The Combined Effects of Varroa destructor Parasitism and Exposure to Neonicotinoids Affects Honey Bee (Apis mellifera L.) Memory and Gene Expression

Abstract

Honey bees (Apis mellifera L.) are exposed biotic and abiotic stressors but little is known about their combined effect and impact on neural processes such as learning and memory, which could affect behaviours that are important for individual and colony survival. This study measured memory with the proboscis extension response (PER) assay as well as the expression of neural genes in bees chronically exposed to three different sublethal doses of the insecticide clothianidin and/or the parasitic mite Varroa destructor. The proportion of bees that positively responded to PER at 24 and 48 h post-training (hpt) was significantly reduced when exposed to clothianidin. V. destructor parasitism reduced the proportion of bees that responded to PER at 48 hpt. Combined effects between the lowest clothianidin dose and V. destructor for the proportion of bees that responded to PER were found at 24 hpt. Clothianidin, V. destructor and their combination differentially affected the expression of the neural-related genes, AmNrx-1 (neurexin), AmNlg-1 (neuroligin), and AmAChE-2 (acetylcholinesterase). Different doses of clothianidin down-regulated or up-regulated the genes, whereas V. destructor tended to have a down-regulatory effect. It appears that clothianidin and V. destructor affected neural processes in honey bees through different mechanisms.

Negative effects of neonicotinoids on male honeybee survival, behaviour and physiology in the field

“…However, we observed that neonicotinoids significantly influenced the behaviour of adult drones, especially in relation to flight, which could have diverse consequences connected to the movement of individuals among colonies and to mating sites known as drone congregation areas (DCAs; Loper et al, 1992). These observations paralleled other studies that found neonicotinoid exposure influenced memory and behaviour in honeybee workers (Morfin et al, 2019(Morfin et al, , 2020. Since short-range drifting of honeybees into non-maternal colonies, as observed in our study, is primarily attributed to orientation errors (Currie, 1987;Currie & Jay, 1991;Free, 1956;Moritz & Neumann, 1996;Pfeiffer & Crailsheim, 1998), our findings may correspond to the reduced orientation and flight abilities previously shown in workers exposed to neonicotinoids Tison et al, 2016;Tosi et al, 2017).…”

Inferring pesticide toxicity to honey bees from a field‐based feeding study using a colony model and Bayesian inference

“…Sublethal doses can also increase susceptibility to pathogens by inhibiting grooming and hygienic behaviors (Wu-Smart and Spivak 2016, Morfin et al 2019a,b). In addition, sublethal doses may reduce foraging success (Yang et al 2008) by inhibiting learning and memory (Decourtye et al 2004, Williamson and Wright 2013, Tison et al 2019, Morfin et al 2020), navigation (Fischer et al 2014, Stanley et al 2015, and locomotor function (Williamson et al 2014, Tosi et al 2018. Future modeling efforts could include these sublethal effects pathways, in combination with Varroa mite pressure, to test whether addition of these mechanisms allows better prediction of transient colony declines at lower pesticide exposure levels.…”

“…Furthermore, some classes of pesticides are relatively stable in the environment, leading to soil contamination that can persist for months or years after application (Goulson 2014, Jones et al 2014. Acute and chronic pesticide exposure to honey bees can lead directly to bee mortality, or indirectly via sublethal effects such as reduced foraging success and flight ability (Henry et al 2012, Fischer et al 2014, Tosi et al 2017, Morfin et al 2019a, impaired olfactory learning (Decourtye et al 2005, Williamson and Wright 2013, Siviter et al 2018, Morfin et al 2020, and increased susceptibility to diseases (Alaux et al 2010, Di Prisco et al 2013, Doublet et al 2015.…”

“…2018, Morfin et al. 2020), and increased susceptibility to diseases (Alaux et al. 2010, Di Prisco et al.…”

First insights into the honey bee (Apis mellifera) brain lipidome and its neonicotinoid-induced alterations associated with reduced self-grooming behavior

“…Bees, and other non-target insects, are potentially exposed to multiple sublethal doses of systemic insecticides by consuming contaminated nectar or pollen [8] . Neonicotinoids affect neural processes, such as learning and memory [9] , [10] , [11] , and behaviors like homing, foraging and hygienic behavior [12] , [13] , [14] , [15] . The negative effects of neonicotinoids on the central nervous system of bees was observed in changes in self-grooming behavior and gene expression [16] , [17] .…”