Abstract
Vachellia campechiana (Mill Seigler & Ebinger) is widely distributed in Mexico and is a dominant species of tailings in Huautla, in the state of Morelos, Mexico. Mining activities carried out in this region generated about 780 thousand tons of bioavailable heavy metal waste (HMs) that were deposited in the environment without any treatment. This study evaluates the bioaccumulation capacity and morphological changes of V. campechiana growing during 1 year in control or tailing substrates (treatments) under greenhouse conditions. The concentration of six HMs was also measured in roots, leaves, and seeds by atomic absorption spectrophotometry. Five metals showed a similar bioaccumulation pattern in the roots and leaves of V. campechiana grown in both substrates: Pb > Fe > Cr > Cu > Zn. The concentrations of Cr, Cu, and Pb were significantly higher in the roots and leaves of individuals growing on the exposed substrate. The presence of essential metals (Cu, Fe, Zn) was only recorded in the seeds, with similar concentrations in both treatments. Seventeen of 18 morphological characters evaluated in V. campechiana decreased in plants exposed to metals. Pb, Cu, and Fe showed a bioconcentration factor greater than one in roots and leaves. The translocation factor showed the following pattern: Cr > Cu = Pb. In conclusion, V. campechiana is a candidate species to phytoremediate environments contaminated with Pb, Cr, and Cu due to its ability to establish itself and turn into the dominant plant species in polluted sites, its ability to bioaccumulate non-essential metals in roots and leaves, and its high rate of HMs translocation.
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Abhilash PC, Pandey VC, Srivastava P, Rakesh PS, Chandran S, Singh N, Thomas AP (2009) Phytofiltration of cadmium from water by Limnocharis flava (L.) Buchenau grown in free-floating culture system. J Hazard Mater 170:791–797. https://doi.org/10.1016/j.jhazmat.2009.05.035
Alcantara-Martinez N, Guizar S, Rivera-Cabrera F, Anicacio-Acevedo BE, Buendia-Gonzalez L, Volke-Sepulveda T (2016) Tolerance, arsenic uptake, and oxidative stress in Acacia farnesiana under arsenate-stress. Int J Phytoremediation 18:671–678. https://doi.org/10.1080/15226514.2015.1118432
Ali H, Khan E, Sajad MA (2013) Phytoremediation of heavy metals-concepts and applications. Chemosphere 91:869–881. https://doi.org/10.1016/j.chemosphere.2013.01.075
Arce MDLR (2001) El género Acacia (leguminosae, mimosoideae) en el Estado de Oaxaca, México. An Jard Bot Madr 58(2):251–275
Armienta MA, Ongley LK, Rodríguez R, Cruz O, Mango H, Villaseñor G (2008) Arsenic distribution in mesquite (Prosopis laevigata) and huizache (Acacia farnesiana) in the Zimapán mining area, México. Geochem Explor Environ Anal 8:191–197
Barceló J, Poschenrieder C (2003) Phytoremediation: principles and perspectives. Contrib Sci 2(3):333–344
Baskin JM, Baskin CC (2004) A classification system for seed dormancy. Seed Sci Res 14:1–16
Bini C, Wahsha M, Fontana S, Maleci L (2012) Effects of heavy metals on morphological characteristics of Taraxacum officinale Web growing on mine soils in NE Italy. J Geochem Explor 123:101–108. https://doi.org/10.1016/j.gexplo.2012.07.009
Brooks RR, Lee J, Reeves RD, Jaffré (1977) Detection of nickeliferous rocks by analysis of herbarium specimens of indicator plants. J Geochem Explor 7:49–57. https://doi.org/10.1016/0375-6742(77)90074-7
Calow P (1993) General principles and overview. In: Calow P (ed) Handbook of ecotoxicology. Blackwell Scientific Publications, London, pp 1–5
Cappa JJ, Pilon-Smits EAH (2014) Evolutionary aspects of elemental hyperaccumulation. Plant 239:267–275. https://doi.org/10.1007/s00425-013-1983-0
Cervantes SMA, Sotelo BME (2002) Guías técnicas para la propagación sexual de 10 especies latifoliadas de selva baja caducifolia en el estado de Morelos 30:1–35
Cervantes-Ramírez LT, Ramírez-López M, Mussali-Galante P, Ortiz-Hernández ML, Sánchez-Salinas E, Tovar-Sánchez E (2018) Heavy metal biomagnification and genotoxic damage in two trophic levels exposed to mine tailings: a network theory approach. Rev Chil Hist Nat 91:1–13. https://doi.org/10.1186/s40693-018-0076-7
Cobbett CS (2000) Phytochelatin biosynthesis and function in heavy-metal detoxification. Curr Opin Plant Biol 3:211–216. https://doi.org/10.1016/S1369-5266(00)80067-9
Cortés-Jiménez EV, Mugica-Álvarez V, González-Chávez MCA, Carrillo-González R, Gordillo MM, Mier MV (2012) Natural revegetation of alkaline tailing heaps at Taxco, Guerrero, México. Int J Phytoremediation 15:127–141. https://doi.org/10.1080/15226514.2012.683208
Covarrubias SA, Cabriales JJP (2017) Contaminación ambiental por metales pesados en México: Problemática y estrategias de fitorremediación. Rev Int Contam Ambie 33:7–21. https://doi.org/10.20937/RICA.2017.33.esp01.01
DalCorso G (2012) Heavy metal toxicity. In: Furini A (ed) Plant and heavy metals. Springer Science & Business Media, Pisa, pp 1–25
Furini A (2012) Plants and heavy metals. Springer Science & Business Media, Pisa
Godbold DL, Kettner C (1991) Lead influences root growth and mineral nutrition of Picea abies seedlings. J Plant Physiol 139:95–99. https://doi.org/10.1016/S0176-1617(11)80172-0
Gold KP, León-Lobos Y, Way M (2004) Manual de recolección de semillas de plantas silvestres para conservación a largo plazo y restauración ecológica. Instituto de Investigaciones Agropecuarias, Centro Regional de Investigación Intihuasi, La Serena Boletín INIA 10:62
Grillet L, Mari S, Schmidt W (2014) Iron in seeds–loading pathways and subcellular localization. Front Plant Sci 4:535. https://doi.org/10.3389/fpls.2013.00535
Gutiérrez ME, Moreno M (1995) Los residuos de la minería mexicana. In: Garfias FJ, Ayala I, Weber LB (eds) Taller para el desarrollo sustentable: residuos peligrosos. México, pp 37–44
Gutiérrez-Ruiz M, Romero F, González-Hernández G (2007) Suelos y sedimentos afectados por la dispersión de jales inactivos de sulfuros metálicos en la zona minera de Santa Bárbara, Chihuahua, México. Rev Mex Cienc Geol 24(2):170–184
He H, Bleby TM, Veneklaas EJ, Lambers H, Kuo J (2012) Morphologies and elemental compositions of calcium crystals in phyllodes and branchlets of Acacia robeorum (Leguminosae: Mimosoideae). Ann Bot 109:887–896. https://doi.org/10.1093/aob/mcs004
Hernández-Acosta E, Mondragón-Romero E, Cristobal-Acevedo D, Rubiños-Panta JE, Robledo-Santoyo E (2009) Vegetación, residuos de mina y elementos potencialmente tóxicos de un jal de Pachuca, Hidalgo, México. Rev Chapingo Ser Cie 15(2):109–114
Hernández-Lorenzo B (2015) Análisis de la anatomía y morfología de Prosopis laevigata, por acumulación de metales pesados en la sierra de Huautla, Morelos. Facultad de Ciencias Biológicas, Universidad Autónoma del Estado de Morelos, Cuernavaca
Iqbal MZ, Saeeda S, Muhammad S (2001) Effects of chromium on an important arid tree (Caesalpinia pulcherrima) of Karachi city, Pakistan. Ekol Bratislava 20:414–422
Kabata-Pendias A (2000) Trace elements in soils and plants. CRC Press, Boca Raton
Lin YF, Aarts MG (2012) The molecular mechanism of zinc and cadmium stress response in plants. Cell Mol Life Sci 69(19):3187–3206. https://doi.org/10.1007/s00018-012-1089-z
Lin J, Jiang W, Liu D (2003) Accumulation of copper by roots, hypocotyls, cotyledons and leaves of sunflower (Helianthus annuus L.). Bioresour Technol 86:151–155. https://doi.org/10.1016/S0960-8524(02)00152-9
Macnair MR (2003) The hyperaccumulation of metals by plants. Adv Bot Res 40:63–105. https://doi.org/10.1016/S0065-2296(05)40002-6
Mahar A, Wang P, Ali A, Awasthi MK, Lahori AH, WangQ ZZ (2016) Challenges and opportunities in the phytoremediation of heavy metals contaminated soils: a review. Ecotoxicol Environ Saf 126:111–121. https://doi.org/10.1016/j.ecoenv.2015.12.023
Maldonado-Magaña A, Favela-Torres E, Rivera-Cabrera F, Volke-Sepulveda TL (2011) Lead bioaccumulation in Acacia farnesiana and its effect on lipid peroxidation and glutathione production. Plant Soil 339:377–389. https://doi.org/10.1007/s11104-010-0589-6
Maleci L, Bini C, Paolillo A (2001) Chromium (III) uptake by Calendula arvensis L. and related phytotoxicity. Proc. VI ICOBTE, Guelph, On., p. 384 (abstract)
Marrero-Coto J, Amores-Sánchez I, Coto-Pérez O (2012) Fitorremediación, una tecnología que involucra a plantas y microorganismos en el saneamiento ambiental. ICIDCA 46(3):52–61
Martínez-Pacheco M (2008) Evaluación de los efectos genotóxicos de metales presentes en el agua de bebida de la población de Huautla, Morelos. Facultad de ciencias. Universidad Nacional Autónoma de México, México
Meharg AA (1994) Integrated tolerance mechanisms: constitutive and adaptive plant responses to elevated metal concentrations in the environment. Plant Cell Environ 17:989–993
Mendez MO, Maier RM (2008) Phytoremediation of mine tailings in temperate and arid environments. Environ Sci Biotechnol 7:47–59. https://doi.org/10.1007/s11157-007-9125-4
Mireles F, Davila JI, Pinedo JL, Reyes E, Speakman RJ, Glascock MD (2012) Assessing urban soil pollution in the cities of Zacatecas and Guadalupe, Mexico by instrumental neutron activation analysis. Microchem J 103:158–164
Mussali-Galante P, Tovar-Sánchez E, Valverde M, del Castillo ER (2013) Biomarkers of exposure for assessing environmental metal pollution: from molecules to ecosystems. Rev Int Contam Ambie 29(1):117–140
Olguín EJ, Sánchez-Galván G (2012) Heavy metal removal in phytofiltration and phycoremediation: the need to differentiate between bioadsorption and bioaccumulation. New Biotechnol 30(1):3–8. https://doi.org/10.1016/j.nbt.2012.05.020
Panda SK, Choudhury S (2005) Chromium stress in plants. J Plant Physiol 17(1):95–102. https://doi.org/10.1590/S1677-04202005000100008
Panda SK, Patra HK (2000) Nitrate and ammonium ions effect on the chromium toxicity in developing wheat seedlings. Proc Natl Acad Sci India 70:75–80
Patra M, Bhowmik N, Bandopadhyay B, Sharma A (2004) Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environ Exp Bot 52:199–223. https://doi.org/10.1016/j.envexpbot.2004.02.009
Prasad MNV (2003) Phytoremediation of metal-polluted ecosystems: hype for commercialization. Russ J Plant Physl 50(5):686–701
Prasad MNV, Greger M, Landberg T, Acacia nilotica L (2001) Bark removes toxic elements from solution: corroboration from toxicity bioassay using Salix viminalis L. in hydroponic system. Int J Phytoremediation 3(1):289–300. https://doi.org/10.1080/15226510108500060
Prieto J, Ramírez GC, Román A, Prieto F (2009) Contaminación y fitotoxicidad en plantas por metales pesados provenientes de suelos y agua. Tro Subtro Agroecosyst 10:29–44
Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181
Rauser WE (1995) Phytochelatins and related peptides. Structure, biosynthesis, and function. Plant Physiol 109:1141
Rengel M, Gil F, Montaño J (2011) Crecimiento y dinámica de acumulación de nutrientes en caña de azúcar. I macronutrientes. Bioagro 23:5–8
Rico ML (2001) El género Acacia (Leguminosae, Mimosoideae) en el Estado de Oaxaca, México. An Jard Bot Madr 58:251–302
Rodríguez-Serrano M, Martínez-de la Casa N, Romero-Puertas M, Del Río L, Sandalio L (2008) Toxicidad del cadmio en plantas. Ecosistemas 17:139–146
Rosas-Ramírez ME (2018) Relación entre la bioacumulación de metales pesados y la concentración de clorofila en Sanvitalia procumbens. Facultad de Ciencias Biológicas. Universidad Autónoma del Estado de Morelos, Cuernavaca
Salas-Luévano MA, Manzanares-Acuña E, Letechipía-de León C, Vega-Carrillo HR (2009) Tolerant and hyperaccumulators autochthonous plant species from mine tailing disposal sites. J Exp Sci Asia 23(1):27–32
Salisbury FT (1968) Las plantas vasculares: forma y funciones. Herrero Hermanos Sucesores, México
Secretaria de Economía (2011) Panorama Minero del estado de Morelos. Servicio Geológico Mexicano, serie panorama minero de los estados, Pachuca
Shanker AK (2003) Physiological, biochemical and molecular aspects of chromium toxicity and tolerance in selected crops and tree species. PhD Thesis, Tamil Nadu Agricultural University, Coimbatore, India
Shanker AK, Cervantes C, Loza-Tavera H, Avudainayagam S (2005) Chromium toxicity in plants. Environ Int 31:739–753. https://doi.org/10.1016/j.envint.2005.02.003
Shiqi L, Yang B, Kou Y, Zeng J, Wang R, Xiao Y, Li F, Lu Y, Mu Y, Zhao C (2018) Assessing the difference of tolerance and phytoremediation potential in mercury contaminated soil of a non-food energy crop, Helianthus tuberosus L. (Jerusalem artichoke). Peer J 6:1–18. https://doi.org/10.7717/peerj.4325
Skeffington RA, Shewry PR, Peterson PJ (1976) Chromium uptake and transport in barley seedlings (Hordeum vulgare L.). Plant 132:209–214
Stacey MG, Patel A, McClain WE, Mathieu M, Remley M, Rogers EE, Gassmann W, Blevins DG, Stacey G (2008) The Arabidopsis AtOPT3 protein functions in metal homeostasis and movement of iron to developing seeds. Plant Physiol 146:589–601
StatSoeft, Inc (2004) STATISTICA (data analysis software system), version 7. www.statsoft.com
Suseela MR, Sinha S, Singh S, Saxena R (2002) Accumulation of chromium and scanning electron microscopic studies in Scirpus lacustris L. treated with metal and tannery effluent. Bull Environ Contam Toxicol 68:540–548. https://doi.org/10.1007/s001280288
Thakur P (1990) Different physiological responses of tomato (Lucopersicom esculetum Mill.) cultivars to drought. Acta Physiol Plant 12:175–182
Tovar-Sánchez E, Cervantes-Ramírez T, Castañeda-Bautista J, Gómez-Arroyo S, Ortiz-Hernández L, Sánchez-Salinas E, Mussali-Galante P (2018) Response of Zea mays to multimetal contaminated soils: a multibiomarker approach. Ecotoxicology 27:1161–1177. https://doi.org/10.1007/s10646-018-1974-9
Tovar-Sánchez E, Suarez-Rodríguez R, Ramírez-Trujillo A, Valencia-Cuevas L, Hernández-Plata I, Mussali-Galante P (2019). The use of biosensors for biomonitoring environmental metal pollution, Biosensors for Environmental Monitoring, Toonika Rinken and Kairi Kivirand, IntechOpen, https://doi.org/10.5772/intechopen.84309. Available from: https://www.intechopen.com/books/biosensors-for-environmental-monitoring/the-use-of-biosensors-for-biomonitoring-environmental-metal-pollution
Tyler G, Zohlen A (1998) Plant seeds as mineral nutrient resource for seedlings—a comparison of plants from calcareous and silicate soils. Ann Bot 81:455–459. https://doi.org/10.1006/anbo.1997.0581
Van der Ent A, Baker AJ, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334. https://doi.org/10.1007/s11104-012-1287-3
Velasco TJA, de la Rosa PDA, Ramírez IME, Volke ST (2005) Evaluación de tecnologías de remediación para suelos contaminados con metales. Etapa II. secretaria del medio ambiente y recursos naturales, México, pp 1–36
Volke ST, Velsco TA, De la Rosa PA, Solórzano OG (2004) Evaluaciones de tecnologías de remediación para suelos contaminados con metales. Etapa I. Secretaria de Medio Ambiente y Recursos Naturales, México
Volke ST, Velsco TA, De la Rosa PA, Solórzano OG (2005) Evaluaciones de tecnologías de remediación para suelos contaminados con metales. Etapa II. Secretaria de Medio Ambiente y Recursos Naturales, México
Waters BM, Sankaran RP (2011) Moving micronutrients from the soil to the seeds: genes and physiological processes from a biofortification perspective. Plant Sci 180:562–574. https://doi.org/10.1016/j.plantsci.2010.12.003
Yadav SK (2010) Heavy metals toxicity in plants: an overview on the role of glutathione and phytochelatins in heavy metal stress tolerance of plants. S Afr J Bot 76:167–179. https://doi.org/10.1016/j.sajb.2009.10.007
Yang X, Feng Y, He Z, Stoffella PJ (2005) Molecular mechanisms of heavy metal hyperaccumulation and phytoremediation. J Trace Elem Med Biol 18:339–353. https://doi.org/10.1016/j.jtemb.2005.02.007
Yong-Eui C, Harada E, Gwang-Hoon K, Eui-Soo Y, Sano H (2004) Distribution of elements on tobacco trichomes and leaves under cadmium and sodium stresses. J Plant Biol 47:75–82
Yoon J, Cao X, Zhou Q, Ma LQ (2006) Accumulation of Pb, Cu, and Zn in native plants growing on a contaminated Florida site. Sci Total Environ 368:456–464. https://doi.org/10.1016/j.scitotenv.2006.01.016
Zar JH (2010) Biostatistical analysis. Prentice-Hall, Upper Saddle River
Zhang Z, Rengel Z, Meney K (2007) Removal of nutrients from secondary-treated municipal wastewater in wetland microcosms using ornamental plant species. Int J Environ Waste Manag 1:363–375
Zimmermann M (2001) Adaptaciones de plantas a estrés abiótico que les permiten vivir y prosperar en diferentes condiciones ambientales. Rev Creces:1–9
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Also, we would like to thank Rosalind Pearson Hedge for her comments and English edition that improved our manuscript.
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This research was supported by a CONACyT scholarship grant to M.S.M. (Grant: 307350).
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Santoyo-Martínez, M., Mussali-Galante, P., Hernández-Plata, I. et al. Heavy metal bioaccumulation and morphological changes in Vachellia campechiana (Fabaceae) reveal its potential for phytoextraction of Cr, Cu, and Pb in mine tailings. Environ Sci Pollut Res 27, 11260–11276 (2020). https://doi.org/10.1007/s11356-020-07730-7
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DOI: https://doi.org/10.1007/s11356-020-07730-7