Skip to main content
Log in

Response of Phytoplankton Community to Low-Dose Atrazine Exposure Combined with Phosphorus Fluctuations

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

The effects of atrazine on a controlled phytoplankton community derived from a natural freshwater wetland exposed to low doses of this photosynthesis-inhibiting herbicide were examined. The community was exposed for 7 weeks to doses of 0.1, 1, and 10 μg L−1 atrazine, combined with changes in nutrient concentration, and the photosynthetic activity, biomass, and community structure were noted during the experiment. Responses of the phytoplankton community were examined in terms of photosynthetic activity, biomass, and community structure. Significant effects of atrazine on the phytoplankton assemblage, in terms of primary production and community structure, were highlighted, even at doses as low as 1 and 0.1 μg L−1, when associated with phosphorus fluctuations. The most abundant Chlorophyceae decreased in concentration with increasing atrazine dose, whereas cyanobacteria were more tolerant to atrazine, particularly with increased nutrient supply. The subinhibitory doses of atrazine used in the present study confirmed the higher sensitivity of long-term exposure of multispecies assemblages under resource competition. Our study supports the emerging hypothesis that the increasing prevalence of cyanobacterial blooms in European aquatic systems may result from a combination of unbalanced nutrient enrichment and selective pressures from multiple toxicants.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alekseeva T, Besse P, Binet F, Delort AM, Forano C, Josselin N, Sancelme M, Tixier CT (2006) Influence of components from soil and earthworm cast on atrazine adsorption and biodegradation. Eur J Soil Sci 57(3):295–307

    Article  CAS  Google Scholar 

  • Altenburger R, Walter H, Grote M (2004) What contributes to the combined effect of a complex mixture? Environ Sci Technol 38:6353–6362

    Article  CAS  Google Scholar 

  • Bailer AJ, Oris JT (1993) Modelling reproductive toxicity in Ceriodaphnia tests. Environ Toxicol Chem 12:787–791

    Article  Google Scholar 

  • Bailer AJ, Oris JT (1997) Estimating inhibition concentrations for different response scales using generalized linear models. Environ Toxicol Chem 16:1554–1559

    Article  CAS  Google Scholar 

  • Bérard A, Pelte T, Menthon E, Druart J-C, Bourrain X (1998) Caractérisation du phytoplancton de deux systèmes limniques vis-à-vis d’un herbicide inhibiteur de la photosynthèse. La méthode PICT (pollution induced community tolerance): application et signification. Ann Limnol 34:269–282

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bérard A, Dorigo U, Mercier I, Becker-Van-Slooten K, Grandjean D, Leboulanger C (2003) Comparaison 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

    Article  CAS  Google Scholar 

  • Benzécri JP (1973) L’analyse des correspondances. Dunod, Paris

    Google Scholar 

  • Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310

    Article  Google Scholar 

  • deNoyelles F Jr, Kettle WD, Sinn DE (1982) The response of plankton communities in experimental ponds to atrazine, the most heavily used pesticide in the United States. Ecology 63:1285–1293

    Article  CAS  Google Scholar 

  • DIREN Bertagne (2001) L’eau en Bretagne-Bilan 2000. Direction Régionale de l’Environnement Bretagne

  • Donohue I, Irvine K (2008) Quantifying variability within waters samples: the need for adequate subsampling. Water Res 42:476–482

    Article  CAS  Google Scholar 

  • Egorova EA, Bukhov NG (2006) Mechanisms and functions of photosystem I-related alternative electron transport pathways in chloroplasts. Russ J Plant Physiol 53:645–657

    Google Scholar 

  • Garcia-Villada L, Rico M, Altamirano M, S!anchez-Martin L, Lopez-Rodas V, Costas E (2004) Occurrence of copper resistant mutants in the toxic cyanobacteria Microcystis aeruginosa: characterisation and future implications in the use of copper sulphate as algaecide. Water Res 38:2207–2213

    Article  CAS  Google Scholar 

  • Graymore M, Stagnitti F, Allinson G (2001) Impacts of atrazine in aquatic ecosystems. Environ Int 26:483–495

    Article  CAS  Google Scholar 

  • Gustavson K, Wangberg SA (1995) Tolerance induction and succession in microalgae communities exposed to copper and atrazine. Aquatic Toxicol 32:283–302

    Article  CAS  Google Scholar 

  • Hambright KD, Zohary T (2000) Phytoplankton species diversity controlled through competitive exclusion and physical disturbances. Limnol Oceanogr 45:110–122

    Google Scholar 

  • Hayes T, Haston K, Tsui M, Hoang A, Haeffele C, Vonk A (2003) Atrazine-induced hermaphroditism at 0.1 ppb in American leopard frogs (Rana Pipiens): laboratory and field evidence. Environ Health Persp 111:568–575

    CAS  Google Scholar 

  • Huber W (1993) Ecotoxicological relevance of atrazine in aquatic systems. Environ Toxicol Chem 12:1865–1881

    Article  CAS  Google Scholar 

  • IFEN (2006) Les pesticides dans les eaux—données 2003 et 2004. Dossier de l’Institut Français de l’Environnement. IFEN

  • Jarvie HP, Neal C, Withers PJA (2006) Sewage-effluent phosphorus: A greater risk to river eutrophication than agricultural phosphorus? Sci Total Environ 360:246–253

    Article  CAS  Google Scholar 

  • Klassen HE, Kadoum AM (1979) Distribution and retention of atrazine and carbofuran in farm pond ecosystems. Arch Environ Contam Toxicol 8:345–353

    Article  Google Scholar 

  • Koenig F (1990) Shade adaptation in cyanobacteria-Further characterization of Anacystis shade phenotype as induced by sublethal concentrations of DCMU-type inhibitors in strong light. Photosynth Res 26:29–37

    CAS  Google Scholar 

  • Lampert W, Fleckner W, Pott E, Schober U, Störkel K-U (1989) Herbicide effects on planktonic systems of different complexity. Hydrobiologia 188–189:415–424

    Google Scholar 

  • Leboulanger C, Rimet F, Lacotte MH, Berard 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

    Article  CAS  Google Scholar 

  • Lorenzen CJ (1967) Determination of chlorophyll and phaeo-pigments: spectrophotometric equations. Limnol Oceanogr 12:343–346

    Article  CAS  Google Scholar 

  • Ma J, Lu N, Qin W, Xu R, Wang Y, Chen X (2006) Differential responses of eight cyanobacterial and green algal species, to carbamate insecticides. Ecotoxicol Environ Safety 63:268–274

    Article  CAS  Google Scholar 

  • Murphy MB, Hecker M, Coady KK, Tompsett AR, Jones PD, Du Preez LH, Everson GJ, Solomon KR, Carr JA, Smith EE, Kendall RJ, Van der Kraak G, Giesy JP (2006) Atrazine concentrations, gonadal gross morphology and histology in ranid frogs collected in Michigan agricultural areas. Aquatic Toxicol 76:230–245

    Article  CAS  Google Scholar 

  • Naselli-Flores L, Padisak J, Dokulil MT, Chorus I (2003) Equilibrium/steady-state concept in phytoplankton ecology. Hydrobiologia 502:395–403

    Article  Google Scholar 

  • Navarro E, Guasch H, Sabater S (2002) Use of microbenthic algal communities in ecotoxicological tests for the assessment of water quality: the Ter river case study. J Appl Phycol 14:41–48

    Article  Google Scholar 

  • Nicholls K, Dillon P (1978) An evaluation of phosphorus-chlorophyll-phytoplankton relationships of lakes. Int Rev Gesamten Hydrobiol 63:141–154

    Article  CAS  Google Scholar 

  • Reynolds CS, Padisak J, Sommer U (1993) Intermediate disturbance in the ecology of phytoplankton and the maintenance of species diversity: a synthesis. Hydrobiologia 249:183–188

    Article  Google Scholar 

  • Reynolds CS, Huszar V, Kruk C, Naselli-Flores L, Melo S (2002) Towards a functional classification of the freshwater phytoplankton. J Plank Res 24:417–428

    Article  Google Scholar 

  • Schwarzenbach RP, Escher BI, Fenner K, Hofstetter TB, Johnson CA, von Gunten U, Wehrli B (2006) The challenge of micropollutants in aquatic systems. Science 313:1072–1077

    Article  CAS  Google Scholar 

  • Seguin F, Leboulanger C, Rimet F, Druart J-C, Bérard A (2001) Effects of atrazine and nicosulfuron on phytoplankton in systems of increasing complexity. Arch Environ Contam Toxicol 40:198–208

    Article  CAS  Google Scholar 

  • Seguin F, Bihan FL, Leboulanger C, Berard A (2002) A risk assessment of pollution: induction of atrazine tolerance in phytoplankton communities in freshwater outdoor mesocosms, using chlorophyll fluorescence as an endpoint. Water Res 36:3227–3236

    Article  CAS  Google Scholar 

  • Simpson EH (1949) Measurement of diversity. Nature 163:688

    Article  Google Scholar 

  • Solomon KR, Baker DB, Richards RP, Dixon KR, Klaine SJ, La Point TW, Kendall RJ, Giddings JM, Giesy JP, Hall LW Jr, Williams WM (1996) Ecological risk assessment of atrazine in North American surface waters. Environ Toxicol Chem 15:31–76

    Article  CAS  Google Scholar 

  • Sommer U (1995) An experimental test of the intermediate disturbance hypothesis using cultures of marine phytoplankton. Limnol Oceanogr 40:1271–1277

    Google Scholar 

  • Steemann-Nielsen E (1952) The use of radioactive carbon (14C) for measuring organic production in the sea. J Cons Int Explor Mer 18:117–140

    Google Scholar 

  • Tang JX, Hoagland KD, Siegfried BD (1997) Differential toxicity of atrazine to selected freshwater algae. Bull Environ Contam Toxicol 59:631–637

    Article  CAS  Google Scholar 

  • Tang J, Hoagland KD, Siegfried BD (1998) Uptake and bioconcentration of atrazine by selected freshwater algae. Environ Toxicol Chem 17:1085–1090

    Article  CAS  Google Scholar 

  • Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton, NJ

    Google Scholar 

  • World Health Organization (2000) Atrazine. In: Directives pour la qualité de l’eau de boisson, vol 2. Critères d’hygiène et documentation à l’appui. WHO, Genève, pp 654–661

    Google Scholar 

Download references

Acknowledgments

This study received financial support from the CNRS through the PEVS/Tranzat program awarded to F. Binet. We are grateful to the people who helped with laboratory analyses and species determination: M. P. Briand, N. Josselin, and L. Brient, from UMR Ecobio, and S. Nogre and J. Morvan, from the Ecole Nationale Supérieure de Chimie at Rennes. We also thank M. Bormans and the two anonymous reviewers for their useful comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Alexandrine Pannard or Françoise Binet.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pannard, A., Le Rouzic, B. & Binet, F. Response of Phytoplankton Community to Low-Dose Atrazine Exposure Combined with Phosphorus Fluctuations. Arch Environ Contam Toxicol 57, 50–59 (2009). https://doi.org/10.1007/s00244-008-9245-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-008-9245-z

Keywords

Navigation