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Determination of the maximum bioaccumulation capacity of various metals in leaves of two Tillandsia species

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Abstract

Tillandsia species are plants from the Bromeliaceae family which display biomonitoring capacities in both active and passive modes. The bioaccumulation potential of Tillandsia aeranthos (Loisiel.) Desf. and Tillandsia bergeri Mez acclimated to Southern/Mediterranean Europe has never been studied. More generally, few studies have detailed the maximum accumulation potential of Tillandsia leaves through controlled experiments. The aim of this study is to evaluate the maximum accumulation values of seven metals (Co, Cu, Mn, Ni, Pb, Pt, and Zn) in T. aeranthos and T. bergeri leaves. Plants were immersed in different mono elemental metallic solutions of Co (II), Cu (II), Mn (II), Ni (II), Pb (II), Pt (IV), and Zn (II) ions at different concentrations. In addition, cocktail solutions of these seven metals at different concentrations were prepared to study the main differences and the potential selectivity between metals. After exposure, the content of these metals in the leaves were measured by inductively coupled plasma-optical emission spectrometry. Data sets were evaluated by a fitted regression hyperbola model and principal component analysis, maximum metal loading capacity, and thermodynamic affinity constant were determined. The results showed important differences between the two species, with T. bergeri demonstrating higher capacity and affinity for metals than T. aeranthos. Furthermore, between the seven metals, Pb and Ni showed higher enrichment factors (EF). T. bergeri might be a better bioaccumulator than T. aeranthos with marked selectivity for Pb and Ni, metals of concern in air quality biomonitoring.

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References

  • Ahmad MSA, Ashraf M (2012) Essential roles and hazardous effects of nickel in plants. In: Whitacre D (ed) Reviews of Environmental Contamination and Toxicology. Rev Environ Contam Toxicol, vol 214. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0668-6_6

  • Argun ME, Dursun S, Ozdemir C, Karatas M (2007) Heavy metal adsorption by modified oak sawdust: thermodynamics and kinetics. J Hazard Mater 141:77–85. https://doi.org/10.1016/j.jhazmat.2006.06.095

    Article  CAS  Google Scholar 

  • Belmonte E, Arriaza B, Arismendi M, Sepúlveda G (2022) Foliar anatomy of three native species of Tillandsia L. from the Atacama Desert, Chile. Plants 11:1–11.

    Article  Google Scholar 

  • Benhammou A, Yaacoubi A, Nibou L, Tanouti B (2005) Adsorption of metal ions onto Moroccan stevensite: Kinetic and isotherm studies. J Colloid Interface Sci 282:320–326. https://doi.org/10.1016/j.jcis.2004.08.168

    Article  CAS  Google Scholar 

  • Beringui K, Huamán De La Cruz AR, Maia LFPG, Gioda A (2021) Atmospheric metal biomonitoring along a highway near atlantic rainforest environmental protection areas in Southeastern Brazil. Bull Environ Contam Toxicol 107:84–91.

    Article  CAS  Google Scholar 

  • Bermudez GMA, Rodriguez JH, Pignata ML (2009) Comparison of the air pollution biomonitoring ability of three Tillandsia species and the lichen Ramalina celastri in Argentina. Environ Res 109:6–14. https://doi.org/10.1016/j.envres.2008.08.014

    Article  CAS  Google Scholar 

  • Bernal R, Valverde T, Hernández-Rosas L (2005) Habitat preference of the epiphyte Tillandsia recurvata (Bromeliaceae) in a semi-desert environment in Central Mexico. Can J Bot 83:1238–1247.

    Article  Google Scholar 

  • Bhalerao SA, Sharma AS, Poojari AC (2015) Toxicity of nickel in plants. Int J Pure Appl Biosci 3:345–355

    Google Scholar 

  • Brighigna L, Ravanelli M, Minelli A, Ercoli L (1997) The use of an epiphyte (Tillandsia caput-medusae morren) as bioindicator of air pollution in Costa Rica. Sci Total Environ 198:175–180. https://doi.org/10.1016/S0048-9697(97)05447-8

    Article  CAS  Google Scholar 

  • Cardoso-Gustavson P, Fernandes FF, Alves ES et al (2016) Tillandsia usneoides: a successful alternative for biomonitoring changes in air quality due to a new highway in São Paulo, Brazil. Environ Sci Pollut Res 23:1779–1788.

    Article  CAS  Google Scholar 

  • Colombo C, Oates CJ, Monhemius AJ, Plant JA (2008) Complexation of platinum, palladium and rhodium with inorganic ligands in the environment. Geochem: Explor Environ Anal 8:91–101

    CAS  Google Scholar 

  • Contreras S, Landahur M, García K et al (2022) Leaf wax composition and distribution of Tillandsia landbeckii reflects moisture gradient across the hyperarid Atacama Desert. Plant Syst Evol 308:1–13.

    Article  Google Scholar 

  • da Costa GM, Petry CT, Droste A (2016) Active versus passive biomonitoring of air quality: genetic damage and bioaccumulation of trace elements in flower buds of Tradescantia pallida var. purpurea. Water Air Soil Pollut 227.

  • Dash S, Panda KK, Panda BB (1988) Biomonitoring of low levels of mercurial derivatives in water and soil by Allium micronucleus assay. Mutat 203(1):11–21. https://doi.org/10.1016/0165-1161(88)90003-9

  • De la Cruz ARH, Ayuque RFO, de la Cruz RWH et al (2020) Air quality biomonitoring of trace elements in the metropolitan area of Huancayo, Peru using transplanted Tillandsia capillaris as a biomonitor. An Acad Bras Cienc 92:1–17.

    Article  Google Scholar 

  • De La Cruz ARH, Molina HY, Monrroy XRV et al (2021) Biomonitoring of potentially toxic elements in two polluted areas from Lurigancho-Chosica Using the genus Tillandsia latifolia and T. purpurea as biomonitor. Bull Environ Contam Toxicol 107:69–76.

    Article  Google Scholar 

  • De La Harpe M, Paris M, Hess J et al (2020) Genomic footprints of repeated evolution of CAM photosynthesis in a neotropical species radiation. Plant Cell Environ 43:2987–3001.

  • de Oliveira RS, de Oliveira Souza S, Aona LYS, et al (2021) Leaf structure of Tillandsia species (Tillandsioideae: Bromeliaceae) by light microscopy and scanning electron microscopy. Microsc Res Tech 1–17.

  • de Souza PM, Heitmann D, Reifenhäuser W et al (2007a) Persistent organic pollutants in atmospheric deposition and biomonitoring with Tillandsia usneoides (L.) in an industrialized area in Rio de Janeiro state, southeast Brazil - Part II: PCB and PAH. Chemosphere 67:1736–1745. https://doi.org/10.1016/j.chemosphere.2006.05.141

    Article  CAS  Google Scholar 

  • de Souza PM, Waller U, Reifenhäuser W et al (2007b) Persistent organic pollutants in atmospheric deposition and biomonitoring with Tillandsia Usneoides (L.) in an industrialized area in Rio de Janeiro state, south east Brazil - Part I: PCDD and PCDF. Chemosphere 67:1728–1735. https://doi.org/10.1016/j.chemosphere.2006.05.145

    Article  CAS  Google Scholar 

  • Derakhshan Z, Faramarzian M, Mahvi AH et al (2016) Assessment of heavy metals residue in edible vegetables distributed in Shiraz, Iran. J Food Qual Hazards Control 3:25–29

    CAS  Google Scholar 

  • Eggli U, Gouda EJ (2020) Bromeliaceae. In: Eggli U, Nyffeler R (eds) Monocotyledons. Illustrated Handbook of Succulent Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-56486-8_73

  • Estrella-Parra E, Flores-Cruz M, Blancas-Flores G et al (2019) The Tillandsia genus: history, uses, chemistry, and biological activity. Bol Latinoam Caribe Plantas Med Aromat 18:239–264

    CAS  Google Scholar 

  • Figueiredo AMG, Alcalá AL, Ticianelli RB et al (2004) The use of Tillandsia usneoides L. as bioindicator of air pollution in São Paulo, Brazil. J Radioanal Nucl Chem 259:59–63. https://doi.org/10.1023/B:JRNC.0000015806.15495.89

    Article  CAS  Google Scholar 

  • Freschi L, Rodrigues MA, Tiné MAS, Mercier H (2010) Correlation between citric acid and nitrate metabolisms during CAM cycle in the atmospheric bromeliad Tillandsia pohliana. J Plant Physiol 167:1577–1583. https://doi.org/10.1016/j.jplph.2010.06.002

    Article  CAS  Google Scholar 

  • Garth ARE (2015) The ecology of Spanish moss (Tillandsia Usneoides ): its growth and distribution. Ecology 45:470–481

    Article  Google Scholar 

  • Gouda EJ (2020) Tillandsia BROMELIACEAE. In: Eggli U, Nyffeler R (eds) Monocotyledons. Illustrated Handbook of Succulent Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-662-56486-8_96

  • Gurgatz BM, Carvalho-Oliveira R, de Oliveira DC et al (2016) Atmospheric metal pollutants and environmental injustice: a methodological approach to environmental risk analysis using fuzzy logic and tree bark. Ecol Indic 71:428–437.

    Article  CAS  Google Scholar 

  • Han X, Naeher LP (2006) A review of traffic-related air pollution exposure assessment studies in the developing world. Environ Int 32:106–120. https://doi.org/10.1016/j.envint.2005.05.020

    Article  CAS  Google Scholar 

  • Inglezakis VJ, Zorpas AA, Loizidou MD, Grigoropoulou HP (2005) The effect of competitive cations and anions on ion exchange of heavy metals. Sep Purif Technol 46:202–207. https://doi.org/10.1016/j.seppur.2005.05.008

    Article  CAS  Google Scholar 

  • Jayakumar K, Jaleel CA (2009) Uptake and accumulation of cobalt in plants : a study based on exogenous cobalt in soybean. Botany Res Int 2:310–314

    CAS  Google Scholar 

  • Jeon MW, Ali MB, Hahn EJ, Paek KY (2006) Photosynthetic pigments, morphology and leaf gas exchange during ex vitro acclimatization of micropropagated CAM Doritaenopsis plantlets under relative humidity and air temperature. Environ Exp Bot 55:183–194. https://doi.org/10.1016/j.envexpbot.2004.10.014

    Article  CAS  Google Scholar 

  • Kovács T, Horváth M, Csordás A, et al (2020) Tobacco plant as possible biomonitoring tool of red mud dust fallout and increased natural radioactivity. Heliyon 6.

  • Lasat M (2002) Editorial: The hazardous substance research centers program: an EPA perspective. Environ Prog 21:8–9. https://doi.org/10.1002/ep.670210402

    Article  Google Scholar 

  • Li P, Zhang J, Sun X et al (2021) Atmospheric Pb induced hormesis in the accumulator plant Tillandsia usneoides. Sci Total Environ 811:152384.

    Article  Google Scholar 

  • Manisalidis I, Stavropoulou E, Stavropoulos A, Bezirtzoglou E (2020) Environmental and health impacts of air pollution: a review. Front Public Health 8:1–13.

    Article  Google Scholar 

  • Marié DC, Chaparro MAE, Lavornia JM et al (2018) Atmospheric pollution assessed by in situ measurement of magnetic susceptibility on lichens. Ecol Indic 95:831–840.

    Article  Google Scholar 

  • Mateos AC, Amarillo AC, Carreras HA, González CM (2018) Land use and air quality in urban environments: Human health risk assessment due to inhalation of airborne particles. Environ Res 161:370–380.

    Article  CAS  Google Scholar 

  • Mendoza-Ramos JE, Talavera-Mendoza O, Lopezaraiza-Mikel ME, et al (2021) Biomonitoring and sourcing toxic elements using vascular epiphytes of the tillandsia genus in the mining region of Taxco de Alarcón, Guerrero, Southern Mexico. Water Air Soil Pollut 232.

  • Mhatre GN, Chaphekar SB (1985) The effect of mercury on some aquatic plants. Environ Pollut 39:207–216

    Article  CAS  Google Scholar 

  • Miranda T, Roth-Nebelsick A, Junginger A, Ebner M (2020) Habitat conditions, spatial distribution and trichome morphology of different species of Tillandsia growing on trees on the Ilha Grande Island, Brazil. Flora 272:151692.

    Article  Google Scholar 

  • Nakos M, Pepelanova I, Beutel S et al (2017) Isolation and analysis of vitamin B12 from plant samples. Food Chem 216:301–308.

    Article  CAS  Google Scholar 

  • Nangeelil K, Hall C, Frey W, Sun Z (2022) Biomarker response of Spanish moss to heavy metal air pollution in the low country of the Savannah River basin. J Radioanal Nucl Chem 331:5185–5191.

    Article  CAS  Google Scholar 

  • Niu L, Xu C, Zhou Y, Liu W (2019) Tree bark as a biomonitor for assessing the atmospheric pollution and associated human inhalation exposure risks of polycyclic aromatic hydrocarbons in rural China *. Environ Pollut 246:398–407.

    Article  CAS  Google Scholar 

  • Palit S, Sharma A, Talukder G (1994) Effects of cobalt on plants. Bot Rev 60:149–181. https://doi.org/10.1007/BF02856575

    Article  Google Scholar 

  • Pandey N, Sharma CP (2002) Effect of heavy metals Co 2+, Ni 2+ and Cd 2+ on growth and metabolism of cabbage. Plant Sci 163:753–758

    Article  CAS  Google Scholar 

  • Pescott OL, Simkin JM, August TA et al (2015) Air pollution and its effects on lichens, bryophytes, and lichen-feeding Lepidoptera: review and evidence from biological records. Biol J Lin Soc 115:611–635. https://doi.org/10.1111/bij.12541

    Article  Google Scholar 

  • Piazzetta KD, Ramsdorf WA, Maranho LT (2019) Use of airplant Tillandsia recurvata L., Bromeliaceae, as biomonitor of urban air pollution. Aerobiologia (bologna) 35:125–137.

    Article  Google Scholar 

  • Pignata ML, Gudio GL, Wannaz ED et al (2002) Atmospheric quality and distribution of heavy metals in Argentina employing Tillandsia capillaris as a biomonitor. Environ Pollut 120:59–68. https://doi.org/10.1016/S0269-7491(02)00128-8

    Article  CAS  Google Scholar 

  • Poczai P, Hyvönen J (2017) The complete chloroplast genome sequence of the CAM epiphyte Spanish moss (Tillandsia usneoides, Bromeliaceae) and its comparative analysis. PLoS ONE 12:1–25.

    Article  Google Scholar 

  • Pourrut B, Shahid M, Dumat C et al (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136.

    CAS  Google Scholar 

  • Pyatt FB, Grattan JP, Lacy D et al (1999) Comparative effectiveness of Tillandsia usneoides L. and Parmotrema praesorediosum (Nyl.) Hale as bio-indicators of atmospheric pollution in Louisiana (U.S.A.). Water Air Soil Pollut 111:317–326. https://doi.org/10.1023/a:1005042427595

    Article  CAS  Google Scholar 

  • Reboredo F, Simões M, Jorge C et al (2019) Metal content in edible crops and agricultural soils due to intensive use of fertilizers and pesticides in Terras da Costa de Caparica (Portugal). Environ Sci Pollut Res 26:2512–2522.

    Article  CAS  Google Scholar 

  • Respondek Z, Jerz D, Świsłowski P, Rajfur M (2022) Active biomonitoring of heavy metal concentrations in aquatic environment using mosses and algae. Water (Switzerland) 14.

  • Rodriguez JH, Pignata ML, Fangmeier A, Klumpp A (2010) Accumulation of polycyclic aromatic hydrocarbons and trace elements in the bioindicator plants Tillandsia capillaris and Lolium multiflorum exposed at PM10 monitoring stations in Stuttgart (Germany). Chemosphere 80:208–215. https://doi.org/10.1016/j.chemosphere.2010.04.042

    Article  CAS  Google Scholar 

  • Rodriguez JH, Wannaz ED, Franzaring J et al (2015) Biomonitoring of airborne fluoride and polycyclic aromatic hydrocarbons in industrial areas of Cordoba, Argentina, using standardized grass cultures of Lolium multiflorum. Atmos Pollut Res 6:444–453.

    Article  CAS  Google Scholar 

  • Rodriguez JH, Wannaz ED, Salazar MJ et al (2012) Accumulation of polycyclic aromatic hydrocarbons and heavy metals in the tree foliage of Eucalyptus rostrata, Pinus radiata and Populus hybridus in the vicinity of a large aluminium smelter in Argentina. Atmos Environ 55:35–42. https://doi.org/10.1016/j.atmosenv.2012.03.026

    Article  CAS  Google Scholar 

  • Rodriguez JH, Weller SB, Wannaz ED et al (2011) Air quality biomonitoring in agricultural areas nearby to urban and industrial emission sources in Córdoba province, Argentina, employing the bioindicator Tillandsia capillaris. Ecol Indic 11:1673–1680. https://doi.org/10.1016/j.ecolind.2011.04.015

    Article  CAS  Google Scholar 

  • Salas-Luévano MA, Mauricio-Castillo JA, González-Rivera ML et al (2017) Accumulation and phytostabilization of As, Pb and Cd in plants growing inside mine tailings reforested in Zacatecas, Mexico. Environ Earth Sci 76:1–12.

    Article  Google Scholar 

  • Sánchez-Chardi A (2016) Biomonitoring potential of five sympatric Tillandsia species for evaluating urban metal pollution (Cd, Hg and Pb). Atmos Environ 131:352–359.

    Article  Google Scholar 

  • Sáyago R, Quesada M, Aguilar R et al (2018) Consequences of habitat fragmentation on the reproductive success of two Tillandsia species with contrasting life history strategies. AoB Plants 10:1–12.

    Google Scholar 

  • Schmidt H, Bernet D, Wahli T et al (1999) Active biomonitoring with brown trout and rainbow trout in diluted sewage plant effluents. J Fish Biol 54:585–596.

    Article  Google Scholar 

  • Schrimpff E (1984) Air pollution patterns in two cities of Colombia, S. A. according to trace substances content of an epiphyte (Tillandsia recurvata L.). Water Air Soil Pollut 21:279–315

    Article  CAS  Google Scholar 

  • Silva DR da, Souza SR de, Silva LC da (2023) Deterioration of extrafloral nectaries and leaf damages caused by air pollution in a Brazilian native species from the Atlantic Forest. Environ Sci Pollut Res 43505–43521.

  • Sreekanth TVM, Nagajyothi PC, Lee KD, Prasad TNVKV (2013) Occurrence, physiological responses and toxicity of nickel in plants. Int J Environ Sci Technol 10:1129–1140.

    Article  CAS  Google Scholar 

  • Subpiramaniyam S (2021) Portulaca oleracea L. for phytoremediation and biomonitoring in metal-contaminated environments. Chemosphere 280:130784.

    Article  CAS  Google Scholar 

  • Subpiramaniyam S, Kaliannan T, Piruthiviraj P (2018) Deposition of absolute and relative airborne metals on eggshells: a field study. Environ Sci Pollut Res 25:2313–2319.

    Article  CAS  Google Scholar 

  • Sun X, Li P, Zheng G (2021) Cellular and subcellular distribution and factors influencing the accumulation of atmospheric Hg in Tillandsia usneoides leaves. J Hazard Mater 414:125529.

    Article  CAS  Google Scholar 

  • Swislowski P, Kríž J, Rajfur M (2020) The use of bark in biomonitoring heavy metal pollution of forest areas on the example of selected areas in Poland. Ecol Chem Eng S 27:195–210.

    CAS  Google Scholar 

  • Urošević MA, Lazo P, Stafilov T et al (2022) Active biomonitoring of potentially toxic elements in urban air by two distinct moss species and two analytical techniques: a pan-Southeastern European study. Air Qual Atmos Health 595–612.

  • van Heerden FR, Marthinus Horak R, Maharaj VJ et al (2007) An appetite suppressant from Hoodia species. Phytochemistry 68:2545–2553. https://doi.org/10.1016/j.phytochem.2007.05.022

    Article  CAS  Google Scholar 

  • Varela Z, Boquete MT, Fernández JA et al (2023) Mythbusters: Unravelling the pollutant uptake processes in mosses for air quality biomonitoring. Ecol Indic 148.

  • Vianna NA, Gonçalves D, Brandão F et al (2011) Assessment of heavy metals in the particulate matter of two Brazilian metropolitan areas by using Tillandsia usneoides as atmospheric biomonitor. Environ Sci Pollut Res 18:416–427. https://doi.org/10.1007/s11356-010-0387-y

    Article  CAS  Google Scholar 

  • Wannaz ED, Abril GA, Rodriguez JH, Pignata ML (2013) Assessment of polycyclic aromatic hydrocarbons in industrial and urban areas using passive air samplers and leaves of Tillandsia capillaris. J Environ Chem Eng 1:1028–1035. https://doi.org/10.1016/j.jece.2013.08.012

    Article  CAS  Google Scholar 

  • Wannaz ED, Carreras HA, Abril GA, Pignata ML (2011) Maximum values of Ni2+, Cu2+, Pb2+ and Zn2+ in the biomonitor Tillandsia capillaris (Bromeliaceae): relationship with cell membrane damage. Environ Exp Bot 74:296–301. https://doi.org/10.1016/j.envexpbot.2011.06.012

    Article  CAS  Google Scholar 

  • Wannaz ED, Pignata ML (2006) Calibration of four species of Tillandsia as air pollution biomonitors. J Atmos Chem 53:185–209. https://doi.org/10.1007/s10874-005-9006-6

    Article  CAS  Google Scholar 

  • Wegener JWM, van Schaik MJM, Aiking H (1992) Active biomonitoring of polycyclic aromatic hydrocarbons by means of mosses. Environ Pollut 76:15–18. https://doi.org/10.1016/0269-7491(92)90111-M

    Article  CAS  Google Scholar 

  • Wilk A, Kalisińska E, Kosik-Bogacka DI et al (2017) Cadmium, lead and mercury concentrations in pathologically altered human kidneys. Environ Geochem Health 39:889–899.

    Article  CAS  Google Scholar 

  • World Health Organization (2002) The World Health Organization Report 2002: reducing risks, promoting healthy life. WHO Library cataloguing-in publication data 232. https://www.who.int/publications/i/item/9241562072

  • World Health Organization (2022) World health statistics 2022 (Monitoring health of the SDGs). In Monitoring health of the SDGs. (‎electronic version).‎ https://www.who.int/publications/i/item/9789240051157

  • Zheng G, Zhang R, Zhou F, Li P (2020) Foliar uptake and transport of atmospheric trace metals bounded on particulate matters in epiphytic Tillandsia brachycaulos. Int J Phytoremediation, pp 1–7

  • Zulfiqar U, Farooq M, Hussain S et al (2019) Lead toxicity in plants: impacts and remediation. J Environ Manage 250.

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Acknowledgements

We gratefully acknowledge Tillandsia PROD (28 chemin du Cailar 30740 Le Cailar, France, contact@tillandsia-prod.com) plant nursery (Pierre Kerrand, Daniel Thomin) for providing us the Tillandsia plants used in this study and for helpful discussions and interest in the project. We also gratefully acknowledge the ICSM, CEA (Damien Bourgeois, Béatrice Baus-Lagarde) for their collaboration and ICP-OES provision for analysis.

Funding

This work was funded by La Region Occitanie, Université de Nîmes and Tillandsia PROD plant nursery (28 chemin du Cailar F-30740 Le Cailar, France, contact@tillandsia-prod.com), which provided all the plants that were necessary for the study (in kind contribution).

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  1. UPR CHROME, Université de Nîmes, CEDEX 1, 30021, Nîmes, France

    Alexandre Gonzalez, Zohra Benfodda, David Bénimélis & Patrick Meffre

  2. ICSM, CEA, CNRS, ENCSM, Université de Montpellier, Marcoule, France

    Damien Bourgeois

  3. UMR INRAE 1158 Transfrontalière BioEcoAgro, BIOlogie Des Plantes et Innovation (BIOPI), UPJV, UFR de Pharmacie, 80037, Amiens, France

    Damien Herfurth, Jean-Xavier Fontaine & Roland Molinié

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Contributions

Alexandre Gonzalez: methodology, software, validation, formal analysis, investigation, writing—original draft preparation, and visualization. Zohra Benfodda: supervision and writing—review and editing. David Bénimélis: resources. Damien Bourgeois: supervision and writing—review and editing. Damien Herfurth: software and formal analysis. Jean-Xavier Fontaine: software, formal analysis, and visualization. Roland Molinié: methodology, software, validation, formal analysis, writing—review and editing, visualization, and supervision. Patrick Meffre: conceptualization, writing—review and editing, supervision, project administration, and funding acquisition. All authors have read and agreed to the published version of the manuscript.

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Gonzalez, A., Benfodda, Z., Bénimélis, D. et al. Determination of the maximum bioaccumulation capacity of various metals in leaves of two Tillandsia species. Environ Sci Pollut Res 31, 29644–29655 (2024). https://doi.org/10.1007/s11356-024-33183-3

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