Abstract
Four species of trees were selected to evaluate the tolerance to heavy crude oil contamination by means of a tolerance index integrating germination, height, biomass and survival as variables. Fresh seeds to Cedrela odorata (tropical cedar), Haematoxylum campechianum (tinto bush), Swietenia macrophylla (mahogany) and Tabebuia rosea (macuilis) were planted in a Vertisol to which heavy crude petroleum was added at four different treatments (C0, 0; C1, 18,940; C2, 44,000; and C3, 57,000 mg kg−1), with the control being uncontaminated soil. The experiment was carried out in a greenhouse during 203 days with a completely random design. The presence of petroleum in soil stimulated and increased germination of S. macrophylla and C. odorata, accelerated the germination of T. rosea and did not affect the germination of H. campechianum. The height and biomass of all species was reduced in the presence of petroleum in the soil. The survival of S. macrophylla and H. campechianum was not affected by petroleum at any concentration studied. On the other hand, C. odorata and T. rosea showed high mortality at all concentrations. The tolerance index showed that S. macrophylla was best at tolerating petroleum in soil and could be employed as a productive alternative for the advantageous use of contaminated sites. The use of tree species could be important because of the great potential of trees for phytoremediation due to their long life, biomass and deep roots that can penetrate and remediate deeper soil layers.
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References
Adam, G., & Duncan, H. (2002). Influence of diesel fuel on seed germination. Environmental Pollution, 120, 363–370.
Arriaga, V., Cervantes, V., & Vargas-Mena, A. (1994). Manual de reforestación con especies nativas. México: Instituto Nacional de Ecología, Secretaria de Desarrollo Social y Universidad Nacional Autónoma de México.
Besalatpour, A., Khoshgoftarmanesh, A. H., Hajabbasi, M. A. & Afyuni, M. (2008). Germination and growth of selected plants in a petroleum contaminated calcareous soil. Soil & Sediment Contamination, 17, 665–676.
Blokhina, O., Virolainen, E., & Fagerstedt, K. V. (2003). Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of Botany, 91, 179–194.
Bossert, I., & Bartha, R. (1984). The fate of petroleum in soil ecosystems. In R. M. Atlas (Ed.), Petroleum microbiology (pp. 434–476). New York: Macmillan.
Brandt, R., Merkl, N., Schultze-Kraft, R., Infante, C., & Broll, G. (2006). Potential of vetiver (Vetiveria zizanioides (L.) Nash) for phytoremediation of petroleum hydrocarbon-contaminated soils in Venezuela. International Journal of Phytoremediation, 8(4), 273–284.
Briggs, G. G., Bromilow, R. H., & Evans, A. A. (1982). Relationship between lipophilicity and root uptake and translocation of non-ionized chemicals by barley. Pesticide Science, 13, 495–504.
Burken, J. G., & Schnoor, J. L. (1998). Predictive relationships for uptake of organic contaminants by hybrid poplar trees. Environment Science and Technology, 32(21), 3379–3385.
Chaineau, C. H., Morel, J. L., & Oudot, J. (1997). Phytotoxicity and plant uptake of fuel oil hydrocarbons. Journal of Environmental Quality, 26, 1478–1483.
Chaineau, C. H., Yepremian, C., Vidalie, J. F., Ducreux, J., & Ballerini, D. (2003). Bioremediation of a crude oil-polluted soil: biodegradation, leaching and toxicity assessments. Water, Air, and Soil Pollution, 144, 419–440.
Chan-Quijano, J. G., Ochoa-Gaona, S., Pérez-Hernández, I., Gutiérrez-Aguirre, M. A., & Saragos-Méndez, J. (2012). Germinación y sobrevivencia de especies arbóreas que crecen en suelos contaminados por hidrocarburos. Teoría y Praxis, 12, 102–119.
CONAFOR. (2013). Comisión Nacional Forestal, SIRE-Paquetes tecnológicos. http://www.conafor.gob.mx/portal/index.php/temas-forestales/reforestacion/fichas-tecnicas. Accessed May 2013.
Cordero, J., & Boshier, D. H. (2003). Árboles de Centroamérica: un manual para extensionistas. San José: OFI-CATIE.
Cunningham, D. S., Anderson, T. A., Schwab, A. P., & Hsu, F. C. (1996). Phytoremediation of soils contaminated with organic pollutants. Advances in Agronomy, 56, 55–114.
Daws, M. I., Garwood, N. C., & Pritchard, H. W. (2005). Traits of recalcitrant seeds in a semi-deciduous tropical forest in Panamá: some ecological implications. Functional Ecology, 19, 874–885.
Dawson, J. J. C., Godsiffe, E. J., Thompson, I. P., Ralebitso-Senior, T. K., Killham, K. S., & Paton, G. I. (2007). Application of biological indicators to assess recovery of hydrocarbon impacted soils. Soil Biology and Biochemistry, 39, 164–177.
Debiane, D., Garcon, G., Verdin, A., Fontaine, J., Durand, R., Shirali, P., Grandmougin-Ferjani, A., & Lounes-Hadj, S. A. (2009). Mycorrhization alleviates benzo[a]pyrene induced oxidative stress in an in vitro chicory root model. Phytochemistry, 70, 1421–1427.
Díaz-Ramírez, I. J. (2004). Biodegradación de hidrocarburos por cultivos mixtos definidos aislados de la rizósfera de Cyperus laxus Lam. PhD Thesis. México D.F: Universidad Autónoma Metropolitana-Iztapalapa.
Freedman, B. (1995). Environmental ecology. The impacts of pollution and other stresses on ecosystem structure and function (2nd ed.). San Diego: Academic.
Gechev, T. S., van Breusegem, F., Stone, J. M., Denev, I., & Laloi, C. (2006). Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays, 28, 1091–1101.
Gianfreda, L., Rao, M. A., Piotrowska, A., Palumbo, G., & Colombo, C. (2005). Soil enzyme activities as affected by anthropogenic alterations: intensive agricultural practices and organic pollution. Science of the Total Environment, 341, 265–279.
Gill, S. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48, 909–930.
Gómez, T. J., Jasso, M. J., Vargas, H. J. J., & Soto, H. M. R. (2006). Deterioro de semilla de dos procedencias de Swietenia macrophylla King., bajo distintos métodos de almacenamiento. Ra Ximhai, 2(1), 223–239.
Gratáo, P., Polle, A., Lea, P. J., & Azevedo, R. A. (2005). Making the life of heavy metal-stressed plants a little easier. Functional Plant Biology, 32, 481–494.
Guerrero-Zúñiga, L. A., & Rodríguez-Dorantes, M. A. (2009). Efecto de la presencia de fenantreno sobre la expresión de proteínas y la actividad enzimática radical de Cyperus hermaphroditus. Polibotánica, 27, 103–130.
Halliwell, B. (2006). Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiology, 141, 312–322.
Hampton, J. G., & Coolbear, P. (1990). Potential versus actual seed performance—can vigour testing provide an answer? Seed Science Technology, 18, 215–228.
Hernández-Ortega, H. A., Alarcón, A., Ferrera-Cerrato, R., Zavaleta-Mancera, H. A., López- Delgado, H. A., & Mendoza-López, M. R. (2011). Arbuscular mycorrhizal fungi on growth, nutrient status, and total antioxidant activity of Melilotus albus during phytoremediation of a diesel-contaminated substrate. Journal of Environmental Management, 95, 319–324.
Inckot, C. R., Oliveira, S. G., Souza, L. A., & Bona, C. (2011). Germination and development of Mimosa pilulifera in petroleum-contaminated soil and bioremediated soil. Flora—Morphology, Distribution, Functional Ecology of Plants, 206, 261–266.
INEGI. (2005). Cuaderno Estadístico Municipal de Centro, Tabasco. Accessed 29 January 13. http://www.inegi.gob.mx/est/contenidos/espanol/sistemas/cem05/info/tab/m004/mapas.pdf.
Labud, V., García, C., & Hernández, T. (2007). Effect of hydrocarbon pollution on the microbial properties of a sandy and a clay soil. Chemosphere, 66, 1863–1871.
Li, X., Feng, Y., & Sawatsky, N. (1997). Importance of soil–water relations in assessing the endpoint of bioremediated soils: plant growth. Plant and Soil, 192, 219–226.
Martí, M. C., Camejo, D., Fernández-García, N., Rellán-Álvarez, R., Marques, S., Sevilla, F., & Jiménez, A. (2009). Effect of oil refinery sludges on the growth and antioxidant system of alfalfa plants. Journal of Hazardous Materials, 172, 879–885.
Merkl, N., Schultze-Kraft, R., & Arias, M. (2006). Effect of the tropical grass Brachiaria brizantha (Hochst. ex A. Rich.) Stapf on microbial population and activity in petroleum-contaminated soil. Microbiological Research, 161, 80–91.
Merkl, N., Schultze-Kraft, R., & Infante, C. (2005). Assessment of tropical grasses and legumes for phytoremediation of petroleum-contaminated soils. Water, Air, and Soil Pollution, 165, 195–209.
Mittler, R. (2002). Oxidative stress, antioxidants y stress tolerance. Trends in Plant Science, 7, 405–410.
Mohsenzade, F., Nasseri, S., Mesdaghinia, A., Nabizadeh, R., Zafari, D., & Chehregani, A. (2009). Phytoremediation of petroleum-contaminated soils: pre-screening for suitable plants and rhizospheral fungi. Toxicological and Environmental Chemistry, 91(8), 1443–1453.
Moller, I. M. (2001). Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 561–591.
Moller, I. M., Jensen, P. E., & Hansson, A. (2007). Oxidative modifications to cellular components in plants. Annual Review of Plant Biology, 58, 459–481.
Mostacedo, B., & Fredericksen, T. S. (2001). Regeneración y silvicultura de bosques tropicales en Bolivia (Proyecto de Manejo Forestal Sostenible (BOLFOR)). Santa Cruz: Editora El País.
Mulawarman, J., Roshetko, M., Sasongko, S. M., & Irianto, D. (2003). Tree seed management—seed sources, seed collection and seed handling: a field manual for field workers and farmers. Bogor: International Centre for Research in Agroforestry (ICRAF) and Winrock International.
Ochoa-Gaona, S., Pérez Hernández, I., Frías Hernández, J. A., Jarquín Sánchez, A., & Méndez Valencia, A. (2011). Estudio prospectivo de especies arbóreas promisorias para la fitorremediación de suelos contaminados por hidrocarburos. Villahermosa, Tabasco, México: Colección Bicentenario-José Narciso Rovirosa. Secretaria de Recursos Naturales y Protección Ambiental y El Colegio de la Frontera Sur.
Pilon-Smits, E. (2005). Phytoremediation. Annual Review of Plant Biology, 56, 15–39.
Porta, A., Filliat, N., & Plata, N. (1999). Phytotoxicity and phytoremediation studies in soils polluted by weathered oil. In A. Lesson & B. C. Alleman (Eds.), Phytoremediation and innovative strategies for specialized remedial applications (pp. 51–56). Columbus: Battelle Press.
Pothuluri, J. V. & Cerniglia, C. E. (1994). Microbial metabolism of polycyclic aromatic hydrocarbons, In G.R Chaudhry (Ed). Biological Degradation and Bioremediation of Toxic Chemicals (pp. 92–124), Portland, OR: Dioscorides.
Quiñones Aguilar, E. E., Ferrera Cerrato, R., Gavi Reyes, F., Fernández Linares, L., Rodríguez Vázquez, R., & Alarcón, A. (2003). Emergencia y crecimiento de maíz en un suelo contaminado con petróleo crudo. Agrociencia, 37(6), 585–594.
Reynoso-Cuevas, L., Gallegos-Martínez, M. E., Cruz-Sosa, F., & Gutiérrez-Rojas, M. (2008). In vitro evaluation of germination and growth of five plant species on medium supplemented with hydrocarbons associated with contaminated soils. Bioresource Technology, 99, 6379–6385.
Rivera-Cruz, M. C., & Trujillo, N. A. (2004). Estudio de toxicidad vegetal en suelos con petróleos nuevo e intemperizado. Interciencia, 29(7), 369–376.
Rivera-Cruz, M. C., Ferrera-Cerrato, R., Sánchez-García, P., Volke-Haller, V., Fernández-Linares, L., & Rodríguez-Vázquez, R. (2004). Descontaminación de suelos con petróleo crudo mediante microorganismos autóctonos y pasto alemán [Echinochloa polystachya (H.B.K.) Hitchc.]. Agrociencia, 38(1), 1–12.
Roy, J. L., & McGill, W. B. (1998). Characterization of disaggregated non wettable surface soils found at old spill site. Canadian Journal of Soil Science, 78, 331–344.
Salanitro, J. P., Dorn, P. B., Huesemann, H. M., Moore, K. O., Rhodes, I. A., Rice Jackson, L. M., Vipond, T. E., Western, M. M., & Wisniewski, H. L. (1997). Crude oil hydrocarbon bioremediation and soil ecotoxicity assessment. Environmental Science and Technology, 31(6), 1769–1776.
Salt, D. E., Smith, R. D., & Raskin, I. (1998). Phytoremediation. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 643–668.
Sautu, A., Baskin, J. M., Baskin, C. C., Deago, J., & Condit, R. (2007). Classification and ecological relationships of seed dormancy in a seasonal moist tropical forest, Panama, Central America. Seed Science Research, 17, 127–140.
Saval, S. (1997). Biorremediación de un suelo contaminado con diesel. Ingeniería y Ciencias Ambientales, 33, 24–30.
Sawatsky, N., & Li, X. (1997). Importance of soil–water relations in assessing the endpoint of bioremediated soils II. Water-repellency in hydrocarbon contaminated soils. Journal of Plant Soil, 192, 227–236.
Schnoor, J. L., Licht, L. A., McCutcheon, S. C., Wolfe, N. L., & Carreira, L. H. (1995). Phytoremediation of organic and nutrient contaminants. Environmental Science and Technology, 29(7), 318A–323A.
SEMARNAT. (2005) Norma Oficial Mexicana NOM-138-SEMARNAT/SS-2003, Límites máximos permisibles de hidrocarburos en suelos y las especificaciones para su caracterización y remediación. México, DF, México: Secretaría del Medio Ambiente y Recursos Naturales, Diario Oficial de la Federación, 29/03/2005.
Sharifi, M., Sadeghi, Y., & Akbarpour, M. (2007). Germination and growth of six plant species on contaminated soil with spent oil. International journal of Environmental Science and Technology, 4(4), 463–470.
Shirdam, R., Zand, D. A., Nabi, B. G., & Mehrdadi, N. (2008). Phytoremediation of hydrocarbon-contaminated soils with emphasis on the effect of petroleum hydrocarbons on the growth of plant species. Phytoprotection, 89(1), 21–29.
US EPA-3540C. (1996). Soxhlet extraction organics. SW-846 Test methods for evaluating solid waste physical/chemical methods. http://www.epa.gov/wastes/hazard/testmethods/sw846/pdfs/3540c.pdf. Accessed 20 June 2012.
Vázquez-Luna, D., Castelán-Estrada, M., Rivera-Cruz, M. C., Ortiz-Ceballos, A. I., & Izquierdo, F. (2010). Crotalaria incana L. y Leucaena leucocephala Lam. (LEGUMINOSAE): Especies indicadoras de toxicidad por hidrocarburos de petróleo en el suelo. Revista Internacional de Contaminación Ambiental, 26(3), 183–191.
Vázquez-Yanes, C., Batis Muñoz, A. I., Alcocer Silva, M. I., Gual Díaz M. & Sánchez Dirzo, C. (1999) Árboles y arbustos potencialmente valiosos para la restauración ecológica y la reforestación. Reporte técnico del proyecto J084. CONABIO—Instituto de Ecología, UNAM http://www.conabio.gob.mx/conocimiento/info_especies/arboles/doctos/introd-J084.html. Accessed 20 may 2013.
Vozzo, J. A. (2002). Tropical tree seed manual. Agricultural Handbook 721. Washington, DC: United States Department of Agriculture, Forest Service.
Walton, B. T., Guthrie, E. A., & Hoylman, A. M. (1994). Toxicant degradation in the rhizosphere. In T. A. Anderson & J. R. Coats (Eds.), Bioremediation through rhizosphere technology (ACS Symposium Series, pp. 11–26). Washington, DC: American Chemical Society.
White Jr., P. M., Wolf, D. C., Thoma, G. J. & Reynold, C. M. (2006). Phytoremediation of alkylated polycyclic aromatic hydrocarbons in a crude oil-contaminated soil. Water, Air, and Soil Pollution, 169, 207–220.
Zamora-Cornelio, L. F., Ochoa-Gaona, S., Vargas Simón, G., Castellanos Albores, J., & de Jong, B. H. J. (2010). Seed germination and key to seedling identification for six native tree species of wetlands from Southeast Mexico. International Journal of Tropical Biology and Conservation, 58(2), 717–732.
Acknowledgements
We thank Manuel Mendoza Carranza y Noel Antonio González Valdivia who provided advice on statistical analysis. Aaron Jarquín Sánchez was most helpful with the soil analysis. José Guadalupe Chan-Quijano helped with laboratory activities. The Consejo Nacional de Ciencia y Tecnología (CONACYT) provided a scholarship (207824) for doctoral studies to Isidro Pérez Hernández. El Colegio de la Frontera Sur provided infrastructure and financial support.
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Pérez-Hernández, I., Ochoa-Gaona, S., Adams Schroeder, R.H. et al. Tolerance of Four Tropical Tree Species to Heavy Petroleum Contamination. Water Air Soil Pollut 224, 1637 (2013). https://doi.org/10.1007/s11270-013-1637-7
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DOI: https://doi.org/10.1007/s11270-013-1637-7