Abstract
Metallothionein-like protein concentrations (MT) and three functionally defined fractions of cholinesterase activity (ChE) were quantified in gill and digestive gland homogenates of tropical cup oysters from 5 nearshore locations in the Colombian Caribbean and correlated with sediment and tissue metal (9 metals) and pesticide (22 organophosphates, OPs, and 20 organochlorines—OCPs), as well as water physical–chemical parameters (salinity, pH, temperature, and dissolved oxygen). Tissue and sediment pesticide concentrations were below detection limits in all samples, whereas sediment and tissue metal concentrations exceeded environmental thresholds at several locations. Tissue MT and ChE biomarkers varied by a factor of 5–6 between locations. Inhibition of cholinesterase activity was negligible for all 5 sites, despite spatial–temporal variation in ChE activity, consistent with below-detection OP concentrations. Tissue MT and ChE biomarkers correlated with tissue and metal sediment concentrations, yet, statistically significant covariance between biomarkers and water chemistry parameters was also observed, indicating that both, metal concentrations and physical–chemical variables, are likely to be responsible for generating the observed spatial–temporal variations in biomarker patterns.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-021-17644-7/MediaObjects/11356_2021_17644_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-021-17644-7/MediaObjects/11356_2021_17644_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-021-17644-7/MediaObjects/11356_2021_17644_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-021-17644-7/MediaObjects/11356_2021_17644_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-021-17644-7/MediaObjects/11356_2021_17644_Fig5_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-021-17644-7/MediaObjects/11356_2021_17644_Fig6_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-021-17644-7/MediaObjects/11356_2021_17644_Fig7_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs11356-021-17644-7/MediaObjects/11356_2021_17644_Fig8_HTML.png)
Similar content being viewed by others
Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Aceto S, Formisano G, Carella F, De Vico G, Gaudio L (2011) The metallothionein genes of Mytilus galloprovincialis: genomic organization, tissue expression and evolution. Mar Genomics 4:61–68
Aguirre- Rubi JR, Luna- Acosta A, Etxebarría N, Soto M, Espinoza F, Ahrens MJ, Marigómez I (2017) Chemical contamination assessment in mangrove-lined Caribbean coastal systems using the oyster Crassostrea rhizophorae as biomonitor species. Environ Sci Pollut Res 25(14):13396–13415
Aguirre-Rubi JR, Luna-Acosta A, Ortiz-Zarragoitia M, Zaldibar IU, Ahrens MJ, Villamil L, Marigómez I (2018) Assessment of ecosystem health disturbance in mangrove-lined Caribbean coastal systems using the oyster Crassostrea rhizophorae as sentinel species. Sci Total Environ 618:718–735
Alonso D, Pineda P, Olivero J, Gonzalez H, Campos N (2000) Mercury levels in muscle of two fish species and sediments from the Cartagena Bay and the Ciénaga Grande de Santa Marta, Colombia. Environ Pollut 109:157–163
Al-Subiai SN, Moody AJ, Mustafa SA, Jha AN (2011) A multiple biomarker approach to investigate the effects of copper on the marine bivalve mollusc, Mytilus edulis. Ecotoxicol Environ Saf 74:1913–1920
Amiard JC, Amiard-Triquet C, Barka S, Pellerin J, Rainbow PS (2006) Metallothioneins in aquatic invertebrates: their role in metal detoxification and their use as biomarkers. Aquat Toxicol 76:160–202
Amiard JC, Journel R, Bacheley H (2008) Influence of field and experimental exposure of mussels (Mytilus sp.) to nickel and vanadium on metallothionein concentration. Comp Biochem Physiol C 147:378–385
Andrade- Brito I, Freire CA, Yamamoto FY, De Assis HCS, Souza-Bastos LR, Cestari MM, De Castilhos Ghisi N, Prodocimo V, Filipak Neto F, Oliveira Ribeiro CA (2012) Monitoring water quality in reservoirs for human supply through multi-biomarker evaluation in tropical fish. J Environ Monit 14:615–625
Attig H, Dagnino A, Negri A, Jebali J, Boussetta H, Viarengo A, Dondero F, Banni M (2010) Uptake and biochemical responses of mussels Mytilus galloprovincialis exposed to sublethal nickel concentrations. Ecotoxicol Environ Saf 73:1712–1719
Barata C, Solayan A, Porte C (2004) Role of B-esterases in assessing toxicity of organophosphorus (chlorpyrifos, malathion) and carbamate (carbofuran) pesticides to Daphnia magna. Aquat Toxicol 66:125–139
Barka S, Pavillon JF, Amiard JC (2001) Influence of different essential and non-essential metals on MTLP levels in the Copepod Tigriopus brevicornis. Comp Biochem Physiol C 128:479–493
Barros- Barrios O, Doria- Argumedo C, Marrugo- Negrete J (2016) Metales pesados (Pb, Cd, Ni, Zn, Hg) en tejidos de Lutjanus synagris y Lutjanus vivanus de la Costa de La Guajira, Norte De Colombia. Vet Zootecnia 10(2):27–41
Batley G, Simpson S (2016) Sediment quality assessment: a practical guide. CSIRO Publishing, Australia
Baudrimont M, Metivaud J, Maury-Brachet R, Ribeyre F, Boudou A (1997) Bioaccumulation and metallothionein response in the Asiatic clam (Corbicula fluminea) after experimental exposure to cadmium and inorganic mercury. Environ Toxicol Chem 16:2096–2106
Bautista- Covarrubias JC, Villaseñor M, Bueno A, Gutierrez D, Voltolina D, Frías-Espericueta MG (2017) Cholinesterase activity in Crassostrea sp. of Nayarit (NW MEXICO) Coastal waters. Rev Int Contam Ambient 33(2):215–220
Bebianno MJ, Barreira LA (2009) Polycyclic aromatic hydrocarbons concentrations and biomarker responses in the clam Ruditapes decussatus transplanted in the Ria Formosa lagoon. Ecotoxicol Environ Saf 72:1849–1860
Bebianno MJ, Nott JA, Langston WJ (1993) Cadmium metabolism in the clam Ruditapes decussata: the role of metallothioneins. Aquat Toxicol 27:315–334
Benali I, Boutiba Z, Grandjean D, De Alencastro LF, Rouane-Hacene O, Chèvre N (2017) Spatial distribution and biological effects of trace metals (Cu, Zn, Pb, Cd) and organic micropollutants (PCBs, PAHs) in mussels Mytilus galloprovincialis along the Algerian west coast. Mar Pollut Bull 115:539–550
Bernal-Hernández YY, Medina-Díaz IM, Robledo-Marenco ML, Velázquez-Fernández JB, Girón-Pérez MI, Ortega-Cervantes L, Maldonado-Vázquez WA, Rojas-García AE (2010) Acetylcholinesterase and metallothionein in oysters (Crassostrea corteziensis) from a subtropical Mexican Pacific estuary. Ecotoxicology 19:819–825
Bocchetti R, Lamberti CV, Pisanelli B, Razzetti EM, Maggi C, Catalano B, Sesta G, Martuccio G, Gabellini M, Regoli F (2008) Seasonal variations of exposure biomarkers, oxidative stress responses and cell damage in the clams, Tapes philippinarum, and mussels, Mytilus galloprovincialis, from Adriatic Sea. Mar Environ Res 66:24–26
Bocquene G, Roig A, Fournier D (1997) Cholinesterases from the common oyster (Crassostrea gigas) evidence for the presence of a soluble acetylcholinesterase insensitive to organophosphate and carbamate inhibitors. FEBS Lett 407:261–266
Bonacci S, Corsi I, Focard S (2006) Cholinesterases in the Antarctic scallop Adamussium colbecki: characterization and sensitivity to pollutants. Ecotoxicol Environ Saf 72:1481–1488
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254
Buchman MF (2008) Screening quick references tables, NOAA OR&R report 08–1, Seattle WA, Office of Response and Restoration division, National oceanic and Atmospheric Administration
Carranza-Lopez L, Alvarez-Ortega N, Caballero-Gallardo K, Gonzalez-Montes A, Olivero-Verbel J (2020) Biomonitoring of lead exposure in children from two fishing communities at Northern Colombia. Biological Trace Element Research
Carvalho FP (2017) Pesticides, environment, and food safety. Food Energy Secur 6:48–60
Ceratto N, Dondero F, Loo JW, Burlando B, Viarengo A (2002) Cloning and sequencing of a novel metallothionein gene in Mytilus galloprovincialis. Comp Biochem Physiol C Toxicol Pharmacol 131(3):217–222
Chakraborty S, Ray M, Ray S (2012) Arsenic toxicity: a heart-breaking saga of a freshwater mollusc. Tissue Cell 44:151–155
Chan CY, Wang WX (2019) Biomarker responses in oysters Crassostrea hongkongensis in relation to metal contamination patterns in the Pearl River Estuary, southern China. Environ Pollut 251:264–276
Choi JY, Yu J, Yang DB, Ra K, Kim KT, Hong GH, Shin KH (2011) Acetylthiocholine (ATC) cleaving cholinesterase (ChE) activity as a potential biomarker of pesticide exposure in the Manila clam, Ruditapes philippinarum, of Korea. Mar Environ Res 71:162–168
Cordy P, Veiga MM, Salih I, Al-Saadi S, Console S, Garcia O, Mesa LA, Velasquez-Lopez P, Roeser M (2011) Mercury contamination from artisanal gold mining in Antioquia, Colombia: the world’s highest per capita mercury pollution. Sci Total Environ 410–41:154–160
Costa M, Zhuang Z, Huang X, Cosentino S, Klein CB, Salnikov K (1994) Molecular mechanisms of nickel carcinogenesis. Sci Total Environ 148:191–199
Cravo A, Pereira C, Gomes T, Cardoso C, Serafim A, Almeida C, Rocha T, Lopes B, Company R, Medeiros A, Norberto R, Pereira R, Araújo O, Bebianno MJ (2012) A multibiomarker approach in the clam Ruditapes decussatus to assess the impact of pollution in the Ria Formosa lagoon, South Coast of Portugal. Mar Environ Res 75:23–34
D’Costa A, Shyama SK, Kumar P, Furtado S (2017) Genotoxic and biochemical biomarker responses in Meretrix casta exposed to environmentally relevant concentrations of cadmium. J Biosens Biomark Diagn 2(1):1–7
Damiens G, His E, Gnassia BM, Quiniou F, Romeo M (2004) Evaluation of biomarkers in oyster larvae in natural and polluted conditions. Comp Biochem Physiol C Toxicol Pharmacol 138(2):121–128
David E, Tanguy A, Riso R, Quiniou L, Laroche J, Moraga D (2012) Responses of Pacific oyster Crassostrea gigas populations to abiotic stress in environmentally contrasted estuaries along the Atlantic coast of France. Aquat Toxicol 109:70–79
De Marchi L, Neto V, Pretti C, Figueira E, Chiellini F, Soares AM, Freitas R (2017) The impacts of emergent pollutants on Ruditapes philippinarum: biochemical responses to carbon nanoparticles exposure. Aquat Toxicol 187:38–47
de Souza PR, de Souza KS, de Assis CRD, de Araújo MC, Silva KCC, de Fátima Xavier da Silva J, Ferreira ACM, da Silva VL, Adam ML, de Carvalho LB, de Souza Bezerra R (2018) Acetylcholinesterase of mangrove oyster Crassostrea rhizophorae: a highly thermostable enzyme with promising features for estuarine biomonitoring. Aquatic Toxicol 197:109–121
Dondero F, Negri A, Boatti L, Marsano F, Mignone F, Viarengo A (2010) Transcriptomic and proteomic effects of a neonicotinoid insecticide mixture in the marine mussel (Mytilus galloprovincialis, Lam.). Sci Total Environ 408:3775–3786
Doran WJ, Cope WG, Rada RG, Sandheinrich MB (2001) Acetylcholinesterase inhibition in the threeridge mussel (Amblema plicata) by chlorpyrifos: implications for biomonitoring. Ecotoxicol Environ Saf 49:91–98
Ellman GL, Courtney KD, Valentino A Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
El-Shenawy NS, Moawad TIS, Mohallal ME, Abdel-Nabi IM, Taha IA (2009) Histopathologic biomarker response of clam, Ruditapes decussates, to organophosphorus pesticides Reldan and Roundup: a laboratory study. Ocean Sci J 44:27–34
Eriksen KDH, Andersen T, Stenersen J (1990) Iso-metallothionein in cod induced by cadmium, zinc and nickel. In: Proceedings of the 12th Annual Conference on Physiological and Biochemical Approaches to the Toxicological Assessment of Environmental Pollution
Escartin E, Porte C (1997) The use of cholinesterase activities from Mytilus galloprovincialis in pollution monitoring. Environ Toxicol Chem 10:2090–2095
Fernandez A, Singh A, Jaffé R (2007) A literature review on trace metals and organic compounds of anthropogenic origin in the Wider Caribbean Region. Mar Pollut Bull 54:1681–1691
Fernandez-Maestre R, Johnson-Restrepo B, Olivero-Verbel J (2018) Heavy metals in sediments and fish in the Caribbean Coast of Colombia: assessing the environmental risk. Int J Environ Res 12:289–301
Franco AJ, León-Luna IM (2010) Geoquímica y concentraciones de metales pesados en un organismo de interés comercial (Corbula caribaea, D’Orbigny, 1842) en la zona submareal superficial de la Ciénaga de Mallorquín-Atlántico. Boletín Científico CIOH 28:69–83
Frasco M, Fournier D, Carvalho F, Guilhermino L (2005) Do metals inhibit acetylcholinesterase (AChE)? Implementation of assay conditions for the use of AChE activity as a biomarker of metal toxicity. Biomarkers 10:360–375
Garcés-Ordóñez O, Vivas-Aguas LJ, Martínez M, Córdoba T, Contreras A, Obando P, Moreno Y, Muñoz J, Nieto Y, Ríos M, Sánchez J, Sánchez D (2016) Diagnóstico y Evaluación de la Calidad de las Aguas Marinas y Costeras del Caribe y Pacífico colombianos. Serie de Publicaciones Periódicas del Invemar No. 4 (2016). REDCAM. Informe Técnico 2015. INVEMAR, MADS y CAR costeras. Santa Marta
Geffard A, Amiard-Triquet C, Amiard JC, Mouneyrac C (2001) Temporal variations of metallothionein and metal concentrations in the digestive gland of oysters (Crassostrea gigas) from a clean and a metal-rich site. Biomarkers 6(2):91–107
Géret F, Jouan A, Turpin V, Bebianno MJ, Cosson RP (2002) Influence of metal exposure on metallothionein synthesis and lipid peroxidation in two bivalve mollusks: the oyster (Crassostrea gigas) and the mussel (Mytilus edulis). Aquat Living Resour 15:61–66
Gold-Bouchot G, Zapata-Pérez O (2004) Contaminación, Ecotoxicología y Manejo Costero. Capítulo 18. Centro de Investigación y de Estudios Avanzados del IPN, Unidad Mérida. En: Rivera-Arriaga E, Villalobos-Zapata GJ, Azuz-Adeath I, Rosado-May F (eds) (2004) El Manejo Costero en México. Universidad Autónoma de Campeche, SEMARNAT, CETYS-Universidad, Universidad de Quintana Roo
Gold-Bouchot G, Zapata O, Ceja V, Rodríguez G, Simá R, Aguirre ML, Vidal VM, Da Ros L, Nasci C (2007) Biological effects of environmental pollutants in American Oyster, Crassostrea virginica: a field study in Laguna de Términos, Mexico. Int J Environ Health Res 1:171–184
Gueguen Y, Denis S, Adrien S, Kevin M, Pierre G, Solène B, Marine N, Patrick B, Herehia H, Serge P, Gilles LM (2017) Response of the pearl oyster Pinctada margaritifera to cadmium and chromium: identification of molecular biomarkers. Mar Pollut Bull 118:420–426
Hamer B, Jakšić Z, Pavičić-Hamer D, Perić L, Medaković D, Ivanković D, Pavičić J, Zilberberg C, Schröder HC, Müller WEG, Smodlaka N, Batel R (2008) Effect of hypoosmotic stress by low salinity acclimation of Mediterranean mussels Mytilus galloprovincialis on biological parameters used for pollution assessment. Aquat Toxicol 89:137–151
Hédouin L, Pringault O, Bustamante P, Fichez R, Warnau M (2011) Validation of two tropical marine bivalves as bioindicators of mining contamination in the New Caledonia lagoon: field transplantation experiments. Water Res 45:483–496
Hernández- Moreno D, Soler F, Míguez MP, Pérez-López M (2010) Brain acetylcholinesterase, malondialdehyde and reduced glutathione as biomarkers of continuous exposure of tench, Tinca tinca, to carbofuran or deltamethrin. Sci Total Environ 408:4976–4983
INVEMAR (2017) Diagnóstico y evaluación de la calidad de las aguas marinas y costeras en el Caribe y Pacífico colombianos. Garcés, O. y L. Espinosa (Eds.). REDCAM: INVEMAR, MADS y CAR costeras. Informe Técnico 2016. Serie de Publicaciones Periódicas No. 4 (2017) del INVEMAR. Santa Marta
Ivanina AV, Taylor C, Sokolova IM (2009) Effects of elevated temperature and cadmium exposure on stress protein response in eastern oysters Crassostrea virginica (Gmelin). Aquat Toxicol 91:245–254
Ivanković D, Pavičić J, Erk M, Filipović-Marijić V, Raspor B (2005) Evaluation of the Mytilus galloprovincialis Lam. digestive gland metallothionein as a biomarker in a long-term field study: seasonal and spatial variability. Mar Pollut Bull 50:1303–1313
Jenny MJ, Ringwood AH, Schey K, Warr GW, Chapman RW (2004) Diversity of metallothioneins in the American oyster, Crassostrea virginica, revealed by transcriptomic and proteomic approaches. Eur J Biochem 271(9):1702–1712
Kimbrough KL, Johnson WE, Lauenstein GG, Christensen JD, Apeti DA (2008) An assessment of two decades of contaminant monitoring in the nation’s coastal zone. NOAA Technical Memorandum NOS NCCOS 74
Lacerda LD, Molisani MM (2006) Three decades of Cd and Zn contamination in Sepetiba Bay, SE Brazil: evidence from the mangrove oyster Crassostraea rhizophorae. Mar Pollut Bull 52:974–977
Leiniö S, Lehtonen KK (2005) Seasonal variability in biomarkers in the bivalves Mytilus edulis and Macoma balthica from the northern Baltic Sea. Comp Biochem Physiol C Toxicol Pharmacol 140:408–421
Lewis M, Mayer F, Powell R, Nelson M, Klaine S, Henry M, Dickson G (1995) Ecotoxicology and risk assessment for wetlands. Society of Environmental Toxicology and Chemistry (SETAC). SETAC Pellston Workshop on Ecotoxicology and Risk Assessment for Wetlands. 30 July- 3 August 1995. Fairmont Hot Springs, Anaconda. Montana
Liu X, Wang WX (2016) Time changes in biomarker responses in two species of oyster transplanted into a metal contaminated estuary. Sci Total Environ 544:281–290
Lüchmann KH, Mattos JJ, Siebert MN, Granucci N, Dorrington TS, Bícego MC, Taniguchi S, Sasaki ST, Daura-Jorge FG, Bainy ACD (2011) Biochemical biomarkers and hydrocarbons concentrations in the mangrove oyster Crassostrea brasiliana following exposure to diesel fuel water-accommodated fraction. Aquat Toxicol 105:652–660
Luo L, Ke C, Guo X, Shi B, Huang M (2014) Metal accumulation and differentially expressed proteins in gill of oyster (Crassostrea hongkongensis) exposed to long-term heavy metal-contaminated estuary. Fish Shellfish Immunol 38:318–329
MacDonald DD, Carr RS, Calder FD, Long ER, Ingersoll CG (1996) Development and evaluation of sediment quality guidelines for Florida coastal waters. Ecotoxicology 5:253–278
Mackay EA, Overnell J, Dunbar B, Davidson I, Hunziker PE, Kägi JHR, Fothergill JE (1993) Complete amino acid sequences of five dimeric and four monomeric forms of metallothionein from the edible mussel Mytilus edulis. Eur J Biochem 218:183–194
Magni P, De Falco G, Falugi C, Franzoni M, Monteverde M, Perrone E, Sgro M, Bolognesi C (2006) Genotoxicity biomarkers and acetylcholinesterase activity in natural populations of Mytilus galloprovincialis among a pollution gradient in the Gulf of Oristano (Sardinia, western Mediterranean). Environ Pollut 142:65–72
Menzies R, Quinete NS, Gardinali P, Seba D (2013) Baseline occurrence of organochlorine pesticides and other xenobiotics in the marine environment: Caribbean and Pacific collections. Mar Pollut Bull 70:289–295
Moncaleano-Niño AM, Barrios-Latorre SA, Poloche-Hernández JF, Becquet V, Huet V, Villamil L, Thomas-Guyon H, Ahrens MJ, Luna-Acosta A (2017) Alterations of tissue metallothionein and vitellogenin concentrations in tropical cup oysters (Saccostrea sp.) following short-term (96 h) exposure to cadmium. Aquat Toxicol 185:160–170
Moncaleano-Niño AM, Luna- Acosta A, Gómez-Cubillos MC, Villamil L, Ahrens MJ (2018) Cholinesterase activity in the cup oyster Saccostrea sp. exposed to chlorpyrifos, imidacloprid and cadmium. Ecotoxicol Environ Saf 151:242–254
Monserrat JM, Bianchini A, Bainy AC (2002) Kinetic and toxicological characteristics of acetylcholinesterase from the gills of oysters (Crassostrea rhizophorae) and other aquatic species. Mar Environ Res 54:781–785
Monserrat JM, Martínez PE, Geracitano LA, Amado LL, Martins CMG, Pinho GLL, Chaves IS, Ferreira-Cravo M, Ventura-Lima J, Bianchini A (2007) Pollution biomarkers in estuarine animals: critical review and new perspectives. Comp Biochem Physiol C Toxicol Pharmacol 146:221–234
Montaudouin X, Paul-Pont I, Lambert C, Gonzalez P, Raymond N, Jude F, Legeay A, Baudrimont M, Dang M, Le Grand F, Le Goïc N, Bourasseau I, Paillard C (2010) Bivalve population health: multistress to identify hot spots. Mar Pollut Bull 60:1307–1318
Mora P, Fournier D, Narbonne JF (1999) Cholinesterases from the marine mussels Mytilus galloprovincialis Lmk. and M. edulis L. and from the freshwater bivalve Corbicula fluminea Muller. Comp Biochem Physiol C 122(3):353–361
Morillo J, Usero J, Gracia I (2004) Heavy metal distribution in marine sediments from the southwest coast of Spain. Chemosphere 55:431–442
Mouneyrac C, Amiard JC, Amiard-Triquet C (1998) Effects of natural factors (salinity and body weight) on cadmium, copper, zinc and metallothionein-like protein levels in resident populations of oysters Crassostrea gigas from a polluted estuary. Mar Ecol Prog Ser 162:125–135
Mourgaud Y, Martinez É, Geffard A, Andral B, Stanisiere JY, Amiard JC (2002) Metallothionein concentration in the mussel Mytilus galloprovincialis as a biomarker of response to metal contamination: validation in the field. Biomarkers 7(6):479–490
Nunes B, Resende ST (2017) Cholinesterase characterization of two autochthonous species of Ria de Aveiro (Diopatra neapolitana and Solen marginatus) and comparison of sensitivities towards a series of common contaminants. Environ Sci Pollut Res 24:12155–12167
Olivero-Verbel J, Johnson- Restrepo B, Baldiris-Avila R, Güette-Fernández J, Magallanes-Carreazo E, Vanegas-Ramírez L, Kunihiko N (2008) Human and crab exposure to mercury in the Caribbean coastal shoreline of Colombia: impact from an abandoned chlor-alkali plant. Environ Int 34:476–482
Pagenkopp Lohan KM, Hill-Spanik KM, Torchin ME, Strong EE, Fleischer RC, Ruiz GM (2015) Molecular phylogenetics reveals first record and invasion of Saccostrea species in the Caribbean. Mar Biol 162:957–968
Peric L, Fafanđel M, Glad M, Bihari N (2012) Heavy metals concentration and Metallothionein content in resident and caged Mussels Mytilus galloprovincialis from Rijeka Bay, Croatia. Fresenius Environ Bull 21(9):2785–2794
Peric L, Ribaric L, Nerlovic V (2013) Cholinesterase activity in the tissues of bivalves Noah’s ark shell (Arca noae) and warty venus (Venus verrucosa): characterization and in vitro sensitivity to organophosphorus pesticide trichlorfon. Comp Biochem Physiol B 165:243–249
Prato E, Biandolino F, Scardicchio C (2006) Test for acute toxicity of copper, cadmium, and mercury in five marine species. Turk J Zool 30:285–290
Ragnarsdottir K (2000) Environmental fate and toxicology of organophosphate pesticides. J Geol Soc 157:859–876
Rajkumar J (2013) Reduced glutathione and acetylcholinesterase expressions in Perna indica exposed to trivalent arsenic. Int J Biol Res 1:1–4
Ramakritinan CM, Chandurvelan R, Kumaraguru AK (2012) Acute toxicity of metals: Cu, Pb, Cd, Hg, and Zn on marine molluscs, Cerithidea cingulata G., and Modiolus philippinarum H. Indian J Geo-Mar Sci 41(2):141–145
Ramdine G, Fichet D, Louis M, Lemoine S (2012) Polycyclic aromatic hydrocarbons (PAHs) in surface sediment and oysters (Crassostrea rhizophorae) from mangrove of Guadeloupe: Levels, bioavailability and effects. Ecotoxicol Environ Saf 79:80–89
Rasmussen LP, Hage E, Karlog O (1983) Histopathological studies of the acute and chronic toxic effects of 2 N-nitroso-compounds on the blue mussel (Mytilus edulis). Nordisk Vet Med 35:306–313
Raspor B, Dragun Z, Erk M, Ivankovic D, Pavicic J (2004) Is the digestive gland of Mytilus galloprovincialis a tissue of choice for estimating cadmium exposure by means of metallothioneins? Sci Total Environ 333:99–108
Riba I, Garcia-Luque E, Blasco J, DelValls T (2003) Bioavailability of heavy metals bound to estuarine sediments as a function of pH and salinity values. Chem Speciat Bioavailab 15:101–114
Roesijadi G, Hansen KM, Unger ME (1997) Concentration-response relationships for Cd, Cu, and Zn and metallothionein mRNA induction in larvae of Crassostrea virginica. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 118:267–270
Salmore AK, Hollis EJ, McLellan SL (2006) Delineation of a chemical and biological signature for stormwater pollution in an urban river. J Water Health 4:247–262
Sandahl JF, Jenkins JJ (2002) Pacific steelhead (Oncorhynchus mykiss) exposed to chlorpyrifos: benchmark concentration estimates for acetylcholinesterase inhibition. Environ Toxicol Chem 21(11):2452–2458
Santos HM, Diniz MS, Costa PM, Peres I, Costa MH, Alves S, Capelo JL (2007) Toxicological effects and bioaccumulation in the freshwater clam (Corbicula fluminea) following exposure to trivalent arsenic. Environ Toxicol 22:502–509
Senger MR, Rosemberg DB, Rico EP, de Bem Arizi M, Dias RD, Bogo MR, Bonan CD (2006) In vitro effect of zinc and cadmium on acetylcholinesterase and ectonucleotidase activities in zebrafish (Danio rerio) brain. Toxicol In Vitro 20:954–958
Serafim A, Company R, Lopes B, Fonseca VF, Franca S, Vasconcelos P, Bebianno MJ, Cabral HN (2012) Application of an integrated biomarker response index (IBR) to assess temporal variation of environmental quality in two Portuguese aquatic systems. Ecol Ind 19:215–225
Singh A, Laurence M (2008) Examination of policies and MEAs commitment by SIDS for sustainable management of the Caribbean Sea. Mar Policy 32:274–282
Singh N, Turner A (2009) Trace metals in antifouling paint particles and their heterogeneous contamination of coastal sediments. Mar Pollut Bull 58:559–564
Sokal RR, Rohlf FJ (1995) Biometry: the principles of statistics in biological research. WH Freeman and Co, New York
Spalding M, Kramer P (2004) The Caribbean. Defying ocean’s end: an agenda for action. Island Press, Washington DC, pp 7–41
Sun M, Liu G, Lin H, Zhang T, Guo W (2018) Effect of salinity on the bioaccumulation and depuration of cadmium in the pacific cupped oyster, Crassostrea gigas. Environ Toxicol Pharmacol 62:88–97
Talesa V, Romani R, Antognelli C, Giovannini E, Rosi G (2002) Different expressions of organophosphate-resistant acetyl-cholinesterases in the bivalve mollusk Scapharca inaequivalvis living in three different habitats. Environ Toxicol Chem 21:102–108
Tejeda- Benitez L, Flegal R, Odigie K, Olivero- Verbel J (2016) Pollution by metals and toxicity assessment using Caenorhabditis elegans in sediments from the Magdalena River, Colombia. Environ Pollut 212:238–250
Thevenod F, Lee WK (2013) Cadmium and cellular signaling cascades: interactions between cell death and survival pathways. Arch Ecotoxicol 87:1743–1786
Thomann RV, Mahony JD, Mueller R (1995) Steady-state model of biota sediment accumulation factor for metals in 2 marine bivalves. Environ Toxicol Chem 14:1989–1998
Tosic M, Restrepo JD, Lonin S, Izquierdo A, Martins F (2019) Water and sediment quality in Cartagena Bay, Colombia: seasonal variability and potential impacts of pollution. Estuar Coast Shelf Sci 216:187–203
Tsangaris C, Kormas K, Strogyloudi E, Hatzianestis I, Neofitou C, Andral B, Galgani F (2010) Multiple biomarkers of pollution effects in caged mussels on the Greek coastline. Comp Biochem Physiol C Toxicol Pharmacol 151(3):369–378
UNEP (2008) Regionally based assessment of persistent toxic substances. UNEP- United Nations- GEF. 211 pp
Unger ME, Chen TT, Murphy CM, Vestling MM, Fenselau Roesijadi G (1991) Primary structure of molluscan metallothioneins deduced from PCR-amplified cDNA and mass spectrometry of purified proteins. Biochem Biophys Acta 1074:371–377
Valbonesi P, Sartor G, Fabbri E (2013) Characterization of cholinesterase activity in three bivalves inhabiting the North Adriatic Sea and their possible use as sentinel organisms for biosurveillance programmes. Sci Total Environ 312:79–88
Vallejo Toro PP, Vásquez Bedoya LF, Correa ID, Bernal Franco GR, Alcantara- Carrió J, Palacio Baena JA (2016) Impact of terrestrial mining and intensive agriculture in pollution of estuarine surface sediments: spatial distribution of trace metals in the Gulf of Urabá, Colombia. Mar Pollut Bull 111(1–2):311–320
Viarengo A (1989) Heavy metals in marine invertebrates: mechanisms of regulation and toxicity at the cellular level. Rev Aquat Sci 1:295–317
Viarengo A, Ponzano E, Dondero F, Fabbri R (1997) A simple spectrophotometric method for metallothionein evaluation in marine organisms: an application to Mediterranean and Antarctic molluscs. Mar Environ Res 44:69–84
Vivas-Aguas LJ, Espinosa L, Sánchez J, Cadavid B, Bautista P, Quintero M, Betancourt J, Parra JP, Parra LG, Cuadrado I, Ibarra K (2012) Diagnóstico y evaluación de la calidad ambiental marina en el Caribe y Pacífico Colombiano. REDCAM. Informe Técnico 2012. INVEMAR. Santa Marta
Vivas-Aguas LJ, Ibarra K, Sánchez J, Martínez M, Nieto Y, Moreno Y, Cuadrado I, Obando P, Garces O, Sánchez D, Villaraga M, Sierra O (2015) Diagnóstico y evaluación de la calidad de las aguas marinas y costeras del Caribe y Pacífico Colombiano. Serie de publicaciones periódicas del INVEMAR No 4 (2015). REDCAM. Informe Técnico 2014. INVEMAR. Santa Marta
Vryzas Z, Ramwell C, Sans C (2020) Pesticide prioritization approaches and limitations in environmental monitoring studies: from Europe to Latin America and the Caribbean. Environ Int 143(105917):1–7
Wang WX, Rainbow PS (2010) Significance of metallothioneins in metal accumulation kinetics in marine animals. Comp Biochem Physiol C Toxicol Pharmacol 152(1):1–8
Weng N, Wang WX (2014) Improved tolerance of metals in contaminated oyster larvae. Aquat Toxicol 146:61–69
Yingprasertchai T, Yu R, Tran T, Chong Kong R, O’Connor W, MacFarlane G (2019) Characterization of the metallothionein gene in the Sydney rock oyster and its expression upon metal exposure in oysters with different prior metal exposure histories. Mar Environ Res 151:104775
Zar JH (2010) Biostatistical analysis, 5th edn. Prentice Hall, New Jersey
Acknowledgements
We thank I. Marigómez, J. Aguirre-Rubi, N. Etxebarria, M. Soto, and colleagues from the Research Centre for Experimental Marine Biology and Biotechnology (Plentzia Marine Station; PiE-UPV/EHU), University of Basque Country, for performing metal analysis in oyster tissues. We, furthermore, thank L. Espinoza (Invemar, Santa Marta) for pesticide analysis, and the municipal marina of Santa Marta for authorizing access to their facilities. This study was carried out in accordance with decree 1376-2013 by the Colombian Ministry for the Environment and Sustainable Development (MADS) under a general collection permit issued to Jorge Tadeo Lozano University by the Colombian National Authority for Environmental Licenses (ANLA, Res.1271-2014).
Funding
Financial support for this study came in part from a research grant from the Spanish Agency for International Development Cooperation (CARIBIOPOL-AECID 11-CAP2-1595), as well as from a research grant from Jorge Tadeo Lozano University (research grant 560–10-13, project MOSAICO-I) and from a scholarship to A.M. from COLCIENCIAS (Announcement No. 528).
Author information
Authors and Affiliations
Contributions
AMMN: conceptualization, methodology, formal analysis, investigation, writing original draft, visualization. MMCC: methodology, formal analysis, writing, review and editing. ALA: conceptualization, methodology, writing, review and editing, funding acquisition. LV: conceptualization, methodology, writing, review and editing. SCR: methodology. MJA: conceptualization, review and editing, project administration, funding acquisition. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Cinta Porte
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Moncaleano-Niño, A.M., Gómez-Cubillos, M.C., Luna-Acosta, A. et al. Monitoring metallothionein-like protein concentrations and cholinesterase activity in tropical cup oysters as biomarkers of exposure to metals and pesticides in the southern Caribbean, Colombia. Environ Sci Pollut Res 29, 25157–25183 (2022). https://doi.org/10.1007/s11356-021-17644-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-17644-7