Skip to main content
Log in

Effects of neonicotinoids on the emergence and composition of chironomids in the Prairie Pothole Region

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

Abstract

The use of neonicotinoid pesticides is widespread throughout agricultural regions, including the Prairie Pothole Region of North America. The occurrence of these pesticides to the abundant adjacent wetlands can result in impacts on nontarget insects, and cascading effects through wetland ecosystems. In the current study, field-based mesocosms were used to investigate the effects of multiple pulses of the neonicotinoid imidacloprid on the emergence and chironomid community composition, in an effort to simulate episodic rain events to Prairie Pothole Wetlands. Sediments from two local wetlands were placed into the mesocosm tanks and three imidacloprid pulses added, each 1 week apart at nominal concentrations of 0.2, 2.0, and 20 μg/L. Overall, a significant decrease in the emergence of adult chironomids was observed within the 2.0 μg/L and greater concentrations, with the subfamilies Chironominae and Tanypodinae showing a greater sensitivity than the members of the subfamily Orthocladiinae. The chironomid community also had a dose-related response, followed by a recovery of the community composition near the end of the experiment. Our results provide additional evidence that repeated pulses of imidacloprid may have effects on chironomids and other sensitive aquatic insects living within Prairie Pothole Wetlands, resulting in reduced food availability. We stress the need for continued monitoring of US surface waters for neonicotinoid compounds and the continuation of additional experiments looking into the impacts on aquatic communities.

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

Similar content being viewed by others

References

  • Alford A, Krupke CH (2017) Translocation of the neonicotinoid seed treatment clothianidin in maize. PLoS One 12:e0173836

    Article  CAS  Google Scholar 

  • Anderson TA, Salice CJ, Erickson RA, McMurry ST, Cox SB, Smith LM (2013) Effects of landuse and precipitation on pesticides and water quality in playa lakes of the southern high plains. Chemosphere 92:84–90

    Article  CAS  Google Scholar 

  • Anderson J, Dubetz C, Palace V (2015) Neonicotinoids in the Canadian aquatic environment: a literature review on current use products with a focus on fate, exposure, and biological effects. Sci Total Environ 505:409–422

    Article  CAS  Google Scholar 

  • Bazzanti M, Bambacigno F (1987) Chironomids as water quality indicators in the river Mignone (Central Italy). Hydrobiol Bull 21:213–222

    Article  Google Scholar 

  • Bengtson S-A (1972) Reproduction and fluctuations in the size of duck populations at Lake Mývatn, Iceland. Oikos 23:35–58

    Article  Google Scholar 

  • Caquet T, Hanson ML, Roucaute M, Graham DW, Lagadic L (2007) Influence of isolation on the recovery of pond mesocosms from the application of an insecticide. II. Benthic macroinvertebrate responses. Environ Toxicol Chem 26:1280–1290

    Article  CAS  Google Scholar 

  • Cavallaro MC, Morrissey CA, Headley JV, Peru KM, Liber K (2017) Comparative chronic toxicity of imidacloprid, clothianidin, and thiamethoxam to Chironomus dilutus and estimation of toxic equivalency factors. Environ Toxicol Chem 36:372–382

    Article  CAS  Google Scholar 

  • Chagnon M, Kreutzweiser D, Mitchell EA, Morrissey CA, Noome DA, Van der Sluijs JP (2015) Risks of large-scale use of systemic insecticides to ecosystem functioning and services. Environ Sci Pollut Res 22:119–134

    Article  CAS  Google Scholar 

  • Colombo V, Mohr S, Berghahn R, Pettigrove VJ (2013) Structural changes in a Macrozoobenthos assemblage after Imidacloprid pulses in aquatic field-based microcosms. Arch Environ Contam Toxicol 65:683–692

    Article  CAS  Google Scholar 

  • Douglas MR, Tooker JF (2015) Large-scale deployment of seed treatments has driven rapid increase in use of neonicotinoid insecticides and preemptive pest management in US field crops. Environ Sci Technol 49:5088–5097

    Article  CAS  Google Scholar 

  • Elbert A, Haas M, Springer B, Thielert W, Nauen R (2008) Applied aspects of neonicotinoid uses in crop protection. Pest Manag Sci 64:1099–1105

    Article  CAS  Google Scholar 

  • Gray LJ (1993) Response of insectivorous birds to emerging aquatic insects in riparian habitats of a tallgrass prairie stream. Am Midl Nat 129:288–300

    Article  Google Scholar 

  • Hayasaka D, Korenaga T, Suzuki K, Saito F, Sánchez-Bayo F, Goka K (2012) Cumulative ecological impacts of two successive annual treatments of imidacloprid and fipronil on aquatic communities of paddy mesocosms. Ecotoxicol Environ Saf 80:355–362

    Article  CAS  Google Scholar 

  • Hladik ML, Kolpin DW (2015) First national-scale reconnaissance of neonicotinoid insecticides in streams across the USA. Environ Chem 13:12–20

    Article  CAS  Google Scholar 

  • Hladik ML, Kolpin DW, Kuivila KM (2014) Widespread occurrence of neonicotinoid insecticides in streams in a high corn and soybean producing region, USA. Environ Pollut 193:189–196

    Article  CAS  Google Scholar 

  • Jeschke P, Nauen R, Schindler M, Elbert A (2010) Overview of the status and global strategy for neonicotinoids. J Agric Food Chem 59:2897–2908

    Article  CAS  Google Scholar 

  • Kreutzweiser DP, Back RC, Sutton TM, Thompson DG, Scarr TA (2002) Community-level disruptions among zooplankton of pond mesocosms treated with a neem (azadirachtin) insecticide. Aquat Toxicol 56:257–273

    Article  CAS  Google Scholar 

  • Liess M, Beketov M (2011) Traits and stress: keys to identify community effects of low levels of toxicants in test systems. Ecotoxicology 20:1328–1340

    Article  CAS  Google Scholar 

  • Main AR, Headley JV, Peru KM, Michel NL, Cessna AJ, Morrissey CA (2014) Widespread use and frequent detection of neonicotinoid insecticides in wetlands of Canada’s prairie pothole region. PLoS One 9:e92821

    Article  CAS  Google Scholar 

  • Main AR, Michel NL, Cavallaro MC, Headley JV, Peru KM, Morrissey CA (2016) Snowmelt transport of neonicotinoid insecticides to Canadian Prairie wetlands. Agric Ecosyst Environ 215:76–84

    Article  CAS  Google Scholar 

  • Merrit RW, Cummins KW, Berg MB (2008) An introduction to the aquatic insects of North America. Kendall/Hunt, Dubuque

  • Mohr S, Berghahn R, Schmiediche R, Hübner V, Loth S, Feibicke M, Mailahn W, Wogram J (2012) Macroinvertebrate community response to repeated short-term pulses of the insecticide imidacloprid. Aquat Toxicol 110:25–36

    Article  CAS  Google Scholar 

  • Morrissey CA, Mineau P, Devries JH, Sanchez-Bayo F, Liess M, Cavallaro MC, Liber K (2015) Neonicotinoid contamination of global surface waters and associated risk to aquatic invertebrates: a review. Environ Int 74:291–303

    Article  CAS  Google Scholar 

  • Mousavi SK, Primicerio R, Amundsen P-A (2003) Diversity and structure of Chironomidae (Diptera) communities along a gradient of heavy metal contamination in a subarctic watercourse. Sci Total Environ 307:93–110

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet G, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Henry M, Stevens H, Szeocs E (2017) vegan: Community Ecology Package. R package version 2.5-3. http://CRAN.R-project.org/package=vegan

  • Pestana J, Alexander A, Culp J, Baird D, Cessna A, Soares A (2009) Structural and functional responses of benthic invertebrates to imidacloprid in outdoor stream mesocosms. Environ Pollut 157:2328–2334

    Article  CAS  Google Scholar 

  • R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/

  • Roessink I, Merga LB, Zweers HJ, Van den Brink PJ (2013) The neonicotinoid imidacloprid shows high chronic toxicity to mayfly nymphs. Environ Toxicol Chem 32:1096–1100

    Article  CAS  Google Scholar 

  • Saether OA (1979) Chironomid communities as water quality indicators. Ecography 2:65–74

    Article  Google Scholar 

  • Sánchez-Bayo F, Goka K (2006) Ecological effects of the insecticide imidacloprid and a pollutant from antidandruff shampoo in experimental rice fields. Environ Toxicol Chem 25:1677–1687

    Article  Google Scholar 

  • Simpson GL (2016) Permute: functions for generating restricted permutations of data. R package version 0.9-4. http://CRAN.R-project.org/package=permute

  • Stehle S, Schulz R (2015) Agricultural insecticides threaten surface waters at the global scale. Proc Natl Acad Sci 112:5750–5755

    Article  CAS  Google Scholar 

  • Sur R, Stork A (2003) Uptake, translocation and metabolism of imidacloprid in plants. Bull Insectol 56:35–40

    Google Scholar 

  • Szöcs E, Van den Brink PJ, Lagadic L, Caquet T, Roucaute M, Auber A, Bayona Y, Liess M, Ebke P, Ippolito A, ter Braak CJF, Brock TCM, Schäfer RB (2015) Analysing chemical-induced changes in macroinvertebrate communities in aquatic mesocosm experiments: a comparison of methods. Ecotoxicology 24:760–769

    Article  CAS  Google Scholar 

  • Tokeshi M (1995) Life cycles and population dynamics, the Chironomidae. Springer, Berlin, pp 225–268

    Google Scholar 

  • Tomizawa M, Casida JE (2008) Molecular recognition of neonicotinoid insecticides: the determinants of life or death. Acc Chem Res 42:260–269

    Article  CAS  Google Scholar 

  • Touart LW, Slimak MW (1989) Mesocosm approach for assessing the ecological risk of pesticides. In: Voshell Jr. JR (ed) Using mesocosms to assess the aquatic ecological risk of pesticides: theory and practice. Entomological Society of America, Lanham, MD, p 33–40

  • Van Buuren S, Groothuis-Oudshoorn K (2010) Mice: multivariate imputation by chained equations in R. J Stat Softw 45:1–68

    Google Scholar 

  • Van den Brink PJ, Ter Braak CJ (1999) Principal response curves: analysis of time-dependent multivariate responses of biological community to stress. Environ Toxicol Chem 18:138–148

    Article  Google Scholar 

  • Van der Sluijs JP, Simon-Delso N, Goulson D, Maxim L, Bonmatin J-M, Belzunces LP (2013) Neonicotinoids, bee disorders and the sustainability of pollinator services. Curr Opin Environ Sustain 5:293–305

    Article  Google Scholar 

  • Weiderholm T (1989) The adult males of Chironomidae (Diptera) of the Holarctic region – Keys and diagnoses. Ent Scand Suppl 34:1–352

  • Wright CK, Wimberly MC (2013) Recent land use change in the Western Corn Belt threatens grasslands and wetlands. Proc Natl Acad Sci 110:4134–4139

    Article  Google Scholar 

Download references

Acknowledgements

We would like to thank Aiden Resh, Katherine Millette, Sara Bachmeier, Madison Sager, and Reed Junco for their assistance in data collection and lab processing of samples. We would also like to acknowledge the assistance provided by Dr. Leonard Ferrington and his expertise in chironomid identification and verification of samples. Also, I would like to acknowledge Dr. Ken Grafton for access and space to conduct the mesocosm study on the North Dakota Agricultural Experimental Station grounds.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nate Williams.

Additional information

Responsible editor: Philippe Garrigues

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Williams, N., Sweetman, J. Effects of neonicotinoids on the emergence and composition of chironomids in the Prairie Pothole Region. Environ Sci Pollut Res 26, 3862–3868 (2019). https://doi.org/10.1007/s11356-018-3683-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-3683-6

Keywords

Navigation