Molecular Biological Effects of Weak Low-Frequency Magnetic Fields: Frequency-Amplitude Efficiency Windows and Possible Mechanisms.

This review covers the phenomenon of resonance-like responses of biological systems to low-frequency magnetic fields (LFMF). The historical development of this branch of magnetobiology, including the most notable biophysical models that explain the resonance-like responses of biological systems to LFMF with a specific frequency and amplitude, is given. Two groups can be distinguished among these models: one considers ion-cofactors of proteins as the primary targets for the LFMF influence, and the other regards the magnetic moments of particles in biomolecules. Attention is paid to the dependence of resonance-like LFMF effects on the cell type. A radical-pair mechanism of the magnetic field's influence on biochemical processes is described with the example of cryptochrome. Conditions for this mechanism's applicability to explain the biological effects of LFMF are given. A model of the influence of LFMF on radical pairs in biochemical oscillators, which can explain the frequency-amplitude efficiency windows of LFMF, is proposed.

Cavefishes in Chronobiological Research: A Narrative Review.

Cavefish are vertebrates living in extreme subterranean environments with no light, temperature changes, and limited food. Circadian rhythms in these fish are suppressed in natural habitats. However, they can be found in artificial light-dark cycles and other zeitgebers. The molecular circadian clock has its peculiarities in cavefish. In Astyanax mexicanus, the core clock mechanism is tonically repressed in the caves due to the overactivation of the light input pathway. A lack of functional light input pathway but rather the entrainment of circadian genes' expression by scheduled feeding were revealed in more ancient Phreatichthys andruzzii. Different evolutionarily determined irregularities in the functioning of molecular circadian oscillators can be expected in other cavefish. The unique property of some species is the existence of surface and cave forms. Along with the ease of maintenance and breeding, it made cavefish a promising model for chronobiological studies. At the same time, a divergence of the circadian system between cavefish populations requires the strain of origin to be indicated in further research.

Influence of Calcium Resonance-Tuned Low-Frequency Magnetic Fields on Daphnia magna.

A biophysical model for calculating the effective parameters of low-frequency magnetic fields was developed by Lednev based on summarized empirical data. According to this model, calcium ions as enzyme cofactors can be the primary target of low-frequency magnetic fields with different parameters tuned to calcium resonance. However, the effects of calcium-resonant combinations of static and alternating magnetic fields that correspond to Lednev's model and differ by order in frequency and intensity were not studied. It does not allow for confidently discussing the primary targets of low-frequency magnetic fields in terms of the magnetic influence on ions-enzyme cofactors. To clarify this issue, we examined the response of freshwater crustaceans Daphnia magna to the impact of combinations of magnetic fields targeted to calcium ions in enzymes according to Lednev's model that differ in order of magnitude. Life-history traits and biochemical parameters were evaluated. Exposure of daphnids to both combinations of magnetic fields led to a long-term delay of the first brood release, an increase in the brood size, a decrease in the number of broods, and the period between broods. The amylolytic activity, proteolytic activity, and sucrase activity significantly decreased in whole-body homogenates of crustaceans in response to both combinations of magnetic fields. The similarity in the sets of revealed effects assumes that different magnetic fields tuned to calcium ions in biomolecules can affect the same primary molecular target. The results suggest that the low-frequency magnetic fields with parameters corresponding to Lednev's model of interaction between biological molecules and ions can remain effective with a significant decrease in the static magnetic background.

Magnetic Fluctuations Entrain the Circadian Rhythm of Locomotor Activity in Zebrafish: Can Cryptochrome Be Involved?

In the 1960s, it was hypothesized that slow magnetic fluctuations could be a secondary zeitgeber for biological circadian rhythms. However, no comprehensive experimental research has been carried out to test the entrainment of free-running circadian rhythms by this zeitgeber. We studied the circadian patterns of the locomotor activity of zebrafish (Danio rerio) under different combinations of light regimes and slow magnetic fluctuations, based on a record of natural geomagnetic variation. A rapid synchronization of activity rhythms to an unusual 24:12 light/dark cycle was found under magnetic fluctuations with a period of 36 h. Under constant illumination, significant locomotor activity rhythms with 26.17 h and 33.07 h periods were registered in zebrafish exposed to magnetic fluctuations of 26.8 h and 33.76 h, respectively. The results reveal the potential of magnetic fluctuations for entrainment of circadian rhythms in zebrafish and genuine prospects to manipulate circadian oscillators via magnetic fields. The putative mechanisms responsible for the entrainment are discussed, including the possible role of cryptochromes.

Influence of Geomagnetic Disturbances at Different Times of Day on Locomotor Activity in Zebrafish (Danio Rerio).

The influence of magnetic fields and natural geomagnetic storms on biological circadian rhythms are actively studied. This study reveals an impact of local natural perturbations in the geomagnetic field that occurred at different times of the day on circadian patterns of locomotor activity of zebrafish. A decrease in zebrafish swimming speed was observed during the geomagnetic disturbances before or after the fluctuations of diurnal geomagnetic variation. However, if the geomagnetic perturbations coincided with the fluctuations of diurnal geomagnetic variation, the decrease in zebrafish swimming speed was insignificant. This result suggests that the biological effects of geomagnetic disturbances may depend on synchronization with the diurnal geomagnetic variation. It implies that the previously published correlations between geomagnetic activity and medical or biological parameters could result from a disruption in circadian biorhythms.

Circadian rhythms in zebrafish (Danio rerio) behaviour and the sources of their variability.

Over recent decades, changes in zebrafish (Danio rerio) behaviour have become popular quantitative indicators in biomedical studies. The circadian rhythms of behavioural processes in zebrafish are known to enable effective utilization of energy and resources, therefore attracting interest in zebrafish as a research model. This review covers a variety of circadian behaviours in this species, including diurnal rhythms of spawning, feeding, locomotor activity, shoaling, light/dark preference, and vertical position preference. Changes in circadian activity during zebrafish ontogeny are reviewed, including ageing-related alterations and chemically induced variations in rhythmicity patterns. Both exogenous and endogenous sources of inter-individual variability in zebrafish circadian behaviour are detailed. Additionally, we focus on different environmental factors with the potential to entrain circadian processes in zebrafish. This review describes two principal ways whereby diurnal behavioural rhythms can be entrained: (i) modulation of organismal physiological state, which can have masking or enhancing effects on behavioural endpoints related to endogenous circadian rhythms, and (ii) modulation of period and amplitude of the endogenous circadian rhythm due to competitive relationships between the primary and secondary zeitgebers. In addition, different peripheral oscillators in zebrafish can be entrained by diverse zeitgebers. This complicated orchestra of divergent influences may cause variability in zebrafish circadian behaviours, which should be given attention when planning behavioural studies.

Cardiovascular Performance Measurement in Water Fleas by Utilizing High-Speed Videography and ImageJ Software and Its Application for Pesticide Toxicity Assessment.

Water fleas are a good model for ecotoxicity studies, and were proposed for this purpose by the United States Environmental Protection Agency, due to their easy culture, body transparency, and high sensitivity to chemical pollution. Cardiovascular function parameters are usually used as an indicator of toxicity evaluation. However, due to the nature of the heart and blood flow, and the speed of the heartbeat, it is difficult to perform precise heartbeat and blood flow measurements with a low level of bias. In addition, the other cardiovascular parameters, including stroke volume, cardiac output, fractional shortening, and ejection fraction, have seldom been carefully addressed in previous studies. In this paper, high-speed videography and ImageJ-based methods were adopted to analyze cardiovascular function in water fleas. The heartbeat and blood flow for three water flea species, Daphnia magna, Daphnia silimis, and Moina sp., were captured by high-speed videography and analyzed using open-source ImageJ software. We found the heartbeat is species-dependent but not size-dependent in water fleas. Among the three water fleas tested, D. magna was identified as having the most robust heartbeat and blood flow rate, and is therefore suitable for the ecotoxicity test. Moreover, by calculating the diameter of the heart, we succeeded in measuring other cardiovascular parameters. D. magna were challenged with temperature changes and a pesticide (imidacloprid) to analyze variations in its cardiovascular function. We found that the heartbeat of D. magna was temperature-dependent, since the heartbeat was increasing with temperature. A similar result was shown in the cardiac output parameter. We also observed that the heartbeat, cardiac output, and heartbeat regularity are significantly reduced when exposed to imidacloprid at a low dose of 1 ppb (parts per billion). The blood flow rate, stroke volume, ejection fraction, and fractional shortening, on the contrary, did not display significant changes. In conclusion, in this study, we report a simple, highly accurate, and cost-effective method to perform physiological and toxicological assessments in water fleas.

The Influence of Changes in Magnetic Variations and Light-Dark Cycle on Life-History Traits of Daphnia magna.

Day-night cycle is the main zeitgeber (time giver) for biological circadian rhythms. Recently, it was suggested that natural diurnal geomagnetic variation may also be utilized by organisms for the synchronization of these rhythms. In this study, life-history traits in Daphnia magna were evaluated after short-term and multigenerational exposure to 16 h day/8 h night cycle, 32 h day/16 h night cycle, diurnal geomagnetic variation of 24 h, simulated magnetic variation of 48 h, and combinations of these conditions. With short-term exposure, the lighting mode substantially influenced the brood to brood period and the lifespan in daphnids. The brood to brood period, brood size, and body length of crustaceans similarly depended on the lighting mode during the multigenerational exposure. At the same time, an interaction of lighting mode and magnetic variations affected to a lesser extent brood to brood period, brood size, and newborn's body length. The influence of simulated diurnal variation on life-history traits in daphnids appeared distinctly as effects of synchronization between periods of lighting mode and magnetic variations during the multigenerational exposure. Newborn's body length significantly depended on the lighting regime when the periods of both studied zeitgebers were unsynchronized, or on the interaction of light regime with magnetic variations when the periods were synchronized. These results confirm the hypothesis that diurnal geomagnetic variation is an additional zeitgeber for biological circadian rhythms. Possible mechanisms for these observed effects are discussed. Bioelectromagnetics. © 2020 Bioelectromagnetics Society.

Delayed consequences of the influence of simulated geomagnetic storms on roach Rutilus rutilus embryos.

This study presents data collected over a 3 year period on the effects of simulated geomagnetic storms (SGMS) on Eurasian roach Rutilus rutilus embryos. Effects were studied during different stages of early development. Rutilis rutilus were raised in ponds for 4 months after exposure to SGMS. The mass, standard length and morphological characteristics of under-yearlings exposed as embryos were recorded. A decrease in length-mass indices in under-yearlings was noted after they had been exposed to SGMS during the first 2 days or during the third and fourth days of early development. Near the time point of 48 h post fertilisation, either no effect or an increased size was observed. In addition, exposure to SGMS led to a redistribution of the vertebral number between the sections of the vertebral column as well as changes in the number of seismosensory system openings in the mandibular and praeoperculum bones of under-yearlings. Observed effects are similar to previously published data on the influence of anthropogenic magnetic fields on roach, namely changes in linear-mass indices, number of vertebrae and number of seismosensory system openings in the mandibular bones of under-yearlings exposed as embryos. Possible mechanisms of magnetic influence on early development of fish are discussed.

The response of Daphnia magna Straus to long-term exposure to simulated geomagnetic storms.

The capability of Daphnia magna to adapt to artificial low-frequency magnetic fields via a maternal effect has been demonstrated previously. The current study assessed the possibility of a maternal effect in response to simulated natural geomagnetic fluctuations. D. magna lines were exposed to simulated geomagnetic storms for two, five, and eight sequential generations. Evaluations were conducted on the 3rd, 6th, and 9th generations of daphnids from experimental and control lines in order to determine the period required for the formation of an adaptive maternal effect. The evaluations showed that larger offspring were produced when maturation and reproduction occurred under the same conditions as those in which the Daphnia had lived in for generations. These observations suggest a manifestation of an adaptive maternal effect occurs in response to long-term exposure to simulated geomagnetic storms. Ecological relevance of geomagnetic storms to natural populations of daphnids is discussed.

A simulated geomagnetic storm unsynchronizes with diurnal geomagnetic variation affecting calpain activity in roach and great pond snail.

It has been suggested that geomagnetic storms could be perceived by organisms via disruption of naturally occurring diurnal geomagnetic variation. This variation, in turn, is viewed by way of a zeitgeber for biological circadian rhythms. The biological effects of a geomagnetic storm, therefore, could depend on the local time of day when its main phase occurs. We have assessed calpain activity in tissues of roach (Rutilus rutilus) and great pond snail (Limnaea stagnalis) after exposure to a simulated geomagnetic storm, reproduced at different times of day, in order to evaluate this hypothesis. Significant decrease in calpain activity was observed in organisms exposed to the simulated geomagnetic storm whose main phase, and initial period of a recovery phase, did not coincide with the expected peak of diurnal geomagnetic variation. The results obtained are considered an experimental confirmation of the aforementioned hypothesis. Improvement of a correlative approach for the assessment of biological effects of geomagnetic activity can be achieved by considering information on the synchronization of geomagnetic storm's main phase with diurnal geomagnetic variation.

Biological effects related to geomagnetic activity and possible mechanisms.

This review presents contemporary data on the biological effects of geomagnetic activity. Correlations between geomagnetic indices and biological parameters and experimental studies that used simulated geomagnetic storms to detect possible responses of organisms to these events in nature are discussed. Possible mechanisms by which geomagnetic activity influences organisms are also considered. Special attention is paid to the idea that geomagnetic activity is perceived by organisms as a disruption of diurnal geomagnetic variation. This variation, in turn, is viewed by way of a secondary zeitgeber for biological circadian rhythms. Additionally, we discuss the utility of cryptochrome as a biological detector of geomagnetic storms. The possible involvement of melatonin and protein coding by the CG8198 gene in the biological effects of geomagnetic activity are discussed. Perspectives for studying mechanisms by which geomagnetic storms affect organisms are suggested. Bioelectromagnetics. 38:497-510, 2017. © 2017 Wiley Periodicals, Inc.

Influence of magnetic field on zebrafish activity and orientation in a plus maze.

We describe an impact of the geomagnetic field (GMF) and its modification on zebrafish's orientation and locomotor activity in a plus maze with four arms oriented to the north, east, south and west. Zebrafish's directional preferences were bimodal in GMF: they visited two arms oriented in opposed directions (east-west) most frequently. This bimodal preference remained stable for same individuals across experiments divided by several days. When the horizontal GMF component was turned 90° clockwise, the preference accordingly shifted by 90° to arms oriented to the north and south. Other modifications of GMF (reversal of both vertical and horizontal GMF components; reversal of vertical component only; and reversal of horizontal component only) did not exert any discernible effect on the orientation of zebrafish. The 90° turn of horizontal component also resulted in a significant increase of fish's locomotor activity in comparison with the natural GMF. This increase became even more pronounced when the horizontal component was repeatedly turned by 90° and back with 1min interval between turns. Our results show that GMF and its variations should be taken into account when interpreting zebrafish's directional preferences and locomotor activity in mazes and other experimental devices.

The response of Daphnia magna Straus to the long-term action of low-frequency magnetic fields.

We exposed Daphnia magna Straus to an extra-low-frequency magnetic field (ELF MF) for several sequential generations to study its affect on size and number of nonviable individuals in Daphnia offspring produced. The lines of D. magna were subjected to ELF MF over three months. The abundance, wet biomass, and morphometric parameters were measured for adults, first brood, and second brood over eight generations. Then, in order to find a maternal effect in the experimental lines of D. magna, separate tests were performed with the control and experimental lines. The number of nonviable offspring in the first five broods and newborns' body lengths in the first five broods were evaluated. The exposure of D. magna to ELF MF led to decreases in size and the biomass and changes in generalized variance of the measured morphometric parameters of Daphnids compared with the control. Daphnids from the experimental lines produced more viable and larger offspring in conditions of ELF MF action as compared with the control. These findings assess the impacts of magnetic fields influenced by anthropogenic factors on Daphnia and possibly the effects of laboratory equipment emitting ELF MF on Daphnia in experimental settings.

The response of European Daphnia magna Straus and Australian Daphnia carinata King to changes in geomagnetic field.

This study investigates the effects of lifelong exposure to reversed geomagnetic and zero geomagnetic fields (the latter means absence of geomagnetic field) on the life history of Daphnia carinata King from Australia and Daphnia magna Straus from Europe. Considerable deviation in the geomagnetic field from the usual strength, leads to a decrease in daphnia size and life span. Reduced brood sizes and increased body length of neonates are observed in D. magna exposed to unusual magnetic background. The most apparent effects are induced by zero geomagnetic field in both species of Daphnia. A delay in the first reproduction in zero geomagnetic field is observed only in D. magna. No adaptive maternal effects to reversed geomagnetic field are found in a line of D. magna maintained in these magnetic conditions for eight generations. Integrally, the responses of D. magna to unusual geomagnetic conditions are more extensive than that in D. carinata. We suggest that the mechanism of the effects of geomagnetic field reversal on Daphnia may be related to differences in the pattern of distribution of the particles that have a magnetic moment, or to moving charged organic molecules owing to a change in combined outcome and orientation of the geomagnetic field and Earth's gravitational field. The possibility of modulation of self-oscillating processes with changes in geomagnetic field is also discussed.

Effects of electromagnetic fields on parthenogenic eggs of Daphnia magna Straus.

Developing parthenogenetic eggs of Daphnia magna were used as a test-system to evaluate the effect of a number of low-frequency electromagnetic fields (EMF) of 75microT density. Two blocks of EMF acting frequencies were found in the studied series-45, 110, and 175Hz, and 435 and 500Hz. Developing parthenogenetic eggs of D. magna exposed to EMF with indicated parameters have shown accelerated rates of embryonic development. Females that developed from exposed eggs have shown deteriorated production characteristics in their first brood. Used test-system may be successfully utilized to detect weak effects directly during embryogenesis. However, results obtained only during daphnids' early developmental stages are incomplete without observations on their further development.