What are the lethal and sub-lethal effects of neonicotinoid insecticides on bees?

Updated July 13, 2019

Neonicotinoids are the most widely used class of insecticides. They attack an insect’s central nervous system, causing paralysis and death. While most uses aren’t intended to kill bees, research shows that significant incidental harm can occur; even at sublethal exposure, neonicotinoids can damage a bee’s ability to communicate, smell, navigate and simply move its body. Here’s what we currently know about the impact of neonics on bees, based on a recent review of the scientific literature on this topic.

After reviewing the literature, the specific effects in a study were each grouped into one of nine different categories. As you can see above, Reproduction is the category of impact most commonly documented. However, this could simply be the result of the number of studies looking at that particular outcome. And Reproduction, like all the categories, covers a range of specific effects. The tables below provide a look at the specific effects within each category.

BEHAVIORS

Effect	Change	Bees	Neonics	References
bee immobility			IM	Moffat et al. 2016
breathing			IM	Hatjina et al. 2013
feeding			TH	Elston et al. 2013
hygienic behavior			IM	Tsvetkov et al. 2017; Wu-Smart & Spivak 2016
locomotor skills in queens			IM	Wu-Smart & Spivak 2016
motor function			CL, DN, IM	Williamson et al. 2014
pollination services			TH	Stanley et al. 2015b
proboscis extension			AC, TH	Alkassab & Kirchner 2016; D̩mares et al. 2016; Thany et al. 2015
swarming			CL&TH	Sandrock et al. 2014a
time grooming			TH	Williamson et al. 2014
worker movement			CL, IM, TH	Scholer & Krischik 2014

COGNITION

Effect	Change	Bees	Neonics	References
learning			TH	Stanley et al. 2015a
memory, long-term			CL, IM	Alkassab & Kirchner 2016; Williamson & Wright 2013
memory, short-term and mid-term			IM, TH	Stanley et al. 2015a; Williamson & Wright 2013

FORAGING

Effect	Change	Bees	Neonics	References
foraging activity			CL	Arce et al. 2016; Wu-Smart et al. 2016
flight duration (chronic exposure)			TH	Tosi et al. 2017
flight duration (acute exposure)			TH	Tosi et al. 2017
flight distance (chronic exposure)			TH	Tosi et al. 2017
flight distance (acute exposure)			TH	Tosi et al. 2017
flight velocity			TH	Tosi et al. 2017
forager recruitment			IM	Gill et al. 2012
foraging performance			IM	Cresswell 2011
foragers returning to patch			IM	Karahan et al. 2015
foraging trips			IM	Karahan et al. 2015
homing capacity			CL, IM, TH	Fischer et al. 2014; Yang et al. 2012
pollen load			IM	Gill et al. 2012; Stanley et al. 2016
pollen stores			IM	Wu-Smart & Spivak 2016
pollen trip (duration)			IM	Gill et al. 2012
pollen trip (successful)			IM	Gill et al. 2012
rate of return to colony			TH	Stanley et al. 2016
time spent foraging			TH	Stanley et al. 2016
workers lost during foraging			IM	Gill et al. 2012

LIFE SPAN

Effect	Change	Bees	Neonics	References
daily mortality			IM	Abbo et al. 2017
life span			CL	Straub et al. 2016; Tsvetkov et al. 2017
mortality			IM	Alaux et al. 2010; Trayner et al. 2016
mortality (synergistic effects)			CL, TH	Sgolastra et al. 2016; Zhu et al. 2017
worker mortality			IM, TH	Mommaerts et al. 2010

PARASITES, PATHOGENS, DISEASE

Effect	Change	Bees	Neonics	References
parasites and pathogens (abundance)			various	Sanchez-Bayo et al. 2016
parasites and pathogens (spread)			various	Sanchez-Bayo et al. 2016
immune response			IM	Czerwinski & Sadd 2017
varroa infestation			CL&TH	Alburaki et al. 2015; Alburaki et al. 2018

PHYSIOLOGY

Effect	Change	Bees	Neonics	References
body mass			IM	Abbo et al. 2017
depolarization in neurons			IM	Moffat et al. 2015
gene expression (variety of genes)			AC, CL, IM, TH	Christen et al. 2016; Simmons & Angelini 2017
hemocyte count			CL	Brandt et al. 2016; Hernandez-Lopez et al. 2017
neural stimulation			CL, IM	Moffat et al. 2016
neural sensitivity to substances			IM	Moffat et al. 2015
size of hypopharyngeal glands			IM	Alaux et al. 2010; Hatjina et al. 2013
thermoregulation			TH	Tosi et al. 2016
vitellogenin levels			IM	Abbo et al. 2017

POPULATIONS

Effect	Change	Bees	Neonics	References
wild bee density			CL	Rundlöf et al. 2015

REPRODUCTION

Effect	Change	Bees	Neonics	References
reproduction			CL	Rundlöf et al. 2015
reproductive success			CL&TH	Williams et al. 2015
adult workers, drones, gynes numbers			CL	Arce et al. 2016
brood cells			IM, TH, CL&TH	Moffat et al. 2016; Sandrock et al. 2014b
brood development			IM	Gill et al. 2012
brood production			IM	Wu-Smart & Spivak 2016
brood size			CL&TH	Sandrock et al. 2014a
colony failure			TC	Ellis et al. 2017
colony growth			CL, IM	Bryden et al. 2013; Rundlöf et al. 2015
colony survival			IM	Tasei et al. 2000
colony weight			TC	Ellis et al. 2017
completed nests			CL&TH	Sandrock et al. 2014b
dead colonies			CL&TH	Alburaki et al. 2015; Alburaki et al. 2018
drones			IM	Mommaerts et al. 2010; Woodcock et al. 2017
drone production			IM, TH	Mommaerts et al. 2010
egg cells			CL, TH	Woodcock et al. 2017
eggs laid			IM, TH	Elston et al. 2013; Wu-Smart & Spivak 2016
females			TH	Moffat et al. 2016
females (proportion to offspring)			CL&TH	Sandrock et al. 2014b
larva produced			TH	Elston et al. 2013
larval morality			CL	Hernandez-Lopez et al. 2017
likeliness to loose queen			AC, CL, IM, TH	Tsvetkov et al. 2017
nest building			TH	Elston et al. 2013
nest reproduction			IM	Mommaerts et al. 2010
offspring able to hatch			CL&TH	Sandrock et al. 2014b
offspring completing development			CL&TH	Sandrock et al. 2014b
offspring production			CL&TH	Sandrock et al. 2014b
ovary size			CL&TH	Williams et al. 2015
population size of adults			CL&TH	Sandrock et al. 2014a
queens laying eggs (percentage)			CL&TH	Williams et al. 2015
queen production			CL, IM, TH, IM&TH	Moffat et al. 2016; Whitehorn et al. 2012; Woodcock et al. 2017
queen replacement			CL&TH	Sandrock et al. 2014a
queen survival			CL, IM	Fauser et al 2017; Scholer & Krischik 2014
reproductive cells			CL, IM&TH	Woodcock et al. 2017
reproductive individuals			TC	Ellis et al. 2017
solitary bee nesting			CL	Rundlöf et al. 2015
sperm quality			CL&TH	Williams et al. 2015
sperm viability			CL, TH	Straub et al. 2016
storage cells			CL, TH	Woodcock et al. 2017
time of development			CL&TH	Abbot et al. 2008
wax cells built			TH	Elston et al. 2013
worker fecundity			IM	Laycock et al. 2012
workers			CL	Woodcock et al. 2017
workers produced			TH	Stanley et al. 2016

SENSORY

Effect	Change	Bees	Neonics	References
olfactory associative behavior			IM	Yang et al. 2012

Methodology

This review is based predominately on two sources of information:

1. Supplementary materials from Mitchell and colleagues’ 2017 study, “A worldwide survey of neonicotinoids in honey”. Table S8 in those materials contains an extensive list of effects and references to the studies demonstrating each effect.

Mitchell, E. A. D., B. Mulhauser, M. Mulot, A. Mutabazi, G. Glauser, and A. Aebi. 2017. “A Worldwide Survey of Neonicotinoids in Honey.” Science, October, 109–11.

2. The IPI database which contains summaries of research articles on pesticides and their effects on invertebrates. The articles in the database have been reviewed and summarized by Xerces Society staff. This list was built from the results of a search for “neonicotinoids, bees”.

Effect: The impact descriptions were taken from the summaries of research in the supplemental materials and the IPI database. When necessary, I referred to the abstracts of the original research work for clarification. In listing the effects and grouping together different studies with similar effects, I was particularly careful not to combine effects that could be subtly but distinctly different (ex. decreases in “nest building” and “nest reproduction” are not necessarily the same thing); I preferred to risk duplicating effects on the list rather than miss an important distinction between them. In the interest of making the list easier to navigate and read, I grouped together effects into different categories that seemed to make sense.

Type of Change: The direction of each impact – “decrease” or “increase” – was also taken from the summaries of research in the supplemental materials and IPI database. When both “decrease” and “increase” are listed, it indicates mixed results within a single study or between studies. “Altered” is my own category for results that did not seem best represented by “decrease” or “increase” or both.

Type of Bees: The category “Honey bees” includes Apis mellifera. “Bumble bees” includes Bombus terrestris and Bombus impatiens. “Solitary bees” includes Osmia bicornis with a single occurrence of Osmia lignaria.

This project is on-going. If you have additional research that you believe should be included in the review, please get in touch with me [link to contact page].