Skip to main content
Log in

Arbuscular Mycorrhizal Colonization in a Mangrove Forest Exposed to Weathering Oil for Half a Century

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Plants establish symbiosis with arbuscular mycorrhizal fungi (AMFs) for nutrient exchange and also for tolerance to contaminants. During February 2019, soil and rhizosphere samples of Laguncularia racemosa (Lr) and Avicennia germinans (Ag) were collected on 4.15 hectares of a mangrove forest established in Histosol affected since 1967 by chronic oil spill in southeastern Mexico. The site was divided into four zones based on the amounts of total hydrocarbons of weathered petroleum (THWPs) accumulated in the soil for half a century. The abundance of intraradical propagules and the colonization structure of the AMFs in the roots of the two mangrove species were compared. The density of phosphate-solubilizing bacteria (PSBs) in soil and rhizosphere samples was also evaluated. The degraded oil stimulated the amount of PSBs in Lr but not in Ag. AMF biodiversity was lower in the Ag root; however, spore abundance was higher. We found abundant spores of Glomus claroideum and Diversispora aurantium in tertiary and quaternary roots of the Ag in soils contaminated with 48462 mg of THWPs. This study provides evidence of the presence and abundance of intraradical propagules in different types of roots, which may be an alternative that contributes to the understanding of oil dissipation and in future applications for the restoration of degraded ecosystems.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Alarcón, A., Delgadillo-Martínez, J., Franco-Ramírez, A., Davies Jr., F. T., & Ferrera-Cerrato, R. (2006). Influence of two polycyclic aromatic hydrocarbons on spore germination, and phytoremediation potential of Gigaspora margarita-Echinochloa polystachya symbiosis in benzo[a]pyrene-polluted substrate. Revista Internacional de Contaminación Ambiental, 22(1), 39–47.

    Google Scholar 

  • Alejandro-Córdova, A., Rivera-Cruz, M. C., Hernández-Cuevas, L. V., Alarcón, A., Trujillo-Narcía, A., & García-de la Cruz, R. (2017). Responses of arbuscular mycorrhizal fungi and grass Leersia hexandra Swartz exposed to soil with crude oil. Water Air and Soil Pollution, 228, 1–12. https://doi.org/10.1007/s11270-017-3247-2.

    Article  CAS  Google Scholar 

  • Aranda, E., Scervino, J. M., Godoy, P., Reina, R., Ocampo, J. A., Wittich, R.-M., & García-Romera, I. (2013). Role of arbuscular mycorrhizal fungus Rhizophagus custos in the dissipation of PAHs under root-organ culture conditions. Environmental Pollution, 181, 182–189. https://doi.org/10.1016/j.envpol.2013.06.034.

    Article  CAS  Google Scholar 

  • Araujo, M. P., Hamacher, C., de Oliveira, F. C., Martinho, P., de Oliveira, C. F., & Gomes, S. M. L. (2020). Assessment of Brazilian mangroves hydrocarbon contamination from a latitudinal perspective. Marine Pollution Bulletin, 150, 110673. https://doi.org/10.1016/j.marpolbul.2019.110673.

    Article  CAS  Google Scholar 

  • Atlas, R. M. (1981). Microbial degradation of petroleum hydrocarbons: an environmental perspective. Microbiology Reviews, 45(1), 180–209. I0146-0749/81/010180-30802.00/0

  • Berg, G., & Smalla, K. (2009). Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiology Ecology, 68(1), 1–13. https://doi.org/10.1111/j.1574-6941.2009.00654.x.

    Article  CAS  Google Scholar 

  • Binet, P., Portal, J. M., & Leyval, C. (2000). Fate of polycyclic aromatic hydrocarbons (PAH) in the rhizosphere and mycorrhizosphere of ryegrass. Plant and Soil, 227, 207–213. https://doi.org/10.1023/A:1026587418611.

    Article  CAS  Google Scholar 

  • Blaszkowski, J. (2019). Arbuscular mycorrhizal fungi (Glomeromycota), endogone and complexipes species deposited in the Departament of Plant Pathology, University of Agriculture in Szczecin, Poland. http://www.zor.zut.edu.pl/Glomeromycota/index.html. Accessed 23 July 2019.

  • Botello, A.V. (2005). Características, composición y propiedades fisicoquímicas del petróleo. In A.V. Botello, J. Rendón-von Osten, G. Gold-Bouchot, G. & C. Agraz-Hernández (Eds.), Golfo de México Contaminación Ambiental: Diagnóstico y Tendencia (pp. 261-268). México: Universidad Autónoma de Campeche. Instituto Nacional de Ecología.

  • Brady, N. C., & Weil, R. R. (2008). The nature and properties of soils. 14th ed. Pearson-Prentice Hall. New Jersey. ISBN 0-13-227938-X

  • Calonne-Salmon, M., Plouznikoff, K., & Declerck, S. (2018). The arbuscular mycorrhizal fungus Rhizophagus irregularis MUCL 41833 increases the phosphorus uptake and biomass of Medicago truncatula, a benzo[a]pyrene-tolerant plant species. Mycorrhiza, 28(8), 761–771. https://doi.org/10.1007/s00572-018-0861-9.

    Article  CAS  Google Scholar 

  • Camarena-Gutiérrez, G. (2012). Interacción planta-hongos micorrícicos arbusculares. Revista Chapingo Serie Ciencias Forestales y Ambientales, 18(3), 409–421. https://doi.org/10.5154/r.rchscfa.2011.11.093.

    Article  Google Scholar 

  • Chandra, B. B., Kumar, S. S., Ranjan, M. R., Kumar, S. B., Kumar, D. S., & Nath, T.H. (2016). Phosphate solubilizing bacteria from mangrove soils of Mahanadi River Delta, Odisha, India. World Journal of Agricultural Research, 4(1), 18-23. 10.12691/wjar-4-1-3

  • Daniels, B. A., & Skipper, H. A. (1982). Methods for the recovery and quantitative estimation of propagules from soil. In N. C. Schenck (Ed.), Methods & Principles of Mycorrhizal Research (pp. 29–35). St. Paul: American Phytopatological Society.

    Google Scholar 

  • Das, S., De, M., Ganguly, D., Kanti, M. T., Mukherjee, A., Kumar, J. T., & Kuma, D. T. (2012). Depth integrated microbial community and physico-chemical properties in mangrove soil of Sundarban, India. Advances in Microbiology, 2, 234–240. https://doi.org/10.4236/aim.2012.23028.

    Article  CAS  Google Scholar 

  • de la Providencia, I. E., Stefani, F. O. P., Labridy, M., St-Arnaud, M., & Hijri, M. (2015). Arbuscular mycorrhizal fungal diversity associated with Eleocharis obtusa and Panicum capillare growing in an extreme petroleum hydrocarbon-polluted sedimentation basin. FEMS Microbiology Letters, 362(12), 1–9. https://doi.org/10.1093/femsle/fnv081.

    Article  CAS  Google Scholar 

  • Díaz, P. G., Ruiz, C. J. A., Medina, G. G., Cano, G. M. A., & Serrano, A. V. (2006). Estadísticas Climáticas Básicas del Estado de Tabasco (Periodo 1961-2003). No. 12. México: INIFAP. CIRGOC. Campo Experimental Cotaxtla. México.

    Google Scholar 

  • DOF (Diario Oficial de la Federación) 2013. Norma Oficial Mexicana NOM-138-SEMARNAT/SSA1-2012, Límites máximos permisibles de hidrocarburos en suelos y lineamientos para el muestreo en la caracterización y especificaciones para la remediación.

  • Dueñas, L. H., & Nieto, R. C. (2010). Dendrología Tropical: Estudio y Caracterización Dendrológica de las Principales Especies Forestales de la Amazonia Peruana (1a. ed.). Universidad Nacional Amazónica de Madre de Dios. Lima. ISBN 978-612-00-0514-9

  • Franco-Ramírez, A., Ferrera-Cerrato, R., Varela-Fregoso, L., Pérez-Moreno, J., & Alarcón, A. (2007). Arbuscular mycorrhizal fungi in chronically petroleum contaminated soils in Mexico and the effects of petroleum hydrocarbons on spore germination. Journal of Basic Microbiology, 47(5), 378–383. https://doi.org/10.1002/jobm.200610293.

    Article  CAS  Google Scholar 

  • Gao, Y., Li, Q., Ling, W., & Zhu, X. (2011). Arbuscular mycorrhizal phytoremediation of soils contaminated with phenanthrene and pyrene. Journal of Hazardous Materials, 185(2-3), 703–709. https://doi.org/10.1016/j.jhazmat.2010.09.076.

    Article  CAS  Google Scholar 

  • Garcés-Ruiz, M., Senés-Guerrero, C., Declerck, S., & Cranenbrouck, S. (2018). Community composition of arbuscular mycorrhizal fungi associated with native plants growing in a petroleum-polluted soil of the Amazon region of Ecuador. MicrobiologyOpen, 8(4), e00703. https://doi.org/10.1002/mbo3.703.

    Article  CAS  Google Scholar 

  • Gerdemann, J. W., & Nicholson, T. H. (1963). Spores of mycorrhizal endogone species extracted from soil by wet sieving and decanting. Transactions of the British Mycological Society, 46(2), 235–244. https://doi.org/10.1016/S0007-1536(63)80079-0.

    Article  Google Scholar 

  • Giovannetti, M., & Mosse, M. (1980). An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytologist, 84(3), 489–500. https://doi.org/10.1111/j.1469-8137.1980.tb04556.x.

  • Guadamarra, F. P., & Álvarez-Sánchez, J. (1999). Abundance of arbuscular mycorrhizal fungi spores in different environments in a tropical rain forest, Veracruz, México. Mycorrhiza, 8(5), 267–270. https://doi.org/10.1007/s005720050244.

    Article  Google Scholar 

  • Gundlach, R. E. (2018). Oil-related mangrove loss east of Bonny River, Nigeria. In C. Makowski & C. Finkl (Eds.), Threats to mangrove forests hazards, vulnerability and management (pp. 267–321). Berlin: Springer.

    Chapter  Google Scholar 

  • Gyaneshwar, P., Naresh, K. G., Parekh, L. J., & Poole, P. S. (2002). Role of soil microorganisms in improving P nutrition of plants. Plant and Soil, 245(1), 83–93. https://doi.org/10.1023/A:1020663916259.

    Article  CAS  Google Scholar 

  • He, F., Chen, H., & Tang, M. (2019). Arbuscular mycorrhizal fungal communities are influenced by host tree species on the Loess Plateau, Northwest China. Forests, 10(10), 1–16. https://doi.org/10.3390/f10100930.

    Article  Google Scholar 

  • Hernández-Ortega, A. H., Alarcón, A., Ferrera-Cerrato, R., Zavaleta-Mancera, H. A., López-Delgado, H. A., & Mendoza-López, M. R., 2012. 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, Suppl. S319eS324. https://doi.org/10.1016/j.jenvman.2011.02.015.

  • Holguín, G., González-Zamorano, G. P., de-Bashan, L. E., Mendoza, R., Amador, E., & Bashan, Y. (2006). Mangrove health in an arid environment encroached by urban development-a case study. Science of the Total Environment, 363(1-3), 260–274. https://doi.org/10.1016/j.scitotenv.2005.05.026.

    Article  CAS  Google Scholar 

  • Iffis, B., St-Arnaud, M., & Hijri, M. (2014). Bacteria associated with arbuscular mycorrhizal fungi within roots of plants growing in a soil highly contaminated with aliphatic and aromatic petroleum hydrocarbons. FEMS Microbiology Letters, 358(1), 44–54. https://doi.org/10.1111/1574-6968.12533.

    Article  CAS  Google Scholar 

  • Iffis, B., St-Arnaud, M., & Hijri, M. (2016). Petroleum hydrocarbon contamination, plant identity and arbuscular mycorrhizal fungal (AMF) community determine assemblages of the AMF spore-associated microbes. Environmental Microbiology, 18(8), 2689–2704. https://doi.org/10.1111/1462-2920.13438.

    Article  CAS  Google Scholar 

  • INVAM (International Culture Collection of Arbuscular & Vesicular-Arbuscular Mycorrhizal Fungi). (2019). http://invam.wvu.edu/thefungi/classification/diversisporaceae/diversispora/eburneum; http://invam.wvu.edu/thefungi/classification/glomaceae/funneliformis/geosporum; http://invam.wvu.edu/thefungi/classification/glomaceae/funneliformis/mossea. Accessed 23 July 2019.

  • Jian, S. Q., Wu, Z., Hu, C., & Zhang, X. (2016). Sap flow in response to rainfall pulses for two shrub species in the semiarid Chinese Loess Plateau. Journal of Hidrology and Hydromechanics, 64(2), 121–132. https://doi.org/10.1515/johh-2016-0023.

    Article  Google Scholar 

  • Jiménez, J. A. (2000). Laguncularia racemosa (L.) Gaertn. f. In J. K. Francis, & C. A. Lowe (Eds.), Bioecología de Árboles Nativos y Exóticos de Puerto Rico y las Indias Occidentales (pp. 302-307). Río Piedras: United States Department of Agriculture.

  • Jiménez, J. A., & Lugo, A. E. (2000). Avicennia germinans (L.) L. In J. K. Francis & C. A. Lowe (Eds.), Bioecología de Árboles Nativos y Exóticos de Puerto Rico y las Indias Occidentales (pp. 59–64). Río Piedras: United States Department of Agriculture.

    Google Scholar 

  • Joner, E. J., & Leyval, C. (2003). Rhizosphere gradients of polycyclic aromatic hydrocarbon (PAH) dissipation in two industrial soils and the impact of arbuscular mycorrhiza. Environmental, Science and Technology, 37, 2371–2375. https://doi.org/10.1021/es020196y.

    Article  CAS  Google Scholar 

  • Kathiresan, K., & Selvam, M. M. (2006). Evaluation of beneficial bacteria from mangrove soil. Botanica Marina, 49(1), 86–88. https://doi.org/10.1515/BOT.2006.011.

    Article  CAS  Google Scholar 

  • Kathiresan, K., Saravanakumar, K., Anburaj, R., Gomathi, V., Abirami, G., Sahu, S. K., & Anandhan, S. (2011). Microbial enzyme activity in decomposing leaves of mangroves. International Journal of Advaced Biotechnology and Research, 2(3), 382–389.

    Google Scholar 

  • Kirk, J. L., Moutoglis, P., Klironomos, J., Lee, H., & Trevors, J. T. (2005). Toxicity of diesel fuel to germination, growth and colonization of Glomus intraradices in soil and in vitro transformed carrot root cultures. Plant and Soil, 270(1-2), 23–30. https://doi.org/10.1007/s11104-004-1013-x.

    Article  CAS  Google Scholar 

  • Little, I. D., Holtzmann, K., Gundlach, R. E., & Galperin, Y. (2018). Sediment hydrocarbons in former mangrove areas, Southern Ogoniland, Eastern Niger Delta, Nigeria. In C. Makowski & W. C. Finkl (Eds.), Threats to mangrove forests hazards, vulnerability, and management (pp. 323–342). Berlin: Springer.

    Chapter  Google Scholar 

  • López-Jiménez, J. G., Rivera-Cruz, M.C., Trujillo-Narcía, A, Aceves-Navarro, L. A., Sol-Sánchez, A., & Sarracino-Martínez, O. (2019). Laguncularia racemosa (Combretaceae) y bacterias terrestres asociadas medio siglo después de la contaminación crónica por hidrocarburos. Revista de Biología Tropical, 67(6), 1194-1209. 10.15517/rbt.v67i6.35861

  • Lovelock, C. E., Andersen, K., & Morton, J. B. (2003). Arbuscular mycorrhizal communities in tropical forests are affected by host tree species and environment. Oecologia, 135(2), 268–279. https://doi.org/10.1007/s00442-002-1166-3.

    Article  Google Scholar 

  • Madigan, M. T., Martinko, J. M., Bender, K. S., Buckley, D. H., & Sthal, D. A. (2015). Brock. Biología de los Microorganismos (14a. ed.). Pearson Educación, S.A. Madrid. ISBN 978-84-9035-279-3

  • Maier, M. R., & Gentry, J. T. (2015). Microorganism and organic pollutants. In L. I. Pepper, P. C. Gerba, & J. T. Gantry (Eds.), Environmental microbiology (pp. 377–411). Walthman: Academic Press Elsevier.

    Chapter  Google Scholar 

  • Marschner, P. (2012). Rhizosphere biology. In P. Marschner (Ed.), Marschner’s mineral nutrition of higher plants (pp. 369–388). Walthman: Academic Press Elsevier.

    Chapter  Google Scholar 

  • Media Cybernetics (2001). Image-Pro Plus version 4.5.1.22 for windows. Silver Spring: Media Cybernetics Inc.

  • Miller, S. P., & Sharitz, R. R. (2000). Manipulation of flooding and arbuscular mycorrhiza formation influences growth and nutrition of two semi-aquatic grasses. Functional Ecology, 14(6), 738–748. https://doi.org/10.1046/j.1365-2435.2000.00481.x.

    Article  Google Scholar 

  • Nardini, C. B., Di Salvo, P. L., & de García, S. I. E. (2011). Micorrizas arbusculares: asociaciones simbióticas e indicadores de calidad ambiental en sistemas de cultivos extensivos. Revista Argentina de Microbiología, 43(4), 311–319.

    Google Scholar 

  • Nwoko, C. O. (2014). Effect of arbuscular mycorrhizal (AM) fungi on the physiological performance of Phaseolus vulgaris grown under crude oil contaminated soil. Journal of Geoscience and Environment Protection, 2(4), 9–14. https://doi.org/10.4236/gep.2014.24002.

    Article  Google Scholar 

  • Omar, M. B., Bolland, L., & Heather, W. A. (1979). A permanent mounting medium for fungi. Bulletin of the British Mycological Society, 13(1), 31–32. https://doi.org/10.1016/S0007-1528(79)80038-3.

    Article  Google Scholar 

  • Orocio, C. J. A. (2014). Evaluación de los hidrocarburos de petróleo intemperizado en Histosol de un manglar en La Venta, Tabasco. Universidad Popular de la Chontalpa. H. Cárdenas, Tabasco, México.

  • Ortiz, O. M. (2009). Historia de la Explotación Petrolera en Tabasco 1900-1960 (1a. ed.). PEMEX. UJAT. México.

  • Paredes, M. M., & Espinosa, V. D. (2010). Ácidos orgánicos producidos por rizobacterias que solubilizan fosfato: una revisión crítica. Terra Latinoamericana, 28(1), 61–70.

    Google Scholar 

  • Paterson, E., Sim, A., Davidson, J., & Daniell, T. J. (2016). Arbuscular mycorrhizal hyphae promote priming of native soil organic matter mineralization. Plant and Soil, 408(1-2), 243–254. https://doi.org/10.1007/s11104-016-2928-8.

    Article  CAS  Google Scholar 

  • Phillips, J. M., & Hayman, D. S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycology Society, 55(1), 158–161. https://doi.org/10.1016/S0007-1536(70)80110-3.

    Article  Google Scholar 

  • Pikovskaya, R. I. (1948). Mobilization of phosphorus in soil in connection with their vital activities of some microbial species. Microbiology, 17, 362–370.

    CAS  Google Scholar 

  • Plante, A. F., Stone, M. M., & McGill, W. B. (2015). The metabolic physiology of soil microorganisms. In E. A. Paul (Ed.), Soil microbiology, ecology, and biochemistry (pp. 245–272). San Francisco: Academic Press Elsevier.

    Chapter  Google Scholar 

  • Pravecek, L. T., Christaman, F. R., & Pfaender, K. F. (2005). Impact of imposed anaerobic conditions and microbial activity on aqueous-phase solubility of polycyclic aromatic hydrocarbons from soil. Environmental Toxicology and Chemistry, 24(2), 286–293. https://doi.org/10.1897/04-109r.1.

    Article  CAS  Google Scholar 

  • Purnobasuki, H. (2013). Characteristics of root caps in four root types of Avicennia marina (Forsk.) Vierh. American Journal of Plant Sciences, 4(4), 853–858. https://doi.org/10.4236/ajps.2013.44105.

    Article  Google Scholar 

  • Rajtor, M., & Piotrowska-Seget, Z. (2016). Prospects for arbuscular mycorrhizal fungi (AMF) to assist in phytoremediation of soil hydrocarbon contaminants. Chemosphere, 162, 105–116. https://doi.org/10.1016/j.chemosphere.2016.07.071.

    Article  CAS  Google Scholar 

  • Ramírez-Viga, T. K., Ramos-Zapata, J. A., Cáceres, G. C. C., Hernández-Cuevas, L., & Guadarrama-Chávez, G. (2020). Arbuscular mycorrhizal association in Conocarpus erectus (Combretaceae) in mangroves from Yucatán, Mexico. Botanical Sciences, 98(1), 66-75. 10.17129/botsci.2363

  • Redecker, D., Schüßler, A., Stockinger, H., Stürmer, S. L., Morton, J. B., & Walker, C. (2013). An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota). Mycorrhiza, 23(7), 515–531. https://doi.org/10.1007/s00572-013-0486-y.

    Article  Google Scholar 

  • Rivera-Cruz, M. C., & Trujillo-Narcía, A. (2004). Estudio de toxicidad vegetal en suelos con petróleo nuevo e intemperizado. Interciencia, 29(7), 369–376.

    Google Scholar 

  • Rodríguez-Rodríguez, N., Rivera-Cruz, M. C., Trujillo-Narcía, A., Almaráz-Suárez, J. J., & Salgado-García, S. (2016). Spatial distribution of oil and biostimulation through the rhizosphere of Leersia hexandra in degraded soil. Water Air and Soil Pollution, 227(9), 1–14. https://doi.org/10.1007/s11270-016-3030-9.

    Article  CAS  Google Scholar 

  • Rosatto-Moda, L., Mello-Prado, R., Castellanos-González, L., Reyes-Hernández, A., Caione, G., & Silva-Campos, N. C. (2014). Solubilización de fuentes de fósforo asociadas a un compuesto orgánico enriquecido con biofertilizantes. Agrociencia, 48(5), 489–500.

    Google Scholar 

  • Saravanakumar, K., Anburaj, R., Gomathi, V., & Kathiresan, K. (2016). Ecology of soil microbes in a tropical mangrove forest of south east coast of India. Biocatalysis and Agricultural Biotechnology, 8, 73–85. https://doi.org/10.1016/j.bcab.2016.08.010.

    Article  Google Scholar 

  • SAS (Statistical Analysis System). (2005). User’s guide, version 9.1.3. Cary: SAS Institute, Inc.

  • Sbrana, C. (2006). Fungal recognition response to host derived signals by arbuscular mycorrhizal fungi. In K. G. Mukerji, C. Manoharachary, & J. Singh (Eds.), Microbial activity in the rhizosphere (pp. 223–243). Berlin: Springer.

    Chapter  Google Scholar 

  • Schüβler, A. (2015). Glomeromycota Philogeny. http://schuessler.userweb.mwn.de/amphylo/. .

  • Thanh, T. H., & Ngoc, D. C. (2017). Isolation and characterization of bacteria of mangrove rhizosphere in the Mekong Delta, Vietnam. International Journal of Innovations in Engineering and Technology, 9(1), 69-79. 10.21172/ijiet.91.11

  • Trujillo-Narcía, A., Rivera-Cruz, M. C., Lagunes-Espinoza, L. C., Palma-López, D. J., Sánchez-Soto, S., & Ramírez-Valverde, G. (2014). Uso de fertilizantes orgánicos en la enmendación de un Fluvisol restaurado tras la contaminación con petróleo. Interciencia, 39(4), 266–273.

    Google Scholar 

  • USEPA (1996). EPA-3540C. Soxhlet extraction organics. SW-846 Test methods for evaluating solid wast physical/chemical methods. http://www.epa.gov/wastes/hazard/testmethods/sw846/pdfs/3540c.pdf. Accessed 30 January 2019.

  • Wang, Y., Qiu, Q., Yang, Z., Hu, Z., Fung-Yee, T. N. V., & Xin, G. (2010). Arbuscular mycorrhizal fungi in two mangroves in South China. Plant and Soil, 331(1-2), 181–191. https://doi.org/10.1007/s11104-009-0244-2.

    Article  CAS  Google Scholar 

  • West, R. C., Psuty, N. P., & Thom, B. G. (1985). Las Tierras Bajas de Tabasco en el Sureste de México (1a. ed.). Gobierno de Estado de Tabasco. México. ISBN 968-889-019-7

  • Wu, F. Y., Yu, Z. Z., Wu, S. C., Lin, X. G., & Wong, M. H. (2011). Phenanthrene and pyrene uptake by arbuscular mycorrhizal maize and their dissipation in soil. Journal of Hazardous Materials, 187(1-3), 341–347. https://doi.org/10.1016/j.jhazmat.2011.01.024.

    Article  CAS  Google Scholar 

  • Zhang, J., Cai, L., Yuan, D., & Chen, M. (2004). Distribution and sources of polynuclear aromatic hydrocarbons in mangrove superficial sediments of Deep Bay, China. Marine Pollution Bulletin, 49(5-6), 479–486. https://doi.org/10.1016/j.marpolbul.2004.02.030.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The first author thanks the Consejo Nacional de Ciencia y Tecnología, México for the scholarship awarded (file 886396) to carry out Master of Science studies. To the owner of the land, Mrs. Darvelia Flores Romero, for allowing access to the mangrove forest for soil sampling.

Funding

This research was partially funded with resources from the Colegio de Postgraduados en Ciencias Agrícolas.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to María del Carmen Rivera-Cruz.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martínez-Hernández, I.A., Rivera-Cruz, M.d.C., Carballar-Hernández, S. et al. Arbuscular Mycorrhizal Colonization in a Mangrove Forest Exposed to Weathering Oil for Half a Century. Water Air Soil Pollut 232, 34 (2021). https://doi.org/10.1007/s11270-021-04986-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-021-04986-8

Keywords

Navigation