Skip to main content

Advertisement

Springer Nature Link
Log in

Blood lead levels, δ-ALAD inhibition, and hemoglobin content in blood of giant toad (Rhinella marina) to asses lead exposure in three areas surrounding an industrial complex in Coatzacoalcos, Veracruz, Mexico

  • Published:
Environmental Monitoring and Assessment Aims and scope Submit manuscript

Abstract

The Coatzacoalcos Region in Veracruz, Mexico houses one of the most important industrial complexes in Mexico and Latin America. Lead is an ubiquitous environmental pollutant which represents a great risk to human health and ecosystems. Amphibian populations have been recognized as biomonitors of changes in environmental conditions. The purpose of this research is to measure exposure to lead and evaluate hematological and biochemical effects in specimens of giant toads (Rhinella marina) taken from three areas surrounding an industrial complex in the Coatzacoalcos River downstream. Lead levels in toads' blood are between 10.8 and 70.6 μg/dL and are significantly higher in industrial sites. We have found a significant decrease in the delta-aminolevulinic acid dehydratase (δ-ALAD) activity in blood from 35.3 to 78 % for the urban–industrial and industrial sites, respectively. In addition, we have identified a strong inverse relationship between the δ-ALAD activity and the blood lead levels (r = −0.84, p < 0.001). Hemoglobin and mean corpuscular hemoglobin levels, as well as the condition factor, are found to be lower at industrial sites compared with the reference sites. Our results suggest that the R. marina can be considered a good biomonitor of the δ-ALAD activity inhibition and hematological alterations at low lead concentrations.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Altland, P. D., & Brace, K. C. (1962). Red cell life span in the turtle and toad. The American Journal of Physiology, 203, 1188–1190.

    CAS  Google Scholar 

  • Andersen, J. B., Hedrick, M. S., & Wang, T. (2003). Cardiovascular responses to hypoxia and anaemia in the toad Bufo marinus. The Journal of Experimental Biology, 206, 857–865.

    Article  Google Scholar 

  • Arrieta, M. A., Peri, S. I., Apartin, C., Rosenberg, C. E., Fink, N. E., & Salibian, A. (2000). Blood lead concentration and delta-aminolevulinic acid dehydratase activity in adult Bufo arenarum. Archives of Physiology and Biochemistry, 108, 275–280.

    CAS  Google Scholar 

  • Arrieta, M. A., Apartin, C., Rosenberg, C. E., Fink, N. E., & Salibian, A. (2001). Blood lead content in peri-urban population of the South American toad Bufo arenarum. The Science of the Total Environment, 271, 99–105.

    Article  CAS  Google Scholar 

  • Arrieta, M. A., Bruzzone, L., Apartín, C., Rosenberg, C. E., Fink, N. E., & Salibián, A. (2004). Biosensors of inorganic lead exposure and effect in an adult amphibian. Archives of Environmental Contamination and Toxicology, 46, 224–230.

    CAS  Google Scholar 

  • ATSDR (2007). Toxicological profile for lead. Agency for Toxic Substances and Disease Registry.

  • Bahena-Manjarrez, J. L., Rosales-Hoz, L., & Carranza-Edwards, A. (2002). Spatial and temporal variation of heavy metals in a tropical estuary. Environmental Geology, 42, 575–582.

    Article  CAS  Google Scholar 

  • Barni, S., Boncompagni, E., Grosso, A., Bertone, V., Freitas, I., Fasola, M., et al. (2007). Evaluation of Rana snk esculenta blood cell response to chemical stressors in the environment during the larval and adult phases. Aquatic Toxicology, 81, 45–54.

    Article  CAS  Google Scholar 

  • Berlin, A., & Schaller, K. H. (1974). European standardized method for the determination of delta-aminolevulinic acid dehydratase activity in blood. Zeitschrift für Klinische Chemie und Klinische Biochemie, 12, 389–390.

    CAS  Google Scholar 

  • Bernanke, J., & Köhler, H. R. (2009). The impact of environmental chemicals on wildlife vertebrates. Reviews of Environmental Contamination and Toxicology, 198, 1–47.

    Article  CAS  Google Scholar 

  • Brauner, C. J., & Wang, T. (1997). The optimal oxygen equilibrium curve: a comparison between environmental hypoxia and anemia. American Zoologist, 37, 101–108.

    Google Scholar 

  • Buekers, J., Redeker, E. S., & Smolders, E. (2009). Lead toxicity to wildlife: derivation of a critical blood concentration for wildlife monitoring based on literature data. The Science of the Total Environment, 407, 3431–3438.

    Article  CAS  Google Scholar 

  • Burger, J. (2006). Bioindicators: types, development, and use in ecological assessment and research. Environmental Bioindicators, 1, 22–39.

    Article  Google Scholar 

  • Cazenave, J., Wunderlin, D. A., Hued, A. C., & Bistoni, M. A. (2005). Haematological parameters in a neotropical fish, Corydoras paleatus (Jenyns,1842) (Pisces, Callichthyidae), captured from pristine and polluted water. Hydrobiologia, 537, 25–33.

    Article  Google Scholar 

  • Chapman, L. J., & McKenzie, D. J. (2009). Behavioral responses and ecological consequences. In J. G. Richards, A. P. Farrell, & C. J. Brauner (Eds.), Fish physiology: hypoxia (pp. 25–77). New York: Academic.

    Google Scholar 

  • Collins, J. P., & Storfer, A. (2003). Global amphibian declines: sorting the hypotheses. Diversity and Distributions, 9, 89–98.

    Article  Google Scholar 

  • Dohm, M. R., Mautz, W. J., Doratt, R. E., & Stevens, J. R. (2008). Ozone exposure affects feeding and locomotor behavior of adult Bufo marinus. Environmental Toxicology and Chemistry, 27, 1209–1216.

    Article  CAS  Google Scholar 

  • Espinosa-Reyes, G., Ilizaliturri, C. A., González-Mille, D. J., Costilla, R., Díaz-Barriga, F., Cuevas, M. C., et al. (2010). DNA damage in earthworms (Eisenia spp.) as an indicator of environmental stress in the industrial zone of Coatzacoalcos, Veracruz, Mexico. Journal of Environmental Science and Health Part A, 45, 49–55.

    CAS  Google Scholar 

  • Feder, M. E., & Burggren, W. W. (1992). Environmental physiology of the amphibians. Chicago: Chicago Press. University of Chicago.

    Google Scholar 

  • Flores, J., & Albert, L. A. (2004). Environmental lead in Mexico, 1990–2002. Reviews of Environmental Contamination and Toxicology, 181, 37–109.

    Article  CAS  Google Scholar 

  • Folmar, L. C. (1993). Effects of chemical contaminants on blood chemistry of teleost fish: a bibliography and synopsis of selected effects. Environmental Toxicology and Chemistry, 12, 337–375.

    Article  CAS  Google Scholar 

  • Fossi, M. C. (1994). Nondestructive biomarkers in ecotoxicology. Environmental Health Perspectives, 102, 49–54.

    Article  Google Scholar 

  • Fossi, M. C., & Marsili, L. (1997). The use of non-destructive biomarkers in the study of marine mammals. Biomarkers, 2, 205–216.

    Article  CAS  Google Scholar 

  • Gans, C., & Gorniak, G. C. (1982). Functional morphology of lingual protrusion in marine toads (Bufo marinus). The American Journal of Anatomy, 163, 195–222.

    Article  CAS  Google Scholar 

  • Gloag, D. (1981). Sources of lead pollution. British Medical Journal (Clinical Research Ed), 282, 41–44.

    Article  CAS  Google Scholar 

  • Gómez-Ramírez, P., Martínez-López, E., María-Mojica, P., Leó-Ortega, M., & García-Fernández, A. J. (2011). Blood lead levels and δ-ALAD inhibition in nestlings of Eurasian eagle owl (Bubo bubo) to assess lead exposure associated to an abandoned mining area. Ecotoxicology, 20, 131–138.

    Article  Google Scholar 

  • Gonzalez-Mille, D. J., Ilizaliturri-Hernández, C. A., Espinosa-Reyes, G., Costilla-Salazar, R., Díaz-Barriga, F., Ize-Lema, I., et al. (2010). Exposure to persistent organic pollutants (POPs) and DNA damage as an indicator of environmental stress in fish of different feeding habits of Coatzacoalcos, Veracruz, Mexico. Ecotoxicology, 19, 1238–1248.

    Article  CAS  Google Scholar 

  • Hall, F. G. (1966). Hemoglobin functions in the blood of Bufo marinus. Journal of Cellular Physiology, 68, 69–73.

    Article  CAS  Google Scholar 

  • Hopkins, W. (2006). Use of tissue residues in reptile ecotoxicology: a call for integration and experimentalism. In S. Gardner & E. Oberdorster (Eds.), Toxicology of reptiles (pp. 35–62). Boca Raton: CRC Press. Taylor and Francis Group.

    Google Scholar 

  • Kabata-Pendias, A. (2007). Trace elements in soils and plants (3rd ed.). Boca Raton: CRC Press.

    Google Scholar 

  • Lee, Y. H., & Stuebing, R. B. (1990). Heavy metal contamination in the river toad, Bufo juxtasper (Inger), near a copper mine in East Malaysia. Bulletin of Environmental Contamination and Toxicology, 45, 272–279.

    Article  CAS  Google Scholar 

  • Linder, G. L., Krest, S. K., & Sparling, D. W. (2003). Amphibian decline: an integrated analysis of multiple stressor effects. Pensacola: Society of Environmental Toxicology and Chemistry (SETAC).

    Google Scholar 

  • Linzey, D., Burroughs, J., Hudson, L., Marini, M., Robertson, J., Bacon, J., et al. (2003). Role of environmental pollutants on immune functions, parasitic infections and limb malformations in marine toads and whistling frogs from Bermuda. International Journal of Environmental Health Research, 13, 125–148.

    Article  CAS  Google Scholar 

  • Martinez-Haro, M., Green, A. J., & Mateo, R. (2011). Effects of lead exposure on oxidative stress biomarkers and plasma biochemistry in waterbirds in the field. Environmental Research, 111, 530–538.

    Article  CAS  Google Scholar 

  • Martínez-López, E., Sousa, A. R., María-Mojica, P., Gómez-Ramírez, P., Guilhermino, L., & García-Fernández, A. J. (2010). Blood δ-ALAD, lead and cadmium concentrations in spur-thighed tortoises (Testudo graeca) from Southeastern Spain and Northern Africa. Ecotoxicology, 19, 670–677.

    Article  Google Scholar 

  • McCoy, K. A., Bortnick, L. J., Campbell, C. M., Hamlin, H. J., Guillette, L. J., & St Mary, C. M. (2008). Agriculture alters gonadal form and function in the toad Bufo marinus. Environmental Health Perspectives, 116, 1526–1532.

    Article  Google Scholar 

  • Pelallo-Martínez, N. A., Ilizaliturri-Hernández, C. A., Espinosa-Reyes, G., Carrizales-Yáñez, L., & González-Mille, D. J. (2011). Assessment of exposure to lead in humans and turtles living in an industrial site in Coatzacoalcos Veracruz, Mexico. Bulletin of Environmental Contamination and Toxicology, 86, 642–645.

    Article  Google Scholar 

  • PEMEX. (1999). La primera refinería de Latinoamérica Refinería Gral. Lázaro Cárdenas. Revista octanaje. Petróleos Mexicanos (PEMEX). Available from http://www.ref.pemex.com/octanaje/23laza.htm. Accessed 3 June 2012.

  • Pérez-Coll, C. S., Herkovits, J., & Salibián, A. (1988). Embryotoxicity of lead on Bufo arenarum. Bulletin of Environmental Contamination and Toxicology, 41, 247–252.

    Article  Google Scholar 

  • Perí, S. I., Arrieta, M. A., Fink, N. E., & Salibián, A. (1998). Delta-aminolevulinic acid dehydratase (ALAD) activity in blood of Bufo arenarum (Anura). Biological Research, 31, 339–342.

    Google Scholar 

  • Perí, S. I., Fink, N. E., & Salibián, A. (1998). Hematological parameters in Bufo arenarum injected with sublethal dose of lead acetate. Biomedical and Environmental Sciences, 11, 70–74.

    Google Scholar 

  • Pizzatto, L., & Shine, R. (2008). The behavioral ecology of cannibalism in cane toads (Bufo marinus). Behavioral Ecology and Sociobiology, 63, 123–133.

    Article  Google Scholar 

  • Pörtner, H. O., MacLatchy, L. M., & Toews, D. P. (1991). Metabolic responses of the toad Bufo marinus to environmental hypoxia: an analysis of the critical PO2. Physiological Zoology, 64, 836–849.

    Google Scholar 

  • Rice, T. M., Blackstone, B. J., Nixdorf, W. L., & Taylor, D. H. (1999). Exposure to lead induces hypoxia-like responses in bullfrog larvae (Rana catesbeiana). Environmental Toxicology and Chemistry, 18, 2283–2288.

    CAS  Google Scholar 

  • Rosales-Hoz, L., & Carranza-Edwards, A. (1998). Heavy metals in sediments from Coatzacoalcos River, Mexico. Bulletin of Environmental Contamination and Toxicology, 60, 553–561.

    Article  CAS  Google Scholar 

  • Rosales-Hoz, L., & Carranza-Edwards, A. (2005). Estudio geoquímico de metales en el estuario del Río Coatzacoalcos. In: V. A. Botello, J. Rendón-Von Osten, G. Gold-Bouchot, C. Agraz-Hernández (Eds.) Golfo de México contaminación e impacto ambiental: diagnostico y tendencias (pp. 389–406). Universidad Autónoma de Campeche, Universidad Autónoma de México, Instituto de Ecología.

  • Rosales-Hoz, L., Cundy, A. B., & Bahena-Manjarrez, J. L. (2003). Heavy metals in sediment cores from a tropical estuary affected by anthropogenic discharges: Coatzacoalcos estuary, Mexico. Estuarine, Coastal and Shelf Science, 58, 117–126.

    Article  CAS  Google Scholar 

  • Rosenberg, C. E., Perí, S. I., Arrieta, M. A., Fink, N. E., & Salibián, A. (1998). Red blood cell osmotic fragility in Bufo arenarum exposed to lead. Archives of Physiology and Biochemistry, 106, 19–24.

    Article  CAS  Google Scholar 

  • Rowe, C. L., Hopkins, W. A., & Coffman, V. R. (2001). Failed recruitment of southern toads (Bufo terrestris) in a trace element-contaminated breeding habitat: direct and indirect effects that may lead to a local population sink. Archives of Environmental Contamination and Toxicology, 40, 399–405.

    Article  CAS  Google Scholar 

  • Ruelas-Inzunza, J., Gárate-Viera, Y., & Páez-Osuna, F. (2007). Lead in clams and fish of dietary importance from Coatzacoalcos estuary (Gulf of Mexico), an industrialized tropical region. Bulletin of Environmental Contamination and Toxicology, 79, 508–513.

    Article  CAS  Google Scholar 

  • Ruelas-Inzunza, J., Páez-Osuna, F., Zamora-Arellano, N., Amezcua-Martínez, F., & Bojórquez-Leyva, H. (2009). Mercury in biota and surficial sediments from Coatzacoalcos estuary, Gulf of Mexico: distribution and seasonal variation. Water, Air, and Soil Pollution, 197, 165–174.

    Article  CAS  Google Scholar 

  • Sparling, D. W., Linder, G., & Bishop, C. A. (2010). Ecotoxicology of amphibians and reptiles (2nd ed.). Pensacola: Society of Environmental Toxicology and Chemistry (SETAC).

    Book  Google Scholar 

  • StatSoft. (2007). STATISTICA (data analysis software system), version 8.0. Tulsa, OK: Statsoft.

  • Stevenson, R. D., & Woods, W. A. (2006). Condition indices for conservation: new uses for evolving tools. Integrative and Comparative Biology, 46, 1169–1190.

    Article  CAS  Google Scholar 

  • Strickler-Shaw, S., & Taylor, D. H. (1991). Lead inhibits acquisition and retention learning in bullfrog tadpoles. Neurotoxicology and Teratology, 13, 167–173.

    Article  CAS  Google Scholar 

  • Stringer, R., Labunska, I., Brigden, K. (2001). Organochlorine and heavy metal contaminants in the environment around the complejo petroquimicos Paharitos, Coatzacoalcos, Mexico (Technique Note). United Kingdom: University of Exeter, Greenpeace Research Laboratories.

  • Subramanian, K. S. (1989). Determination of lead in blood by graphite furnace atomic absorption spectrometry—a critique. The Science of the Total Environment, 89, 237–250.

    Article  CAS  Google Scholar 

  • Te-Hao, C., Gross, J. A., & Karasov, W. H. (2006). Sublethal effects of lead on northern leopard frog (Rana pipiens) tadpoles. Environmental Toxicology and Chemistry, 25, 1383–1389.

    Article  Google Scholar 

  • Trejo-Acevedo, A., Díaz-Barriga, F., Carrizales, L., Domínguez, G., Costilla, R., Ize-Lema, I., et al. (2009). Exposure assessment of persistent organic pollutants and metals in Mexican children. Chemosphere, 74, 974–980.

    Article  CAS  Google Scholar 

  • Triebskorn, R., Böhmer, J., Braunbeck, T., Honnen, W., Köhler, H. R., Lehmann, R., et al. (2001). The project VALIMAR (VALIdation of bioMARkers for the assessment of small stream pollution): objectives, experimental design, summary of results, and recommendations for the application of biomarkers in risk assessment. Journal of Aquatic Ecosystem Stress and Recovery, 8, 161–178 (formerly Journal of Aquatic Ecosystem Health).

    Article  CAS  Google Scholar 

  • Venturino, A., Rosenbaum, E., De Castro, A. C., Anguiano, O. L., Gauna, L., De Schroeder, T. F., et al. (2003). Biomarkers of effect in toads and frogs. Biomarkers, 8, 167–186.

    Article  CAS  Google Scholar 

  • Wang, M. Z., & Jia, X. Y. (2009). Low levels of lead exposure induce oxidative damage and DNA damage in the testes of the frog Rana nigromaculata. Ecotoxicology, 18, 94–99.

    Article  Google Scholar 

  • Wood, S. C. (1990). Effect of hematocrit on behavioral thermoregulation of the toad Bufo marinus. The American Journal of Physiology, 258, 848–851.

    Google Scholar 

  • Wood, S. C. (1991). Interactions between hypoxia and hypothermia. Annual Review of Physiology, 53, 71–85.

    Article  CAS  Google Scholar 

  • Wood, S. C., & Gonzales, R. (1996). Hypothermia in hypoxic animals: mechanisms, mediators, and functional significance. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology, 113, 37–43.

    Article  CAS  Google Scholar 

  • Wood, S., & Malvin, G. (1991). Physiological significance of behavioral hypothermia in hypoxic toads (Bufo marinus). The Journal of Experimental Biology, 159, 203–215.

    CAS  Google Scholar 

  • Zhang, Y., Huang, D., Zhao, D., Long, J., Song, G., & An’na, L. (2007). Long-term toxicity effects of cadmium and lead on Bufo raddei tadpoles. Bulletin of Environmental Contamination and Toxicology, 79, 178–183.

    Article  CAS  Google Scholar 

  • Zug, G. R., & Zug, P. B. (1979). The marine toad, Bufo marinus: a natural history resumé of native populations. Washington: Smithsonian Institution Press.

    Google Scholar 

  • Zupanovic, Z., Musso, C., Lopez, G., Louriero, C. L., Hyatt, A. D., Hengstberger, S., et al. (1998). Isolation and characterization of iridoviruses from the giant toad Bufo marinus in Venezuela. Diseases of Aquatic Organisms, 33, 1–9.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from the Dirección General de Investigación sobre la Contaminación Urbana y Regional del Instituto Nacional de Ecología [No. de convenio INE/A1-047/2007], SEMARNAT, and El Colegio de la Frontera Sur [No. de Fondo FORDECyT-143303]. Special thanks to Prof. J. Jesus Guerrero Cabrera from language center of San Luis Potosí Autonomous University and Biol. Susan Quackenbush for English language editing of the manuscript.

Author information

Authors and Affiliations

  1. Departamento Toxicología Ambiental, Facultad de Medicina, Universidad Autónoma de San Luis Potosí, Avenida Venustiano Carranza 2405, CP 78210, San Luis Potosí, SLP, México

    César Arturo Ilizaliturri-Hernández, Donaji Josefina González-Mille, Jesús Mejía-Saavedra, Guillermo Espinosa-Reyes & Iván Pérez-Maldonado

  2. El Colegio de la Frontera Sur (ECOSUR), Unidad San Cristóbal, Carretera Panamericana y Periférico Sur s/n, CP 29290, San Cristobal de Las Casas, Chiapas, México

    Arturo Torres-Dosal

Authors
  1. César Arturo Ilizaliturri-Hernández
    View author publications

    Search author on:PubMed Google Scholar

  2. Donaji Josefina González-Mille
    View author publications

    Search author on:PubMed Google Scholar

  3. Jesús Mejía-Saavedra
    View author publications

    Search author on:PubMed Google Scholar

  4. Guillermo Espinosa-Reyes
    View author publications

    Search author on:PubMed Google Scholar

  5. Arturo Torres-Dosal
    View author publications

    Search author on:PubMed Google Scholar

  6. Iván Pérez-Maldonado
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to César Arturo Ilizaliturri-Hernández.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ilizaliturri-Hernández, C.A., González-Mille, D.J., Mejía-Saavedra, J. et al. Blood lead levels, δ-ALAD inhibition, and hemoglobin content in blood of giant toad (Rhinella marina) to asses lead exposure in three areas surrounding an industrial complex in Coatzacoalcos, Veracruz, Mexico. Environ Monit Assess 185, 1685–1698 (2013). https://doi.org/10.1007/s10661-012-2660-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10661-012-2660-7

Keywords

Profiles

  1. César Arturo Ilizaliturri-Hernández View author profile
  2. Guillermo Espinosa-Reyes View author profile