Enhanced trace element concentrations in tissues of the clam Ruditapes decussatus transplanted to areas influenced by human activities (Ria Formosa, Portugal)





trace elements, biological parameters, Ruditapes decussatus, Ria Formosa


To examine the extent to which human activities near the Ria Formosa coastal lagoon influence the accumulation of trace elements (TE) in Ruditapes decussatus, individuals were transplanted from a natural bank located in the lower lagoon to three sites located in clam growth grounds under the influence of a small city (Faro), a fish farming centre (Olhão) and a site near the lagoon inlet (Lavajo). Concentrations were determined in substrate of the clam grounds and in the digestive gland, gills, mantle plus siphons, and remaining tissues of clams in four periods of the year. These measurements were accomplished with the monthly survey of the gametogenic stages, condition index, proteins, glycogen, total lipids, pH and osmolarity of hemolymph. Arsenic, Cu, Mn, V, Cr and Pb were preferentially linked to the digestive gland, while Cd was linked to the gills. TE concentrations in the digestive gland and remaining tissues were higher in winter, most likely reflecting additional inputs associated with rain. The lack of disruptions in biological parameters and the prolonged period of spawning and gonad recovery in clams suggest that the current TE availability in the lagoon has a minor influence on the reproductive cycle and hence on clam production.


Download data is not yet available.


Abdi H., Williams L.J. 2010. Principal component analysis. Wiley Interdiscip. Rev. Comput. Stat. 2: 433-459. https://doi.org/10.1002/wics.101

Águas M.P.N. 1985. Simulação da circulação hidrodinâmica na Ria Formosa. Sist. lagunares do Algarve. Semin. Comemorativo do Dia Mund. do Ambiente. PMid:3838177

Amiard J.C., Amiard-Triquet C., Barka S., et al. 2006. Metallothioneins in aquatic invertebrates: Their role in metal detoxification and their use as biomarkers. Aquat. Toxicol. 76: 160-202. https://doi.org/10.1016/j.aquatox.2005.08.015 PMid:16289342

ATSDR 2015.The priority list of hazardous substances that will be the candidates for Toxicological profiles [WWW Document]. Accessed 20/06/2016 at Bebianno M.J. 1995. Effects of pollutants in the Ria Formosa Lagoon, Portugal. Sci. Total Environ. 171: 107-115.

Bebianno M.J., Langston W.J. 1993. Turnover rate of metallothionein and cadmium in Mytilus edulis. Biometals 6: 239-244. https://doi.org/10.1007/BF00187762 PMid:8260794

Bebianno M.J., Serafim M.A. 2003. Variation of metal and metallothionein concentrations in a natural population of Ruditapes decussatus. Arch. Environ. Contam. Toxicol. 44: 53-66. https://doi.org/10.1007/s00244-002-2004-7 PMid:12434219

Bebianno M.J., Serafim M.A.P., Rita M.F. 1994. Involvement of metallothionein in cadmium accumulation and elimination in the clam Ruditapes decussata. Bull. Environ. Contam. Toxicol. 53: 726-732. https://doi.org/10.1007/BF00196946 PMid:7833610

Breitwieser M., Viricel A., Graber M., et al. 2016. Short-term and long-term biological effects of chronic chemical contamination on natural populations of a marine bivalve. PLoS One 11: e0150184. https://doi.org/10.1371/journal.pone.0150184 PMid:26938082 PMCid:PMC4777565

Bryan G.W., Waldichuk M., Pentreath R.J., et al. 1979. Bioaccumulation of marine pollutants [and Discussion]. Philos. Trans. R. Soc. B Biol. Sci. 286: 483-505.

Caetano M., Vale C., Bebianno M. 2002. Distribution of Fe, Mn, Cu and Cd in upper sediments and sediments-trap material of Ria Formosa (Portugal). J. Coast. Res. 36: 118-123.

Caetano M., Madureira M.J., Vale C. 2007. Exchange of Cu and Cd across the sediment-water interface in intertidal mud flats from Ria Formosa (Portugal). Hydrobiologia 587: 147-155. https://doi.org/10.1007/s10750-007-0673-y

Caetano M., Vale C., Anes B., et al. 2013. The Condor seamount at Mid-Atlantic Ridge as a supplementary source of trace and rare earth elements to the sediments. Deep Sea Res. Part II Top. Stud. Oceanogr. 98(PA): 24-37.

Capuzzo J.M., Moore M.N., Widdows J. 1988. Effects of toxic chemicals in the marine environment: predictions of impacts from laboratory studies. Aquat. Toxicol. 11: 303-311. https://doi.org/10.1016/0166-445X(88)90080-X

Cooper S., Bonneris E., Michaud A., et al. 2013. Influence of a step-change in metal exposure (Cd, Cu, Zn) on metal accumulation and subcellular partitioning in a freshwater bivalve, Pyganodon grandis. A long-term transplantation experiment between lakes with contrasting ambient metal levels. Aquat. Toxicol. 132-133: 73-83. https://doi.org/10.1016/j.aquatox.2013.01.021 PMid:23466431

Cortesão C., Mendes R., Vale C. 1986. Metais pesados em bivalves e sedimentos na Ria Formosa, Algarve. Bol. Inst. Nac. Investig. das pescas 14: 3-28.

Costanza R., D'Arge R., Groot R. de, et al. 1997. The value of the world's ecosystem services and natural capital. Nature 387: 253-260. https://doi.org/10.1038/387253a0

Cravo A., Pereira C., Gomes T., et al. 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. PMid:22001190

Cravo A., Cardeira S., Pereira C., et al. 2014. Exchanges of nutrients and chlorophyll a through two inlets of Ria Formosa, South of Portugal, during coastal upwelling events. J. Sea Res. 93: 63-74. https://doi.org/10.1016/j.seares.2014.04.004

Cunha A.H., Santos R.P., Gaspar A.P., et al. 2005. Seagrass landscape-scale changes in response to disturbance created by the dynamics of barrier-islands: A case study from Ria Formosa (Southern Portugal). Estuar. Coast. Shelf Sci. 64: 636-644. https://doi.org/10.1016/j.ecss.2005.03.018

Delgado M., Pérez-Camacho A. 2005. Histological study of the gonadal development of Ruditapes decussatus (L.) (Mollusca: Bivalvia) and its relationship with available food. Sci. Mar. 69: 87-97. https://doi.org/10.3989/scimar.2005.69n187

DGRM 2013. Recursos da Pesca. Direcção Geral das Pescas e Aquicultura. Série estatística 2011 22 A-B, 181 pp.

EC 2001. Commission regulation (EC) no. 466/2001 of 8 March 2001 setting maximum levels for certain contaminants in foodstuffs, Official Journal of the European Communities. Brussels, L77.

Falcão M., Vale C. 1990. Study of the Ria Formosa ecosystem: benthic nutrient remineralization and tidal variability of nutrients in the water. Hydrobiologia 207: 137-146. https://doi.org/10.1007/BF00041450

Falcão M., Vale C. 1998. Sediment-water exchanges of ammonium and phosphate in intertidal and subtidal areas of a mesotidal coastal lagoon (Ria Formosa). Hydrobiologia 374: 193-201. https://doi.org/10.1023/A:1017083724636

Falcão M., Caetano M., Serpa D., et al. 2006. Effects of infauna harvesting on tidal flats of a coastal lagoon (Ria Formosa, Portugal): Implications on phosphorus dynamics. Mar. Environ. Res. 61: 136-148. https://doi.org/10.1016/j.marenvres.2005.08.002 PMid:16242182

Folch J., Lees M., Sloane-Stanley G. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: 497-509. PMid:13428781

Folk R.L., Ward W.C. 1957. Brazos River Bar: A study in the significance of grain size parameters. J. Sediment. Petrol. 27: 3-26. https://doi.org/10.1306/74D70646-2B21-11D7-8648000102C1865D

Gauthier-Clerc S., Pellerin J., Blaise C., et al. 2002. Delayed gametogenesis of Mya arenaria in the Saguenay fjord (Canada): a consequence of endocrine disruptors? Comp. Biochem. Physiol. Part C Toxicol. Pharmacol. 131: 457-467.

Guimarães M.H.M.E., Cunha A.H., Nzinga R.L., et al. 2012. The distribution of seagrass (Zostera noltii) in the Ria Formosa lagoon system and the implications of clam farming on its conservation. J. Nat. Conserv. 20: 30-40. https://doi.org/10.1016/j.jnc.2011.07.005

Gustafson L.L., Stoskopf M.K., Bogan A.E., et al. 2005. Evaluation of a nonlethal technique for hemolymph collection in Elliptio complanata, a freshwater bivalve (Mollusca: Unionidae). Dis. Aquat. Organ. 65: 159-165. https://doi.org/10.3354/dao065159 PMid:16060269

Hamza-Chaffai A. 2014. Usefulness of bioindicators and biomarkers in pollution biomonitoring. Int. J. Biotechnol. Wellness Ind. 3: 19-26. https://doi.org/10.6000/1927-3037.2014.03.01.4

Ivanina A.V, Beniash E., Etzkorn M., et al. 2013. Short-term acute hypercapnia affects cellular responses to trace metals in the hard clams Mercenaria mercenaria. Aquat. Toxicol. 140-141: 123-133. https://doi.org/10.1016/j.aquatox.2013.05.019 PMid:23796537

Libes S.M. 1992. An Introduction to Marine Biogeochemistry. New York, John Wiley and Sons, 734 pp.

Lima M.I.P. de, Santo F.E., Ramos A.M., et al. 2013. Recent changes in daily precipitation and surface air temperature extremes in mainland Portugal, in the period 1941-2007. Atmos. Res. 127: 195-209. https://doi.org/10.1016/j.atmosres.2012.10.001

Luna-Acosta A., Bustamante P., Budzinski H., et al. 2015. Persistent organic pollutants in a marine bivalve on the Marennes-Oléron Bay and the Gironde Estuary (French Atlantic Coast) - part 2: potential biological effects. Sci. Total Environ. 514: 511-522. https://doi.org/10.1016/j.scitotenv.2014.10.050 PMid:25666833

Lushchak V.I. 2011. Environmentally induced oxidative stress in aquatic animals. Aquat. Toxicol. 101: 13-30. https://doi.org/10.1016/j.aquatox.2010.10.006 PMid:21074869

Mantel L.H., Farmer L.L. 1983. Internal Anatomy and Physiological Regulation. In: Mantel L.H. (ed.), The Biology of Crustacea, vol. 5. Academic Press, New York, pp. 54-161.

Marsh J.B., Weinstein D.B. 1966. Simple charring method for determination of lipids. J. Lipid Res. 7: 574-576. PMid:5965305

Matias D., Joaquim S., Ramos M., et al. 2011. Biochemical compounds' dynamics during larval development of the carpet-shell clam Ruditapes decussatus (Linnaeus, 1758): Effects of mono-specific diets and starvation. Helgol. Mar. Res. 65: 369-379. https://doi.org/10.1007/s10152-010-0230-3

Matias D., Joaquim S., Matias A.M., et al. 2013. The reproductive cycle of the European clam Ruditapes decussatus (L., 1758) in two Portuguese populations: Implications for management and aquaculture programs. Aquaculture 406-407: 52-61. https://doi.org/10.1016/j.aquaculture.2013.04.030

McFarland K., Divine J., Volety A. 2011. Influence of acute change salinity on osmolarity of hemolymph in the green mussel, Perna viridis, and the eastern oyster, Crassostrea virginica. J. Shellfish Res. 30: 532.

Mil-Homens M., Vale C., Raimundo J., et al. 2014. Major factors influencing the elemental composition of surface estuarine sediments: The case of 15 estuaries in Portugal. Mar. Pollut. Bull. 84: 135-146. https://doi.org/10.1016/j.marpolbul.2014.05.026 PMid:24933166

Mudge S.M., Bebianno M.J. 1997. Sewage contamination following an accidental spillage in the Ria Formosa, Portugal. Mar. Pollut. Bull. 34: 163-170. https://doi.org/10.1016/S0025-326X(96)00082-3

Newton A., Mudge S.M. 2003. Temperature and salinity regimes in a shallow, mesotidal lagoon, the Ria Formosa, Portugal. Estuar. Coast. Shelf Sci. 57: 73-85. https://doi.org/10.1016/S0272-7714(02)00332-3

Newton A., Icely J.D., Falcão M., et al. 2003. Evaluation of eutrophication in the Ria Formosa coastal lagoon, Portugal. Cont. Shelf Res. 23: 1945-1961. https://doi.org/10.1016/j.csr.2003.06.008

Nicholson S., Lam P.K.S. 2005. Pollution monitoring in Southeast Asia using biomarkers in the mytilid mussel Perna viridis (Mytilidae: Bivalvia). Environ. Int. 31: 121-132. https://doi.org/10.1016/j.envint.2004.05.007 PMid:15607786

Nobre A.M., Ferreira J.G., Newton A., et al. 2005. Management of coastal eutrophication: Integration of field data, ecosystem-scale simulations and screening models. J. Mar. Syst. 56: 375-390. https://doi.org/10.1016/j.jmarsys.2005.03.003

Pacheco L., Vieira A., Ravasco J. 1989. Crescimento e reprodução de Ruditapes decussatus na Ria Formosa (Sul de Portugal). Bentos 6: 129-136.

Raimundo J., Vale C. 2008. Partitioning of Fe, Cu, Zn, Cd, and Pb concentrations among eleven tissues of Octopus vulgaris from the Portuguese coast. Cien. Mar. 34: 297-305.

Raimundo J., Vale C., Caetano M., et al. 2013. Natural trace element enrichment in fishes from a volcanic and tectonically active region (Azores archipelago). Deep Sea Res. Part II Top. Stud. Oceanogr. 98: 137-147. https://doi.org/10.1016/j.dsr2.2013.02.009

Reinfelder J.R., Fisher N.S., Luoma S.N., et al. 1998. Trace element trophic transfer in aquatic organisms: A critique of the kinetic model approach. Sci. Total Environ. 219: 117-135. https://doi.org/10.1016/S0048-9697(98)00225-3

Serafim M.A., Bebianno M.J. 2001. Variation of metallothionein and metal concentrations in the digestive gland of the clam Ruditapes decussatus: sex and seasonal effects. Environ. Toxicol. Chem. 20: 544-552. https://doi.org/10.1897/1551-5028(2001)020<0544:VOMAMC>2.0.CO;2

Shakir F.K., Audilet D., Drake A.J., et al. 1994. A rapid protein determination by modification of the Lowry procedure. Anal. Biochem. 216: 232-233. https://doi.org/10.1006/abio.1994.1031 PMid:8135358

Simões M.de L.S., Vaz M.C.T.A., Silva J.J.R.F. da 1981. Stability constants of chloro-complexes of cadmium(ii) in sea-water medium. Talanta 28: 237-240.

Soares P.M.M., Cardoso R.M., Ferreira J.J., et al. 2015. Climate change and the Portuguese precipitation: ENSEMBLES regional climate models results. Clim. Dyn. 45: 1771-1787. https://doi.org/10.1007/s00382-014-2432-x

Vila-Concejo A., Matias A., Ferreira Ó., et al. 2002. Recent evolution of the natural inlets of a barrier island system in southern Portugal. J. Coast. Res. 752: 741-752.

Viles F.J., Silverman L. 1949. Determination of starch and cellulose with Anthrone. Anal. Chem. 21: 950-953. https://doi.org/10.1021/ac60032a019

Walne P.R. 1976. Experiments on the culture in the sea of the butterfish Venerupis decussata L. Aquaculture 8: 371-381. https://doi.org/10.1016/0044-8486(76)90119-8

Weinberg J.R., Leavitt D.F., Lancaster B.A, et al. 1997. Experimental field studies with Mya arenaria (Bivalvia) on the induction and effect of hematopoietic neoplasia. J. Invertebr. Pathol. 69: 183-194. https://doi.org/10.1006/jipa.1996.4641 PMid:9056469

Windom H.L., Schropp S.J., Calder F.D., et al. 1989. Natural trace metal concentrations in estuarine and coastal marine sediments of the southeastern United States. Environ. Sci. Technol. 23: 314-320. https://doi.org/10.1021/es00180a008

Yatoo M.I., Saxena A., Deepa P.M., et al. 2013. Role of trace elements in animals: a review. Vet. World 6: 963-967. https://doi.org/10.14202/vetworld.2013.963-967



How to Cite

Botelho MJ, Costa ST, Matias D, Soares F, Joaquim S, Vale C. Enhanced trace element concentrations in tissues of the clam Ruditapes decussatus transplanted to areas influenced by human activities (Ria Formosa, Portugal). scimar [Internet]. 2017Jun.30 [cited 2022Sep.27];81(2):229-3. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1704




Most read articles by the same author(s)