Changes in tolerance to herbicide toxicity throughout development stages of phototrophic biofilms

Aquatic Toxicology

Volumn 144-145, Issue , 2013, Pages 310-321

  Paule, A ^a,b   Roubeix, V ^c   Lauga, B ^d   Duran, R ^d   Delmas, F ^c   Paul, E ^e,f   Rols, J L ^a,b  

^a UNIVERSITÉ PAUL SABATIER   (France)

^b Institut National Polytechnique   (France)

^c CEMAGREF   (France)

^d UNIVERSITÉ DE PAU ET DES PAYS DE L'ADOUR   (France)

^e UNIVERSITÉ DE TOULOUSE   (France)

^f UMR792 INGÉNIERIE DES SYSTÈMES BIOLOGIQUES ET DES PROCÉDÉS   (France)

Author keywords

Bacterial communities; Diatoms; Ecological succession; Ecotoxicology; Phototrophic biofilms

Indexed keywords

ALACHLOR; CHLOROPHYLL A;

ALACHLOR; BIOACCUMULATION; BIOFILM; BIOINDICATOR; COMMUNITY COMPOSITION; DEVELOPMENTAL STAGE; DIATOM; ECOTOXICOLOGY; EXPERIMENTAL STUDY; MICROBIAL COMMUNITY; POLLUTION EFFECT; POLLUTION TOLERANCE;

ARTICLE; BIOFILM; CARBON SOURCE; CHLOROPHYCEAE; CONTROLLED STUDY; CYANOBACTERIUM; DIATOM; DRY MASS; ECOTOXICOLOGY; GROWTH INHIBITION; HERBICIDE TOLERANCE; MICROBIAL BIOMASS; MICROBIAL COLONIZATION; MICROBIAL COMMUNITY; MICROCOSM; NONHUMAN; PHOTOTROPHY; PRIORITY JOURNAL;

BACTERIAL COMMUNITIES; DIATOMS; ECOLOGICAL SUCCESSION; ECOTOXICOLOGY; PHOTOTROPHIC BIOFILMS;

ACETAMIDES; BIODIVERSITY; BIOFILMS; CLUSTER ANALYSIS; DIATOMS; DRUG TOLERANCE; HERBICIDES; TIME FACTORS; WATER POLLUTANTS, CHEMICAL;

EID: 84887355541     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.09.024     Document Type: Article

References (77)

1. Abrantes N., Pereira R., Gonçalves F. Occurrence of pesticides in water, sediments, and fish tissues in a lake surrounded by agricultural lands: concerning risks to humans and ecological receptors. Water Air Soil Pollut. 2010, 212:77-88.
2. Admiraal W., Blanck H., Buckert-De Jong M., Guasch H., Ivorra N., Lehmann V., Nystrom B.A.H., Paulsson M., Sabater S. Short-term toxicity of zinc to microbenthic algae and bacteria in a metal polluted stream. Water Res. 1999, 33(9):1989-1996.
3. Battin T.J., Kaplan L.A., Newbold J.D., Hansen C.M.E. Contributions of microbial biofilms to ecosystem processes in stream mesocosms. Nature 2003, 426:439-442.
4. Berthon V., Bouchez A., Rimet F. Using diatom life-forms and ecological guilds to assess organic pollution and trophic level in rivers: a case study of rivers in south-eastern France. Hydrobiologia 2011, 673:259-271.
5. Biggs B.J.F. Patterns in benthic algae of stream. Algal Ecology. Freshwater Benthic Ecosystem 1996, 31-56. Academic Press, San Diego. R.J. Stevenson, M.L. Bothwell, R.L. Lowe (Eds.).
6. Böger P., Matthes B., SchmalfuB J. Towards the primary target of chloroacetamides - new findings pave the way. Pest Manag. Sci. 2000, 56:497-508.
7. Bonnet J.L., Bonnemoy F., Dusser M., Bohatier J. 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. 2007, 22:78-91.
8. Carder J.P., Hoagland K.D. Combined effects of alachlor and atrazine on benthic algal communities in artificial streams. Environ. Toxicol. Chem. 1998, 17:1415-1420.
9. Chesters G., Simsiman G.V., Levy J., Alhajjar B.J., Fathulla R.N., Harkin J.M. Environmental fate of alachlor and metolachlor. Rev. Environ. Contam. Toxicol. 1989, 110:1-74.
10. Choi K.H., Dodds F.C. Comparison of two kinds of Biolog microplates (GN and ECO) in their ability to distinguish among aquatic microbial communities. J. Microbiol. Methods 1999, 36:203-213.
11. Clarke K.R. Non parametric multivariate analyses of changes in community structure. Aust. J. Ecol. 1993, 18:117-143.
12. Debenest T., Pinelli E., Coste M., Silvestre J., Mazzella N., Madigou C., Delmas F. Sensitivity of freshwater periphytic diatoms to agricultural herbicides. Aquat. Toxicol. 2009, 93:11-17.
13. Dorigo U., Bourrain X., Bérard A., Leboulanger C. Seasonal changes in the sensitivity of river microalgae to atrazine and isoproturon along a contamination gradient. Sci. Total Environ. 2004, 318:101-144.
14. Downing H.W., Delorenzo M.E., Fulton M.H., Scott G.I., Madden C.J., Kucklick J.R. Effects of the agricultural pesticides atrazine, chlorothalonil, and endosulfan on South Florida microbial assemblages. Ecotoxicology 2004, 13:245-260.
15. Duong T., Morin S., Coste M., Herlory O., Feurtet-Mazel A., Boudou A. Experimental toxicity and bioaccumulation of cadmium in freshwater periphytic diatoms in relation with biofilm maturity. Sci. Total Environ. 2010, 408:552-562.
16. DeLorenzo M.E., Scott G.I., Ross P.E. Toxicity of pesticides to aquatic microorganisms: a review. Environ. Toxicol. Chem. 2001, 20:84-98.
17. Ensz A.P., Knapp C.W., Graham D.W. Influence of autochthonous dissolved organic carbon and nutrient limitation on alachlor biotransformation in aerobic aquatic systems. Environ. Sci. Technol. 2003, 37:4157-4162.
18. Fairchild J.F., Ruessler D.S., Haverland P.S., Carlson A.R. Comparative sensitivity of Selenastrum capricornutum and Lemna minor to sixteen herbicides. Arch. Environ. Contam. Toxicol. 1997, 32:353-357.
19. Fairchild J.F., Ruessler D.S., Carlson A.R. Comparative sensitivity of five species of macrophytes and six species of algae to atrazine, metribuzin, alachlor, and metolachlor. Environ. Toxicol. Chem. 1998, 17:1830-1834.
20. Foley M.E., Sigler V., Gruden C.L. A multiphasic characterization of the impact of the herbicide acetochlor on freshwater bacterial communities. ISME J. 2008, 2:56-66.
21. Graham W.H., Graham D.W., Denoyelles F., Smith V.H., Larive C.K., Thurman E.M. Metolachlor and alachlor breakdown product formation patterns in aquatic field mesocosms. Environ. Sci. Technol. 1999, 33:4471-4476.
22. Graham D.W., Miley M.K., Denoyelles F., Smith V.H., Thurman E.M., Carter R. Alachlor transformation patterns in aquatic field mesocosms under variable oxygen and nutrient conditions. Water Res. 2000, 34:4054-4406.
23. Guasch H., Munoz I., Roses N., Sabater S. Changes in atrazine toxicity throughout succession of stream periphyton communities. J. Appl. Physiol. 1997, 9:137-146.
24. Guasch H., Ivorra N., Lehmann V., Paulsson M., Real M., Sabater S. Community composition and sensitivity of periphyton to atrazine in flowing waters: the role of environmental factors. J. Appl. Physiol. 1998, 10:203-213.
25. Guasch H., Admiraal W., Sabater S. Contrasting effects of organic and inorganic toxicants on freshwater periphyton. Aquat. Toxicol. 2003, 64:165-175.
26. Guasch H., Bonet B., Bonnineau C., Corcoll N., Lopez-Doval J.C., Munoz I., Ricart M., Serra A., Clements W. How to link field observations with causality? Field and experimental approaches linking chemical pollution with ecological alterations. Emerging and Priority Pollutants in Rivers, The Handbook of Environmental Chemistry 2012, vol. 19:181-218. Springer-Verlag, Berlin, Heidelberg.
27. Hillebrand H., Sommer U. Effect of continuous nutrient enrichment on microalgae colonizing hard substrates. Hydrobiologia 2000, 426:185-192.
28. Hughes R., Byrnes J., Kimbro D., Stachowicz J. Reciprocal relationship and potential feedbacks between biodiversity and disturbance. Ecology Let. 2007, 10:849-864.
29. Ivorra N., Bremer S., Guasch H., Kraak M.H.S., Admiraal W. Differences in the sensitivity of benthic microalgae to Zn and Cd regarding biofilm development and exposure history. Environ. Toxicol. Chem. 2000, 19(5):1332-1339.
30. Junghans M., Backhaus T., Faust M., Scholze M., Grimme L.H. Predictability of combined effects of eight chloroacetanilide herbicides on algal reproduction. Pest Manag. Sci. 2003, 59:1101-1110.
31. Jurgensen T.A., Hoagland K.D. Effects of short-term pulses of atrazine on attached algal communities in a small stream. Arch. Environ. Contam. Toxicol. 1990, 19:617-623.
32. Knapp C.W., Graham D.W., Berardesco G., deNoyelles F., Cutak B.J., Larive C.K. Nutrient level, microbial activity, and alachlor transformation in aerobic aquatic systems. Water Res. 2003, 37:4761-4769.
33. Kreuger J. Pesticides in stream water within an agricultural catchment in southern Sweden, 1990-1996. Sci. Total Environ. 1998, 216:227-251.
34. Kröpfl K., Vladár P., Szabó K., Acs E., Borsodi A.K., Szikora S., Caroli S., Záray G. Chemical and biological characterisation of biofilms formed on different substrata in Tisza river (Hungary). Environ. Pollut. 2006, 144:626-631.
35. Laabs V., Wehrhan A., Pinto A., Dores E., Amelung W. Pesticide fate in tropical wetlands of Brazil; an aquatic microcosm study under semi-field conditions. Chemosphere 2007, 67:975-989.
36. Lane C.M., Taffs K.H., Corfield J.L. A comparison of diatom community structure on natural and artificial substrata. Hydrobiologia 2003, 493(1-3):65-79.
37. Lawrence J.R., Kopf G., Headley J.V., Neu T.R. Sorption and metabolism of selected herbicides in river biofilm communities. Can. J. Microbiol. 2001, 47:634-641.
38. Leflaive J., Céréghino R., Danger M., Lacroix G., Ten-Hage L. Assessment of self -organizing maps to analyse sole - carbon source utilization profiles. J. Microbiol. Methods 2005, 62:89-102.
39. Liu H.J., Xiong M. Comparative toxicity of racemic metolachlor and S-metolachlor to Chlorella pyrenoidosa. Aquat. Toxicol. 2009, 93:100-106.
40. Lyautey E., Lacoste B., Ten-Hage L., Rols J.L., Garabetian F. Analysis of bacterial diversity in river biofilms using 16S rDNA PCR-DGGE: methodological settings and fingerprints interpretation. Water Res. 2005, 39:380-388.
41. Lyautey E., Jackson C.R., Cayrou J., Rols J.L., Garabetian F. Bacterial community succession in natural river biofilm assemblages. Microb. Ecol. 2005, 50:589-601.
42. Mac Cann K. The diversity-stability debate. Nature 2000, 405:228-233.
43. Mohr S., Feibicke M., Berghahn R., Schmiediche R., Schmidt R. Response of plankton communities in freshwater pond and stream mesocosms to the herbicide metazachlor. Environ. Pollut. 2008, 152:530-542.
44. Montuelle B., Dorigo U., Berard A., Volat B., Bouchez A., Tlili A., Gouy V., Pesce S. 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 2011, 657:123-141.
45. Morin S., Bottin M., Mazzella N., Macary F., Delmas F., Winterton P., Coste M. Linking diatom community structure to pesticide input as evaluated through a spatial contamination potential (Phytopixal): a case study in the Neste river system (South-West France). Aquat. Toxicol. 2009, 94:28-39.
46. Murdock J.N., Dodds W.K. Linking benthic algal biomass to stream substratum topography. J. Phycol. 2007, 43:449-460.
47. Noack U., Geffke T., Balasubramanian R., Papenbrock J., Braune M., Scheerbaum D. Effects of the herbicide metazachlor on phytoplankton and periphyton communities in outdoor mesocosms. Acta Hydrochim. Hydrobiol. 2004, 31:482-490.
48. Osborne C.A., Rees G.N., Bernstein Y., Janssen P.H. New threshold and confidence estimates for terminal restriction fragment length polymorphism analysis of complex bacterial communities. Appl. Environ. Microbiol. 2006, 72:1270-1278.
49. Pappas J.L., Stoermer E.F. Quantitative method for determining a representative algal sample count. J. Phycol. 1996, 32:693-696.
50. Passy S.I. Diatom ecological guilds display distinct and predictable behavior along nutrient and disturbance gradients in running waters. Aquat. Bot. 2007, 86:171-178.
51. Paule A., Lauga B., Ten-Hage L., Morchain J., Duran R., Paul E., Rols J.L. A photosynthetic rotating annular bioreactor (Taylor-Couette type flow) for phototrophic biofilms cultures. Water Res. 2011, 45:6107-6118.
52. Paule A., Lyautey E., Garabetian F., Rols J.L. Autogenic versus environmental control during development of river biofilm. Ann. Limnol-Int. J. Lim. 2009, 45:1-10.
53. Payraudeau S., Junker P., Imfeld G., Gregoire C. Characterizing hydrological connectivity to identify critical source areas for pesticides losses. 18th World IMACS/MODSIM Congress: Interfacing Modelling and Simulation with Mathematical and Computational Sciences 2009, 1879-1885.
54. Pesce S., Fajon C., Bardot C., Bonnemoy F., Portelli C., Bohatier J. Effects of the phenylurea herbicide diuron on natural riverine microbial communities in an experimental study. Aquat. Toxicol. 2006, 78:303-314.
55. Pesce S., Bouchez A., Montuelle B. Effects of organic herbicides on phototrophic microbial communities in freshwater ecosystems. Rev. Environ. Contam. Toxicol. 2011, 214:87-124.
56. Pratt J.R., Barreiro R. Influence of trophic status on the toxic effects of herbicide: a microcosm study. Arch. Environ. Contam. Toxicol. 1998, 35:404-411.
57. Relyea R.A. A cocktail of contaminants: how mixtures of pesticides at low concentrations affect aquatic communities. Oecologia 2009, 159:363-376.
58. Rimet F., Bouchez A. Use of diatom life-forms and ecological guilds to assess pesticide contamination in rivers: lotic mesocosm approaches. Ecol. Indic. 2011, 11:489-499.
59. Roubeix V., Mazzella N., Mechin B., Coste M., Delmas F. Impact of the herbicide metolachlor on river periphytic diatoms: experimental comparison of descriptors at different biological organization levels. Ann. Limnol-Int. J. Lim. 2011, 47:239-249.
60. Roubeix V., Mazzella N., Schouler L., Fauvelle V., Morin S., Coste M., Delmas F., Margoum C. Variations of periphytic diatom sensitivity to the herbicide diuron and relation to species distribution in a contamination gradient: implications for biomonitoring. J. Environ. Monit. 2011, 13:1768-1774.
61. Roubeix V., Fauvelle V., Tison-Rosebery J., Mazzella N., Coste M., Delmas F. Assessing the impact of chloroacetanilide herbicides and their metabolites on periphyton in the Leyre River (SW France) via short term growth inhibition tests on autochthonous diatoms. J. Environ. Monit. 2012, 14:1655-1663.
62. Singh S., Datta P. Growth and survival potentials of immobilized diazotrophic cyanobacterial isolates exposed to common ricefield herbicides. World J. Microbiol. Biotechnol. 2005, 21:441-446.
63. Smith C.J., Danilowicz B.S., Clear A.K., Costello F.J., Wilson B., Meijer W.G. T-Align, a web-based tool for comparison of multiple terminal restriction fragment length polymorphism profiles. FEMS Microbiol. Ecol. 2005, 54:375-380.
64. Spawn R., Hoagland K.D., Siegfried B. Effects of alachlor on an algal community from a midwestern agricultural stream. Environ. Toxicol. Chem. 1997, 16:785-793.
65. Taghavi L., Probst J.L., Merlina G., Marchand A.L., Durbe G., Probst A. Flood event impact on pesticide transfer in a small agricultural catchment (Montousse at Aurade, south west France). Int. J. Environ. Anal. Chem. 2010, 90:3-6.
66. Tlili A., Dorigo U., Montuelle B., Margoum C., Carluer N., Gouy V., Bouchez A., Berard A. Responses of chronically contaminated biofilms to short pulses of diuron - an experimental study simulating flooding events in a small river. Aquat. Toxicol. 2008, 87:252-263.
67. 3- dependence of the tolerance of autotrophic and heterotrophic biofilm communities to copper and diuron. Aquat. Toxicol. 2010, 98:165-177.
68. Tlili A., Montuelle B., Berard A., Bouchez A. Impact of chronic and acute pesticide exposures on periphyton communities. Sci. Total Environ. 2011, 409:2102-2113.
69. Utermöhl H. Zur vervollkommnung der quantitativen phytoplankton methodik. Mitteilungen Internationale Vereinigung für Theoretische und Angewandte Limnologie 1958, 9:1-38.
70. Valloton N., Moser D., Eggen R.I.L., Junghans M., Chèvre N. S-metolachlor pulse exposure on the algae Scenedesmus vacuolatus: effects during exposure and the subsequent recovery. Chemosphere 2008, 73:395-400.
71. Vercraene-Eairmal M., Lauga B., Saint Laurent S., Mazella N., Boutry S., Simon M., Solange K., Delmas F., Duran R. Diuron biotransformation and its effects on biofilm bacterial community structure. Chemosphere 2010, 81:837-843.
72. Villeneuve A., Bouchez A., Montuelle B. In situ interactions between the effects of season, current velocity and pollution on a river biofilm. Freshw. Biol. 2011, 56:2245-2259.
73. Villeneuve A., Montuelle B., Bouchez A. Effects of flow regime and pesticides on periphytic communities: evolution and role of biodiversity. Aquat. Toxicol. 2011, 102:123-133.
74. Villeneuve A., Larroudé S., Humbert J.F. Herbicide contamination of freshwater ecosystem: impact on microbial communities. Pesticides - Formulations, Effects, Fate 2011, 285-312. InTech, Rijeka, Croatia. M. Stoytcheva (Ed.).
75. Wicke D., Bockelmann U., Reemtsma T. Environmental influences on the partitioning and diffusion of hydrophobic organic contaminants in microbial Biofilms. Environ. Sci. Technol. 2008, 42:1990-1996.
76. Zhang Q.G., Zhang D.Y. Species richness destabilizes ecosystem functioning in experimental aquatic microcosms. Oikos 2006, 112:218-226.
77. Zippel B., Neu T.R. Growth and structure of phototrophic biofilms under controlled light conditions. Water Sci. Technol. 2005, 52:203-209.