Abstract
The response of a laboratory-raised phytoplankton assemblage to copper and zinc enrichment was studied. Higher intracellular accumulation of both the test metals caused disappearance of metal sensitive species, loss of diversity and species richness, reduced growth rate, Chl a and biovolume; however, the community could recover after 14 days of incubation. Cyanobacteria showed marked sensitivity to both the test metals besides some diatoms, such as, Cyclotella meneghiniana and Melosira granulata. Metal enrichment enhanced the relative abundance of species like Scenedesmus quadricauda, Oocystis borgei, Achnanthes exigua, Fragilaria capucina and Nitzschia amphibia, and these were apparently metal tolerant. Cu and Zn stress induces formation of lipid bodies (bigger in size as well as in number) and morphological abnormalities in diatoms. Among these two metals, Cu impact was higher than Zn despite the fact that the intracellular accumulation of Zn was higher than Cu. Deformed raphe and mixed deformities in diatoms were exclusively found under heavy metal stress which was well supported by regression analysis. Finally the present study gives new insight for using diatoms as an effective tool for biomonitoring and biofuel production.
Similar content being viewed by others
Notes
Algal Image database of India (AIDI) (2014) http://indianalgae.co.in.
ANSP Algal Image Database from the phycology Section, Patrick centre for environmental research, The academy of Natural sciences. http://diatom.acnatsci.org/AlgaeImage/.
Guiry MD, Guir GM (2014) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org.
References
Arini A, Durant F, Coste M, Delmas F, Feurtet-Mazel A (2013) Cadmium decontamination and reversal potential of teratological forms of the diatom Planothidium frequentissimum (Bacillariophyceae) after experimental contamination. J Phycol 49(2):361–370
Bere T, Tundisi JG (2012) Cadmium and lead toxicity on tropical freshwater periphyton communities under laboratory-based mesocosm experiments. Hydrobiologia 680:187–197
Biggs BJF, Kilroy C (2000) Stream periphyton monitoring manual. The New Zealand Ministry for the Environment, Christchurch
Cattaneo A, Couillard Y, Wunsam S, Courcelles M (2004) Diatom taxonomic and morphological changes as indicators of metal pollution and recovery in Lac Dufault (Québec, Canada). J Paleolimnol 32:163–175
Cohn SA, Pickett-Heaps JD (1988) The effects of colchicine and dinitrophenol on the in vivo rates of anaphase A and B in the diatom Surirella. Eur J Cell Biol 46:523–530
Cohn SA, Farrell JF, Munro JD, Ragland RL, Weitzell RE Jr, Wibisono BL (2003) The effect of temperature and mixed species composition on diatom motility and adhesion. Diatom Res 18:225–243
Duong TT, Morin S, Herlory O, Feurtet-Mazel A, Coste M, Boudou A (2008) Seasonal effects of cadmium accumulation in periphytic diatom communities of freshwater biofilms. Aquat Toxicol 90:19–28
Einicker-Lamas M, Mezian GA, Fernandes TB, Silva FLS, Guerra F, Miranda K, Attias M, Oliveira MM (2002) Euglena gracilis as a model for the study of Cu2+ and Zn2+ toxicity and accumulation in eukaryotic cells. Environ Pollut 120:779–786
Falasco E, Bona F, Badino G, Hoffmann L, Ector L (2009a) Diatom teratological forms and environmental alterations: a review. Hydrobiologia 623:1–35
Falasco E, Bona F, Ginepro M, Hlúbiková D, Hoffmann L, Ector L (2009b) Morphological abnormalities of diatom silica walls in relation to heavy metal contamination and artificial growth conditions. Water SA 35:595–605
Foster PL (1982a) Species associations and metal contents of algae from rivers polluted by heavy-metals. Freshw Biol 12:17–39
Foster PL (1982b) Metal resistances of Chlorophyta from river polluted by Heavy-metals. Freshwater Biol. 12:41–61
Gächter R, Máreš A (1979) MELIMEX, an experimental heavy metal pollution study: Effects of increased heavy metal loads on phytoplankton communities. Schweiz Z Hydrol 41:228–246
Genter RB (1995) Benthic algal populations respond to aluminum, acid and aluminum-acid mixtures in artificial streams. Hydrobiologia 306:7–19
Gold C, Feurtet-Mazel A, Coste M, Boudou A (2003) Effects of cadmium stress on periphytic diatom communities in indoor artificial streams. Freshw Biol 48:316–328
Guasch H, Paulsson M, Sabater S (2002) Effect of copper on algal communities from oligotrophic calcareous streams. J Phycol 38:241–248
Hildebrand M, Davis AK, Smith SR, Traller JC, Abbriano R (2012) The place of diatoms in the biofuels industry. Biofuels 3:221–240
Hill BH, Williamgham WT, Parrish LP, McFarland BH (2000) Periphyton community responses to elevated metal concentrations in a Rocky Mountain stream. Hydrobiologia 428:161–169
Hillebrand H, Durselen C, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424
Hirst H, Ingrid JU, Jüttner I, Ormerod SJ (2002) Comparing the responses of diatoms and macroinvertebrates to metals in upland streams of Wales and Cornwall. Freshw Biol 47:1752–1765
Ivorra N, Hettelaar J, Kraak MHS, Sabater S, Admiraal W (2002) Responses of biofilms to combined nutrient and metal exposure. Environ Toxicol Chem 21:626–632
Jones GJ, Nichols PD, Johns RB, Smith JD (1987) The effect of mercury and cadmium on the fatty-acid and sterol composition of the marine diatom Asterionella glacialis. Phytochemistry 26:1343–1348
Kumar D, Yadav A, Gaur JP (2012) Growth, composition and metal removal potential of a Phormidium bigranulatum dominated mat at elevated levels of cadmium. Aquat Toxicol 116–117:24–33
Lavoie I, Lavoie M, Fortin C (2012) A mine of information: benthic algal communities as biomonitors of metal contamination from abandoned tailings. Sci Total Environ 425:231–241
Le Faucheur S, Behra R, Sigg L (2005) Thiol and metal contents in periphyton exposed to elevated copper and zinc concentrations: a field and microcosm study. Environ Sci Technol 39:8099–8107
Leland HV, Carter JL (1984) Effects of copper on species composition of periphyton in a Sierra Nevada, California, stream. Freshwater Biol 14:281–296
Liu ZY, Wang GC, Zhou BC (2008) Effect of iron on growth and lipid accumulation in Chlorella vulgaris. Bioresour Technol 99:4717–4722
Loez CR, Topalián ML, Salibián A (1995) Effects of zinc on the structure and growth dynamics of a natural assemblage reared in the laboratory. Environ Pollut 8:275–281
Meador JP, Sibley TH, Swartzman GWL, Taub FB (1998) Copper tolerance by the freshwater algal species Oocystis pusilla and its ability to alter free-ion copper. Aquat Toxicol 44:69–82
Medley CL, Clements WH (1998) Responses of diatom communities to heavy metals in streams: the influence of longitudinal variation. Ecol Appl 8:631–644
Meylan S, Behra R, Sigg L (2004) Influence of metal speciation in natural freshwater on bioaccumulation of copper and zinc in periphyton: a microcosm study. Environ Sci Technol 30:3104
Monteiro M, Oliveira R, Vale C (1995) Metal stress on the plankton communities of Sodo river (Portugal). Water Res 29:695–701
Morin S, Duong TT, Dabrin A, Coynel A, Herlory O, Baudrimont M, Delmas F, Durrieu G, Schäfer J, Winterton P, Blanc G, Coste M (2008a) Long-term survey of heavy-metal pollution, biofilm contamination and diatom community structure in the Riou Mort watershed, South-West France. Environ Pollut 151:532–542
Morin S, Duong TT, Herlory O, Feurtet-Mazel A, Coste M (2008b) Cadmium toxicity and bioaccumulation in freshwater biofilms. Arch Environ Contam Toxicol 5:173–186
Oliveira R (1985) Phytoplankton community response to a mine effluent rich in copper. Hydrobiologia 128:61–69
Pandey LK, Kumar D, Yadav A, Rai J, Gaur JP (2014) Morphological abnormalities in periphytic diatoms as a tool for biomonitoring of heavy metal pollution in a river. Ecol Indic 36:272–279
Pillai S, Behra R, Nestler H, Suter MJF, Sigg L, Schirmer K (2014) Linking toxicity and adaptive responses across the transcriptome, proteome, and phenotype of Chlamydomonas reinhardtii exposed to silver. Proc Natl Acad Sci USA. doi:10.1073/pnas.1319388111
Pinto E, Sigaud-Kutner TCS, Leita˜o MAS, Okamoto OK, Morse D, Colepicolo P (2003) Heavy metal-induced oxidative stress in algae. J Phycol 39:1008–1018
Rai LC, Mallick N (1993) Heavy metal toxicity to algae under synthetic microcosm. Ecotoxicology 2:231–242
Rai PK, Tripathi BD (2008) Heavy metals in industrial wastewater, soil and vegetables in Lohta village, India. Toxicol Environm Chem 90:247–257
Rai LC, Gaur JP, Kumar HD (1981) Phycology and heavy metal pollution. Biol Rev 56:99–151
Rai PK, Mishra A, Tripathi BD (2010) Heavy metal and microbial pollution of the river Ganga: a case study of water quality at Varanasi. Aquat Ecosyst Health Manag 13:352–361
Ramachandra TV, Mahapatra DM, Karthick B, Gordon R (2009) Milking diatoms for sustainable energy: biochemical engineering versus gasoline-secreting diatom solar panels. Ind Eng Chem Res 48:8769–8788
Roig B, Valat C, Behro C, Allan IJ, Guigues N, Mills GA, Ulitzur N, Greenwood R (2007) The use of field studies to establish the performance of a range of tools for monitoring water quality. Trends Anal Chem 8:1243–1251
Ruggiu D, Luglie A, Cattaneo A, Panzani P (1998) Paleoecological evidence for diatom response to metal pollution in lake Orta (N. Italy). J Paleolimnol 20:333–345
Rushforth SR, Brotherson JD, Fungladda N, Evenson WE (1981) The effects of dissolved heavy metals on attached diatoms in the Uintah Basin of Utah, U.S.A. Hydrobiologia 83:313–323
Sabater S (2000) Diatom communities as indicators of environmental stress in the Guadiamar River, S-W. Spain, following a major mine tailings spill. J Appl Phycol 12:113–124
Sabater S, Navarro E, Guasch H (2002) Effects of copper on algal communities at different current velocities. J Appl Phycol 14:391–398
Serra A, Corcoll N, Guasch H (2009) Copper accumulation and toxicity in fluvial periphyton: The influence of exposure history. Chemosphere 74:633–641
Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553
Shehata SA, Lasheen MR, Kobbia IA, Ali GH (1999) Toxic effect of certain metals mixture on some physiological and morphological characteristics of freshwater algae. Water Air Soil Pollut 110:119–135
Sigmon CF, Kania HJ, Beyers RJ (1977) Reductions in biomass and diversity resulting from exposure to mercury in artificial streams. J Fish Res Board Can 34:493–500
Soldo D, Hari R, Sigg L, Behra R (2005) Tolerance of Oocystis nephrocytioides to copper: intracellular distribution and extracellular complexation of copper. Aquat Toxicol 71:307–317
Takamura N, Kasai F, Watanabae MM (1989) Effects of Cu, Cd and Zn on photosynthesis of freshwater benthic algae. J Appl Phycol 1:39–52
Tripathi BN, Singh A, Gaur JP (2000) Impact of heavy metal pollution on algal assemblages. Environ Sci 9:1–7
Tripathi BN, Mehta SK, Amar A, Gaur JP (2006) Oxidative stress in Scenedesmus sp. during short- and long-term exposure to Cu2+ and Zn2+. Chemosphere 62:538–544
Wetzel RG, Likens GE (1979) Limnological analyses. Saunders, Philadelphia
Whitton BA (1970a) Toxicity of heavy metals to Chlorophyta from flowing waters. Arch Mikrobiol 72:553–560
Whitton BA (1970b) Toxicity of heavy metals to freshwater algae: a review. Phykos 9:116–125
Acknowledgments
We thank the Head, Department of Botany, and the coordinator, Centre of Advanced Study in Botany, Banaras Hindu University, for necessary facilities. LKP thanks UGC and CSIR, New Delhi, for financial assistance in the form of SRF. This work was supported by Incheon National University (International Cooperative Research Grant). We are grateful to Dr. J.C. Taylor (North-West University, South Africa) for generous gift of Pleurax.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pandey, L.K., Han, T. & Gaur, J.P. Response of a phytoplanktonic assemblage to copper and zinc enrichment in microcosm. Ecotoxicology 24, 573–582 (2015). https://doi.org/10.1007/s10646-014-1405-5
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-014-1405-5