Spontaneous honeybee behaviour is altered by persistent organic pollutants

Ecotoxicology, Dec 2016

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.

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Spontaneous honeybee behaviour is altered by persistent organic pollutants

Ecotoxicology Spontaneous honeybee behaviour is altered by persistent organic pollutants Jade Drummond 0 1 ● Sally M. Williamson 0 1 ● Ann E. Fitchett 0 1 ● Geraldine A. Wright 0 1 ● Sarah J. Judge 0 1 0 Institute of Neuroscience, Newcastle University , Newcastle upon Tyne NE2 4HH , UK 1 Medical Toxicology Centre, Newcastle University , Newcastle upon Tyne NE2 4AA , UK 2 Sarah J. Judge 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 fieldrelevant 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. Honeybee ● Apis mellifera ● Lindane ● Pesticide; ● Polychlorinated biphenyl ● Pollutant Introduction Exposure to environmental chemicals below the lethal dose threshold can adversely affect honeybee populations (Mullin et al. 2010; Wu et al. 2011) . The ability of honeybees to survive or adapt to other environmental influences may be comprised by chemicals which alter the normal behaviour of the honeybee. Understandably the vast majority of studies examining the sublethal effects of environmental chemicals on honeybee behaviour have focussed on currently used pesticides (Desneux et al. 2007). Sublethal doses of pesticides including neonicotinoid, pyrethroid, phenylpyrazole and organophosphate insecticides have been shown to alter honeybee motor activity (Charreton et al. 2015; Williamson et al. 2013b, 2014) , learning and memory, (Decourtye et al. 2004; Han et al. 2010b; Lambin et al. 2001; Williamson et al. 2013b) , and appetite and foraging behaviour (Colin et al. 2004; Dively et al. 2015; Han et al. 2012, 2010a; Vandame et al. 1995) . However, currently used agrochemicals are not the only environmental chemicals in honeybee habitats. Persistent organic pollutants (POPs) are characterised by their chemical structure and environmental persistence (Jones and de Voogt 1999) . They decay very slowly and their lipophilic properties lead to bioaccumulation. As a consequence of their environmental persistence and toxicity in human and wildlife populations, the production of certain POPs is restricted (Lallas 2001) . However, these chemicals continue to be detected in the environment (Muir and Howard 2006) , including in beeswax collected from honeybee hives (Chauzat and Faucon 2007; Ravoet et al. 2015) . The presence of POPs in beeswax is unsurprising given the lipid content of beeswax, the lipophilicity of POPs, and because honeybees bioconcentrate chlorinated compounds. Jan and Cerne (1993) demonstrated that honeybees exposed to polychlorinated biphenyl isomers (PCBs) produced beeswax and honey enriched with these pollutants. Polluted beeswax can affect the health of honeybee colonies; Wu et al. (2011) and Zhu et al. (2014) reported that beeswax contaminated with pesticide residues affects the health of both larvae and adult honeybees either through direct contact and/or ingesting honey stored in contaminated beeswax cells. There is an assumption that POPs are unlikely to transfer or be present in honey as they are highly lipophilic. However, POPs such as PCBs and organochlorine pesticides are found in honey (Anderson and Wojtas 1986; Herrera et al. 2005; Kujawski et al. 2012; Sanchez-Bayo and Goka 2014; Wang et al. 2010) . As they are not routinely monitored, data on PCB concentrations in honey is limited, but nevertheless PCB concentrations of more than 500 ng/g have been detected in honey samples from North America and (...truncated)


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Jade Drummond, Sally M. Williamson, Ann E. Fitchett, Geraldine A. Wright, Sarah J. Judge. Spontaneous honeybee behaviour is altered by persistent organic pollutants, Ecotoxicology, 2017, pp. 141-150, Volume 26, Issue 1, DOI: 10.1007/s10646-016-1749-0