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Phytoremediation potential and ecological and phenological changes of native pioneer plants from weathered oil spill-impacted sites at tropical wetlands

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Abstract

Pioneer native plant species from weathered oil spill-affected sites were selected to study their potential for phytoremediation on the basis of their ecological and phenological changes during the phytoremediation process. Experiments were conducted in field and in greenhouse. In field, native plants from aged oil spill-impacted sites with up 400 g of weathered petroleum hydrocarbons per kilogram soil were selected. In the impacted sites, the principal dominant plant species with potential for hydrocarbons removal were Cyperus laxus, Cyperus esculentus, and Ludwigia peploides. In greenhouse, the phenology of the selected plant species was drastically affected by the hydrocarbons level above 325 g total petroleum hydrocarbons (TPH) per kilogram soil after 2 years of phytoremediation of soils from the aged oil spill-impacted sites. From the phytoremediation treatments, a mix-culture of C. laxus, C. esculentus, and L. peploides in soil containing 325 g TPH/kg soil, from which 20.3 % were polyaromatic hydrocarbons (PAH) and 34.2 % were asphaltenes (ASF), was able to remove up 93 % of the TPH, while in unvegetated soil the TPH removal was 12.6 %. Furthermore, evaluation of the biodiversity and life forms of plant species in the impacted sites showed that phytoremediation with C. esculentus, alone or in a mix-culture with C. laxus and L. peploides, reduces the TPH to such extent that the native plant community was progressively reestablished by replacing the cultivated species resulting in the ecological recovery of the affected soil. These results demonstrate that native Cyperus species from weathered oil spill-affected sites, specifically C. esculentus and C. laxus, alone or in a mix-culture, have particular potential for phytoremediation of soils from tropical wetlands contaminated with weathered oil hydrocarbons.

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References

  • Abedi-Koupai J, Ezzatian R, Vossoughi-Shavari M, Yaghmaei S, Borghei M (2007) The effects of microbial population on phytoremediation of petroleum contaminated soils using tall fescue. Int J Agr Biol 9:242–246

    CAS  Google Scholar 

  • Amadi A, Dickson AA, Maate GO (1993) Remediation of oil polluted soils: 1. Effect of organic and inorganic nutrient supplements on the performance of maize (Zea mays L). Water Air Soil Pollut 66:59–76

    Article  CAS  Google Scholar 

  • Ashworth J, Keyes D, Kirk R, Lessard R (2001) Standard procedure in the hydrometer method for particle size analysis. Commun Soil Sci Plant Anal 32(5-6):633–642

    Article  CAS  Google Scholar 

  • Baskin CC, Baskin JM (1988) Germination ecophysiology of herbaceous plant species in a temperate region. Am J Bot 75:286–305

    Article  Google Scholar 

  • Brown JL, Nadeau RJ (2002) Restoration of petroleum-contaminated soil using phased bioremediation. Biorem J 6:315–319

    Article  CAS  Google Scholar 

  • CIMADES (Interdisciplinary Commission of Environmental and Social Development) (2000) Descripción de la infraestructura petrolera y del entorno ambiental del Activo Cinco Presidentes. Gobierno del estado de Tabasco, México, p 42

    Google Scholar 

  • Collins SL, Glenn SM, Gibson DJ (1995) Experimental analysis of intermediate disturbance and initial floristic composition: decoupling cause and effect. Ecology 76:486–492

    Article  Google Scholar 

  • Cox GW (1981) Laboratory manual of general ecology. W.C. Brown Publishers-San Diego State University, U.S.A., p 237

    Google Scholar 

  • Escalante-Espinoza E, Gallegos-Martínez ME, Favela-Torres E, Gutierrez-Rojas M (2005) Improvement of the hydrocarbon phytoremediation rate by Cyperus laxus Lam. inoculated with a microbial consortium in a model system. Chemosphere 59:405–413

    Article  Google Scholar 

  • Fidalgo O, Bononi VLR (1984) Técnicas de colecta, preservaçao e herborizaçao de material botánico. Instituto de Botánica-U, Sao Paulo, p 106

    Google Scholar 

  • Fulbgriht TE (1996) Viewpoint: a theoretical basis for planning woody plant control to maintain species diversity. J Range Management 49:554–559

    Article  Google Scholar 

  • Gallegos-Martínez M, Gómez-Santos A, González-Cruz L, Montes de Oca-García A, Yáñez-Trujillo L, Zermeño-Eguía Lis J, Gutierrez-Rojas M (2000) Diagnostic and resulting approaches to restore petroleum-contaminated soil in a Mexican tropical swamp. Water Sci Technol 42:377–384

    Google Scholar 

  • Gentry AH (1988) Changes in plant community diversity and floristic composition on environmental and geographical gradients. Ann Mo Bot Garden 75:1–34

    Article  Google Scholar 

  • Gutierrez CMC, Zavala CJ (2002) Hydromorphic pedofeatures in hydrocarbon polluted tropical soils. Terra Latinoamericana 20:101–111

    Google Scholar 

  • Handa IT, Jefferies RL (2000) Assisted revegetation trials in degraded salt-marshes. J Appl Ecol 37:944–958

    Article  Google Scholar 

  • INEGI (Instituto Nacional de Estadística Geografía e Informática) (2001) Anuario estadístico del estado de Tabasco. Gobierno del estado de Tabasco, México, p 480

    Google Scholar 

  • Ke L, Wong TWY, Tam NFY (2002) Fate of polycyclic aromatic hydrocarbon (PAH) contamination in a mangrove swamp in Hong Kong following an oil spill. Marine Pollut Bull 45:339–347

    Article  CAS  Google Scholar 

  • Kulakow PA, Schwab AP, Banks MK (2000) Screening plant species for growth on weathered, petroleum hydrocarbon-contaminated sediments. Int J Phytoremediat 2:297–317

    Article  CAS  Google Scholar 

  • Lambers H, Chapin FS, Pons TL (1998) Plant physiological ecology. Springer, New York, p 289

    Book  Google Scholar 

  • Lin Q, Mendelssohn IA, Carney K, Bryner NP, Walton WD (2002a) Salt marsh recovery and oil spill remediation after in-situ burning: effect of water depth and burn duration. Environ Sci Technol 36:578–581

    Article  Google Scholar 

  • Lin Q, Mendelssohn IA, Siudan MT, Lee K, Venosa AD (2002b) The dose-response relationship between no. 2 fuel oil and the growth of salt marsh grass, Spartina alterniflora. Marine Pollut Bull 44:879–902

    Article  Google Scholar 

  • Lin Q, Mendelssohn IA, Bryner NP, Walton WD (2005a) In-situ burning of oil in coastal marshes. 1: vegetation recovery and soil temperature as a function of water depth, oil type and marsh type. Environ Sci Technol 39:1848–1854

    Article  CAS  Google Scholar 

  • Lin Q, Mendelssohn IA, Carney K, Miles S, Bryner NP, Walton WD (2005b) In-situ burning of oil in coastal marshes. 2. Oil spill cleanup efficiency as a function of oil type, marsh type, and water depth. Environ Sci Technol 39:1855–1860

    Article  CAS  Google Scholar 

  • Liste H-H, Felgentreu D (2006) Crop growth, culturable bacteria, and degradation of petrol hydrocarbons (PHCs) in a long-term contaminated field soil. Appl Soil Ecol 31:43–52

    Article  Google Scholar 

  • Lot A (2004) Flora y vegetación de los humedales de agua dulce en la zona costera del Golfo de México. In: Caso M, Pisanty I, Ezcurra E (eds) Diagnóstico ambiental del Golfo de México. Instituto Nacional de Ecología, México, pp 521–553

    Google Scholar 

  • Lot A, Chiang F (1986) Manual de herbario, administración y manejo de colecciones, técnicas de recolección y preparación de ejemplares botánicos. Consejo Nacional de la Flora de México, México, D.F, p 143

    Google Scholar 

  • Mackey RL, Currie DJ (2001) The diversity-disturbance relationship: is it strong and peaked? Ecology 82:3479–3492

    Google Scholar 

  • Maila MP, Cloete TE (2002) Germination of Lepidium sativum as a method to evaluate polycyclic aromatic hydrocarbons (PAHs) removal from contaminated soil. Internat Biodeterior Biodegrad 50:107–113

    Article  CAS  Google Scholar 

  • Martínez MG, Santos AG, Cruz LG, de Oca García MM, Trujillo LY, Lis JZE, Gutierrez-Rojas M (2000) Diagnostic and resulting approaches to restore petroleum-contaminated soil in a Mexican tropical swamp. Water Sci Technol 42(5-6):377–384

    Google Scholar 

  • Mendelssohn IA, Lin Q, Bryner NP, Walton WD, Twilley WH, Mullin JV (2002) In-situ oil burning in the marshland environment-recovery and regrowth of Spartina alterniflora, Spartina patens, and Sagittaria lancifolia plants. Proceedings of the twenty-fifth artic and marine oil spill program technical seminar. Environment Canada, In, pp 785–802, http://fire.nist.gov/bfrlpubs/fire02/PDF/f02068.pdf

    Google Scholar 

  • Merkl N., Schultze-Kraft R. 2005. Phytoremediation of petroleum-contaminated soils in the tropics. In: Deutscher Tropentag. The Global Food & Product Chain - Dynamics, Innovations, Conflicts, Strategies. University of Hohenheim, Oct. 11–13. Book of Abstract. http://www.tropentag.de/2005/abstracts/links/Merkl_BJt2Mok2.php

  • Merkl N, Schultze-Kraft R, Infante C (2004) Phytoremediation of petroleum-contaminated soils in the tropics—Preliminary assessment of the potential of species from eastern Venezuela. J Appl Bot Food Qual 78:185–192

    Google Scholar 

  • Merkl N, Schultze-Kraft R, Infante C (2005) Assessment of tropical grasses and legumes for phytoremediation of petroleum-contaminated soils. Water Air Soil Pollut 165:195–209

    Article  CAS  Google Scholar 

  • Molina-Barahona L, Rodriguez-Vazquez R, Hernandez-Velasco M, Vega-Jarquin C, Zapata-Perez O, Mendoza-Cantu A, Albores A (2004) Diesel removal from contaminated soils by biostimulation and supplementation with crop residues. Appl Soil Ecol 27:165–175

    Article  Google Scholar 

  • Mückschel C, Otte A (2003) Morphometric parameters: an approach for the indication of environmental conditions on calcareous grassland. Agric Ecosyst Environm 98:213–225

    Article  Google Scholar 

  • Müller-Dumbois D, Ellemberg H (1974) Aims and methods of vegetation ecology. John Wiley and sons, New York, p 547

    Google Scholar 

  • Noble IR, Slayter RO (1980) The use of vital attributes to predict successional changes in plant communities subject to recurrent disturbances. Vegetatio 43:5–21

    Article  Google Scholar 

  • Palmroth MRT, Pitchel J, Puhakka JA (2002) Phytoremediation of subartic soil contaminated with diesel fuel. Biores Technol 84:221–228

    Article  CAS  Google Scholar 

  • Palmroth MRT, Koskinen PEP, Pichtel J, Vaajasaari K, Joutti A, Tuhkanen TA, Puhakka JA (2006) Field-scale assessment of phytotreatment of soil contaminated with weathered hydrocarbons and heavy metals. J Soils Sediments 6:128–136

    Article  CAS  Google Scholar 

  • Pérez-Vargas J, Poggi-Varaldo HM, Calva-Calva G, Ríos-Leal E, Rodríguez-Vázquez R, Ferrera-Cerrato R, Esparza-García F (2000) Nitrogen fixing bacteria capable of using kerosene hydrocarbons as a sole carbon source. Water Sci Technol 42:407–410

    Google Scholar 

  • Perez-Vargas J, Poggi-Varaldo HM, Calva-Calva G, Albores RA, Rodriguez-Vazquez R, Esparza-Garcia F, Ferrera-Cerrato R (2001) Azomonas: an NFB capable of using kerosene as a carbon source. In: Magar VS, Von Fahnestock FM, Leeson A (eds) Ex situ biological treatment technologies, vol 6(6). Columbus, Battelle Press, pp 219–226

    Google Scholar 

  • Ponce-Velez G, Botello AV, Diaz-Gonzalez G (2006) Organic and inorganic pollutants in marine sediments from northern and southern continental shelf of the Gulf of Mexico. Int J Environment and Pollution 26:295–311

    Article  CAS  Google Scholar 

  • Primack RB, Kang H (1989) Measuring fitness and natural selection in wild plant populations. Ann Rev Ecol Syst 20:367–396

    Article  Google Scholar 

  • Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Ann Rev Ecol Syst 16:179–214

    Article  Google Scholar 

  • Rivera Casado NA, Rodríguez Vázquez R, Montes Horcasitas M del C, Pérez Vargas J, Gómez Guzmán O, Calva Calva G (2008). Hidrocarburos aromáticos y fenilpropanoides presentes en la rizósfera de plantas de Cyperus laxus crecido en suelos contaminados con hidrocarburos. Tecnocultura 7(20): 4-15. http://difusion.tese.edu.mx/tese2010/loader.aspx?n = NFKNRAQG

  • Rivera Casado NA, Montes Horcasitasa Mdel C, Rodríguez Vázquez R, Esparza García FJ, Pérez Vargas J, Ariza Castolo A, Ferrera-Cerrato R, Gómez Guzmán O, Calva Calva G (2015) The Fatty acid profile analysis of Cyperus laxus used for phytoremediation of soils from aged oil spill-impacted sites revealed that this is a C18:3 plant species. PLoS One 10(10):e0140103. doi:10.1371/journal.pone.0140103.eCollection2015

    Article  Google Scholar 

  • Rivera-Cruz MD, Ferrera-Cerrato R, Sánchez-García P, Volke-Haller V, Fernández-Linares L, Rodríguez-Vázquez R (2004) Decontamination of soils polluted with crude petroleum using indigenous microorganisms and aleman grass [Echinochloa polystachya (H.B.K.) Hitchc.]. Agrociencia 38:1–12

    Google Scholar 

  • SPSS Inc., 2006. SPSS, v. 15.0, Chicago, IL.

  • Sudová R, Pavlíková D, Macek T, Vosátka M (2007) The effect of EDDS chelate and inoculation with the arbuscular mycorrhizal fungus Glomus intraradices on the efficacy of lead phytoextraction by two tobacco clones. Appl Soil Ecol 35:163–173

    Article  Google Scholar 

  • Tischer S, Hübner T (2002) Model trials for phytoremediation of hydrocarbon-contaminated sites by the use of different plant species. Intern J Phytorem 4:187–203

    Article  CAS  Google Scholar 

  • US-EPA (U.S. Environmental Protection Agency) 1986. Method 8015B. Nonhalogenated organics using GC/FID. SW-846 Ch 4.3.1. http://www.caslab.com/EPA-Methods/PDF/8015b.pdf

  • US-EPA (U.S. Environmental Protection Agency) 1996. Method 3550B. SW-846 Ch 4.2.1. Ultrasonic extraction—organics. http://www.trincoll.edu/~henderso/textfi~1/416%20notes/3550b.pdf

  • Vazquez FG, Sharma VK, Perez-Cruz L (2002) Concentrations of elements and metals in sediments of the southeastern Gulf of Mexico. Environ Geol 42:41–46

    Article  CAS  Google Scholar 

  • Vitaliano JJ, Reid RN, Frame AB, Packer DB, Arlen L, Sacco JN (2002) Comparison of benthic invertebrate assemblages at Spartina alterniflora marshes reestablished after an oil spill and existing marshes in the Arthur Kill (NY/NJ). Mar Pollut Bull 44:1100–1108

    Article  CAS  Google Scholar 

  • Wolters V, Silver WL, Bignell DE, Coleman DC, Lavelle P, van Der Putten WH, De Ruiter P, Rusek J, Wall DH, Wardle DA, Brussaard L, Dangerfield JM, Brown VK, Giller KE, Hooper DU, Sala O, Tiedje J, van Veen JA (2000) Effects of global changes on above and belowground biodiversity in terrestrial ecosystems: implications for ecosystems functioning. Bioscience 50:1089–1098

    Article  Google Scholar 

  • Zavala CJ (1988) Regionalización natural de la zona petrolera de Tabasco. Casos de estudio. Instituto Nacional de Investigación sobre Recursos Bióticos. División Regional. Gobierno del estado de Tabasco, México, p 183

    Google Scholar 

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Acknowledgments

This work was supported by the Consejo Nacional de Ciencia y Tecnología (CONACyT México: 211085-5-29307B). Special acknowledgment is given to CIMADES for the technical assistance during the field studies thorough the extraction and production oil zone in Tabasco, México. Felipe de J. Palma Cruz acknowledges a doctoral fellowship (83286) from CONACyT.

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Correspondence to Graciano Calva-Calva.

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Palma-Cruz, F.d.J., Pérez-Vargas, J., Rivera Casado, N.A. et al. Phytoremediation potential and ecological and phenological changes of native pioneer plants from weathered oil spill-impacted sites at tropical wetlands. Environ Sci Pollut Res 23, 16359–16371 (2016). https://doi.org/10.1007/s11356-016-6675-4

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