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Trematodes coupled with neonicotinoids: effects on blood cell profiles of a model amphibian

Abstract

Habitat loss, climate change, environmental contaminants, and parasites and pathogens are among the main factors thought to act singly or together in causing amphibian declines. We tested for combined effects of neonicotinoid pesticides and parasites (versus parasites-only) on mortality, growth, and white blood cell profiles of a model amphibian: the northern leopard frog (Rana pipiens). We first exposed infectious stages of frog trematodes (cercariae of Echinostoma spp.) to low and high concentrations of thiamethoxam or clothianidin versus water-only controls. There were no differences in survival of trematode cercariae between treatments. For the main experiment, we exposed tadpoles to clean water versus high concentrations of clothianidin or thiamethoxam for 2 weeks and added trematode cercariae to all tanks after 1 week. Exposure of tadpoles and parasites to high concentrations of thiamethoxam or clothianidin did not affect parasite infection success. Tadpole survival was not different between treatments before or after parasite addition and there were no significant differences in tadpole snout-to-vent lengths or developmental stages between treatments. Tadpoles exposed to thiamethoxam + parasites had smaller widths than parasite-only tadpoles, whereas tadpoles exposed to clothianidin + parasites had higher eosinophil to leukocyte ratios compared to parasite-only tadpoles. Tadpoles of both neonicotinoid + parasite treatments had significantly lower monocyte to leukocyte ratios relative to parasite-only tadpoles. High concentrations of neonicotinoid combined with parasites appear to influence tadpole immune function important for further defense against parasites and pathogens. This work highlights the need for more holistic approaches to ecotoxicity studies, using multiple stressors.

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Acknowledgements

We would like to thank Justin Marchand and Ashley McFee from Carleton University for their assistance with monitoring tadpoles. We would also like to thank André Morrill and Jillian Rohonczy from Carleton University for their assistance with data analysis and France Maisonneuve and Eric Pelletier from Environment and Climate Change Canada for their assistance with the chemical analyses.

Availability of data and material

The datasets used during the current study are available in the published article and as a supplementary information file.

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Funding

Funding for this project was provided by Environment and Climate Change Canada (SR01-2018) and from a grant (100118) from the Natural Science and Engineering Research Council of Canada (NSERC) awarded to M.R. Forbes.

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Authors and Affiliations

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Contributions

Conceptualization and experimental design: Melody J. Gavel, Sarah D. Young, Mark R. Forbes, and Stacey A. Robinson; experimental work and data collection: Melody J. Gavel, Sarah D. Young, and Noémie Blais; data analysis: Melody J. Gavel; writing and editing: Melody J. Gavel, Sarah D. Young, Mark R. Forbes, and Stacey A. Robinson; supervision: Mark R. Forbes and Stacey A. Robinson.

Corresponding author

Correspondence to Stacey A. Robinson.

Ethics declarations

All procedures involving animals were performed in compliance with the ethical standards for the care and use of animals (SR01-2018 approved by Wildlife East Animal Care Committee of Environment and Climate Change Canada and BL-2206 approved by the University of Ottawa Animal Care Committee). No studies with human participants are contained in this article.

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Not applicable.

Conflict of interest

The authors declare no competing interests.

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Section Editor: Elizabeth Marie Warburton

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Gavel, M., Young, S., Blais, N. et al. Trematodes coupled with neonicotinoids: effects on blood cell profiles of a model amphibian. Parasitol Res 120, 2135–2148 (2021). https://doi.org/10.1007/s00436-021-07176-x

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  • DOI: https://doi.org/10.1007/s00436-021-07176-x

Keywords

  • Amphibian
  • Helminth
  • Leukocyte differentials
  • Neonicotinoid
  • Pesticide
  • Parasite