Springer Nature is making Coronavirus research free. View research | View latest news | Sign up for updates

Growth of four tropical tree species in petroleum-contaminated soil and effects of crude oil contamination


Under greenhouse conditions, we evaluated establishment of four tree species and their capacity to degrade crude oil recently incorporated into the soil; the species were as follows: Cedrela odorata (tropical cedar), Haematoxylum campechianum (tinto bush), Swietenia macrophylla (mahogany), and Tabebuia rosea (macuilis). Three-month-old plants were planted in soil with three treatments of heavy petroleum and a control (C0 0 mg kg−1; C1 18,000 mg kg−1; C2 31,700 mg kg−1; C3 47,100 mg kg−1) with four repetitions per treatment and species; the experiment was carried out for 245 days. Height and biomass of all species significantly diminished as petroleum concentration increased, although plant survival was not affected. The quantity of colony-forming units (CFU) of rhizospheric bacteria varied among tree species and treatments; petroleum stimulated bacterial CFU for S. macrophylla. The number of fungi CFU for S. macrophylla and T. rosea was significantly greater in C0 than in soil with petroleum, but among species and among different concentrations, no significant differences were found. The greatest percentage of total petroleum hydrocarbon (TPH) degradation was found in C1 for soil without plants (45 %). Differences from the remaining treatments (petroleum concentrations in soil and plant species) were not significant (P < 0.05). Among all trees, H. campechianum had the greatest TPH degradation (32.5 % in C2). T. rosea (C1) and H. campechianum (C2) resulted in petroleum degradation at levels ranging from 20.5 to 32.5 %. On the basis of this experiment, the tree species used did not improve TPH degradation. However, all of them showed high rates of survival and vigor. So, as tree species provide goods and services, experiments with inoculation of hydrocarbonclastic microorganisms, addition of fertilizers, and mixture of tree and grasses are recommended.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5


  1. Adam G, Duncan H (2002) Influence of diesel fuel on seed germination. Environ Pollut 120:363–370

  2. Adams RH, Zavala-Cruz J, Morales-García F (2008) Concentración residual de hidrocarburos en suelo del trópico II: Afectación a la fertilidad y su recuperación. Interciencia 33:483–489

  3. Alkorta I, Garbisu C (2001) Phytoremediation of organic contaminants in soils. Bioresource Technol 79:273–276

  4. Amadi AA, Dickson A, 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

  5. Aprill W, Sims RC (1990) Evaluation of the use of prairie grasses for stimulating polycyclic aromatic hydrocarbon treatment in soil. Chemosphere 20:253–265

  6. Aronson J, Milton S, Blignaut J (2007) Restoring natural capital: science, business, and practice. Island Press, Washington, DC

  7. Atlas RM (1995) Bioremediation of petroleum pollutants. Int Biodeter Biodegr 1:317–327

  8. Ayotamuno MJ, Kogbara RB (2007) Determining the tolerance level of Zea mays (maize) to a crude oil polluted agricultural soil. Afr J Biotechnol 6:1332–1337

  9. Bawa KS, Kress WJ, Nadkarni NM, Lele S (2004) Beyond paradise—meeting the challenges in tropical biology in the 21st century. Biotropica 36:437–446

  10. Binet P, Portal JM, Leval C (2000) Dissipation of 3–6 ring polycyclic aromatic in the rhizosphere of ryegrass. Soil Biol Biochem 32:2011–2017

  11. Boyle JJ, Shann JR (1998) The influence of planting and soil characteristics on mineralization of 2,4,5-T in rhizosphere soil. J Environ Q 27:704–709

  12. Briggs GG, Bromilow RH, Evans AA (1982) Relationship between lipophilicity and root uptake and translocation of non-ionized chemicals by barley. Pestic Sci 13:495–504

  13. Burken JG, Schnoor JL (1998) Predictive relationships for uptake of organic contaminants by hybrid poplar trees. Environ Sci Technol 32:3379–3385

  14. Chaineau CH, Morel JL, Oudot J (1997) Phytotoxicity and plant uptake of fuel oil hydrocarbons. J Environ Qual 26:1478–1483

  15. Chaney RL, Malik M, Li ML, Brown SL, Angle JS, Baker MJS (1997) Phytoremediation of soil metals. Curr Opin Biotech 8:279–284

  16. Cunningham DS, Berti RW (1993) Remediation of contaminated soils with green plants: an overview. In Vitro Cell Dev Biol 29:207–212

  17. Cunningham SD, Ow DW (1996) Promises and prospect of phytoremediation. Plant Physiol 110:715–719

  18. De Oliveira SG (2006) Crescimento, nutrição e estrutura do lenho juvenil de três espécies florestais com potencial de fitorremediação em solos contaminados com petróleo. Teses, Engenharia Florestal, Área de concentração em Silvicultura, do Setor de Ciências Agrárias da Universidade Federal do Paraná, Brazil

  19. Díaz-Martínez ME, Alarcón A, Ferrera-Cerrato R, Almaraz-Suarez JJ, García-Barradas O (2013) Crecimiento de Casuarina equisetifolia (Casuarinaceae) en suelo con diésel, y aplicación de bioestimulación y bioaumentación. Rev Biol Trop 61:1039–1052

  20. Díaz-Ramírez IJ, Ramírez-Saad H, Gutiérrez-Rojas M, Favela-Torres E (2003) Biodegradation of Maya crude oil fractions by bacterial strains and a defined mixed culture isolated from Cyperus laxus rhizosphere soil in a contaminated site. Can J Microbiol 12:755–761

  21. EPA (1986) Method 418.1 mod. Petroleum hydrocarbon. Total recoverable spectrophotometer infrared. Environmental Protection Agency, Washington, DC

  22. EPA (1996) Method 3540C Soxhlet extraction. Environmental Protection Agency, Washington, DC Accessed 14 September 2015

  23. FAO (1990) Guidelines for soil profile description, 3rd (revised) edn. FAO Rome/ISRIC, Wageningen

  24. Fernández LLC, Rojas ANG, Roldán CTG, Ramírez IME, Zegarra MHG, Uribe HR, Reyes ARJ, Flores HD, Arce OJM (2006) Manual de técnicas de análisis de suelos aplicadas a la remediación de sitios contaminados. Instituto Mexicano del Petróleo, Secretaría de Medio Ambiente y Recursos Naturales, Instituto Nacional de Ecología, Mexico

  25. Ferrera-Cerrato R, Alarcón A, Mendoza-López MR, Sangabriel W, Trejo-Aguilar D, Cruz-Sánchez JS, López-Ortiz C, Delgadillo-Martínez J (2007) Fitorremediación de un suelo contaminado con combustóleo utilizando Phaseolus coccineus y fertilización orgánica e inorgánica. Agrociencia 41:817–826

  26. Freedman B (1989) Environmental ecology: the impacts of pollution and other stresses on ecosystem structure and function. Academic Press, New York EEUU. 400 p

  27. Freedman B (1995). Environmental ecology. The ecological effects of pollution, disturbance and others stresses. San Diego California

  28. Frick CM, Farrell RE, Germida JJ (1999) Assessment of phytoremediation as an in-situ technique for cleaning oil-contaminated sites. Petroleum Technology Alliance of Canada, Calgary

  29. Gao YZ, Zhu LZ (2004) Plant uptake, accumulation and translocation of phenanthrene and pyrene in soils. Chemosphere 55:1169–1178

  30. García-López E, Zavala-Cruz J, Palma-López DJ (2006) Caracterización de las comunidades vegetales en un área afectada por derrames de hidrocarburos. TERRA Latinoamericana 24:17–26

  31. Gechev TS, van Breusegem F, Stone JM, Denev I, Laloi C (2006) Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28:1091–1101

  32. Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Bioch 48:909–930

  33. Gunther T, Dornberger U, Fritsche W (1996) Effect of ryegrass on biodegradation of hydrocarbons in soil. Chemosphere 33:203–215

  34. Haeseler F, Blanchet D, Druelle V, Werner P, Vandecasteele JP (1999) Ecotoxicological assessment of soils of former manufactured gas plant sites: bioremediation potential and pollutant mobility. J Environ Sci Technol 33(24):4379–4384

  35. Hernández-Acosta E, Gutiérrez-Castorena MC, Rubiños-Panta JE, Alvarado-López J (2006) Caracterización del suelo y plantas de un sitio contaminado con hidrocarburos. TERRA Latinoamericana 24(4):463–470

  36. Hobbs JR, Jentsch A, Temperton MV (2004) Restoration as an assembly and succession mediated by disturbance. In: Temperton VM, Hobbs RJ, Nuttle TJ, Halle S (eds) Assembly rules and restoration ecology: bridging the gap between theory and practice. Island Press, Washington, DC, pp. 150–167

  37. Holl KD, Loik ME, Lin EHV, Samuels IA (2000) Tropical montane forest restoration in Costa Rica: overcoming barriers to dispersal and establishment. Restor Ecol 8(4):339–349

  38. Hooper E, Legendre P, Condit R (2005) Barriers to forest regeneration of deforested and abandoned land in Panama. J Appl Ecol 42:1165–1174

  39. Hutchinson LS, Banks KM, Schwab PA (2001) Bioremediation and biodegradation phytoremediation of aged petroleum sludge: effect of inorganic fertilizer. J Environ Qual 30:395–403

  40. INEGI (2012). Cuaderno Estadístico Municipal de Centro, Tabasco Accessed 02 Oct 2013

  41. Kim SJ, Choi DH, Sim DS, Oh TS (2005) Evaluation of bioremediation effectiveness on crude oil-contaminated sand. Chemosphere 59:845–852

  42. Krcmar E, Van Kooten GC, Vertinsky I (2005) Managing forest and marginal agricultural land for multiple tradeoffs: compromising on economic, carbon and structural diversity objectives. Ecol Model 185:451–468

  43. Lin Q, Mendelssohn IA (1996) A comparative investigation of the effects of Louisiana crude oil on the vegetation of fresh, brackish, and salt marsh. Mar Poll Bull 32:202–209

  44. Lin Q, Mendelssohn IA, Suidan MT, Lee K, Venosa AD (2002) The dose-response relationship between no. 2 fuel oil and the growth of the salt marsh grass, Spartina alterniflora. Mar Pollut Bull 44:897–902

  45. Liu H, Weisman D, Ye Y, Cui B, Huang Y, Colón-Carmona A, Wang Z (2009) An oxidative stress response to polycyclic aromatic hydrocarbon exposure is rapid and complex in Arabidopsis thaliana. Plant Sci 176:375–382

  46. Martí MC, Camejo D, Fernández-García N, Rellán-Álvarez R, Marqués S, Sevilla F, Jiménez A (2009) Effect of oil refinery sludges on the growth and antioxidant system of alfalfa plants. J Hazard Mater 172:879–885

  47. Mayo-López TM, Adams HR, Domínguez-Rodríguez IV, Guzmán-Osorio JF (2010) Organic amendment optimization for treatment of hydrocarbon contaminated soil using the chemical biological stabilization process. Afri J Biotechnol 9:7079–7085

  48. Merkel N, Schulte-Kraft R, Infante C (2004) Phytoremediation of petroleum-contaminated soils in the tropics—preselection of plant species from eastern Venezuela. J Appl Bot Food Qual 78:185–192

  49. 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(1):195–209

  50. Mills MA, Bonner JS, McDonald TJ, Page CA, Autenrieth RL (2003) Intrinsic bioremediation of a petroleum-impacted wetland. Mar Pollut Bull 46:887–899

  51. Miranda-Martínez MR, Delgadillo-Martínez J, Alarcón A, Ferrera-Cerrato R (2007) Degradación de fenantreno por microorganismos en la rizosfera del pasto alemán. TERRA Latinoamericana 25(1):25–33

  52. Mittler R (2002) Oxidative stress, antioxidants y stress tolerance. Trends Plant Sci 7:405–410

  53. 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. Toxicol Environ Chem 91(8):1443–1453

  54. Moller IM (2001) Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Ann Rev Plant Phys 52:561–591

  55. Moller IM, Jensen PE, Hansson A (2007) Oxidative modifications to cellular components in plants. Annu Rev Plant Biol 58:459–481

  56. Montagnini F (2004) Plantaciones forestales con especies nativas. Una alternativa para la producción de madera y la provisión de servicios ambientales. Recursos Naturales y Ambiente 43:28–35

  57. Muratova YA, Dmitrieva VT, Panchenko VL, Turkovskaya VO (2008) Phytoremediation of oil-sludge-contaminated soil. Int J Phytoremediat 10:486–502

  58. NOM-138-SEMARNAT/SS 2003 Norma Oficial Mexicana que establece los límites máximos permisibles de hidrocarburos en suelos y las especificaciones para su caracterización y remediación.

  59. Núñez-López RA, Meas Y, Ortega R, Olguín EJ (2004) Fitorremediación fundamentos y aplicaciones. Ciencia 55:69–82

  60. Ochoa-Gaona S, Pérez Hernández I, Frías Hernández JA, Jarquín Sánchez A, Méndez Valencia A (2011) Estudio prospectivo de especies arbóreas promisorias para la fitorremediación de suelos contaminados por hidrocarburos. Villahermosa, Tabasco, Mexico: Colección Bicentenario-José Narciso Rovirosa. Secretaria de Recursos Naturales y Protección Ambiental y El Colegio de la Frontera Sur. Villahermosa, Tabasco, Mexico

  61. Ochoa-Gaona, S., Zamora-Cornelio, LF, Cabrera-Pérez, S, González-Valdivia, NA, Pérez-Hernández, I, López Moreno, V (2012) Flora leñosa útil de la sierra de Tenosique, Tabasco, Mexico. Ed. Fray Bartolomé de las Casas, San Cristóbal de las Casas, Chiapas, Mexico

  62. Olson EP, Castro A, Joern M, DuTeau MN, Pilon-Smits HAE, Reardon FK (2007) Comparison of plant families in a greenhouse phytoremediation study on an aged polycyclic aromatic hydrocarbon-contaminated soil. J Environ Qual 36:1461–1469

  63. Osuji LC, Egbuson EJ, Ojinnaka CM (2006) Assessment and treatment of hydrocarbon inundated soils using inorganic nutrient (NPK) supplements: II. A case study of eneka oil spillage in Niger Delta, Nigeria. Environ Monit Assess 115:265–278

  64. Peng S, Zhou Q, Cai Z, Zhang Z (2009) Phytoremediation of petroleum contaminated soils by Mirabilis jalapa L. in a greenhouse plot experiment. J Hazard Mater 168:1490–1496

  65. Pennington TD, Sarukhán J (2005) Árboles tropicales de México. Manual para la identificación de las principales especies, 3rd edn. Universidad Nacional Autónoma de México-Fondo de Cultura Económica, Mexico

  66. Pérez-Hernández I, Ochoa-Gaona S, Adams Schroeder HR, Rivera-Cruz MC, Geissen V (2013) Tolerance of four tropical tree species to heavy petroleum contamination. Water Air Soil Poll. doi:10.1007/s11270-013-1637-7

  67. Qiu X, Leland TW, Shah SI, Sorensen DL, Kendall EW (1997) Grass remediation for clay soil contaminated with polycyclic aromatic hydrocarbons. In: Kruger EL, Anderson TA, Coats JR (eds) Phytoremediation of soil and water contaminants, vol 664. American Chemical Society, Washington, D.C ACS Symposium Series, pp. 186–199

  68. Reilley KA, Banks MK, Schwab AP (1996) Organic chemicals in the environment: dissipation of polycyclic aromatic hydrocarbons in the rhizosphere. J Environ Qual 25:212–219

  69. Reynoso-Cuevas L, Gallegos-Martínez ME, 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 Techn 99:6379–6385

  70. Rivera-Cruz MC, Trujillo NA (2004) Estudio de toxicidad vegetal en suelos con petróleos nuevo e intemperizado. Interciencia 29:369–376

  71. Rivera-Cruz MC, 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 alemán grass [Echinochloa polystachya (H.B.K.) Hitchc.]. Agrociencia 38:1–12

  72. Rivera-Cruz MC, Maldonado-Chávez E, Trujillo-Narcía A (2012) Effects of crude oil on the growth of Brachiaria mutica and Leucaena leucocephala and on soil and plant macronutrients. Trop Subtrop Agroecosyt 15:30–39

  73. Roncal-García S, Soto-Pinto L, Castellanos-Albores J, Ramírez-Marcial N, de Jong B (2008) Sistemas agroforestales y almacenamiento de carbono en comunidades indígenas de Chiapas, Mexico. Interciencia 33:200–206

  74. Sadowsky MJ (1999) Phytoremediation: past promises and future practices. In: Bell CR, Brylinsky M, Johnson-Green P (eds) Plant-microbe interactions. Microbial biosystems: new frontiers. Proceedings of the 8th International Symposium on Microbial Ecology. Atlantic Canada Society for Microbial Ecology, Halifax

  75. Schneider DR, Billingsley B (1990) Bioremediation. A desk manual for the environmental professional. Cahners Publishing Company, Newton

  76. Schroder PJ, Harvey P, Schwitzgubel PJ (2002) Prospects for the phytoremediation of organic pollutants in Europe. Environ Sci Pollut R 9:1–3

  77. Siddiqui S, Adams WA (2001) The fate of diesel hydrocarbons in soils and their effect on the germination of perennial ryegrass. J Environ Pollut 118:49–62

  78. Slocum MG, Aide TM, Zimmerman JK, Navarro L (2006) A strategy for restoration of montane forest in anthropogenic fern thickets in the Dominican Republic. Restor Ecol 14:526–536

  79. Tate RL (1995) Soil microbiology. Wiley, New York

  80. Tisdall JM (1996) Formation of soil aggregates and accumulation of soil organic matter. In: Carter M, Steward BA (eds) Structure and organic matter storage in agricultural soils. Lewis Publishers, Boca Raton, pp. 57–87

  81. Van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol R 67:503–549

  82. Vazquez-Yanes C, Batis Muñoz AI, Alcocer Silva MI, 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. Mexico

  83. White PM Jr, Wolf DC, Thoma GJ, Reynold CM (2006) Phytoremediation of alkylated polycyclic aromatic hydrocarbons in a crude oil-contaminated soil. Water Air Soil Pollut 169:207–220

  84. Zar JH (1999) Biostatistical analysis. Prentice Hall, New Jersey

  85. Zavala-Cruz J, Gavi-Reyes F, Adams-Schoroeder RH, Ferrera-Cerrato R, Palma-López D, Vaquera-Huerta H, Domínguez-Ezquivel JM (2005) Oil spills on soils and adaptation of tropical grass in Activo Cinco Presidentes, Tabasco, Mexico. TERRA Latinoamericana 23:293–302

Download references


Thanks to Manuel Mendoza Carranza and Noel Antonio Gonzales Valdivia for suggestions regarding statistical analyses, to Candelario Torres Salvador and Guadalupe Chan Quijano for support in laboratory analyses, to Dr. Bernardus H.J. de Jong for financing part of the soil and microbiological analyses, to the Council of Science and Technology (CONACyT according to its Spanish initials) for scholarship no. 297824 for Isidro Pérez Hernández doctoral studies, and to El Colegio de la Frontera Sur for providing infrastructure and laboratories.

Author information

Correspondence to S. Ochoa-Gaona.

Additional information

Responsible editor: Elena maestri



Table 5 Probabilities of two-way ANOVA of post hoc Tukey test for bacterial CFU of the rhizosphere of the four evaluated species
Table 6 Probabilities of two-way ANOVA of post hoc Tukey test for fungi CFU of the rhizosphere of the four evaluated species
Table 7 Probabilities of two-way ANOVA of post hoc Tukey test for HTP degradation of the four evaluated species

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Pérez-Hernández, I., Ochoa-Gaona, S., Adams, R.H. et al. Growth of four tropical tree species in petroleum-contaminated soil and effects of crude oil contamination. Environ Sci Pollut Res 24, 1769–1783 (2017).

Download citation


  • Trees
  • Stress
  • Hydrocarbons
  • Remediation
  • Toxicity
  • Tolerance