Spontaneous honeybee behaviour is altered by persistent organic pollutants

Abstract

The effect of environmental pollutants on honeybee behaviour has focused mainly on currently used pesticides. However, honeybees are also exposed to persistent organic pollutants (POPs). The aim of this laboratory based study was to determine if exposure to sublethal field-relevant concentrations of POPs altered the spontaneous behaviour of foraging-age worker honeybees. Honeybees (Apis mellifera) were orally exposed to either a sublethal concentration of the polychlorinated biphenyl (PCB) mixture Aroclor 1254 (100 ng/ml), the organochlorine insecticide lindane (2.91 ng/ml) or vehicle (0.01% DMSO, 0.00015% ethanol in 1M sucrose) for 1–4 days. The frequency of single event behaviours and the time engaged in one of four behavioural states (walking, flying, upside down and stationary) were monitored for 15 min after 1, 2, 3 and 4 days exposure. Exposure to Aroclor 1254 but not lindane increased the frequency and time engaged in honeybee motor activity behaviours in comparison to vehicle. The Aroclor 1254—induced hyperactivity was evident after 1 day of exposure and persisted with repeated daily exposure. In contrast, 1 day of exposure to lindane elicited abdominal spasms and increased the frequency of grooming behaviours in comparison to vehicle exposure. After 4 days of exposure, abdominal spasms and increased grooming behaviours were also evident in honeybees exposed to Aroclor 1254. These data demonstrate that POPs can induce distinct behavioural patterns, indicating different toxicokinetic and toxicodynamic properties. The changes in spontaneous behaviour, particularly the PCB-induced chronic hyperactivity and the associated energy demands, may have implications for colony health.

Caste‐ and pesticide‐specific effects of neonicotinoid pesticide exposure on gene expression in bumblebees

“…Neonicotinoids target nicotinic acetylcholine receptors (nAChRs) which they bind to and thus excite; this can result in paralysis, convulsions and death (Matsuda et al, 2001). Controlled exposure experiments using honeybees and bumblebees have shown that exposure at comparable concentrations to those found in nectar and pollen can have sublethal effects on learning and memory (Siviter, Koricheva, Brown, & Leadbeater, 2018;Stanley, Smith, & Raine, 2015), cognition and problem solving (Baracchi, Marples, Jenkins, Leitch, & Chittka, 2017;Samuelson, Chen-Wishart, Gill, & Leadbeater, 2016;Williamson & Wright, 2013), motor function (Drummond, Williamson, Fitchett, Wright, & Judge, 2016;Williamson, Willis, & Wright, 2014), foraging performance (Gill & Raine, 2014;Henry et al, 2012;Stanley, Russell, Morrison, Rogers, & Raine, 2016), navigation abilities (Fischer et al, 2014) and the immune system (Brandt, Gorenflo, Siede, Meixner, & Büchler, 2016;Brandt et al, 2017;Di Prisco et al, 2013). Despite the growing interest in the link between neonicotinoid exposure and toxicity to bees, we know little about the molecules and genes through which neonicotinoid action is mediated, or whether neonicotinoids may also affect "off-target" processes that are not mediated by nAChRs.…”

Sublethal Exposure Effects of the Neonicotinoid Clothianidin Strongly Modify the Brain Transcriptome and Proteome in the Male Moth Agrotis ipsilon

“…This also includes DMSO. Whether in vertebrates or invertebrates, DMSO effects can be deleterious, with the observation of some cases of cell toxicity [ 42 ], sterility [ 43 ], or neurotoxicity [ 44 ], but also beneficial, with some report of the neutralization or attenuation of pathologies [ 45 ] or with no observed effect [ 46 ]. Our results confirm that DMSO, a solvent used in many studies, even at very low doses, can influence gene and protein expression and that these effects need to be taken into account in differential studies.…”

Bioindicators and biomonitoring: honeybees and hive products as pollution impact assessment tools for the Mediterranean area

“…Hence, bees can be used to detect chemical impairment of their habitat by studying various endpoints: mortality (in the case of pesticides to which they are very sensitive); physiological, biochemical, or behavioral changes; and the response of the population distribution to sublethal pollutant toxicity (Dolores Hernando et al 2018). The levels of residues on or within their bodies and the contamination of beehive products reflect the pollutant content of their environment (Porrini et al 2002;Badiou-Beneteau et al 2013;Codling et al 2016;Cousin et al 2019;Drummond et al 2017;El-Saad et al 2017;Hernandez et al 2019).…”

“…Later, honeybees were most commonly used to monitor the levels of pesticides in fields and on vegetables visited by honeybees (Quigley et al 2019;Codling et al 2016;Kasiotis et al 2014;Barganska et al 2018;de Oliveira et al 2016). Several persistent organic pollutants (including explosive residues) originating from industrial and urban activities have also been isolated from bee samples and evaluated (Garcia-Valcarcel et al 2016;Drummond et al 2017;Simic et al 2019;Gómez-Ramos et al 2019). More recently, nanomaterials and nanoparticles have been added to the list of contaminants that honeybees can be used to monitor in the environment (Milivojevic et al 2015;Kojic et al 2020;Hooven et al 2019;Glavan et al 2017).…”