Skip to main content
Log in

Sublethal Effects of Three Pesticides on Larval Survivorship, Growth, and Macromolecule Production in the Aquatic Midge, Chironomus tentans (Diptera: Chironomidae)

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

Abstract

Effects of long-term exposure to each of three pesticides including atrazine, DDT, and chlorpyrifos on larval survivorship, growth, and macromolecule (total body protein and RNA) production were evaluated in the aquatic midge, Chironomus tentans, under laboratory conditions. Newly hatched larvae were exposed to atrazine at 30 and 150 μg/L, DDT at 0.01 and 0.05 μg/L, or chlorpyrifos at 0.02 and 0.10 μg/L throughout one life cycle. Larval survivorship was evaluated at 20 d and the end of the test, and larval growth at 20 d. Chlorpyrifos at 0.1 μg/L reduced the midge survivorship by 67% after 20-d exposure. However, neither atrazine nor DDT affected larval survivorship. The ash-free dry weight of midge larvae exposed to chlorpyrifos at 0.1 μg/L was 1.5-fold greater than that of the control whereas neither atrazine nor DDT showed a significant effect on the ash-free dry weight. In addition, exposures of midges to chlorpyrifos at 0.1 μg/L increased the adult emergence rate by 81% as compared to the control although the actual number of adults that emerged from chlorpyrifos-treated larvae was significantly decreased. Both the increased ash-free dry weight of larvae and increased adult emergence rate were likely caused by reduced competition for both food and space among the survivors due to increased larval mortality. Although neither total protein nor total RNA production was significantly affected in larvae exposed to each pesticide for 20 d, a significantly higher number of males over females (ratio = 4) emerged from midges exposed to DDT at 0.05 μg/L. Our study indicates that chronic exposure to low concentrations of chlorpyrifos and DDT results in significant mortality of midge larvae and alteration of the sex ratio of adult emergence, respectively. Because midges are important components of the food web, our results suggest that effects elicited directly or indirectly by long-term pesticide exposures may potentially disrupt both food chains and community structure in aquatic environments.

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.

Figure 1

Similar content being viewed by others

References

  • Anderson TD, Lydy MJ (2002) Increased toxicity to invertebrates associated with a mixture of atrazine and organophosphate insecticides. Environ Toxicol Chem 21:1507–1514

    Article  CAS  Google Scholar 

  • Anderson TD, Zhu KY (2004) Synergistic and antagonistic effects of atrazine on the toxicity of organophosphorodithioate- and organophosphorothioate-insecticides to Chironomus tentans (Diptera: Chironomidae). Pestic Biochem Physiol 80:54–64

    Article  CAS  Google Scholar 

  • Ankley GT, Benoit DA, Hoke RA, Leonard EN, West CW, Phipps GL, Mattson VC, Anderson LA (1993) Development and evaluation of test methods for benthic invertebrates and sediment: effects of flow rate and feeding on water quality and exposure conditions. Arch Environ Contam Toxicol 25:12–19

    Article  CAS  Google Scholar 

  • Ankley GT, Benoit DA, Balogh JC, Reynoldson TB, Day KE, Hoke RA (1994) Evaluation of potential confounding factors in sediment toxicity tests with three freshwater benthic invertebrates. Environ Toxicol Chem 13:627–635

    CAS  Google Scholar 

  • Armitage PD, Cranston PS, Pinder LCV (1995) The Chironomidae: Biology and ecology of non-biting midges. Chapman & Hall, New York

    Google Scholar 

  • Benoit DA, Sibley PK, Juenemann JL, Ankley GT (1997) Chironomus tentans life-cycle test: Design and evaluation for use in assessing toxicity of contaminated sediments. Environ Toxicol Chem 16:1165–1176

    Article  CAS  Google Scholar 

  • Burton GA, Norberg-King TJ, Ingersoll CG, Benoit DA, Ankley GT, Winger PV, Kubitz J, Lazorchak JM, Smith ME, Greer E, Dwyer FJ, Call DJ, Day KE (1996) Interlaboratory study of precision: Hyalella azteca and Chironomus tentans freshwater sediment toxicity assays. Environ Toxicol Chem 15:1335–1343

    Article  CAS  Google Scholar 

  • Chung RA, Huang IL, Brown RW (1967) Studies of DNA, RNA and protein synthesis in Hela S cells exposed to DDT and dieldrin. J Agric Food Chem15:254–259

    Article  Google Scholar 

  • Dewey SL (1986) Effects of the herbicide atrazine on aquatic insect community structure and emergence. Ecology 67:148–162

    Article  CAS  Google Scholar 

  • Eaton HJ, Lydy MJ (2000) Assessment of water quality in Wichita, Kansas, using index of biotic integrity and analysis of bed sediment and fish tissue for organochlorine insecticides. Arch. Environ Contam Toxicol 39:531–540

    Article  CAS  Google Scholar 

  • Gauss JD, Woods PE, Winner RW, Skillings JH (1985) Acute toxicity of copper to three stages of Chironomus tentans as affected by water hardness and alkalinity. Environ Pollut Ser A 37:149–157

    Article  CAS  Google Scholar 

  • Hoffman ER, Fisher SW (1995) Comparison of a field and laboratory-derived population of Chironomus riparius (Diptera: Chironomidae): Biochemical and fitness evidence for population divergence. J Econ Entomol 87:318–325

    Google Scholar 

  • Hoffman RS, Capel PD, Larson SJ (2000) Comparison of pesticides in eight US urban streams. Environ Toxicol Chem 19: 2249 – 2258

    Article  CAS  Google Scholar 

  • Hoke RA, Ankley GT, Kosian PA, Cotter M, Vandermeiden FM, Balcer M, Phipps GL, West C, Cox J (1997) Equilibrium partitioning as the basis for an integrated laboratory and field assessment of the impacts of DDT, DDE and DDD in sediments. Ecotoxicology 6:101–125

    Article  CAS  Google Scholar 

  • Jin-Clark Y, Lydy MJ, Zhu KY (2002) Effects of atrazine and cyanazine on chlorpyrifos toxicity in Chironomus tentans (Diptera: Chironomidae). Environ Toxicol Chem 3:598–603

    Article  Google Scholar 

  • Kiely T, Donaldson D, Grube A (2004) Pesticides industry sales and usage: 2000 and 2001 market estimates. U.S. EPA, Washington, DC

    Google Scholar 

  • Kosalwat P, Knight A (1987) Chronic toxicity of copper to a partial life cycle of the midge, Chironomus decorus. Arch Environ Contam Toxicol 16:283–290

    Article  CAS  Google Scholar 

  • Larson SJ, Gilliom RJ, Capel P (1999) Pesticides in streams of the United States. Initial results from the National Water Quality Assessment Program. US Geological Survey Water Resources Investigation Report 98-4222. US Geological Survey, Reston, VA

  • Lydy MJ, Belden JB, Ternes MA (1999) Effects of temperature on the toxicity of M-parathion, chlorpyrifos, and pentachlorobenzene to Chironomus tentans. Arch Environ Contam Toxicol 37: 542–547

    Article  CAS  Google Scholar 

  • Macek KJ, Burton KS, Sauter S, Gnilka S, Dean JW (1976) Chronic toxicity of atrazine to selected aquatic invertebrates and fishes. EPA-600/3-76-047U.S. National Technical Information Service, Springfield, VA

  • Myhr BC (1973) A screen for pesticide toxicity to protein and RNA synthesis in hella cells. J Agric Food Chem 21:362–367

    Article  CAS  Google Scholar 

  • Pape-Lindstrom PA, Lydy MJ (1997) Synergistic toxicity of atrazine and organophosphate insecticides contravenes the response addition mixture model. Environ Toxicol Chem 16: 2415–2420

    Article  CAS  Google Scholar 

  • Poly Software International (2002) ProStat version 3, Poly Software International. Pearl River, New York

    Google Scholar 

  • Richards SM, Kendall RJ (2002) Biochemical effects of chlorpyrifos on two developmental stages of Xenopus laevis. Environ Toxicol Chem 21:1826–1835

    Article  CAS  Google Scholar 

  • Saxena PK, Lal SR (1981) Seasonal changes in testes and thumb pads of the toad, Bufo marinus (Linn.) and their correlation with fluctuations in the environmental factors. Anat Anz 149:337–344

    CAS  Google Scholar 

  • Schroder I, Meyer M, Mucke D (1970) Effects of the herbicides 2, 4-D aminotriazole, atrazine, chlorprophan and chlorflunerol on nucleic-acid biosynthesis in the ascomycete Neurospora crassa. Weed Res 10:172–177

    Article  Google Scholar 

  • Sibley PK, Ankley GT, Cotter AM, Leonard EN (1996) Predicting chronic toxicity of sediments spiked with zinc: an evaluation of the acid-volatile sulfide model using a life-cycle test with the midge Chironomus tentans. Environ Toxicol Chem 15:2102–2112

    Article  CAS  Google Scholar 

  • Sibley PK, Benoit DA, Ankley GT (1997a) The significance of growth in Chironomus tentans sediment toxicity tests: Relationship to reproduction and demographic endpoints. Environ Toxicol Chem 16:336–345

    Article  CAS  Google Scholar 

  • Sibley PK, Monson PD, Ankley GT (1997b) The effect of gut contents on dry weight estimates of Chironomus tentans larvae: implications for interpreting toxicity in freshwater sediment toxicity tests. Environ Toxicol Chem 16:1721–1726

    Article  CAS  Google Scholar 

  • Sibley PK, Benoit DA, Balcer MD, Phipps GL, West CW, Hoke RA, Ankley GT (1999) In situ bioassay chamber for assessment of sediment toxicity and bioaccumulation using benthic invertebrates. Environ Toxicol Chem 18: 2325–2336

    Article  CAS  Google Scholar 

  • USGS (1999) The quality of our nation’s waters: nutrients and pesticides. Circular 1225, US Geological Survey, Reston, VA

  • USGS (2000) Pesticides in stream sediment and aquatic biota. Fact Sheet 092-00, US Geological Survey, Reston, VA

  • US EPA (1993) Standard operating procedures for laboratory cultures of Chironomus tentans. ERL-D-Sop CTI-015, Office of Research and Development, US Environmental Protection Agency, Duluth, MN

  • US EPA (2000) Methods for measuring the toxicity and bioaccumulation of sediment-associated contaminants with freshwater vertebrates, 2nd ed, EPA 600/R-99/064, US Environmental Protection Agency, Cincinnati, OH

  • Watts MM, Pascoe D (2000) Comparison of Chironomus riparius Meigen and Chironomus tentans Fabricius (Diptera: Chironomidae) for assessing the toxicity of sediments. Environ Toxicol Chem 19:1885–1892

    Article  CAS  Google Scholar 

  • Zhu KY, Gao JR (1999) Increased activity associated with reduced sensitivity of acetylcholinesterase in organophosphate-resistant greenbug, Schizaphis graminum (Homoptera: Aphididae). Pestic Sci 55:11–17

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Sharon R. Starkey for her technical assistance and Dr. Jeff Whitworth for reviewing an earlier version of this manuscript. This research was partially supported by the USDA NRI program through Southern Illinois University-Carbondale and the Kansas Agricultural Experiment Station, Kansas State University to K.Y.Z. and the Fulbright scholarship to M.R. This manuscript is contribution No. 06-27-J from the Kansas Agricultural Experiment Station. The Chironomus tentans voucher specimens (110) are located in the Museum of Entomological and Prairie Arthropod Research, Kansas State University, Manhattan, Kansas, USA.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kun Yan Zhu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rakotondravelo, M.L., Anderson, T.D., Charlton, R.E. et al. Sublethal Effects of Three Pesticides on Larval Survivorship, Growth, and Macromolecule Production in the Aquatic Midge, Chironomus tentans (Diptera: Chironomidae). Arch Environ Contam Toxicol 51, 352–359 (2006). https://doi.org/10.1007/s00244-005-0219-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-005-0219-0

Keywords

Navigation