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Pollution-induced community tolerance (PICT) as a tool for monitoring Lake Geneva long-term in situ ecotoxic restoration from herbicide contamination

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Abstract

Chemical monitoring revealed a regular decrease in herbicide concentration in Lake Geneva since last decades that may be linked to an ecotoxic restoration of nontarget phytoplanktonic communities. The Pollution-induced community tolerance (PICT) approach was tested as a tool to monitor the ecotoxic restoration of Lake Geneva for herbicides from 1999 to 2011. We conducted monthly assessments in 1999 and in 2011 for the tolerance of the phytoplankton communities to two herbicides (atrazine and copper), using PICT bioassays. The taxonomical composition of the communities was determined on the same collecting dates. The herbicide concentration decrease during the 12 years significantly influenced the composition of communities. The PICT monitoring indicated that a significant tolerance decrease in the community to both herbicides accompanied the herbicide concentration decrease. PICT measurements for atrazine and copper also changed at the intra-annual level. These variations were mainly due to community composition shifts linked to seasonal phosphorus and temperature changes. PICT monitoring on a seasonal basis is required to monitor the mean tolerance of communities. PICT appeared to be a powerful tool that reflected the toxic effects on environmental communities and to monitor ecotoxic ecosystem restoration.

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References

  • Anneville O, Souissi S, Gammeter S, Straile D (2004) Seasonal and inter-annual scales of variability in phytoplankton assemblages: comparison of phytoplankton dynamics in three peri-alpine lakes over a period of 28 years. Freshw Biol 49:98–115

    Article  Google Scholar 

  • Anneville O, Souissi S, Ibanez F et al (2002) Temporal mapping of phytoplankton assemblages in Lake Geneva: annual and interannual changes in their patterns of succession. Limnol Oceanogr 47:1355–1366

    Article  Google Scholar 

  • Bérard A, Benninghoff C (2001) Pollution-induced community tolerance (PICT) and seasonal variations in the sensitivity of phytoplankton to atrazine in nanocosms. Chemosphere 45:427–437

    Article  Google Scholar 

  • Bérard A, Dorigo U, Humbert JF et al (2002) La méthode PICT (Pollution-Induced Community Tolerance) appliquée aux communautés algales: intérêt comme outil de diagnose et d’évaluation du risque écotoxicologique en milieu aquatique. Ann Limnol - Int J Limnol 38:247–261. doi:10.1051/limn/2002020

    Article  Google Scholar 

  • Bérard A, Dorigo U, Mercier I et al (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. doi:10.1016/S0045-6535(03)00674-X

    Article  CAS  Google Scholar 

  • Bérard A, Leboulanger C, Pelte T (1999a) Tolerance of Oscillatoria limnetica Lemmermann to atrazine in natural phytoplankton populations and in pure culture: influence of season and temperature. Arch Environ Contam Toxicol 37:472–479. doi:10.1007/s002449900541

    Article  Google Scholar 

  • Bérard A, Pelte T, Druart JC (1999b) Seasonal variations in the sensitivity of Lake Geneva phytoplankton community structure to atrazine. Arch Für Hydrobiol 145:277–295

    Google Scholar 

  • Blanck H, Dahl B (1998) Recovery of marine periphyton communities around a Swedish marina after the ban of TBT use in antifouling paint. Mar Pollut Bull 36:437–442

    Article  CAS  Google Scholar 

  • Blanck H, Eriksson KM, Grönvall F et al (2009) A retrospective analysis of contamination and periphyton PICT patterns for the antifoulant irgarol 1051, around a small marina on the Swedish west coast. Mar Pollut Bull 58:230–237. doi:10.1016/j.marpolbul.2008.09.021

    Article  CAS  Google Scholar 

  • Blanck H, Wängberg S-\AAke, Molander S (1988) Pollution-induced community tolerance—a new ecotoxicological tool. Funct. Test. Aquat Biota Estim Hazards Chem ASTM International, 100 Barr Harbor Drive, PO Box C700, West Conshohocken, PA 19428-2959, pp 219–230

  • Blanc P, Corvi C, Khim-Heang S, Rapin F (2000) Physico-chemical evolution of Geneva Lake waters. 33–58

  • Chalifour A, Juneau P (2011) Temperature-dependent sensitivity of growth and photosynthesis of Scenedesmus obliquus, Navicula pelliculosa and two strains of Microcystis aeruginosa to the herbicide atrazine. Aquat Toxicol 103:9–17. doi:10.1016/j.aquatox.2011.01.016

    Article  CAS  Google Scholar 

  • Chèvre N, Edder P, Ortelli D et al (2008) Risk assessment of herbicide mixtures in a large European lake. Environ Toxicol 23:269–277. doi:10.1002/tox.20337

    Article  CAS  Google Scholar 

  • Dorigo U, Bérard A, Bouchez A et al (2010) Transplantation of microbenthic algal assemblages to assess structural and functional recovery after diuron exposure. Arch Environ Contam Toxicol 59:555–563. doi:10.1007/s00244-010-9511-8

    Article  CAS  Google Scholar 

  • Druart JC, Rimet F (2008) Protocoles d’analyse du phytoplancton de l’INRA: prélèvement, dénombrement et biovolumes. 96

  • Dufrêne M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366

    Google Scholar 

  • Fechner LC, Gourlay-Francé C, Tusseau-Vuillemin M-H (2014) Linking community tolerance and structure with low metallic contamination: a field study on 13 biofilms sampled across the seine river basin. Water Res 51:152–162. doi:10.1016/j.watres.2013.12.002

    Article  CAS  Google Scholar 

  • Gawler M, Balvay G, Blanc P et al (1988) Plankton ecology of Lake Geneva: a test of the PEG-model. Arch Für Hydrobiol 114:161–174

    Google Scholar 

  • Gregorio V, Büchi L, Anneville O et al (2012) Risk of herbicide mixtures as a key parameter to explain phytoplankton fluctuation in a great lake: the case of Lake Geneva, Switzerland. Ecotoxicology 21:2306–2318. doi:10.1007/s10646-012-0987-z

    Article  CAS  Google Scholar 

  • Guasch H, Sabater S (1998) Light history influences the sensitivity to atrazine in periphytic algae. J Phycol 34:233–241. doi:10.1046/j.1529-8817.1998.340233.x

    Article  CAS  Google Scholar 

  • Gustavson K, Petersen S, Pedersen B et al (1999) Pollution-induced community tolerance (PICT) in coastal phytoplankton communities exposure to copper. Hydrobiologia 416:125–138

    Article  Google Scholar 

  • Gustavson K, Wängberg S-\AA (1995) Tolerance induction and succession in microalgae communities exposed to copper and atrazine. Aquat Toxicol 32:283–302

    Article  CAS  Google Scholar 

  • Hillebrand H, Dürselen C-D, Kirschtel D et al (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424

    Article  Google Scholar 

  • Huertas IE, Rouco M, López-Rodas V, Costas E (2010) Estimating the capability of different phytoplankton groups to adapt to contamination: herbicides will affect phytoplankton species differently. New Phytol 188:478–487. doi:10.1111/j.1469-8137.2010.03370.x

    Article  CAS  Google Scholar 

  • INERIS (2014a) Atrazine. 21

  • INERIS (2014b) Copper. 16

  • Knauer K, Leimgruber A, Hommen U, Knauert S (2010) Co-tolerance of phytoplankton communities to photosynthesis II inhibitors. Aquat Toxicol 96:256–263. doi:10.1016/j.aquatox.2009.11.001

    Article  CAS  Google Scholar 

  • Larras F, Bouchez A, Rimet F, Montuelle B (2012) Using bioassays and species sensitivity distributions to assess herbicide toxicity towards benthic diatoms. PLoS One 7:e44458. doi:10.1371/journal.pone.0044458

    Article  CAS  Google Scholar 

  • Larras F, Keck F, Montuelle B et al (2014) Linking diatom sensitivity to herbicides to phylogeny: a step forward for biomonitoring? Environ Sci Technol 48:1921–1930. doi:10.1021/es4045105

    Article  CAS  Google Scholar 

  • Leboulanger C, Rimet F, Hème de Lacotte M, Bérard A (2001) Effects of atrazine and nicosulfuron on freshwater microalgae. Environ Int 26:131–135

    Article  CAS  Google Scholar 

  • Lockert CK, Hoagland KD, Siegfried BD (2006) Comparative sensitivity of freshwater algae to atrazine. Bull Environ Contam Toxicol 76:73–79. doi:10.1007/s00128-005-0891-9

    Article  CAS  Google Scholar 

  • McCune B, Mefford M (2006) PC-ORD. Multivariate analysis of ecological data. Version 5.18. MJM Softw

  • Millie DF, Hersh CM, Dionigi CP (1992) Simazine-induced inhibition in phytoacclimated populations of Anabaena circinalis (cyanophyta). J Phycol 28:19–26. doi:10.1111/j.0022-3646.1992.00019.x

    Article  CAS  Google Scholar 

  • Molander S, Blanck H (1992) Detection of pollution-induced community tolerance (PICT) in marine periphyton communities established under diuron exposure. Aquat Toxicol 22:129–144

    Article  CAS  Google Scholar 

  • Nyström B, Paulsson M, Almgren K, Blank H (2000) Evaluation of the capacity for development of atrazine tolerance in periphyton from a Swedish freshwater site as determined by inhibition of photosynthesis and sulfolipid synthesis. Environ Toxicol Chem 19:1324–1331

    Article  Google Scholar 

  • Oksanen J, Blanchet F, Kindt R et al (2014) Package “Vegan”: Community Ecology Package.

  • Ortelli D, Edder P, Klein A, Ramseier Gentile S (2012) Metals and organic micropollutants in Geneva Lake waters. 51–66

  • Padisák J, Crossetti LO, Naselli-Flores L (2009) Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia 621:1–19. doi:10.1007/s10750-008-9645-0

    Article  Google Scholar 

  • Pérez P, Estévez-Blanco P, Beiras R, Fernández E (2006) Effect of copper on the photochemical efficiency, growth, and chlorophyll a biomass of natural phytoplankton assemblages. Environ Toxicol Chem 25:137–143

    Article  Google Scholar 

  • 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 44:1941–1949. doi:10.1016/j.watres.2009.11.053

    Article  CAS  Google Scholar 

  • R Development Core Team (2013). R: a language and environment for statistical computing. Vienna, Austria

  • Reynolds CS, Huszar V, Kruk C et al (2002) Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24:417–428

    Article  Google Scholar 

  • Rimet F, Druart J-C, Anneville O (2009) Exploring the dynamics of plankton diatom communities in Lake Geneva using emergent self-organizing maps (1974–2007). Ecol Inform 4:99–110. doi:10.1016/j.ecoinf.2009.01.006

    Article  Google Scholar 

  • Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22

    Article  Google Scholar 

  • Rotter S, Sans-Piché F, Streck G et al (2011) Active bio-monitoring of contamination in aquatic systems—an in situ translocation experiment applying the PICT concept. Aquat Toxicol 101:228–236. doi:10.1016/j.aquatox.2010.10.001

    Article  CAS  Google Scholar 

  • Schmitt-Jansen M, Altenburger R (2005) Predicting and observing responses of algal communities to photosystem II-herbicide exposure using pollution-induced community tolerance and species-sensitivity distributions. Environ Toxicol Chem 24:304–312. doi:10.1897/03-647.1

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Suresh Kumar K, Dahms H-U, Lee J-S et al (2014) Algal photosynthetic responses to toxic metals and herbicides assessed by chlorophyll a fluorescence. Ecotoxicol Environ Saf 104:51–71. doi:10.1016/j.ecoenv.2014.01.042

    Article  CAS  Google Scholar 

  • Tlili A, Bérard A, Roulier J-L et al (2010) PO43− dependence of the tolerance of autotrophic and heterotrophic biofilm communities to copper and diuron. Aquat Toxicol 98:165–177. doi:10.1016/j.aquatox.2010.02.008

    Article  CAS  Google Scholar 

  • Tlili A, Corcoll N, Bonet B et al (2011a) In situ spatio-temporal changes in pollution-induced community tolerance to zinc in autotrophic and heterotrophic biofilm communities. Ecotoxicology 20:1823–1839. doi:10.1007/s10646-011-0721-2

    Article  CAS  Google Scholar 

  • Tlili A, Maréchal M, Bérard A et al (2011b) Enhanced co-tolerance and co-sensitivity from long-term metal exposures of heterotrophic and autotrophic components of fluvial biofilms. Sci Total Environ 409:4335–4343. doi:10.1016/j.scitotenv.2011.07.026

    Article  CAS  Google Scholar 

  • Tlili A, Bérard A, Blanck H et al (2015) Pollution induced community tolerance (PICT): towards an ecologically relevant risk assessment of chemicals in aquatic systems. Freshw Biol. doi:10.1111/fwb.12558

    Google Scholar 

  • Uthermöl H (1931) Neue wege in der quantitativen Erfassung des Planktons (mit besonderer Berücksichtigung des Ultraplanktons). Verhandlungen Int Ver Für Limnol 567–596

  • Wetzel RG (2001) Limnology: lake and river ecosystems, 3rd edition Elsevier, Academic press

  • Wood RJ, Mitrovic SM, Kefford BJ (2014) Determining the relative sensitivity of benthic diatoms to atrazine using rapid toxicity testing: a novel method. Sci Total Environ 485–486:421–427. doi:10.1016/j.scitotenv.2014.03.115

    Article  CAS  Google Scholar 

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Acknowledgments

The authors thank Bo Nyström for his participation on 1999 PICT campaigns and the ecotoxicology INRA network for fruitful comments. This work is part of the IMPALAC program funded by The Ministère Français de l’Ecologie et du Développement Durable (convention 2100212555). The data used in this study were kindly provided by SOERE OLA-IS (INRA Thonon-les-Bains, CIPEL).

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Correspondence to Agnès Bouchez.

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Responsible editor: Philippe Garrigues

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Larras, F., Rimet, F., Gregorio, V. et al. Pollution-induced community tolerance (PICT) as a tool for monitoring Lake Geneva long-term in situ ecotoxic restoration from herbicide contamination. Environ Sci Pollut Res 23, 4301–4311 (2016). https://doi.org/10.1007/s11356-015-5302-0

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