Comparison of metabolomic responses of earthworms to sub-lethal imidacloprid exposure in contact and soil tests
Eisenia fetida earthworms were exposed to sub-lethal levels of imidacloprid for 48 h via contact filter paper tests and soil tests. After the exposure, 1H nuclear magnetic resonance (NMR) metabolomics was used to measure earthworm sub-lethal responses by analyzing the changes in the polar metabolite profile. Maltose, glucose, malate, lactate/threonine, myo-inositol, glutamate, arginine, lysine, tyrosine, leucine, and phenylalanine relative concentrations were altered with imidacloprid exposure in soil. In addition to these metabolites (excluding leucine and phenylalanine), fumarate, ATP, inosine, betaine, scyllo-inositol, glutamine, valine, tryptophan, alanine, tyrosine, and isoleucine relative concentrations shifted with imidacloprid exposure during contact tests. Metabolite changes in E. fetida earthworms exposed to imidacloprid showed a non-linear concentration response and an upregulation in gluconeogenesis. Overall, imidacloprid exposure in soil induces a less pronounced response in metabolites glucose, maltose, fumarate, adenosine-5′-triphosphate (ATP), inosine, scyllo-inositol, lactate/threonine, and tyrosine in comparison to the response observed via contact tests. Thus, our study highlights that tests in soil can result in a different metabolic response in E. fetida and demonstrates the importance of different modes of exposure and the extent of metabolic perturbation in earthworms. Our study also emphasizes the underlying metabolic disruption of earthworms after acute sub-lethal exposure to imidacloprid. These observations should be further examined in different soil types to assess the sub-lethal toxicity of imidacloprid to soil-dwelling earthworms.
KeywordsEisenia fetida Neonicotinoids Energy disruption Contact exposure Soil exposure Gluconeogenesis
We extend our gratitude to Dr. Ronald Soong for technical assistance and valuable discussions.
We thank the National Sciences and Engineering Research Council (NSERC) of Canada Strategic Partnership Grant (STPGP 494273-16) for funding this study.
- Baskaran S, Kookana RS, Naidu R (1999) Degradation of bifenthrin, chlorpyrifos and imidacloprid in soil and bedding materials at termiticidal application rates. Pestic Sci 55:1222–1228Google Scholar
- Bonmatin JM, Moineau I, Charvet R, Colin ME, Fleche C, Bengsch ER (2005) Behaviour of imidacloprid in fields. Toxicity for honey bees. In: Lichtfouse E, Schwarzbauer J, Robert D (eds) Environmental chemistry: Green chemistry and pollutants in ecosystems. Springer, pp 483–494Google Scholar
- Bundy JG, Lenz EM, Bailey NJ, Gavaghan CL, Svendsen C, Spurgeon D, Hankard PK, Osborn D, Weeks JM, Trauger SA, Speir P, Sanders I, Lindon JC, Nicholson JK, Tang H (2002) Metabonomic assessment of toxicity of 4-fluoroaniline, 3,5-difluoroaniline and 2-fluoro-4-methylaniline to the earthworm Eisenia veneta (rosa): identification of new endogenous biomarkers. Environ Toxicol Chem 21:1966–1972CrossRefGoogle Scholar
- Cang T, Dai D, Yang G, Yu Y, Lv L, Cai L, Wang Q, Wang Y (2017) Combined toxicity of imidacloprid and three insecticides to the earthworm, Eisenia fetida (Annelida, Oligochaeta). Environ Sci Pollut Res 24:8722–8730Google Scholar
- Dittbrenner N, Moser I, Triebskorn R, Capowiez Y (2011) Assessment of short and long-term effects of imidacloprid on the burrowing behaviour of two earthworm species (Aporrectodea caliginosa and Lumbricus terrestris) by using 2D and 3D post-exposure techniques. Chemosphere 84:1349–1355CrossRefGoogle Scholar
- Edwards CA, Bohlen PJ (1992) The effects of toxic chemicals on earthworms. Rev Environ Contam Toxicol 125:23–100Google Scholar
- EFSA (2012) Statement on the findings in recent studies investigating sub-lethal effects in bees of some neonicotinoids in consideration of the uses currently authorised in Europe. EFSA J 10:2752Google Scholar
- Ekman DR, Teng Q, Villeneuve DL, Kahl MD, Jensen KM, Durhan EJ, Ankley GT, Collette TW (2009) Profiling lipid metabolites yields unique information on sex- and time-dependent responses of fathead minnows (Pimephales promelas) exposed to 17α-ethynylestradiol. Metabolomics 5:22–32CrossRefGoogle Scholar
- Horton ML, Scrimgeour KG, Perry MD, Rawn JD (2006) Principles of biochemistry. Pearson Prentice Hall, Upper Saddle RiverGoogle Scholar
- McKelvie JR, Wolfe DM, Celejewski MA, Alaee M, Simpson AJ, Simpson MJ (2011) Metabolic responses of Eisenia fetida after sub-lethal exposure to organic contaminants with different toxic modes of action. Environ Pollut 159:3620–3626Google Scholar
- Medrzycki P, Montanari R, Bortolotti L, Sabatini AG, Maini S, Porrini C (2003) Effects of imidacloprid administered in sub-lethal doses on honey bee behaviour. Laboratory tests. Bull Insectol 56:59–62Google Scholar
- Nelson DL, Lehninger AL, Cox MM (2012) Lehninger principles of biochemistry. W.H. Freeman, New YorkGoogle Scholar
- OECD (1984) Test no. 207: Earthworm, acute toxicity tests. OECD Publishing, ParisGoogle Scholar
- Pisa LW, Amaral-Rogers V, Belzunces LP, Bonmatin JM, Downs CA, Goulson D, Kreutzweiser DP, Krupke C, Liess M, McField M, Morrissey CA, Noome DA, Settele J, Simon-Delso N, Stark JD, Van Der Sluijs JP, Van Dyck H, Wiemers M (2015) Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res 22:68–102CrossRefGoogle Scholar
- Pollak P (2011) Fine chemicals: the industry and the business. Second edition. Wiley, pp 312Google Scholar
- Whitfield Åslund ML, McShane H, Simpson MJ, Simpson AJ, Whalen JK, Hendershot WH, Sunahara GI (2012) Earthworm sub-lethal responses to titanium dioxide nanomaterial in soil detected by 1H NMR metabolomics. Environ Sci Technol 46:1111–1118Google Scholar
- Zang Y, Zhong Y, Luo Y, Kong ZM (2000) Genotoxicity of two novel pesticides for the earthworm, Eisenia fetida. Environ Pollut 108:271–278Google Scholar