Abstract
Pollution-induced community tolerance (PICT) approaches involve comparing tolerance levels of natural communities to a particular contaminant or a contaminant mixture using short-term toxicity tests performed under controlled conditions. However, results from toxicity tests can be modulated by various environmental and experimental conditions, raising questions about their reproducibility and comparability. In this context, the present study aimed to determine the influence of exposure duration, periphyton suspension concentration, and periphyton maturation stage on the measurement of short-term effects of copper on phototrophic periphyton communities. Our results showed the very weak influence of exposure duration in the tested range (2–6 h) on toxicity level, whereas periphyton biomass in the tested suspension (in terms of both chlorophyll a concentrations and dry weight), proved a crucial determinant in toxicity assessment. Results also highlighted the potential tolerance increase with the periphyton maturation stage. This parameter conditioned the positive linear relationship between tolerance level and periphyton suspension concentration, leading to an increase in the linear regression slope with the maturation stage. This suggests that such a relationship is probably highly periphyton-dependent. Consequently, to enable data toxicity comparisons, an a priori normalization of the periphyton suspension biomass is necessary, and PICT approaches require the use, as much of possible, of periphyton with similar maturation stage. Finally, the present study clearly shows that a better standardization of PICT approaches could help to improve reproducibility. It could thus facilitate the comparison of tolerance levels measured in the same study (e.g., spatial and/or temporal and/or inter-treatment comparison) as well as the comparison obtained from different experimental and in situ research.
Similar content being viewed by others
References
Ahuja P, Gupta R, Saxena RK (1999) Zn2+ biosorption by Oscillatoria anguistissima. Process Biochem 34:77–85
Barranguet C, Charantoni E, Plans M, Admiraal W (2000) Short-term response of monospecific and natural algal biofilms to copper exposure. Eur J Phycol 35:397–406
Barranguet C, Plans M, van der Grinten E, Sinke JJ, Admiraal W (2002) Development of photosynthetic periphyton affected by dissolved and sorbed copper in a eutrophic river. Environ Toxicol Chem 21:1955–1965
Berard A, Dorigo U, Mercier I, Becker-van Slooten K, Grandjean D, Leboulanger C (2003) Comparison of the ecotoxicological impact of the triazines Irgarol 1051 and atrazine on microalgal cultures and natural microalgal communities in Lake Geneva. Chemosphere 53:935–944
Blanck H (2002) A critical review of procedures and approaches used for assessing pollution-induced community tolerance (PICT) in biotic communities. Hum Ecol Risk Assess 8:1003–1034
Blanck H, Dahl B (1996) Pollution-induced community tolerance (PICT) in marine periphyton in a gradient of tri-n-butyltin (TBT) contamination. Aquat Toxicol 3:59–77
Blanck H, Wängberg SA, Molander S (1988) Pollution-induced community tolerance – A new ecotoxicological tool. In: Cairns J, Pratt JR (eds) Functional testing of aquatic biota for estimating hazards of chemicals, Vol STP 988. American Society for Testing and Materials, Philadelphia, pp 219–230
Blanck H, Admiraal W, Cleven RFMJ, Guasch H, van den Hoop MAGT, Ivorra N, Nystrom B, Paulsson M, Petterson RP, Sabater S, Tubbing GMJ (2003) Variability in zinc tolerance, measured as incorporation of radio-labeled carbon dioxide and thymidine, in periphyton communities sampled from 15 European river stretches. Arch Environ Con Tox 44:17–29
Boivin MY, Massieux B, Breure AM, van den Ende FP, Greve GD, Rutgers M, Admiraal W (2005) Effects of copper and temperature on aquatic bacterial communities. Aquat Toxicol 71:345–356
Dahl B, Blanck H (1996) Toxic effects of the antifouling agent Irgarol 1051 on periphyton communities in coastal water microcosms. Mar Pollut Bull 32:342–350
Dorigo U, Bérard A, Rimet F, Bouchez A, Montuelle B (2010) In situ assessment of periphyton recovery in a river contaminated by pesticides. Aquat Toxicol 98:396–406
Duong TT, Morin S, Coste M, Herlory O, Feurtet-Mazel A, Boudou A (2010) Experimental toxicity and bioaccumulation of cadmium in freshwater periphytic diatoms in relation with periphyton maturity. Sci Total Environ 408:552–562
Eklund BT, Kautsky L (2003) Review on toxicity testing with marine macroalgae and the need for method standardization—exemplified with copper and phenol. Mar Pollut Bull 46:171–181
Fechner LC, Gourlay-France C, Uher E, Tusseau-Vuillemin MH (2010) Adapting an enzymatic toxicity test to allow comparative evaluation of natural freshwater periphyton’ tolerance to metals. Ecotoxicology 19:1302–1311
Fechner LC, Dufour M, Gourlay-France C (2012) Pollution-induced community tolerance of freshwater periphyton: measuring heterotrophic tolerance to Pb using an enzymatic toxicity test. Ecotoxicology 21:2123–2131
Gold C, Feurtet-Mazel A, Coste M, Boudou A (2003a) Effects of cadmium stress on periphytic diatom communities in indoor artificial streams. Freshwater Biol 48:316–328
Gold C, Feurtet-Mazel A, Coste M, Boudou A (2003b) Impacts of Cd and Zn on the development of periphytic diatom communities in artificial streams located along a river pollution gradient. Arch Environ Con Tox 44:189–197
Guasch H, Admiraal W, Sabater S (2003) Contrasting effects of organic and inorganic toxicants on freshwater periphyton. Aquat Toxicol 64:165–175
Guasch H, Navarro E, Serra A, Sabater S (2004) Phosphate limitation influences the sensitivity to copper in periphytic algae. Freshwater Biol 49:463–473
Gustavson K, Petersen S, Pedersen B, Stuer-Lauridsen F, Pedersen S, Wangberg SA (1999) Pollution-induced community tolerance (PICT) in coastal phytoplankton communities exposure to copper. Hydrobiologia 416:125–138
Hjorth M, Dahllof I, Forbes VE (2006) Effects on the function of three trophic levels in marine plankton communities under stress from the antifouling compound zinc pyrithione. Aquat Toxicol 77:105–115
Imfeld G, Vuilleumier S (2012) Measuring the effects of pesticides on bacterial communities in soil: a critical review. Eur J Soil Biol 49:22–30
Ivorra N, Bremer S, Guasch H, Kraak MHS, Admiraal W (2000) Differences in the sensitivity of benthic microalgae to Zn and Cd regarding periphyton development and exposure history. Environ Toxicol Chem 19:1332–1339
Kim Tiam S, Morin S, Pesce S, Feurtet-Mazel A, Moreira A, Gonzalez P, Mazzella N (2014) Environmental effects of realistic pesticide mixtures on natural periphyton communities with different exposure histories. Sci Total Environ 473:496–506
Knopper LD, Siciliano SD (2002) A hypothetical application of the pollution-induced community tolerance concept in megafaunal communities found at contaminated sites. Hum Ecol Risk Assess 8:1057–1066
Lambert AS, Morin S, Artigas J, Volat B, Coquery M, Neyra M, Pesce S (2012) Structural and functional recovery of microbial periphyton after a decrease in copper exposure: influence of the presence of pristine communities. Aquat Toxicol 109:118–126
Millward RN, Grant A (2000) Pollution‐induced tolerance to copper of nematode communities in the severely contaminated restronguet creek and adjacent estuaries, Cornwall, United Kingdom. Environ Toxicol Chem 19:454–461
Monteiro CM, Castro PML, Malcata FX (2012) Metal uptake by microalgae: underlying mechanisms and practical applications. Biotechnol Progr 28:299–311
Montuelle B, Dorigo U, Berard A, Volat B, Bouchez A, Tlili A, Gouy V, Pesce S (2010) The periphyton as a multimetric bioindicator for assessing the impact of land use on rivers: an overview of the ArdiSres-Morcille experimental watershed (France). Hydrobiologia 657:123–141
Moreno-Garrido I, González-Delvalle M, Lubián LM (1997) Acumulación de cobre en microalgas usadas en acuicultura. Actas del VII Seminario de Químmica Marina, Servicio de Publicaciones de la Universidad de Cádiz: 279–286
Moreno-Garrido I, Lubián LM, Soares AMVM (2000) Influence of cellular density on determination of EC50 in microalgal growth inhibition tests. Ecotox Environ Safe 47:112–116
Morin S, Pesce S, Tlili A, Coste M, Montuelle B (2010) Recovery potential of periphytic communities in a river impacted by a vineyard watershed. Ecol Indic 10:419–426
Niklinska M, Chodak M, Laskowski R (2006) Pollution-induced community tolerance of microorganisms from forest soil organic layers polluted with Zn or Cu. Appl Soil Ecol 32:265–272
Pesce S, Margoum C, Montuelle B (2010) In situ relationships between spatio-temporal variations in diuron concentrations and phototrophic periphyton tolerance in a contaminated river. Water Res 44:1941–1949
Peterson CG, Stevenson RJ (1989) Substratum conditioning and diatom colonization in different current regimes. J Phycol 25:790–793
Potapova M, Charles DF (2005) Choice of substrate in algae-based water-quality assessment. J N Am Benthol Soc 24:415–427
Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22
R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing: Vienna. http://www.R-project.org
Sabater S, Guasch H, Ricart M, Romani A, Vidal G, Klunder C, Schmitt-Jansen M (2007) Monitoring the effect of chemicals on biological communities. The periphyton as an interface. Anal Bioanal Chem 387:1425–1434
Schelske C (1984) In situ and natural phytoplankton assemblage bioassays. Algae as ecological indicators. Academic, New York 1984: 15–47, 6 fig, 106 ref
Schmitt-Jansen M, Veit U, Dudel G, Altenburger R (2008) An ecological perspective in aquatic ecotoxicology: approaches and challenges. Basic Appl Ecol 9:337–345
Schreiber U, Muller JF, Haugg A, Gademann R (2002) New type of dual-channel PAM chlorophyll fluorometer for highly sensitive water toxicity biotests. Photosynth Res 74:317–330
Serra A, Guasch H (2009) Effects of chronic copper exposure on fluvial systems: linking structural and physiological changes of fluvial periphyton with the in-stream copper retention. Sci Total Environ 407:5274–5282
Soldo D, Behra R (2000) Long-term effects of copper on the structure of freshwater periphyton communities and their tolerance to copper, zinc, nickel and silver. Aquat Toxicol 47:181–189
Steemann NE, Wium-Andersen S (1970) Copper ions as poison in the sea and in freshwater. Mar Biol 6:93–97
Tien CJ, Chen CS (2013) Patterns of metal accumulation by natural river periphyton during their growth and seasonal succession. Arch Environ Con Tox 64:605–616
Tlili A, Montuelle B (2011) Microbial pollution-induced community tolerance. Tolerance to environmental contaminants. CRC, Boca Raton, pp 85–108
Tlili A, Berard A, Roulier JL, Volat B, Montuelle B (2010) PO4 3− dependence of the tolerance of autotrophic and heterotrophic periphyton communities to copper and diuron. Aquat Toxicol 98:165–177
Tlili A, Corcoll N, Bonet B, Morin S, Montuelle B, Berard A, Guasch H (2011) In situ spatio-temporal changes in pollution-induced community tolerance to zinc in autotrophic and heterotrophic periphyton communities. Ecotoxicology 20:1823–1839
Tobar, JL, Boubeta-Novas J, Arredondo-Vega BO, FábregasJ (1993) Incorporación de cobre en la microalga marina Tetraselmis suecica en función de su concentración en el medio. Actas III Congreso Latinoamericano de Ficología
Acknowledgments
We thank ATT for English-language editing. We also thank Bernard Motte, Christophe Rosy, and Bernadette Volat for technical support, and Irstea’s Water Chemistry Laboratory (LAMA). This study was partially funded by the French National Research Agency (project ANR-CESA-Potomac 2012–2015).
Author information
Authors and Affiliations
Corresponding author
Additional information
Responsible editor: Philippe Garrigues
Rights and permissions
About this article
Cite this article
Lambert, A.S., Pesce, S., Foulquier, A. et al. Improved short-term toxicity test protocol to assess metal tolerance in phototrophic periphyton: toward standardization of PICT approaches. Environ Sci Pollut Res 22, 4037–4045 (2015). https://doi.org/10.1007/s11356-014-3505-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-014-3505-4