Skip to main content

Advertisement

Log in

Relationships between soil nutrient status and nutrient-related leaf traits in Brazilian cerrado and seasonal forest communities

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

In Brazil, cerrado and seasonal forest occur in close proximity but on soils with very different chemistry and texture. We aimed to compare species from these two vegetation types in terms of leaf N and P concentrations (of green and senesced leaves) and proportional nutrient resorption, quantifying the relationships among these traits, with other key leaf traits, and with soil properties.

Methods

We collected topsoil at 100 25 m2 sample plots in south-eastern Brazil and measured leaf traits of 89 woody species occurring therein, expressing them as community-weighted means. Soil nutrient status was indexed using eight standard variables.

Results

In terms of properties such as pH, clay content, and cation exchange capacity, cerrado soils were deemed as being less “fertile” than forest soils, yet cerrado and forest sites did not differ in soil total N or available P (which themselves were negatively correlated). On average, forest species showed higher proportional P resorption but lower N resorption. Leaves with higher nutrient concentrations were less scleromorphic.

Conclusion

In Brazilian cerrado and forests, variation in green- and senesced-leaf nutrients was better aligned with generalised measures of soil fertility than with total N or available P and showed far more clear patterns than nutrient resorption efficiencies.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? J Ecol 84:597–608

    Article  Google Scholar 

  • Aerts R, Chapin FS (1999) The mineral nutrition of wild plants revisited. Adv Ecol Res 30:1–67

    Article  Google Scholar 

  • Batalha MA, Mantovani W (1999) Chaves de identificação das espécies vegetais vasculares baseada em caracteres vegetativos para a ARIE Cerrado Pé-de-Gigante (Santa Rita do Passa Quatro, SP). Revista do Instituto Florestal 11:137–158

    Google Scholar 

  • Batalha MA, Mantovani W (2005) Alguns aspectos das comunidades vegetais. In: Pivello VR, Varanda EM (eds) O cerrado Pé-de-Gigante: ecologia e conservação - Parque Estadual de Vassununga. Secretaria do Meio Ambiente, São Paulo

    Google Scholar 

  • Batalha MA, Aragaki S, Mantovani W (1998) Chave de identificação das espécies vasculares do cerrado em Emas (Pirassununga, SP) baseada em caracteres vegetativos. Boletim de Botânica da Universidade de São Paulo 17:85–108

    Article  Google Scholar 

  • Bradstreet RB (1965) The Kjeldahl method for organic nitrogen. Academic, New York

    Google Scholar 

  • Chapin FS III (1980) The mineral nutrition of wild plants. Annu Rev Ecol Syst 11:233–260

    Article  CAS  Google Scholar 

  • Cole MM (1986) The savannas biogeography and geobotany. Academy, London

    Google Scholar 

  • Coutinho LM (1990) Fire in the ecology of the Brazilian cerrado. In: Goldammer JG (ed) Fire in the tropical biota. Springer, Berlin, pp 82–105

    Chapter  Google Scholar 

  • Craine JM (2009) Resource strategies of wild plants. Princeton University Press, Princeton

    Book  Google Scholar 

  • Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321

    CAS  PubMed  PubMed Central  Google Scholar 

  • Development Core Team R (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Durigan G, Ratter JA (2006) Successional changes in cerrado and cerrado/forest ecotonal vegetation in western São Paulo State, Brazil, 1962–2000. Edinb J Bot 633:119–130

    Article  Google Scholar 

  • Embrapa (2012) Manual de métodos de análise de solos. Embrapa, Brasília

    Google Scholar 

  • Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives. Sinauer, Sunderland

    Google Scholar 

  • Fujita Y, Bodegom PM, Witte JPM (2013) Relationships between nutrient-related plant traits and combinations of soil N and P fertility measures. PloS One 8, e83735

    Article  PubMed  PubMed Central  Google Scholar 

  • Furley PA (1999) The nature and diversity of neotropical savanna vegetation with particular reference to the Brazilian cerrados. Glob Ecol Biogeogr 8:223–241

    Article  Google Scholar 

  • Furley PA, Ratter JA (1988) Soil resources and plant communities of the central Brazilian Cerrado and their development. J Biogeogr 15:97–108

    Article  Google Scholar 

  • Garnier E, Cortez J, Billès G, Navas ML, Roumet C, Debussche M, Laurent G, Blanchard A, Aubry D, Bellmann A, Neill C, Toussaint JP (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637

    Article  Google Scholar 

  • Goodland R, Pollard R (1973) The Brazilian cerrado vegetation: a fertility gradient. J Ecol 61:219–224

    Article  Google Scholar 

  • Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 982:1169–1194

    Article  Google Scholar 

  • Grimshaw HM (1987) The determination of total phosphorus in soils by acid digestion. In: Rowland AP (ed) Chemical analysis in environmental research. Natural Environment Research Council, Abbotts Ripton, pp 92–95

    Google Scholar 

  • Güsewell S (2004) N:P ratios in in terrestrial plants: variation and functional significance. New Phytol 164:243–266

    Article  Google Scholar 

  • Harrell FE Jr, Dupont C (2014) Hmisc: Harrell miscellaneous. R Foundation for Statistical Computing, Vienna, URL: http://CRAN.R-project.org/package=Hmisc

    Google Scholar 

  • Hayes P, Turner BL, Lambers H, Laliberté E (2014) Foliar nutrient concentrations and resorption efficiency in plants in contrasting nutrient-acquisition strategies along a 2-million-year dune chronosequence. J Ecol 102:396–410

    Article  CAS  Google Scholar 

  • Hoffmann WA, Franco AC (2003) Comparative growth analysis of tropical forest and savanna woody plants using phylogenetically independent contrasts. J Ecol 91:475–484

    Article  Google Scholar 

  • Hoffmann WA, Orthen B, Franco AC (2004) Constraints to seedling success of savanna and forest trees across the savanna-forest boundary. Oecologia 140:252–260

    Article  PubMed  Google Scholar 

  • Hoffmann WA, Franco AC, Moreira MZ, Haridasan M (2005) Specific leaf area explains differences in leaf traits between congeneric savanna and forest trees. Funct Ecol 19:932–940

    Article  Google Scholar 

  • Hoffmann WA, Geiger EL, Gotsch SG, Rossatto DR, Silva LCR, Lau OL, Haridasan M, Franco AC (2012) Ecological thresholds at the savanna-forest boundary: how plant traits, resources and fire govern the distribution of tropical biomes. Ecol Lett 15:759–768

    Article  PubMed  Google Scholar 

  • Hunke P, Mueller EN, Schröder B, Zeilofer P (2015) The Brazilian Cerrado: assessment of water and soil degradation in catchments under intensive agricultural use. Ecohydrology 8:1154–1180

    Article  Google Scholar 

  • Ibanez T, Hély C, Gaucherel C (2013) Sharp transitions in microclimatic conditions between savanna and forest in New Caledonia: Insights into the vulnerability of forest edges to fire. Aust Ecol 38:680–687

    Article  Google Scholar 

  • Jongman RHG, Braak CJF, Tongeren OFR (1995) Data analysis in community and landscape ecology. Cambridge University, Cambridge

    Book  Google Scholar 

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

    Article  Google Scholar 

  • Köppen W (1931) Grundriss der Klimakunde. Gruyter, Berlin

    Google Scholar 

  • Krebs CJ (1998) Ecological methodology. Harper Collins, New York

    Google Scholar 

  • Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305

    Article  PubMed  Google Scholar 

  • Lambers H, Raven JA, Shaver GR, Smith SE (2008a) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103

    Article  PubMed  Google Scholar 

  • Lambers H, Chapin FS, Pons TL (2008b) Plant physiological ecology. Springer, New York

    Book  Google Scholar 

  • Lambers H, Brundrett MC, Ravel JA, Hopper SD (2010) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 334:11–31

    Article  CAS  Google Scholar 

  • Lambers H, Ahmedi I, Berkowitz O, Dunne C, Finnegan PM, Hardy GESJ, Jost R, Laliberté E, Pearse SJ, Teste FP (2013) Phosphorus nutrition of phosphorus-sensitive Australian native plants: threats to plant communities in a global biodiversity hotspot. Conserv Physiol 1:1–21. doi:10.1093/conphys/cot010

    Article  Google Scholar 

  • Lehmann CER, Archibald SA, Hoffmann WA, Bond WJ (2011) Deciphering the distribution of the savanna biome. New Phytol 191:197–209

    Article  PubMed  Google Scholar 

  • Loveless AR (1961) A nutritional interpretations of sclerophylly based on differences in the chemical composition of sclerophyllous and mesophytic leaves. Ann Bot 25:168–184

    CAS  Google Scholar 

  • Maire V, Wright IJ, Prentice IC, Baties NH, Bhaskar R, Bodegon PM, Cornwell WK, Ellsworth D, Niinemets Ü, Ordonez A, Reich PB, Santiago LS (2015) Global effects of soil and climate on leaf photosynthetic traits and rates. Glob Ecol Biogeogr 6:706–717

    Article  Google Scholar 

  • Mao R, Song CC, Zhang XH, Wang XW, Zhang ZH (2013) Response of leaf, sheath and stem nutrient resorption to 7 years of N addition in freshwater wetland of Northeast China. Plant Soil 346:385–394

    Article  Google Scholar 

  • Menge DNL, Hedin LO, Pacala SW (2012) Nitrogen and phosphorus limitation over long-term ecosystem development in terrestrial ecosystems. PloS One 7, e42045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murphy BP, Bowman DMJS (2012) What controls the distribution of tropical forest and savanna? Ecol Lett 15:748–758

    Article  PubMed  Google Scholar 

  • Näsholm T, Kielland K, Ganated U (2009) Uptake of organic nitrogen by plants. New Phytol 182:31–48

    Article  PubMed  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) Vegan: community ecology package. R Foundation for Statistical Computing, Vienna, URL: http://CRAN.R-project.org/package=vegan

    Google Scholar 

  • Pérez-Harguindeguy N, Díaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte MS, Cornwell WK, Craine JM, Gurvich DE, Urcelay C, Veneklaas EJ, Reich PB, Poorter L, Wright IJ, Ray P, Enrico L, Pausas JG, Vos AC, Buchmann N, Funes G, Quétier F, Hodgson CJG, Thompson K, Morgan HD, Steege H, Heijden MGA, Sack L, Blonder B, Poschlod P, Vaieretti MV, Conti G, Staver AC, Aquino S, Cornelissen JHC (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234

    Article  Google Scholar 

  • Pivello VR, Bitencourt MD, Mantovani W, Mesquita-Junior HN, Batalha MA, Shida CN (1998) Proposta de zoneamento ecológico para a Reserva de Cerrado Pé-de-Gigante (Santa Rita do Passa Quatro, SP). Braz J Ecol 2:108–118

    Google Scholar 

  • Puyravaud JP, Pascal JP, Dufour C (1994) Ecotone structure as an indicator of changing forest-savanna boundaries (Linganamakki region, southern India). J Biogeogr 21:581–593

    Article  Google Scholar 

  • Rasband WS (2014) ImageJ. U. S. National Institutes of Health, Bethesda

    Google Scholar 

  • Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: traits, spectra, and strategies. Int J Plant Sci 164:S143–S164

    Article  Google Scholar 

  • Rossatto DR, Hoffmann WA, Franco AC (2009) Differences in growth patterns between co-occurring forest and savanna trees affect the forest–savanna boundary. Funct Ecol 23:689–698

    Article  Google Scholar 

  • Ruggiero PGC, Batalha MA, Pivello VR, Meirelles ST (2002) Soil-vegetation relationships in cerrado (Brazilian savanna) and semi-deciduous forest, Southeastern Brazil. Plant Ecol 160:1–16

    Article  Google Scholar 

  • Sarmiento G (1984) The ecology of neotropical Savannas. Harvard University, Cambridge

    Book  Google Scholar 

  • Schachtman DP, Reid RJ, Ayling SM (1998) Phosphorus uptake by plants: from soil to cell. Plant Physiol 116:447–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schimel JP, Bennett J (2004) Nitrogen mineralization: challenges of a changing paradigm. Ecology 85:591–602

    Article  Google Scholar 

  • Scholes RJ, Hall DO (1996) The carbon budget of tropical savannas, woodlands, and grasslands. In: Breymeyer AK, Hall DO, Melillo JM, Agren GI (eds) Global change: effects on coniferous forests and grasslands. SCOPE, Vol. 56. Wiley, Chichester, pp. 69–100

    Google Scholar 

  • Schwartz D, Foresta H, Mariotti A, Balesdent J, Massimba JP, Girardin C (1996) Present dynamics of the savanna-forest boundary in the Congolese Mayombe: a pedological, botanical and isotopic (13C and 14C) study. Oecologia 106:516–524

    Article  Google Scholar 

  • See CR, Yanai RD, Fisk MC, Vadeboncoeur MA, Quintero BA, Fahey TJ (2015) Soil nitrogen affects phosphorus recycling: foliar resorption and plant-soil feedbacks in a northern hardwood forest. Ecology 96:2488–2498

    Article  PubMed  Google Scholar 

  • Silva DM, Batalha MA (2008) Soil–vegetation relationships in cerrados under different fire frequencies. Plant Soil 311:87–96

    Article  CAS  Google Scholar 

  • SMA. Secretaria de Estado do Meio Ambiente (1997) Cerrado: bases para conservação e uso sustentável das áreas de cerrado do estado de São Paulo. SMA, São Paulo

    Google Scholar 

  • Soil Survey Staff (2014) Keys to soil taxonomy. USDA, Washington

    Google Scholar 

  • Souza AF, Martins FR (2004) Microsite specialization and spatial distribution of Geonoma brevispata, a clonal palm in south-eastern Brazil. Ecol Res 19:521–532

    Article  Google Scholar 

  • Staver AC, Archibald S, Levin SA (2011) The global extent and determinants of Savanna and forest as alternative biome states. Science 334:230–232

    Article  CAS  PubMed  Google Scholar 

  • Sutherland WJ (2006) Ecological census techniques. Cambridge University, Cambridge

    Book  Google Scholar 

  • Turner IM (1994) Sclerophylly: primarily protective? Funct Ecol 8:669–675

    Article  Google Scholar 

  • Van Heerwaarden LM, Toet S, Aerts R (2003) Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: facts and solutions. Oikos 101:664–669

    Article  Google Scholar 

  • Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB (2012) Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr 82:205–220

    Article  Google Scholar 

  • Viani RAC, Rodrigues RR, Dawson TE, Oliveira RS (2011a) Functional differences between woodland savannas and seasonally dry forests from south-eastern Brazil: Evidence from 15N natural abundance studies. Aust Ecol 36:974–982

    Article  Google Scholar 

  • Viani RAG, Rodrigues RR, Dawson TE, Oliveira RS (2011b) Savanna soil fertility limits growth but not survival of tropical forest tree seedlings. Plant Soil 349:341–353

    Article  CAS  Google Scholar 

  • Viani RA, Rodrigues RR, Dawson TE, Lambers H, Oliveira RS (2014) Soil pH accounts for differences in species distribution and leaf nutrient concentrations of Brazilian woodland savannah and seasonally dry forest species. Perspect Plant Ecol Evol Syst 16:64–74

    Article  Google Scholar 

  • Vitousek PM, Porder S, Houlton BZ, Chadwick OA (2010) Terrestrial phosphorus limitations: mechanisms, implications, and nitrogen-phosphorus interactions. Ecol Appl 20:5–15

    Article  PubMed  Google Scholar 

  • Vourlitis GL, Lobo FA, Lawrence S, Holt K, Zappia A, Pinto OB Jr, Nogueira JS (2014) Nutrient resorption in tropical savanna forests and woodlands of central Brazil. Plant Ecol 215:963–975. doi:10.1007/s11258-014-0348-5

    Article  Google Scholar 

  • Warman L, Bradford MG, Moles AT (2013) A broad approach to abrupt boundaries: looking beyond the boundary at soil attributes within and across tropical vegetation types. PloS One 8, e60789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wright IJ, Westoby M (2003) Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Funct Ecol 17:10–19

    Article  Google Scholar 

  • Wright IJ, Westoby M, Reich PB (2002) Convergence towards higher leaf mass per area in dry and nutrient-poor habitats has different consequences for leaf lifespan. J Ecol 90:534–543

    Article  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 

  • Yuan ZY, Chen HYH (2015) Negative effects of fertilization on plant nutrient resorption. Ecology 96:373–380

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to São Paulo Research Foundation (FAPESP, grant 2012/18295-4) and to Coordination for the Improvement of Higher Education Personnel (CAPES, grant BEX 12105/13-9) for the scholarships granted to RCM; to the National Council for Scientific and Technological Development for financial support and scholarship granted to MAB (CNPq, grant 305912/2013-5); to São Paulo Forestry Institute, for the research permit; to the Vaçununga State Park staff, for logistical assistance; to M Groppo and WM Mantovani, for helping us with species identification; to N Abe, ALS Albino, KR Coelho, P Dodonov, JR Freitas, CS Gonçalves, DT Gregolin, LA Joaquim, MB Leite, PP Loiola, WB Nascimento, CG Netto, LV Nóbrega, BA Severian, A Viscardi, and CB Zanelli, for valuable help with field work; and to GH Carvalho for revising a previous version of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Raquel C. Miatto.

Additional information

Responsible Editor: Hans Lambers.

Appendix

Appendix

Table 3

Table 3 Species and number of individuals sampled in cerrado and seasonal forest in the Vaçununga State Park, south-eastern Brazil
Table 4 Leaf functional traits and nutrient concentration of species sampled in cerrado and seasonal forest in the Vaçununga State Park, south-eastern Brazil
Table 5 Mean, standard deviation and range of each soil feature in the cerrado and in the seasonal forest. Clay (g.kg−1), cation exchange capacity (CEC, mmol.kg−1), organic matter (OM, mmol.kg−1), pH, and sum of bases (SB, mmol.kg−1), available phosphorus (P, mg.kg−1), total nitrogen (N, mg.kg−1), Aluminium (Al, mmol.kg−1), Cations K+ (K, mmol.kg−1), Ca2+ (Ca, mmol.kg−1), Mg+ (Mg, mmol.kg−1), as well as potential acidity (H.Al, mmol.kg−1), percentage of base saturation (V, %), percentage of aluminium saturation (m, %), silt, and sand proportions (1:1000)
Table 6 Loadings of each soil variable on the first two principal components. Clay, cation exchange capacity (CEC), organic matter (OM), pH, and sum of bases (SB) contributed more strongly to PC1. Available phosphorus (P), total nitrogen (N), and aluminium contributed more strongly to PC2
Table 7 Average soil aluminium concentration of species sampled in cerrado and seasonal forest in the Vaçununga State Park, south-eastern Brazil. We calculated the mean Al concentration across all sites where the species occurred within each vegetation type. We expected cerrado species, or at least some families, to be more associated with high Al sites and forest species to be more associated with low Al sites. Unexpectedly, forest species can occupy, on average, sites with higher Al concentration and there is no pattern of aggregation, in terms of species relatedness, towards high or low Al sites in both vegetation types. Species occurring in both vegetation types, highlighted in bold, tend to be plastic: whereas some were more associated with high Al sites in the forest, others were more associated with high Al sites in the cerrado. Perhaps the soil Al concentration is not a good predictor of either cerrado or forest species preferences or floristic distinctiveness in regards do high or low Al soils. Perhaps what really matters is the difference in species tolerance against the toxic forms of aluminium that are predominant under the more acid soils of cerrado. Although cerrado soils had higher Al concentrations than the forest (Table 5), some forest plots had surprising high Al concentrations. Some of the high Al species in the forest were rare species (Table 3) occurring incidentally in these uncommon high Al plots

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miatto, R.C., Wright, I.J. & Batalha, M.A. Relationships between soil nutrient status and nutrient-related leaf traits in Brazilian cerrado and seasonal forest communities. Plant Soil 404, 13–33 (2016). https://doi.org/10.1007/s11104-016-2796-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-016-2796-2

Keywords

Navigation