Skip to main content
SpringerLink
Log in

In situ spatio-temporal changes in pollution-induced community tolerance to zinc in autotrophic and heterotrophic biofilm communities

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Pollution-induced community tolerance (PICT) uses increased tolerance in populations at contaminated sites as an indicator of contaminant effects. However, given the broad structural and functional complexity that characterizes biological communities, the acquisition of PICT could vary with (i) target community, (ii) intensity of toxicant exposure, (iii) the species succession stage, and (iv) the physicochemical characteristics of the studied site. To assess the spatio-temporal changes of zinc-induced tolerance in fluvial biofilm communities, we conducted an in situ study in Osor River (North-East Catalonia, Spain), which has zinc contamination. Biofilms were developed for 5 weeks in a non-metal-polluted site, and were then transferred to different sites in Osor River with different levels of zinc contamination. The spatio-temporal changes of biofilm PICT to zinc was determined using photosynthetic activity bioassays and respiration-induced aerobic bioassays at T0, and at 1, 3 and 5 weeks of exposure. We also performed physicochemical characterization of the sites, taxonomic analysis of diatoms, bacterial and fungal diversity and profiled pigments of phototrophic communities. We used multivariate ordination to analyze results. In addition to natural species succession, the intensity of metal pollution exerted structural pressure by selecting the most metal-tolerant species, but differently depending on the type of biofilm. Zn-tolerance values indicated that exposure to high levels of zinc had effects that were similar to a longer exposure to lower levels of zinc.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Agencia Catalana de l’Aigua (ACA) (2009) http://aca-web.gencat.cat

  • Armstrong GA, Hearst JE (1996) Genetics and molecular biology of carotenoid pigment biosynthesis. FASEB J 10:228–237

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Barranguet C, Plans M, van der Grinten E, Sinke JJ, Admiraal W (2002) Development of photosynthetic biofilms affected by dissolved and sorbed copper in a eutrophic river. Environ Toxicol Chem 21:1955–1965

    Article  CAS  Google Scholar 

  • Barranguet C, van den Ende FP, Rutgers M, Breure AM, Greijdanus M, Sinke JJ, Admiraal W (2003) Copper-induced modifications of the trophic relations in riverine algal-bacterial biofilms. Environ Toxicol Chem 22:1340–1349

    CAS  Google Scholar 

  • Battin TJ, Kaplan LA, Newbold JD, Hansen CME (2003) Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 426:439–442

    Article  CAS  Google Scholar 

  • Bérard A, Dorigo U, Humbert JF, Leboulanger C, Seguin F (2002) Application of the Pollution-Induced Community Tolerance (PICT) method to algal communities: its values as a diagnostic tool for ecotoxicological risk assessment in the aquatic environment. Annls Limnol I J Limnol 38:247–261

    Article  Google Scholar 

  • Besemer K, Singer G, Limberger R, Chlup AK, Hochedlinger G, Hodl I, Baranyi C, Battin TJ (2007) Biophysical controls on community succession in stream biofilms. Appl Environ Microb 73:4966–4974

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Blanck H, Wänkberg S-Å, Molander S (1988) Pollution-induced community tolerance—a new ecotoxicological tool. In: Cairs J, Jr., Pratt JR (eds) Functional testing of aquatic biota for estimating hazards of chemicals. ASTM STP 988, 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 Contam Toxicol 44:17–29

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Borcard D, Legendre P, Drapeau P (1992) Partialling out the spatial component of ecological variation. Ecology 73:1045–1055

    Article  Google Scholar 

  • Campbell CD, Chapman SJ, Cameron CM, Davidson MS, Potts JM (2003) A rapid microtiter plate method to measure carbon dioxide evolved from carbon substrate amendments so as to determine the physiological profiles of soil microbial communities by using whole soil. Appl Environ Microbiol 69:3593–3599

    Article  CAS  Google Scholar 

  • Cattaneo A, Kerimian T, Roberge M, Marty J (1997) Periphyton distribution and abundance on substrata of different size along a gradient of steam trophy. Hydrobiologia 354:101–110

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Adams WWI (2006) Photoprotection in an ecological context: the remarkable complexity of thermal energy dissipation. New Phytol 172:11–21

    Article  CAS  Google Scholar 

  • Demmig-Adams B, Winter K, Krüger A, Czygan FC (1987) Photoinhibition and zeaxanthin formation in intact leaves. A possible role of the xanthophyll cycle in the dissipation of excess light. Plant Physiol 84:218–224

    Article  Google Scholar 

  • Dorigo U, Bourrain X, Berard A, Leboulanger C (2004) Seasonal changes in river microalgae sensitivity to atrazine and isoproturon, along a contamination gradient. Sci Total Environ 318:101–114

    Article  CAS  Google Scholar 

  • Dorigo U, Leboulanger C, Berard 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

    Article  Google Scholar 

  • Dorigo U, Berard 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ferreira Da Silva E, Almeida SFP, Nunes ML, Luís AT, Borg F, Hedlund M, Marques De Sá C, Patinha C, Teixeira P (2009) Heavy metal pollution downstream the abandoned Coval da Mó mine (Portugal) and associated effects on epilithic diatom communities. Sci Total Environ 407:5620–5636

    Article  CAS  Google Scholar 

  • Feurtet-Mazel A, Gold C, Coste M, Boudou A (2003) Study of periphytic diatom communities exposed to metallic contamination through complementary field and laboratory experiments. J Phys IV 107:467–470

    CAS  Google Scholar 

  • Genter RB, Cherry DS, Smith EP, Cairns JJ (1987) Algal-priphyton population and community changes from zinc stress in stream mesocosms. Hydribiologia 153:87–92

    Article  Google Scholar 

  • Guasch H, Sabater S (1998) Light history influences the sensitivity to atrazine in periphytic algae. J Phycol 34:233–241

    Article  CAS  Google Scholar 

  • Guasch H, Paulsson M, Sabater S (2002) Effect of copper on algal communities from oligotrophic calcareous streams. J Phycol 38:241–248

    Article  CAS  Google Scholar 

  • Guasch H, Admiraal W, Sabater S (2003) Contrasting effects of organic and inorganic toxicants on freshwater periphyton. Aquat Toxicol 64:165–175

    Article  CAS  Google Scholar 

  • Guasch H, Navarro E, Serra A, Sabater S (2004) Phosphate limitation influences the sensitivity to copper in periphytic algae. Freshw Biol 49:463–473

    Article  CAS  Google Scholar 

  • Guasch H, Leira M, Montuelle B, Geiszinger A, Roulier JL, Tornés E, Serra A (2009) Use of multivariate analyses to investigate the contribution of metal pollution to diatom species composition: search for the most appropriate cases and explanatory variables. Hydrobiologia 627:143–158

    Article  CAS  Google Scholar 

  • Guasch H, Atli G, Bonet B, Corcoll N, Leira M, Serra A (2010) Discharge and the response of biofilms to metal exposure in Mediterranean rivers. Hydrobiologia 657:143–157

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Hill WR, Larsen IL (2005) Growth dilution of metals in microalgal biofilms. Environ Sci Technol 39:1513–1518

    Article  CAS  Google Scholar 

  • Ivorra N, Hettelaar J, Tubbing GMJ, Kraak MHS, Sabater S, Admiraal W (1999) Translocation of microbenthic algal assemblages used for in situ analysis of metal pollution in rivers. Arch Environ Contam Toxicol 37:19–28

    Article  CAS  Google Scholar 

  • Ivorra N, Bremer S, Guasch H, Kraak MHS, Admiraal W (2000) Differences in the sensitivity of benthic microalgae to Zn and Cd regarding biofilm development and exposure history. Environ Toxicol Chem 19:1332–1339

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Jackson CR (2003) Changes in community properties during microbial succession. Oikos 101(2):444–448

    Article  Google Scholar 

  • Jeffrey SW, Vesk M (1997) Introduction to marine phytoplankton and their pigment signatures. In: Jeffrey SW, Mantoura RFC, Wright SW (eds) Phytoplankton pigments in oceanography. UNESCO Publishing, Paris, pp 37–84

    Google Scholar 

  • Jeffrey SW, Mantoura RFC, Wright SW (1997) Phytoplankton pigments in oceanography: monographs on oceanographic methodologies. UNESCO, Paris

    Google Scholar 

  • Khoshmanesh A, Lawson F, Prince IG (1997) Cell surface area as a major parameter in the uptake of cadmium by unicellular green microalgae. Chem Eng J 65:13–19

    Article  CAS  Google Scholar 

  • Krammer K, Lange-Bertalot H (1986-1991) Bacillariophyceae 1. Teil: Naviculaceae, 2. Teil: Bacillariaceae, Epithemiaceae, Surirellaceae, 3. Teil: Centrales, Fragilariaceae, Eunotiaceae, 4. Teil: Achnanthaceae. Kritische Ergänzungen zu Navicula (Lineolatae) und Gomphonema, Vol G. Fischer Verlag, Stuttgart

  • Lehmann V, Tubbing GMJ, Admiraal W (1999) Induced metal tolerance in microbenthic communities from three lowland rivers with different metal loads. Arch Environ Contam Toxicol 36:384–391

    Article  CAS  Google Scholar 

  • Mahmoud HMA, Goulder R, Carvalho GR (2005) The response of epilithic bacteria to different metals regime in two upland streams: assessed by conventional microbiological methods and PCR-DGGE. Arch Hydrobiol 163:405–427

    Article  CAS  Google Scholar 

  • Mølander 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  Google Scholar 

  • Morin S, Vivas-Nogues M, Duong TT, Boudou AMC, Delmas F (2007) Dynamics of benthic diatom colonization in a cadmium/zinc-polluted river (Riou Mort, France). Fundam Appl Limnol 168:179–187

    Article  CAS  Google Scholar 

  • Morin S, Duong TT, Dabrin A, Coynel A, Herlory O, Baudrimont M, Delmas F, Durrieu G, Schafer J, Winterton P, Blanc G, Coste M (2008) 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

    Article  CAS  Google Scholar 

  • Paulsson M, Nystrom B, Blanck H (2000) Long-term toxicity of zinc to bacteria and algae in periphyton communities from the river Gota Alv, based on a microcosm study. Aquat Toxicol 47:243–257

    Article  CAS  Google Scholar 

  • Pérès F, Lorin D, Grollier T, Feurtet-Mazel A, Coste M, Ribeyre F, Ricard M, Boudou A (1996) Effects of the phenylurea herbicide isoproturon on periphytic diatom communities in freshwater indoor microcosms. Environ Pollut 94:141–152

    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

    Article  CAS  Google Scholar 

  • Ranjard LFP, Lata J-C, Muogel C, Thioulouse J, Nazaret S (2001) Characterization of bacterial and fungal soil communities by automated ribosomal intergenic spacer analysis fingerprints: biological and methodological variability. Appl Environ Microbiol 67:4479–4487

    Article  CAS  Google Scholar 

  • Sabater S, Guasch H, Ricart M, Romaní A, Vidal G, Klünder C, Schmitt-Jansen M (2007) Monitoring the effect of chemicals on biological communities. The biofilm as an interface. Anal Bioanal Chem 387:1425–1434

    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

    Article  CAS  Google Scholar 

  • Schreiber U, Müller 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

    Article  CAS  Google Scholar 

  • Serra A, Corcoll N, Guasch H (2009) Copper accumulation and toxicity in fluvial periphyton: the influence of exposure history. Chemosphere 74:633–641

    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 

  • Stevenson RJ, Peterson CG (1989) Variation in benthic diatom (Bacillariophyceae) immigration with habitat characteristics and cell morphology. J Phycol 25:120–129

    Article  Google Scholar 

  • Ter Braak CJF, Smilauer P (1998) CANOCO Reference Manual and User’s Guide to Canoco for Windows: Software for Canonical Community Ordination (Version 4). Microcomputer Power, Ithaca, NY

  • Tlili A, Montuelle B (2011) Microbial pollution-induced community tolerance. In: Amiart-Triquet C, Rainbow PS, Roméo M (eds) Tolerance to environmental contaminants. CRCpress, Boca Raton, pp 65–108

    Google Scholar 

  • Tlili A, Dorigo U, Montuelle B, Margoum C, Carluer N, Gouy V, Bouchez A, Berard A (2008) Responses of chronically contaminated biofilms to short pulses of diuron—an experimental study simulating flooding events in a small river. Aquat Toxicol 87:252–263

    Article  CAS  Google Scholar 

  • Tlili A, Bérard A, Roulier JL, Volat B, Montuelle B (2010) PO43-dependence of the tolerance of autotrophic and heterotrophic biofilm communities to copper and diuron. Aquat Toxicol 98:165–177

    Article  CAS  Google Scholar 

  • Tlili A, Marechal M, Montuelle B, Volat B, Dorigo U, Bérard A (2011) Use of the MicroRespTM method to assess pollution-induced community tolerance to metals for lotic biofilms. Environ Pollut 159:18–24

    Article  CAS  Google Scholar 

  • Villeneuve A, Bouchez A, Montuelle B (2010) Influence of slight differences in environmental conditions (light, hydrodynamics) on the structure and function of the periphyton. Aquat Sci 72(1):33–44

    Article  Google Scholar 

  • Waring J, Baker NR, Underwood GJC (2007) Responses of estuarine intertidal microphytobenthic algal assemblages to enhanced ultraviolet B radiation. Global Change Biol 13(7):1398–1413

    Article  Google Scholar 

  • Wilhelm C, Rudolph I, Renner W (1991) A quantitative method based on HPLC-aided pigment analysis to monitor structure and dynamics of the phytoplankton assemblage – A study from lake meerfelder maar (Eife, germany). Arch Hydrobiol 123:21–35

    CAS  Google Scholar 

  • Zhou Y, Yao J, Choi M, Chen Y, Chen H, Mohammad R, Zhuang R, Chen H, Wang F, Maskow T, Zaray G (2009) A combination method to study microbial communities and activities in zinc contaminated soil. J Hazard Mater 169:875–881

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank C. Rosy for his technical help with the molecular and pigment analyses, Silvia Corcoll for developing the “Osor” Watershed Map by GIS, and the company ATT for proofreading the English-language version of the manuscript. We are grateful to the Onema (French National Agency for Water and Aquatic Ecosystems) and the Rhône-Alpes region (Explora’doc Grant) for providing financial support. This study was also supported by the Spanish Ministry project FLUVIALMULTISTRESS (CTM2009-14111-C02-01) and the EC project KEYBIOEFFECTS (MRTN-CT-2006-035695). The University of Girona “Serveis Tècnics de Recerca” offered their facilities and technical assistance for the metal analyses.

Author information

Authors and Affiliations

  1. CEMAGREF, UR MAEP, 3 quai Chauveau, CP, 69336, Lyon Cedex 09, France

    Ahmed Tlili & Bernard Montuelle

  2. Department of Environmental Sciences, Faculty of Sciences, Institute of Aquatic Ecology, University of Girona (UdG), Campus Montilivi, 17071, Girona, Spain

    Natalia Corcoll, Berta Bonet & Helena Guasch

  3. CEMAGREF, UR REBX, 50 avenue de Verdun, 33612, Cestas Cedex, France

    Soizic Morin

  4. INRA, UMR EMMAH 1114, Domaine Saint-Paul—Site Agroparc, 84914, Avignon Cedex 9, France

    Annette Bérard

Authors
  1. Ahmed Tlili
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Natalia Corcoll
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Berta Bonet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Soizic Morin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bernard Montuelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Annette Bérard
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Helena Guasch
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ahmed Tlili.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-011-0721-2

Keywords

Search

Navigation