Abstract
Background and aims
The Brazilian Atlantic Forest has been affected by the deposition of Ni and Zn, among other heavy metals adsorbed on atmospheric particles, which can be incorporated into the soil. If available in the soil, they can be absorbed by plant roots. The study aimed at testing experimentally the hypotheses: 1) Ni and Zn depositions increase their bioavailable fractions in the soil; 2) pioneer tree species absorb Ni and Zn from the soil in higher level and less growth changes than non-pioneer species.
Methods
The experiment was carried out with six pioneer and non-pioneer species native to the Atlantic Forest, grown for 90 days in: soil with balanced fertilization (control) and in soil enriched with Ni, Zn or Ni + Zn. At the end, the concentrations of Ni and Zn were determined in four soil fractions (F1: soluble; F2: linked to oxides/hydroxides; F3: linked to organic matter: F4: residual metals) and in leaves, stems/branches and roots. Mobility factors in soil, concentration ratios between treatments and respective controls, translocation efficiency and relative growth rate in height, leaf number and total biomass were also calculated.
Results
The results showed that Ni and Zn concentrations increased significantly in the bioavailable soil fractions (F1, F2). The absolute content of Ni and Zn in the plants directly reflected the soil level in the available forms.
Conclusions
Pioneer tree species absorb Ni and Zn in higher level and show less changes in growth than non-pioneer tree species.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability (data transparency)
Data is available by request to the authors.
Code availability
Not applicable.
References
Ambrosini VG, Rosa DJ, Basso A, Borghezan M, Pescador R, Miotto A, de Melo GWB, Soares CRFS, Comin JJ, Brunetto G (2016) Liming as an ameliorator of copper toxicity in black oat (Avena strigosa Schreb.). J Plant Nutr, 40:3, 404–416. https://doi.org/10.1080/01904167.2016.1240203
Ambrosini VG, Rosa DJ, Prado JPC, Borghezan M, Melo GWB, de; Soares, C. R. F. de S., Comin, J. J., Simão, D. G., Brunetto, G., (2015) Reduction of copper phytotoxicity by liming: a study of the root anatomy of young vines (Vitis labrusca L.). Plant Physiol Biochem 96:270–280. https://doi.org/10.1016/j.plaphy.2015.08.012
Benincasa, M.M.P.(1988). Análise de crescimento de plantas; noções básicas s. Jaboticabal: FUNEP. 42p.
Bochicchio R, Sofo A, Terzano R, Gattullo CE, Amato M, Scopa A (2015) Root architecture and morphometric analysis of Arabidopsis thaliana grown in Cd/Cu/Zn-gradient agar dishes: A new screening technique for studying plant response to metals. Plant Physiol Biochem 91:20–27. https://doi.org/10.1016/j.plaphy.2015.03.010
Bogusz A, Oleszczuk P (2018) Sequential extraction of nickel and zinc in sewage sludge- or biochar/sewage sludge-amended soil. Sci Total Environ 636:927–935. https://doi.org/10.1016/j.scitotenv.2018.04.072
Bogusz A, Oleszczuk P (2019) Adsorption and desorption of heavy metals by the sewage sludge and biochar-amended soil. Environ Geochem Health 41:1663–1664. https://doi.org/10.1007/s10653-017-0036-1
Boukhris A, Laffont-Schwob I, Mezghani I, El Kadri L, Prudent P, Pricop A, Tatoni T, Chaieb M (2016) Screening biological traits and fluoride contents of native vegetations in arid environments to select efficiently fluoride-tolerant native plant species for in-situ phytoremediation. Chemosfere 119:217–223. https://doi.org/10.1016/j.chemosphere.2014.06.007
Brokbartold M, Grupe M, Marschner B (2012) Effectiveness of different soil amendments to reduce the Pb and Zn extractability and plant uptake in soils contaminated by anticorrosion paints beneath pylons. J Plant Nutr Soil Sci 175:443–455. https://doi.org/10.1002/jpln.201100198
Cetesb, (2016). Relatório de qualidade ambiental do estado de São Paulo. Valores Orientadores para Solo e Água Subterrânea no Estado de São Paulo. (www. https://cetesb.sp.gov.br/solo/valores-orientadores-para-solo-e-agua-subterranea.)
Chanu LB, Gupta A (2016) Phytoremediation of lead using Ipomoea aquatica Forsk. In hydroponic solution. Chemosphere 156:407–411
Chen GN, Shah KJ, Shi L, Chiang PC, You ZY (2019) Red soil amelioration and heavy metal immobilization by a multi-element mineral amendment: performance and mechanisms. Environ Pollut 254:9. https://doi.org/10.1016/j.envpol.2019.112964
Costa-Böddeker S, Benion H, Jesus TA, Albuquerque AL, Figueira RCL, Bicudo DC (2012) Paleolimnologically inferred eutrophication of a shallow, tropical, urban reservoir in southeast Brazil. J Paleolimnol 48:751–776. https://doi.org/10.1007/s1093-012-9642-1
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. https://doi.org/10.1016/j.envexpbot.2010.06.003
Fernandes AJ, Reis LAM, Carvalho A. (2002). Caracterização do meio físico. In: Bicudo DC, Forti MC, Bicudo CEM (eds) Parque Estadual das Fontes do Ipiranga: unidade de conservação ameaçada pela urbanização de São Paulo. Secretaria do Meio Ambiente do Estado de São Paulo, São Paulo, pp 49–62.
Ferreira ML, Ribeiro AP, Albuquerque CR, Ferreira APNL, Figueira RCL, Lafortezza R (2017) Air contaminants and litter fall decomposition in urban forest areas: The case of São Paulo - SP, Brazil. Environ Res 155:314–320. https://doi.org/10.1016/j.envres.2017.02.023
Gonnelli C, Renella G (2013) Chromium and Nickel. In: B. J. Alloway and J. T. Trevors (eds.). Heavy Metals in Soils. Trace Metals and Metalloids in Soils and their Bioavailability. Springe. Third Edition pp. 325
Janoš P, Vávrová J, Herzogová L, Pilařová V (2010) Effects of inorganic and organic amendments on the mobility (leachability) of heavy metals in contaminated soil: A sequential extraction study. Geoderma 159:335–341. https://doi.org/10.1016/j.geoderma.2010.08.009
Joly C, Metzger JP, Tabarelli M (2014) Experiences from the Brazilian Atlantic Forest: ecological findings and conservation initiatives. New Phytol 204:459–473. https://doi.org/10.1111/nph.12989
Kabala C, Singh BR (2001) Fractionation and mobility of copper, lead, and zinc in soil profiles in the vicinity of a copper smelter. J Environ Qual 30:485–492. https://doi.org/10.2134/jeq2001.302485x
Kabata-Pendias. (2011). Trace elements in soils and plants. 4 th ed. Wyd. Nauk PWN, Warsaw, 400p. Pendias.
Kalaiarasan G, Balakrishnan RM, Sethunath NA, Manoharan S (2018) Source apportionment studies on particulate matter (PM10 and PM2.5) in ambient air of urban Mangalore. India Journal of Environmental Management 217:815–824. https://doi.org/10.1016/j.jenvman.2018.04.040
Karmakar D, Padhy PK (2019) Air pollution tolerance, anticipated performance, and metal accumulation indices of plant species for greenbelt development in urban industrial área. Chemosphere 237:124522. https://doi.org/10.1016/j.ecoleng.2020.105790
Keshavarzi A, Kumar V (2019) Spatial distribution and potential ecological risk assessment of heavy metals in agricultural soils of Northeastern Iran. Geology, Ecology, and Landscapes 4(2):87–103. https://doi.org/10.1080/24749508.2019.1587588
Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534. https://doi.org/10.1146/annurev-arplant-042809-112156
Lira PK, Tambosi LR, Ewers RM, Metzger JP (2012) Land-use and land-cover change in Atlantic Forest landscapes. For Ecol Manage 278:80–89
Lopes M, Ribeiro Dos Santos A, Zuliani Sandrin Camargo C, Bulbovas P, Giampaoli P, Domingos M (2015) Soil chemical and physical status in semideciduous Atlantic Forest fragments affected by atmospheric deposition in central-eastern São Paulo State, Brazil. iForest - Biogeosciences For. E1–e11. https://doi.org/10.3832/ifor1258-007.
Ma LQ, Rao GN (1997) Chemical fractionation of cadmium, copper, nickel and zinc in contaminated soils. J Environ Qual 26:259–264. https://doi.org/10.2134/jeq1997.00472425002600010036x
Macieira BPB, Locosselli GM, Buckeridge MS, Hartmann H, Cuzzuol GRF (2020) Stem and leaf functional traits allow successional classification in six pioneer and non-pioneer tree species in Tropical Moist Broadleaved Forests. Ecol Ind 113:106254. https://doi.org/10.1016/j.ecolind.2020.106254
Mao et al. (2017) (Mao, L.C., Younga, S.D. Tye A.M, Bailey, E.H. 2017. Predicting trace metal solubility and fractionation in Urban soils fromisotopic exchangeability. Environmental Pollution 231, 1529 – 1542). https://doi.org/10.1016/j.envpol.2017.09.013.
Marques MCM, Trindade W, Bohn A, Grelle CEV (2021) The Atlantic Forest: an introduction to the megadiverse forest of South America. In: Marques M.C.M., Grelle C.E.V. (eds) The Atlantic Forest. Springer, Cham. https://doi.org/10.1007/978-3-030-55322-7_1.
Motuzova GV, Minkina TM, Karpova EA, Barsova NU, Mandzhieva SS (2014) Soil contamination with heavy metals as a potential and real risk to the environment. J Geochem Explor 144, 241e 246. https://doi.org/10.1016/j.gexplo.2014.01.026
Naidu R, Krishnamurti GSR, Bolan NS, Wenzel W, Megharaj M (2001) Heavy metal interactions in soils and implications for soil microbial biodiversity, in: Prasad, M.N.V. (Ed.), Metals in the environment, analysis by biodiversity, CRC Press, Taylor & Francis Group, Boca
Nakazato RK, Lourenço IS, Esposito MP, Lima MEL, Campos ROA, Rinaldi MCS, Domingos M (2021) Trace metals at the tree-litter-soil- interface in Brazilian Atlantic Forest plots surrounded by sources of air pollution. Environ Pollut 268:115797. https://doi.org/10.1016/j.envpol.2020.115797
Palm E, Nissim WG, Giordano C, Mancuso; S; Azzarello; E. (2017) Root potassium and hydrogen flux rates as potential indicators of plant response to zinc, copper and nickel stress. Environ Exp Bot 143:38–50. https://doi.org/10.1016/j.envexpbot.2017.08.009
Patra DK, Pradha C, Patra HK (2020) Toxic metal decontamination by 578 phytoremediation approach: Concept, challenges, opportunities and future perspectives. Environ Technol Inno. 18, 100672
Portes MT, Damineli DSC, Ribeiro RV, Monteiro JAF, Souza GM (2010) Evidence of higher photosynthetic plasticity in the early successional Guazuma ulmifolia Lam. compared to the late successional Hymenaea courbaril L. grown in contrasting light environments. Braz J Biol 70:75–83. https://doi.org/10.1590/S1519-69842010000100011
Rai PR (2016) Impacts of particulate matter pollution on plants: Implications for environmental biomonitoring. Ecotoxicol Environ Saf 129:120–136. https://doi.org/10.1016/j.ecoenv.2016.03.012
van Raij B, Andrade JC, Cantarella H, Quaggio JA (2001) Análise química para avaliação da fertilidade de solos tropicais. Campinas Instituto Agronômico. 285p
Rauret G, Lopez-Sanchez JF, Sahuquillo A, Rubio R, Davidson C, Ure A, Quevauviller PH (1999) Improvement of the BCR three step sequential extraction procedure. J Environ Monit 1999(1):57–61. https://doi.org/10.1039/A807854H
Rees M, Condit R, Crawley M, Palaca S, Tilman D (2001) Long-term studies of vegetation dynamics. – Science 293:650–655. https://doi.org/10.1126/science.1062586
Rieuwerts JS, Ashnore MR, Farago ME, Thornton I (2006) The influence of soil characteristics on the extractability of Cd, Pb and Zn in upland and moorland soils. Sci Total Environ 366:864–875. https://doi.org/10.1016/j.scitotenv.2005.08.023
Rieuwerts JS (2007) The mobility and bioavailability of trace metals in tropical soils: A review. Chem Speciat Bioavailab 19:75–85. https://doi.org/10.3184/095422907X211918
Sanchez-Lopes, Gonzalez RC, Gonzalez-Chaves MCA, Rosas-Saito GH, Vangronsveld J (2015) Phytobarriers: Plants capture particles containing potentially toxic elements originating from mine tailings in semiarid regions. Environ Pollut (2015) 33e42. https://doi.org/10.1016/j.envpol.2015.05.0100
Sánchez-Martín MJ, García-Delgado M, Lorenzo LF, Rodríguez-Cruz MS, Arienzo M (2007) Heavy metals in sewage sludge amended soils determined by sequential extractions as a function of incubation time of soils. Geoderma 142:262–273. https://doi.org/10.1016/j.geoderma.2007.08.012
Sarma H (2011) Metal hyperaccumulation in plants: A review focusing on phytoremediation technology. J Environ Sci Technol 4:118–138. https://doi.org/10.3923/jest.2011.118.138
Shah V, Daverey A (2020) Phytoremediation: A multidisciplinary approach to clean up heavy metal contaminated soil. Environ Technol Innov 18:100774. https://doi.org/10.1016/j.eti.2020.100774
Shinozaki K, Uemura M, Bailey-Serres J, Bray EA, Weretilnyk ER, to abiotic stress. In: Buchanan, B. B., Gruissem, W., Jones, R. L. (eds) (2015) Biochemistry & Molecular Biology of Plants, 2nd edn. John Wiley & Sons Ltd, Chichester, pp 1051–1100
Siqueira MC, Kanashiro S, Domingos M, Rinaldi MCS, Tavares AR (2021) Physiological and biochemical changes in tree seedlings growing in urban forest soil contaminated with copper in São Paulo, Brazil. Plant Soil 464:149–163. https://doi.org/10.1007/s11104-021-04948-3
Song Y, Maher BA, Li F, Wang X, Sun X, Zhang H (2015) Particulate matter deposited on leaf of five evergreen species in Beijing, China: Source identification and size distribution. Atmos Environ 105:53–60. https://doi.org/10.1016/j.atmosenv.2015.01.032
Tanus MR, Pastore M, Bianchini RS, Gomes EPC (2012) Estrutura e composição de um trecho de Mata Atlântica no Parque Estadual das Fontes do Ipiranga, São Paulo, SP, Brasil. Hoehnea 39:157–168. https://doi.org/10.1590/S2236-89062012000100010
Uriarte M, Lasky JR, Boukili VK, Chazdon RL (2016) A trait-mediated, neighborhood approach to quantify climate impacts on successional dynamics of tropical rainforests. Funct Ecol 30(2):157–167. https://doi.org/10.1111/1365-2435.12576
Violante A, Cozzolino V, Perelomov L, Caporale AG, Pigna M (2010) Mobility and bioavailability of heavy metals and metalloids in soil environments. J Soil Sci Plant Nutr 10(3):268–292. https://doi.org/10.4067/S0718-9562010000100005
Zhao M, Zeng S, Liu S, Jing L (2020) Metal accumulation by plants growing in China: Capacity, synergy, and moderator effects. Ecol Eng 148:105790. https://doi.org/10.1016/j.ecoleng.2020.105790
Acknowledgements
We are grateful to the Coordination for the Improvement of Higher Education Personnel (CAPES) and São Paulo Research Foundation (FAPESP, grant number: 2016 / 25642-3), for the scholarships granted to the first author; Parque Estadual das Fontes do Ipiranga, for permitting the soil collection used in the experiment, and Dr. Jorge A. S; Tenório, from Polytechnic School of University of São Paulo, for the soli and plant analyses. The manuscript was edited for grammar, spelling, vocabulary and sentence structure by Rebbeca Hennig.
Funding
This work was supported by Coordination for the Improvement of Higher Education Personnel (CAPES, Brazil) and The São Paulo Research Foundation (FAPESP, Brazil scholarship number granted: 2016 / 25642-3).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Solange Eulália Brandão, Mirian CS Rinaldi and Marisa Domingos: Conceptualization, methodology, validation, formal analysis, research, writing, visualization and project administration. Geane M. Barbosa, Matheus C. Siqueira, Rafaela de O. A. Campos, and Ana C. F. Dalsin: Methodology and research. The first draft of the manuscript was written by Solange Eulália Brandão and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflicts of interest/Competing interests
The authors declare that there is no conflict of interest.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Responsible Editor: Juan Barcelo.
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Brandão, S.E., Barbosa, G.M., Siqueira, M.C. et al. Nickel and zinc absorption and growth of Atlantic Forest trees cultivated in polluted soil. Plant Soil 471, 463–475 (2022). https://doi.org/10.1007/s11104-021-05228-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11104-021-05228-w