, Volume 50, Issue 5, pp 595–605 | Cite as

Sublethal exposure to clothianidin during the larval stage causes long-term impairment of hygienic and foraging behaviours of honey bees

  • Nuria MorfinEmail author
  • Paul H. Goodwin
  • Adriana Correa-Benitez
  • Ernesto Guzman-Novoa
Original article


Most studies on the effects of neonicotinoid insecticides on neural processes of honey bees are based on behaviours performed by adult bees exposed as adults. It is unclear how the developing brains of honey bee larvae are affected by sublethal doses of neonicotinoid insecticides when measuring neural processes through behavioural performance in adult bees. In this study, larvae were exposed to three sublethal doses of clothianidin and evaluated 25–36 days later for hygienic and foraging behaviours as adult bees. The medium and highest sublethal doses of clothianidin significantly reduced hygienic and foraging activity. The greatest effects were on the proportion of adult bees foraging and carrying pollen. These results show that exposure of larvae to clothianidin results in negative effects extending into the adulthood of bees, possibly compromising the colony’s fitness by impairing pathogen control mechanisms and by reducing pollen collection.


honey bee larvae  hygienic behavior  foraging behavior  neonicotinoids neural processes 



We thank Paul Kelly, Nancy Bradbury, Dave Stotesbury, Santiago Magaña, Brook Wallace, Stephanie Otto, Patrick Boelsteri, Iván Darío Samur, Cassandra Wiesner, Catherin VanderHeyden and Wendy Shipsides for their assistance during the experiments. We also thank Greg J. Hunt and Nigel Raine for their valuable comments of earlier versions of the manuscript.

Authors’ contributions

EG project planning and design; NM field experiments and data collection; NM, EG, PHG and AC data analyses. NM, PHG and EG wrote the paper. All authors read and approved the final manuscript.

Funding information

This work was partially supported by a New Directions grant from the Ontario Ministry of Agriculture Food and Rural Affairs (OMAFRA) and by a grant from the Pinchin family to EG.

Compliance and ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


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Copyright information

© INRA, DIB and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Environmental SciencesUniversity of GuelphGuelphCanada
  2. 2.Departamento de Abejas, Conejos y Organismos AcuáticosFMVZ, UNAMMexico CityMexico

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