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Increased aggression and reduced aversive learning in honey bees exposed to extremely low frequency electromagnetic fields


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Honey bees, Apis mellifera, are a globally significant pollinator species and are currently in decline, with losses attributed to an array of interacting environmental stressors. Extremely low frequency electromagnetic fields (ELF EMFs) are a lesser-known abiotic environmental factor that are emitted from a variety of anthropogenic sources, including power lines, and have recently been shown to have a significant impact on the cognitive abilities and behaviour of honey bees. Here we have investigated the effects of field-realistic levels of ELF EMFs on aversive learning and aggression levels, which are critical factors for bees to maintain colony strength. Bees were exposed for 17 h to 100 μT or 1000 μT ELF EMFs, or a sham control. A sting extension response (SER) assay was conducted to determine the effects of ELF EMFs on aversive learning, while an intruder assay was conducted to determine the effects of ELF EMFs on aggression levels. Exposure to both 100 μT and 1000 μT ELF EMF reduced aversive learning performance by over 20%. Exposure to 100 μT ELF EMFs also increased aggression scores by 60%, in response to intruder bees from foreign hives. These results indicate that short-term exposure to ELF EMFs, at levels that could be encountered in bee hives placed under power lines, reduced aversive learning and increased aggression levels. These behavioural changes could have wider ecological implications in terms of the ability of bees to interact with, and respond appropriately to, threats and negative environmental stimuli.
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Increased aggression and reduced aversive
learning in honey bees exposed to extremely
low frequency electromagnetic fields
Sebastian ShepherdID
*, Georgina Hollands
, Victoria C. Godley
, Suleiman M. Sharkh
Chris W. Jackson
, Philip L. Newland
1Biological Sciences, University of Southampton, Highfield Campus, Southampton, United Kingdom,
2Department of Entomology, Purdue University, West Lafayette, Indiana, United States of America,
3Mechatronics, Mechanical Engineering, University of Southampton, Highfield Campus, Southampton,
United Kingdom
Honey bees, Apis mellifera, are a globally significant pollinator species and are currently in
decline, with losses attributed to an array of interacting environmental stressors. Extremely
low frequency electromagnetic fields (ELF EMFs) are a lesser-known abiotic environmental
factor that are emitted from a variety of anthropogenic sources, including power lines, and
have recently been shown to have a significant impact on the cognitive abilities and behav-
iour of honey bees. Here we have investigated the effects of field-realistic levels of ELF
EMFs on aversive learning and aggression levels, which are critical factors for bees to main-
tain colony strength. Bees were exposed for 17 h to 100 μT or 1000 μT ELF EMFs, or a
sham control. A sting extension response (SER) assay was conducted to determine the
effects of ELF EMFs on aversive learning, while an intruder assay was conducted to deter-
mine the effects of ELF EMFs on aggression levels. Exposure to both 100 μT and 1000 μT
ELF EMF reduced aversive learning performance by over 20%. Exposure to 100 μT ELF
EMFs also increased aggression scores by 60%, in response to intruder bees from foreign
hives. These results indicate that short-term exposure to ELF EMFs, at levels that could
be encountered in bee hives placed under power lines, reduced aversive learning and
increased aggression levels. These behavioural changes could have wider ecological impli-
cations in terms of the ability of bees to interact with, and respond appropriately to, threats
and negative environmental stimuli.
Over the last 30 years there has been a decline in the numbers of the economically and ecolog-
ically important honey bee [1,2]. Honey bee declines are part of a much larger global problem
of pollinator declines [3] with major causes attributed to a combination of interacting, and
mainly anthropogenically driven, environmental stressors including, habitat loss, pesticide
exposure, pathogens and parasites [4]. Electromagnetic pollution is emerging as a lesser-
PLOS ONE | October 10, 2019 1 / 13
Citation: Shepherd S, Hollands G, Godley VC,
Sharkh SM, Jackson CW, Newland PL (2019)
Increased aggression and reduced aversive
learning in honey bees exposed to extremely low
frequency electromagnetic fields. PLoS ONE 14
(10): e0223614.
Editor: Adam G Dolezal, University of Illinois at
Urbana-Champaign, UNITED STATES
Received: June 7, 2019
Accepted: September 24, 2019
Published: October 10, 2019
Copyright: ©2019 Shepherd et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the manuscript and its Supporting
Information files.
Funding: SS was funded by a Mayflower
Studentship from the University of Southampton.
The funder had no role in study design, data
collection and analysis, decision to publish, or
preparation of the manuscript. Publication of this
article was funded in part by Purdue University
Libraries Open Access Publishing Fund.
known abiotic environmental factor that has the potential to affect insect biology and thus
may contribute to the environmental stress load that insects currently experience in global eco-
systems [5,6].
Extremely low frequency electromagnetic fields (ELF EMFs) are a specific type of non-ion-
ising electromagnetic radiation in the frequency range 3–300 Hz that are emitted from anthro-
pogenic devices. Pollution of the environment with ELF EMFs has increased dramatically in
the last century, with a major source for ELF EMFs being power transmission lines [7]. ELF
EMF exposure has recently been associated with a variety of different effects on insects includ-
ing changes in developmental biology [8,9], locomotor behaviour [6,10], molecular biology
[11,12], and immune response [13].
Honey bees may be particularly at risk to ELF EMF pollution in the environment. At
ground level, ELF EMF intensity under power transmission lines can reach 100 μT, while fly-
ing insects can be exposed to much higher levels close to conductors where ELF EMF levels
can be over 1,000 μT [5]. Some studies suggest exposure to ELF EMFs from power lines may
be stressful for honey bees [14,15] whilst it has also been reported [16] that bees hived under
power lines will readily abscond. Moreover, Greenberg et al. [17] found that bee hives exposed
to power lines had increased motor activity, abnormal propolisation, reduced weight gain of
hives, queen loss, impaired production of queen cells, decreased sealed brood and poor winter
survival, leading to a federal US precaution to not store hives under power lines [18]. While
these studies show no direct experimental evidence for ELF EMF effects on bees, they at least
suggest that ELF EMF exposure may be a factor that contributed to, or caused, the stress
responses of the bees observed in these studies.
In their environment bees are exposed to a variety of negative environmental stimuli and
cues, which are also critical for bees to perceive and respond to, such as weather, toxins [19],
or biotic threats such as colony diseases and parasites [20,21], invading robber bees from
other colonies [20] and predators [2123]. How colonies respond to these environmental
stresses is critical to their long-term fitness. Bees must be able to detect these negative stimuli
[20], learn that they are associated with a negative effect [19], enact an appropriate aggressive
response [22], and even communicate this information to other individuals [23]. For example,
guard bees when confronted with a threat (e.g. predator or intruder) may enter the hive to
release alarm pheromone by extruding their sting, raising their abdomen and fanning their
wings [24,25].
Surprisingly little is known about aversive learning, and how it is affected by environmental
stimuli, despite its importance in maintaining colony fitness. A sting extension response (SER)
assay [26,27] has been developed to study aversive learning in bees in which a conditioned
stimulus (CS) (often olfactory) is applied and associated with an unconditioned stimulus (US)
of a weak electric shock. Over repeated conditioning trials bees learn to associate the negative
US with the CS. The SER assay can therefore provide valuable information in a controlled
experimental environment of how potential stressors such as ELF EMFs can affect bees [28].
For example, SER has been used to investigate the impacts of the neonicotinoid insecticide
imidacloprid on honey bee aversive learning [29]. In addition, intruder assays have been used
to assess aggressive responses of honey bees, including to conspecifics [3033]. Environmental
stresses which could affect the ability of bees to learn about negative environmental cues, or
respond appropriately to environmental cues, could therefore be detrimental to honey bee col-
ony health.
Here we have used both the SER and intruder assays to determine whether short term expo-
sure to ELF EMFs, at levels equivalent to those found at ground level under high-voltage trans-
mission power lines, can affect aversive learning and aggression in honey bees. We have
utilised these well-established assays in the laboratory where the levels of EMF exposure of
Extremely low frequency electromagnetic fields increase aggression and reduce aversive learning in honey bees
PLOS ONE | October 10, 2019 2 / 13
Competing interests: The authors have declared
that no competing interests exist.
individual bees can be precisely controlled, and under consistent conditions free from stray
fields and other confounding stimuli.
Materials and methods
Magnetic fields
Electromagnetic fields were generated with a custom-made Helmholtz coil [5] which produced
homogenous 50 Hz sinusoidal AC electromagnetic fields with a range of field strength from
~10 μT—10,000 μT. Field strength (magnetic flux density) was measured with a Model GM2
Magnetometer (Alphalab Inc., USA). For control exposures no current was passed through the
coil system. For SER experiments control, 100 μT and 1000 μT 50 Hz EMF treatments were
applied, while for intruder assay experiments control and 100 μT ELF EMF treatments were
Honey bees were kept at the University of Southampton Highfield Campus apiary (50˚ 56’
10’’N, 1˚ 23’ 39’’W) and experiments conducted from June-August, 2017. Foragers were iden-
tified by the pollen in their corbiculae and transported to an insectary in the Institute for Life
Sciences at the University of Southampton, where they were immobilized on wet ice and trans-
ferred into appropriate containers for SER and Intruder Assay experiments.
Sting extension response assay
Bees were collected individually from 3 hives and harnessed in custom made SER cradles cut
from Perspex, with a similar design to Vergoz et al. [27]. Bees were placed ventral side upwards
in a metal fork of the cradle, such that the fork held the bee by the thorax, with prongs in place
around the petiole and neck of the bee (Fig 1A). This fork also served as an electrode for an
Fig 1. Sting extension response protocol. A) Harnessing of a bee in an SER cradle for EMF exposure. Tesa
tape was
applied around the thorax to hold the bee between the fork prongs. B) Aversive sting extension response to the CS in
SER conditioning trials. The inset shows the extended stinger in more detail. C) SER Timetable showing a
representation of an individual conditioning trial. The bee was acclimatised to the arena for 20 s, before CS (linalool)
application. After 6 s of CS, CS and US (12 V shock) were paired for 2 s, after which both CS and US were switched off.
A further 32 s of clear airflow was allowed for odour to be removed from the arena.
Extremely low frequency electromagnetic fields increase aggression and reduce aversive learning in honey bees
PLOS ONE | October 10, 2019 3 / 13
aversive shock stimulus during the SER assay (Fig 1B). Tesa
tape was then placed laterally
across the cradle and between the prongs of the fork across the thorax to restrain the bee in the
cradle. Bees were then fed to satiation with a 50% w/v sucrose solution and were then ready for
overnight treatment (17 h).
An experimental arena (W ×D×H = 60 ×45 ×55 cm) was used with an odour delivery
system at one end and an extraction fan at the other to remove any odours from the arena. The
odour delivery system allowed a constant airflow to be supplied to the arena. A clear airflow,
and the CS, were delivered in separate channels in the multichannel system which joined via
Teflon tubing before it discharged into the arena at a single release point. Electronic valves
allowed the airflow to switch between CS and clear airflow channels. The CS used was 8 μl of
97% linalool (Sigma-Aldrich, UK) which was pipetted onto filter paper to be placed in the CS
delivery channel. The channel with clear air was always open when no odour was delivered. To
deliver the CS, airflow was switched from the clear air channel to the odour delivery channel
such that bees were supplied with a constant airflow, and would associate any stimulus with
the odour and not a change in airflow.
For SER experiments bees were exposed to control, 100 μT or 1000 μT EMFs for 17 h and
following exposure SER trials began immediately. This treatment was chosen to represent a
field-realistic scenario where bee hives are placed under transmission and where bees have
been reported to show negative responses [17]. 357 bees completed the SER assay. An SER cra-
dle containing a harnessed bee was placed into the experimental arena of the odour delivery
system. Bees were exposed to a clear airflow for 20 s (Fig 1C). During this time the SER cradle
was attached to a DC power-supply with a 12 V output. The airflow was then switched from
clean air to linalool airflow, representing the CS. The CS lasted 8 s. For the final 2 s of the CS
the bee was shocked at 12 V from the DC power supply, representing the unconditioned stim-
ulus (US) thus pairing US and CS for 2 s. The US and CS finished at the same time (28 s into
the trial). The clear airflow was then left on for 32 s with the bee in the arena to reinforce the
association of the CS with the US and to allow the extractor to remove linalool from the arena.
The length of one complete conditioning trial for a bee was 60 s (Fig 1C).
Conditioning trials were repeated 5 times for each individual bee with an inter-trial interval
of 10 min. If a bee did not respond during linalool delivery or electric shock then a ‘failed
response’ was recorded. Bees that failed to respond more than once in conditioning trials
(n = 16, 4.5% of 357) were excluded from analyses. No bees exhibited a pre-learned aversive
response to linalool in the first conditioning trial, and therefore no bees had to be excluded
from analysis for this reason. After all exclusions were made, 341 bees remained that com-
pleted the SER assay for inclusion in statistical analyses (S1 Table).
If a bee responded only after the shock stimulus then a non-conditioned sting extension
response was recorded (i.e. the bee responded to US but not CS). As in previous aversive learn-
ing studies responses to the conditioned stimulus have been described only when a bee extends
its sting during the CS application, and are defined as a ‘sting extension response’ (Fig 1A and
1B). The proportions of conditioned sting extension responses over 5 trials were analysed to
assess the effects of short-term ELF EMF exposure on aversive learning in honey bees.
This aversive learning approach therefore measures acquisition and short-term retention of
information, and thus has comparability with the results of the intruder assay where bees
encounter a new individual from a foreign hive.
Intruder assay
Bees were collected from 5 different hives in groups of 20 bees from the same hive of origin.
Each group of 20 was split into 2 paired cohorts of 10 (S2 Table), and stored in separate petri
Extremely low frequency electromagnetic fields increase aggression and reduce aversive learning in honey bees
PLOS ONE | October 10, 2019 4 / 13
dishes fitted with 50% w/v sucrose feeders. For each pair of 10-bee cohorts (from the same
hive of origin) 1 cohort was exposed to a 100 μT ELF EMF and the other exposed to control
conditions (both at 22 ±1˚C) for 17 h overnight. The intruder assay was conducted the next
The sample period for the intruder assay began when a forager bee from a 6
(and differ-
ent) hive was introduced into each petri dish. Focal sampling of the ‘intruder’ bee was con-
ducted continuously for 10 min to assess the behaviour of recipient bees towards the intruder.
Behaviours were categorized on an aggressive severity index adapted from Richard et al. [31]
(Table 1) and the aggressive severity indices summed for a full 10 min sample period to give an
overall aggression score for that sample. In total 60 intruder assay samples were conducted
(n = 30 per treatment, with 6 assays/treatment/hive).
Statistical analysis
Data were analysed in SPSS (v.24, IBM SPSS Inc.) and Graphpad Prism (v.7, Graph Pad Soft-
ware Inc.). Where appropriate, homogeneity of variance and normality assumptions were
tested. For all models assessing the effects of treatments on binomial SER data, binomial error
structure and logit link function were used, and where appropriate pairwise contrasts with
Bonferroni adjusted significance were used in post-hoc analyses.
To determine whether ELF EMF exposure or ‘hive or origin’ affected the initial aversive
responsiveness of bees a generalized linear model (GLM) with ‘EMF treatment’ and ‘hive of
origin’ as interacting factors was used. To analyse the effect of ELF EMF exposure on sting
extension responses, a generalized mixed effect model (GLMM) was used with ‘EMF treat-
ment’, ‘hive of origin’, and ‘conditioning trial’ as interacting factors. For GLMMs trial 1 was
not included in analyses (i.e. trials 2–5 were used), as learning cannot occur in the first trial.
For intruder assay analysis, aggression scores were totalled from each trial and data log
transformed to satisfy normality assumptions for parametric statistical analyses. A two-way
Repeated Measures ANOVA was conducted to determine the effects of ‘EMF’, and ‘Hive of
Origin’ on log-transformed aggression score data, with data paired by their collection cohort.
Data plotted in aggression score graphs is back-transformed.
Sting extension response
ELF EMFs do not reduce the ability of bees to respond to aversive stimuli. To deter-
mine whether short-term exposure to EMF (control, 100 μT, or 1000 μT) affected the ability of
bees to respond with an aversive extension of the sting, the proportions of bees which did not
Table 1. Aggressive severity behavioural index used in the intruder assay adapted from Richard et al. [31].
Behaviour Definition Aggressive Severity
Aggressive antennation Antennation directed towards the intruder or touching the
intruder with antennae
Stalking Follows and moves towards intruder for more than 5 seconds 1
Crawl over Moves directly on top of the intruder 1
Antennation with
mandibles open
Antennation directly towards the intruder with mandibles
Biting Uses mandibles to grasp the intruder 3
Abdomen flexion The abdomen is flexed but the stinger is not extruded 4
Stinging attempts The stinger is visibly extruded towards the intruder 5
Extremely low frequency electromagnetic fields increase aggression and reduce aversive learning in honey bees
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fail to respond to the US (i.e. non-learned sting extension to an aversive stimulus) between
each treatment were compared. After 17 h control exposure 95.0% of bees (n = 119) exhibited
aversive responses (Fig 2), whereas 96.6% (n = 118) responded following exposure to 100 μT
and 95.0% (n = 120) responded following exposure to 1000 μT EMFs. Thus, the initial aversive
responsiveness of honey bees was not affected by any interaction between the ELF EMF ‘treat-
ment’ or the honey bee ‘hive of origin’ (GLM, χ
<0.001, d.f. = 4, P >0.99), nor were there
any main effects of ‘treatment’ (GLM, χ
<0.001, d.f. = 2, P >0.99) or ‘hive of origin’ (GLM,
<0.001, d.f. = 2, P >0.99).
ELF EMFs reduce learning performance of the sting extension response. For control
bees, and those exposed to 100 μT and 1000 μT ELF EMFs, the proportion of bees exhibiting a
sting extension response increased with each conditioning trial (GLMM, F
= 26.08,
P<0.0001). For bees maintained under control conditions 29% showed SER after trial 3 while
50% showed SER after conditioning trial 5 (Fig 3). By contrast, after bees were exposed to
100 μT ELF EMFs only 12% of bees showed SER after trial 3 and 32% after trial 5. Following
exposure to 1000 μT ELF EMFs 19% showed an SER after trial 3 and 27% after trial 5. EMF
treatments were found to significantly reduce the proportions of SER in honey bees (GLMM,
= 15.01, P <0.0001). A greater proportion of control exposed bees exhibited SER than
Fig 2. Aversive responses of honey bees in the SER assay. The effect of ELF EMF treatment on the proportion of
aversive responsiveness to 12 V electric shock aversive stimuli. Exact proportions are plotted. Results show that ELF
EMFs had no effect on the aversive responses of bees to electrical stimulation.
Extremely low frequency electromagnetic fields increase aggression and reduce aversive learning in honey bees
PLOS ONE | October 10, 2019 6 / 13
both 1000 μT (Pairwise comparison, Bonferroni adjusted P <0.001) and 100 μT (Pairwise
comparison, Bonferroni adjusted P = 0.001) exposed bees. There was no ‘treatment’ ‘trial’
interaction (GLMM, F
= 0.82, P = 0.56).
In this analysis of the effects of ELF EMF exposure on sting extension responses, hive
of origin was removed as a factor to improve model fit as it was found to have no effect on the
proportion of SER to the CS (GLMM, F
= 0.17, P = 0.84), nor any interaction with ‘treat-
ment’ (GLMM, F
= 1.38, P = 0.24) ‘conditioning trial’ (GLMM, F
= 0.24, P = 0.96) or
three-way interaction (GLMM, F
= 0.33, P = 0.99).
Intruder assay
Bees exposed to 100 μT ELF EMF exhibited greater aggressive behaviour to introduced bees,
than bees not exposed to ELF EMFs (Fig 4). Bee cohorts which received a control treatment
Fig 3. Effects of ELF EMFs on aversive learning in honey bees. Effect of short-term ELF EMF exposure on the
proportion of aversive responses to the conditioned stimulus (linalool) for each of the trials. For each treatment the
proportion of bees showing a learned response increased. The exact proportion of responses is plotted.
Extremely low frequency electromagnetic fields increase aggression and reduce aversive learning in honey bees
PLOS ONE | October 10, 2019 7 / 13
displayed an aggression score of 12.87 ±1.69 (mean ±SEM) whereas bee cohorts exposed to
100 μT EMF exhibited a mean aggression score of 20.70 ±2.14 (mean ±SEM, Standard Error
of the Mean). EMF exposure significantly increased the average aggression scores across bees
from all hives (F
= 11.42, P = 0.0024). There was no impact of Hive (F
= 0.65, P = 0.63)
or any HiveEMF interaction effect (F
= 0.75, P = 0.56) on aggression score. This indicates
Fig 4. The effect of ELF EMFs on honey bee aggression levels. Exposure to a 100 μT ELF EMF significantly increased
the Aggression Score. Mean ±SEM are shown. Statistical analyses were conducted on log-transformed data. Data
plotted are reverse log-transformed from data used in statistical analysis.
Extremely low frequency electromagnetic fields increase aggression and reduce aversive learning in honey bees
PLOS ONE | October 10, 2019 8 / 13
that short-term ELF EMF exposure, at levels that can be encountered at ground level or in
proximity to a high voltage transmission power lines, led to an increase in aggressive behaviour
of bees directed towards conspecifics.
Short-term exposure to 50 Hz ELF EMFs reduced aversive learning performance and
increased aggression at levels as low as 100 μT. This directly shows, for the first time, that
short-term ELF EMF exposure at levels which can be encountered at ground level under high-
voltage transmission power lines can affect honey bees, in terms of both their conditioning to
negative stimuli, and the intensity of their aggressive behaviour.
In locusts ELF EMFs have been shown to affect neural circuits controlling limb movement
and muscular force [6]. During the stinging response in honey bees the protraction of the tip
of the abdomen, and the alternate sliding of barbed lancets of the stinging apparatus, are coor-
dinated by four large abdominal muscles [3436] whose activity are regulated by neural cir-
cuits in the terminal abdominal ganglion [22]. Given that a sting extension response was
evoked by the US in over 95% of trials, it is unlikely that the effects on aversive learning were
due to the effects of EMF at the neuromuscular level. Similarly, the effects of EMF were not
due to changes in the sting extension motor pattern as bees could still extend their abdomens
to electric shocks. Instead ELF-EMF induced reductions in SER performance are solely down
to a reduced ability to learn the aversive stimuli, and not the motor pattern involved in
responding to the stimuli.
The mechanisms underlying the effects of ELF EMFs on honey bee aversive learning and
aggression may be diverse. While the neural pathways underlying appetitive learning in the
honey bee brain are well characterised [37,38], less is known of the neural architecture under-
lying aversive learning. The biogenic amines dopamine and octopamine have critical roles in
associative learning in honey bees [39]. Vergoz et al. [27] for example, found that aversive
learning is impaired after the injection of dopaminergic antagonists, and Jarriault et al. [40]
found that dopamine was released in mushroom bodies in the honey bee brain after electric
shock stimulation of the abdomen. These findings suggest that dopamine may have a key role
in memory formation in honey bee aversive learning. Furthermore, the honey bee alarm pher-
omone has been shown to increase levels of the biogenic amines serotonin and dopamine,
with increases in these amine levels being associated with increased likelihood of a bee to sting
[41]. Some studies investigating the effects of EMF on invertebrates have suggested that
increased biogenic amine levels lead to increases in behavioural activity [42,43]. While no
studies have yet analysed changes in dopamine levels following ELF EMF exposure, these pre-
vious studies suggest that biogenic amine levels may be a potential area to investigate to eluci-
date the underlying mechanisms of ELF EMF induced changes in insect behaviour. Moreover,
ELF EMFs have been shown to have effects on neuronal signalling in insects [6], and therefore
there is the potential for ELF EMF induced effects on dopaminergic neurons or other neural
circuits which are involved in aversive learning pathways. ELF EMF induced changes in behav-
iour could also be underpinned by molecular changes such as gene expression. For example
short-term ELF EMF exposure has been shown to increase heat-shock protein expression in
locusts [6] and Drosophila [12].
The ecological implications of these effects are diverse. On the one hand the reduced ability
to learn new negative stimuli could lead to an increased latency of honey bee colonies to
respond to novel threats. Maliszewska et al. [10] found that short-term exposure of American
cockroaches to 7,000 μT ELF EMFs increased the latency of responses to a negative heat stimu-
lus. The increase in latency could clearly be detrimental to individuals in the ability to avoid
Extremely low frequency electromagnetic fields increase aggression and reduce aversive learning in honey bees
PLOS ONE | October 10, 2019 9 / 13
harmful environmental stimuli. On the other hand, we found that bees exposed to ELF EMFs
showed increased aggression levels. Rittschof et al. [33] found that increased levels of aggres-
sion in honey bees are associated with greater resilience to environmental stresses and to
immune challenge. However, direct short-term ELF EMF exposure at 2,000 μT in Lepidop-
teran larvae has been associated with changes in immune response parameters such as
increased apoptotic-like hemocytes, reduced hemolyph total protein and reduced hemocyte
cell count, which could suggest short-term ELF EMF exposures might lead to reduced resil-
ience to immune challenge [13]. It is not known if ELF EMFs affect immune response in
honey bees at field-realistic ELF EMF intensities, lower than those that have been studied with
Lepidoptera, and thus it is not known if ELF EMF exposure would confer greater resilience to
immune challenge alongside increased aggression levels in bees. In addition, in the environ-
ment if a bee perceives a negative stimulus a sting response often results in sting autonomy,
with a rupture of the abdomen that causes the eventual death of the bee [44,45]. Less aggres-
sive responses to negative stimuli such as aggressive buzzing and flight bombardment can be
successful methods of warding off threats in a manner that is less detrimental to a colony in
terms of bee loss [25,45]. The effects of environmental stressors and the consequences of
increased aggression on this aversive decision making processes (other than increased sting
autonomy) are not-known.
While it is unclear what the ecological consequences of increased aggression may be for
bees exposed to ELF EMFs, the implications of reduced aversive learning performance are
more distinct. It is imperative that honeybees are able to perceive, learn, and avoid threats in
the environment [28,39]. Reductions in the ability to learn about negative stimuli could have
implications for the abilities of bees to deal with predatory/invader threats [20,22], detecting/
avoiding deleterious stimuli [19] and responding to negative stimuli that require action e.g.
attacking/removing diseased individuals from the hive [20], all of which could have detrimen-
tal effects on bee colonies. Although it is not yet known how bees will actually respond in the
field, it is clear that the reduction in aversive learning seen here with short-term 100 μT expo-
sures could be detrimental to honeybees on an ecological level. A number of studies have
described bee colonies failing that are hived under high-voltage transmission power lines,
where EMF levels can reach 100 μT [1417]. There is the possibility that with hives located
under power lines, the long-term chronic exposure to ELF EMFs could continually reduce
cognitive abilities both with regards to aversive and appetitive learning, potentially leading to
some of the negative effects found in these studies.
Reductions in learning could be detrimental to individual and colony survivability. There
are large potential ecological consequences for reduced ability to learn about aversive and
appetitive stimuli for bees. Future studies should focus on whether there are ecological effects
of ELF EMF exposure, with direct measurements of chronic EMF exposure under power lines,
as well as determining what physiological/molecular processes may be affected by this kind of
exposure. These effects may not be confined to managed honey bees as there may be much
wider implications for wild bees and even other pollinators that require power line strips for
critical habitat refuge [4650]. The underlying mechanisms, as well as the potential ecological
implications of ELF EMF pollution in the field must be further investigated to determine the
effects of ELF EMF pollution on insect biology and ecology, including crucial pollination eco-
system services.
Supporting information
S1 Table. The number of bees in SER analyses (after exclusions) for each hive and treatment.
Extremely low frequency electromagnetic fields increase aggression and reduce aversive learning in honey bees
PLOS ONE | October 10, 2019 10 / 13
S2 Table. The number of bees in intruder assay analyses for each hive and treatment.
S1 Dataset. Datasets for A) SER data B) Aggression data.
Author Contributions
Conceptualization: Sebastian Shepherd, Suleiman M. Sharkh, Chris W. Jackson, Philip L.
Formal analysis: Sebastian Shepherd.
Investigation: Sebastian Shepherd, Georgina Hollands, Victoria C. Godley.
Methodology: Sebastian Shepherd, Georgina Hollands, Victoria C. Godley, Chris W. Jackson,
Philip L. Newland.
Resources: Suleiman M. Sharkh.
Supervision: Chris W. Jackson, Philip L. Newland.
Writing – original draft: Sebastian Shepherd, Philip L. Newland.
Writing – review & editing: Sebastian Shepherd, Georgina Hollands, Victoria C. Godley,
Suleiman M. Sharkh, Philip L. Newland.
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... Such radiation significantly reduces the hatching ratio of adult queens whose larvae were exposed and may alter pupal development [9]. Extremely-low-frequency electromagnetic fields (ELF EMFs) from powerlines impair the cognitive and motor abilities of exposed honey bees [10], reduce their aversive learning, and increase aggression [11]. In combination with pesticides, high-frequency electromagnetic fields (HF EMFs) cause American foul brood, higher bee mortality, queen failures, and excessive drone brood and honey storage [12]. ...
... Due to the ever increasing dependency of many communities all over the world on electrical devices and wired and wireless communication, the growing presence of ambient electromagnetic radiation (EMR), for the time being at least, is inexorable [2,11], as are the continuing urban sprawl and concomitant disappearance of native habitats. Many apiarists have no choice but to keep their hives in urban environments with higher EMR levels [9] due to the increasing unavailability of spaces in close proximity untouched by residential or commercial development. ...
... Table A9 gives the Pearson's correlation coefficients and the corresponding p values of (AVGEMF,TEMP), and (AVEMG,HUMID) (see Table A3 for the descriptions Table A11 summarize the hyperparameter statistics of the top 30% of the RFR and SVMR models ranked by the maximum R 2 . The NT (number of trees) hyperparameter values of the top RFR models were in the chosen range of (50-150) (see Table A6); the MTD (maximum tree depth) hyperparameter values of the RFR models were in the range (10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25) in almost all models; in one model, the MTD was <10 in July. The hyperparameter values of the top SVMR models were all in the chosen ranges. ...
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Since bee traffic is a contributing factor to hive health and electromagnetic radiation has a growing presence in the urban milieu, we investigate ambient electromagnetic radiation as a predictor of bee traffic in the hive’s vicinity in an urban environment. To that end, we built two multi-sensor stations and deployed them for four and a half months at a private apiary in Logan, Utah, U.S.A. to record ambient weather and electromagnetic radiation. We placed two non-invasive video loggers on two hives at the apiary to extract omnidirectional bee motion counts from videos. The time-aligned datasets were used to evaluate 200 linear and 3,703,200 non-linear (random forest and support vector machine) regressors to predict bee motion counts from time, weather, and electromagnetic radiation. In all regressors, electromagnetic radiation was as good a predictor of traffic as weather. Both weather and electromagnetic radiation were better predictors than time. On the 13,412 time-aligned weather, electromagnetic radiation, and bee traffic records, random forest regressors had higher maximum R2 scores and resulted in more energy efficient parameterized grid searches. Both types of regressors were numerically stable.
... Cognition is an important part of honey bee survival, as they must be able to learn and react to both negative and positive cues in the environment, such as predators or foraging locations (Shepherd et al., 2019). This ability however has the potential to be threatened by stressors in the environment. ...
... Vergoz et al (2007) found this method did not have such a high learning rate, with just over 40% of bees showing a conditioned response by the 5th trial. A study by Shepherd et al. (2019) similarly found that up to 50% of control bees could learn the response. ...
... A common feature of the stressors that affect bees is that they lead to a decrease in the cognitive abilities of bees, which in turn can affect the health of the colony (Shepherd et al., 2019). In their natural environment bees are exposed to a variety of both positive and negative cues. ...
The European honey, Apis Melifera L., is the most commonly managed bee in the world, but despite an increase in the global stocks of honey bees, areas such as Europe (-26.5%) and North America (-49.5%) have experienced notable declines at the colony level. Although less data is available on the position of honey bees in the tropics, what is available suggests that there is a deficit of 210,00 honey bee hives compared to global trends. These declines are driven by a number of synergistic stressors, including land use change, pesticide exposure, as well as pathogen and parasite infection. This thesis investigates how in a tropical environment, Belize, the Africanised honey bee is impacted by the landscape, and in particular their subsequent diet and exposure to pesticides. Apiculture is one of the most widespread agricultural activities practised globally, with an estimated 94 million honey bee colonies present worldwide in 2020. Beekeeping offers substantial benefits to local people, particularly in rural developing communities, where it provides economic opportunities, through the production of honey, wax and bee bread. In addition, the impact of landscape on honey bee learning in the UK was also analysed, and for the first time directly compares visual learning across a gradient of landscapes, contributing to the growing knowledge of bee behaviour and cognition. Analysis of the honey bee pollen diet across the Toledo and Cayo districts of Belize was carried out by identifying the pollen grains in bee bread samples. The most abundant and frequently occurring taxa were identified and community compositions studied. Tree species were found to be of particular importance, making up 80% of the 10 most relatively abundant species. This study contributes to the growing body of research highlighting the importance of trees in bee diets. No relationship was found between the most abundant pollen taxa and their nutritional make up based on crude protein levels, suggesting that the abundance of the pollen in the environment is more likely the driver behind its dominance in the bee bread. The effects of landscape diversity on species richness, species diversity and community compositions of pollen found in bee bread was compared in the Toledo and Cayo districts. A negative relationship was found between landscape diversity and both pollen richness and diversity. This may be due to the complex relationship between each plant/pollen taxa and the landscape, as well as bee preference. A high abundance of preferred species within the landscape acts to lower the diversity and richness of pollen with the honey bees diet. This data suggests that the presence and dominance of preferred species in the landscape is more important than landscape diversity when it comes to determining honey bee diet. The presence of pesticides in bee bread samples from honey bee hives located across a gradient off natural and agricultural landscapes was also investigated. Pesticides were not found in any of the samples, suggesting that exposure of honey bees to pesticides via their pollen diet does not represent a risk in Belize. The lack of pollen contamination of pesticides is likely due to the bees preference of tree pollen which does not receive pesticide treatment, and is unlikely to experience accidental treatment due to the main application methods in Belize, knapsack spraying. Finally, the effects of landscape complexity and composition on honey bee cognition was studied directly in the field. Visual learning, a crucial component of bee behaviour used to find food resources, was compared across a gradient of landscapes with a range of complexity, whilst compositional changes were kept to a minimum. To do this a field adapted version of the proboscis extension response was utilised, and bees were taught to associate different coloured paper strips with positive and negative rewards. Results showed that as landscape edge density increased bee learning reduced, and while landscape diversity increased so did bee learning. This is important as to ensure colony survival, bees must learn foraging routes, find profitable flowers, develop spatial maps as well as recognise intruders. Landscape has been shown to be an influential factor in both determining the pollen diet of bees as well as their learning ability, but in Belize did not contribute to pesticide exposure through their pollen diet, likely due to the pesticide application methods and bee preference for tree species. When placing bee hives in both Belize and the UK, it is therefore important to consider there placement in terms of landscape, to increase the likelihood of developing a strong and successful colony.
... The exposure to both 100 μT and 1000 μT extremely low frequency electromagnetic fields (ELF EMFs) led to a reduction of more than 20 percent in aversive learning performance. Furthermore, exposure to 100 μT ELF EMFs led to a 60 percent increase in aggression scores, particularly in response to intruder bees from foreign hives (Shepherd et al., 2019). The presence of these magnetic fields was found to enhance foraging flights and induce a tendency among workers to exhibit group behaviour in paper wasp Polybia paulista (Pereira et al., 2015). ...
... As a result, any observed effects are likely attributable to alterations in their metabolic processes. Exposure to EMFs and stress have the potential to stimulate animals, leading to increased levels of aggression, anxiety, locomotor activity, and the tendency to produce flight behaviors [25,26,32,35,36]. The metabolic state of an organism is influenced by its overall level of activity; for instance, a heightened activity corresponds to an increase in the sense of hunger and CO 2 production, thereby facilitating the opportunity to rectify energy deficits [37]. ...
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(1) Background: The growing ubiquity of electromagnetic fields (EMF) due to rapid technological progress raises concerns about potential health implications. While laboratory experiments have generated inconclusive findings about adverse effects, EMFs have demonstrated efficacy in magnetotherapy. Earlier studies indicate that an EMF can trigger stress responses in organisms, the outcomes of which are dependent on the intensity of the EMF. (2) Methods: This study aims to explore the effects of extremely low-frequency EMF (50 Hz, 1 mT, or 7 mT) on metamorphosis and metabolism rates, which are indicators of stress, across different developmental stages of Tenebrio molitor, including adults, pupae, and larvae. (3) Results: Our findings reveal that exposure to EMF leads to accelerated weight loss, increased adult metabolism, and higher mortality; however, EMF exposure appears to have no impact on sugar levels or the rate and success of metamorphosis. Notably, significant changes were only observed under the influence of a strong EMF (7 mT), while the weaker EMF (1 mT) did not yield statistically significant outcomes. (4) Conclusion: The obtained results suggest that an extremely low-frequency EMF can be considered a stressor, with its effects contingent upon the specific parameters of exposure and the developmental stage of the experimental model.
... Reactions to EMF (50 Hz, 1-7 mT) exposure as a stress factor can be observed as changes in behavior and physiology of insects leading to an increase in motor activity (Wyszkowska et al. 2006) and aggression level (Shepherd et al. 2019), impaired response to noxious heat (Maliszewska et al. 2018), reduced cognitive abilities (Shepherd et al. 2018), increase in stress protein levels (Wyszkowska et al. 2016), and enhanced oxidative stress response (Zhang et al. 2016). We have shown that male crickets responded to the exposure to EMF by increasing tyramine (by 65% relative to the control), serotonin (25%), and dopamine (50%) levels and reducing octopamine level (by 25%) in their brain. ...
Full-text available
The electromagnetic field (EMF) is ubiquitous in the environment, constituting a well-known but poorly understood stressor. Few studies have been conducted on insect responses to EMF, although they are an excellent experimental model and are of great ecological importance. In our work, we tested the effects of EMF (50 Hz, 7 mT) on the cricket Gryllus bimaculatus: the male calling song pattern, female mate choice, and levels of biogenic amines in the brain. Exposure of males to EMF increased the number and shortened the period of chips in their calling song (by 2.7% and 5% relative to the control song, respectively), but not the sound frequency. Aged (3-week-old) females were attracted to both natural and EMF-modified male signals, whereas young (1-week-old, virgin) females responded only to the modified signal, suggesting its higher attractance. Stress response of males to EMF may be responsible for the change in the calling song, as suggested by the changes in the amine levels in their brains: an increase in dopamine (by 50% relative to the control value), tyramine (65%), and serotonin (25%) concentration and a decrease in octopamine level (by 25%). These findings indicate that G. bimaculatus responds to EMF, like stressful conditions, which may change the condition and fitness of exposed individuals, disrupt mate selection, and, in consequence, affect the species’ existence. Graphical Abstract
... A major concern of the effects of Radio Frequency Electromagnetic Radiation (RF-EMR) on animals is tissue heating due to the specific absorption rate of the propagated wave. Short-term exposure to Extremely Low Frequency-ElectroMagnetic Fields (ELF-EMF) at 50 Hz, comparable to those found around power lines, reduced learning performance and increased bee aggression in Ref. [69]. ...
... Electromagnetic fields also affect the health of the honey bees. Despite the fewer studies, increased aggressiveness and reduction of the ability for development was demonstrated when the bees were exposed at low frequency electromagnetic fields comparable to those found around power lines [10]. However, it is still difficult to prove the causal relationship between the above factors and the reduced bee population, and to predict future consequences. ...
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A mathematical model has been developed to assess the digitization of the beekeeping sector. For this purpose, the summarized results of questionnaire surveys of 37 apiaries located in the regions of Plovdiv and Pleven municipalities in Bulgaria were used. For evaluation on the degree of digitization of the apiaries we took under consideration only what software and hardware products are used. The results showed a low degree of digitization of the studied apiaries-in 27 out of 37 studied apiaries there were no data about the use of software and hardware applications, and the average level of digitization for the studied apiaries according to the model we developed was within 8-9 %. A survey on the awareness of those employed in the beekeeping about some basic digital products for collecting, storing and distributing information and their willingness to use them in the future was also conducted. It was found that between 21% and 35% of the respondents were not familiar with the basic digital products. Far more worrying was that between 50 % and 70% of respondents stated that they were familiar with the listed digital products, but did not intend to use them in the near future.
Urbanization and the increasing use of wireless technologies lead to higher emission rates of radiofrequency electromagnetic fields (RF-EMF) in populated areas. This anthropogenic electromagnetic radiation is a form of environmental pollution and a potential stressor on bees or other flying insects. Cities often have a high density of wireless devices operating on microwave frequencies, which generate electromagnetic frequencies e.g. in the 2.4 and 5.8 GHz bands commonly used by the wireless technologies. To date the effects of nonionizing electromagnetic radiation on the vitality and behavior of insects are poorly understood. In our experiment we used honey bees as model organisms and analyzed the effects of defined exposures to 2.4 and 5.8 GHz on brood development, longevity and homing ability under field conditions. To generate this radiation, we used a high-quality radiation source which generates a consistent, definable and realistic electromagnetic radiation, engineered for this experiment by the Communications Engineering Lab (CEL) at the Karlsruhe Institute of Technology. Our results show significant effects of long-term exposures on the homing ability of foraging honey bees, but no effects on brood development and adult worker longevity. Using this novel and high-quality technical set-up, this interdisciplinary work provides new data on the effects of these widely used frequencies on important fitness parameters of free-flying honey bees.
Full-text available
Electromagnetic field (EMF) is ubiquitous in the environment, constituting a well-known, but poorly understood stressor. Few studies have been conducted on insect responses to EMF, although they are an excellent experimental model and are of great ecological importance. In our work, we tested the effects of EMF (50 Hz, 7 mT) on the cricket Gryllus bimaculatus : the male calling song pattern, female mate choice and levels of biogenic amines in the brain. Exposure of males to EMF modified the number and period of chips in their calling song, but not the sound frequency. Aged (3-weeks-old) females were attracted to both natural and EMF-modified male signals, whereas young (1-week-old, virgin) females responded only to the modified signal, suggesting its higher attractance. A stress response of males to EMF may be responsible for the change in the calling song, as suggested by changes in the amine levels in their brains (an increase in dopamine, tyrosine, and serotonin concentration and a decrease in octopamine level). These findings indicate that G. bimaculatus responds to EMF like to stressful conditions, which may change the condition and fitness of exposed individuals, disrupt mate selection and, in consequence, affect the species existence.
Full-text available
Environmental stressors frequently have sublethal consequences for animals, often affecting the mean of phenotypic traits in populations. However, effects on inter‐individual variability are poorly understood. Since phenotypic variability is the basis for adaptation, any change due to stressors may have important implications for population resilience. Here, we explored this possibility in bees by analysing raw datasets from 23 studies (5618 bees) in which individuals were first exposed to stressors and then tested for cognitive tasks. While all types of stressors decreased the mean cognitive performance of bees, they increased cognitive variability. Focusing on 14 pesticide studies, we found that the mode of exposure to stressors and the dose were critical. Mean cognitive performance was more affected by a chronic exposure than by an acute exposure. Yet, cognitive variability increased with increasing doses following both exposure durations. Policy implications. Current guidelines for the authorization of plant protection products on the European market prioritize acute over chronic toxicity assessments on non‐target organisms. By overlooking the consequences of a chronic exposure, regulatory authorities may register new products or doses that are harmful to bee populations. Our findings call for more research on stress‐induced phenotypic variation and its incorporation into policy guidelines to help identify levels and modes of exposure animals can cope with.
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Abstract In Drosophila melanogaster, aversive (electric shock) stimuli have been shown to activate subpopulations of dopaminergic neurons with terminals in the mushroom bodies (MBs) of the brain. While there is compelling evidence that dopamine (DA)-induced synaptic plasticity underpins the formation of aversive memories in insects, the mechanisms involved have yet to be fully resolved. Here we take advantage of the accessibility of MBs in the brain of the honey bee to examine, using fast scan cyclic voltammetry, the kinetics of DA release and reuptake in vivo in response to electric shock, and to investigate factors that modulate the release of this amine. DA increased transiently in the MBs in response to electric shock stimuli. The magnitude of release varied depending on stimulus duration and intensity, and a strong correlation was identified between DA release and the intensity of behavioural responses to shock. With repeated stimulation, peak DA levels increased. However, the amount of DA released on the first stimulation pulse typically exceeded that evoked by subsequent pulses. No signal was detected in response to odour alone. Interestingly, however, if odour presentation was paired with electric shock, DA release was enhanced. These results set the stage for analysing the mechanisms that modulate DA release in the MBs of the bee.
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Extremely low frequency electromagnetic field (ELF EMF) pollution from overhead powerlines is known to cause biological effects across many phyla, but these effects are poorly understood. Honey bees are important pollinators across the globe and due to their foraging flights are exposed to relatively high levels of ELF EMF in proximity to powerlines. Here we ask how acute exposure to 50 Hz ELF EMFs at levels ranging from 20-100 µT, found at ground level below powerline conductors, to 1000-7000 µT, found within 1 m of the conductors, affects honey bee olfactory learning, flight, foraging activity and feeding. ELF EMF exposure was found to reduce learning, alter flight dynamics, reduce the success of foraging flights towards food sources, and feeding. The results suggest that 50 Hz ELF EMFs emitted from powerlines may represent a prominent environmental stressor for honey bees, with the potential to impact on their cognitive and motor abilities, which could in turn reduce their ability to pollinate crops.
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Exposure to electromagnetic field (EMF) induces physiological changes in organism that are observed at different levels-from biochemical processes to behavior. In this study, we evaluated the effect of EMF exposure (50 Hz, 7 mT) on cockroach's response to noxious heat, measured as the latency to escape from high ambient temperature. We also measured the levels of lipid peroxidation and glutathione content as markers of oxidative balance in cockroaches exposed to EMF. Our results showed that exposure to EMF for 24, 72 h and 7 days significantly increases the latency to escape from noxious heat. Malondialdehyde (MDA) levels increased significantly after 24-h EMF exposure and remained elevated up to 7 days of exposure. Glutathione levels significantly declined in cockroaches exposed to EMF for 7 days. These results demonstrate that EMF exposure is a considerable stress factor that affects oxidative state and heat perception in American cockroach.
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The defence of a society often requires that some specialized members coordinate to repel a threat at personal risk. This is especially true for honey bee guards, which defend the hive and may sacrifice their lives upon stinging. Central to this cooperative defensive response is the sting alarm pheromone, which has isoamyl acetate (IAA) as its main component. Although this defensive behaviour has been well described, the neural mechanisms triggered by IAA to coordinate stinging have long remained unknown. Here we show that IAA upregulates brain levels of serotonin and dopamine, thereby increasing the likelihood of an individual bee to attack and sting. Pharmacological enhancement of the levels of both amines induces higher defensive responsiveness, while decreasing them via antagonists decreases stinging. Our results thus uncover the neural mechanism by which an alarm pheromone recruits individuals to attack and repel a threat, and suggest that the alarm pheromone of honey bees acts on their response threshold rather than as a direct trigger.
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Global declines in insects have sparked wide interest among scientists, politicians, and the general public. Loss of insect diversity and abundance is expected to provoke cascading effects on food webs and to jeopardize ecosystem services. Our understanding of the extent and underlying causes of this decline is based on the abundance of single species or taxo-nomic groups only, rather than changes in insect biomass which is more relevant for ecological functioning. Here, we used a standardized protocol to measure total insect biomass using Malaise traps, deployed over 27 years in 63 nature protection areas in Germany (96 unique location-year combinations) to infer on the status and trend of local entomofauna. Our analysis estimates a seasonal decline of 76%, and midsummer decline of 82% in flying insect biomass over the 27 years of study. We show that this decline is apparent regardless of habitat type, while changes in weather, land use, and habitat characteristics cannot explain this overall decline. This yet unrecognized loss of insect biomass must be taken into account in evaluating declines in abundance of species depending on insects as a food source, and ecosystem functioning in the European landscape.
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Worldwide mobile telephone and microwave use have resulted in an increasing presence of extremely low-frequency electromagnetic field radiations (ELF-EMFs) in ecosystems. ELF-EMFs have been associated with altered physiological processes that can adversely affect exposed organisms. In this study, Trichoplusia ni Hübner larvae were exposed for 24, 48, or 72 h to ELF-EMFs (60 Hz and 2.0 mT) to assess effects on immune response parameters and fertility. Trichoplusia ni life cycle and fertility were not affected by 24-h exposure. However, the number of apoptotic-like cells and cellular immune response significantly increased (P < 0.01) after 72-h exposure (2- and 1.1-fold, respectively), whereas hemolymph total protein and hemocyte cells were reduced (P < 0.01; 16 and 50%, respectively) after 48-h exposure. Hemocyte cell type analysis resulted in significantly (P < 0.01) higher granulocytes number in the unexposed (2-fold increase) and oenocytoids in the 72-h-exposed larvae (28.6-fold increase). Quantitative retrotranscription (RT-qPCR) showed that after 72-h ELF-EMF exposure, the antimicrobial peptides cecropin, lysozyme, gallerimycin, and pgrp were downregulated by 24,866.0, 2.69-, 119.1-, and 1.45-fold, respectively, whereas attacin and defensin were upregulated by 1.59- and 1.85-fold, respectively. The effect of ELF-EMFs on the T. ni larvae immune response and their potential impact on its physiology and susceptibility to pathogens are discussed. This information may provide new insight of ELF-EMFs on other pest species, as well as for the preservation of ecologically important species.
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Declines in pollinator abundance and diversity are not only a conservation issue, but also a threat to crop pollination. Maintained infrastructure corridors, such as those containing electricity transmission lines, are potentially important wild pollinator habitat. However, there is a lack of evidence comparing the abundance and diversity of wild pollinators in transmission corridors with other important pollinator habitats. We compared the diversity of a key pollinator group, bumblebees (Bombus spp.), between transmission corridors and the surrounding semi-natural and managed habitat types at 10 sites across Sweden’s Uppland region. Our results show that transmission corridors have no impact on bumblebee diversity in the surrounding area. However, transmission corridors and other maintained habitats such as roadsides have a level of bumblebee abundance and diversity comparable to semi-natural grasslands and host species that are important for conservation and ecosystem service provision. Under the current management regime, transmission corridors already provide valuable bumblebee habitat, but given that host plant density is the main determinant of bumblebee abundance, these areas could potentially be enhanced by establishing and maintaining key host plants. We show that in northern temperate regions the maintenance of transmission corridors has the potential to contribute to bumblebee conservation and the ecosystem services they provide.
1. The study of wild bumblebee nests has been hindered by the difficulty in locating and observing them. Here, 47 wild nests were located using a sniffer dog and volunteers. The entrances to 32 nests were filmed continuously to identify successful nests (those that produced gynes) and observe vertebrate species interactions. 2. Of the 47 nests, 71% and 21% produced gynes in 2010 and 2011, respectively. 3. A total of 39 vertebrate species were filmed at entrances but the majority did not interact with the nests. Great tits ( Parus major ) depredated or attempted to depredate bees on 32 occasions at the entrances to 10 nests, something that has not previously been described. Small mammals were very often recorded accessing entrances to bumblebee nests, but whether they depredated bees was not known, and frequently visited nests were no less likely to produce gynes. Eight nests were entered by adult wax moths, Aphomia sociella . 4. The faeces of 1179 workers from 29 Bombus terrestris nests were screened microscopically for parasites. Crithidia bombi infections were apparent in 49% of worker bees, while Nosema bombi and Apicystis bombi were present in 5.5% and 0.68% of bees, respectively. Nests with a high prevalence of C. bombi infection were less likely to produce gynes, the first evidence of a direct impact of this common parasite on bumblebee colony reproduction in wild nests. 5. Overall, our data indicate that bumblebee nests are at the heart of a rich web of interactions between many different predator and parasite species.
Results from a continuing study of possible environmental effects associated with a prototype 1100-kV power line are described. Possible effects on wildlife, cattle, crops, pasture grasses, honeybees and trees are considered; results for the 1981 study period are reported.
Purpose: Extremely low frequency (ELF) magnetic fields as essential ecological factor may induce specific responses in genetically different lines. The subject of this study was to investigate the impact of ELF magnetic field on fitness components and locomotor activity of five Drosophila subobscura isofemale (IF) lines. Materials and methods: Each D. subobscura IF line, arbitrarily named: B16/1, B24/4, B39/1, B57/2 and B69/5, was maintained in five full-sib inbreeding generations. Their genetic structures were defined based on the mitochondrial DNA variability. Egg-first instar larvae and one-day-old flies were exposed to ELF magnetic field (50 Hz, 0.5 mT, 48 h) and thereafter, fitness components and locomotor activity of males and females in an open field test were observed for each selected IF line, respectively. Results: Exposure of egg-first instar larvae to ELF magnetic field shortened developmental time, and did not affect viability and sex ratio of D. subobscura IF lines. Exposure of one-day-old males and females IF lines B16/1 and B24/4 to ELF magnetic field significantly decreased their locomotor activity and this effect lasted longer in females than males. Conclusions: These results indicate various responses of D. subobscura IF lines to the applied ELF magnetic field depending on their genetic background.