Abstract
This work reports changes of Cr, Cu, Zn, Cd, Hg and Pb concentrations in the dissolved fraction, suspended particulate matter and immobilised Phaeodactylum tricornutum Bohlin (Bacillariophyceae), as well as of microalgae specific growth rates, during a 5-month period dredging operation in a contaminated area of the Tagus estuary, Portugal. Trace element concentrations showed broad variations in the dissolved fraction and suspended particulate matter, presumably reflecting rapid exchanges of redox-sensitive elements between water and particles, in conjunction with the dilution effect caused by the tidal excursion. Immobilised cells exposed to dredging environmental conditions showed significantly higher concentrations of Cr, Cu, Zn, Cd, Hg and Pb than under no dredging conditions. Concomitantly, specific cell growth was significantly lower, suggesting that elements released with dredging affect the microalgae physiology. The results obtained in this in situ work imply that the dissolved fraction and the suspended particulate matter are relatively ineffective indicators of the trace element enhancement during dredging and pointed out immobilised P. tricornutum as a reliable and efficient biomonitoring tool for the assessment of trace element remobilisation.
Similar content being viewed by others
References
Anderson DM, Morel FMM (1978) Copper sensitivity of Gonyaulax tamarensis. Limnol Oceanogr 23:283–295
Bozeman J, Koopman B, Bitton G (1989) Toxicity testing using immobilized algae. Aquat Toxicol 14:345–352
Brand LE, Sunda WG, Guillard RRL (1986) Reduction of marine phytoplankton reproduction rates by copper and cadmium. J Exp Mar Biol Ecol 96:225–250
Cabrita MT, Raimundo J, Pereira P, Vale C (2013) Optimizing alginate beads for the immobilisation of Phaeodactylum tricornutum in estuarine waters. Mar Environ Res 87–88:37–43
Caçador I, Vale C, Catarino F (1996) Accumulation of Zn, Pb, Cu, Cr and Ni in sediments between roots of the Tagus Estuary salt marshes, Portugal. Estuar Coast Shelf Sci 42(3):393–403
Caetano M, Madureira MJ, Vale C (2003) Metal remobilisation during resuspension of anoxic contaminated sediment: short-term laboratory study. Water Air Soil Pollut 143:23–40
Caetano M, Fonseca N, Cesário R, Vale C (2007) Mobility of Pb in salt marshes recorded by total content and stable isotopic signature. Sci Total Environ 380(1–3):84–92
Canário J, Vale C, Caetano M (2005) Distribution of monomethyl mercury and mercury in surface sediments of the Tagus Estuary (Portugal). Mar Pollut Bull 50:1142–1145
Cotté-Krieff M-H, Guieu C, Thomas AJ, Martin J-M (2000) Sources of Cd, Cu, Ni and Zn in Portuguese coastal waters. Mar Chem 71:199–214
Cundy AB, Croudace IW, Cearreta A, Irabien MJ (2003) Reconstructing historical trends in metal input in heavily-disturbed, contaminated estuaries: studies from Bilbao, Southampton Water and Sicily. Appl Geochem 18:311–325
de Bettencourt AMM (1988) On arsenic speciation in the Tagus Estuary. Neth J Sea Res 22(3):205–212
De Filippis LF (1979) The effect of heavy metal compounds on the permeability of Chlorella cells. Z Pflanzenphysiol 92:39–49
Dortch Q, Whitledge TE (1992) Does nitrogen or silicon limit phytoplankton production in the Mississippi River plume and nearby regions? Cont Shelf Res 12:1293–1309
Eggleton J, Thomas KV (2004) A review of factors affecting the release and bioavailability of contaminants during sediment disturbance events. Environ Int 30:973–980
EPA (2002) Method 1631, Revision E: mercury in water by oxidation, purge and trap, and cold vapor atomic fluorescence spectrometry. EPA-821-R-02-019. US Environmental Protection Agency, Office of Water
Fisher NS, Bohé M, Teyssié J-L (1984) Accumulation and toxicity of Cd, Zn, Ag, and Hg in four marine phytoplankters. Mar Ecol Prog Ser 18:201–213
Förstner U, Wittmann GTW (1979) Metal pollution in the aquatic environment. Springer, Berlin
González-Dávila M (1995) The role of phytoplankton cells on the control of heavy metal concentration in seawater. Mar Chem 48(3–4):215–236
Grasshoff K, Ehrhardt M, Kremling M (1983) Methods of seawater analysis. Chemie, Weinheimer
Guillard RRL, Ryther JH (1962) Studies on marine planktonic diatoms, I. Cyclotella nana Hustedt and Detonula confervaceae (Cleve) Gran. Can J Microbiol 8(2):229–239
Hampel M, Canário J, Branco V, Vale C, Blasco J (2009) Environmental levels of linear alkylbenzene sulfonates (LAS) in sediments from the Tagus estuary (Portugal): environmental implications. Environ Monit Assess 149:151–161
Hertzberg S, Jensen A (1989) Studies of alginate-immobilized marine microalgae. Bot Mar 32(4):267–273
Horvatić J, Peršić V (2007) The effect of Ni2+, Co2+, Zn2+, Cd2+ and Hg2+ on the growth rate of marine diatom Phaeodactylum tricornutum Bohlin: microplate growth inhibition test. B Environ Contam Toxicol 79:494–498
Kennish MJ (2002) Environmental threats and environmental future of estuaries. Environ Conserv 29:78–107
Kenny AJ, Rees HL (1994) The effects of marine gravel extraction on the macrobenthos early post-dredging recolonization. Mar Pollut Bull 28:442–447
Küpper H, Setlik I, Spiller M, Küpper FC, Prasil O (2002) Heavy-metal-induced inhibition of photosynthesis: targets of in vivo heavy metal chlorophyll formation. J Phycol 38:429–441
Luoma SN, Bryan GW, Langston WJ (1982) Scavenging of heavy metals from particulates by brown seaweeds. Mar Pollut Bull 13:394–396
Maciorowski AF, Little LW, Sims RC, Sims JL (1983) Bioassays: procedures and results. J Water Pollut Con F 55(6):801–816
Marques CR, Pereira R, Antunes SC, Cachada A, Duarte AC, Gonçalves F (2011) In situ aquatic bioassessment of pesticides applied on rice fields using a microalga and daphnids. Sci Total Environ 409(18):3375–3385
Meeravali NN, Kumar SJ (2000) Comparison of open microwave digestion and digestion by conventional heating for the determination of Cd, Cr, Cu and Pb in algae using transverse heated electrothermal atomic absorption spectrometry. Fresenius J Anal Chem 366(3):313–315
Moreira dos Santos M, Moreno-Garrido I, Gonçalves F, Soares AMVM, Ribeiro R (2002) An in situ bioassay for estuarine environments using the microalga Phaeodactylum tricornutum. Environ Toxicol Chem 21(3):567–574
Moreira SM, Moreira-Santos M, Guilhermino L, Ribeiro R (2006) Immobilization of the marine microalga Phaeodactylum tricornutum in alginate for in situ experiments: bead stability and suitability. Enzym Microbiol Technol 38(1–2):135–141
Nayar S, Goh BPL, Chou LM (2004) Environmental impact of heavy metals from dredged and resuspended sediments on phytoplankton and bacteria assessed in in situ mesocosms. Ecotoxicol Environ Saf 59:349–369
Newell RC, Seiderer LJ, Hitchcock DR (1998) The impact of dredging works in coastal waters: a review of the sensitivity to disturbance and subsequent recovery of biological resources on the seabed. Oceanogr Mar Biol Annu Rev 36:127–178
Nogueira JFM, Simplício B, Florêncio MH, Bettencourt AMM (2003) Levels of tributyltin in sediments from the Tagus estuary. Nature Reserve Estuaries 26(3):798–802
Nriagu JO (1990) Global metal pollution—poisoning the biosphere? Environment 32:7–33
Nyholm N, Källqvist T (1989) Methods for growth inhibition toxicity tests with freshwater algae. Environ Toxicol Chem 8(8):689–703
Pan K, Wang W-X (2012) Trace metal contamination in estuarine and coastal environments in China. Sci Total Environ 421–422:3–16
Polkowska-Motrenko H, Danko B, Dybczyński R, Koster-Ammerlaan A, Bode P (2000) Effect of acid digestion method on cobalt determination in plant materials. Anal Chim Acta 408(1–2):89–95
Rainbow PS (2006) Biomonitoring of trace metals in estuarine and marine environments. Australas J Ecotoxicol 12:107–122
Ricard M (1987) Atlas du Phytoplancton Marin, Diatomophycees, volume 2. Centre National de la Recherche Scientifique, Paris, France
Shaw AJ (1990) Heavy metal tolerance in plants: evolutionary aspects. CRC, Boca Raton, FL
Sicko-Goad LM, Schelske CL, Stoermer EF (1984) Estimation of intracellular carbon and silica content of diatoms from natural assemblages using morphometric techniques. Limnol Oceanogr 29(6):1170–1178
Sunda WG, Huntsman SA (1998) Processes regulating cellular metal accumulation and physiological effects: phytoplankton as model systems. Sci Total Environ 219(2–3):165–181
Thomas WH, Hollibaugh JT, Seibert DLR, Wallace GT Jr (1980) Toxicity of a mixture of ten metals to phytoplankton. Mar Ecol Prog Ser 2:213–220
Twist H, Edwards AC, Codd GA (1997) A novel in situ biomonitor using alginate immobilised algae (Scenedesmus subspicatus) for the assessment of eutrophication in flowing surface waters. War Res 31(8):2066–2072
Uncles RJ, Stephens JA, Law DJ (2006) Turbidity maximum in the macrotidal, highly turbid Humber Estuary, UK: flocs, fluid mud, stationary suspensions and tidal bores. Estuar Coast Shelf Sci 67(1–2):30–52
Vale C (1990) Temporal variations of particulate metals in the Tagus River Estuary. Sci Total Environ 97(98):137–154
Vale C, Sundby B (1987) Suspended sediment fluctuations in the Tagus estuary on semi-diurnal and fortnightly time scales. Estuar Coast Shelf Sci 25(5):495–508
Vale C, Ferreira A, Micaelo C, Caetano M, Pereira E, Madureira MJ, Ramalhosa E (1998) Mobility of contaminants in relation to dredging operations in a mesotidal estuary (Tagus estuary, Portugal). Water Sci Technol 37:25–31
Vale C, Canário J, Caetano M, Lavrado J, Brito P (2008) Estimation of the anthropogenic fraction of elements in surface sediments of the Tagus Estuary (Portugal). Mar Pollut Bull 56(7):1364–1367
Windom HL, Schropp SJ, Calder FD, Ryan JD, Smith RG, Burney LC, Lewis FG, Rawlinson CH (1989) Natural trace metal concentrations in estuarine and coastal marine sediments of the south eastern United States. Environ Sci Technol 23(3):314–320
Zhang H, Davison W (1999) Diffusional characteristics of hydrogels used in DGT and DET techniques. Anal Chim Acta 398:329–340
Zhou Q, Zhang J, Fu J, Shi J, Jiang G (2008) Biomonitoring: an appealing tool for assessment of metal pollution in the aquatic ecosystem. Anal Chim Acta 606:135–150
Acknowledgments
Maria Teresa Cabrita, Joana Raimundo and Patrícia Pereira acknowledge the grants by “Fundação para a Ciência e a Tecnologia” (FCT, grant nos SFRH/BPD/50348/2009, SFRH/BPD/91498/2012 and SFRH/BPD/69563/2010, respectively). Joana Raimundo also acknowledge grant within the Project “FP7-CoExist—Aquaculture and fisheries in the coastal zone”. We appreciate the collaboration of Rui Silva in the field work and assistance of Margarida Muro and Leonor Cavalinhos for microalgae culture maintenance.
Author information
Authors and Affiliations
Corresponding author
Additional information
Resposible editor: Gerald Thouand
Rights and permissions
About this article
Cite this article
Cabrita, M.T., Raimundo, J., Pereira, P. et al. Immobilised Phaeodactylum tricornutum as biomonitor of trace element availability in the water column during dredging. Environ Sci Pollut Res 21, 3572–3581 (2014). https://doi.org/10.1007/s11356-013-2362-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-013-2362-x