Hostname: page-component-848d4c4894-ttngx Total loading time: 0 Render date: 2024-05-19T02:45:17.930Z Has data issue: false hasContentIssue false

Effects of nutrient addition on polyphenol and nutrient concentrations in leaves of woody species of a savanna woodland in Central Brazil

Published online by Cambridge University Press:  11 October 2019

Tamiel Khan Baiocchi Jacobson*
Affiliation:
Faculdade UnB Planaltina, Universidade de Brasília, Planaltina-DF, 73300-000, Brazil
Mercedes Maria da Cunha Bustamante
Affiliation:
Departamento de Ecologia, Universidade de Brasília, Brasília-DF, 70919-970, Brazil
*
*Author for correspondence: Tamiel Khan Baiocchi Jacobson, Email: tamiel@unb.br

Abstract

We investigated whether changes in nutrient availability affected N, P, S and polyphenol concentrations in different leaf-development stages of three brevideciduous and three evergreen dominant woody species in a nutrient-limited savanna woodland in Central Brazil. Treatments included eight years of annual fertilization with 100 kg ha−1 of N, P, N plus P and control, each replicated in four randomized 15 × 15-m plots. All species increased S concentrations (minimum 28%) in young and mature leaves in fertilized plots. Dalbergia miscolobium decreased total phenol concentrations with P (−34.3%, −23.7%) and NP fertilization (−28.2%, −17.1%). Blepharocalyx salicifolius increased total phenol (27.6%, 18.8%) and tannin (46.3%; 43.5%) in P fertilized and increased total phenol (33.9%) and tannin (27.8%, 43.5%) in NP fertilized plots. Total phenol concentration decreased with leaf age in Ouratea hexasperma, Styrax ferrugineus and Blepharocalyx salicifolius, which also decreased tannin concentration with leaf age. For all treatments, brevideciduous species had higher N, P, total phenols and tannin concentrations and lower S concentration than evergreens. These differences between phenological groups suggest that tropical ecosystems responses to environmental changes are more complex than anticipated by global vegetation models, with consequences for predictions in ecosystem functions and resilience.

Type
Research Article
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature cited

Aerts, R and Chapin, FS (2000) The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Advances in Ecological Research 30, 167.Google Scholar
Bieras, AC and Sajo, MDG (2009) Leaf structure of the cerrado (Brazilian savanna) woody plants. Trees – Structure and Function 23, 451471.CrossRefGoogle Scholar
Bobbink, R, Hicks, K, Galloway, J, Spranger, T, Alkemade, R, Ashmore, M, Bustamante, M, Cinderby, S, Davidson, E, Dentener, F, Emmett, B, Erisman, JW, Fenn, M, Gilliam, F, Nordin, A, Pardo, L and De Vries, W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity : a synthesis. Ecological Applications 20, 3059.CrossRefGoogle Scholar
Bryant, JP, Chapin, FS and Klein, DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40, 357368.CrossRefGoogle Scholar
Bustamante, MMC, Medina, E, Asner, G, Nardoto, GB and Garcia-Montiel, DC (2006) Nitrogen cycling in tropical and temperate savannas. Biogeochemistry 79, 209237.CrossRefGoogle Scholar
Bustamante, MMC, Brito, DQ, Kozovits, AR, Luedemann, G, Mello, TRB, Siqueira Pinto, A, Munhoz, CBR and Takahashi, FSC (2012) Effects of nutrient additions on plant biomass and diversity of the herbaceous-subshrub layer of a Brazilian savanna (Cerrado). Plant Ecology 213, 795808.CrossRefGoogle Scholar
Chan, KX, Wirtz, M, Phua, SY, Estavillo, GM and Pogson, BJ (2013) Balancing metabolites in drought: the sulfur assimilation conundrum. Trends in Plant Science 18, 1829.CrossRefGoogle ScholarPubMed
Chapin, FS (1995) New cog in the nitrogen cycle. Nature 377, 1920.Google Scholar
Coley, PD, Bryant, JP and Chapin, FS (1985) Resource availability and plant antiherbivore defense. Science 230, 895899.CrossRefGoogle ScholarPubMed
Covelo, F and Gallardo, A (2004) Green and senescent leaf phenolics showed spatial autocorrelation in a Quercus robur population in northwestern Spain. Plant and Soil 259, 267276.CrossRefGoogle Scholar
Eiten, G (1983) Classificação da vegetação do Brasil. CNPq, Brasília. 305 pp.Google Scholar
EMBRAPA (1999) Manual de análises químicas de solos, plantas e fertilizantes. Embrapa, Brasília. 370 pp.Google Scholar
Escarpa, A and González, M (2001) Approach to the content of total extractable phenolic compounds from different food samples by comparison of chromatographic and spectrophotometric methods. Analytica Chimica Acta 427, 119127.CrossRefGoogle Scholar
Forrest, GI and Bendall, DS (1969) The distribution of polyphenols in the tea plant (Camellia sinensis L.). The Biochemical Journal 113, 741755.CrossRefGoogle Scholar
Franco, AC, Bustamante, M, Caldas, LS, Goldstein, G, Meinzer, FC, Kozovits, AR, Rundel, P and Coradin, VTR (2005) Leaf functional traits of Neotropical savanna trees in relation to seasonal water deficit. Trees 19, 326335.CrossRefGoogle Scholar
Françoso, RD (2014) Padrões biogeográficos e composição das comunidades arbóreas do Cerrado brasileiro. PhD thesis. University of Brasília, Brasília, Brasil. 159 pp.Google Scholar
Françoso, RD, Haidar, RF and Machado, RB (2016) Tree species of South America central savanna: endemism, marginal areas and the relationship with other biomes. Acta Botanica Brasilica 30, 19.CrossRefGoogle Scholar
Goldstein, G, Meinzer, FC, Bucci, SJ, Scholz, FG, Franco, AC and Hoffmann, WA (2008) Water economy of neotropical savanna trees: six paradigms revisited. Tree Physiology 28, 395404.CrossRefGoogle ScholarPubMed
Gonçalves-Alvim, SJ, Korndorf, G and Fernandes, GW (2006) Sclerophylly in Qualea parviflora (Vochysiaceae): influence of herbivory, mineral nutrients, and water status. Plant Ecology 187, 153162.CrossRefGoogle Scholar
Gonçalves-Alvim, SJ, Lana, TC, Ranieri, BD and Fernandes, GW (2011) Test of hypotheses about herbivory and chemical defences of Qualea parviflora (Vochysiaceae) in Brazilian Cerrado. Revista Brasileira de Botânica 34, 223230.Google Scholar
Hagerman, AE (2002) Tannin Chemistry Handbook. https://www.users.miamioh.edu/hagermae/.Google Scholar
Hagerman, AE and Butler, LG (1978) Protein precipitation method for the quantitative determination of tannins. Journal of Agricultural and Food Chemistry 26, 809812.CrossRefGoogle Scholar
Haridasan, M (1992) Observations on soils, foliar nutrient concentrations and floristic composition of cerrado sensu stricto and cerradão communities in central Brazil. In Proctor, J, Ratter, JA and Furley, PA (eds), Nature and Dynamics of Forest-savanna. London: Chapman & Hall, pp. 171184.Google Scholar
Haridasan, M (1994) Solos do Distrito Federal. In Novais-Pinto, M (ed.), Cerrado: caracterização, ocupação e perspectivas – o caso do Distrito Federal. Brasília: Editora da UnB/SEMATEC, pp. 321344.Google Scholar
Hättenschwiler, S and Vitousek, PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends in Ecology and Evolution 15, 238242.CrossRefGoogle ScholarPubMed
Hättenschwiler, S, Hagerman, AE and Vitousek, PM (2003) Polyphenols in litter from tropical montane forests across a wide range in soil fertility. Biogeochemistry 64, 129148.CrossRefGoogle Scholar
Hättenschwiler, S, Tiunov, AV and Scheu, S (2005) Biodiversity and litter decomposition in terrestrial ecosystems. Annual Review of Ecology, Evolution, and Systematics 36, 191218.CrossRefGoogle Scholar
Haukioja, E, Ossipov, V, Koricheva, J, Honkanen, T, Larsson, S and Lempka, K (1998) Biosynthetic origin of carbon-based secondary compounds: cause of variable responses of woody plants to fertilization? Chemoecology 8, 133139.CrossRefGoogle Scholar
Herms, DA and Mattson, WJ (1992) The dilemma of plants: to grow or defend. Quarterly Review of Biology 67, 283335.CrossRefGoogle Scholar
Jacobson, TKB (2009) Composição, estrutura e funcionamento de um cerrado sentido restrito submetido a adição de nutrientes em médio prazo. PhD thesis. University of Brasília, Brasíla, Brasil. 172 pp.Google Scholar
Jacobson, TKB, Santos, JGD, Duarte, JB, Farias, JG and Kliemann, HJ (2005) Influência de fatores edáficos na produção de fenóis totais e taninos de duas espécies de barbatimão. Pesquisa Agropecuária Tropical 35, 163169.Google Scholar
Jacobson, TKB, Bustamante, MMC and Kozovits, AR (2011) Diversity of shrub tree layer, leaf litter decomposition and N release in a Brazilian cerrado under N, P and N plus P additions. Environmental Pollution 159, 22362242.CrossRefGoogle Scholar
Kozovits, AR, Bustamante, MMC, Garofalo, CR, Bucci, S, Franco, AC, Goldstein, G and Meinzer, FC (2007) Nutrient resorption and patterns of litter production and decomposition in a neotropical savanna. Functional Ecology 21, 10341043.CrossRefGoogle Scholar
Kraus, TEC, Yu, Z, Preston, CM, Dahlgren, RA and Zasoski, RJ (2003) Linking chemical reactivity and protein precipitation to structural characteristics of foliar tannins. Journal of Chemical Ecology 29, 703–30.CrossRefGoogle ScholarPubMed
Kraus, TEC, Zasoski, RJ and Dahlgren, RA (2004) Fertility and pH effects on polyphenol and condensed tannin concentrations in foliage and roots. Plant and Soil 262, 95109.CrossRefGoogle Scholar
Lenza, E and Klink, CA (2006) Comportamento fenológico de espécies lenhosas em um cerrado sentido restrito de Brasília, DF. Revista Brasileira de Botânica 29, 627638.Google Scholar
Lehmann, CER, Archibald, SA, Hoffmann, WA and Bond, WJ (2011) Deciphering the distribution of the savanna biome. New Phytologist 191, 197209.CrossRefGoogle ScholarPubMed
McCulloch, CE, Searle, SR and Neuhaus, JM (2008) Generalized, Linear, and Mixed Models. New York, NY: Wiley. 424 pp.Google Scholar
McKee, KL, Feller, IC, Popp, M and Wanek, W (2002) Mangrove isotopic 15N and 13C fractionation accross a nitrogen vs. phosphorus limitation gradient. Ecology 83, 10651075.Google Scholar
Montes, R and Medina, E (1977) Seasonal changes in nutrient content of leaves of savanna trees with different behaviour. Geo-Eco-Trop 4, 295307.Google Scholar
Myers, N, Mittermeier, RA, Mittermeier, CG, Da Fonseca, GAB and Kent, J (2000) Biodiversity hotspots for conservation priorities. Nature 403, 853858.CrossRefGoogle ScholarPubMed
Nardoto, GB, Bustamante, MMC, Pinto, AS and Klink, CA (2006) Nutrient use efficiency at ecosystem and species level in savanna areas of Central Brazil and impacts of fire. Journal of Tropical Ecology 22, 191201.CrossRefGoogle Scholar
Nitao, JK, Zangerl, AR and Berenbaum, MR (2002) CNB: requiescat in pace? Oikos 98, 540546.Google Scholar
Northup, RR, Dahlgren, RA and Yu, Z (1995a) Intraspecific variation of conifer phenolic concentration on a marine terrace soil acidity gradient; a new interpretation. Plant and Soil 171, 255262.CrossRefGoogle Scholar
Northup, RR, Yu, Z, Dahlgren, RA and Vogt, K (1995b) Polyphenol control of nitrogen release from pine litter. Nature 377, 227229.CrossRefGoogle Scholar
Northup, R, Dahlgren, R and McColl, J (1998) Polyphenols as regulators of plant-litter-soil interactions in northern California’s pygmy forest: a positive feedback? Biogeochemistry 42, 189220.CrossRefGoogle Scholar
Ratter, JA, Bridgewater, S and Ribeiro, JF (2012) Analysis of the floristic composition of the Brazilian cerrado vegetation III: comparison of the woody vegetation of 376 areas. Edinburgh Journal of Botany 60, 57109.Google Scholar
Santos, SC, Costa, WF, Ribeiro, JP, Guimarães, DO, Ferri, PH, Ferreira, HD and Seraphin, JC (2002) Tannin composition of barbatimão species. Fitoterapia 73, 292299.CrossRefGoogle ScholarPubMed
Saraceno, MI (2006) Efeitos da fertilização a longo prazo no metabolismo fotossintético, nas características foliares e no crescimento em árvores do Cerrado. MSc Dissertation, University of Brasília, Brasília, Brasil. 54 pp.Google Scholar
Sarmiento, G (1984) The Ecology of Neotropical Savannas. Cambridge, MA: Harvard University Press. 234 pp.CrossRefGoogle Scholar
Scholz, FG, Bucci, SJ, Goldstein, G, Moreira, MZ, Meinzer, FC, Domec, JC, Villalobos-Vega, R, Franco, AC and Miralles-Wilhelm, F (2008) Biophysical and life-history determinants of hydraulic lift in neotropical savanna trees. Functional Ecology 22, 773786.CrossRefGoogle Scholar
Sieh, D, Watanabe, M, Devers, EA, Brueckner, F, Hoefgen, R and Krajinky, F (2013) The arbuscular mycorrhizal symbiosis influences sulfur starvation responses of Medicago truncatula. New Phytologist 197, 606616.CrossRefGoogle ScholarPubMed
Skidmore, AK, Ferwerda, JG, Mutanga, O, Van Wieren, SE, Peel, M, Grant, RC, Prins, HHT, Balcik, FB and Venus, V (2010) Forage quality of savannas – simultaneously mapping foliar protein and polyphenols for trees and grass using hyperspectral imagery. Remote Sensing of Environment 114, 6472.CrossRefGoogle Scholar
Souza, JP (2012) Ecological significance of leaf longevity of cerrado woody species. In Bezerra, D and Ferreira, TS (eds), Evergreens: Types, Ecology and Conservation. New York, NY: Nova Science Publishers, pp. 149159.Google Scholar
Sternberg, LDS, Bucci, S, Franco, A, Goldstein, G, Hoffman, WA, Meinzer, FC, Moreira, MZ and Scholz, F (2004) Long range lateral root activity by neo-tropical savanna trees. Plant and Soil 270, 169178.CrossRefGoogle Scholar
Villar, R and Merino, J (2001) Comparison of leaf construction costs in woody species with differing leaf-spans in contrasting ecosystems. New Phytologist 151, 213226.CrossRefGoogle Scholar
Wright, DM, Jordan, GJ, Lee, WG, Duncan, RP, Forsyth, DM, Coomes, DA (2010) Do leaves of plants on phosphorus-impoverished soils contain high concentrations of phenolic defence compounds? Functional Ecology 24, 5261.CrossRefGoogle Scholar
Yu, Z and Dahlgren, RA (2000) Evaluation of methods for measuring polyphenols in conifer foliage. Journal of Chemical Ecology 26, 21192140.CrossRefGoogle Scholar
Zar, JH (1999) Biostatistical Analysis. Englewood Cliffs, NJ: Prentice-Hall. 663 pp.Google Scholar
Supplementary material: File

Jacobson and Bustamante supplementary material

Table S1

Download Jacobson and Bustamante supplementary material(File)
File 17 KB
Supplementary material: File

Jacobson and Bustamante supplementary material

Table S2

Download Jacobson and Bustamante supplementary material(File)
File 18.7 KB