Skip to main content
SpringerLink
Log in

Can ecological strategies be explained by photochemical efficiency in ironstone outcrops vegetation?

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

Abstract

Aims

Vegetation in ironstone outcrops is under potential environmental stressors. The aim of this work was to understand the relationships between the ecological strategies of species from ironstone outcrops in Brazil and their photosynthetic adjustments, and to contribute for the selection of species for the recovery of mined environments.

Methods

A total of 22 species belonging to 12 families were selected over canga vegetation. The physiological characteristics, chlorophyll a fluorescence and chlorophyll indices, were evaluated during the rainy and dry seasons. Analysis of competitor, stress-tolerator and ruderal (CSR) ecological strategies was performed during the rainy season for each species using functional leaf characteristics.

Results

The species presented the following ecological strategies: tolerance to stress (74.76%), competition (22.31%) and ruderality (2.93%). Despite a weak correlation between the ecological stress-tolerant strategy and photosynthetic variables, the low soil fertility and reduced rainfall during the dry season led to photochemical adjustments. The species were divided into five distinct groups based on the ability to use and dissipate excess light energy. Some species showed maintenance or increments in photochemical efficiency parameters, chlorophyll indices, and the capacity to avoid damage to the photosynthetic complex through a photoprotective process during the dry season.

Conclusions

The photochemical responses observed highlighted the diversity of adaptive strategies found in plant species from ironstone outcrops. The different photosynthetic adjustments are related to the competition capacity and stress tolerance mechanisms. Thus, the analyzed physiological parameters can be used for selecting plant species for the recovery of environments impacted by mining companies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  • Abrahão A, Costa PB, Lambers H, Andrade SAL, Sawaya ACHF, Ryan MH, Oliveira RS (2019) Soil types select for plants with matching nutrient-acquisition and-use traits in hyperdiverse and severely nutrient-impoverished Campos rupestres and cerrado in Central Brazil. J Ecol 107:1302–1316

    Article  Google Scholar 

  • Alves R, Silva N, Oliveira J, Medeiros D (2014) Circumscribing campo rupestre–megadiverse Brazilian rocky montane savanas. Braz J Biol 74:355–362

    Article  CAS  PubMed  Google Scholar 

  • Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113

    Article  CAS  PubMed  Google Scholar 

  • Baraldi R, Canaccini F, Cortes S, Magnani F, Rapparini F, Zamboni A, Raddi S (2008) Role of xanthophyll cycle-mediated photoprotection in Arbutus unedo plants exposed to water stress during the Mediterranean summer. Photosynthetica 46:378–386

    Article  CAS  Google Scholar 

  • Barbosa NP, Fernandes GW, Carneiro MA, Júnior LA (2010) Distribution of non-native invasive species and soil properties in proximity to paved roads and unpaved roads in a quartzitic mountainous grassland of southeastern Brazil (rupestrian fields). Biol Invasions 12:3745–3755

    Article  Google Scholar 

  • Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynth Res 25:173–185

    Article  CAS  PubMed  Google Scholar 

  • Bond WJ (2016) Ancient grasslands at risk. Science 351:120–122

    Article  CAS  PubMed  Google Scholar 

  • Buisson E, Le Stradic S, Silveira FA, Durigan G, Overbeck GE, Fidelis A, Fernandes GW, Bond WJ, Hermann JM, Mahy G (2019) Resilience and restoration of tropical and subtropical grasslands, savannas, and grassy woodlands. Biol Rev 94:590–609

    Article  PubMed  Google Scholar 

  • Caminha-Paiva D, Gomes VM, Cunha-Blum J, Alves MJ, Rosa DC, Santiago JC, Negreiros D, Fernandes GW (2022) Floristic mosaics of the threatened brazilian campo rupestre. Nature Conservation Research. Заповедная наука 7:10–18

  • Carmona CP, de Bello F, Azcárate FM, Mason NW, Peco B (2019) Trait hierarchies and intraspecific variability drive competitive interactions in Mediterranean annual plants. J Ecol 107:2078–2089

    Article  Google Scholar 

  • Castro SA, Silveira FA, Marcato MS, Lemos-Filho JP (2018) So close, yet so different: divergences in resource use may help stabilize coexistence of phylogenetically-related species in a megadiverse grassland. Flora 238:72–78

    Article  Google Scholar 

  • Cornelissen J, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich D, Reich PB, Ter Steege H, Morgan H, Van Der Heijden M (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380

    Article  Google Scholar 

  • da Silva Moraes AC, Vitória AP, Rossatto DR, de Miranda LAP, Funch LS (2017) Leaf phenology and morphofunctional variation in Myrcia amazonica DC.(Myrtaceae) in gallery forest and “campo rupestre” vegetation in the Chapada Diamantina, Brazil. Braz J Bot 40:439–450

    Article  Google Scholar 

  • Dayrell RL, Arruda AJ, Pierce S, Negreiros D, Meyer PB, Lambers H, Silveira FA (2018) Ontogenetic shifts in plant ecological strategies. Funct Ecol 32:2730–2741

    Article  Google Scholar 

  • De Carvalho F, De Souza FA, Carrenho R, de Souza Moreira FM, da Conçeição JE, Fernandes GW (2012) The mosaic of habitats in the high-altitude Brazilian rupestrian fields is a hotspot for arbuscular mycorrhizal fungi. Appl Soil Ecol 52:9–19

    Article  Google Scholar 

  • Demmig-Adams B, Adams WW (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21

    Article  CAS  PubMed  Google Scholar 

  • Denney DA, Jameel MI, Bemmels JB, Rochford ME, Anderson JT (2020) Small spaces, big impacts: contributions of micro-environmental variation to population persistence under climate change. AoB Plants 12:plaa005

    Article  PubMed  PubMed Central  Google Scholar 

  • Do Carmo FF, Jacobi CM (2016) Diversity and plant trait-soil relationships among rock outcrops in the Brazilian Atlantic rainforest. Plant Soil 403:7–20

    Article  Google Scholar 

  • do Carmo FF, de Campos IC, Jacobi CM (2016) Effects of fine-scale surface heterogeneity on rock outcrop plant community structure. J Veg Sci 27:50–59

    Article  Google Scholar 

  • Dudley N, Eufemia L, Fleckenstein M, Periago ME, Petersen I, Timmers JF (2020) Grasslands and savannahs in the UN Decade on Ecosystem Restoration. Restor Ecol 28:1313–1317

  • Fenollosa E, Munné-Bosch S (2018) Physiological Plasticity of Plants Facing Climate Change. Annual Plant Reviews online 3:837–866

    Google Scholar 

  • Forup ML, Henson KS, Craze PG, Memmott J (2008) The restoration of ecological interactions: plant–pollinator networks on ancient and restored heathlands. J Appl Ecol 45:742–752

    Article  Google Scholar 

  • Franco AC, Matsubara S, Orthen B (2007) Photoinhibition, carotenoid composition and the co-regulation of photochemical and non-photochemical quenching in neotropical savanna trees. Tree Physiol 27:717–725

    Article  CAS  PubMed  Google Scholar 

  • Genty B, Harbinson J, Cailly AL., Rizza F (1996) Fate of excitation at PS II in leaves: the nonphotochemical side. In third BBSRC Robert Hill symposium on photosynthesis, March (Vol. 31)

  • Giulietti AM, De Menezes NL, Pirani JR, Meguro M, Wanderley MDGL (1987) Flora da Serra do Cipó, Minas Gerais: caracterização e lista das espécies. Boletim de Botânica da universidade de São Paulo 9:1–151

  • Giulietti AM, Pirani JR, Harley RM (1997) Espinhaço Range region, eastern Brazil. In: Davis SD, Heywood VH, Herrera-MacBryde O, Villa-Lobos J, Hamilton AC (eds.) Centres of plant diversity: a guide and strategy for their conservation. Information Press, Oxford, pp 397–404

  • Gomes VM, Assis IR, Hobbs RJ, Fernandes GW (2021) Glomalin-related soil protein reflects the heterogeneity of substrate and vegetation in the campo rupestre ecosystem. J Soil Sci Plant Nutr:1–11

  • Grime JP, Pierce S (2012) The evolutionary strategies that shape ecosystems. Wiley, Hoboken

    Book  Google Scholar 

  • Grime J, Thompson K, Hunt R, Hodgson J, Cornelissen J, Rorison I, Hendry G, Ashenden T, Askew A, Band S (1997) Integrated screening validates primary axes of specialisation in plants. Oikos 79:259–281

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

    Article  CAS  Google Scholar 

  • Hopper SD, Lambers H, Silveira FA, Fiedler PL (2021) OCBIL theory examined: reassessing evolution, ecology and conservation in the world’s ancient, climatically buffered and infertile landscapes. Biol J Linn Soc 133:266–296

  • Jacobi CM, do Carmo FF, de Castro VR (2008) Estudo fitossociológico de uma comunidade vegetal sobre canga como subsídio para a reabilitação de áreas mineradas no Quadrilátero Ferrífero, MG. Revista Árvore 32:345–353

    Article  Google Scholar 

  • Kaiser E, Correa Galvis V, Armbruster U (2019) Efficient photosynthesis in dynamic light environments: a chloroplast's perspective. Biochem J 476:2725–2741

    Article  CAS  PubMed  Google Scholar 

  • Laliberté E, Zemunik G, Turner BL (2014) Environmental filtering explains variation in plant diversity along resource gradients. Science 345:1602–1605

    Article  PubMed  Google Scholar 

  • Lambers H, Oliveira RS (2019) Introduction: history, assumptions, and approaches. Plant physiological ecology. Springer, Berlin

  • Lambers H, Brundrett MC, Raven JA, Hopper SD (2011) Plant mineral nutrition in ancient landscapes: high plant species diversity on infertile soils is linked to functional diversity for nutritional strategies. Plant Soil 348:7–27

    Article  CAS  Google Scholar 

  • Le Stradic S, Fernandes GW, Buisson E (2018) No recovery of campo rupestre grasslands after gravel extraction: implications for conservation and restoration. Restor Ecol 26:S151–S159

    Article  Google Scholar 

  • Lemos Filho JPD (2000) Fotoinibição em três espécies do cerrado (Annona crassifolia, Eugenia dysenterica e Campomanesia adamantium) na estação seca e na chuvosa. Braz J Bot 23:45–50

    Article  Google Scholar 

  • Manzoni S, Čapek P, Mooshammer M, Lindahl BD, Richter A, Šantrůčková H (2017) Optimal metabolic regulation along resource stoichiometry gradients. Ecol Lett 20:1182–1191

    Article  PubMed  Google Scholar 

  • Melis A, Spangfort M, Andersson B (1987) Light-absorption and electron-transport balance between photosystem II and photosystem I in spinach chloroplasts. Photochem Photobiol 45:129–136

    Article  CAS  Google Scholar 

  • Messias MCTB, Leite MGP, Neto JAAM, Kozovits AR, Tavares R (2013) Soil-vegetation relationship in quartzitic and ferruginous Brazilian rocky outcrops. Folia Geobotanica 48:509–521

    Article  Google Scholar 

  • Navarro-Cano JA, Goberna M, Verdú M (2019) Using plant functional distances to select species for restoration of mining sites. J Appl Ecol 56:2353–2362

    Article  Google Scholar 

  • Negreiros D, Fernandes GW, Silveira FA, Chalub C (2009) Seedling growth and biomass allocation of endemic and threatened shrubs of rupestrian fields. Acta Oecol 35:301–310

    Article  Google Scholar 

  • Negreiros D, Fernandes GW, Berbara RLL, Rodarte LHO, Pimentel de Ulhôa Barbosa N (2011) Caracterização físico-química de solos quartzíticos degradados e áreas adjacentes de campo rupestre na Serra do Cipó, MG, Brasil. Neotropical Biology & Conservation 6:156–161

  • Negreiros D, Le Stradic S, Fernandes GW, Rennó HC (2014) CSR analysis of plant functional types in highly diverse tropical grasslands of harsh environments. Plant Ecol 215:379–388

    Article  Google Scholar 

  • Nunes JA, Schaefer CE, Ferreira Júnior WG, Neri AV, Correa GR, Enright NJ (2015) Soil-vegetation relationships on a banded ironstone'island', Carajás plateau, Brazilian eastern Amazonia. An Acad Bras Cienc 87:2097–2110

    Article  CAS  PubMed  Google Scholar 

  • Parr CL, Lehmann CE, Bond WJ, Hoffmann WA, Andersen AN (2014) Tropical grassy biomes: misunderstood, neglected, and under threat. Trends Ecol Evol 29:205–213

    Article  PubMed  Google Scholar 

  • Pereira EG, Siqueira-Silva AI, de Souza AE, Melo NMJ, Souza JP (2018) Distinct ecophysiological strategies of widespread and endemic species from the megadiverse campo rupestre. Flora 238:79–86

    Article  Google Scholar 

  • Perez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte M, Cornwell W, Craine J, Gurvich D (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust Bot 61:167–234

    Article  Google Scholar 

  • Perez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte M, Cornwell WK, Craine JM, Gurvich DE (2016) Corrigendum to: new handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 64:715–716

    Article  Google Scholar 

  • Pierce S, Negreiros D, Cerabolini BE, Kattge J, Díaz S, Kleyer M, Shipley B, Wright SJ, Soudzilovskaia NA, Onipchenko VG (2017) A global method for calculating plant CSR ecological strategies applied across biomes world-wide. Funct Ecol 31:444–457

    Article  Google Scholar 

  • Reich PB (2014) The world-wide ‘fast–slow’plant economics spectrum: a traits manifesto. J Ecol 102:275–301

    Article  Google Scholar 

  • Resende F, Fernandes G, Coelho M (2013) Economic valuation of plant diversity storage service provided by Brazilian rupestrian grassland ecosystems. Braz J Biol 73:709–716

    Article  CAS  PubMed  Google Scholar 

  • Rios CO, Siqueira-Silva AI, Pereira EG (2021) How does drought affect native grasses’ photosynthesis on the revegetation of iron ore tailings? Environ Sci Pollut Res 28:14797–14811

    Article  CAS  Google Scholar 

  • R Core Team (2016) R: A Language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

  • Schaefer CE, Cândido HG, Corrêa GR, Nunes JA, Arruda DM (2016) Soils associated with rupestrian grasslands. Ecology and Conservation of Mountaintop grasslands in Brazil. Springer, Berlin

  • Schützendübel A, Polle A (2002) Plant responses to abiotic stresses: heavy metal-induced oxidative stress and protection by mycorrhization. J Exp Bot 53:1351–1365

    PubMed  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 2012:1–26

  • Silva CE, Kellner JR, Clark DB, Clark DA (2013) Response of an old-growth tropical rainforest to transient high temperature and drought. Glob Chang Biol 19:3423–3434

    PubMed  Google Scholar 

  • Silveira FA, Negreiros D, Barbosa NP, Buisson E, Carmo FF, Carstensen DW, Conceição AA, Cornelissen TG, Echternacht L, Fernandes GW (2016) Ecology and evolution of plant diversity in the endangered campo rupestre: a neglected conservation priority. Plant Soil 403:129–152

    Article  CAS  Google Scholar 

  • Siqueira-Silva AI, Rios CO, Pereira EG (2019) Iron toxicity resistance strategies in tropical grasses: the role of apoplastic radicular barriers. J Environ Sci 78:257–266

    Article  CAS  Google Scholar 

  • Skirycz A, Castilho A, Chaparro C, Carvalho N, Tzotzos G, Siqueira JO (2014) Canga biodiversity, a matter of mining. Front Plant Sci 5:653

    Article  PubMed  PubMed Central  Google Scholar 

  • Sperry JS (2000) Hydraulic constraints on plant gas exchange. Agric For Meteorol 104:13–23

    Article  Google Scholar 

  • Tameirão LB, Caminha-Paiva D, Negreiros D, Veloso MDDM, Berbara RL, Dias LE, Pierce S, Fernandes GW (2021) Role of environmental filtering and functional traits for species coexistence in a harsh tropical montane ecosystem. Biol J Linn Soc 133:546–560

    Article  Google Scholar 

  • Teixeira PC, Donagemma GK, Fontana A, Teixeira WG (2017) Manual de métodos de análise de solo in: EMBRAPA (ed), Embrapa Solos. Brasília, DF, pp 573

  • Turcotte MM, Levine JM (2016) Phenotypic plasticity and species coexistence. Trends Ecol Evol 31:803–813

    Article  PubMed  Google Scholar 

  • Turner BL, Condron LM (2013) Pedogenesis, nutrient dynamics, and ecosystem development: the legacy of TW Walker and JK Syers. Springer, Berlin

    Google Scholar 

  • Vasconcelos J, da Silva Lopes JM, de Ruivo M (2016) Solos metalíferos: atributos químicos nas diferentes fitofisionomias da Serra Sul, Serra dos Carajás, Pará, Brasil metalliferous soils: chemical attributes in different phytophysiognomies of the Serra Sul, Serra dos Carajás, Pará, Brazil. Bol Mus Para Emílio Goeldi Cienc Nat 11:49–55

    Article  Google Scholar 

  • Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–320

    Article  CAS  PubMed  Google Scholar 

  • Vieira EA, das Graças Silva M, Moro CF, Laura VA (2017) Physiological and biochemical changes attenuate the effects of drought on the Cerrado species Vatairea macrocarpa (Benth.) Ducke. Plant Physiol Biochem 115:472–483

    Article  CAS  PubMed  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JH, Diemer M (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

  • Zappi DC, Moro MF, Meagher TR, Nic Lughadha E (2017) Plant biodiversity drivers in Brazilian Campos Rupestres: insights from phylogenetic structure. Front Plant Sci 8. https://doi.org/10.3389/fpls.2017.02141

Download references

Acknowledgements

The authors thank Fernando A. de Oliveira e Silveira, Daniel Negreiros and Eliemar Campostrini for valuable feedback.

Funding

This work was supported by the Foundation for Research Development of Minas Gerais State (FAPEMIG) and Vale S.A.. E. G. Pereira is supported by the National Council for Scientific and Technological Development (CNPq) with a research productivity grant.

Author information

Authors and Affiliations

  1. Graduate program in Plant Biology, Institute of Biological Sciences, Federal University of Minas Gerais (UFMG), Belo Horizonte, Minas Gerais, Brazil

    Camilla Oliveira Rios

  2. Institute of Biological and Health Sciences, Federal University of Viçosa (UFV), Campus Florestal, Florestal, Minas Gerais, Brazil

    Paulo Antônio Pimentel & Eduardo Gusmão Pereira

  3. Faculty of Agrobiology and Food Resources, Department of Plant Physiology, Slovak University of Agriculture, Nitra, Slovakia

    Marek Živčák & Marián Brestič

Authors
  1. Camilla Oliveira Rios
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paulo Antônio Pimentel
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marek Živčák
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marián Brestič
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eduardo Gusmão Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

EGP: Funding acquisition and resources, project administration, supervision, conceptualization, formal analysis, writing-reviewing, and editing. COR: conceptualization, investigation, formal analysis, writing-original draft. PAP: investigation, writing-reviewing and editing. MZ and MB: formal analysis, writing-reviewing, and editing. All authors approved the manuscript.

Corresponding author

Correspondence to Eduardo Gusmão Pereira.

Ethics declarations

Competing interests

The authors declare that they have no conflict of interest. All authors approved the manuscript.

Additional information

Responsible Editor: Hans Lambers.

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(PDF 370 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rios, C.O., Pimentel, P.A., Živčák, M. et al. Can ecological strategies be explained by photochemical efficiency in ironstone outcrops vegetation?. Plant Soil 480, 105–120 (2022). https://doi.org/10.1007/s11104-022-05562-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-022-05562-7

Keywords

Search

Navigation