Abstract
The responses of aquatic organisms to chronic exposure to environmental concentrations of toxicants, often found in mixtures, are poorly documented. Here passive sampler extracts were used in experimental contamination of laboratory channels, to investigate their effects on natural biofilm communities. A realistic mixture of pesticides extracted from Polar Organic Chemical Integrative Samplers was used to expose biofilms in laboratory channels to total pesticide concentrations averaging 0.5 ± 0.1 μg l−1. The level of exposure was representative of field conditions in terms of relative proportions of the substances but the exposure concentration was not maintained (decreasing concentrations between contamination occasions). The impact on the structural as well as the functional characteristics of the autotrophic and heterotrophic components was determined, using biofilm grown in uncontaminated conditions (reference site) and in sites exposed to pesticides (contaminated site). The exposure imposed did not significantly modify the structure or functions of reference biofilms, nor did it modify tolerance as measured by mixture EC50 (EC50 mix). In contrast, the communities from the more contaminated downstream section lost tolerance following decreased dose exposure, but community composition remained fairly stable. Overall, these results indicate that low levels of contamination did not lead to strong changes in community structure, and 14-day changes in tolerance seemed to depend mainly on physiological adaptation, suggesting that other environmental factors or longer-lasting processes prevailed. This study reports the first attempt to use passive sampler extracts as a realistic composite contaminant for experimental exposure of biofilms, with promising perspectives in further ecotoxicology studies.
Similar content being viewed by others
References
Aldén Demoling L, Bååth E (2008) No long-term persistence of bacterial Pollution-Induced Community tolerance in tylosin-polluted soil. Environ Sci Technol 42(18):6917–6921. doi:10.1021/es8004706
Alvarez DA, Petty JD, Huckins JN, Jones-Lepp TL, Getting DT, Goddard JP, Manahan SE (2004) Development of a passive, in situ, integrative sampler for hydrophilic organic contaminants in aquatic environments. Environ Toxicol Chem 23(7):1640–1648
Artigas J, Arts G, Babut M, Caracciolo AB, Charles S, Chaumot A, Combourieu B, Dahllöf I, Despréaux D, Ferrari B, Friberg N, Garric J, Geffard O, Gourlay-Francé C, Hein M, Hjorth M, Krauss M, De Lange HJ, Lahr J, Lehtonen KK, Lettieri T, Liess M, Lofts S, Mayer P, Morin S, Paschke A, Svendsen C, Usseglio-Polatera P, van den Brink N, Vindimian E, Williams R (2012) Towards a renewed research agenda in ecotoxicology. Environ Pollut 160:201–206
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59(1):89–113. doi:10.1146/annurev.arplant.59.032607.092759
Blanck H, Wängberg SA, Molander S (1988) Pollution-Induced Community tolerance: a new ecotoxicological tool. In: Cairns J Jr., Pratt JR (eds) Functional testing of aquatic biota for estimating hazards of chemicals. American Society for Testing and Materials, Philadelphia, pp 219–230
Chèvre N, Loepfe C, Singer H, Stamm C, Fenner K, Escher BI (2006) Including mixtures in the determination of water quality criteria for herbicides in surface water. Environ Sci Technol 40(2):426–435. doi:10.1021/es050239l
Choubert J-M, Martin-Ruel S, Coquery M (2009) Prélèvement et échantillonnage des substances prioritaires et émergentes dans les eaux usées. Les prescriptions techniques du projet de recherche AMPERES. Tech Sci Méthodes 4:88–101
Dorigo U, Leboulanger C, Bérard A, Bouchez A, Humbert JF, Montuelle B (2007) Lotic biofilm community structure and pesticide tolerance along a contamination gradient in a vineyard area. Aquat Microb Ecol 50:91–102
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(1):19–28
Escher BI, Quayle P, Muller R, Schreiber U, Mueller JF (2006) Passive sampling of herbicides combined with effect analysis in algae using a novel high-throughput phytotoxicity assay (Maxi-Imaging-PAM). J Environ Monit 8(4):456–464
Forbes VE, Palmqvist A, Bach L (2006) The use and misuse of biomarkers in ecotoxicology. Environ Toxicol Chem 25(1):272–280. doi:10.1897/05-257r.1
Geiszinger A, Bonnineau C, Faggiano L, Guasch H, López-Doval JC, Proia L, Ricart M, Ricciardi F, Romaní A, Rotter S, Muñoz I, Schmitt-Jansen M, Sabater S (2009) The relevance of the community approach linking chemical and biological analyses in pollution assessment. Trends Anal Chem 28(5):619–626
Guasch H, Navarro E, Serra A, Sabater S (2004) Phosphate limitation influences the sensitivity to copper in periphytic algae. Freshwat Biol 49(4):463–473
Helsel DR (1990) Less than obvious—statistical treatment of data below the detection limit. Environ Sci Technol 24(12):1766–1774. doi:10.1021/es00082a001
Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314
Knauert S (2008) Toxicity of pesticides and their mixture to primary producers. PhD thesis, Philosophish-Naturwissenschaftlichen Fakultät, Universität Basel
Knauert S, Escher B, Singer H, Hollender J, Knauer K (2008) Mixture toxicity of three photosystem II inhibitors (atrazine, isoproturon, and diuron) toward photosynthesis of freshwater phytoplankton studied in outdoor mesocosms. Environ Sci Technol 42(17):6424–6430. doi:10.1021/es072037q
Krammer K, Lange-Bertalot H (1986–1991) Bacillariophyceae 1. Teil: Naviculaceae. p 876; 2. Teil: Bacillariaceae, Epithemiaceae, Surirellaceae, p 596; 3. Teil: Centrales, Fragilariaceae, Eunotiaceae, p 576; 4. Teil: Achnanthaceae. Kritische Ergänzungen zu Navicula (Lineolatae) und Gomphonema. p 437, vol Band 2/1-4. Süßwasserflora von Mitteleuropa. G. Fischer Verlag, Stuttgart
Laviale M, Morin S, Créach A (2011) Short term recovery of periphyton photosynthesis after pulse exposition to the photosystem II inhibitors atrazine and isoproturon. Chemosphere 84(5):731–734
Lissalde S, Mazzella N, Fauvelle V, Delmas F, Mazellier P, Legube B (2011) Liquid chromatography coupled with tandem mass spectrometry method for thirty-three pesticides in natural water and comparison of performance between classical solid phase extraction and passive sampling approaches. J Chromatogr A 1218(11):1492–1502
Mazzella N, Dubernet J-F, Delmas F (2007) Determination of kinetic and equilibrium regimes in the operation of polar organic chemical integrative samplers: application to the passive sampling of the polar herbicides in aquatic environments. J Chromatogr A 1154(1–2):42–51
Mazzella N, Lissalde S, Moreira S, Delmas F, Mazellier P, Huckins JN (2010) Evaluation of the use of performance reference compounds in an Oasis-HLB adsorbent based passive sampler for improving water concentration estimates of polar herbicides in freshwater. Environ Sci Technol 44(5):1713–1719. doi:10.1021/es902256m
McCune B, Mefford MJ (1999) Multivariate analysis of ecological data, version 4.01. MJM Software, Gleneden Beach, Oregon USA
Montuelle B, Dorigo U, Bérard 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 Ardières-Morcille experimental watershed (France). Hydrobiologia 1–19. doi:10.1007/s10750-010-0105-2
Morin S, Duong TT, Herlory O, Feurtet-Mazel A, Coste M (2008) Cadmium toxicity and bioaccumulation in freshwater biofilms. Arch Environ Contam Toxicol 54(2):173–186
Morin S, Pesce S, Tlili A, Coste M, Montuelle B (2010a) Recovery potential of periphytic communities in a river impacted by a vineyard watershed. Ecol Indic 10(2):419–426
Morin S, Proia L, Ricart M, Bonnineau C, Geiszinger A, Ricciardi F, Guasch H, Romaní A, Sabater S (2010b) Effects of a bactericide on the structure and survival of benthic diatom communities. Vie Milieu 60(2):107–114
Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2010) vegan: community ecology package. R package version 1.17-2. http://CRAN.R-project.org/package=vegan
Pesce S, Margoum C, Montuelle B (2010) In situ relationships between spatio-temporal variations in diuron concentrations and phototrophic biofilm tolerance in a contaminated river. Water Res 44(6):1941–1949
Pesce S, Morin S, Lissalde S, Montuelle B, Mazzella N (2011) Combining polar organic chemical integrative samplers (POCIS) with toxicity testing to evaluate pesticide mixture effects on natural phototrophic biofilms. Environ Pollut 159(3):735–741
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core team (2009) nlme: linear and nonlinear mixed effects models. R package version 3.1-96
Plan Ecophyto (2018) de Réduction des Usages de Pesticides 2008–2018. http://agriculture.gouv.fr/IMG/pdf/PLAN_ECOPHYTO_2018-2-2.pdf. Accessed 20 April 2012
Rabiet M, Margoum C, Gouy V, Carluer N, Coquery M (2010) Assessing pesticide concentrations and fluxes in the stream of a small vineyard catchment: effect of sampling frequency. Environ Pollut 158(3):737–748
Relyea R, Hoverman J (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9(10):1157–1171. doi:10.1111/j.1461-0248.2006.00966.x
Ricart M, Barceló D, Geiszinger A, Guasch H, Alda MLd, Romaní AM, Vidal G, Villagrasa M, Sabater S (2009) Effects of low concentrations of the phenylurea herbicide diuron on biofilm algae and bacteria. Chemosphere 76(10):1392–1401
Riedl J, Altenburger R (2007) Physicochemical substance properties as indicators for unreliable exposure in microplate-based bioassays. Chemosphere 67(11):2210–2220
Schmitt-Jansen M, Altenburger R (2008) Community-level microalgal toxicity assessment by multiwavelength-excitation PAM fluorometry. Aquat Toxicol 86(1):49–58
Schmitt-Jansen M, Veit U, Dudel G, Altenburger R (2008) An ecological perspective in aquatic ecotoxicology: approaches and challenges. Basic Appl Ecol 9(4):337–345
Shaw M, Negri A, Fabricius K, Mueller JF (2009) Predicting water toxicity: pairing passive sampling with bioassays on the Great Barrier Reef. Aquat Toxicol 95(2):108–116
Tlili A, Bérard A, Roulier J-L, Volat B, Montuelle B (2010) PO4 3− dependence of the tolerance of autotrophic and heterotrophic biofilm communities to copper and diuron. Aquat Toxicol 98(2):165–177
Tlili A, Montuelle B (2011) Microbial Pollution-Induced Community tolerance. In: Amiard-Triquet C, Rainbow PS, Roméo M (eds) Tolerance to environmental contaminants. CRC Press, Boca Raton, pp 85–108
Tlili A, Marechal M, Montuelle B, Volat B, Dorigo U, Bérard A (2011) Use of the MicroResp(TM) method to assess pollution-induced community tolerance to metals for lotic biofilms. Environ Pollut 159(1):18–24
Ylla I, Borrego C, Romaní AM, Sabater S (2009) Availability of glucose and light modulates the structure and function of a microbial biofilm. FEMS Microbiol Ecol 69(1):27–42. doi:10.1111/j.1574-6941.2009.00689.x
Zabiegała B, Kot-Wasik A, Urbanowicz M, Namieśnik J (2010) Passive sampling as a tool for obtaining reliable analytical information in environmental quality monitoring. Anal Bioanal Chem 396(1):273–296. doi:10.1007/s00216-009-3244-4
Acknowledgments
The French National Office for the Aquatic Environment (ONEMA-CEMAGREF agreement, action 26) and the Cemagref’s “PestExpo” Research Program provided financial support for this experiment. The authors thank Marjorie Maréchal, Bernard Motte, Cécile Nassiet, Christophe Rosy, Bernadette Volat and Josiane Gahou for technical help.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Morin, S., Pesce, S., Kim-Tiam, S. et al. Use of polar organic chemical integrative samplers to assess the effects of chronic pesticide exposure on biofilms. Ecotoxicology 21, 1570–1580 (2012). https://doi.org/10.1007/s10646-012-0910-7
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-012-0910-7