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)