Skip to main content
SpringerLink
Log in

Influence of the natural growth environment on the sensitivity of phototrophic biofilm to herbicide

  • Crop protection: environment, human health, and biodiversity
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Ecotoxicological experiments were performed in laboratory-scale microcosms to investigate community-level structural responses of river phototrophic biofilms from different environments to herbicide exposure. Biofilms were initially cultivated on artificial supports placed in situ for 4 weeks at two sites, site M, located in an agricultural watershed basin and site S, located in a forested watershed basin. The biofilms were subsequently transferred to microcosms and, after an acclimatisation phase of 7 days were exposed to alachlor at 10 and 30 μg L−1 for 23 days. Alachlor effects were assessed by a combination of structural parameters, including biomass (ash-free dry mass and chlorophyll a), molecular fingerprinting of the bacterial community (polymerase chain reaction (PCR)-denaturing gradient gel electrophoresis (DGGE)) and diatom species composition. Alachlor impacted the chlorophyll a and ash-free dry mass levels of phototrophic biofilms previously cultivated at site S. The structural responses of bacterial and diatom communities were difficult to distinguish from changes linked to the microcosm incubation period. Phototrophic biofilms from site S exposed at 30 μg L−1 alachlor were characterised by an increase of Achnanthidium minutissimum (K-z.) Czarnecki abundance, as well as a higher proportion of abnormal frustules. Thus, phototrophic biofilms with different histories, exhibited different responses to alachlor exposure demonstrating the importance of growth environment. These observations also confirm the problem of distinguishing changes induced by the stress of pesticide toxicity from temporal evolution of the community in the microcosm.

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

Similar content being viewed by others

References

  • Antić N, Radišić M, Radović T, Vasiljević T, Grujić S, Petković A, Dimkić M, Laušević M (2014) Pesticide residues in the Danube River Basin in Serbia—a survey during 2009–2011. Clean Soil Air Water. doi:10.1002/clen.201200360

    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 (1996) Effect of four organic solvents on natural phytoplankton assemblages: consequences for ecotoxicological experiments on herbicides. Bull Environ Contam Toxicol 57:183–190

    Article  Google Scholar 

  • Biggs BJF (1996) Patterns in benthic algae of streams. In: Stevenson RJ, Bothwell ML, Lowe RL (eds) Algal ecology: freshwater benthic ecosystems. Academic Press, San Diego, pp 31–56

    Chapter  Google Scholar 

  • Böger P, Matthes B, Schmalfu BJ (2000) Towards the primary target of chloroacetamides—new findings pave the way. Pest Manag Sci 56:497–508

    Article  Google Scholar 

  • Bonnet JL, Bonnemoy F, Dusser M, Bohatier J (2007) Assessment of the potential toxicity of herbicides and their degradation products to nontarget cells using two microorganisms, the Bacteria Vibrio fishcheri and the Ciliate Tetrahymena pyriformis. Environ Toxicol 22:78–91

    Article  CAS  Google Scholar 

  • Carder JP, Hoagland KD (1998) Combined effects of alachlor and atrazine on benthic algal communities in artificial streams. Environ Toxicol Chem 17:1415–1420

    Article  CAS  Google Scholar 

  • Caron DA (1994) Inorganic nutrients, bacteria, and the microbial loop. Microb Ecol 28:295–298

    Article  CAS  Google Scholar 

  • Chesters G, Simsiman GV, Levy J, Alhajjar BJ, Fathulla RN, Harkin JM (1989) Environmental fate of alachlor and metolachlor. Rev Environ Contam Toxicol 110:1–74

    CAS  Google Scholar 

  • Chiron S, Abian J, Ferrer M, Sanchezbaeza F, Messeguer A, Barcelo D (1995) Comparative photodegradation rates of alachlor and bentazone in natural water and determination of breakdown products. Environ Toxicol Chem 14:1287–1298

    Article  CAS  Google Scholar 

  • Cho CW, Thuy Pham TP, Kim S, Kim YR, Jeon YC, Yun YS (2009) Toxicity assessment of common organic solvents using a biosensor based on algal photosynthetic activity measurement. J Appl Phycol 21:683–689

    Article  CAS  Google Scholar 

  • Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clements WH, Newman MC (2002) Community ecotoxicology. John Wiley and Sons, Chichester

    Book  Google Scholar 

  • Compo J, Masiá A, Blasco C, Picó Y (2013) Occurrence and removal efficiency of pesticides in sewage treatment plants of four Mediterranean River Basins. J Hazard Mater 263:146–157

    Article  Google Scholar 

  • Coste M, Boutry S, Tison-Rosebery J, Delmas F (2009) Improvements of the Biological Diatom Index (BDI): description and efficiency of the new version (BDI-2006). Ecol Indic 9:621–650

    Article  CAS  Google Scholar 

  • Debenest T (2007) Characteristics of impact of agricultural pollutions on the benthic diatoms. PhD thesis, Université de Bordeaux 1, Bordeaux (in French)

  • Debenest T, Pinelli E, Coste M, Silvestre J, Mazzella N, Madigou C, Delmas F (2009) Sensitivity of freshwater periphytic diatoms to agricultural herbicides. Aquat Toxicol 93:11–17

    Article  CAS  Google Scholar 

  • Debenest T, Silvestre J, Coste M, Pinelli E (2010) Effects of pesticides on freshwater diatoms. Whitacre DM (ed) Reviews of environmental contamination and toxicology, 87. Reviews of environmental contamination and toxicology 203

  • DeLorenzo ME, Scott GI, Ross PE (2001) Toxicity of pesticides to aquatic micro-organisms: a review. Environ Toxicol Chem 20:84–98

    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 

  • 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 biofilm maturity. Sci Total Environ 408:552–562

    Article  CAS  Google Scholar 

  • El Jay A (1996) Toxic effects of organic solvents on the growth of Chlorella vulgaris and Selenastrum capricornutum. Bull Environ Contam Toxicol 57:191–198

    Article  Google Scholar 

  • Ensz AP, Knapp CW, Graham DW (2003) Influence of autochthonous dissolved organic carbon and nutrient limitation on alachlor biotransformation in aerobic aquatic systems. Environ Sci Technol 37:4157–4162

    Article  CAS  Google Scholar 

  • Fairchild JF, Ruessler DS, Haverland PS, Carlson AR (1997) Comparative sensitivity of Selenastrum capricornutum and Lemna minor to sixteen herbicides. Arch Environ Contam Toxicol 32:353–357

    Article  CAS  Google Scholar 

  • Feminella JW, Hawkins CP (1995) Interactions between stream herbivores and periphyton: a quantitative analysis of past experiments. J N Am Benthol Soc 14:465–509

    Article  Google Scholar 

  • Foley ME, Sigler V, Gruden CL (2008) A multiphasic characterization of the impact of the herbicide acetochlor on freshwater bacterial communities. ISME J 2:56–66

    Article  CAS  Google Scholar 

  • Geiszinger A, Bonnineau C, Faggiano L, Guasch H, Lopez-Doval JC, Proia L, Ricart M, Ricciardi F, Romani A, Rotter S, Munoz I, Schmitt-Jansen M, Sabater S (2009) The relevance of the community approach linking chemical and biological analyses in pollution assessment. Trends Anal Chem 28:619–626

    Article  CAS  Google Scholar 

  • Graham DW, Miley MK, Denoyelles F, Smith VH, Thurman EM, Carter R (2000) Alachlor transformation patterns in aquatic field mesocosms under variable oxygen and nutrient conditions. Water Res 34:4054–4062

    Article  CAS  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 

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

    Article  Google Scholar 

  • Junghans M, Backhaus T, Faust M, Scholze M, Grimme LH (2003) Predictability of combined effects of eight chloroacetanilide herbicides on algal reproduction. Pest Manag Sci 59:1101–1110

    Article  CAS  Google Scholar 

  • Jurgensen TA, Hoagland KD (1990) Effects of short-term pulses of atrazine on attached algal communities in a small stream. Arch Environ Contam Toxicol 19:617–623

    Article  CAS  Google Scholar 

  • Kasai F (1999) Shifts in herbicide tolerance in paddy field periphyton following herbicide application. Chemosphere 38:919–931

    Article  CAS  Google Scholar 

  • Knapp CW, Graham DW, Berardescoa G, deNoyelles JF, Cutakd BJ, Larive CK (2003) Nutrient level, microbial activity, and alachlor transformation in aerobic aquatic systems. Water Res 37:4761–4769

    Article  CAS  Google Scholar 

  • Lawrence JR, Kopf G, Headley JV, Neu TR (2001) Sorption and metabolism of selected herbicides in river biofilm communities. Can J Microbiol 47:634–641

    Article  CAS  Google Scholar 

  • Lyautey E, Lacoste B, Ten-Hage L, Rols JL, Garabetian F (2005) Analysis of bacterial diversity in river biofilms using 16S rDNA PCR-DGGE: methodological settings and fingerprints interpretation. Water Res 39:380–388

    Article  CAS  Google Scholar 

  • Lynch TR, Johnson HE, Adams WJ (1985) Impact of atrazine and hexachlorobiphenyl on the structure and function of model stream ecosystems. Environ Toxicol Chem 4:399–413

    Article  CAS  Google Scholar 

  • Ma J, Chen J (2005) How to accurately assay the algal toxicity of pesticides with low water solubility. Environ Pollut 136:267–273

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Muyzer G, Brinkhoff T, Nubel U, Santegoeds C, Schafer H, Wawer C (1997) Denaturing gradient gel electrophoresis (DGGE) in microbial ecology. In: Kowalchuk GA, De Bruijn FJ, Head IM, Akkermans D, Van Elsa JD (eds). Kluwer Academic Dordrecht, pp 1–27

  • Niederlehner BR, Cairns J (1992) Community response to cumulative toxic impact—effects of acclimation on zinc tolerance of Aufwuchs. Can J Fish Aquat Sci 49:2155–2163

    Article  CAS  Google Scholar 

  • Okumura Y, Koyama J, Takaku H, Satoh H (2001) Influence of organic solvents on the growth of marine microalgae. Arch Environ Contam Toxicol 41:123–128

    Article  CAS  Google Scholar 

  • Paule A, Lyautey E, Garabetian F, Rols JL (2009) Autogenic versus environmental control during development of river biofilm. Ann Limnol Int J Limnol 45:1–10

    Article  Google Scholar 

  • Paule A, Lauga B, Ten-Hage L, Morchain J, Duran R, Paul E, Rols JL (2011) A photosynthetic rotating annular bioreactor (Taylor-Couette type flow) for phototrophic biofilms cultures. Water Res 45(18):6107–6118

    Article  CAS  Google Scholar 

  • Paule A, Roubeix V, Lauga B, Duran R, Delmas F, Paul E, Rols JL (2013) Changes in tolerance to herbicide toxicity throughout development stages of phototrophic biofilms cultivated in rotating annular bioreactor. Aquat Toxicol 144–145:310–321

    Article  Google Scholar 

  • Payraudeau S, Junker P, Imfeld G, Gregoire C (2009) Characterizing hydrological connectivity to identify critical source areas for pesticides losses. In: 18thWorld IMACS/MODSIM Congress: Interfacing modelling and simulation with mathematical and computational sciences, Cairns, Australia, 1879–1885

  • Pérès F, Coste M, Ribeyre F, Ricard M, Boudou A (1997) Effects of methylmercury and inorganic mercury on periphytic diatom communities in freshwater indoor microcoms. J Appl Phycol 9:215–227

    Article  Google Scholar 

  • Pesce S, Fajon C, Bardot C, Bonnemoy F, Portelli C, Bohatier J (2006) Effects of the phenylurea herbicide diuron on natural riverine microbial communities in an experimental study. Aquat Toxicol 78:303–314

    Article  CAS  Google Scholar 

  • Pesce S, Batisson I, Bardot C, Fajon C, Portelli C, Montuelle B, Bohatier J (2009) Response of spring and summer riverine microbial communities following glyphosate exposure. Ecotoxicol Environ Saf 72:1905–1912

    Article  CAS  Google Scholar 

  • Pesce S, Martin-Laurent F, Rouard N, Robin A, Montuelle B (2010) Evidence for adaptation of riverine sediment microbial communities to diuron mineralization: incidence of runoff and soil erosion. J Soil Sediment 10:698–707

    Article  CAS  Google Scholar 

  • Robles-Molina J, Gilbert-López B, García-Reyes JF, Molina-Díaz A (2014) Monitoring of selected priority and emerging contaminants in the Guadalquivir River and other related surface waters in the province of Jaén, South East Spain. Sci Total Environ 479–480:247–257

    Article  Google Scholar 

  • Roubeix V, Mazzella N, Mechin B, Coste M, Delmas F (2011) Impact of the herbicide metolachlor on river periphytic diatoms: experimental comparison of descriptors at different biological organization levels. Ann Limnol Int J Limnol 47:239–249

    Article  Google Scholar 

  • 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 biofilm as an interface. Anal Bioanal Chem 387:1425–1434

    Article  CAS  Google Scholar 

  • Singh S, Datta P (2005) Growth and survival potentials of immobilized diazotrophic cyanobacterial isolates exposed to common ricefield herbicides. World J Microbiol Biotechnol 21:441–446

    Article  CAS  Google Scholar 

  • Spawn RL, Hoagland KD, Siegfried BD (1997) Effects of alachlor on an algal community from a midwestern agricultural stream. Environ Toxicol Chem 16:785–793

    Article  CAS  Google Scholar 

  • Stevenson RJ, Bothwell ML, Lowe RL (1996) Algal ecology: freshwater benthic ecosystems. Academic Press, San Diego, 753 pp

    Google Scholar 

  • Stratton GW, Corke CT (1981) Effect of acetone on the toxicity of atrazine towards photosynthesis in Anabaena. J Environ Health B16:21–33

    Article  CAS  Google Scholar 

  • Taghavi L, Probst JL, Merlina G, Marchand AL, Durbe G, Probst A (2010) Flood event impact on pesticide transfer in a small agricultural catchment (Montousse at Aurade, south west France). Int J Environ Anal Chem 90:390–405

    Article  CAS  Google Scholar 

  • Tiam SK, Morin S, Pesce S, Feurtet-Mazel A, Moreira A, Gonzalez P, Mazzella N (2014) Environmental effects of realistic pesticide mixtures on natural biofilm communities with different exposure histories. Sci Total Environ 473–474:496–506

    Article  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, Montuelle B, Berard A, Bouchez A (2011) Impact of chronic and acute pesticide exposures on periphyton communities. Sci Total Environ 409:2102–2113

    Article  CAS  Google Scholar 

  • Valloton N, Moser D, Eggen RIL, Junghans M, Chèvre N (2008) S-metolachlor pulse exposure on the alga Scenedesmus vacuolatus: effects during exposure and the subsequent recovery. Chemosphere 73:395–400

    Article  Google Scholar 

  • Vercraene-Eairmal M, Lauga B, Saint Laurent S, Mazzella N, Boutry S, Simon M, Karama S, Delmas F, Duran R (2010) Diuron biotransformation and its effects on biofilm bacterial community structure. Chemosphere 81:837–843

    Article  CAS  Google Scholar 

  • Wendt-Rasch L, Van den Brink PJ, Crum SJH, Woin P (2004) The effects of a pesticide mixture on aquatic ecosystems differing in trophic status: responses of the macrophyte Myriophyllum spicatum and the periphytic algal community. Ecotoxicol Environ Saf 57:383–398

    Article  CAS  Google Scholar 

  • Wetzel RG (1983) Opening remarks. In: Wetzel RG (ed) Periphyton of freshwater ecosystems. Junk, Boston

    Chapter  Google Scholar 

Download references

Acknowledgements

This work was funded by the French National Programme EC2CO-Environmental Microbiology—and by the Midi-Pyrénées Council Programme of the Pyrenean working community. We thank J. Ferriol and D. Dalger for assistance with the DGGE and water chemistry analysis, respectively. We also thank the ‘Association des Agriculteurs d’Auradé’ for the access to site M.

Author information

Authors and Affiliations

  1. University de Toulouse, UPS, INP, EcoLab (Laboratoire d’écologie fonctionnelle et environnement), 118 route de Narbonne, 31062, Toulouse, France

    A. Paule, A. Lamy & J. L. Rols

  2. CNRS, EcoLab, 31062, Toulouse, France

    A. Paule, A. Lamy & J. L. Rols

  3. IRSTEA, UR Ecosystèmes Aquatiques et Changements Globaux (EABX), 50 avenue de Verdun, 33612, Cestas, France

    V. Roubeix & F. Delmas

Authors
  1. A. Paule
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Lamy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. V. Roubeix
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. F. Delmas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. L. Rols
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Paule.

Additional information

Responsible editor: Philippe Garrigues

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Photographs of the two study sites M and S chosen for in situ production of natural phototrophic biofilm. (DOC 4929 kb)

Fig. S2

Different views of artificial substrates (polyethylene plates, 50 × 100 × 5 mm) used for in situ production and collection of natural phototrophic biofilms (site M on the photography). (DOC 3864 kb)

Fig. S3

Schema of one microcosm subdivided into three compartments by vertically glass slides. Water recirculation is realised with a submerged pump. Seven polyethylene plates are positioned in the main compartment. (DOC 103 kb)

Fig. S4

A normal diatom frustule (left) versus an abnormal form (right) of Achnanthidium minutissimum observed in the 30 μg L−1 alachlor-contaminated microcosms at 23 days of incubation during the experiment S. Scale bar, 10 μm. (DOC 167 kb)

Table S1

Values of the pesticides levels obtained from the previous studies (Debenest 2007, Paule et al. 2009) of the two study sites M and S during the springs of the years 2005, 2006 and 2007. (DOC 3883 kb)

Table S2

Values of the nitrate (NO3 −) levels obtained from the previous studies (Debenest 2007, Paule et al. 2009) of the two study sites M and S during the springs of the years 2005 and 2007. (DOC 3870 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Paule, A., Lamy, A., Roubeix, V. et al. Influence of the natural growth environment on the sensitivity of phototrophic biofilm to herbicide. Environ Sci Pollut Res 22, 8031–8043 (2015). https://doi.org/10.1007/s11356-014-3429-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-014-3429-z

Keywords

Search

Navigation