Biomarkers of PAHs exposure in crabs Ucides cordatus: Laboratory assay and field study
Abstract
Pyrene metabolites in urine and micronucleus in haemocytes of crabs (Ucides cordatus) were tested as biomarkers of exposure to oil derived PAHs in mangrove sediments. The goal was to verify how well pyrene metabolites in urine represent levels of oil contamination in mangroves and whether the micronuclei assay indicates exposure. For this, bioassays were performed using crabs from clean and contaminated areas, and field studies were conducted in four mangroves. Results of the bioassay show that U. cordatus assimilates, metabolises, and excretes pyrene in urine as pyrene-1-glucoside, pyrene-sulphate and pyrene-conjugate. OH-pyrene-sulphate was the major metabolite produced/excreted over 120 h of observation by crabs from the clean mangrove. The production/excretion of pyrene-1-glucoside in this case increased linearly with time at a rate of 2.3 x 10(-10)mol L(-1)day(-1). The number of micronuclei in haemocytes also increased with the time after pyrene inoculation, indicating that exposure to pyrene triggers genotoxic and mutagenic response. In crabs from a heavily oil-contaminated mangrove pyrene-1-glucoside was the major metabolite, an indication that production/excretion of a certain metabolite varies depending on adaptation of the animal to the environment. A highly significant correlation was found between the concentration of pyrene metabolites in urine of field crabs expressed as OH-pyrene equivalents and the sum of 38 PAHs determined in hepatopancreas/sediments (r=0.825, n=23, p<0.05). The response of these crabs to the micronuclei assay was not significantly related to concentration of individual or total PAHs. Nevertheless, metabolite results prove U. cordatus as excellent bioindicator for evaluating environmental quality in mangrove areas as related to PAHs and oil contamination.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Pyrene is associated with increased heart rate, genotoxicity, and altered agonistic interactions in crabs.
“Pyrene has been associated with increased heart rate [72], genotoxicity [73], and altered agonistic interactions in crabs [74].”
From Wildfire Ash Alters Freshwater Crustacean Behavior: Disentangling the Contributions of Suspended Macroparticles and Ash‐Induced Alkalinization (2026) · cites this paper as [73]
Cites
Environmental Chemistry of Soils
McBride, M. B. (1994) · Medical Entomology and Zoology · Cited by 5,871 · see citing works
Countryman, P. I., & Heddle, J. A. (1976) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/0027-5107(76)90105-6 · Cited by 815 · see citing works
Wang, Z., Fingas, M. F., & Page, D. S. (1999) · Journal of Chromatography A · doi:10.1016/s0021-9673(99)00120-x · Cited by 653 · see citing works
Manahan, S. E. (1999) · CRC Press eBooks · doi:10.1201/9780367803247 · Cited by 553 · see citing works
Dailianis, S., Domouhtsidou, G. P., Raftopoulou, E. K., Kaloyianni, M. G., & Dimitriadis, V. K. (2003) · Marine Environmental Research · doi:10.1016/s0141-1136(03)00005-9 · Cited by 185 · see citing works
Aas, E., Beyer, J., & Goksøyr, A. (2000) · Biomarkers · doi:10.1080/135475000230505 · Cited by 183 · see citing works
Beyer, J., Sandvik, M., Hylland, K., Fjeld, E., Egaas, E., Aas, E., Skåre, J. U., & Goksøyr, A. (1996) · Aquatic Toxicology · doi:10.1016/s0166-445x(96)00798-9 · Cited by 170 · see citing works
PAH in fish bile detected by fixed wavelength fluorescence
Aas, E., Beyer, J., & Goksøyr, A. (1998) · Marine Environmental Research · doi:10.1016/s0141-1136(97)00034-2 · Cited by 102 · see citing works
Scarpato, R., Migliore, L., Cognetti-Alfinito, G., & Barale, R. (1990) · Marine Pollution Bulletin · doi:10.1016/0025-326x(90)90191-a · Cited by 93 · see citing works
The micronucleus assay in Crassostrea gigas for the detection of seawater genotoxicity
Burgeot, T., His, E., & Galgani, F. (1995) · Mutation Research/Genetic Toxicology · doi:10.1016/0165-1218(95)90022-5 · Cited by 88 · see citing works
Lin, E. L. C., Cormier, S. M., & Racine, R. N. (1994) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5620130504 · Cited by 88 · see citing works
Escartı́n, E., & Porte, C. (1999) · Marine Pollution Bulletin · doi:10.1016/s0025-326x(99)00162-9 · Cited by 87 · see citing works
Biomarker responses in flounder (Platichthys flesus) and their use in pollution monitoring
Goksøyr, A., Beyer, J., Egaas, E., Grøsvik, B. E., Hylland, K., Sandvik, M., & Skaare, J. U. (1996) · Marine Pollution Bulletin · doi:10.1016/s0025-326x(96)00131-2 · Cited by 79 · see citing works
Farias, C. D. O., Hamacher, C., Wagener, Â. D. L. R., & Scofield, A. D. L. (2008) · Organic Geochemistry · doi:10.1016/j.orggeochem.2007.12.008 · Cited by 76 · see citing works
Self-citationSites of release of Putative Sex Pheromone and Sexual Behaviour in Female (Crustacea: Decapoda)
Bamber, S., & Naylor, E. (1997) · Estuarine Coastal and Shelf Science · doi:10.1006/ecss.1996.0211 · Cited by 60 · see citing works
Stroomberg, G. J., de Knecht, J. A., Ariese, F., van Gestel, C. A. M., & Velthorst, N. H. (1999) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5620181014 · Cited by 58 · see citing works
Fossi, M. C., Casini, S., Savelli, C., Corbelli, C., Franchi, E., Matteï, N., Sanchez-Hernandez, J. C., Corsi, I., Bamber, S., & Depledge, M. H. (2000) · Chemosphere · doi:10.1016/s0045-6535(99)00300-8 · Cited by 56 · see citing works
Sublethal responses in caged organisms exposed to sediments affected by oil spills.
Morales-Caselles, C., Martín-Díaz, M. L., Riba, I., Sarasquete, C., & DelValls, T. (2008) · Chemosphere · doi:10.1016/j.chemosphere.2008.02.060 · Cited by 55 · see citing works
Krahn, M. M., Ylitalo, G. M., Buzitis, J., Bolton, J. L., Wigren, C. A., Chan, S.-L., & Varanasi, U. (1993) · Marine Pollution Bulletin · doi:10.1016/0025-326x(93)90035-i · Cited by 53 · see citing works
Watson, G., Andersen, O., Galloway, T. S., & Depledge, M. H. (2004) · Aquatic Toxicology · doi:10.1016/j.aquatox.2003.11.006 · Cited by 47 · see citing works
Dissanayake, A., & Galloway, T. S. (2004) · Marine Environmental Research · doi:10.1016/j.marenvres.2004.03.072 · Cited by 46 · see citing works
Nudi, A. H., Wagener, Â. D. L. R., Francioni, E., Scofield, A. D. L., SETTE, C. B., & Veiga, A. (2006) · Environment International · doi:10.1016/j.envint.2006.11.001 · Cited by 44 · see citing works
Self-citationDissanayake, A., Galloway, T. S., & Jones, M. B. (2008) · Marine Environmental Research · doi:10.1016/j.marenvres.2008.07.006 · Cited by 43 · see citing works
Biomonitoring of Polycyclic Aromatic Hydrocarbon inPerna pernafrom Guanabara Bay, Brazil
Francioni, E., Wagener, Â. D. L. R., Scofield, A. L., & Cavalier, B. (2005) · Environmental Forensics · doi:10.1080/15275920500351759 · Cited by 42 · see citing works
Self-citationUrinary PAH Metabolites as Biomarkers of Exposure in Aquatic Environments
Fillmann, G., Watson, G., Howsam, M., Francioni, E., Depledge, M. H., & Readman, J. W. (2004) · Environmental Science & Technology · doi:10.1021/es0350839 · Cited by 38 · see citing works
Self-citationHattori, G. Y., & Pinheiro, M. A. A. (2003) · Revista Brasileira de Zoologia · doi:10.1590/s0101-81752003000200022 · Cited by 37 · see citing works
Violante, F. S., Sanguinetti, G., Barbieri, A., Accorsi, A., Mattioli, S., Cesari, R., Fimognari, C., & Hrelia, P. (2003) · Environmental Research · doi:10.1016/s0013-9351(02)00060-9 · Cited by 29 · see citing works
Formation of pyrene metabolites by the terrestrial isopod Porcellio scaber
Stroomberg, G. J., Reuther, C., Kozin, I. S., Brummelen, T. C. V., van Gestel, C. A. M., Gooijer, C., & Cofino, W. P. (1996) · Chemosphere · doi:10.1016/0045-6535(96)00316-5 · Cited by 24 · see citing works
Eickhoff, C. V., Gobas, F. A. P. C., & Law, F. C. P. (2003) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5620220108 · Cited by 20 · see citing works
VIJAYAVEL, K., & Balasubramanian, M. (2007) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2007.01.011 · Cited by 17 · see citing works
Koenig, S., Savage, C., & Kim, J. P. (2008) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2008.08.010 · Cited by 14 · see citing works
Krone, C. A., Stein, J. E., & Varanasi, U. (1992) · Chemosphere · doi:10.1016/0045-6535(92)90424-p · Cited by 10 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Bayen, S. (2012) · Environment International · doi:10.1016/j.envint.2012.07.008 · Cited by 429 · see citing works
Nemr, A. E., Moneer, A. A., Ragab, S., & Sikaily, A. E. (2016) · The Egyptian Journal of Aquatic Research · doi:10.1016/j.ejar.2016.05.003 · Cited by 68 · see citing works
Duarte, L. F. D. A., de Souza, C. A., Nobre, C. R., Pereira, C. D. S., & Pinheiro, M. A. A. (2016) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2016.07.018 · Cited by 65 · see citing works
Pinheiro, M. A. A., Duarte, L. F. D. A., Toledo, T. R., Adam, M. L., & Torres, R. A. (2013) · Environmental Monitoring and Assessment · doi:10.1007/s10661-013-3172-9 · Cited by 63 · see citing works
Marine protected areas in Latin America and Caribbean threatened by polycyclic aromatic hydrocarbons
Nunes, B. Z., Zanardi‐Lamardo, E., Choueri, R. B., & Castro, Í. B. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.116194 · Cited by 60 · see citing works
Marine sponges as bioindicators of oil and combustion derived PAH in coastal waters
Batista, D., Tellini, K., Nudi, A. H., Massone, T. P., Scofield, A. D. L., & Wagener, Â. D. L. R. (2013) · Marine Environmental Research · doi:10.1016/j.marenvres.2013.09.022 · Cited by 47 · see citing works
Self-citationNeta, R. N. F. C., Andrade, T. D. S. D. O. M., de Oliveira, S. R. S., Torres, A. R., Cardoso, W. D. S., Santos, D. M. S., de Jesus, W. B., Serra, I. M. R. D. S., & Brito, N. M. (2019) · Environmental Science and Pollution Research · doi:10.1007/s11356-019-04849-0 · Cited by 29 · see citing works
Formation and identification of PAHs metabolites in marine organisms
SETTE, C. B., Pedrete, T. D. A., Feitosa-Felizzola, J., Nudi, A. H., Scofield, A. D. L., & Wagener, Â. D. L. R. (2013) · Marine Environmental Research · doi:10.1016/j.marenvres.2013.02.004 · Cited by 27 · see citing works
Self-citationOccurrence of Sexual Hormones in Sediments of Mangrove in Brazil
Froehner, S., Machado, K. S., Stefen, E., & Nolasco, M. A. (2011) · Water Air & Soil Pollution · doi:10.1007/s11270-010-0732-2 · Cited by 24 · see citing works
Mello, L. C., Costa, A. B., Moraes, A. S. B., Lima, A. D. F., dos Santos, R. P., da Silva, V. A., Abessa, D. M. D. S., & Cavalcante, R. M. (2024) · Journal of Environmental Management · doi:10.1016/j.jenvman.2024.121991 · Cited by 13 · see citing works
Aigberua, A. O., Izah, S. C., & Aigberua, A. A. (2023) · Environmental Monitoring and Assessment · doi:10.1007/s10661-023-10970-y · Cited by 12 · see citing works
Falcão, C. B. R., Pinheiro, M. A. A., Torres, R. A., & Adam, M. L. (2020) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2020.111232 · Cited by 11 · see citing works
Pinheiro, M. A. A., Kriegler, N., de Souza, C. A., & Duarte, L. F. D. A. (2021) · Wetlands · doi:10.1007/s13157-021-01427-4 · Cited by 11 · see citing works
Gladston, R. C., Lima, A. D. F., & Cavalcante, R. M. (2024) · Marine Pollution Bulletin · doi:10.1016/j.marpolbul.2024.117443 · Cited by 10 · see citing works
Andrade‐Rivas, F., Afshari, R., Yassi, A., Mardani, A., Taft, S., Guttmann, M., Rao, A. S., Thomas, S. E., Takaro, T. K., & Spiegel, J. (2021) · Environmental Research · doi:10.1016/j.envres.2021.112575 · Cited by 10 · see citing works
Armstrong, E. K., Mondon, J. A., Miller, A. D., Revill, A. T., Stephenson, S. A., Tan, M. H., Greenfield, P. A., Tromp, J. J., Corbett, P. A., & Hook, S. E. (2022) · Environmental Toxicology and Chemistry · doi:10.1002/etc.5413 · Cited by 9 · see citing works
Oil spill effects in biota and traditional populations from protected areas of Brazil’s Northeast
Mello, L. C., Cavalcante, R. M., Bastos, L. M., Nossol, A. B. D. S., Martins, M. M., Cesar‐Ribeiro, C., Pauly, G. D. F. E., & Abessa, D. M. D. S. (2025) · Human and Ecological Risk Assessment An International Journal · doi:10.1080/10807039.2025.2467336 · Cited by 7 · see citing works
Caliani, I., Stefano Cannicci, A., Pretti, C., Baratti, M., Contini, G., Vitale, M., Casini, S., Fossi, M. C., Iannucci, A., & Fratini, S. (2022) · Chemosphere · doi:10.1016/j.chemosphere.2022.137129 · Cited by 6 · see citing works
Ramos, M. A. V., Rocha, S. S., Winkaler, E. U., Nóbrega, G. N., Carvalho, J. D. C., Santos, A. Z. D. S., & Otero, X. L. (2024) · Water Air & Soil Pollution · doi:10.1007/s11270-024-07037-0 · Cited by 5 · see citing works
Vasco-Viteri, S., Cabrera, M., Pérez‐González, A., Hauser‐Davis, R. A., MOULATLET, G. M., & Capparelli, M. V. (2023) · Chemosphere · doi:10.1016/j.chemosphere.2023.139157 · Cited by 5 · see citing works
Velho, A. M. A., Aiub, C. A. F., Mazzei, J. L., Corrêa, S. M., Soares, M. L. G., & Felzenszwalb, I. (2012) · Journal of Environmental Protection · doi:10.4236/jep.2012.38087 · Cited by 4 · see citing works
Lima, A. D. F., C., G., Santos, M. C. M., Bezerra, L. E. A., & Cavalcante, R. M. (2025) · Chemosphere · doi:10.1016/j.chemosphere.2025.144729 · Cited by 3 · see citing works
Ihunwo, O. C., & Ibezim-Ezeani, M. U. (2021) · Turkish Journal of Fisheries and Aquatic Sciences · doi:10.4194/1303-27142-v21_05_04 · Cited by 3 · see citing works
Toutou, M. M. M. (2022) · Egyptian Journal of Aquatic Biology and Fisheries · doi:10.21608/ejabf.2022.246874 · Cited by 2 · see citing works
Mota, T. A., Winkaler, E. U., de Oliveira, G. H., & Rocha, S. S. (2021) · Research Society and Development · doi:10.33448/rsd-v10i6.15638 · Cited by 2 · see citing works
Pham, K., Cock, A. D., Ho, L. T., Domínguez‐Granda, L., Berghe, W. V., Spanoghe, P., & Goethals, P. L. M. (2025) · Environmental Pollution · doi:10.1016/j.envpol.2025.127355 · Cited by 1 · see citing works
Freitas-Silva, I., Santana, J. D. L., Alves, V. D., Yogui, G. T., Zanardi‐Lamardo, E., Pereira, C. F., & Souza-Filho, J. F. (2026) · Environmental Pollution · doi:10.1016/j.envpol.2026.128260 · Cited by 1 · see citing works
Sánchez, F. J. R., Santos, M. A. A., Viana, T. D. S., & Figueiredo, J. A. G. (2024) · Caderno Pedagógico · doi:10.54033/cadpedv21n6-128 · Cited by 1 · see citing works
Pereira‐Silva, P. B., Pacheco, D. R., Kirsch, G., Araujo, R. M. G., Oscar, B. V. C., Matias, W. G., Santos, S., & Figueiredo, B. R. S. (2026) · Environmental Toxicology · doi:10.1002/tox.70178
Barka, S., Ouanes, Z., Krifa, M., Kilani, S., Ghédira, L. C., & Hamza‐Chaffai, A. (2017) · doi:10.5150/cmcm.2017.016
Contaminantes en aves marinas de Sudamérica, una revisión sistemática
Romero, M. B., Boudet, L. C., Gerpe, M., & Polizzi, P. (2024) · El Hornero · doi:10.56178/eh.v39i2.1487
Protazio, G. D. S., Ribeiro, E. B., de Oliveira, S. R. S., de Jesus, W. B., & Neta, R. N. F. C. (2025) · doi:10.29327/5539040.3-7
Oliveira, L. B., Moreno, L. C. G. E. A. I., de Oliveira, S. R. S., Benjamin, L. D. A., Sousa, D. B. P., Protazio, G. D. S., de Sousa, A. L., de Andrade, T. P., Ribeiro, E. B., Castro, J. D. S., et al. (2026) · Environmental Monitoring and Assessment · doi:10.1007/s10661-026-16077-4
- Authors
- Nudi, A. H., Wagener, A. D. L. R., Francioni, E., Sette, C. B., Sartori, A. V., & Scofield, A. D. L.
- Affiliations
- Pontifícia Universidade Católica do Rio de Janeiro (BR)
- Escola Nacional de Saúde Pública Sergio Arouca (BR)
- Venue
- Environmental Research
- Publisher
- Elsevier BV
- Published
- 2010-02
- Volume
- 110
- Issue
- 2
- Pages
- 137-145
- ISSN
- 0013-9351 (ISSN-L)
- OpenAlex
- W1985578720
- Cited by
- 35
- References
- 32
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 5 · 2023: 2 · 2022: 3 · 2021: 4 · 2020: 2 · 2019: 1 · 2018: 1 · 2017: 1 · 2016: 2 · 2015: 1 · 2013: 3 · 2012: 2
- FWCI
- 1.46
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Environmental Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
- Topics
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Environmental Toxicology and Ecotoxicology
- Physical Sciences › Environmental Science › Health, Toxicology and Mutagenesis › Toxic Organic Pollutants Impact
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Carcinogens and Genotoxicity Assessment
- Keywords
- polycyclic aromatic hydrocarbons, pyrene, Ucides cordatus, genotoxicity, oil pollution, mangrove sediments, bioindicators
- MeSH terms
- Animals, Brazil, Brachyura, Glucuronates, Male, Microscopy, Fluorescence, Polycyclic Aromatic Hydrocarbons, Pyrenes, Water Pollutants, Chemical, Micronucleus Tests, Biomarkers, Statistics, Nonparametric, Geologic Sediments, Avicennia, Ecotoxicology
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
