Electromagnetic field exposure affects the calling song, phonotaxis, and level of biogenic amines in crickets

doi:10.21203/rs.3.rs-2957977/v1

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Research Article

Electromagnetic field exposure affects the calling song, phonotaxis, and level of biogenic amines in crickets

https://doi.org/10.21203/rs.3.rs-2957977/v1

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published 27 Jul, 2023

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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.

Electromagnetic field

HPLC

stress

mating behaviour

communication

insects

The electromagnetic field (EMF) has always been naturally present in the environment. However, the increasing number of artificial sources of EMF (e.g. powerlines, wiring, electrical appliances, wireless communication), with an enormous range of new frequencies, modulations, and intensities, constitutes an emerging source of environmental pollution and raises concern about their unfavourable effects on organisms (Comba and Fazzo, 2009; Mattsson and Simkó, 2012; WHO, 2007). So far, little has been done to consider the potential environmental impacts of EMF, although it seems to represent a potentially significant environmental stressor (Blank and Goodman, 2009) that can lead to memory deficits (Jadidi et al., 2007), stress, anxiety (Liu et al., 2008) and depression-like behaviour (Szemerszky et al., 2010).

The majority of research in the area concerns mammals, practically neglecting lower organisms, such as insects, which are great models to study the impact of EMF at multiple levels of biological organization, including cognitive, behavioural, ecological, physiological, and molecular effects and their mechanisms (Baier et al., 2002; Horch et al., 2017; Wyszkowska et al., 2018). Moreover, given the great contribution of insects to global biodiversity and ecosystem services, as well as their multiple environmental and economic roles (e.g. as pests, pollinators, food sources, predators, herbivores, etc.), knowledge of their responses to emerging pollution sources is crucial for understanding the functioning of contemporary ecosystems, identifying potential economic threats, and designing novel measures of pest control and biodiversity conservation (Schowalter et al., 2018). Recently, EMF has been pointed out as one of the reasons for the rapid decline of the honeybee, known as an important pollinator of global importance. Current trends show substantial declines in insects in general, for at least the last three decades (Hallmann et al., 2017; Leather, 2018).

One of the mechanisms of negative effects of EMF on organisms can be the disruption of mating behaviour, including sending and receiving sexual signals and finding suitable partners. By assessing species-specific sexual signals, individuals make informed decisions about optimal mate selection, resulting in reproductive fitness benefits. However, these communication systems are susceptible to interference from human-made factors present in the environment, leading to their disruption and fitness reduction due to inefficient mate choice.

In the present study, we analysed the effect of EMF (50 Hz, 7 mT) on the reproductive behaviour of the two-spotted cricket Gryllus bimaculatus. This species is an important model organism in neurobiological, physiological, developmental, and regeneration research (Horch et al., 2017; Mito and Noji, 2008). Its mating behaviour is well understood and described: males rub their forewings together (Baker et al., 2019) generating species-specific acoustic signals, known as calling songs used to communicate information critical for reproduction (location and quality of the male) to females.

We hypothesized that exposure to EMF would affect the quality of male calling songs and, in consequence, their attractiveness to females. Moreover, we assumed that EMF would cause changes in the levels of biogenic amines in the insect brain, indicating increased stress.

Animals

Crickets Gryllus bimaculatus (De Geer) were raised in a laboratory colony on a 14h:10h light and dark cycle (lights on at 6:00 h) at 28 ± 2ºC. They were fed with insect food (Sankyo Lab, Tokyo Japan) and water ad libitum. Each developmental stage was kept in a plastic box (300 mm x 500 mm x 250 mm). Newly emerged virgin females and males were collected from the culture every day to create cohorts of the same age. Insects were kept in single and mixed-sex cultures. After sexual maturation, 1- and 3 weeks-old crickets were used in experiments.

Electromagnetic field exposure system

The electromagnetic field (EMF) with the domination of magnetic component was generated by a 19 cm diameter coil designed by EiE (Elektronika & Elektromedycyna Sp. J., Otwock, Poland). This exposure system has been described in detail previously (Bieńkowski and Wyszkowska, 2014; Trawiński et al., 2010). The coil generated a homogeneous, sine-wave alternating EMF at 50 Hz. The distribution of magnetic flux density within the coil along the Z and X axes is shown in Fig. 1. The non-homogeneity of the field within the area containing the animal chamber was approximately 10%. The magnetic field strength was controlled before each experiment using a Gaussmeter (Model GM2, AlphaLab, Inc, USA). Animals were exposed to EMF (50 Hz, 7 mT) in a glass exposure chamber (diameter: 10 cm, height: 7.5 cm) located within the coil. The temperature in the exposure chamber was set to 24 ± 1℃ and monitored using thermocouples.

Calling song recording and analysis

Individual calling songs of males were recorded digitally at a constant temperature (24 ± 1°C) using a portable audio recorder: Linear PCM recorder, model PCM-D50 (Sony Corporation, Tokyo, Japan). Recordings were made during the first 3 h of the dark cycle. A female, selected randomly from the bulk stock, was put together with a male into an exposure chamber, which was then closed using a lid fitted with a wire flyscreen. The exposure chamber with the insects was located inside the coil. The exposure lasted for 10 min and consisted of the initial period before the EMF was turned on (3 min), actual exposure to the EMF (4 min) and the post-exposure period after the EMF was turned off (3 min). As soon as the male began to court the female, the audio was recorded. Recordings were obtained for 15 males and included three 1-min measurement periods: (1) “before” (2nd-3rd min of the exposure), (2) “during” (0.5–1.5 min after the EMF was turned on) and (3) “after” (2nd-3rd min after the EMF was turned off) the exposure to the EMF. The song recordings were analysed using WavePad software ver. 10.26 (NCH Software, CO, USA) and freeware Audacity 3.2.1 (https://www.audacityteam.org/). Parameters measured during each 1-min measurement period of the calling song were: (1) the chirp period (Fig. 2): a mean of 10 random chirps; (2) chirp rate: the number of chirps per min measured directly in oscillograms; (3) the dominant frequency (highest peak) [Hz] obtained from the spectrum using the Fast Fourier Transform.

Phonotaxis experiment

Male calling songs were recorded by exposing an animal in the exposure chamber for 5 min to the EMF and then for another 5 min with the EMF turned off. The exposure conditions were the same as described above for the calling song analysis. Thus, natural and EMF-modified signals used in this experiment were obtained from the same individual, ensuring that females responded to the EMF impact on males, rather than to inter-individual differences in signal quality.

A single female cricket was positioned on the top of a Styrofoam trackball (φ = 10 cm, 8.7 g) in its natural walking posture (Fig. 3). The tip of a wire holder was fixed to the centre of the pronotum with a mixture of beeswax and resin to keep the animal in place. The walking insect moved in place, changing the position of the trackball (Hedwig, 2017). The motion of the trackball was recorded using optical motion sensors repurposed from a computer mouse (Taylor et al., 2015). Tracking data were collected and processed with the custom-made software that kept track of changes in x and y coordinates as the ball rotated in response to the insect movements (Owaki et al., 2021). The trackball movements allowed us to determine the insect’s speed and walking direction (Hedwig, 2017).

Experiments were conducted on females responding to a male calling song (85 dB) played from a loudspeaker situated on the left side of the experimental arena (Fig. 3). Females were divided into two groups: 3 weeks old (which had a contact with males before in a mixed-sex colony, N = 16) and 1 week old (virgins, no previous contacts with males, N = 16) and placed individually on the ball. They were acclimated to the experimental set-up for 3 min prior to the experiment. Then, all individuals were exposed to the "control" signal (a calling song recorded under control conditions) for 5 min. Then, after a 5-min interval, the females from the experimental group (N = 8 per each age group) were exposed to the "changed" signal (a calling song of a male exposed to EMF) for 5 min, whereas the control females (N = 8 per each age group) were again exposed to the "control" signal. All trials were performed in darkness at 24 ± 1°C.

Phonotaxis data analysis

The entire recording (two 5-min periods) was divided into 5-s intervals. For each interval, using the XY coordinates describing the cricket position, we determined (1) the angle between the direction of translocation and the direction straight towards the signal source, and (2) the translocation distance. The angles ranged from 0 to 360°, with values close to 0 and 360° pointing towards the signal, those approaching 180° pointing away from the signal and those around 90 or 270° perpendicular to the signal direction. As we were only interested in the axis parallel to the signal direction (i.e. it did not matter whether a cricket deviated left or right from this direction), we transformed the angle values (D) according to the formula:

$${D}^{{\prime }}=\left\{\begin{array}{c}90^\circ -D for D\le 180^\circ \\ D-270^\circ for D>180^\circ \end{array}\right.$$

The transformed variable ranged from − 90 to 90°, direction towards the signal being 90°, direction away from the signal: -90° and direction perpendicular to the signal position: 0°. Thus, a circular angle variable was transformed into a linear variable that could be analysed using standard statistical methods. Then, for each of the two 5-min periods, we calculated (1) the mean direction (angle, D’); (2) the difference between the total distances moved towards and away from the signal (including only movements with directions higher than 45° or lower than − 45°); (3) the difference between the total times spent on moving towards and away from the signal (again, only when the modulus of the direction > 45°). The latter two variables were calculated according to the formula:

$${\Delta }\text{M}= \left({M}_{T}-{M}_{A}\right)/\left({M}_{T}+{M}_{A}\right)$$

Where ΔM – the difference in movement time/distance between both directions, M_T, M_A – the movement time/distance towards and away from the signal, respectively. These variables ranged from − 1 to 1, indicating the prevalence of movement away (-1), irrespective of (0) and towards (1) the signal.

Biogenic amine levels

The levels of serotonin (5-HT), dopamine (DA), octopamine (OA) and tyramine (TA) were measured in male crickets randomly divided into two groups: individuals exposed individually to the EMF in the exposure chambers (see above) for 10 min (N = 10) and control individuals (N = 8). The control insects were tested under the same experimental conditions, but in the absence of EMF (the ambient magnetic field strength < 10 µT).

Immediately after the exposure, crickets were frozen using liquid N₂. Their brains were dissected out in the ice-cold cricket physiological saline (140 mM NaCl, 10 mM KCl, 1.6 mM CaCl₂, 2 mM MgCl₂, 44 mM glucose, 2 mM TES, pH 7.2), put separately into glass homogenisers and homogenised in 50 µl of ice-cold 0.1 M perchloric acid containing 5 ng of 3, 4-dihydroxybenzylamine (DHBA, SIGMA, St Louis, MO, USA) as an internal standard. After centrifugation of the homogenate (0°C, 15000 rpm, 30 min), 40 µl of the supernatant was collected. Biogenic amines in each sample were measured using high-performance liquid chromatography (HPLC) with electrochemical detection (ECD) (Aonuma, 2020; Aonuma and Watanabe, 2012; Owaki et al., 2021; Wada-Katsumata et al., 2011). The HPLC-ECD system was composed of a pump (EP-300, EICOM Co., Kyoto, Japan), an auto-sample injector (M-510, EICOM Co., Kyoto, Japan), and a C18 reversed-phase column (250 mm × 4.6 mm internal diameter, 5 µm average particle size, CAPCELL PAK C18MG, Shiseido, Tokyo, Japan) heated to 30°C in a column oven. A glass carbon electrode (WE-GC, EICOM Co.) was used for electrochemical detection (ECD-100, EICOM Co.). The detector potential was set at 880 mV versus an Ag/AgCl reference electrode, also maintained at 30°C in a column oven. The mobile phase containing 0.18 M chloroacetic acid and 16 µM disodium EDTA was adjusted to pH 3.6 with NaOH. Sodium-1-octanesulfonate at 1.85 mM as an ion-pair reagent and CH₃CN at 8.40% (v/v) as an organic modifier were added to the mobile phase solution. The flow rate was kept at 0.7 ml/min. The chromatographs were acquired using the computer program PowerChrom (eDAQ Pty Ltd, Denistone East, NSW, Australia). The supernatants of samples were injected directly into the HPLC column. After the acquisition, they were processed to obtain the level of biogenic amines in the same sample by the ratio of the peak area of substances to the internal standard DHBA (3,4-Dihydroxybenzylamine, SIGMA).

Statistical analysis

Data were analyzed using IBM SPSS Statistics for Windows, Version 25.0. Armonk (IBM Corp. Released 2017., NY: IBM Corp.) and GraphPad Prism version 7.00 for Windows (GraphPad Software, La Jolla California USA). All data were tested for normality (Shapiro test) and homogeneity of variance (Levene test).

A Principal Component Analysis (PCA) (correlation matrix, varimax rotation with Kaiser normalization) was applied to the variables characterising the recorded songs (chirp period, chirp rate, dominating frequency). The obtained principal components were analysed using 1-way repeated measures ANOVAs to check differences between the three parts of the song generated by each male individual. Significant ANOVA effects were further evaluated with sequential-Bonferroni-corrected t-tests for paired data.

As the female phonotaxis data were strongly heteroscedastic, we applied nonparametric tests to compare the experimental groups: pairwise Mann-Whitney tests to compare age groups and control vs. changed signal treatments, as well as Wilcoxon signed-rank tests to compare the first vs. second 5-min. observation period. Furthermore, we applied one-sample t-tests (for which the homoscedasticity assumption does not apply) to compare the mean values of the response variables for each experimental group and period against a theoretical value of 0, indicating no reaction to the signal. The results were sequential-Bonferroni corrected for multiple comparisons within each group of tests.

A PCA (correlation matrix, varimax rotation with Kaiser normalization) was applied to the biogenic amine levels (5-HT, DA, OA, TA) in the brain. The obtained principal components were compared between the control and EMF-exposed individuals using sequential-Bonferroni corrected t-tests.

Characteristics of male calling songs

The PCA extracted two principal components (PC1 and PC2) (Fig. 4). PC1 was positively associated with the chirp rate and negatively correlated with the chirp period, whereas PC2 depended on the value of the dominant frequency. PC1 scores differed among the song parts (repeated measures ANOVA: F_{2, 28} = 5.3, P = 0.011) with the values obtained during the exposure to EMF significantly larger than those obtained before and after the exposure (Fig. 4). The chirp rate during the exposure to EMF (182.7 ± 7.128 chirps/min) was higher by 2.7% and 4.7% than before (178.7 ± 8.111 chirps/min) and after (174.2 ± 7.706 chirps/min) the exposure, respectively (Fig. S1). The chirp period during the exposure to EMF (331 ± 11.1 ms) was shorter by 5.1% and 3.7% than before (350.8 ± 14.48 ms) and after (343.7 ± 13.41 ms) the exposure (Fig. S1), respectively. No significant differences among the song parts were found for PC2 scores; repeated measures ANOVA: F_{2, 28} = 2.31, P = 0.118). The spectrograms of calling songs showed high-energy peaks around 5.5 kHz (Fig. 2).

Phonotaxis of females

In all treatments and periods except the control 1-week old individuals during the first period, crickets tended to head towards the signal source, but this effect was significant only for the animals exposed to the EMF-changed signal (second period, both age groups) and for the 3-week old control crickets in the second period (Table 1a). This is indicated by a significant movement direction angle towards the signal source (all three groups, Fig. 5), the difference in time spent on the movement towards vs. away from the signal (all three groups, Fig. 6a), and/or the difference in distance moved towards vs. away from the signal (the 1- and 3-week old crickets exposed to the changed signal, Fig. 6b).

The 1-week-old crickets exposed to the changed signal during the second observation period modified their behaviour compared to the first period (Table 1b). Moreover, the behaviour of these individuals in the second period differed significantly from the 1-week-old control individuals (Table 1c), as well as from the 3-week-old individuals exposed to the changed signal (Table 1d). The 1-week-old individuals exposed to the changed signal exhibited more directional movement (Fig. 5), spent relatively more time moving towards the signal (Fig. 6a), and/or moved relatively longer distances in the signal direction (Fig. 6b).

Table 1

Behaviour of female crickets (1- or 3 weeks old) responding to control male signals and signals changed by the electromagnetic field.
			Movement angle		Net movement time		Net distance
Treatment	Age	Period	t/Z	P	t/Z	P	t/Z	P
a. Comparisons with a theoretical value of 0 (one-sample t-tests)
Changed	1w	1st	1.41	0.202	1.31	0.230	1.87	0.103
Changed	1w	2nd	8.85	< 0.001*	15.32	< 0.001*	41.72	< 0.001*
Changed	3w	1st	0.17	0.867	0.66	0.529	0.86	0.417
Changed	3w	2nd	3.67	0.008*	3.70	0.008*	5.21	0.001*
Control	1w	1st	1.38	0.210	0.59	0.576	0.58	0.579
Control	1w	2nd	1.07	0.318	1.29	0.237	1.43	0.196
Control	3w	1st	2.36	0.050	3.00	0.020	2.32	0.053
Control	3w	2nd	4.27	0.004*	4.89	0.002*	2.49	0.042
b. Comparisons between the first and second observation period (Wilcoxon tests)
Changed	1w		-2.52	0.012*	-2.52	0.012*	-2.38	0.017
Changed	3w		-0.98	0.327	-0.98	0.327	-0.70	0.484
Control	1w		-2.24	0.025	-1.68	0.093	-1.40	0.161
Control	3w		0.00	1.000	-0.84	0.401	-0.14	0.889
c. Comparisons between treatments (Mann-Whitney tests)
	1w	1st	-2.10	0.036	-1.26	0.208	-1.58	0.115
	1w	2nd	-2.94	0.003*	-2.74	0.006*	-2.74	0.006*
	3w	1st	-1.37	0.172	-1.16	0.248	-0.63	0.529
	3w	2nd	0.00	1.000	-0.21	0.833	-0.42	0.674
d. Comparisons between cricket ages (Mann-Whitney tests)
Changed		1st	-0.53	0.600	-0.32	0.753	-0.32	0.753
Changed		2nd	-2.42	0.016	-2.27	0.023	-2.59	0.010*
Control		1st	-2.10	0.036	-1.58	0.115	-1.79	0.074
Control		2nd	-0.84	0.401	-0.95	0.344	-0.63	0.528
Treatments: Changed, Control – changed signal treatment, Control – control treatment; ages: 1w – 1 week, 3w – 3 weeks; periods: 1st – the first 5-min period (the control signal for all individuals), 2nd – the second 5-min period (the changed or control signal, depending on the treatment). Net movement time/distance – relative difference between times/distances moved towards vs. away from the signal
Asterisks indicate significant differences after applying the sequential Bonferroni corrections for multiple comparisons

Table 1 Behaviour of female crickets (1- or 3 weeks old) responding to control male signals and signals changed by the electromagnetic field.

Amine levels

The PCA extracted two principal components (PC1 and PC2). PC1 was associated with the levels of 5-HT, DA, and TA, whereas PC2 was associated with the level of OA (Fig. 7). The scores of PC1 and PC2 differed among the individuals exposed to EMF and control animals (t-tests: t₁₆ = 3.38, P = 0.002, t₁₆ = 2.26, P = 0.019, respectively). The crickets exposed to EMF had higher levels of 5-HT, DA, and TA (PC1), and lower levels of OA (PC2), compared to the control animals (Fig. 7, Fig. S2).

In this work, we assessed changes in spectral, temporal, and functional features of the male calling song of Gryllus bimaculatus due to the exposure to EMF. In our experiments, we used the EMF with parameters (50 Hz, 7 mT) known of their biological effects, including modification of motor activity (Pešić et al., 2004), induction of depression-like behavior and corticosterone secretion (Kitaoka et al., 2013), free radical generation in the brain (Ciejka et al., 2011), modulation of the antioxidative defense and some of the fitness-related traits (Todorović et al., 2012), and impairment of spatial memory (Jadidi et al., 2007). Additionally, European Union Directive 2013/35/EU (Directive, 2013) indicated that EMF of 50 Hz and > 6 mT caused measurable biological effects. Under natural conditions, flying insects can be exposed to EMF of such intensity, e.g. bees flying at a distance of 1 cm from a powerline conductor (Petrović et al., 2013). Moreover, high-voltage power lines emitting EMF are often in the trajectory of many species (i.e. insects, birds). Nevertheless, even much lower intensities of EMF give rise to signals that can affect animal behaviour thousands of kilometers away from the source, e.g. EMF caused by storms increased the take-off rate of locusts that initiated flights (Bergh, 1979). Also, exposure to EMF of 20 µT at 50 Hz reduced the olfactory learning of bees (Shepherd et al., 2018). Our study can be a good reference for further analysis of how high levels of EMF might impact other insects providing valuable ecosystem services. Moreover, responses of insects can be extrapolated to estimate the risks and benefits of human treatments. EMF of similar parameters as that used in our study is commonly applied in magnetotherapy and widely used in the treatment of patients with such diseases as epilepsy, and rheumatoid arthritis, as well as in fracture and wound healing (Ciejka et al., 2011).

Our experiments have shown that male crickets exposed to an electromagnetic field generate calling songs with an increased chirp rate and shortened chirp period compared to the control group but without the dominant sound frequency change. The observed effects may be related to the direct effects of the EMF on the neuromuscular system (e.g. motor neurons). Another explanation is an indirect or parallel EMF action through a stress reaction (increased motor activity and/or changes in stress-related hormone levels).

Given the current knowledge of electric and magnetic phenomena and their biological effects, it is possible that the central nervous system and sensory processes could be affected by EMF exposure, resulting in changes in forewing movement frequency observed here. Observations supporting this assumption include: (1) the effect of exposure to EMF (50 Hz, 7 mT) on neural circuits controlling appendage movement and muscular force in locusts (Wyszkowska et al., 2016), EMF (50 Hz, 1 mT), (2) the influence of EMF on Ca²⁺ channel expression in neuronal synapses leading to changes in neuronal activity (Sun et al., 2016), (3) significant change in the Ca²⁺ influx after EMF (50 Hz, 50 µT) exposure (Barbier et al., 1996), (4) changes in the cell membrane potential and distribution of ions due to EMF exposure, e.g. through the modification of the Na⁺/K⁺ ATPase activity, as the frequency of the enzyme turnover rate is close to 50 Hz (Blank, 2005). Shepherd et al. (2021) observed a wing-beat frequency increase in locusts exposed to EMF (50 Hz, 1–7 mT) and suggested that the central pattern generator composed of interneurons and motor neurons, as well as mechanosensory signals may be directly affected by EMF.

The male calling song informs a female about the species identity and location of a sexually mature male and enables the female to approach the male by phonotaxis. The treadmill setups (usually a free-spinning Styrofoam ball) are popular for long trials in phonotactic choice tests (Hiraguchi and Yamaguchi, 2000). This setup allows to track the trajectory of a single individual in a very controlled environment. However, it monitors only one individual at a time and insects are usually restrained, so they cannot jump, roll over, or accelerate suddenly (Guerra et al., 2010; Hedwig, 2017).

Our results showed that the melody changed by the presence of EMF was more attractive than the natural signal to young (virgin) females but not to aged (3-week-old) females, which were attracted to both the changed and natural signals. The shorter chirp periods imply greater energetic investment per unit time. Our findings are consistent with Wagner et al. (1995) conclusions that females prefer energetically costly male displays, likely to be produced by males in better condition, e.g. with higher pathogen resistance (Ryder and Siva–Jothy, 2000). Moreover, females were found to prefer songs resembling those emitted by males during aggressive encounters (Pollack, 1982). In several species, aggression is linked to the reproductive success, as females prefer or are constrained to mate with dominant males because individuals in good condition (genetic/aerobic/energetic/body) can invest more energy into acoustic signaling and aggression (Bunting and Hedrick, 2018). Perhaps this is why young females in our study selected the changed signal even though the natural call song was still not attractive to them.

The reproductive value should decline with age, thus aged females should exhibit a higher motivation to mate and be less selective than younger females. In accordance with this assumption, we showed a lower selectivity of aged females with regard to signal quality. Prosser et al. (1997) revealed that older females of Gryllus integer (25–28 days after imaginal exclusion) exhibited greater movement toward a male calling song than younger females (11–14 days after imaginal exclusion). Aged females seemed more motivated to mate while younger females appeared more selective, only exhibiting preferences in trials with multiple mate opportunities, which is in line with our findings. On the other hand, in our study, the tendency to approach the preferred (i.e. changed) signal was higher in 1-week-old females compared to older individuals (Fig. 6b), indicating that the young age group was particularly susceptible to environmental changes induced by EMF. The EMF-modified signal seems to be a stronger and more attractive stimulus for young cricket females compared to the natural calling sound of this species (acting more strongly and on younger females), suggesting a pre-existing bias in female preferences (Basolo, 1990) and indicating potentially strong environmental effects of EMF pollution. It should be noted that, if the exposure to EMF modifies mating signal parameters used by females to recognize the quality of signaling males, it may disrupt mate selection and switch the attraction of females towards suboptimal male individuals. Over a longer perspective, this may lead to deterioration in the individual fitness of animals living in areas exposed to artificial electromagnetic fields.

Reactions to EMF (50 Hz, 1–7 mT) exposure as a stress factor can be observed as changes in behaviour 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, serotonin, and dopamine levels and reducing octopamine level in their brain. It is not clear whether these changes directly affected wing activity and modified calling song characteristics, or are indicators of stress, which affected cricket behaviour through some other mechanisms (e.g. direct effect of EMF on motor neurons, see above). Moreover, the observed changes in the brain of insects exposed to EMF may indicate potential further physiological and behavioural consequences, finally leading to the deterioration of their functioning, fitness, and survival over a longer time scale. In mammals, dysfunctions in monoamine neurotransmission are implicated in neurological disorders, including Parkinson’s disease, schizophrenia, anxiety, and depression (Kobayashi, 2001; Taylor et al., 2005). This also suggests insects as potential models to study the effects of EMF on humans.

Some studies have suggested that biogenic amine levels may be a potential area to elucidate the underlying mechanisms of EMF effects on insect behaviour (Wyszkowska et al., 2006). Important processes in the regulation of motor behavior are initiated by the neuroendocrine system (Bunting and Hedrick, 2018; Nässel and Winther, 2010; Ohkawara and Aonuma, 2016). Biogenic amines play a role in aggression, motivation, and mood as neurotransmitters, neuromodulators, and neurohormones in vertebrate and invertebrate nervous systems (Farooqui, 2007; Ohkawara and Aonuma, 2016; Roeder, 2005; Roeder et al., 2003).

Octopamine (OA) and its biological precursor tyramine (TA) are the most frequent insect amines. Within the CNS, they act directly on the central pattern generator of flight and mating behavior, affect motivational states, and mediate aspects of aggression (Adamo et al., 1995; Hoyer et al., 2008; Matsumoto and Sakai, 2001; Zhou et al., 2008). In the periphery, they sensitize sensory receptors, control neuromuscular transmission and muscle contraction kinetics, and enhance flight muscle glycolysis (Aonuma and Watanabe, 2012; Brembs et al., 2007; Pflüger and Duch, 2000; Roeder, 2005; Szczuka et al., 2013; Vierk et al., 2009; Watanabe et al., 2011). Octopamine acts as a stress-responsive hormone and neuromodulator, which, under EMF exposure, can be rapidly released into the hemolymph leading to a decrease in its concentration in the brain, as shown in our study. Increased TA level may be caused by external stimuli such as EMF and/or by OA depletion and activation of the synthesis mechanism. High levels of OA may also induce secondary effects including the desensitization of octopaminergic receptors or reduction of endogenous octopamine release by autoregulation (Robertson and Juorio, 1976).

Dopamine (DA) and serotonin (5-HT) are associated with motor control, arousal, and aggressive behaviours (Aonuma, 2020; Dyakonova and Krushinsky, 2013; Johnson et al., 2009; Kume et al., 2005; Stevenson et al., 2000). The increased dopamine level has been shown to drive high activity through cryptochrome (Kumar et al., 2012), whose role was also described in light-dependent magnetoreception in insects (Gegear et al., 2008; Netušil et al., 2021). DA was shown to be a key element in the response of Drosophila to metabolic, oxidative, and mechanical stressors (Neckameyer, 1998). Moreover, DA was released in the honeybee brain after electric shock stimulation (Jarriault et al., 2018) and, together with 5-HT, in response to alarm pheromone, increasing the likelihood of stinging (Nouvian et al., 2018). Kume et al. (2005) confirmed the participation of DA in the regulation of insect arousal (hyperactivity and shortening of the rest phase). Chen et al. (2008), on the other hand, showed depressed brain OA levels (similar to our study) and DA levels, as well as the unchanged 5-HT level in bees exposed to stress. In the light of the above-cited results, the increase in dopamine and serotonin levels in the cricket brain observed in our study suggests a stress-related response of these insects to EMF.

The present work for the first time demonstrated changes in biogenic amine levels in the insect brain occurring following exposure to EMF (50 Hz, 7 mT). Previously, changes in levels of biogenic amines under the influence of extremely low frequency-EMF have been determined in rats. Exposure to EMF (60 Hz, 2 mT) produced a significant increase in the levels of 5-HT and DA but a decrease in norepinephrine (a functional analogue of OA in vertebrates) in the rat brain (Chung et al., 2014), which is consistent with our observations. Similarly, EMF (10 Hz, 1.8–3.8 mT, 1h x 14d) exposure increased the rate of synthesis (turnover) of DA and 5-HT in the rat frontal cortex (Sieroń et al., 2004). Another study showed that the affinity of serotonin 5-HT (2A) receptors decreased and their density increased in the prefrontal cortex of rats after EMF (50 Hz, 0.5 mT) exposure (Janać et al., 2009).

In insects, amines were measured after exposure to a static electric field (34–164 kV/m) (Newland et al., 2015), which reduced 5-HT and DA levels, and increased OA level in the Drosophila brain. Drosophila avoided a static electric field and the wings were involved in its detection. The observed behaviour was related to the movement of electric charges on the surface of the insect body. However, such a mechanism is not expected during exposure to an alternating magnetic field, as in our study.

The electromagnetic field (EMF, 50 Hz, 7 mT) exposure of the cricket Gryllus bimaculatus leads to behavioural and physiological changes. Findings indicate that changes in the chirp rate might be a stress-related behaviour and are accompanied by changes in the levels of stress hormones in the brain, which in turn might have an impact on mating behaviour.

The reproduction of crickets is important to the worlds of plants, animals, and humans. The cricket diet contains a lot of cellulose-rich plant materials. Bacteria and fungi easily decompose cricket fecal matter, increasing the energy and nutrient flows in the ecosystem. This provides plants with a rich source of easily available essential growth factors. Crickets also help control plant communities in both natural and human-made ecosystems. Additionally, they are essential food sources for insectivores (Roger, 2021). In our work, crickets were only a model indicating that such a phenomenon may be much more common in nature, including other insect species. Changes in calling songs induced by EMF exposure may confuse mating, which can lead to adverse health outcomes, alter population dynamics, and impair sexual selection. Ultimately, it may be of ecological importance unless adaptations to cope with anthropogenic disturbance appear in human-impacted populations (Bent et al., 2021). EMF is becoming a very strong and important environmental factor. Concerns cannot be limited only to the human health, but also the ecological significance of EMF should be considered. Our results lead to a call for further studies on the effects of anthropogenic electromagnetic field on insects (including pollinators and insect models), as well as the identification of key knowledge gaps in this field to improve our understanding of the effects of EMFs in the environment (Vanbergen et al., 2019).

Acknowledgments

This study was supported by the Japan Society for the Promotion of Science (JSPS/OF215/022 -L16551)

Supplementary Information The online version contains supplementary material available at

Author contribution Joanna Wyszkowska: Conceptualization; Methodology; Formal analysis; Investigation; Writing - original draft; Writing - review & editing; Visualization; Funding acquisition. Jarosław Kobak: Formal analysis; Writing - review & editing; Visualization. Hitoshi Aonuma: Conceptualization; Methodology; Formal analysis; Writing - review & editing; Resources; Supervision; Funding acquisition.

Funding This study was supported by the Japan Society for the Promotion of Science (JSPS/OF215/022 -L16551)

Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper

Data availability The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Ethics approval Not applicable for this study.

Consent for publication Not applicable.

Consent to participate Not applicable.

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Electromagnetic field exposure affects the calling song, phonotaxis, and level of biogenic amines in crickets

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Electromagnetic field exposure system

Calling song recording and analysis

Phonotaxis experiment

Phonotaxis data analysis

Biogenic amine levels

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Characteristics of male calling songs

Phonotaxis of females

Amine levels

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