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Physiological parameters and plasticity as key factors to understand pioneer and late successional species in the Atlantic Rainforest

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Abstract

Although there has been a long tradition in plant ecology of grouping species into functional groups, there is a lack of consensus regarding both the successional status of species and the dynamics of forest recovery. Therefore, plant species are commonly classified into two groups: early successional pioneers and late successional or even climax species. Here, we aimed to answer the following question: if pioneer and late successional species have different photosynthetic characteristics, will these differences be translated to improved performance when plants are grown under similar conditions, particularly high irradiance and different water regimes? To this end, we investigated gas exchange, photoprotection, plasticity, and nutritional traits in ten native species that were subject to natural variations in photosynthetically active radiation, rainfall, and air temperature throughout the year. Our results provided evidence that photosynthesis is directly dependent on nitrogen and phosphorus. Remarkably, this characteristic increased in importance when the species were grouped into pioneer and late successional species compared with each species separately. Furthermore, principal component analysis demonstrated that physiological traits are excellent parameters for characterizing the pioneer and late successional plants growing in situ under the same irradiance. Our findings indicate that the responses of trees to seasonal variations depend on their ability to absorb nutrients to meet the mineral requirements to sustain long-term growth. We further analyzed the mechanisms that allow woody species to cope with drought stress.

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References

  • Abrams MD, Mostoller SA (1995) Gas exchange, leaf structure and nitrogen in contrasting successional tree species growing in open and understory sites during a drought. Tree Physiol 15:361–370

    Article  CAS  Google Scholar 

  • Camargos-Antunes W, Rêgo KM, Rodrigues AMC, Ometto JP, Jarma-Orozco A, Pompelli MF (2016) Spondias tuberosa trees grown in tropical, wet environments are more susceptible to drought than those grown in arid environments. Revista Colombiana de Ciencias Hortícolas 10:9–27

    Article  Google Scholar 

  • Dusenge ME, Wallin G, Gârdesten J, Niyonzima F, Adolfsson L, Nsabimana D, Uddling J (2015) Photosynthetic capacity of tropical montane tree species in relation to leaf nutrients, successional strategy and growth temperature. Oecologia 117:1183–1194

    Article  Google Scholar 

  • Ellis AR, Hubbell SP, Potvin C (2000) In situ field measurements of photosynthetic rates of tropical tree species: a test of the functional group hypothesis. Can J Bot 78:1336–1347

    Google Scholar 

  • Ewe SM, Sternberg LSL (2003) Seasonal gas exchange characteristics of Schinus terebinthifolius in a native and disturbed upland community in Everglades National Park, Florida. For Ecol Manag 179:27–36

    Article  Google Scholar 

  • Faber-Langendoen D (1992) Ecological constraints on rain forest management at Bajo Calima, western Colombia. For Ecol Manag 53:213–244

    Article  Google Scholar 

  • Favaretto VF, Martinez CA, Soriani HH, Furriel RPM (2011) Differential responses of antioxidant enzymes in pioneer and late-successional tropical tree species grown under sun and shade conditions. Environ Exp Bot 70:20–28

    Article  CAS  Google Scholar 

  • Gustafsson M, Gustafsson L, Alloysius D, Falck J, Yap S, Karlsson A, Ilstedt U (2016) Life history traits predict the response to increased light among 33 tropical rainforest tree species. For Ecol Manag 362:20–28

    Article  Google Scholar 

  • Gyimah R, Nakao T (2007) Early growth and photosynthetic responses to light in seedlings of three tropical species differing in successional strategies. New For 33:217–236

    Article  Google Scholar 

  • Hogan KP, Smith AP, Samaniego M (1995) Gas exchange in six tropical semi-deciduous canopy tree species during the wet and dry seasons. Biotropica 27:324–333

    Article  Google Scholar 

  • Howell TA (1995) Comparison of vapor-pressure-deficit calculation methods—southern high plains. J Irrig Drain Eng. https://doi.org/10.1061/(asce)0733-9437(1995)1121:1062(1191)

    Article  Google Scholar 

  • Hsie BS, Mendes KR, Antunes WC, Endres L, Campos MLO, Souza FC, Santos ND, Singh B, Arruda ECP, Pompelli MF (2015) Jatropha curcas L. (Euphorbiaceae) modulates stomatal traits in response to leaf-to-air vapor pressure deficit. Biomass Bioenergy 81:273–281

    Article  Google Scholar 

  • Jia Y, Gray VM (2004) Influence of phosphorus and nitrogen on photosynthetic parameters and growth in Vicia faba L. Photosynthetica 42:535–542

    Article  CAS  Google Scholar 

  • Krause GH, Koroleva OY, Dalling W, Winter K (2001) Acclimation of tropical tree seedlings to excessive light in simulated tree-fall gaps. Plant Cell Environ 24:1345–1352

    Article  CAS  Google Scholar 

  • Larcher W (2006) Physiological plant ecology. Springer, Berlin

    Google Scholar 

  • Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Ann Rev Plant Physiol Plant Mol Biol 45:633–662

    Article  CAS  Google Scholar 

  • Mendes KR, Marenco RA (2015) Photosynthetic traits of tree species in response to leaf nutrient content in the central Amazon. Theor Exp Plant Physiol 27:51–59

    Article  CAS  Google Scholar 

  • Moraes GABK, Chaves ARM, Martins SCV, Barros RS, DaMatta FM (2010) Why is it better to produce coffee seedlings in full sunlight than in the shade? A morphophysiological approach. Photosynthetica 48:199–207

    Article  Google Scholar 

  • Pearcy RW (1987) Photosynthetic gas exchange responses of Australian tropical forest trees in canopy, gap and understorey micro-environments. Funct Ecol 1:169–178

    Article  Google Scholar 

  • Peel MC, Finlayson BL, McMahon TA (2007) Updated world map of the Köppen-Geiger climate classification. Hydrol Earth Syst Sci 11:1633–1644

    Article  Google Scholar 

  • Pessoa LM, Pinheiro TS, Alves MCJL, Pimentel RMM, Zickel CS (2009) Flora lenhosa em um fragmento urbano de Floresta Atlântica em Pernambuco. Rev Geogr 26:247–262

    Google Scholar 

  • Pompelli MF, Martins SCV, Antunes WC, Chaves ARM, DaMatta FM (2010) Photosynthesis and photoprotection in coffee leaves is affected by nitrogen and light availabilities in winter conditions. J Plant Physiol 167:1052–1060

    Article  CAS  Google Scholar 

  • Poorter H, Garnier E (2007) Ecological significance of inherent variation in relative growth rate and its components. In: Pugnaire FI, Valladares F (eds) Functional plant ecology. CRC Press, Florida

    Google Scholar 

  • R-Core-Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reich PB, Ellsworth DS, Uhl C (1995) Leaf carbon and nutrient assimilation and conservation in species of differing status in oligotrophic Amazonian forest. Funct Ecol 9:65–76

    Article  Google Scholar 

  • Ribeiro RV, Souza GM, Oliveira RF, Machado EC (2005) Photosynthetic responses of tropical tree species from different succesional groups under contrasting irradiance conditions. Rev Bras Bot 28:149–161

    Article  Google Scholar 

  • Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153

    Article  Google Scholar 

  • Sanches MC, Ribeiro SP, Dalvi VC, da Silva MB, de Souza HC, Lemos-Filho JP (2010) Differential leaf traits of a neotropical tree Cariniana legalis (Mart.) Kuntz (Lecythidaceae): comparing saplings and emergent trees. Trees 24:79–88

    Article  Google Scholar 

  • Schlichting CD, Smith H (2002) Phenotypic plasticity: linking molecular mechanisms with evolutionary outcomes. Evol Ecol 16:189–211

    Article  Google Scholar 

  • Silva FC (2009) Manual de análises químicas de solos, plantas e fertilizantes, 2nd edn. Embrapa Informação Tecnológica, Brasília

    Google Scholar 

  • Silva-Junior V, Souza DG, Queiroz RT, Souza LG, Ribeiro EMS, Santos BA (2018) Landscape urbanization threatens plant phylogenetic diversity in the Brazilian Atlantic Forest. Urban Ecosyst 21:625–634

    Article  Google Scholar 

  • SOS Mata Atlântica F (2016) Acesso às Informações do Atlas dos Remanescentes Florestais, Fundação SOS Mata Atlântica, São Paulo. Relatório técnico, estudos ambientais complementares, download dos mapas em formato SHAPE

  • Strauss-Debenedetti S, Bazzaz FA (1991) Plasticity and acclimation to light in tropical Moraceae of different successional positions. Oecologia 87:377–387

    Article  CAS  Google Scholar 

  • Sudene (2017) Programa de monitoramento climático em tempo real da região Nordeste, Centro de Previsão de Tempo e Estudos Climáticos, Cachoeira Paulista

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

    Article  Google Scholar 

  • Valladares F, Niinemets U (2008) Shade tolerance, a key plant feature of complex nature and consequences. Annu Rev Ecol Evol Syst 39:237–257

    Article  Google Scholar 

  • van Bodegom PM, Douma JC, Witte JPM, Ordonez JC, Bartholomeus RP, Aerts R (2012) Going beyond limitations of plant functional types when predicting global ecosystem-atmosphere fluxes: exploring the merits of traits-based approaches. Glob Ecol Biogeogr 21:625–636

    Article  Google Scholar 

  • Veloso HP, Rangel-Filho ALR, Lima JCA (1991) Classificação da vegetação brasileira adaptada a um sistema universal. IBGE, Rio de Janeiro

    Google Scholar 

  • Wickham H, Chang W (2016) Ggplot2: create elegant data visualisations using the grammar of graphics. https://CRAN.Rproject.org/package=ggplot2. Acessed 26 July 2019

  • Wright SJ, Kitajima K, Kraft NJB, Reich PB, Wright IJ, Bunker DE, Condit R, Dalling JW, Davies SJ, Díaz S, Engelbrecht BMJ, Harms KE, Hubbell SP, Marks CO, Ruiz-Jaen MC, Salvador CM, Zanne AE (2010) Functional traits and the growth-mortality trade-off in tropical trees. Ecology 91:3664–3674

    Article  Google Scholar 

  • Zappi DC, Ranzato Filardi FL, Leitman P, Souza VC, Walter BMT, Pirani JR, Morim MP, Queiroz LP, Cavalcanti TB, Mansano VF, Forzza RC (2015) Growing knowledge: an overview of seed plant diversity in Brazil. Rodriguésia 66:1085–1113

    Article  Google Scholar 

  • Zelitch I (1982) The close relationship between net photosynthesis and crop yield. Bioscience 32:796–802

    Article  Google Scholar 

Download references

Acknowledgements

The authors thank to Agência Estadual de Meio Ambiente–CPRH by Secretaria de Meio Ambiente do Estado de Pernambuco (Grants 03/2013 and 11/2004) and the Foundation for Science and Technology of Pernambuco, FACEPE (Grants APQ-0239-2.03/15) for financially supporting this research. We also thank the scholarships granted by the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES-Brazil) to WBS. The authors acknowledge the helpful comments made by the anonymous referees on previous versions of our manuscript.

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Authors and Affiliations

  1. Departamento de Biologia, Universidade Federal Rural de Pernambuco, Recife, PE, Brazil

    Orlando de Oliveira dos Santos

  2. Departamento of Climatologia, Universidade Federal do Rio Grande do Norte, Natal, RN, Brazil

    Keila Rego Mendes

  3. Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, MG, Brazil

    Samuel Vitor Cordeiro Martins, Willian Batista-Silva & Wagner Luiz Araújo

  4. Instituto Pernambucano de Educação Superior, Recife, PE, Brazil

    Marcos André dos Santos

  5. Agência Estadual de Meio Ambiente, Recife, PE, Brazil

    Joselma Maria de Figueirôa

  6. Departamento de Agronomia, Universidade Federal Rural de Pernambuco, Recife, PE, Brazil

    Edivan Rodrigues de Souza

  7. Instituto Federal Catarinense, Rio do Sul, SC, Brazil

    Denise Fernandes

  8. Laboratório de Ecofisiologia Vegetal, Departmento de Botânica, Universidade Federal de Pernambuco, Recife, PE, 50670-901, Brazil

    Marcelo Francisco Pompelli

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  1. Orlando de Oliveira dos Santos
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  2. Keila Rego Mendes
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  3. Samuel Vitor Cordeiro Martins
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Correspondence to Keila Rego Mendes or Marcelo Francisco Pompelli.

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11738_2019_2931_MOESM4_ESM.tif

Suplementary Fig. 1. Heat map based on correlation matrix between all gas exchange and fluorescence parameters, registered in field conditions where hot colors represent positive correlation, cool colors represent negative correlation and white colors represent no significant correlation based on Pearson’s correlation test. (A) Schinus terebinthifolia, (B) Chorisia glaziovii, (C) Erythrina velutina, (D) Caesalpinia echinata, and (E) Clusia nemorosa. Photosynthetic Active Radiation (PAR), net photosynthesis (PN), stomatal conductance (gs), intrinsic water use efficiency (WUEi), leaf temperature measured in the leaf few seconds after gas exchange measurements (Tleaf), internal-to-ambient CO2 concentration ratio (Ci:Ca), vapor pressure deficit (VPD), variable-to-maximum chlorophyll fluorescence of light-adapted leaves (Fv’:Fm’), electron transport rate (ETR) (TIFF 227 kb)

11738_2019_2931_MOESM5_ESM.tif

Suplementary Fig. 2. Heat map based on correlation matrix between all gas exchange and fluorescence parameters, registered in field conditions where hot colors represent positive correlation, cool colors represent negative correlation and white colors represent no significant correlation based on Pearson’s correlation test. (A) Tabebuia aurea, (B) Licania tomentosa, (C) Xylopia frutescens, (D) Manilkara huberi, and (E) Eugenia uniflora. Photosynthetic Active Radiation (PAR), net photosynthesis (PN), stomatal conductance (gs), intrinsic water use efficiency (WUEi), leaf temperature measured in the leaf few seconds after gas exchange measurements (Tleaf), internal-to-ambient CO2 concentration ratio (Ci:Ca), vapor pressure deficit (VPD), variable-to-maximum chlorophyll fluorescence of light-adapted leaves (Fv’:Fm’), electron transport rate (ETR) (TIFF 230 kb)

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dos Santos, O.d., Mendes, K.R., Martins, S.V.C. et al. Physiological parameters and plasticity as key factors to understand pioneer and late successional species in the Atlantic Rainforest. Acta Physiol Plant 41, 145 (2019). https://doi.org/10.1007/s11738-019-2931-9

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