating plant trade-offs dictated by the LES. Finally, we expect our findings to contribute to a better understanding of the tropics in global climate models.
Similar content being viewed by others
Data availability
The complete data set used in this paper can be found at the following link: https://doi.org/10.17632/38npddpnts.1
Change history
30 December 2020
A Correction to this paper has been published: https://doi.org/10.1007/s10533-020-00735-x
References
Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608. https://doi.org/10.2307/2261481
Aerts R, Chapin FSIII (1999) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67. https://doi.org/10.1016/S0065-2504(08)60016-1
Amundson R, Austin AT, Schuur EA, 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 17:1031. https://doi.org/10.1029/2002GB001903
Anav A, Friedlingstein P, Beer C, Ciais P, Harper A, Jones C, Murray-Tortarolo G, Papale D, Parazoo NC, Peylin P, Piao S, Sitch S, Viovy N, Wiltshire A, Zhao M (2015) Spatiotemporal patterns of terrestrial gross primary production: a review. Rev Geophys 53:785–818. https://doi.org/10.1002/2015RG000483
Aranibar JN, Otter L, Macko AS, Feral CJW, Epstein HE, Dowty PR, Eckardt F, Shugart HH, Swap RJ (2004) Nitrogen cycling in the soil-plant system along a precipitation gradient in the Kalahari sands. Glob Chang Biol 10:359–373. https://doi.org/10.1046/j.1529-8817.2003.00698.x
Arruda DM, Fernandes-Filho EI, Solar RRC, Schaefer CEGR (2017) Combining climatic and soil properties better predicts covers of Brazilian biomes. Sci Nat 104:32. https://doi.org/10.1007/s00114-017-1456-6
Asner GP, Martin RE (2016) Convergent elevation trends in canopy chemical traits of tropical forests. Glob Chang Biol 22:2216–2227. https://doi.org/10.1111/gcb.13164
Austin AT, Sala OE (1999) Foliar delta15N is negatively correlated with rainfall along the IGBP transect in Australia. Aust J Plant Physiol 26:293–295
Austin AT, Vitousek PM (1998) Nutrient dynamics on a precipitation gradient in Hawaii. Oecologia 113:519–529. https://doi.org/10.1007/s004420050405
Balzotti CS, Asner GP, Taylor PG, Cleveland CC, Cole R, Martin RE, Nasto M, Osborne BB, Porder S, Townsend AR (2016) Environmental controls on canopy foliar nitrogen distributions in a Neotropical lowland forest. Ecol Appl 26:2451–2464. https://doi.org/10.1002/eap.1408
Barros V, Melo A, Santos M, Nogueira L, Frosi G, Santos MG (2020) Different resource-use strategies of invasive and native woody species from a seasonally dry tropical forest under drought stress and recovery. Plant Physiol Biochem 147:181–190. https://doi.org/10.1016/j.plaphy.2019.12.018
Basu S, Ghosh S, Sanyal P (2019) Spatial heterogeneity in the relationship between precipitation and carbon isotopic discrimination in C3 plants: inferences from a global compilation. Glob Planet Chang 176:123–131. https://doi.org/10.1016/j.gloplacha.2019.02.002
Bonilha RM, Casagrande JC, Soares MR, Reis-Duarte RM (2012) Characterization of the soil fertility and root system of restinga forests. R Bras Ci Solo 36:1804–1813. https://doi.org/10.1590/S0100-06832012000600014
Brazil Flora Group (2015) Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia 66:1085–1113. https://doi.org/10.1590/2175-7860201566411
Brienen RJW, Phillips OL, Feldpausch TR, Gloor E, Baker TR, Lloyd J, Lopez-Gonzalez G, Monteagudo-Mendoza A, Malhi Y, Lewis SL, Vásquez Martinez R, Alexiades M, Álvarez Dávila E, Alvarez-Loayza P, Andrade A, Aragão LEOC, Araujo-Murakami A, Arets EJMM, Arroyo L, Aymard JAC, Bánki OS, Baraloto C, Barroso J, Bonal D, Boot RGA, Camargo JLC, Castilho CV, Chama V, Chao KJ, Chave J, Comiskey JA, Cornejo Valverde F, da Costa L, de Oliveira EA, Di Fiore A, Erwin TL, Fauset S, Forsthofer M, Galbraith DR, Grahame ES, Groot N, Hérault B, Higuchi N, Honorio Coronado EN, Keeling H, Killeen TJ, Laurance WF, Laurance S, Licona J, Magnussen WE, Marimon BS, Marimon-Junior BH, Mendoza C, Neill DA, Nogueira EM, Núñez P, Pallqui Camacho NC, Parada A, Pardo-Molina G, Peacock J, Peña-Claros M, Pickavance GC, Pitman NCA, Poorter L, Prieto A, Quesada CA, Ramírez F, Ramírez-Angulo H, Restrepo Z, Roopsind A, Rudas A, Salomão RP, Schwarz M, Silva N, Silva-Espejo JE, Silveira M, Stropp J, Talbot J, ter Steege H, Teran-Aguilar J, Terborgh J, Thomas-Caesar R, Toledo M, Torello-Raventos M, Umetsu RK, van der Heijden GMF, van der Hout P, Guimarães Vieira IC, Vieira SA, Vilanova E, Vos VA, Zagt RJ (2015) Long-term decline of the Amazon carbon sink. Nature 519:344–348. https://doi.org/10.1038/nature14283
Buchmann N, Guehl J, Barigah T, Ehleringer JR (1997) Interseasonal comparison of CO2 concentrations, isotopic composition, and carbon dynamics in an Amazonian rainforest (French Guiana). Oecologia 110:120–131. https://doi.org/10.1007/s004420050140
Bustamante MMC, Martinelli LA, Silva DA, Camargo PB, Klink CA, Domingues TF, Santos RV (2004) 15N natural abundance in woody plants and soils of the central brazilian savanas (cerrado). Ecol Appl 14:200–213. https://doi.org/10.1890/01-6013
Climate-Data (2020) Dados climáticos para cidades mundiais. ©Climate-Data.org. https://pt.climate-data.org/. Accessed 20 Apr 2020.
Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, Ter Steege H, Morgan HD, Van Der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380. https://doi.org/10.1071/BT02124
Cox PM, Betts RA, Jones CD, Spall SA, Totterdell IJ (2000) Acceleration of global warming due to carbon-cycle feedbacks in a coupled climate model. Nature 408:184–187. https://doi.org/10.1038/35041539
Craine JM, Elmore AJ, Aidar MPM, Bustamante M, Dawson TD, Hobbie EA, Kahmen A, Mack MC, McLauchlan KK, Michelsen A, Nardoto GB, Pardo LH, Pefiuelas J, Reich PB, Schuur EAG, Stock WD, Ternpler 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. https://doi.org/10.1111/j.1469-8137.2009.02917.x
Currie DJ (1991) Energy and large-scale patterns of animal- and plant speciesrichness. Am Nat 137:27–49
Currie DJ, Paquin V (1987) Large-scale biogeographical patterns of species richness of tree. Nature 329:326–327. https://doi.org/10.1038/329326a0
Davidson EA, Carvalho CJR, Figueira AM, Ishida FY, Ometto JPHB, Nardoto GB, Sabá RT, Hayashi SN, Leal EC, Vieira ICG, Martinelli LA (2007) Recuperation of nitrogen cycling in Amazonian forests following agricultural abandonment. Nature 447:995–999. https://doi.org/10.1038/nature05900
DeFries RS, Foley JA, Asner GP (2004) Land-use choices: balancing human needs and ecosystem function. Front Ecol Environ 2:249–257. https://doi.org/10.1890/1540-9295(2004)002[0249:LCBHNA]2.0.CO;2
Díaz S, Cabido M (2001) Vive la différence: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655. https://doi.org/10.1016/S0169-5347(01)02283-2
Diefendorf AF, Mueller KE, Wing SL, Koch PL, Freeman KH (2010) Global patterns in leaf 13C discrimination and implications for studies of past and future climate. Proc Natl Acad Sci USA 107(13):5738–5743. https://doi.org/10.1073/pnas.0910513107
Domingues TF, Ometto JPHB, Nepstad DC, Brando PM, Martinelli LA, Ehleringer JR (2018) Ecophysiological plasticity of Amazonian trees to long-term drought. Oecologia 187:933–940. https://doi.org/10.1007/s00442-018-4195-2
Duvert C, Hutley LB, Beringer J, Bird MI, Birkel C, Maher DT, Northwood M, Rudge M, Setterfield SA, Wynn JG (2020) Net landscape carbon balance of a tropical savanna: relative importance of fire and aquatic export in offsetting terrestrial production. Glob Chang Biol 26:5899–5913. https://doi.org/10.1111/gcb.15287
Ehleringer JR, Hall AE, Farquhar GD (1993) Stable isotopes and plant carbon: water relations. Academic Press, London
Eiten G (1972) The Cerrado vegetation of Brazil. Bot Rev 38:201–341. https://doi.org/10.1007/BF02859158
Evans TL, Costa M, Tomas WM, Camilo AR (2014) Large-scale habitat mapping of the Brazilian Pantanal wetland: a synthetic aperture radar approach. Remote Sens Environ 155:89–108. https://doi.org/10.1016/j.rse.2013.08.051
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345. https://doi.org/10.1146/annurev.pp.33.060182.001533
Farquhar GD, Ehleringer JR, Hubick KT (1989a) Carbon isotope discrimination and photosynthesis. Annu Rev Plant Phyiol 40:503–537. https://doi.org/10.1146/annurev.pp.40.060189.002443
Farquhar GD, Hubick KT, Condon AG, Richards RA (1989b) Carbon isotope fractionation and plant water-use efficiency. In: Rundel PW, Ehleringer JR, Nagy KA (eds) Stable isotopes in ecological research. Springer, New York, pp 21–40
Field R, O’Brien EM, Whittaker RJ (2005) Global models for prediction woody plant richness from climate: development and evaluation. Ecology 86:2263–2277. https://doi.org/10.1890/04-1910
Freitas ADS, Sampaio EVSB, Menezes RSC, Tiessen H (2010a) 15N natural abundance of non-fixing woody species in the Brazilian dry forest (caatinga). Isot Environ Healt S 56:210–218. https://doi.org/10.1080/10256016.2010.488805
Freitas ADS, Sampaio EVSB, Santos CERS, Fernandes AR (2010b) Biological nitrogen fixation in tree legumes of the Brazilian semi-arid caatinga. J Arid Environ 74:344–349. https://doi.org/10.1016/j.jaridenv.2009.09.018
Freitas ADS, Sampaio EVSB, Ramos APS, Barbosa MRV, Lyra RP, Araújo EL (2015) Nitrogen isotopic patterns in tropical forests along a rainfall gradient in Northeast Brazil. Plant Soil 391:109–122. https://doi.org/10.1007/s11104-015-2417-5
Friedlingstein P, Cox P, Betts R, Bopp L, von Bloh W, Brovkin V, Cadule P, Doney S, Eby M, Fung I, Bala G, John J, Jones C, Joos F, Kato T, Kawamiya M, Knorr W, Lindsay K, Matthews HD, Raddatz T, Rayner P, Reich C, Roeckner E, Schnitzler KG, Schnur R, Strassmann K, Weaver AJ, Yoshikawa C, Zeng N (2006) Climate Carbon cycle feedback analysis: results from the C4MIP model intercomparison. J Clim 19:3337–3353. https://doi.org/10.1175/JCLI3800.1
Friedlingstein P, Jones MW, O’Sullivan M, Andrew RM, Hauck J, Peters GP, Peters W, Pongratz J, Sitch S, Quéré CL, Bakker DCE, Canadell JG, Ciais P, Jackson RB, Anthoni P, Barbero L, Bastos A, Bastrikov V, Becker M, Bopp L, Buitenhuis E, Chandra N, Chevallier F, Chini LP, Currie KI, Feely RA, Gehlen M, Gilfillan D, Gkritzalis T, Goll DS, Gruber N, Gutekunst S, Harris I, Haverd V, Houghton RA, Hurtt G, Ilyina T, Jain AK, Joetzjer E, Kaplan JO, Kato E, Goldewijk KK, Korsbakken JI, Landschützer P, Lauvset SK, Lefèvre N, Lenton A, Lienert S, Lombardozzi D, Marland G, McGuire PC, Melton JR, Metz N, Munro DR, Nabel JEMS, Nakaoka SI, Neill C, Omar AM, Ono T, Peregon A, Pierrot D, Poulter B, Rehder G, Resplandy L, Robertson E, Rödenbeck C, Séférian R, Schwinger J, Smith N, Tans PP, Tian H, Tilbrook B, Tubiello FN, van der Werf GR, Wiltshire AJ, Zaehle S (2019) Global carbon budged 2019. Earth Syst Sci Data 11:1783–1838. https://doi.org/10.5194/essd-11-1783-2019
Furian S, Barbiéro L, Boulet R (1999) Organisation of the soil mantle in tropical southeastern Brazil (Serra do Mar) in relation to landslides processes. Catena 38:65–83. https://doi.org/10.1016/S0341-8162(99)00015-6
Fyllas NM, Patiño S, Baker TR, Nardoto GB, Martinelli LA, Quesada CA, Paiva R, Schwarz M, Horna V, Mercado LM, Santos A, Arroyo L, Jiménez EM, Luizão FJ, Neill DA, Silva N, Prieto A, Rudas A, Silveira M, Vieira ICG, Lopez-Gonzalez G, Malhi Y, Phillips OL, Lloyd J (2009) Basin-wide variations in foliar properties of Amazonian forest: phylogeny, soils and climate. Biogeosciences 6:2677–2708. https://doi.org/10.5194/bg-6-2677-2009
Han W, Fang J, Guo D, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168:377–385. https://doi.org/10.1111/j.1469-8137.2005.01530.x
Handley LL, Austin AT, Robinson D, Scrimgeour CM, Raven JA, Heaton THE, Schmidt S, Stewart GR (1999) The 15N natural abundance (δ15N) of ecosystem samples reflects measures of water availability. Aust J Plant Physiol 26:185–199. https://doi.org/10.1071/PP98146
Heaton TH (1987) The 15N/14N ratios of plants in South Africa and Namibia: relationship to climate and coastal/saline environments. Oecologia 74:236–246. https://doi.org/10.1007/BF00379365
Hilton RG, Galy A, West AJ, Hovius N, Roberts GG (2013) Geomorphic control on the δ15N of mountain forests. Biogeosciences 10:1693–1705. https://doi.org/10.5194/bg-10-1693-2013
Hobbie EA, Högberg P (2012) Nitrogen isotopes link mycorrhizal fungi and plants to nitrogen dynamics. New Phytol 196:367–382. https://doi.org/10.1111/j.14698137.2012.04300.x
Hobbie EA, Macko SA, Shugart HH (1999) Insights into nitrogen and carbon dynamics of ectomycorrhizal and saprotrophic fungi from isotopic evidence. Oecologia 118:353–360. https://doi.org/10.1007/s004420050736
Högberg P (1997) Transley review no. 95 15N natural abundance in soil-plant systems. New Phytol 137:179–203. https://doi.org/10.1046/j.1469-8137.1997.00808.x
Högberg P, Johannisson C (1993) 15N abundance of forests is correlated with losses of nitrogen. Plant Soil 157:147–150. https://doi.org/10.1007/BF02390237
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. https://doi.org/10.1073/pnas.0510185103
Houlton BZ, Sigman DM, Schuur EAG, Hedin LO (2007) A climate-driven switch in plant nitrogen acquisition within tropical forest communities. Proc Natl Acad Sci USA 104:8902–8906. https://doi.org/10.1073/pnas.0609935104
Huntingford C, Zelazowski P, Galbraith D, Mercado LM, Sitch S, Fisher R, Lomas M, Walker AP, Jones CD, Booth BBB, Malhi Y, Hemming D, Kay G, Good P, Lewis SL, Phillips OL, Atkin OK, Lloyd J, Gloor E, Zaragoza-Castells J, Meir P, Betts R, Harris PP, Nobre C, Marengo J, Cox PM (2013) Simulated resilience of tropical rainforests to CO2-induced climate change. Nat Geosci 6:268–273. https://doi.org/10.1038/ngeo1741
IBGE – Instituto Brasileiro de Geografia e Estatística (2012) Manual técnico da vegetação brasileira. IBGE, Rio de Janeiro
Joly CA, Assis MA, Bernacci LC, Tamashiro JY, Campos MCR, Gomes JAMA, Lacerda MS, Santos FAM, Pedroni F, Pereira LS, Padgurschi MCG, Prata BEM, Ramos E, Torres RB, Rochelle A, Martins FR, Alvez LF, Vieira SA, Martinelli LA, Camargo PB, Aidar MPM, Eisenlohr PV, Simões E, Villani JP, Belinello R (2012) Floristic and phytosociology in permanent plots of the Atlantic Rainforest along an altitudinal gradiente in southeastern Brazil. Biota Neotrop 12. https://doi.org/10.1590/S1676-06032012000100012
Joly CA, Padgurschi MCG, Pires APF, Agostinho AA, Marques AC, Amaral AG, Cervone COFO, Adams C, Baccaro FB, Sparovek G, Overbeck GE, Espindola GM, Vieira ICG, Metzger JP, Sabino J, Farinaci JS, Queiroz LP, Gomes LC, da Cunha MMC, Piedade MTF, Bustamante MMC, May P, Fearnside P, Prado RB, Loyola RD (2019) Apresentando o Diagnóstico Brasileiro de Biodiversidade e Serviços Ecossistêmicos. In: Joly CA, Scarano FR, Seixas CS, Metzger JP, Ometto JP, Bustamante MMC, Padgurschi MCG, Pires APF, Castro PFD, Gadda T, Toledo P (eds.) 1° Diagnóstico Brasileiro de Biodiversidade e Serviços Ecossistêmicos, Editora Cubo, São Carlos, pp 351. . https://doi.org/10.4322/978-85-60064-88-5
Kattge J, Díaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G, Garnier E, Westoby M, Reich PB, Wright IJ, Cornelissen JHC, Violle C, Harrison SP, van Bodegom PM, Reichstein M, Enquist BJ, Soudzilovskaia NA, Ackerly DD, Anand M, Atkin O, Bahn M, Baker TR, Baldocchi D, Bekker R, Blanco CC, Blonder B, Bond WJ, Bradstock R, Bunker DE, Casanove F, Cavender-Bares J, Chambers JQ, Chapin FD, Chave J, Coomes D, Cornwell CJM, Dobrin BH, Duarte L, Durka W, Elser J, Esser G, Estiarte M, Fagan WF, Fang J, Fernández Mendez F, Fidelis A, Finegan B, Flores O, Ford H, Frank D, Freschet GT, Fyllas NM, Gallagher RV, Green WA, Gutierrez AG, Hickler T, Higgins SI, Hodgson JG, Jalili A, Jansen S, Joly CA, Kerkhoff AJ, Kirkup D, Kitajima K, Kleyer M, Klotz S, Knops JMH, Kramer K, Kühn I, Kurokawa H, Laughlin D, Lee TD, Leishman M, Lens F, Lenz T, Lewis SL, Lloyd J, Llusià J, Louault F, Ma S, Mahecha MD, Manning P, Massad T, Medlyn BE, Messier J, Moles AT, Müller SC, Nadrowski K, Naeem S, Niinemets Ü, Nöllert S, Nüske A, Ogaya R, Oleksyn J, Onipchenko VG, Onoda Y, Ordoñez J, Overbeck G, Ozinga WA, Patiño S, Paula S, Pausas JG, Peñuelas J, Phillips OL, Pillar V, Poorter H, Poorter L, Poschlod P, Prinzing A, Proulx R, Rammig A, Reinsch S, Reu B, Sack L, Salgado-Negret B, Sardans J, Shiodera S, Shipley B, Siefert A, Sosinski E, Soussana JF, Swaine E, Swenson N, Thompson K, Thorton P, Waldram M, Weiher E, White M, White S, Wright SJ, Yguel B, Zaehle S, Zanne AE, Wirth C (2011) Try – a global database of plant traits. Glob Chang Biol 17:2905–2935. https://doi.org/10.1111/j.1365-2486.2011.02451.x
Kohn MJ (2010) Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo)ecology and (paleo)climate. Proc Natl Acad Sci USA 107:19691–19695. https://doi.org/10.1073/pnas.1004933107
Kreft H, Jetz W (2007) Global patterns and determinants of vascular plant diversity. Proc Natl Acad Sci USA 104:5925–5930. https://doi.org/10.1073/pnas.0608361104
Lenton TM, Held H, Kriegler E, Hall JW, Lucht W, Rahmstorf S, Schellnhuber HJ (2008) Tipping elements in the Earth’s climate system. Proc Natl Acad Sci USA 105:1786–1793. https://doi.org/10.1073/pnas.0705414105
Lins SRM, Coletta LD, Ravagnani EC, Gragnani JG, Mazzi EA, Martinelli LA (2016) Stable carbon composition of vegetation and soils across an altitudinal range in the coastal Atlantic Forest of Brazil. Trees 30:1315–1329. https://doi.org/10.1007/s00468-016-1368-7
Lovejoy TE, Nobre C (2019) Amazon tipping point: last chance for action. Sci Adv 5:eaba2949. https://doi.org/10.1126/sciadv.aba2949
Luizão RCC, Luizão FJ, Paiva RQ, Monteiro TF, Sousa LS, Kruijt B (2004) Variation of carbon and nitrogen cycling processes along a topographic gradient in a central Amazonian forest. Glob Chang Biol 10:592–600. https://doi.org/10.1111/j.1529-8817.2003.00757.x
Machado ICS, Barros LM, Sampaio EVSB (1997) Phenology of Caatinga species at Serra Talhada, PE. Biotropica 29:57–68
Mardegan SF, Nardoto GB, Higuchi N, Moreira MZ, Martinelli LA (2009) Nitrogen availability patterns in white-sand vegetations of Central Brazilian Amazon. Trees 23:479–488. https://doi.org/10.1007/s00468-008-0293-9
Martins SC, Neto ES, Piccolo MC, Almeida DQA, Camargo PB, Carmo JB, Porder S, Lins SRM, Martinelli LA (2015) Soil texture and chemical characteristics along an elevation range in the coastal Atlantic forest of Southeast Brazil. Geoderma Reg 5:106–116. https://doi.org/10.1016/j.geodrs.2015.04.005
Medina E, Minchin P (1980) Stratification of δ13C values of leaves in Amazonian rain forests. Oecologia 45:377–378. https://doi.org/10.1007/BF00540209
Mendonça BAF, Filho EIF, Schaefer CEGR, Mendonça JGF, Vasconcelos BNF (2017) Soil-vegetation relationships and community structure in a “terra-firme”-white-sand vegetation gradient in Viruá National Park, northern Amazon, Brazil. An Acad Bras Cienc 89:1269–1293. https://doi.org/10.1590/0001-3765201720160666
Miatto RC, Wright IJ, Batalha MA (2016) Relationships between soil nutrient status and nutrient-related leaf traits in Brazilian cerrado and seasonal forest communities. Plant Soil 404:13–33. https://doi.org/10.1007/s11104-016-2796-2
Michelsen A, Schmidt IK, Jonasson S, Quarmby C, Sleep D (1996) Leaf 15N abundance of subartic plants provides field evidence that ericoid, ectomycorrhizal and non-and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia 105:53–63. https://doi.org/10.1007/BF00328791
Moles AT, Perkins SE, Laffan SW, Flores-Moreno H, Awasthy M, Tindall ML, Sack L, Pitman A, Kattge J, Aarssen LW, Anand M, Bahn M, Blonder B, Cavender-Bares J, Cornelissen JHC, Cornwell WK, Díaz S, Dickie JB, Freschet GT, Griffiths JG, Gutierrez AG, Hemmings FA, Hickler T, Hitchcock TD, Keighery M, Kleyer M, Kurokawa H, Leishman MR, Liu K, Niinemets Ü, Onipchenko V, Onada Y, Penuelas J, Pillar VD, Reich PB, Shiodera S, Siefert A, Sosinski EE Jr, Soudzilovskaia NA, Swaine EK, Swenson NG, van Bodegom PM, Warman L, Weiher E, Wright IJ, Zhang H, Zobel M, Bonser SP (2014) Which is a better predictor of plant traits: temperature of precipitation? J Veg Sci 25:1167–1180. https://doi.org/10.1111/jvs.12190
Moreira FMS, Silva MF, Miana FS (1992) Occurrence of nodulation in legume species in the Amazon region of Brazil. New Phytol 121:563–570. https://doi.org/10.1111/j.1469-8137.1992.tb01126.x
Morellato LPC, Haddad CFB (2000) Introduction: the Brazilian Atlantic Forest. Biotropica 32:786–792. https://doi.org/10.1111/j.1744-7429.2000.tb00618.x
Morellato LPC, Talora DC, Takahasi A, Bencke CC, Romera EC, Zipparro VB (2000) Phenology of Atlantic rain forest trees: a comparative study. Biotropica 32:811–823. https://doi.org/10.1111/j.1744-7429.2000.tb00620.x
Nardoto GB, Ometto JPHB, Ehleringer JR, Higuchi N, Bustamante MMC, Martinelli LA (2008) Understanding the influences of spatial patterns on N availability within the Brazilian Amazon Forest. Ecosystems 11:1234–1256. https://doi.org/10.1007/s10021-008-9189-1
Nardoto GB, Quesada CA, Patiño S, Saiz G, Baker TR, Schwarz M, Schrodt F, Feldpausch TR, Domingues TF, Marimon BS, Marimon Junior BH, Vieira ICG, Silveira M, Bird MI, Phillips OL, Lloyd J, Martinelli LA (2014) Basin-wide variations in Amazon forest nitrogen cycling characteristics as inferred from plant and soil 15N:14N measurements. Plant Ecol Divers 7:173–187. https://doi.org/10.1080/17550874.2013.807524
Oliveira GC, Francelino MR, Arruda DM, Fernandes-Filho EI, Schaefer CEGR (2019) Climate and soils at the Brazilian semiarid and the forest-Caatinga problem: new insights and implications for conservation. Environ Res Lett 14:104007. https://doi.org/10.1088/1748-9326/ab3d7b
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. https://doi.org/10.1007/s10533-006-9008-8
Overbeck GE, Müller SC, Fidelis A, Pfadenhauer J, Pillar VD, Blanco CC, Boldrini I, Both R, Forneck ED (2007) Brazil’s neglected biome: the South Brazilian Campos. Perspect Plant Ecol 9:101–116. https://doi.org/10.1016/j.ppees.2007.07.005
Pardo LH, Templer PH, Goodale CL, Duke S, Groffman PM, Adams MB, 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 MJ, 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. https://doi.org/10.1007/s10533-006-9015-9
Pereira EJAL, Ferreira PJS, Ribeiro LCS, Carvalho TS, Pereira HBB (2019) Policy in Brazil (2016-2019) threaten conservation of the Amazon rainforest. Environ Sci Policy 100:8–12. https://doi.org/10.1016/j.envsci.2019.06.001
Porder S, Hilley GE (2011) Linking chronosequences with the rest of the world: predicting soil phosphorus content in denuding landscapes. Biogeochemistry 102:153–166. https://doi.org/10.1007/s10533-010-9428-3
Porder S, Asner GP, Vitousek PM (2005) Ground-based and remotely sensed nutrient availability across a tropical landscape. P Natl Acad Sci USA 102:10909–10912. https://doi.org/10.1073/pnas.0504929102
Pugnaire FI, Morillo JA, Peñuelas J, Reich PB, Bardgett RD, Gaxiola A, Wardle DA, van der Putten WH (2019) Climate change effects on plant-soil feedbacks and consequences for biodiversity and functioning of terrestrial ecosystems. Sci Adv 5:eaaz1834. https://doi.org/10.1126/sciadv.aaz1834
Reich PB, Walters MB, Ellsworth DS (1997) From tropics to tundra: global convergence in plant functioning. Proc Natl Acad Sci USA 94:13730–13734. https://doi.org/10.1073/pnas.94.25.13730
Reich PB, Ellsworth DS, Walters MB, Vose JM, Gresham C, Volin JC, Bowman WD (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969. https://doi.org/10.1890/0012-9658(1999)080[1955:GOLTRA]2.0.CO;2
Ribeiro EMS, Arroyo-Rodríguez V, Santos BA, Tabarelli M, Leal IR (2015) Chronic anthropogenic disturbance drives the biological impoverishment of the Brazilian Caatinga vegetation. J Appl Ecol 52:611–620. https://doi.org/10.1111/1365-2664.12420
Ribeiro K, Sousa-Neto ER, Carvalho Junior JÁ, Lima JRS, Menezes RSC, Duarte-Neto PJ, Guerra GS, Ometto JPHB (2016) Land cover changes and greenhouse gas emissions in two different soil covers in the Brazilian Caatinga. Sci Total Environ 571:1048–1057. https://doi.org/10.1016/j.scitotenv.2016.07.095
Richter DD, Babbar LI (1991) Soil diversity in the tropics. Adv Ecol Res 21:315–389. https://doi.org/10.1016/S0065-2504(08)60100-2
Rödig E, Cuntz M, Ramming A, Fischer R, Taubert F, Huth A (2018) The importance of forest structure for carbon fluxes of the Amazon rainforest. Environ Res Lett 13:054013. https://doi.org/10.1088/1748-9326/aabc61
Sanchez PA, Buol SW (1974) Soils of the tropics and the world food crisis. Science 188:598–603. https://doi.org/10.1126/science.188.4188.598
Sanchez PA, Logan TJ (1992) Myths and science about the chemistry and fertility of soils in the tropics. In: Lal R, Sanchez PA (eds) Myths and science of soil of the tropics, SSSA special publications no. 29. Soil Science Society of America/American Society of Agronomy, Madison, pp 35–46. https://doi.org/10.2136/sssaspecpub29.c3
Sano EE, Rosa R, Brito JLS, Ferreira LG (2010) Land cover mapping of the tropical savanna region in Brazil. Environ Monit Assess 166:113–124. https://doi.org/10.1007/s10661-009-0988-4
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. https://doi.org/10.1007/s00442-004-1542-2
Sardans J, Alonso R, Carnicer J, Fernández-Martínez M, Vivanco MG, Peñuelas J (2016) Factors influencing the foliar elemental composition and stoichiometry in forest trees in Spain. Perspect Plant Ecol 18:52–69. https://doi.org/10.1016/j.ppees.2016.01.001
Schimel D (1995) Terrestrial ecosystems and the carbon cycle. Glob Chang Biol 1:77–91. https://doi.org/10.1111/j.1365-2486.1995.tb00008.x
Schimel D, Stephens BB, Fisher JB (2015a) Effect of increasing CO2 on the terrestrial carbon cycle. Proc Natl Acad Sci USA 112:436–441. https://doi.org/10.1073/pnas.1407302112
Schimel D, Pavlick R, Fisher JB, Asner GP, Saatchi S, Townsend P, Miller C, Frankenber C, Hibbard K, Cox P (2015b) Observing terrestrial ecosystems and the carbon cycle from space. Glob Chang Biol 21:1762–1776. https://doi.org/10.1111/gcb.12822
Schuur EAG, Matson PA (2001) Net primary productivity and nutrient cycling across a mesic to wet precipitation gradient in Hawaiian montane forest. Oecologia 128:431–422. https://doi.org/10.1007/s004420100671
Sousa-Neto E, Carmo JB, Keller M, Martins SC, Alves LF, Vieira SA, Piccolo MC, Camargo PB, Couto HTZ, Joly CA, Martinelli LA (2011) Soil-atmosphere exchange of nitrous oxide, methane and carbon dioxide in a gradient of elevation in the coastal Brazilian Atlantic forest. Biogeosciences 8:733–742. https://doi.org/10.5194/bg-8-733-2011
Souza LQ, Freitas ADS, Sampaio EVSB, Moura PM, Menezes RSC (2012) How much nitrogen is fixed by biological symbiosis in tropical dry forests? 1. Trees and shrubs. Nutr Cycl Agroecosyst 2:171–179. https://doi.org/10.1007/s10705-012-9531-z
Souza CM, Shimbo JZ, Rosa MR, Parente LL, Alencar AA, Rudorff BFT, Hasenack H, Matsumoto M, Ferreira LG, Souza-Filho PWM, de Oliveira SW, Rocha WF, Fonseca AV, Marques CB, Diniz CG, Costa D, Monteiro D, Rosa ER, Vélez-Martin E, Weber EJ, Lenti FEB, Paternost FF, Pareyn FGC, Siqueira JV, Vieira JL, Neto LCF, Saraiva MM, Sales MH, Salgado MPG, Vasconcelos R, Galano S, Mesquita VV, Azevedo T (2020) Reconstructing three decades of lande use and landa cover changes in Brazilian Biomes with Landsat archive and Earth engine. Remote Sens 12:2735. https://doi.org/10.3390/rs12172735
Sprent JI, Geoghegan IE, Whitty PW, James EK (1996) Natural abundance of 15N and 13C in nodulated legumes and other plants in the cerrado and neighbouring regions of Brazil. Oecologia 105:440–446. https://doi.org/10.1007/BF00330006
Stein A, Gerstner K, Kreft H (2014) Environmental heterogeneity as a universal driver os species richness across taxa, biomes and spatial scales. Ecol Lett 14:866–880. https://doi.org/10.1111/ele.12277
Swap RJ, Aranibar JN, Dowty PR, Gilhooly IIIWP, Macko SA (2004) Natural abundance of 13C and 15N in C3 and C4 vegetation of southern Africa: patterns and implications. Glob Chang Biol 10:350–358. https://doi.org/10.1046/j.1529-8817.2003.00702.x
Tabarelli M, Silva JMC, Gascon C (2004) Forest fragmentation, synergisms and the impoverishment of neotropical forests. Biodivers Conserv 13:1419–1425. https://doi.org/10.1023/B:BIOC.0000019398.36045.1b
Tiessen H, Chacon P, Cuevas E (1994) Phosphorus and nitrogen status in soils and vegetation along a toposequence of dystrophic rainforests on the Upper Rio Negro. Oecologia 99:145–150. https://doi.org/10.1007/BF00317095
Townsend AR, Cleveland CC, Asner GP, Bustamante MMC (2007) Controls over foliar N:P ratios in tropical rain forests. Ecology 88:107–118. https://doi.org/10.1890/00129658(2007)88[107:COFNRI]2.0.CO;2
Townsend AR, Asner GP, Cleveland CC (2008) The biogeochemical heterogeneity of tropical forests. Trends Ecol Evol 23:424–431. https://doi.org/10.1016/j.tree.2008.04.009
Van der Merwe NJ, Medina E (1991) The canopy effect, carbon isotope ratios and foodwebs in Amazonia. J Archaeol Sci 18:249–259. https://doi.org/10.1016/0305-4403(91)90064-V
Van der Werf GR, Randerson JT, Giglio L, van Leeuwen TT, Chen Y, Rogers BM, Mu M, van Marle MJR, Morton DC, Collatz GJ, Yokelson RJ, Kasibhatla PS (2017) Global fire emissions estimates during 1997–2016. Earth Syst Sci Data 9:697–720. https://doi.org/10.5194/essd-9-697-2017
Vitousek PM, Sanford RL Jr (1986) Nutrient cycling in moist tropical forest. Annu Rev Ecol Syst 17:137–167. https://doi.org/10.1146/annurev.es.17.110186.001033
Vitousek PM, Cassman K, Cleveland C, Crews T, Field CB, Grimm NB, Howarth RW, Marino R, Martinelli L, Rastetter EB, Sprent JI (2002) Towards an ecological understanding of biological nitrogen fixation. Biogeochemistry 57:1–54. https://doi.org/10.1023/A:1015798428743
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 96:1561–1574. https://doi.org/10.1890/14-0834.1
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 Ü, 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. https://doi.org/10.1038/nature02403
Yue C, Ciais P, Houghton RA, Nassikas AA (2020) Contribution of land use to the interannual variability of the land carbon cycle. Nat Commun 11:3170. https://doi.org/10.1038/s41467-020-16953-8
Zhang J, He N, Liu C, Xu L, Chen Z, Li Y, Wang R, Yu G, Sun W, Xiao C, Chen HYH, Reich PB (2020) Variation and evolution of C:N ratio among different organs enable plants to adapt to N-limited environments. Glob Chang Biol 26:2534–2543. https://doi.org/10.1111/gcb.14973
Zhao N, Yu G, He N, Wang Q, Guo D, Zhang X, Wang R, Xu Z, Jiao C, Li N, Jia Y (2016) Coordinated pattern of multi-element variability in leaves and roots across Chinese forest biomes. Glob Ecol Biogeogr 25:359–367. https://doi.org/10.1111/geb.12427
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Robert W. Howarth.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original version of this article was revised: The initial online publication contained typesetting mistakes in the author information. The original article has been corrected.
This paper is an invited contribution to the 35th Anniversary Special Issue, edited by Sujay Kaushal, Robert Howarth, and Kate Lajtha.
The initial online publication contained typesetting mistakes in the author information. The original article has been corrected.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Martinelli, L.A., Nardoto, G.B., Soltangheisi, A. et al. Determining ecosystem functioning in Brazilian biomes through foliar carbon and nitrogen concentrations and stable isotope ratios. Biogeochemistry 154, 405–423 (2021). https://doi.org/10.1007/s10533-020-00714-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-020-00714-2