Skip to main content
SpringerLink
Log in

Pollution-induced community tolerance in benthic macroinvertebrates of a mildly lead-contaminated lake

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Pollution-induced community tolerance (PICT) has been used to demonstrate effects of sediment contamination on microbes and meiofauna. Our study explored the potential to detect PICT in benthic macroinvertebrates of a lake with long-term mild lead (Pb) contamination. We collected macrobenthos from two areas in Caddo Lake, Texas, a control area (CO) with a mean sediment Pb level of 11 μg/g and Goose Prairie (GP) where sediment Pb levels averaged 74 μg/g. Upon return to the laboratory, we exposed macroinvertebrates to a lethal lead concentration and assessed 48-h mortality. Mortality of CO macrobenthos was significantly higher than that of GP macrobenthos, providing evidence that these communities differed in their tolerance to lead. A comparison of macrobenthos community composition between the areas showed that the GP macrobenthos lacked metal-sensitive taxa such as gastropods and amphipods (which were present at CO). Similarly, a higher proportion of the GP benthos belonged to metal-tolerant taxa such as isopods and chironomids. Thus, changes in community composition appeared to be at least partly responsible for differences in community tolerance. Our results showed that a sediment Pb concentration below effect-based sediment quality guidelines had a measurable impact on macrobenthos, thus demonstrating that results from single-species toxicity tests may underestimate impacts on communities. This study also confirms that the PICT approach with macroinvertebrates is a feasible and potentially powerful approach for detecting contaminant impacts.

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

  • Adeyemi JA, Klerks PL (2013) Occurrence of copper acclimation in the least killifish Heterandria formosa, and associated biochemical and physiological mechanisms. Aquat Toxicol 130:51–57. doi:10.1016/j.aquatox.2013.01.001

    Article  Google Scholar 

  • Allert AL, DiStefano RJ, Fairchild JF, Schmitt CJ, McKee MJ, Girondo JA, Brumbaugh WG, May TW (2013) Effects of historical lead–zinc mining on riffle-dwelling benthic fish and crayfish in the Big River of southeastern Missouri, USA. Ecotoxicology 22:506–521. doi:10.1007/s10646-013-1043-3

    Article  CAS  Google Scholar 

  • Balthis WL, Hyland JL, Fulton MH, Pennington PL, Cooksey C, Key PB, DeLorenzo ME, Wirth EF (2010) Effects of chemically spiked sediments on estuarine benthic communities: a controlled mesocosm study. Environ Monitor Assessm 161:191–203

    Article  CAS  Google Scholar 

  • Berkson J (1951) Why I prefer logits to probits. Biometrics 7:327–339

    Article  Google Scholar 

  • Blanck H (2002) A critical review of procedures and approaches used for assessing pollution-induced community tolerance (PICT) in biotic communities. Human Ecol Risk Assessm 8:1003–1034

    Article  Google Scholar 

  • Blanck H, Dahl B (1996) Pollution-induced community tolerance (PICT) in marine periphyton in a gradient of tri-n-butyltin (TBT) contamination. Aquat Toxicol 35:59–77

    Article  CAS  Google Scholar 

  • Boivin M-EY, Breure AM, Posthuma L, Rutgers M (2002) Determination of field effects of contaminants—significance of pollution-induced community tolerance. Human Ecol Risk Assessm 8:1035–1055

    Article  Google Scholar 

  • Bonada N, Prat N, Resh VH, Statzner B (2006) Developments in aquatic insect biomonitoring: a comparative analysis of recent approaches. Annu Rev Entomol 51:495–523

    Article  CAS  Google Scholar 

  • Bufflap SE, Allen HE (1995) Sediment pore water collection methods for trace metal analysis: a review. Water Res 29:165–177. doi:10.1016/0043-1354(94)E0105-F

    Article  CAS  Google Scholar 

  • Clements WH (1999) Metal tolerance and predator-prey interactions in benthic macroinvertebrate stream communities. Ecol Appl 9:1073–1084

    Google Scholar 

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

    Book  Google Scholar 

  • Clements WH, Rohr JR (2009) Community responses to contaminants: using basic ecological principles to predict ecotoxicological effects. Environ Toxicol Chem 28:1789–1800

    Article  CAS  Google Scholar 

  • Eaton AD, Clesceri LS, Greenberg AE, Franson MAH, American Public Health Association, American Water Works Association, Water Environment Federation (1995) Standard methods for the examination of water and wastewater, 19th edn. American Public Health Association, Washington, DC

    Google Scholar 

  • Fernández-Calviño D, Arias-Estévez M, Díaz-Raviña M, Bååth E (2011) Bacterial pollution induced community tolerance (PICT) to Cu and interactions with pH in long-term polluted vineyard soils. Soil Biol Biochem 43:2324–2331. doi:10.1016/j.soilbio.2011.08.001

    Article  Google Scholar 

  • Grant A (2002) Pollution tolerant species and communities: intriguing toys or invaluable monitoring tools? Human Ecol Risk Assessm 8:955–970

    Article  Google Scholar 

  • Hoffman DJ, Rattner BA, Burton AB Jr, Cairns J Jr (1995) Handbook of ecotoxicology. CRC Press, Boca Raton, FL

    Google Scholar 

  • Hunt JW, Anderson BS, Phillips BM, Tjeerdema RS, Taberski KM, Wilson CJ, Puckett HM, Stephenson M, Fairey R, Oakden J (2001) A large-scale categorization of sites in San Francisco Bay, USA, based on the sediment quality triad, toxicity identification evaluations, and gradient studies. Environ Toxicol Chem 20:1252–1265. doi:10.1002/etc.5620200614

    Article  CAS  Google Scholar 

  • King RS, Richardson CJ (2002) Evaluating subsampling approaches and macroinvertebrate taxonomic resolution for wetland bioassessment. J N Am Benthol Soc 21:150–171. doi:10.2307/1468306

    Article  Google Scholar 

  • Klerks PL (2002) Adaptation, ecological impacts, and risk assessment: insights from research at Foundry Cove, Bayou Trepagnier and Pass Fourchon. Human Ecol Risk Assessm 8:971–982

    Article  Google Scholar 

  • Klerks PL, Levinton JS (1989) Rapid evolution of metal resistance in a benthic oligochaete inhabiting a metal-polluted site. Biol Bull 176:135–141

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • MacDonald DD, Ingersoll CG, Berger TA (2000) Development and evaluation of consensus-based sediment quality guidelines for freshwater ecosystems. Arch Environ Contam Toxicol 39:20–31

    Article  CAS  Google Scholar 

  • Malaj E, Grote M, Schäfer RB, Brack W, von der Ohe PC (2012) Physiological sensitivity of freshwater macroinvertebrates to heavy metals. Environ Toxicol Chem 31:1754–1764. doi:10.1002/etc.1868

    Article  CAS  Google Scholar 

  • Marqués MJ, Martínez-Conde E, Rovira JV (2003) Effects of zinc and lead mining on the benthic macroinvertebrates of a fluvial ecosystem. Water Air Soil Pollut 148:363–388. doi:10.1023/A:1025411932330

    Article  Google Scholar 

  • Millward RN, Grant A (1995) Assessing the impact of copper on nematode communities from a chronically metal-enriched estuary using pollution-induced community tolerance. Mar Pollut Bull 30:701–706

    Article  CAS  Google Scholar 

  • Millward RN, Grant A (2000) Pollution-induced tolerance to copper of nematode communities in the severely contaminated Restronguet Creek and adjacent estuaries, Cornwall, United Kingdom. Environ Toxicol Chem 19:454–461

    Article  CAS  Google Scholar 

  • Millward RN, Klerks PL (2002) Contaminant-adaptation and community tolerance in ecological risk assessment: introduction. Human Ecol Risk Assessm 8:921–932

    Article  Google Scholar 

  • Morgan AJ, Kille P, Stürzenbaum SR (2007) Microevolution and ecotoxicology of metals in invertebrates. Environ Sci Technol 41:1085–1096

    Article  CAS  Google Scholar 

  • Muyssen BTA, Janssen CR (2004) Multi-generation cadmium acclimation and tolerance in Daphnia magna Straus. Environ Pollut 130:309–316

    Article  CAS  Google Scholar 

  • Newman MC (1995) Quantitative methods in quantitative ecotoxicology. Lewis Publishers, Boca Raton

    Google Scholar 

  • Niklińska M, Chodak M, Laskowski R (2006) Pollution-induced community tolerance of microorganisms from forest soil organic layers polluted with Zn or Cu. Appl Soil Ecol 32:265–272. doi:10.1016/j.apsoil.2005.08.002

    Article  Google Scholar 

  • Pesce S, Lissalde S, Lavieille D, Margoum C, Mazzella N, Roubeix V, Montuelle B (2010) Evaluation of single and joint toxic effects of diuron and its main metabolites on natural phototrophic biofilms using a pollution-induced community tolerance (PICT) approach. Aquat Toxicol 99:492–499. doi:10.1016/j.aquatox.2010.06.006

    Article  CAS  Google Scholar 

  • Rice KC (1999) Trace-element concentrations in streambed sediment across the conterminous United States. Environ Sci Technol 33:2499–2504

  • Rotter S, Sans-Piché F, Streck G, Altenburger R, Schmitt-Jansen M (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, Veit U, Dudel G, Altenburger R (2008) Ecological perspective in aquatic ecotoxicology: approaches and challenges. Basic Appl Ecol 9:337–345

    Article  CAS  Google Scholar 

  • Schumacher BA (2002) Methods for the determination of total organic carbon (TOC) in soils and sediments. United States Environmental Protection Agency, Washington, DC

    Google Scholar 

  • Smith JG, Brandt CC, Christensen SW (2011) Long-term benthic macroinvertebrate community monitoring to assess pollution abatement effectiveness. Environ Manag 47:1077–1095

    Article  Google Scholar 

  • Tlili A, Berard A, Blanck H, Bouchez A, Cássio F, Eriksson KM, Morin S, Montuelle B, Navarro E, Pascoal C, Pesce S, Schmitt-Jansen M, Behra R (2016) Pollution-induced community tolerance (PICT): towards an ecologically relevant risk assessment of chemicals in aquatic systems. Freshwat Biol 61:2141–2151

    Article  CAS  Google Scholar 

  • Tlili A, Maréchal M, Bérard A, Volat B, Montuelle B (2011) 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

  • United States Environmental Protection Agency (2007) Method 3051a: microwave assisted acid digestion of sediments, sludges, soils, and oils. United States Environmental Protection Agency, Washington, DC

    Google Scholar 

  • Wilson JT (2003) Occurrence of and trends in selected sediment-associated contaminants in Caddo Lake, east Texas, 1940–2002. Water-Resources Investigations Report 03-4253. United States Geological Survey, Washington, DC

    Google Scholar 

Download references

Acknowledgments

This work was funded with student grants from the University of Louisiana at Lafayette Graduate Student Organization and the Ecology Center of the University of Louisiana at Lafayette. We thank Marvin “Trey” Mace III, Courtney Curtis, Emmanuel Blankson, Johanna Farmer, and Kruuttika Satbhai for the assistance in field sampling and/or laboratory processing of samples. We thank Kate Hayes-Huer for the assistance with the manuscript preparation.

Author information

Authors and Affiliations

  1. Department of Biology, University of Louisiana at Lafayette, P.O. Box 43602, Lafayette, LA, 70504, USA

    Andrew Y. Oguma & Paul L. Klerks

Authors
  1. Andrew Y. Oguma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul L. Klerks
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paul L. Klerks.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Thomas Hein

Electronic supplementary material

ESM 1

(DOCX 35 kb).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oguma, A.Y., Klerks, P.L. Pollution-induced community tolerance in benthic macroinvertebrates of a mildly lead-contaminated lake. Environ Sci Pollut Res 24, 19076–19085 (2017). https://doi.org/10.1007/s11356-017-9553-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-9553-9

Keywords

Search

Navigation