Environmental Science and Pollution Research

, Volume 26, Issue 16, pp 15884–15893 | Cite as

Biochemical and morphological responses in Ucides cordatus (Crustacea, Decapoda) as indicators of contamination status in mangroves and port areas from northern Brazil

  • Raimunda Nonata Fortes Carvalho NetaEmail author
  • Ticianne de Sousa de Oliveira Mota Andrade
  • Suelen Rosana Sampaio de Oliveira
  • Audalio Rebelo Torres Junior
  • William da Silva Cardoso
  • Débora Martins Silva Santos
  • Wanda dos Santos Batista
  • Ilka Márcia R. de Sousa Serra
  • Natilene Mesquita Brito
Research Article


The aims of this study were to analyze biochemical and morphological responses (glutathione S-transferase activity and branchial lesions) in Ucides cordatus (crabs) and to verify how the species is responding to environmental contamination in a port (potentially contaminated area) and mangrove (reference area; Amazon Coast, Maranhão, Brazil). Adult males were captured bimonthly for a period of 1 year. Higher GST activity (1.03 ± 0.07 μmol min−1 mg protein−1) was observed in crabs in the port when compared with those in the reference area (p < 0.05). The greatest number of branchial lesions (serious alterations) was recorded in crabs only in the port area. The GST activity increased until serious lesions appeared; after this limit, GST activity decreased dramatically to very low levels, thus resulting in irreversible lesions (lamella collapse). The mathematical model based on the two parameters evaluated in U. cordatus showed that the port area experienced substantial contamination impact, while the mangroves (reference area) presented moderate environmental quality.


Environmental monitoring Heavy metals Estuarine environment Biomarker Branchial lesions Glutathione-S-transferase Mathematical model 



The authors thank the staff of the Laboratory of Biomarkers in Aquatic Organisms (LABOAq), the Research Group in Ecotoxicology and Monitoring of Aquatic Environments (GPEMAAq) and Group in Aquatic Biology (BioAqua) for technical support. We also thank the Maranhão State Research Foundation (Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Estado do Maranhão-FAPEMA) for the financial support and the Coordination for the Improvement of Higher Education Personnel (CAPES) for the granting of the master’s degree to the second author. We thank Catherine Dandie, PhD, from Edanz Group ( for editing a draft of this manuscript.


  1. Amado LL, da Rosa CE, Leite AM, Moraes L, Pires WV, Leães Pinho GL, Martins CMG, Robaldo RB, Nery LEM, Monserrat JM (2006) Biomarkers in croakers Micropogonias furnieri (Teleostei: Sciaenidae) from polluted and non-polluted areas from the Patos lagoon estuary (southern Brazil): evidences of genotoxic and immunological effects. Mar Pollut Bull 52:199–206CrossRefGoogle Scholar
  2. Antaq (2018) Agência Nacional de Transportes Aquaviários. Principais portos do Brasil. Accessed 20 Jan 2018
  3. Bayen S (2012) Occurrence, bioavailability and toxic effects of trace metals and organic contaminants in mangrove ecosystems: a review. Environ Int 48:84–101CrossRefGoogle Scholar
  4. Bernet D, Schmidt H, Meier W, Burkhardt-Holm P, Wahli T (1999) Histopathology in fish: proposal for a protocol to assess. J Fish Dis 22:25–34CrossRefGoogle Scholar
  5. Bertrand L, Monferrán MV, Mouneyrac C, Amé MV (2018) Native crustacean species as a bioindicator of freshwater ecosystem pollution: a multivariate and integrative study of multi-biomarker response in active river monitoring. Chemosphere 206:265–277CrossRefGoogle Scholar
  6. Bickham JW, Sandhu S, Hebert PD, Chikhi L, Athwal R (2000) Effects of chemical contaminants on genetic diversity in natural populations: implications for biomonitoring and ecotoxicology. Mutat Res Rev Mutat Res 463:33–51CrossRefGoogle Scholar
  7. Branco JO (1993) Aspectos bioecológicos do caranguejo Ucides cordatus (Linnaeus, 1763) (Crustacea, Decapoda) do manguezal do Itacorubi, Santa Catarina, BR. Arq Biol Tecnol 36:133–148Google Scholar
  8. Buruaem LM, Hortellani MA, Sarkis JE, Costa-Lotufo LV, Abessa DM (2012) Contamination of port zone sediments by metals from large marine ecosystems of Brazil. Mar Pollut Bull 64:479–488CrossRefGoogle Scholar
  9. Camargo MMP, Martinez CBR (2006) Biochemical and physiological biomarkers in Prochilodus lineatus submitted to in situ tests in an urban stream in southern Brazil. Environ Toxicol Pharmacol 21:61–69CrossRefGoogle Scholar
  10. Carvalho-Neta RNF, Abreu-Silva AL (2010) Sciades herzbergii oxidative stress biomarkers: an in situ study of an estuarine ecosystem (São Marcos’ bay, Maranhão, Brazil). Braz J Oceanogr 58:11–17CrossRefGoogle Scholar
  11. Carvalho-Neta RNF, Torres Junior AR, Abreu-Silva AL (2012) Biomarkers in catfish Sciades herzbergii (Teleostei: Ariidae) from polluted and non-polluted areas (São Marcos’ bay, northeastern Brazil). Appl Biochem Biotech 166:1–12CrossRefGoogle Scholar
  12. Carvalho-Neta RNF, Sousa DBP, Almeida ZS, Santos DMS, Tchaicka L (2014) A histopathological and biometric comparison between catfish (Pisces, Ariidae) from a harbor and a protected area. Brazil. Aquat Biosyst 10:1–7CrossRefGoogle Scholar
  13. Carvalho-Neta RNF, Barbosa GL, Torres HS, Pinheiro Sousa DB, Castro JS, santos DMS, Tchaicka L, Almeida ZS, Teixeira EG, Torres Junior AR (2017) Changes in Glutathione S-Transferase Activity and Parental Care Patterns in a Catfish (Pisces, Ariidae) as a Biomarker of Anthropogenic Impact in a Brazilian Harbor. Arch Environ Contam Toxicol 72:132–141Google Scholar
  14. Castro ACL, Correia MMF, Nascimento AR, Piedade-Júnior RN, Gama LRM, Sousa MM, Sousa RCC (2008) Aspectos bioecológicos do caranguejo-uçá (Ucides cordatus cordatus, L. 1763) (Decapoda, Brachyura) nos manguezais da ilha de São Luís e litoral oriental do Estado do Maranhão, Brasil. Amazon Ciên Desenvolv 3:17–36Google Scholar
  15. Castro JS, Franca C, Fernandes J, Silva JS, Teixeira EG, Carvalho-Neta RNF (2018) Biomarcadores histológicos em brânquias de Sciades herzbergii (Siluriformes, Ariidae) capturados no Complexo Estuarino de São Marcos, Maranhão. Arq Bras Med Vet Zootec 70:410–418CrossRefGoogle Scholar
  16. Chatterjee MVSFE, Silva Filho EV, Sarkar SK, Sella SM, Bhattacharya A, Satpathy KK, Bhattacharya BD (2007) Distribution and possible source of trace elements in the sediment cores of a tropical macrotidal estuary and their ecotoxicological significance. Environ Int 33:346–356CrossRefGoogle Scholar
  17. Compere P, Wanson S, Pequeux A, Gilles R, Goffinet G (1989) Ultrastructural changes in the gill epithelium of the green crab Carcinus maenas in relation to the external salinity. Tissue Cell 21:299–318CrossRefGoogle Scholar
  18. Conama (2012) Resolução n° 454/12 do Conselho Nacional do Meio Ambiente. Accessed 10 May 2017
  19. Costa CR, Olivi P, Botta CMR, Espindola ELG (2008) A toxicidade em ambientes aquáticos: discussão e métodos de avaliação. Quim Nova 31:1820–1830CrossRefGoogle Scholar
  20. De Almeida Duarte LF, Souza CA, Nobre CR, Pereira CDS, Pinheiro MAA (2016) Multi-level biological responses in Ucides cordatus (Linnaeus, 1763) (Brachyura, Ucididae) as indicators of conservation status in mangrove areas from the western Atlantic. Ecotoxicol Environ Saf 133:176–187CrossRefGoogle Scholar
  21. De Almeida Duarte LF, de Souza CA, Pereira CDS, Pinheiro MAA (2017) Metal toxicity assessment by sentinel species of mangroves: in situ case study integrating chemical and biomarkers analyses. Ecotoxicol Environ Saf 145:367–376CrossRefGoogle Scholar
  22. Duruibe JO, Ogwuegbu MOC, Egwurugwu JN (2007) Heavy metal pollution and human biotoxic effects. Int J Phys 2:112–118Google Scholar
  23. Gamfeldt L, Lefcheck JS, Byrnes JEK, Cardinale BJ, Duffy JM, Griffin JN (2015) Marine biodiversity and ecosystem functioning: what's known and what's next? Oikos 124:252–265CrossRefGoogle Scholar
  24. Harbison PAT (1986) Mangrove muds—a sink and a source for trace metals. Mar Pollut Bull 17:246–250CrossRefGoogle Scholar
  25. Harris RR, Santos MCF (2000) Heavy metal contamination and physiological variability in the Brazilian mangrove crabs Ucides cordatus and Callinectes danae (Crustacea: Decapoda). Mar Biol 137:691–703CrossRefGoogle Scholar
  26. Hayes JD, Flanagan JU, Jowsey IR (2005) Glutathione transferases. Annu Rev Pharmacol Toxicol 45:51–88CrossRefGoogle Scholar
  27. Júnior JMDCA, Ferreira TO, Suarez-Abelenda M, Nóbrega GN, Albuquerque AGBM, de Carvalho BA, Otero XL (2016) The role of bioturbation by Ucides cordatus crab in the fractionation and bioavailability of trace metals in tropical semiarid mangroves. Mar Pollut Bull 111:194–202CrossRefGoogle Scholar
  28. Karami A, Christianus A, ZamriIshak ArifSye M, Courtenay SC (2011) The effects of intramuscular and intraperitoneal injections of benzo[a]pyrene on selected biomarkers in Clarias gariepinus. Ecotoxicol Environ Saf 74:1558–1566CrossRefGoogle Scholar
  29. Ken JH, Habig WH, Jakoby WB (1976) Mechanism for several activities of the glutathione S-transferases. J Biol Chem 251:6183–6188Google Scholar
  30. Lam PK (2009) Use of biomarkers in environmental monitoring. Ocean Coast Manag 52:348–354CrossRefGoogle Scholar
  31. Lavarías S, García C, Crespo R, Pedrini N, Heras H (2013) Study of biochemical biomarkers in freshwater prawn Macrobrachium borellii (Crustacea: Palaemonidae) exposed to organophosphate fenitrothion. Ecotoxicol Environ Saf 96:10–16CrossRefGoogle Scholar
  32. Luoma SN (1983) Bioavailability of trace metals to aquatic organisms—a review. Sci Total Environ 28:1–22CrossRefGoogle Scholar
  33. Magalhães DP, Ferrão Filho AS (2008) A Ecotoxicologia como ferramenta no biomonitoramento de ecossistemas aquáticos. Oecol Bras 12:355–381Google Scholar
  34. Maharajan A, Narayanasamy Y, Ganapiriya V, Shanmugavel K (2015) Histological alterations of a combination of Chlorpyrifos and Cypermethrin (Nurocombi) insecticide in the fresh water crab, Paratelphusa jacquemontii (Rathbun). JOBAZ 72:104–112Google Scholar
  35. Marmion M, Luoto M, Heikkinen RK, Thuiller W (2009) The performance of state-of-the-art modelling techniques depends on geographical distribution of species. Ecol Model 220:3512–3520CrossRefGoogle Scholar
  36. Negro CL (2015) Histopathological effects of endosulfan to hepatopancreas, gills and ovary of the freshwater crab Zilchiopsis collastinensis (Decapoda: Trichodactylidae). Ecotoxicol Environ Saf 113:87–94CrossRefGoogle Scholar
  37. Norena-Barroso E, Simá-Álvarez R, Gold-Bouchot GE, Zapata-Pérez O (2004) Persistent organic pollutants and histological lesions in Mayan catfish Ariopsis assimilis from the estuary of Chetumal, Mexico. Mar Pollut Bull 48:263–269CrossRefGoogle Scholar
  38. Nudi AH, Wagener ALR, Francioni E, Scofield AL, Sette CB, Veiga A (2007) Validation of Ucides cordatus as a bioindicator of oil contamination and bioavailability in mangroves by evaluating sediment and crab PAH records. Environ Int 33:315–327CrossRefGoogle Scholar
  39. Nudi AH, Wagener ALR, Francioni E, Sette CB, Sartori AV, Scofield ADL (2010) Biomarkers of PAHs exposure in crabs Ucides cordatus: laboratory assay and field study. Environ Res 110:137–145CrossRefGoogle Scholar
  40. Osman AGM, Reheem AMA, AbuelFadl KY, GadEl-Rab AG (2010) Enzymatic and histopathologic biomarkers as indicators of aquatic pollution in fishes. Nat Sci 2:1302–1311Google Scholar
  41. Pinheiro MAA, Silva PPG, Duarte LFA, Almeida AA, Zanotto FP (2012) Accumulation of six metals in the mangrove crab Ucides cordatus (Crustacea: Ucididae) and its food source, the red mangrove Rhizophora mangle (Angiosperma: Rhizophoraceae). Ecotoxicol Environ Saf 81:114–121CrossRefGoogle Scholar
  42. Pinheiro MAA, Duarte LFA, Toledo TR, Adam ML, Torres RA (2013) Habitat monitoring and genotoxicity in Ucides cordatus (Crustacea: Ucididae), as tools to manage a mangrove reserve in southeastern Brazil. Environ Monit Assess 185:8273–8285CrossRefGoogle Scholar
  43. Rainbow PS, Amiard-Triquet C, Amiard JC, Smith BD, Langston WJ (2000) Observations on the interaction of zinc and cadmium uptake rates in crustaceans (amphipods and crabs) from coastal sites in UK and France differentially enriched with trace metals. Aquat Toxicol 50:189–204CrossRefGoogle Scholar
  44. Rand GM, Petrocelli SR (1995) Fundamentals of aquatic toxicology. In: Petrocelli SR (ed) Rand GM. Fundamentals of Aquatic Toxicology. Methods and Applications. Hemisphere Publishing Corporation, Washington, pp 1–28Google Scholar
  45. Rao KV, Rao NS (1997) Composition of dredged spoils of Indian harbours: part I—heavy metals. Sci Total Environ 207:13–19CrossRefGoogle Scholar
  46. Rebelo MF, Rodriguez EM, Santos EA, Ansaldo M (2000) Histopathological changes in gills of the estuarine crab Chasmagnathus granulata (Crustacea-Decapoda) following acute exposure to ammonia. Comp Biochem Physiol C 125:157–164Google Scholar
  47. Ribeiro CA, Vollaire Y, Sanchez-Chardi A, Roche H (2005) Bioaccumulation and the effects of organochlorine pesticides, PAH and heavy metals in the eel (Anguila anguila) at the Camargue nature reserve, France. Aquat Toxicol 74:53–69CrossRefGoogle Scholar
  48. Santos MCF (2002) Drinking and osmoregulation in the mangrove crab Ucides cordatus following exposure to benzene. Comp Biochem Physiol 133:29–42CrossRefGoogle Scholar
  49. Soto-Jiménez MF, Páez-Osuna F (2001) Distribution and normalization of heavy metal concentrations in mangrove and lagoonal sediments from Mazatlan Harbor (SE gulf of California). Estuar Coast Shelf Sci 53:259–274CrossRefGoogle Scholar
  50. Sousa DBP, Almeida ZS, Carvalho-Neta RNF (2013) Integrated analysis of two biomarkers in Sciades herzbergii (Ariidae, Siluriformes) to assess the environmental impact at São Marcos’ bay, Maranhão. Brazil Lat Am J Aquat Res 41:305–312Google Scholar
  51. Umbuzeiro GDA, Kummrow F, Roubicek DA, Tominaga MY (2006) Evaluation of the water genotoxicity from Santos estuary (Brazil) in relation to the sediment contamination and effluent discharges. Environ Int 32:359–364CrossRefGoogle Scholar
  52. USEPA (1995) Method 3051. Test methods for evaluating solidwaste (microwave-assisted acid digestion for sediments,sludges, soils and oils). Washington, DC: US EnvironmentalProtection AgencyGoogle Scholar
  53. Valdez Domingos FV, Azevedo M, Silva MD, Randi MAF, Freire CA, de Assis HS, Ribeiro CO (2007) Multibiomarker assessment of three Brazilian estuaries using oysters as bioindicators. Environ Res 105:350–363CrossRefGoogle Scholar
  54. Van der Oost R, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149CrossRefGoogle Scholar
  55. Vasanthi LA, Muruganandam A, Revathi P, Baskar P, Jayapriyan K, Baburajendran R, Munuswamy N (2014) The application of histo-cytopathological biomarkers in the mud crab Scylla serrata (Forskal) to assess heavy metal toxicity in Pulicat Lake, Chennai. Mar Pollut Bull 81:85–93CrossRefGoogle Scholar
  56. Ventura EC, Gaelzer LR, Zanette J, Marques MRF, Bainy ACD (2002) Biochemical indicators of contaminant exposure in spotted pigfish (Orthopristis ruber) caught at three bays of Rio de Janeiro coast. Mar Environ Res 54:775–779CrossRefGoogle Scholar
  57. Vitorino HA, Ortega P, Alta RYP, Zanotto FP, Espósito BP (2018) Evaluation of iron loading in four types of hepatopancreatic cells of the mangrove crab Ucides cordatus using ferrocene derivatives and iron supplements. Environ Sci Pollut Res Int 25:15962–15970CrossRefGoogle Scholar
  58. Vitozzi L, De Angelis GA (1991) Critical review of comparative acute toxicity data on freshwater fish. Aquat Toxicol 19:167–204CrossRefGoogle Scholar
  59. Yi X, Ding H, Lu Y, Liu H, Zhang M, Jiang W (2007) Effects of long-term alachlor exposure on hepatic antioxidant defense and detoxifying enzyme activities in crucian carp (Carassius auratus). Chemosphere 68:1576–1581CrossRefGoogle Scholar
  60. Zhang C, Yu ZG, Zeng GM, Jiang M, Yang ZZ, Cui F, Hu L (2014) Effects of sediment geochemical properties on heavy metal bioavailability. Environ Int 73:270–281CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Raimunda Nonata Fortes Carvalho Neta
    • 1
    Email author
  • Ticianne de Sousa de Oliveira Mota Andrade
    • 2
  • Suelen Rosana Sampaio de Oliveira
    • 3
  • Audalio Rebelo Torres Junior
    • 4
  • William da Silva Cardoso
    • 1
  • Débora Martins Silva Santos
    • 1
  • Wanda dos Santos Batista
    • 2
  • Ilka Márcia R. de Sousa Serra
    • 1
  • Natilene Mesquita Brito
    • 5
  1. 1.Department of Chemistry and BiologyState University of Maranhão (UEMA)São LuísBrazil
  2. 2.Postgraduate Program of Aquatic Resources and Fishery (PPGRAP/UEMA)State University of Maranhão (UEMA)São LuísBrazil
  3. 3.Postgraduate Program of OceanographyFederal University of Maranhão (UFMA)São LuísBrazil
  4. 4.Marine Sciences InstituteFederal University of Maranhão (UFMA)São LuísBrazil
  5. 5.Federal Institute of EducationScience and Technology of Maranhao (IFMA)São LuisBrazil

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