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Native and alien herbaceous plants in the Brazilian Cerrado are (co-)limited by different nutrients

Abstract

Background and aims

The diverse flora of the Brazilian Cerrado is threatened by agricultural expansion, nutrient enrichment and invasion of alien plants. We performed a fertilization experiment to investigate the nature of nutrient limitation in Cerrado vegetation, and evaluate whether native and alien invasive species are limited by the same or different nutrients.

Methods

We applied various combinations of nutrients (phosphorus (P), nitrogen (N), and a mixture of other macro- and micro-nutrients (‘cations treatment’)) to six types of Cerrado vegetation. We then studied over a 3-year period how these treatments affected the aboveground biomass of native forbs, native C3 and C4 grasses, and invasive C4 grasses.

Results

The full nutrient treatment (N + P+ ‘cations’) significantly increased total community biomass across our sites, but P alone had no effect. The nutrient treatments also affected the relative abundance of functional plant groups in the six vegetation types. P addition, either alone or in combination with other nutrients, increased the biomass of alien C4 grasses, where present, whereas the cations treatment stimulated growth of the native C4 grasses. Addition of N + P reduced the biomass of native C3 grasses.

Conclusions

Our results indicate co-limitation by several nutrients, including P, perhaps N, and at least one other nutrient. Further research is needed to determine what the other nutrient (or nutrients) may be. Native and invasive species appear to be limited by different nutrients, with P alone stimulating growth of African C4 grasses. This should be considered in managing both natural and invaded communities.

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References

  • Abrahão A, Lambers H, Sawaya ACHF, Mazzafera P, Oliveira RS (2014) Convergence of a specialized root trait in plants from nutrient-impoverished soils: phosphorus-acquisition strategy in a nonmycorrhizal cactus. Oecologia 176:345–355

    Article  PubMed  Google Scholar 

  • Adler PB, Seabloom EW, Borer ET, Hillebrand H, Hautier Y, Hector H, HarpoleWS O’HLR, Grace JB, Anderson TM, Bakker JD, Biederman LA, Brown CS, Buckley YM, Calabrese LB, Chu C-J, Cleland EE, Collins SL, Cottingham KL, Crawley MJ, Damschen EI, Davies KF, DeCrappeo NM, Fay PA, Firn J, Frater P, Gasarch EI, Gruner DS, Hagenah N, Lambers JHR, Humphries H, Jin VL, Kay AD, Kirkman KP, Klein JA, Knops JMH, La Pierre KJ, Lambrinos JG, Li W, MacDougall AS, McCulley RL, Melbourne BA, Mitchell CE, Moore JL, Morgan JW, Mortensen B, Orrock JL, Prober SM, Pyke DA, Risch AC, Schuetz M, Smith MD, Stevens CJ, Sullivan LL, Wang G, Wragg PD, Wright JP, Yang LH (2011) Productivity is a poor predictor of plant species richness. Science 333:1750–1753

    Article  CAS  PubMed  Google Scholar 

  • Aires FS (2009) Desenvolvimento de técnica de manejo, sem uso de agentes químicos, no controle da espécies invasora Melinis minutiflora Beauv. (capim-gordura) para aplicação em áreas de campo sujo. Master’s thesis, Universidade de Brasília, Brasília

  • Almeida-Neto M, Prado PI, Kubota U, Bariani JM, Aguirre GH, Lewinsohn TM (2010) Invasive grasses and native Asteraceae in the Brazilian Cerrado. Plant Ecol 209:109–122

    Article  Google Scholar 

  • Barger NN, D’Antonio CM, Ghneim T, Brink K, Cuevas E (2002) Nutrient limitation to primary productivity in a secondary savanna in Venezuela. Biotropica 34:493–501

    Article  Google Scholar 

  • Batmanian GJ, Haridasan M (1985) Primary production and accumulation of nutrients by the ground layer community of cerrado vegetation of central Brazil. Plant Soil 88:437–440

    Article  Google Scholar 

  • Bilbao B, Medina E (1990) Nitrogen-use efficiency for growth in a cultivated African grass and a native South American pasture grass. J Biogeogr 17:421–425

    Article  Google Scholar 

  • Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman J-W, Fenn M, Gilliam F, Nordin A, Pardo L, de Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecol Appl 20:30–59

    Article  CAS  PubMed  Google Scholar 

  • Bustamante MMC, Medina E, Asner GP, Nardoto GB, Garcia-Montiel DC (2006) Nitrogen cycling in tropical and temperate savannas. Biogeochem 79:209–237

    Article  Google Scholar 

  • Bustamante MMC, de Britto DQ, Kozovits AR, Luedemann G, de Mello TRB, Pinto AS, Munhoz CBR, Takahashi FSC (2012) Effects of nutrient additions on plant biomass and diversity of the herbaceous-subshrub layer of a Brazilian savanna (Cerrado). Plant Ecol 213:795–808

    Article  Google Scholar 

  • Carmona R, Martins CR (2010) Dormência e armazenabilidade de sementes de capim-gordura. Revista Brasileira de Sementes 32(4):71–79

    Article  Google Scholar 

  • Cassidy TM, Fownes JH, Harrington RA (2004) Nitrogen limits an invasive perennial shrub in forest understory. Biol Inv 6:113–121

    Article  Google Scholar 

  • Cech PG, Kuster T, Edwards PJ, Olde VH (2008) Effects of herbivory, fire and N2-fixation on nutrient limitation in a humid African savanna. Ecosystems 11:991–1004

    Article  CAS  Google Scholar 

  • Ceulemans T, Stevens CJ, Duchateau L, Jacquemyn H, Gowing DJG, Merckx R, Wallace H, van Rooijen N, Goethem T, Bobbink R, Dorland E, Gaudnik C, Alard D, Corcket E, Muller S, Dise NB, Dupré C, Dieckmann M, Honnay O (2014) Soil phosphorus constrains biodiversity across European grasslands. Global Change Biology doi: 1 < 0.0010/gcb.12650

  • Chapin FS, Vitousek PM, van Cleve K (1986) The nature of nutrient limitation in plant communities. Am Nat 127:48–58

    Article  Google Scholar 

  • Copeland SM, Bruna EM, Barbosa Silva LV, Mack MC, Vasconcelos HL (2012) Short-term effects of elevated precipitation and nitrogen on soil fertility and plant growth in a Neotropical savanna. Ecosphere 3(4):31

    Article  Google Scholar 

  • Crawley MJ, Johnston AE, Silvertown J, Dodd M, Mazancourt C, Heard MS, Henman DF, Edwards GR (2005) Determinants of species richness in the Park Grass experiment. Am Nat 165(2):179–192

    Article  CAS  PubMed  Google Scholar 

  • D’Antonio CM, Mack MC (2006) Nutrient limitation in a fire-derived, nitrogen-rich Hawaiian grassland. Biotropica 38:458–467

    Article  Google Scholar 

  • Daehler CC (2003) Performance comparisons of co-occurring native and invasive grasses: implications for conservation and restoration. Ann Rev Ecol Evol Syst 34:183–211

    Article  Google Scholar 

  • Davidson EA, Howarth RW (2007) Nutrients in synergy. Nature 449:1000–1001

    Article  CAS  PubMed  Google Scholar 

  • de Oliveira OC, de Oliveira IP, Ferreira E, Alves BJR, Miranda CHB, Vilela L, Urquiaga S (2001) Response of degraded pastures in the Brazilian cerrado to chemical fertilisation. Pasturas Tropicales 23:14–18

    Google Scholar 

  • DiTomasso A, Aarssen LW (1989) Resource manipulations in natural vegetation: a review. Vegetatio 84:9–29

    Article  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 

  • Fay PA, Prober SM, Harpole WS, Knops JMH, Bakker JD, Borer ET, Lind EM, MacDougall AS, Seabloom EW, Wragg PD, Adler PB, Blumenthal DM, Buckley YM, Chu C, Cleland EE, Collins SL, Davies KF, Du G, Feng X, Firn J, Gruner DS, Hagenah N, Hautier Y, Heckman RW, Jin VL, Kirkman KP, Klein J, Ladwig LM, Li Q, McCulley RL, Melbourne BA, Mitchell CE, Moore JL, Morgan JW, Risch AC, Schütz M, Stevens CJ, Wedin DA, Yang LH (2015) Grassland productivity limited by multiple nutrients. Nature Plants 1:1–5

    Article  Google Scholar 

  • Ferreira AS, de Oliveira RS, dos Santos MA, Borges EN (2008) Atividade respiratória da microbiota e conteúdo de glicose em resposta à adição de fósforo em solo de Cerrado. Revista Brasileira de Ciência do Solo 32:1891–1897

    Article  CAS  Google Scholar 

  • Furley PA, Ratter JA (1988) Soil resources and plant communities of the central Brazilian Cerrado and their development. J Biogeogr 15(1):97–108

    Article  Google Scholar 

  • Goedert WJ (1983) Management of the Cerrado soils of Brazil: a review. J Soil Sci 34:405–428

    Article  CAS  Google Scholar 

  • Gough L, Osenberg CW, Gross KL, Collins SL (2000) Fertilization effects on species density and primary productivity in herbaceous plant communities. Oikos 89:428–439

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Güsewell S, Koerselman W, Verhoeven JTA (2002) Time-dependent effects of fertilization on plant biomass in floating fens. J Veg Sci 13:705–718

    Article  Google Scholar 

  • Haridasan M (1992) Observations on soils, foliar nutrient concentrations and floristic composition of cerrado sensu stricto and cerradao communities in Central Brazil. In: Furley PA, Ratter JA (eds) Nature and dynamics of forest-savanna boundaries. Chapman & Hall, London

    Google Scholar 

  • Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862

    Article  PubMed  Google Scholar 

  • Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM (1990) Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71:478–491

    Article  Google Scholar 

  • Johnson D, Leake JR, Lee JA (1999) The effects of quantity and durations of simulated pollutant nitrogen deposition on root-surface phosphatase activities in calcareous and acid grasslands: a bioassay approach. New Phyt 141:433–442

    Article  CAS  Google Scholar 

  • Kozovits AR, Bustamante MMC, Garofalo CR, Bucci S, Franco AC, Goldstein G, Meinzer FC (2007) Nutrient resorption and patterns of litter production and decomposition in a Neotropical Savanna. Funct Ecol 21:1034–2043

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Lannes LS, Bustamante MMC, Edwards PJ, Olde Venterink H (2012) Alien and endangered plants in the Brazilian Cerrado exhibit contrasting relationships with vegetation biomass and N:P stoichiometry. New Phytol 196:816–823

    Article  CAS  PubMed  Google Scholar 

  • Lilienfein J, Wilcke W, Zimmermann R, Gerstberger P, Araujo GM, Zech W (2001) Nutrient storage in soil and biomass of native Brazilian Cerrado. J Plant Nutr Soil Sci 164:487–495

    Article  CAS  Google Scholar 

  • Meier M (1991) Nitratbestimmung in Boden-Proben (N-min-Methode). LaborPraxis, Berlin

    Google Scholar 

  • Mendonça RC, Felfili JM, Walter BMT, Silva Júnior MC, Rezende AV, Filgueira JS, Nogueira PE (2008) Flora vascular do cerrado: um ‘checklist’ com 11.430 espécies. In: Sano SM, Almeida SP, Ribeiro JF (eds) Cerrado ambiente e flora, 2nd edn. Embrapa Informação Tecnológica, Brasília

    Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier C, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858

    Article  CAS  PubMed  Google Scholar 

  • Nardoto GB, Bustamante MMC, Pinto AS, Klink CA (2006) Nutrient use efficiency at ecosystem and species level in savanna areas of Central Brazil and impacts of fire. J Trop Ecol 22:191–201

    Article  Google Scholar 

  • Olde Venterink H (2011) Does phosphorus limitation promote species-rich plant communities? Plant Soil 345:1–9

    Article  CAS  Google Scholar 

  • Olde Venterink H, van der Vliet RE, Wassen MJ (2001) Nutrient limitation along a productivity gradient in wet meadows. Plant Soil 234:171–179

    Article  CAS  Google Scholar 

  • Olde Venterink H, Kardel I, Kotowski W, Peeters WHM, Wassen MJ (2009) Long-term effects of drainage and hay-removal on nutrient dynamics and limitation in the Biebrza mires, Poland. Biogeochem 93:235–252

    Article  Google Scholar 

  • Oliveira RS, Galvão HC, de Campos MCR, Eller CB, Pearse SJ, Lambers H (2015) Mineral nutrition of campos rupestres plant species on contrasting nutrient-impoverished soil types. New Phytol 205:1183–1194

    Article  CAS  PubMed  Google Scholar 

  • Perreijn K (2002) Symbiotic nitrogen fixation by leguminous trees in tropical rain forest in Guyana. PhD thesis, Universiteit Utrecht, Utrecht

  • Pivello VR (2011) Invasões biológicas no Cerrado brasileiro: Efeitos da introdução de espécies exóticas sobre a biodiversidade. ECOLOGIA.INFO 33

  • Pivello VR, Shida CN, Meirelles ST (1999) Alien grasses in Brazilian savannas: a threat to biodiversity. Biodivers Conserv 8:1281–1294

    Article  Google Scholar 

  • Ribeiro JF, Walter BMT (1998) Fitofisionomias do bioma Cerrado. In: Sano SM, Almeida SP (eds) Cerrado: ambiente e flora. Embrapa CPAC, Planaltina

    Google Scholar 

  • Sarmiento G, Goldstein G, Meinzer F (1985) Adaptive strategies of woody species in neotropical savannas. Biol Rev 60:315–355

    Article  Google Scholar 

  • Sarmiento G, da Silva MP, Naranjo ME, Pinillos M (2006) Nitrogen and phosphorus as limiting factors for growth and primary production in a flooded savanna in the Venezuelan Llanos. J Trop Ecol 22:203–212

    Article  Google Scholar 

  • Sharpley A, Jarvie HP, Buda A, May L, Spears B, Kleinman P (2014) Phosphorus legacy: overcoming the effects of past management practices to mitigate future water quality impairment. J Environ Qual 42:1308–1326

    Article  Google Scholar 

  • Siemann E, Rogers WE (2007) The role of soil resources in an exotic tree invasion in Texas coastal prairie. J Ecol 95:689–697

    Article  Google Scholar 

  • Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL, Milchunas DG, Pennings S (2005) Functional- and abundance-based mechanisms explain diversity loss due to N fertilization. Proc Natl Acad Sci U S A 102:4387–4392

    PubMed Central  Article  CAS  PubMed  Google Scholar 

  • Tejos R (1984) Efecto del potasio y azufre sobre el pastizal nativo de una sabana. I. Producción. Zootec Trop 2:74–89

    Google Scholar 

  • Tomassen HBM, Smolders AJP, Limpens J, Lamers LPM, Roelofs JGM (2004) Expansion of invasive species on ombrotrophic bogs: dessication or high N deposition? J Appl Ecol 41:139–150

    Article  CAS  Google Scholar 

  • Townsend AR, Cleveland CC, Houlton BZ, Alden CB, White JWC (2011) Multi-element regulation of the tropical forest carbon cycle. Front Ecol Environ 9(1):9–17

    Article  Google Scholar 

  • van de Riet BP, Barendregt A, Brouns K, Hefting MM, Verhoeven JTA (2010) Nutrient limitation in species-rich Calthion grasslands in relation to opportunities for restoration in a peat meadow landscape. Appl Veg Sci 13:315–325

    Google Scholar 

  • van Duren IC, Petgel DM (2000) Nutrient limitations in wet, drained and rewetted fen meadows: evaluation of methods and results. Plant Soil 220:35–47

    Article  Google Scholar 

  • Villela DM, Haridasan M (1994) Response of the ground layer community of a cerrado vegetation in central Brazil to liming and irrigation. Plant Soil 163:25–31

    Google Scholar 

  • Zhang ZJ, Wang ZD, Holden J, Xu XH, Wang H, Ruan JH, Xu H (2012) The release of phosphorus from sediment into water in subtropical wetlands: a warming microcosm experiment. Hydrol Process 26(1):15–26

    Article  Google Scholar 

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Acknowledgments

This study was funded by the Swiss National Science Foundation (project 31003A_122563), ETH North South Centre and University of Brasilia. We thank the staff of IBGE Reserve for logistical support and Yann Hautier for helpful suggestions on a draft version of the manuscript.

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Correspondence to Luciola S. Lannes.

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Responsible Editor: Hans Lambers

Appendices

Appendix 1

Fig. 3
figure 3

Monthly precipitation during the period of the experiment at the IBGE Ecological Reserve. Data from the IBGE meteorological station (http://www.recor.org.br)

Appendix 2

Table 3 Number of plots per experimental site containing invasive C4 grasses, native forbs, native C3 grasses and invasive C4 grasses at the beginning of the experiment.

Appendix 3

Table 4 Soil characteristics for the six experimental sites used in this study. Differences were tested by means of ANOVA + Tukey test Averages and SE are shown. n = 3, P < 0.05

Appendix 4. Forms and dosages of nutrients applied in the fertilization plots.

Control (control) – Water only.

Nitrogen (N) – 20 g m−2 of nitrogen supplied as NH4NO3.

Phosphorus (P) – 5 g m−2 of phosphorus supplied as Na2HPO4.

Nitrogen and phosphorus (N + P) – Simultaneous addition of nitrogen and phosphorus as described above.

Cations and micronutrients (‘cations’) – This treatment was applied to test whether other nutrient than N or P was limiting growth. The combination of cations followed Cech et al. (2008). It consisted of 5 g m−2 of potassium (KCl) + 5 g m−2 of calcium (CaCl2.2H2O) + 1.4 g m−2 of magnesium (MgSO4.7H2O) + 0.04 g m−2 of iron (FeCl2.4H2O) + 0.032 g m−2 of manganese (MnCl2.4H2O) + 0.012 g m−2 of zinc (ZnSO4.7H2O) + 0.020 g m−2 of boron (H3BO3) + 0.016 g m−2 of copper (CuSO4.5H2O) + 0.002 g m−2 of molybdenum (Na2MoO4.2H2O).

All nutrients (N + P+ ‘cations’) – Simultaneous addition of nitrogen, phosphorus and cations as described above.

Appendix 5

Table 5 Effects of 3 years of vegetation clipping on biomass of the control plots. F values and significance levels resulting from one-way ANOVA are shown. N = 5. For P < 0.05, one significant value was detected (shown in bold)

Appendix 6

Fig. 4
figure 4

Aboveground biomass responses to the six fertilization treatments in six sites in the Cerrado in the three years of experiment. The effects of nutrient additions on total biomass and biomass partitioned into functional groups were tested using ANOVA + 2-sided Dunnett test, P < 0.05. Error bars correspond to the standard errors of the mean of total biomass (n = 5). Asterisks indicate significant differences between the treatments and control plots, placed above the error bars for total biomass and indicated in the respective sub-bar for the functional groups

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Lannes, L.S., Bustamante, M.M.C., Edwards, P.J. et al. Native and alien herbaceous plants in the Brazilian Cerrado are (co-)limited by different nutrients. Plant Soil 400, 231–243 (2016). https://doi.org/10.1007/s11104-015-2725-9

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Keywords

  • Invasive grasses
  • Nutrient limitation
  • N:P ratio
  • Nutrients
  • Savanna
  • Stoichiometry