Abstract
Ambient levels of nonionizing electromagnetic fields (EMF) have risen sharply in the last five decades to become a ubiquitous, continuous, biologically active environmental pollutant, even in rural and remote areas. Many species of flora and fauna, because of unique physiologies and habitats, are sensitive to exogenous EMF in ways that surpass human reactivity. This can lead to complex endogenous reactions that are highly variable, largely unseen, and a possible contributing factor in species extinctions, sometimes localized. Non-human magnetoreception mechanisms are explored. Numerous studies across all frequencies and taxa indicate that current low-level anthropogenic EMF can have myriad adverse and synergistic effects, including on orientation and migration, food finding, reproduction, mating, nest and den building, territorial maintenance and defense, and on vitality, longevity and survivorship itself. Effects have been observed in mammals such as bats, cervids, cetaceans, and pinnipeds among others, and on birds, insects, amphibians, reptiles, microbes and many species of flora. Cyto- and geno-toxic effects have long been observed in laboratory research on animal models that can be extrapolated to wildlife. Unusual multi-system mechanisms can come into play with non-human species — including in aquatic environments — that rely on the Earth’s natural geomagnetic fields for critical life-sustaining information. Part 2 of this 3-part series includes four online supplement tables of effects seen in animals from both ELF and RFR at vanishingly low intensities. Taken as a whole, this indicates enough information to raise concerns about ambient exposures to nonionizing radiation at ecosystem levels. Wildlife loss is often unseen and undocumented until tipping points are reached. It is time to recognize ambient EMF as a novel form of pollution and develop rules at regulatory agencies that designate air as ‘habitat’ so EMF can be regulated like other pollutants. Long-term chronic low-level EMF exposure standards, which do not now exist, should be set accordingly for wildlife, and environmental laws should be strictly enforced — a subject explored in Part 3.
Introduction: electromagnetic fields — natural and man-made
In Part 1 of this three-part series, rising ambient EMF levels were explored. Part 2 focuses specifically on the unique magnetoreception physiologies found in wildlife as well as the mechanisms by which they interact with the Earth’s natural geomagnetic fields and man-made EMF at intensities now commonly found in the environment. Part 2 Supplements contain tables of studies showing effects at extremely low intensity exposures comparable to today’s ambient levels.
Energy is a part of nature affecting every living thing in positive, negative and neutral ways. The Earth itself is a dipole magnet with a north and a south pole. All living things have evolved within the protective cradle of the Earth’s natural geomagnetic fields. In fact, magnetic oscillations emanate from the Earth’s molten iron core around 10 times per second (10 Hz) where relaxed but alert human thought/brainwaves occur between 8 and 14 Hz.
In addition to the Earth’s natural emanations, vast Schumann Resonances (SR) that constantly circle the globe were theorized in 1952 by physicist Windfried Otto Schumann and reliably measured in the 1960s [1, 2]. SR are a global electromagnetic phenomenon caused by a complex relationship between lightening at the Earth’s surface and the ionosphere. Excited by the 2,000 thunderstorms that occur globally at any given time and approximately 50 flashes of lightening every second, the space between Earth and the ionosphere 60 miles (97 km) above it form a resonant cavity and closed waveguide [3]. Schumann Resonances occur in the ELF bands between 3 and 60 Hz with distinct fundamental peaks around 7.83 Hz. Since the 1960s, scientists have discovered that variations in the resonances correspond to seasonal changes in solar activity, the Earth’s magnetic environment, in atmospheric water aerosols and various other earth-bound phenomena, including increased weather activity due to climate change. There are an estimated 1.2 billion lightening flashes globally each year, 25 million in the U.S. alone [4], not all of which are of sufficient length to contribute to the resonances.
The electromagnetic spectrum.
The electromagnetic spectrum is divided into ionizing and nonionizing radiation. Ionizing radiation falls at and above the ultra violet range in the light frequencies. Examples of ionizing radiation include gamma rays, cosmic rays, X-rays and various military and civilian nuclear activities. It is the nonionzing bands that we have completely filled in with modern technology.
Many behavioral aspects in biology are thought to be synchronized with both the Earth’s natural fields and the Schumann Resonances. Many species rely on the Earth’s natural fields for daily movement, seasonal migration, reproduction, food-finding, and territorial location, as well as diurnal and nocturnal activities. Human circadian rhythms, mainly regulated by light targeting signaling pathways in the hypothalamic suprachiasmatic nucleus, are known to be finely tuned to the Earth’s day/night cycles as well as natural seasonal variations, as are most species [5], [6], [7], [8]. Artificial ELF-EMF is also known to adversely affect human circadian clocks, possibly through modulation in circadian clock gene expression itself [9].
Nonionizing electromagnetic fields (EMF; 0–300 GHz) include all the frequencies that fall between visible light below the ultraviolet range and the Earth’s natural static fields. The nonionizing bands are used in virtually everything involved with communications and energy propagation so useful in modern life, including electric power production/distribution, all wireless technologies and accompanying infrastructure for cell phones, WiFi, baby/home monitoring systems, ‘smart’grid/meters, all ‘smart’ technology/devices, 2-through-5G Internet of Things, AM/FM broadcast radio and television, shortwave and HAM radio, surveillance/security systems, satellites, radar, many military applications, and myriad medical diagnostic tools like MRI’s, to name but a few (see Figure 1).
In its natural state, very little radiofrequency radiation (RFR) reaches the Earth’s surface. Aside from the Earth’s natural extremely low frequency (ELF) direct current (DC) magnetic fields, lightening and sunlight would primarily comprise our normal exposures to the electromagnetic spectrum. Most harmful radiation coming from outer space is blocked by the Earth’s magnetosphere. But now, for the first time in evolutionary history, we have infused the Earth’s surface with a blanket of artificial energy exposures with no clear understanding of what the consequences may be.
And although “natural,” not all energy is alike. Man-made exposures contain propagation characteristics — such as alternating current, modulation, complex signaling characteristics (e.g., pulsed, digital, and phased array), unusual wave forms (e.g., square and sawtooth shapes), and at heightened power intensities at the Earth’s surface that simply do not exist in nature. These are all man-made artifacts. In our embrace of technology, we have completely altered the Earth’s electromagnetic signature in which all life has evolved, in essence bypassing the magnetosphere’s protection. And because so much of wireless technology is satellite based, increasing exposures are no longer just ground-generated. All atmospheric levels are now affected by increasing ambient exposures (see Part 1 and Part 1 Supplement). This is especially true in the lower atmosphere, which is ‘habitat’ (beyond mere oxygen and clean air standards) for all species that mate, migrate, and feed in the air — including birds, mammals (such as bats), insects and some arachnids.
Species extinctions
There has been an unprecedented rate of biodiversity decline in recent decades according to the International Union for Conservation of Nature [10] which maintains a “Red List of Threatened Species” that is considered the world’s most comprehensive source on the global conservation status of animal, fungi and plant species — all critical indicators of planetary health.
IUCN’s 2018 list showed that 26,000 species are threatened with extinction, which reflected more than 27% of all species assessed. This was greatly increased from their 2004 report that found at least 15 species had already gone extinct between 1984 and 2004, and another 12 survived only in captivity. Current extinction rates are now at least 100 to 1,000 times higher than natural rates found in the fossil record.
The more recent May 2019 report by the Intergovernmental Science and Policy Platform on Biodiversity and Ecosystem Services, Paris, France [11] projected that at least 1 million plant and animal species worldwide are at imminent threat of extinction if our current human actions and activities are not immediately reversed. A review of 73 reports by Sanchez-Bayo and Wyckhuys [12] found those rates had greatly accelerated. The authors noted that biodiversity of insects in particular is threatened worldwide with dramatic declines that could lead to a 40% extinction of insect species over the next several decades. In terrestrial ecosystems they found Lepidoptera, Hymenoptera, and Coleoptera (dung beetles) were most affected, while in aquatic ecosystems Odonata, Plecoptera, Trichoptera and Ephemeroptera have already lost a considerable proportion of species. Affected insect groups included niche specialist species, as well as common and generalist species, many of which are critically important for pollination, as well as seed, fruit, nut and honey production, and natural pest control, among others of immeasurable economic and ecological value.
Humans are the primary cause for most declines via habitat destruction/degradation; over-exploitation for food, pets, cattle and medicine; artificially introduced species; pollution/contamination; pesticides; and disease. Climate change is increasingly established as a serious threat, as well as agricultural practices like monoculture crops for cattle feed, biofuels, and timber. New pesticides and weed killers introduced within the last 20 years, using neonicotinoids, glyphosphate, and fipronil, are especially damaging since they are long-lasting and capable of sterilizing soil of beneficial microorganisms, including worms and grubs, which can then extend to areas far beyond applications sites.
One example of multi-factorial damage includes the iconic American Monarch butterfly (Danaus plexippus) which is found across America and Southern Canada and generally geographically divided into eastern and western migratory groups by the Rocky Mountains. That species has declined by a full 99.4% in the west since the 1980s — 85% of that being since 2017 [13, 14]. According to the Center for Biological Diversity [15], the eastern monarch population has shrunk by 90% in the past two decades. Massive habitat loss, wildfires, climate change, droughts, enhanced storm ferocity, and the 1990s introduction of Monsanto “Roundup Ready” crops capable of surviving herbicides that kill other weeds — including milkweed, which monarchs need for breeding and as their sole food supply along their migratory routes — are thought to be the primary culprits.
Here, we argue, environmental EMF should be added to this list since many insects and other living species have sensitive receptors for EMF, e.g., monarchs were found to have light sensitive magnetoreceptors in their antennae that serve as an inclination compass when daylight is absent [16]. RFR is also known to alter the time period needed for a butterfly to complete morphogenesis, plus gastrulation and larval growth can be accelerated [17]. And the devastating loss of pollinating insects like honey bees and other wild pollinators may also be related to environmental EMF (see “Insects” below.)
Anecdotally, many people recall when there were significantly more insects and far more abundant wildlife. Since about 1980, there has been a steady, almost imperceptible, biodiversity diminishment among many species globally [18], [19], [20]. In 2018, scientists estimated that the largest king penguin colony shrank by 88% in just 35 years [21] due in major part to effects from climate change, while according to the International Scientific Committee for Tuna and Tuna-like Species in the North Pacific Ocean, over 97% of bluefin tuna have disappeared from the world’s oceans, primarily due to industrial overfishing but exacerbated by oil spills, contamination, and climate change. Tree and cave-dwelling bats until recently were common, including in the Eastern United States. Now with the massive impacts from White-nosed Syndrome (a fatal bat fungal disease), annual wind-turbine bat collision mortality estimated at nearly 1 million per year in the U.S. alone [22, 23], and pesticide use, few bats are seen. Bats species are also sensitive to EMF. Impacts from EMF as now seen in extensive reviews add only yet another troubling variable for all wildlife [24], [25], [26], [27], [28], [29], [30], [31], [32], [33], [34], [35], [36].
Since all food webs are uniquely tied together, there are negative cascading effects across all ecosystems. Birds that eat insects are hard hit: 8-in-10 partridges have disappeared from French farmlands while there has been a 50–80% reduction in nightingales and turtledoves respectively in the UK. Since 1980 the number of birds that typically inhabit Europe’s farmlands has shrunk by 55%, while in the last 17 years, French farmland-bird counts dropped by a full third. Intensified agricultural practices are thought responsible, with loss of insects being the largest contributor [12, 37]. In the United States, of the 1,027 species of migratory birds currently protected under the Migratory Bird Treaty Act of 1918, an estimated 40% are in decline based on breeding bird surveys [38], Christmas Bird Counts [39], and other monitoring tools [22, 23]. This trend is comparable to what is happening globally. What role EMF plays in these declines is unclear but remains a disturbing possibility. Nor do we understand the limits of tolerance any given species has for environmental disturbance — some show high flexibility while others thrive only within the narrowest ranges.
One estimate of Earth’s species finds that since 1970, wild animal populations have been reduced on average by 60%. Popularly called the “sixth mass extinction” [40], the term connotes the sixth time in the Earth’s history that large numbers of species have rapidly disappeared over a relatively short period, this time due to human activity, not asteroid strikes or volcanic activity. Though not officially so-designated, many now refer to this most recent geologic/ecosystem period as the “Anthropocene” — the Age of Man [41], [42], [43], [44], [45], [46].
Insect populations have been especially hard hit with extinctions eight times faster than that of mammals, birds and reptiles [12]. Insect total mass is falling by an estimated 2.5% per year, suggesting they could vanish by the next century. And what affects insect populations affects everything in the food web in one way or another. Loss of insect diversity and abundance can cause devastating effects throughout food webs and endanger entire ecosystems [12]. In Europe, Hallmann et al. [47] found a more than 75% decline over 27 years in total flying insect biomass in 63 protected areas, many throughout Germany. There was an 82% decline in mid-summer flying insect mass. Many European insect species migrate from distances as far away as Africa. The researchers noted that changes in weather, land use, and habitat characteristics alone cannot explain the overall decline and that there may be more than one unrecognized factor involved in evaluating declines in overall species abundance. That unrecognized factor may be the steadily rising ambient EMF that directly parallels these declines (see Part 1, Supplement 1).
Similar alarming invertebrate declines were discovered in the Western Hemisphere in 2017 when American entomologist Bradford Lister, after 40 years, revisited the El Yunque National Forest in Puerto Rico to follow up on a study begun in 1976 [48]. In the ensuing decades, populations of arthropods, including numerous flying insects, centipedes and spiders, had fallen by 98% in El Yunque, a pristine tropical rainforest within the U.S. National Forest System. Insectivores — including birds, lizards, and toads — showed similar declines, with some species vanishing entirely. After controlling for factors like habitat degradation or loss and pesticide use, the researchers concluded that climate change was the primary factor since the average maximum temperature in that rainforest had increased by 4 °F during that period. They did not factor in the large U.S. military VLF installation in Aquada that communicates with submarines all over the world, or the multiple sweeping over-the-horizon phased array radar units aimed at Puerto Rico from coastal sites in the U.S. that irradiate deep into that forest, or the multiple NOAA Doppler weather radar sites scattered all over the small island to track hurricanes, or the many cell towers there too.
These global declines are truly alarming with implications for planetary health as well as human and wildlife integrity. Many who study this say that climate change alone is not the only factor and that something new is going on [47]. The question is: could steadily rising environmental EMF, as one of the most ubiquitous but unrecognized new environmental genotoxins introduced since the 1980s, be contributing to these unprecedented species losses, beginning with insects but now manifesting in other species too? The upper microwave bands couple maximally with some insects the size of fruit flies and are capable of creating devastating resonance and other effects. Historically, radiofrequency radiation (RFR) impacts to insects were among the first biological effects to be studied [49] with the hope of discovering new forms of insect control [50]. All insect metamorphic developments have been studied, including egg, larva, pupa, and adult stages. One hypothesis holds that some adult species are more sensitive than at larval stages because adult appendages act as conducting pathways to the body (see “Insects” below).
It is these exact frequency bands between 30 kHz and 3 GHz used in telecommunications technology that have been on the rise during this period. And 5G is on the horizon which may specifically target insect populations (see Part 1).
Species sensitivity to EMFs
Other species have vastly more complex electromagnetic sensing tools than humans, as well as unique physiologies that evolved to sense weak fields. Many species are highly sensitive to the Earth’s natural electromagnetic fields, as well as geographic and seasonal variations. In fact, it appears that most living things — including many species of mammals, birds, fish, and bacteria — are tuned to the Earth’s electromagnetic background in ways once considered as “superpowers” but are now known to be physiological, even as mechanisms are still imperfectly understood. For example, many animals have been observed sensing earthquakes long before human instruments detect them, including snakes and scorpions that seek shelter; cattle that stampede; birds that sing at the wrong times of day; and female cats that frantically move kittens [7].
This ability is likely due, in part, to numerous species reacting to changes in the Earth’s magnetic field and electrostatic charges in the air detected through a naturally occurring mineral called magnetite found in many species [51, 52]. In fact, honey bees are able to detect static magnetic field fluctuations as weak as 26 nT against background earth-strength magnetic fields that are much higher [53] and to sense weak alternating fields at frequencies of 10 and 60 Hz [54]. Magnetite reacts a million times more strongly to external electromagnetic fields than any other known magnetic material. Authors Kobayshi and Kirchvink [52] and Kirchvink et al. [53, 54] hypothesized results were consistent with biophysical predictions of a magnetite-based magnetoreceptor. Other mechanisms, like radical pair mechanisms and cryptochromes, may also be responsible (see “Mechanisms” below).
Much has been written about magnetoreception — the term used to describe how species sense electromagnetic fields — which is well established but not well understood. Many species use information about the Earth’s natural fields for migration, mating, food-finding, homing, nesting, and numerous other activities. Migratory bird species [55, 56], honey bees [57], fish [58], mammals [59], bats [60], numerous insect species [61], mollusks [62], and even bacteria [63] are known to sense Earth’s magnetic fields in various ways. Magnetoreception may enable some bird species to actually see the Earth’s fields [64].
Some insect and arachnid species (e.g., Trichobothria) can detect natural atmospheric electric fields [65] which trigger ballooning behavior — e.g., climbing to the highest place, letting out silk, and traveling on wind currents using hair-like Trichobothria that detects airborne vibrations, currents, and electrical charge. Some have been found as high as 2.5 mi (4 km) in the sky, dispersing over hundreds of kilometers. Morley and Robert [65] found that the presence of a weak natural vertical e-field elicited ballooning behavior and takeoff in the spiders; their mechano-sensory hairs function as putative sensory receivers which are activated by natural weak electric-fields in response to both e-field and air-flow stimuli. The researchers hypothesized that atmospheric electricity was key to the mass migration patterns of some arthropod fauna.
Even soil nematodes (Caenorhabditis elegans) orient to earth-strength magnetic fields in their burrowing behaviors and a recent study by Vidal-Gadea [66] found that weak static fields slightly above Earth’s natural fields determined stem cell regeneration in flatworms (Planaria) [67].
Large ruminant mammalian species also orient to the Earth’s fields. Grazing cattle and deer were first observed aligning to geomagnetic field lines by Begall et al. [68]. Using satellite imagery, field observations, and measuring “deerbeds” in snow, they noted that domestic cattle across the globe, as well as grazing and resting red (Cervus alphas) and roe (Capreolus capreolus) deer, consistently align their body axis in a general north–south direction and that roe deer also orient their heads northward when grazing or resting. Burda et al. [69] discovered, however, that manmade ELF-EMF disrupted the north-south alignment with the geomagnetic field in resting cattle and roe deer when they found body orientation was random on pastures under or near power lines, with the disturbed pattern diminishing with distance from conductors. Cattle exposed to various magnetic field patterns directly beneath or near power lines exhibited distinct patterns of alignment. They concluded there was evidence for magnetic sensation in large mammals, as well as overt behavioral reactions to weak ELF-MF in vertebrates, implying cellular and molecular effects. Slaby et al. [70] also found cattle align along a north-south axis but suggested that such alignment may depend on herd density as the affect disappeared in herds with higher numbers. Fedrowitz [71] expanded this to include bovine sensitivity to other weak ELF-EMF from powerlines but with observed effects due to combined electric and magnetic fields rather than the electric field exposure alone (see “Bovines”below).
Cerveny et al. [72] found red fox (Vulpes vulpes) use geomagnetic fields during hunting. Even domestic dogs were found by Hart et al. [73] to be sensitive to small variations in the Earth’s orientation in their excretion habits, preferring a general north-south axis for both defecation and urination depending on geomagnetic field changes. And Nießner et al. [74] found dogs and some other species may actually “see” geomagnetic fields through blue-light sensing photoreceptor proteins in their eyes called cryptochromes.
According to the US/UK World Magnetic Model [75], sensitivity to the geomagnetic field may further complicate issues for migratory species (e.g., some turtles, sea animals, birds, and insects) because the Earth’s magnetic north pole is shifting faster than at any time in human history. Compared to the period between 1900 and 1980, it has greatly accelerated to about 30 mi (50 km) distance per year — moving west from over Canada’s Ellesmere Island, its traditional allocation for most of recorded history — toward Russia [76]. Magnetic north fluctuates according to changes in the Earth’s molten core, unlike true north which aligns according to the Earth’s axis. This trend may indicate a coming pole reversal with north and south trading places, something that occurs approximately every 400,000 years with the last being about 780,000 years ago. Some animals may be capable of recalibrating navigational cues but that remains to be seen. Since some migratory bird species may see geomagnetic fields through special receptor cells in their eyes and via other mechanisms, they could be thrown off course. It is unclear how many other species also see geomagnetic fields but some crustaceans and several insect species, especially those with compound eye structures consisting of thousands of ommatidia — tiny independent photoreception units with a cornea, lens, and photoreceptor cells that orient in different directions and distinguish brightness and many more bands of color than humans — are good candidates. Compared to single-aperture eyes, compound eyes have a very large view angle that can detect fast movement and in some cases light polarization.
In aquatic environments, some lakes have more than 200 species of fish that use some form of electromagnetism to locate food and reproduce. Electric eels can deliver a 500-V zap to kill prey. Sharks have an array of electromagnetic sensors. These include: magnetic field receptors in their mouths, eyes that are 10 times more sensitive than humans, and their perception of tiny electric neuronal discharges from the moving muscles in prey (including humans) guides their attacking/feeding behavior (see “Fish”below). Sharks are often attracted by low-level electromagnetic fields surrounding underwater electric cables and are sometimes electrocuted when they mistake the conduit for living prey and bite into it. Many fish have lateral lines on either side of their bodies that are composed of magnetite, which allows fish to swim in synchronous schools [52].
Many other animals evolved special receptor organs to detect environmental EMF. The duck-billed platypus (Ornithorhynchus anatinus), a semi-aquatic primitive egg-laying mammal, has thousands of electric sensors on its bill skin. As noted in Lai [77], using these electroreceptors and interacting with another type of mechanoreceptor, a platypus can detect an electric field of 20 μV/cm [78] — equivalent to that produced by the muscles of a shrimp. The information is processed by the somatosensory cortex of the platypus to fix the location of prey. This type of electroreception is common in the three species of monotremes: platypus, and long (Zaglossus bruijni) and short-bill (Tachyglossus aculeatus) echidna. Electric fish (elasmobranchs) emit EMF that covers a distance of several centimeters [79, 80]. This allows location of potential prey by comparing its electrical properties with that in its immediate vicinity. Their electroreceptors have been shown to detect a field of 5 nV/cm. Such EMF-sensing systems are highly sensitive and efficient but also highly vulnerable to disruption by unnatural fields. Organisms that use the geomagnetic field for migration have the capability not only to detect the field but also the orientation of the field.
Anthropogenic light frequencies affect wildlife in ways we have only recently grasped. Ecological studies have found that artificial light-at-night is disrupting nocturnal animals in devastating ways, including disorientation and disruption in breeding and migration cycles in turtles, flying insects, birds, butterflies and a host of other wildlife including mammals [81], [82], [83], [84]. As much as 30% of nocturnal vertebrates and over 60% of invertebrates may be affected by artificial light [85]. Illumination reflected off of clouds known as “sky glow” can produce unnaturally bright conditions at night from various wavelength spectra that impact different species, with the potential to alter the balance of species interactions [86, 87]. It has been found that changing the color of the light can help some species yet harm another [88]. For instance, low-pressure sodium lights that have more yellow in their spectrum reduce moth deaths around the bulbs, but salamanders cannot navigate from one pond to the next under yellow or red light. Some frogs have been observed to freeze for hours, even after lights have been turned off, and to suspend both feeding and reproduction [83].
One of nature’s great mysteries involves “natal homing behavior” — the ability of some animal species to return to their original location of birth in order to reproduce, sometimes over great distances. Natal homing behavior is known in sea turtles [89]; eels [90]; and salmon [91], among other species. The underlying mechanism, though imperfectly understood, involves such species “remembering” the geomagnetic field configurations of their birthplace via a process known as “imprinting,” and thus can locate and return to it even if they are thousands of miles/kilometers away at reproduction time. Apparently, newborns of these species are imprinted with the memory of the intensity and the inclination angle of the local geomagnetic field. This information is then later used to locate their place of birth where they return to breed.
The question is whether man-made EMF could distort this imprinting memory in later locating the site. For example, what if RFR-emitting facilities are located near turtle breeding sites? Could that interfere with imprinting? There is some evidence from Landler et al. [92] of adverse effects in turtles. The researchers found that RFR could disrupt a natural orientation, establish its own orientation, and reverse completely a natural orientation, indicating a need for research to further investigate as we simply do not know the full effects to other species from anthropogenic EMF.
Energy conduction in different species: unique physiologies and morphologies
The unique physiology and morphology of non-human species create additional complexities. For instance, quadrapedal species with four feet on the ground have different and potentially more efficient conductivity than bipedal species with two feet. One example is bovine heightened sensitivity to increased ground current near high tension lines [93, 94] and cell towers [95], [96], [97]. Also, bodies that are predominately parallel to the ground, which includes most four-legged mammals, rather than a perpendicular upright gait, conduct EMF in different ways than vertical species like humans, apes, and other primates. Species that hug the ground, like snakes, salamanders, and frogs, have unique exposures to ground currents, especially on rainy nights when water, as a conductive medium, can increase exposures [98]. This may make some species more sensitive to artificial ground current caused by electric utility companies using the Earth as their neutral return back to the substation for excess alternating current on their lines instead of running additional neutral lines on utility poles [99].
Hair and whiskers and related appendages in various species are known to detect small variations in electromagnetic fields as well as water and weather alterations [100]. In fact, ants have been observed to use their antennae as “EMF antennas” when subjected by researchers to external electromagnetic fields, aligning themselves to “channel” RFR away from the colony [7]. Species such as birds, as well as some insects with compound eyes structures, can see vastly more colors than humans, while cats, dogs, and owls, for instance, hear many more sound frequencies at incredibly low levels.
Magnetoreception mechanisms: electroreceptor cells, magnetite, cryptochromes/radical pairs
According to Lai [77], “…in order for an environmental entity to affect the functions of an organism, the following criteria have to be met: the organism should be able to detect the entity; the level of the entity should be similar to those in the normal ambient environment which is generally much lower than the level of the entity used in experimental studies; and the organism must have response mechanisms tuned to certain parameters of the entity that allow immediate detection of the presence and changes of the entity. Thus, a variation of the entity would be detected as an aberrant input and trigger a response reaction. In order to understand how man-made EMF affects wildlife, the above criteria must be considered, including multiple sensory mechanisms that vary from species to species.”
The questions are: How do diverse species detect weak natural geomagnetic signals, distinguish the subtle internal microcurrent and magnetic fields inherent to all biology from external fields, then get beyond both internal and external background noise to make use of that electromagnetic information?
There are three primary mechanisms used to understand magnetoreception:
Magnetic induction of weak electrical signals in specialized sensory receptors [101].
In the induction model (mechanism 1), according to Lin [102], the first category of electrodynamic interactions with weak magnetic fields is epitomized by elasmobranchs, including sharks, rays, and skates, with heads that contain long jelly-filled canals with high electrical conductivity known as the Ampullae of Lorenzini. As these fish swim through the Earth’s geomagnetic lines of flux, small voltage gradients are induced in these canals with electric field detections as low as 0.5 μV/m [101] The polarity of the induced field in relation to the geomagnetic field provides directional cues for the fish. However, in birds, insects, and land-based animals, such cells have not been found, indicating this may not be a universal mechanism but rather are environment/species-specific factors [111].
The magnetomechanical model (mechanism 2) involves the naturally occurring iron-based crystalline mineral called magnetite found in most species [52]. Its function is most simply demonstrated in magnetotactic bacteria [63] with high iron content where biogenic magnetite is manufactured in 20–30 single domain crystal chains [112]. Orientation is patterned according to the geomagnetic field. Blakemore et al. [113] found that magnetotactic bacteria in the northern hemisphere migrate toward the north pole of the geomagnetic field whereas the same strains migrate toward the South Pole in the southern hemisphere. At the equator, they are nearly equally divided in north- and- south seeking orientations [114]. And they all migrate downward in response to the geomagnetic field’s vertical component, which, in aqueous environments may be essential for their survival in bottom sediments.
Among the many species where magnetite has been found include the cranium and neck muscles of pigeons [115, 116]; denticles of mollusks [117, 118]; and the abdominal area of bees [119]. Tenforde [103] delineated other species with localized magnetite, including dolphins, tuna, salmon, butterflies, turtles, mice, and humans.
The third mechanistic model (mechanism 3) getting research attention today involves a complex free-radical-pair reaction and conversion of the forms of electrons (singlet-triplet inter-conversion) in a group of protein compounds known as cryptochromes. Cryptochromes have been found in the retinas of nocturnal migratory songbirds by Heyers et al. [55] and Moller et al. [56], showing complex communication with the brain for orientation when relying on magnetoreception. Gegear et al. [61] found cryptochromes to be a critical magnetoreception component in fruit flies (Drosophila melanogaster). As noted in Lai [77], cryptochrones are also present in the retinas of some animals [120]. RFR [121] and oscillating magnetic fields [122] have been reported to disrupt the migratory compass orientation in migratory birds. There are also reports that indicate the presence of cryptochromes in plants, which may be responsible for the effect of EMF on plant growth [123]. Cryptochromes are also known to be involved with circadian rhythms [56, 124]. For an excellent review on plausibility, theories, and complexities of cryptochrome/radical pairs, see Ritz et al. [111].
Many species likely use a combination of these mechanisms as well as more subtle influences as yet undetected. The vector of the geomagnetic field may provide the directional information, while intensity and/or inclination provide the positional information needed for orientation. In behavioral studies [125, 126], Wiltschko et al. found that birds used both magnetite and cryptochrome mechanisms when they responded to a short, strong magnetic pulse capable of changing magnetization of magnetite particles, while their orientation was light-dependent and easily disrupted by high-frequency magnetic fields in the MHz range indicating radical pair processes. These findings suggest that along with electrophysiological and histological studies, birds have a radical pair mechanism located in the right eye that provides compass-like directional information while magnetite in the upper beak senses magnetic intensity, thus providing positional information. However, Pakhomov et al. [122] pointed out that the songbird magnetic compass can be disrupted by an oscillating 1.403-MHz magnetic field of 2–3 nT, at a level that cannot be explained by the radical-pair mechanism.
Light plays a significant role [127], which is of environmental concern today as more technology moves toward using the infrared bands for communications and the increase of satellites create artificial/unfamiliar star-like lights in the night sky that are potentially capable of impacting night migration patterns. There is other evidence that species use a combination of photoreceptors and magnetite-based magnetoreception. As mentioned above, in birds the two mechanisms exist side by side, mediating different types of magnetic information as needed, such as flight on sunny vs. cloudy days or nocturnal flights, and they can be easily disrupted [106, 128], [129], [130]. Birds may co-process visual information with magnetic information and be able to distinguish between the two [131, 132]. This function likely occurs in the eye or higher avian brain areas via light-dependent information processing and radical pair cryptochromes [131, 133]. Birds’ magnetic compass is an inclination compass and RFR fields in the Larmor frequencies near 1.33 MHz were found to disrupt birds’ orientation in an extremely sensitive resonance relationship. Blue-light absorbing photopigment cryptochromes have been found in the retinas of birds. RFR appears to directly interfere with the primary processes of magnetoreception and disable the avian compass as long as the exposure is present [126, 128].
Mammals have also demonstrated magnetoreception indicating radical-pair mechanisms. Malkemper et al. [134] found that the surface-dwelling wood mouse (Apodemus sylvaticus) built nests in the northern and southern sectors of a visually symmetrical, circular arena, using the ambient magnetic field, or in a field rotated by 90°, indicating the animals used magnetic cues. When the mice were also tested in the ambient magnetic field with a superimposed radio frequency magnetic field (100 nT, 0.9 to 5 MHz frequency sweep), they changed preference from north-south to east-west nest building. But unlike birds that have been found sensitive to a constant Larmor frequency exposure at 1.33 MHz, that range had no effect on mice orientation. Individual animal physiology clearly plays a role in how various species respond. Malewski et al. [135] also found that the Earth’s magnetic field acts as a common directional indicator in five species of subterranean digging rodents. And for the first time, research also found that human brain waves exhibit a strong response to ecologically-relevant rotations of Earth-strength magnetic fields [136].
We need far better understanding of magnetoreception’s neural, cellular, and molecular processes because the ultimate question is, given our constant rising background levels of EMF, is this ambient noise reaching a tipping point beyond which species simply cannot “hear?” Are we artificially overwhelming living species’ ability to function with innate natural biological sensors that evolved over eons in a far more “electro-silent” world? The electroreception mechanisms described above — electroreceptors, magnetite, and cryptochrone/radical-pairs — enable living organisms to detect the presence and immediate changes in environmental fields of very low intensity. And thus they can be easily disturbed by the presence of unfamiliar low-intensity man-made fields.
Electrohypersensitivity in humans has also shown instantaneous response to EMF at low intensity [137]. According to Lai [77], one wonders whether the underlying mechanisms of electrohypersensivity are similar to those described above. Electrohypersensitivity may be a remnant of the evolutionary responses of living organisms to electromagnetic fields — particularly magnetic fields — in the environment. Similarities include responsiveness to very low-field intensity; the response is persistent and built into the physiology of an organism; and the response is immediate and reacts quickly to the fields. Cryptochrome-free radical mechanisms may be involved. Some people are more sensitive than others. Perhaps non-sensitive people can tolerate and compensate for effects, and/or have lost responsiveness to natural magnetic fields and thus have become evolutionarily aberrant. Electrosensitivity is an issue in need of more careful and systematic study and has yet to be broadly highlighted as a health or public welfare concern.
One recent theory by Johnsen et al. [138] postulates that magnetoreception in animal species may be “noisy” — meaning that the magnetic signal is small compared to thermal and other receptor noise, for instance. They speculate that magnetoreception may serve as a redundant “as-needed” source of information, otherwise animal species would use it as their primary source of information. Many species, they note, preferentially exploit non-magnetic cues first if they are available despite the fact that the Earth’s geomagnetic field is pervasive and ever-present. They speculate that magnetic receptors may thus be unable to instantaneously attain highly precise magnetic information, and therefore more extensive time-averaging and/or other higher-order neural processing of magnetic information is required. This may render “…the magnetic sense inefficient relative to alternative cues that can be detected faster and with less effort.” Magnetoreception may have been maintained, however, they said by natural selection because the geomagnetic field may sometimes be the only available source of directional and/or positional information.
We already know that some species use various mechanisms to detect EMFs as noted throughout this paper. With new environmental factors from anthropogenic causes, such as artificial light-at-night, air/water pollution, climate change impacting visibility as environmental cues, and rising background RFR — all of which can obscure natural information — magnetoreception may, in fact, become more necessary as an evolutionary survival tool as time goes on, not less.
Other mechanisms of biological significance: DNA — direct and indirect effects
(See Part 2, Supplements 1 and 2, for tables of ELF and RFR genetics studies)
A significant biological effect in any toxicology research involves the basic genetics of an exposed organism. Genetic effects consist mainly of gene expression, chromatin conformational changes, and genotoxicity. All such effects can influence normal physiological functions. Relevant to this paper is the fact that genetic effects are found at EMF levels similar to those in ambient environments, far below levels from communication devices and infrastructure (see Part 1, Supplement 1).
DNA, the fundamental building block of all life, is a molecular double helix that is coiled, twisted and folded within the nucleus of each living cell. It is essentially identical among species with variations only in number and specific genes along chromosomes on DNA’s twisted chains that distinguish various species and their characteristics from one another. DNA damage repeatedly seen in one species can therefore be extrapolated to other species, although not all species react the same to external stimuli.
Many factors, both endogenous and exogenous, damage DNA which is then normally repaired by DNA enzymes. But an absence of adequate repair can result in the accumulation of damaged DNA, which will eventually lead to aging, cell death (apotosis) and/or cancer. DNA breaks occur as both single and double strand events; double strand breaks are difficult to repair correctly and can lead to mutations. DNA damage from endogenous factors can include free radical formation from mitochondrial respiration and metabolism; exogenous factors include chemicals, ionizing and nonionizing radiation, and ultra violet light among others [139].
In several early studies, Lai and Singh [140, 141] found both double and single strand DNA breaks in the brain cells of rats exposed to RFR for 2 h at 2,450 MHz, and whole body SAR levels of 0.6 and 1.2 W/kg. The effects were interestingly blocked by antioxidants [142] suggesting free radical involvement, which could indicate an indirect cause for DNA damage (see below). The low-intensity genetic effects listed in Part 2 Supplements 1 and 2 are at 0.1 W/kg and less. Therefore, the Lai and Singh [140, 141] RFR studies are not included in those Supplements. Very similar effects have also been found by Lai and Singh [143, 144] with 60-Hz magnetic field exposure.
There has also been much study of ELF genetic effects. As discussed in Phillips et al. [139], numerous studies found that ELF-EMF leads to DNA damage [143], [144], [145], [146], [147], [148], [149], [150], [151], [152], [153], [154], [155], [156], [157], [158]. Two studies [159, 160] showed that ELF also affects DNA repair mechanisms. Sarimov et al. [161] found chromatin conformational changes in human lymphocytes exposed to a 50-Hz magnetic field at 5–20 µT. EMF-induced changes in cellular free radicals are also well studied [77, 162].
Others investigated DNA damage early on but without the availability of today’s more sensitive assays. Sarkar et al. [163] exposed mice to 2,450-MHz microwaves at a power density of 1 mW/cm2 for 2 h/day over 120, 150, and 200 days. They found DNA rearrangement in the testis and brain of exposed animals that suggested DNA strand breakage. Phillips et al. [164] were the first to use the comet assay to study two different forms of cell phone signals — multi-frequency time division multiple access (TDMA) and integrated digital enhanced network (iDEN) — on DNA damage in Molt-4 human lymphoblastoid cells using relatively low intensities of 2.4–26 W/g for 2–21 h. The authors reported seeming conflicting increases and decreases in DNA damage, depending on the type of signal studied, as well as the intensity and duration of exposure. They speculated the fields could affect DNA repair mechanisms in cells, accounting for the conflicting results.
In a recent literature review of EMF genetic effects by Lai [165], analysis found more research papers reporting effects than no effects. For RFR, 224 studies (65%) showed genetic effects while 122 publications (35%) found no effects. For ELF and static-EMF studies, 160 studies (77%) found effects while in 43 studies (23%) no effects were seen.
Research now points to the duration, signaling characteristics, and type of exposure as the determining factors in potential damage [164, 166], not the traditional demarcation between ionizing and nonionzing radiation. Long-term, low-level nonionizing radiation exposures common today are thought to be as detrimental to living cells as are short-term, high-intensity exposures from ionizing radiation. Effects may just take longer to manifest [167]. Nonionizing EMF at environmental levels does cause genetic damage. These have also been shown in humans exposed to environmental levels of EMF in both ELF and RFR ranges [168], [169], [170], [171]. Conceivably, similar genetic effects could happen in other species living in similar environments.
This body of genetics work goes against the pervasive myth that low-level, low-intensity nonionizing radiation cannot cause detrimental genetic effects. That premise is in fact the bedrock belief upon which vested interests and government agencies rely in support of current exposure standards. But in fact, biological systems are far more complex than physics models can ever predict [6, 8, 172]. A new biological model is needed because today’s exposures no longer fit that framework [173] for humans and wildlife. Enough research now indicates a reassessment is needed, perhaps including the very physics model used to back those traditional approaches (see Part 1).
Direct mechanisms: DNA as fractal antennas, cell membranes, ion channels
DNA as fractal antennas
There are several likely mechanisms for DNA damage from nonionizing radiation far below heating thresholds, both direct and indirect, intracellular, intercellular, and extracellular. Such mechanisms potentially apply to all wildlife. One direct mechanism theorizes that DNA itself acts as a fractal antenna for EMF/RFR [174], capable of receiving information from exogenous exposures.
According to Blank and Goodman [174], DNA has interesting electrical characteristics due to its unique structure of intertwined strands connected by rungs of molecules called nucleotides (also called bases), with each rung composed of two nucleotides (one from each strand) in bonded pairs. The nucleotides are held together by hydrogen bonds in close proximity that results in a strong attraction between the two strands. There are electrons on both molecular surfaces making the symmetrical nucleotides capable of conducting electron current along the entire DNA chain, a phenomenon called electron transfer. This makes DNA a most efficient electrical conductor, something not lost on nanotechnology researchers.
DNA may also act as an efficient fractal antenna due to its tightly packed shape within the cell nucleus. Blank and Goodman [174] characterized DNA properties in different frequency ranges, and considered electronic conduction within DNA’s compact construction in the nucleus. They concluded that the wide frequency range of observed interactions seen with EMF is the functional characteristic of a fractal antenna, and that DNA itself possesses the two structural characteristics of fractal antennas — electronic conduction and self symmetry. They noted that these properties contribute to greater reactivity of DNA with EMF in the environment, and that direct DNA damage could account for cancer increases, as well as the many other biological effects seen with EMF exposures.
A fractal is a self-repetitive pattern of sometimes geometric shapes, marked by a larger originating design progressing to small identical designs with a potentially unlimited periphery. Each part of the shape looks like the whole shape. Fractal designs are quite common in nature, e.g., in snail/mollusk shells, some deciduous tree leaves and conifer needles, pine cones, many flowering plants, some reptile scales, bird feathers and animal fur patterns, snowflakes, and crystals forming on cold winter glass windows. Minerals — both inert and biological — can also be fractals.
The varying sizes within fractals are what make them inherently multi-frequency. By mimicking nature, repetitive fractal patterns are also designed into mechanical transceiver antennas that radiate in multiband frequencies with more or less efficiency [175]. Cell phones, WiFi, digital TV, and many other transceivers use fractal antennas to operate.
The complex twisted shape and coiled structure of DNA — small coils coiled into larger coils, or coiled coils, which Blank and Goodman [174] note that no matter how far you zoom in or out, the shape looks the same — is the exact structure of a fractal that maximizes the length of an antenna within a compact space while boosting multi-frequency signals. As such, DNA may be acting as a hidden intracellular biological fractal capable of interacting with exogenous EMF across a range of frequencies. In fact, one of DNA’s fundamental functions may be specifically to interact with exogenous natural energy and as such may be more sensitive to EMF than other larger protein molecules within any living system. Once thought safely tucked away and protected within the nucleus, DNA may be acting as a most efficient electrical conductor at the nexus of all life. This interesting theory, unfortunately, has not been followed up by others to test its biological validity although fractals have been mimicked widely in technology.
Cell membranes/ion channels
Another direct effect from EMF is at the cell membrane itself. While DNA is life’s fundamental building block, cells are DNA’s complex electron-coherent architectural expression. The cell’s membrane is far more than just a boundary. It is rather the most important ordering tool in the biological space between intracellular and extracellular activities, “… a window through which a unitary biological element can sense its chemical and electrical environment” [176]. And it is replete with microcurrent.
The cell’s outer surface contains molecules that receive innumerable electrochemical signals from extracellular activities. Specific binding portals on the cell membrane set in motion a sequence leading to phosphorylation of specific enzymes that activate proteins for cellular ‘work.’ That includes everything from information processing in the central nervous system, mechanical functions such as muscle movements, nutrient metabolism, and the defense work of the immune system, among many others including the production of enzymes, hormones, antibodies, and neurotransmitters [177]. Complex microcurrent signaling pathways exist from the cell’s outside to the inside via protein intramembraneous particles in the phospholipid plasma membrane. These convey information on external stimuli to the cell’s interior to allow cellular function.
The cell membrane also has electrical properties. Microcurrent constantly moves from the interior to the exterior and vice versa of the cell membrane. According to Adey and Sheppard [176], some of these properties influence proteins that form voltage gated membrane channels, which is one way that cells control ion flow and membrane electromagnetic potential essential to life. There are specific windows that react according to frequency, amplitude, and duration differences, indicating a nonlinear and non-equilibrium character to exogenous exposures on cells [177], [178], [179], [180], [181], [182], [183], [184], [185].
Some pulsed fields are more biologically active than non-pulsed fields and different forms of pulsing also create different effects. As far back as 1983, Goodman et al. [186] found pulsed weak electromagnetic fields modified biological processes via DNA transcription when a repetitive single pulse and the repetitive pulse train were used. The single pulse increased the specific activity of messenger RNA after 15 and 45 min while the pulse train increased specific activity only after 45 min of exposure. Digital technology simulates pulsing and is the most common form of environmental exposure today.
Cellular calcium ion channels have long been of interest and may be particularly sensitive targets for EMFs due to possible increased calcium flux through the channels which can lead to secondary responses mediated through Ca2+/calmodulin stimulation of nitric oxide synthesis, calcium signaling, elevated nitric oxide (NO), NO signaling, peroxynitrite, free radical formation, and oxidative stress — many with implications to DNA as hypothesized by Pall [187]. Calcium is essential to signal transduction between cells and is significant to everything from metabolism, bone/cell/blood regeneration, hormone production and neurotransmissions among many others. These cellular calcium responses to EMF indicate an artificial change in the signaling processes at the cell membrane — considered a switchboard for information between the exterior environment and intracellular activities that guide cell differentiation and control growth [188].
Pall [187] cited 23 studies of effects to voltage gated calcium channels (VGCC) and noted nonthermal mechanisms were the most likely since many studies showed effects were blocked by calcium channel blockers (widely prescribed for heart irregularities having nothing to do with thermal issues). Pall [189] noted that many other studies showed EMF changes in calcium fluxes and intracellular calcium signaling. He hypothesized that alterations in intracellular calcium activity may explain some of the myriad biological effects seen with EMF exposure, including oxidative stress, DNA breaks, some cancers, infertility, hormonal alterations, cardiac irregularities, and diverse neuropsychiatric effects. These end points need further study and verification.
There is much to be learned about calcium effects as studies are contradictory. Changes in free radicals (see below) also affect calcium metabolism. There are more studies showing EMF effects on free radicals than calcium changes. Calcium activates the nitric oxide free radical pathway but there are only a few studies of this pathway following EMF exposure — less than 5% of EMF-oxidative change studies are on nitric oxide mechanisms. Also of interest is the fact that power density and frequency windows were seen in early research at rising harmonic increments along the electromagnetic spectrum beginning in the ELF bands [190], [191], [192], [193], [194], [195]. Observed effects were quite dramatic in what researchers described as calcium efflux or ‘dumping’ from cells. The most dramatic effects were seen at 180 Hz in the ELF range. This appears to contradict Pall’s work [189] cited above as increased calcium efflux is the opposite of what Pall’s hypothesis would predict, e.g., calcium influx. With more research both calcium influx and efflux effects may be found to be caused by different variables and/or EMF exposures.
In addition, exogenous signaling characteristics are also important to how cells react to both ELF and RFR ranges. Building on the work that demonstrated carrier waves of 50 and 147 MHz, when sinusoidally amplitude modulated at 16 Hz ELF in in vitro chick brain tissue [190, 191] and in live awake cat brain models [196] that created frequency windows for calcium efflux, Blackman et al. [194] additionally found that signaling characteristics were also significant. Research showed that calcium efflux occurred only when tissue samples are exposed to specific intensity ranges of an ELF-modulated carrier wave; unmodulated carrier waves did not affect ion efflux. Blackman et al. [194] further wrote that cells may be capable of demodulating signals. The authors reported that 16-Hz sinusoidal fields, in the absence of a carrier wave, altered the efflux rate of calcium ions and showed a frequency-dependent, field-induced enhancement of calcium-ion efflux within the ranges 5–7.5 V/m and 35–50 V/m (peak-to-peak incident field in air) with no enhancement within the ranges 1–2, 10–30, and 60–70 V/m. This body of work indicates that living cells interact with, and are capable of taking direction from, exogenous fields in far more complex ways than ever imagined, at intensities barely above background levels. This work may be particularly important to new technology that turns previously wired ELF frequencies into wireless applications, such as “wireless electricity” to charge electric cars.
Blackman et al. [197] found for the first time a link between the ELF/EMF being studied and the density of the natural local geomagnetic field (LGF) in the production of a biological response. Calcium efflux changes could be manipulated by controlling the LGF along with ELF and RF-EMF exposures. In a local geomagnetic field at a density of 38 μT, 15- and 45-Hz electromagnetic signals had been shown to induce calcium ion efflux from the exposed tissues, whereas 1- and- 30-Hz signals did not. Bawin and Adey [190] found a reduction in efflux when using an electric field; Blackman et al. [194] found an increase when using an electromagnetic field, thus identifying/isolating for the first time the significance of the magnetic field component in exposure parameters. Building on the window ranges noted above, Blackman et al. [197] demonstrated that the enhanced calcium efflux field-induced 15-Hz signal could be rendered ineffective when the LGF is reduced to 19 μT with Helmholtz coils. In addition, the ineffective 30-Hz signal became effective when the LGF was altered to k25.3 μT or to +76 μT. The results demonstrated that the net intensity of the local geomagnetic field is an important cofactor in biological response and a potentially hidden variable in research. The results, they noted, appear to describe a resonance-like relationship in which the frequency of the electromagnetic field can induce a change in calcium efflux proportional to LGF density (see Liboff [198, 199] below for more detail).
The bottom line is that changes of this magnitude at the cellular level — be it directly to DNA within the nucleus or via voltage gated channels at the cell’s membrane — can lead to direct effects on DNA within and across species. The evidence cited above illustrates the degree, likelihood, and variety of impacts from EMF directly on cellular physiology that are capable of affecting DNA in all living systems in myriad ways.
Indirect mechanisms: free radicals, stress proteins, resonance, Earth’s geomagnetic fields
Free radicals
An indirect, or secondary, mechanism for DNA damage would be through free radical formation within cells, which is the most consistently reported with both ELF and RFR exposures under many different conditions in biological systems. According to Phillips et al. [139], free radicals may also interact with metals like iron [142, 151, 152, 158] and play a role in genotoxic effects from something called the Fenton effect — a process “…catalyzed by iron in which hydrogen peroxide, a product of oxidative respiration in the mitochondria, is converted into hydroxyl free radicals, which are very potent and cytotoxic molecules” [139].
The significance of free radical processes may eventually answer some questions regarding how EMF interacts with biological systems. There are about 200–300 papers showing EMF effects on free radicals [77, 168, 200]. Free radicals are important compounds involved in numerous biological functions that affect many species. Increases in free radicals explain effects from damage to macromolecules such as DNA, protein, and membrane lipids; increased heat shock proteins; neurodegenerative diseases; and many more.
Yakymenko et al. [168] published a review on oxidative stress from low-level RFR and found induced molecular effects in living cells, including significant activation of key pathways generating reactive oxygen species (ROS), activation of peroxidation, oxidative damage in DNA, and changes in the activity of antioxidant enzymes. In 100 peer-reviewed studies, 93 confirmed that RFR induced oxidative effects in biological systems and that their involvement in cell signaling pathways could explain a high pathogenic range of biological/health effects. They concluded that low-intensity RFR should be recognized as one of the primary mechanisms of biological activity of nonionizing radiation. In a follow-up study, Yakymenko et al. [200] investigated the oxidative and mutagenic effects of low intensity GSM 1,800 MHz RFR on developing quail embryos exposed in ovo (0.32 μW/cm2, 48 s On, 12 s Off) during 5 days before and 14 days through the incubation period. They found statistically significant oxidative effects in embryonic cells that included a 2-fold increase in superoxide generation rate, an 85% increase in nitrogen oxide generation, and oxidative damage to DNA up to twice the increased levels of 8-oxo-dG in cells of 1-day old chicks. RFR exposure almost doubled embryo mortality and was statistically significant. They concluded that such exposures should be recognized as a risk factor for living cells, including embryonic integrity.
Lai [77] focused a review on static magnetic field ELF-EMF and found that changes in free radical activities are one of the most consistent effects. Such changes can affect numerous physiological functions including DNA damage, immune system and inflammatory response, cell proliferation and differentiation, wound healing, neural electrical activities, and behavior. Given that many species have proven sensitive to natural static geomagnetic fields and use such information in critical survival skills, some wildlife species may also be adversely affected via free radical alterations from anthropogenic exposures. But Lai [77] noted the inherent contradictions from EMF-induced changes in free radicals, particularly on cell proliferation and differentiation since those processes can affect cancer development as well as growth and development. Induced free-radical changes may therefore have therapeutic applications in killing cancer cells via the generation of the highly cytotoxic hydroxyl free radical by the Fenton Reaction (noted above), thereby creating a non-invasive low-side-effect cancer therapy.
Stress proteins
Another potentially indirect effect to DNA is via protein synthesis required by all cells to function. A living animal converts animal and plant proteins that it ingests into other proteins needed for life’s activities — antibodies, for instance, are a self-manufactured protein. DNA is critical to protein synthesis and can create in humans about 25,000 different kinds of proteins with which the body can then create 2,000,000 types in order to fully function.
There are many different classes of proteins. These include stress proteins stimulated by potentially harmful environmental factors to help cells cope and repair damage due to factors like acute temperatures, changes in oxygen levels, chemicals/heavy metals exposure, viral/bacterial infections, ultraviolet light and other ionizing and nonionizing radiation exposures [124].
The presence of stress proteins indicates healthy repair action by an organism and is considered beneficial up to a point as a protective mechanism. According to Blank and Goodman [201], “The 20 different stress protein families are evolutionarily conserved and act as ‘chaperones’ in the cell when they ‘help’ repair and refold damaged proteins and transport them across cell membranes. Induction of the stress response involves activation of DNA.” Stress proteins are also considered a yardstick to determine what living cells experience as stress that requires remediation in the first place — something not always obvious, especially with subtle environmental exposures like low-level EMF barely above natural background levels.
Whether an effect is thermal or nonthermal, adverse or simply observed biologically, has been subject to fierce debate for decades; thus tissue-heating DNA pathways are also central to this paper. Heat as a cellular stressor was first observed in the 1960s by Italian researcher Ferruccio Ritossa in fruit flies (D. melanogaster) when experimental temperatures were accidentally raised by a few degrees and he observed enlarged chromosomes at particular sites. (Drosophilae are often used in research because they only have four pairs of chromosomes, are relatively easy to work with, have a fast breeding cycle, and lay numerous eggs.) As cited in Blank [124], as Ritossa’s observation became better understood, with effects subsequently seen over decades in animals, plants and yeast cells, it came to be called the “heat shock response.” Extensive research established that the heat shock response lead to the formation of a unique protein class — heat shock proteins (HSP) that repair other proteins from potentially fatal temperature damage, as well as assist cells to be more thermo-tolerant. Research has gone on to prove that cells produce other similar proteins to various stressors, now generally called stress proteins but most are still categorized as “HSP” from the original demarcation.
Goodman and Blank [202, 203] found that EMF is a cellular stressor even at low intensities in the absence of elevated temperatures. They found the protein distribution patterns synthesized in response to ELF-EMF resembled those of heat shock with the same sequence of changes even though the energy of the two stimuli differed by many orders of magnitude. Their results indicated that ELF-EMF stimulates a similar gene expression pathway as that of thermal shock and is itself a cellular stressor. Of particular significance is the fact that over-expression of stress genes is found in a number of human tumors and is characteristic of a variety of neoplasia [202]. Increased stress proteins are seen in numerous animal model studies pertinent to wildlife.
Blank and Goodman [201] further noted that both ELF and RFR activate the cellular stress response despite the large energy difference between them; that the same cellular pathways respond in both frequency ranges; and that models suggest that EMF can interact directly with electrons in DNA. They note that low energy EMF interacts with DNA to induce the stress response while the increased energy in RFR can lead to DNA strand breaks. As such, this makes the stress response a frequency-dependent direct and indirect cause of DNA damage — a significant finding. They concluded that exposure standards should not be based on exposure intensity alone but on biological responses long before thermal thresholds are met or crossed.
Resonance and geomagnetic fields
There are other important direct and indirect ways that EMFs interact with and effect biological systems, including various forms of resonance — cyclotron, electron paramagnetic, nuclear, and stochastic — as well as through inherently produced biological materials such as magnetite found in bird brains and many other species (see below).
Resonance is the phenomenon that occurs when a certain aspect of a force (like a frequency wave) matches a physical characteristic (like a cell or whole living organism) and the power inherent in the force is transferred to the physical object causing it to resonate or vibrate. Within the object, the resonance is self-perpetuating. The classic example is of an opera singer hitting high C in the presence of a crystal goblet for a sustained period until it shatters.
Following the work of Blackman et al. [197] who found the Earth’s local geomagnetic fields (LGF) could influence calcium ions moving through membrane channels (see above), Liboff [198, 199] proposed that cyclotron resonance was a plausible mechanism for coupling interactions between the LGM and living cells. Liboff found cyclotron resonance consistent with other indications that showed many membrane channels have helical configurations; that the model could apply to other circulating charged components within the cell; and that cyclotron resonance could lead to direct resonant electromagnetic energy transfer to selected cell compartments.
All resonance is based on a relationship. Cyclotron resonance is based on the relationship between a constant magnetic field and an oscillating (time-varying) electric or magnetic field that can affect the motion of charged particles such as ions, some molecules, electrons, atomic nuclei, or DNA in living tissue. Living systems are filled with charged particles necessary for life, including calcium, sodium, lithium, and potassium ions that all pass through the cell membrane and are capable of affecting DNA. Cyclotron resonance occurs when an ion is exposed to a steady magnetic field (such as the Earth’s) which causes the ion to move in a circular orbit at a right angle to the field. The speed of the orbit is determined by the charge and mass of the ion and the strength of the magnetic field. If an electric field is added that oscillates at exactly the same frequency and that is also at a right angle to the magnetic field, energy will be transferred from the electric field to the ion causing it to move faster. The same effect can be created by applying an additional magnetic field parallel to the constant magnetic field. This is important because it provides a plausible mechanism for how living cells interact with both natural and artificial fields, and explains how vanishingly low levels of EMFs can create major biological activity when concentrated on ion particles. It also points to living systems’ ability to demodulate — or take direction from — certain aspects of electromagnetic information from both natural and artificial exposures [7]. Resonance should not be underestimated. It applies to all frequencies and is not based on power density alone.
Another subtle energy relationship in biology is called stochastic resonance that has been determined to be significant in how various species interact with their natural environments, in some instances for their survival. Stochastic resonance is a phenomenon where a signal below normal sensing can be boosted by adding wide-spectrum white noise signals. The frequencies in the white noise that match the original signal’s frequencies will resonate with each other and amplify the original signal while not amplifying the rest of the white noise. This increase in what is called the signal-to-noise ratio makes the original signal more prominent. Some fish, for instance, can “hear” predators better in the noise of running water than in still water due to stochastic resonance (see “Fish” below.).
The signal-to-noise ratio has been a prominent aspect of EMF research with some scientists long holding that energy exposures below the body’s natural signal-to-noise ratio could not possibly damage living tissue. But the most recent research that finds effects to DNA from low intensity EMF indicates that many variables affect biological processes, often in nonlinear patterns far below the signal-to-noise ratio. Some of the most cutting edge research — with an eye toward treating human in utero birth defects and adult limb regeneration — is being done by manipulating the electric charge across cell membranes (called membrane potential) via intentional manipulation of genes that form ion channels. Pai et al. [204] found that by putting ion channels into cells to raise the voltage up or down, they could control the size and location of the brain in embryonic African clawed frogs (Xenopus laevis), thus demonstrating the importance of microcurrents on membrane potential in growth and development. The research group also studied endogenous bioelectricity on clawed frog brain patterning during embryogenesis, noting that early frog embryos exhibit a characteristic hyperpolarization of cells lining the neural tube. Disruption of this spatial gradient of the transmembrane potential (V mem) diminished or eliminated the expression of early brain markers in frogs, causing anatomical mispatterning, including absent or malformed regions of the brain. This effect was mediated by voltage-gated calcium signaling and gap-junctional communication. The authors hypothesized that voltage modulation is a tractable strategy for intervention in certain classes of birth defects in humans but they did not make the leap to potential environmental damage to other species from such ambient exposures.
In general, whether direct, indirect, or synergistic, to understand ambient effects to wildlife, one also needs to know if effects are cumulative, what compensatory mechanisms a species may have, and when or if homeostasis will deteriorate to the point of no return [205]. In looking at environmental contaminants, we have historically focused on chemicals for both direct and indirect effects such as endocrine disruption. But primary biological manifestation is more physical than chemical since the only thing that distinguishes one chemical from another on the Periodic Table is the amount of electrons being traded up and down on the scale. Chemicals are actually secondary manifestations of initial atomic principles, not the other way around. Plus, the synergistic effects of the Earth’s natural fields can no longer be dismissed as an interesting artifact that is not biologically active or relevant. All living systems are first and foremost expressions of biological energy in various states of relationship.
For a Table of more low-level effects studies on DNA, see Part 2, Supplements 1 and 2.
What the studies show
The literature is voluminous on EMF effects to nonhuman species, going back at least to the 1930s using modern methods of inquiry. We have, after all, been using animal, plant, and microbial models in experiments for decades. We may in fact know less about effects to humans than to other species.
In this paper, we focused on exposures common in today’s environment. In Part 1, Rising Background Levels, we defined low level RFR as power density of 0.001 mW/cm2 (1 μW/cm2), or a SAR of 0.001 W/kg. Part 2 Supplements 3 and 4 contain extensive tables with pertinent studies that apply to fauna and flora, respectively. The sections that follow in Part 2 on individual species include selected studies of particular interest to how EMF couples with, and potentially affects, wildlife. In most studies, as illustrated in Part 2, Supplement 3, the intensity of the incident EMF was provided in μW/cm2 or V/m. To be consistent throughout the paper, we converted intensity in the studies to μW/cm2. However, such conversion (i.e. V/m to μW/cm2) tends to overestimate the exposure level and does not represent the full picture. Therefore where studies provided the amount of energy absorbed, e.g., the specific absorption rate (SAR), they were also included in Supplement 3 (in W/kg). Very low levels of energy absorption have shown effects in all living organisms studied.
Levitt and Lai [167] reported numerous biological effects from RFR at very low intensities and SARs comparable to far-field exposures within 197–492 ft (60–150 m) from cell towers. Included were in vivo and in vitro low-intensity RFR studies. Effects included genetic, growth and reproductive changes; increased permeability of the blood brain barrier; changes in stress proteins; behavioral responses; and molecular, cellular, genetic, and metabolic alterations. All are applicable to migratory birds, mammals, reptiles, and other wildlife and to plant communities, and to far-field exposures in general. (An update of that table appears in Part 2 Supplement 3.) It is apparent that environmental levels of RFR can elicit biological/health effects in living organisms. Although there are not enough data on low-intensity effects of static ELF-EMF to formulate a separate table, some effects of low-intensity static ELF-EMF are also described throughout this paper. ELF genotoxic effects can be found in Part 2, Supplement 2 and ELF in flora are also listed separately in Part 2, Supplement 4.
Effects, however, do not easily translate from the laboratory to the field. Cucurachi et al. [31] reported on 113 studies with a limited number of ecological studies. The majority were conducted in laboratory settings using bird embryos or eggs, small rodents, and plants. In 65% of the studies, effects from EMF (50% of the animal studies and about 75% of the plant studies) were found at both high and low intensities, indicating broad potential effects. But lack of standardization among the studies and limited sampling size made generalizing results from organism to ecosystem difficult. The researchers concluded that due to the number of variables, no clear dose–response relationship could be determined. Nevertheless, effects from some studies were well documented and can serve as predictors for effects to wild migratory birds and other wildlife.
As noted elsewhere throughout this paper, living organisms can sense and react to very low-intensity electromagnetic fields necessary for their survival as seen, for instance, in studies by Nicholls and Racey [206, 207] on bats and many others. Bats are already in serious trouble in North America from white-nosed syndrome and commercial wind turbine blade collisions. Due to the increased use of tracking radars for bird and bat studies, impacts will likely only increase [22, 23]. Presence of low levels of RFR from tracking radars could adversely affect bat foraging activity, which in turn could affect the composition of insect populations in the vicinity. Many insects, including honey bees (Apis mellifera var) and butterflies also depend on the Earth’s electromagnetic fields for orientation and foraging. Presence of exogenous RFR can disturb these functions. This is particularly relevant for pollinator insects, such as bees and butterflies. Pollinators are essential in producing commercial crops for human consumption, including almonds, apples, pears, cherries, numerous berry crops, citrus fruits, melons, tomatoes, sunflowers, soybeans, and much more. The strongest disruptive effect to insect pollinators occurs at 1.2 MHz known as the Larmor frequency [208] which is related to radical pair resonance and superoxide radical formation. This is an important indication that effects from RFR are frequency-dependent.
Lai [77], citing Shepherd et al. [209], noted that EMF can disrupt the directional sense in insects. The fact that many animals are able to differentiate the north and south poles of a magnetic field known as the polarity compass [68, 73, 134, 210, 211] indicates they are susceptible to having that important sense impaired. These polarity compass traits confer survival competitiveness to organisms but are of particular concern since directional cues can be easily disturbed by man-made EMF [69, 134, 212].
Bird migration also depends on proper sensing and orientation to natural electromagnetic fields. A study by Engels et al. [213] showed that magnetic noise at 2 kHz–9 MHz (within the range of AM radio transmission) could disrupt magnetic compass orientation in migratory European Robins (Erithacus rubecula). The disruption can occur at a vanishingly low level of 0.01 V/m, or 0.0000265 μW/cm2. Similar effects of RFR interference on magnetoreception have also been reported in a night-migratory songbird [214] and the European Robin [126]. Migration is already a taxing and dangerous activity for birds; adding another potential negative impact to bird survival is troubling.
Lai [77] also noted that another consideration is the “natal homing behavior” exhibited in some animals that return to their natal birth places to reproduce. These include sea turtles [89]; eels [90]; and salmon [91]. Newborns of these animals are imprinted with the memory of the intensity and the inclination angle of the local geomagnetic field, later used to locate their place of birth when they return to breed. There are indications that man-made EMF can distort this imprinting memory to locate the site (see “Fish” and “Turtles” below). This has important consequences to the survival of particular species since it interrupts their reproductive processes.
It is clear that biological effects can occur at levels of man-made RFR in our present environment, thereby conceivably altering delicate ecosystems from a largely unrecognized danger.
Mammals
The majority of EMF laboratory research, some going back to the 1800s, has been conducted on a variety of mammal species using mice, rats, rabbits, monkeys, pigs, dogs, and others. (The second and third most used models are on insects and yeast respectively.) Thus, with varying degrees of confidence, we know a significant amount about how energy couples with, and affects, laboratory mammalian species across a range of frequencies. However, this evidence does not automatically transfer at the same confidence level regarding how this vast body of research applies to wildlife, including mammalian species.
There is unfortunately a dearth of field research on EMF effects to wildlife. Referenced below, however, are many potential indicator studies. The effects seen include reproductive, behavioral, mating, growth, hormonal, cellular, and others.
Rodents
Rodents are the most frequently used mammalian species in laboratory research across a range of frequencies and intensities. While studies are inconsistent, there are enough troubling indications regarding potential EMF implications for wildlife.
In the RFR range, there have been several reviews of fertility and other issues in rodent models with citations too numerous to mention here — see La Vignera e al. [215] and Merhi [216] — but some stand out as potentially pertinent to wildlife.
Magras and Xenos [217] investigated effects of RFR on prenatal development in mice, using RFR measurements and in vivo experiments at several locations near an "antenna park," with measured RFR power densities between 0.168 and 1.053 μW/cm2. Divided into two groups were 12 pairs of mice, placed in locations of different power densities, and mated five times. One hundred eighteen newborns were collected, measured, weighed, and examined macro- and microscopically. With each generation, researchers found a progressive decrease in the number of newborns per dam ending in irreversible infertility. However, the crown-rump length, body weight, and number of lumbar, sacral, and coccygeal vertebrae, was improved in prenatal development of some newborns. RFR was below exposure standards and comparable to far-field exposures that mice could experience in the wild.
Aldad et al. [218], in a laboratory setting, investigated cell phone RFR (800–1,900 MHz, SAR of 1.6 W/kg) exposures in in-utero mouse models and effects on neurodevelopment and behavior. They found significant adult behavioral effects in prenatally exposed mice vs. controls. Mice exposed in-utero were hyperactive, had decreased memory and anxiety, and altered neuronal developmental programming. Exposed mice had dose-response impaired glutamatergic synaptic transmission onto layer V pyramidal neurons of the prefrontal cortex. This was the first evidence of neuropathology in mice from in-utero RFR at cell phone frequencies, now the most prevalent in the environment. Effects persisted into adulthood and were transmissible to next generations. Such changes can affect survival in wild populations.
Meral et al. [219] looked at effects in guinea pigs (Cavia parcels) from 900 MHz cell phone frequency exposures on brain tissue and blood malondialdehyde (MDA), glutathione (GSH), retinol (vitamin A), vitamin D(3) and tocopherol (vitamin E) levels, as well as catalase (CAT) enzyme activity. Fourteen male guinea pigs were randomly divided into control and RFR-exposed groups containing seven animals each. Animals were exposed to 890- to- 915 MHz RFR (217 Hz pulse rate, 2 W maximum peak power, SAR 0.95 W/kg) from a cellular phone for 12 h/day (11 h 45 min stand-by and 15 min spiking mode) for 30 days. Controls were housed in a separate room without cell phone radiation. Blood samples were collected through cardiac puncture; biochemical analysis of brain tissue was done after decapitation at the end of the 30-day period. Results found MDA levels increased (p<0.05), and GSH levels and CAT enzyme activity decreased, while vitamins A, E and D(3) levels did not change significantly in the brain tissue of exposed animals. In blood samples of the exposed group, MDA, vitamins A, D(3) and E levels, and CAT enzyme activity increased (p<0.05), while GSH levels decreased (p<0.05). They concluded that cell phone radiation could cause oxidative stress in brain tissue of guinea pigs but more studies were needed to determine if effects are harmful and/or affect neural functions.
Lai et al. [220] found that Sprague-Dawley rats exposed to RFR during water maze testing showed spatial working memory deficits compared to controls. But similar studies [221], [222], [223] did not find performance effects in spatial tasks or alterations in brain development after similar exposures. However, subsequent studies in the last two decades have shown memory and learning effects in animals and humans after RFR exposure [224].
Several studies also investigated RFR behavioral effects in rodent models on learning, memory, mood disturbances, and anxiety behaviors with contradictory results. Daniels et al. [225] found decreased locomotor activity, increased grooming and increased basal corticosterone levels in rats exposed to RFR for 3 h per day at 840 MHz, but no significant differences were seen between controls and test animals in spatial memory testing or morphological brain assessment. The researchers concluded that RFR exposure may lead to abnormal brain functioning.
Lee et al. [226, 227] looked specifically at effects on pregnant mice and rat testicular function from combined RFR mobile network signal characteristics used in wideband code division multiple access (W-CDMA) or CDMA used in 3G mobile communications. Experiments showed no observable adverse effects on development, reproduction, or mutation in tested subjects. And no significant effects were seen by Poulletier de Gannes et al. [228] in in-utero and post-natal development of rats with wireless fidelity (WiFi) at 2,450 MHz. Also, Imai et al. [229] found no testicular toxicity from 1.95 GHz W-CDMA.
One extremely high frequency (EHF) study comparable to 5G on a mouse model by Kolomytseva et al. [230] looked at leukocyte numbers and the functional activity of peripheral blood neutrophils. In healthy mice, under whole-body exposures to low-intensity extremely-high-frequency electromagnetic radiation (EHF, 42.0 GHz, 0.15 mW/cm2, 20 min daily) found that the phagocytic activity of peripheral blood neutrophils was suppressed by about 50% (p<0.01 as compared with the sham-exposed control) in 2–3 h after the single exposure. Effects persisted for 1 day and thereafter returned to normal within 3 days. But a significant modification of the leukocyte blood profile was observed in mice exposed to EHF for 5 days after exposure cessation. Leukocytes increased by 44% (p<0.05 as compared with sham-exposed animals). They concluded that EHF effects can be mediated via metabolic systems and further said results indicated whole-body low-intenstiy EHF exposure of healthy mice had a profound effect on the indices of nonspecific immunity. These low levels will be common near 5G infrastructure.
In well-designed non-rodent mammal field studies, Nicholls and Racey [206, 207], found that foraging bats showed aversive behavioral responses near large air traffic control and weather radars. Four civil air traffic control (ATC) radar stations, three military ATC radars and three weather radars were selected, each surrounded by heterogeneous habitat. Three sampling points were carefully selected for matched habitats, type, structure, altitude and surrounding land class at increasing distances from each station. Radar field strengths were taken at three distances from the source: close proximity (<656 ft/200 m) with a high EMF strength >2 V/m (1.06 μW/cm2), an intermediate line-of sight point (656–1,312 ft/200–400 m) with EMF strength <2 V/m, and a control location out of radar sight (>1,312 ft/400 m) registering 0 V/m. Bat activity was recorded three times for a total of 90 samples, 30 within each field strength category. Measured from sunset to sunrise, they found that bat activity was significantly reduced in habitats exposed to an EMF greater than 2 V/m compared to 0 EMF sites, but such reduced activity was not significantly different at lower EMF levels within 400 m of the radar. They concluded that the reduced bat activity was likely due to thermal induction and an increased risk of hyperthermia. This was a large field study near commercial radar installations with mostly high intensity exposures but low-level effects cannot be excluded given known magneto-sensitivity in bats.
In another field study using a small portable marine radar unit significantly less powerful than their earlier measured field study, Nicholls and Racey [207] found the smaller signal could also deter bats’ foraging behaviors. First, in summer 2007, bat activity was compared at 20 foraging sites in northeast Scotland during experimental trials with radar switched on, and in controls with no radar signal. After sunset, bat activity was recorded for a period of 30 min with the order of the trials alternating between nights. Then in summer 2008, aerial insects were sampled at 16 of the sites using two small light-suction traps, one with a radar signal, the other a control. Bat activity and foraging were found significantly reduced when the radar signal was unidirectional, creating a maximized exposure of 17.67–26.24 V/m (83–183 μW/cm2). The radar had no significant effect on the abundance of insects captured by the traps despite reduced bat activity.
Balmori [231] also noted significantly reduced bat activity in a free-tailed bat colony (Tadarida teniotis) where the number of bats decreased when several cell towers were placed 262 ft (80 m) from the colony.
In the ELF range, Janać et al. [232] investigated ELF/MF effects — comparable to powerline and stray voltage ground current — on motor behavior patterns in Mongolian gerbils (Meriones unguiculatus) and found age-dependent changes in locomotion, stereotypy, and immobility in 3- and 10-month-old males. Animals were continuously exposed to ELF-MF (50 Hz; 0.1, 0.25 and 0.5 mT) for seven days with behavior monitored for 60 min in the open field after the 1st, 2nd, 4th, and 7th day (to capture immediate effects), as well as three days after exposure (to capture delayed effects). They found that exposure to 3-month-old gerbils increased motor behavior (locomotion and stereotypy), and therefore decreased immobility. In the 3-month old gerbils, ELF/MF also showed a delayed effect (except at 0.25 mT) on stereotypy and immobility. In 10-month-old gerbils, ELF/MF of 0.1, 0.25 and 0.5 mT induced decreased locomotion, a slight increase in stereotypy, and pronounced stimulation of motor behavior. Increased motor behavior was observed three days after exposure, indicating long lasting effects. Researchers concluded that in 3- and 10-month-old gerbils, specific temporal patterns of motor behavior changes were induced by ELF/MF due to age-dependent morpho-functional differences in brain areas that control motor behavior.
The above is a very small sample of rodent studies. See Part 2 Supplements 1 and 2 for more genetic effects to rodents, and Supplement 3 for additional studies.
Bovines
Due to domestication and easy accessibility, there are numerous studies of dairy cows (Bos taurus) which appear particularly sensitive to both natural and man-made EMFs. Fedrowitz [71] published a thorough review with citations too numerous to mention here. Noted in the review is the fact that bovines, although easily accessible, are difficult to study with precision due to their size, which creates handling and dosimetric complexities. Also noted are that bovines today are at their milk- and beef-production physiological limits, and that the addition of even a weak stressor may be capable of altering a fragile bovine physiological balance. It is clear in the Fedrowitz review that cows respond to environmental exposures from a broad range of frequencies and properties, even as some studies lack good exposure assessment. RFR exposure created avoidance behavior, reduced ruminating and lying times, and alterations in oxidative stress enzymes among other problems, while ELF-EMF found contradictory evidence affecting milk production, fat content, hormone imbalances and important changes in other physiological parameters. Cows have also been found sensitive to stray voltage and transient harmonics with problematic milk production, health, reproduction and behavioral effects.
The question is how much of this body of work could translate to other ruminants and large mammals on-field or in the wild such as deer/cervids — behaviorally, reproductively, and physiologically. Stray voltage and ELF-EMF near powerlines, and rural area RFR from both ground-based and satellite transmitters, for instance, may affect wild migratory herds and large ungulates in remote areas that go undetected.
Bovines and RFR
Loscher and Kas [233] observed abnormal behavior in a dairy herd kept in close proximity to a TV and radio transmitter. They found reduction in milk yield, health problems, and behavioral abnormalities. After evaluating other factors, they concluded the high levels of RFR were possibly responsible. They removed one cow with abnormal behavior to another stable 20 km away from the antenna, resulting in normalization of behavior within five days. Symptoms reappeared when the cow was returned to the stable near the antennas. In a later survey, Loscher [234] also found effects of RFR on the production, health and behavior of farm animals, including avoidance behavior, alterations in oxidative stress parameters, and ruminating duration.
Balode [59] obtained blood samples from female brown cows from a farm close to, and in front of, the Skrunda Radar – located in Latvia at an early warning radar system operating in the 156–162 MHz frequency range — and samples from cows in a control area. They found micronuclei in peripheral erythrocytes were significantly higher in the exposed cows, indicating DNA damage.
Stärk et al. [235] investigated short-wave (3–30 MHz) RFR on salivary melatonin levels in dairy cattle, with one herd at a farm located at 1,640 ft/500 m (considered higher exposure) and a second control herd located 13,123 ft/4,000 m from the transmitter (considered unexposed). The average nightly magnetic field strength readings were 21-fold greater on the exposed farm (1.59 mA/m) than on the control farm (0.076 mA/m). At both farms, after initially monitoring five cows’ salivary melatonin concentrations at 2-h intervals during night dark phase for 10 consecutive days, and with the short-wave transmitter switched off during three of the 10 days (off phase), samples were analyzed using a radioimmunoassay. They reported that mean values of the two initial nights did not show a statistically significant difference between exposed and unexposed cows and concluded that chronic melatonin reduction was unlikely. But on the first night of re-exposure after the transmitter had been off for three days, the difference in salivary melatonin concentration between the two farms (3.89 pg/ml, CI: 2.04, 7.41) was statistically significant, indicating a two-to-seven-fold increase of melatonin concentration. They concluded that a delayed acute effect of EMF on melatonin concentration could not be excluded and called for further trials to confirm results.
Hässig et al. [95] conducted a cohort study to evaluate the prevalence of nuclear cataracts in veal calves near mobile phone base stations with follow-up of each dam and its calf from conception through fetal development and up to slaughter. Particular emphasis was focused on the first trimester of gestation (organogenesis). Selected protective antioxidants (superoxide dismutase, catalase, glutathione peroxidase [GPx]) were assessed in the aqueous humor of the eye to evaluate redox status. They found that of 253 calves, 79 (32%) had various degrees of nuclear cataracts, but only 9 (3.6%) of calves had severe nuclear cataracts. They concluded that a relationship between the location of veal calves with nuclear cataracts in the first trimester of gestation and the strength of antennas was demonstrated. The number of antennas within 328–653 ft (100–199 m) was associated with oxidative stress and there was an association between oxidative stress and the distance to the nearest base station. Oxidative stress was increased in eyes with cataract (OR per kilometer: 0.80, confidence interval 95 % 0.62, 0.93). But the researchers further concluded that it had not been shown that the antennas actually affected stress. Hosmer-Lemeshow statistics showed an accuracy of 100% in negative cases with low radiation, and only 11.11% accuracy in positive cases with high radiation. This reflected, in their opinion, that there are a lot of other likely causes for nuclear cataracts beside base stations and called for additional studies on EMF during embryonic development.
Hässig et al. [96] further examined a dairy farm in Switzerland where a large number of calves were born with nuclear cataracts after a mobile phone base station was erected near the barn. Calves showed a 3.5 times higher risk for heavy cataracts if born there compared to the Swiss average. All usual causes for cataracts could be excluded but they nevertheless concluded that the incidence remained unknown.
Bovines and swine: ELF-EMF, stray electric current
Bovines appear unusually sensitive to ELF-EMF from stray current caused by both normal industrial and faulty grounding methods near high tension transmission lines close to dairy farms. Stray current can cover large areas and occurs when current flows between the grounded circuit conductor (neutral) of a farm and the Earth through dairy housing equipment like metal grates. It typically involves small, steady power frequency currents [99], not high transient shocks, although that also can sometimes occur under wet weather conditions. According to Hultgren [236], dairy cattle can perceive alternating currents exceeding 1 mA between the mouth and all four hooves with behavioral effects in cows usually occurring above 3 mA. Stray current can act as a major physical stressor in cows and other animals [237]. This may also be happening in wild migratory species moving through such areas.
At the request of dairymen, veterinarians, and county extension agents in Michigan, U.S., Kirk et al. [238] investigated stray current on 59 Michigan dairy farms. On 32 farms, stray current sources were detected. Where voltage exceeded 1 V alternating current, increased numbers of dairy cows showed abnormal behavior in the milking facility and increased prevalence of clinical mastitis. Recovery from the stray current-induced abnormalities was related to the type of abnormality and the magnitude of the exposure voltage.
Burchard et al. [239] in a small but well-controlled alternating exposure study of non-pregnant lactating Holstein cows found a longer estrous cycle in cows exposed to a vertical electric field of 10 kV/m and a uniform horizontal magnetic field of 30 μT at 60 Hz, compared to when they were not exposed. Rodriguez et al. [240] also found that exposure to EMF may increase the duration of the bovine estrous cycle. Burchard et al. [241] evaluated effects on milk production in Holsteins exposed to a vertical electric field of 10 kV/m and a uniform horizontal MF of 30 μT at 60 Hz and found an average decrease of 4.97, 13.78, and 16.39% in milk yield, fat corrected milk yield, and milk fat, respectively in exposed groups, and an increase of 4.75% in dry matter food intake. And Buchard et al. [242] in two experiments investigated blood thyroxine (T4) levels in lactating pregnant and non-lactating non-pregnant Holstein cows exposed to 10 kV/m, 30 µT EMF and found a significant change depending on the time of blood sampling in exposed groups. They concluded that exposure of dairy cattle to ELF-EMF could moderately affect the blood levels of thyroxine.
Hillman et al. [93, 94] reported that harmonic distortion and power quality itself could be another variable in bovine sensitivity to stray current. They found behavior, health, and milk production were adversely affected by transients at the 3rd, 5th, 7th, and triplen harmonic currents on utility power lines after a cell tower was found charging the ground neutral with 10+ V, causing the distortion. After installing a shielded neutral isolation transformer between the utility and the dairy, the distortion was reduced to near zero. Animal behavior improved immediately and milk production, which had been suppressed for three years, gradually returned to normal within 18 months.
Swine (Sus scrofa domesticus) — like rats and mice — have demonstrated aversive behavior to ELF-EMF electric fields. Hjeresen et al. [243] found miniature pigs, exposed to 60‐Hz electric fields (30 kV/m for 20 h/day, 7 days/week up to 6 months) preferred an absence of the field during a 23.5‐h period by spending more time out of the electric field than in it during sleep periods. And Sikov et al. [244], as part of a broad study of Hanford Miniature swine on reproductive and developmental toxicology (including teratology) over three breeding cycles found a strong association between chronic exposure to a vertical uniform electric field (60‐Hz, 30‐kV/m, for 20 h/day, 7 days/week) and adverse developmental effects vs. control. They concluded that an association exists between chronic exposure to strong electric fields and adverse developmental effects in swine (75% malformations in exposed vs. 29% sham) in first generation with consistent results in two subsequent generations.
Avian
Birds are important indicators of ecosystem well-being and overall condition. Even subtle effects can be apparent due to their frequent presence in RFR areas. Their hollow feathers have dielectric and piezoelectric properties, meaning they are conductive and capable of acting as a waveguide directing external RFR energy directly and deeply into avian body cavities [245], [246], [247], [248], [249]. Their thin skulls have both magnetite and radical pair receptors (see “Mechanisms” above) and they are highly mobile — often traveling across great migratory distances of tens to as much as a hundred thousand kilometers round-trip per year, resulting in potential multi-frequency cumulative effects from chronic near, middle, and far-field exposures. Avian populations are declining worldwide, especially among migratory species. This means that birds may be uniquely sensitive to adverse effects from environmental RFR since their natural habitat is air and they often fly at lateral levels with infrastructure emissions, bringing them that much closer to generating sources.
Tower and building construction, as direct obstacles, are known hazards to birds. One tower at 150 feet (46 m) above ground level is thought to account for as many as 3,000 songbird deaths per month in migratory pathways during peak migration [250] and communication tower collisions have been documented to kill more than 10,000 migratory birds in one night at a TV tower in Wisconsin [251, 252]. It has been known for years that the songbird populations of North America and Europe are plummeting. Only recently were towers considered a significant factor. But is the problem solely due to obstacles in direct migratory pathways or is something else involved?
RFR from towers may be acting as an attractant to birds due to their singular physiology. Avian eyes and beaks are uniquely magnetoreceptive with both magnetite and cryptchrome radical pair receptors. One definitive study by Beason and Semm [253] demonstrated that the common cell phone frequency (900-MHz carrier frequency, modulated at 217 Hz) at nonthermal intensities, produced firing in several types of nervous system neurons in Zebra Finches (Taeniopygia guttate). Brain neurons of irradiated anesthetized birds showed changes in neural activity in 76% of responding cells, which increased their firing rates by an average 3.5-fold vs. controls. Other responding cells exhibited a decrease in rates of spontaneous activity. The Beason and Semm study [253] could explain why birds may be attracted to cell towers, a theoretical premise they previously observed with Bobolinks (Dolichonyx oryzivorus; [254]).
RFR may also act as an avian stressor/irritant. Early work by Wasserman et al. [255] in field studies on 12 flocks of migratory birds subjected to various combinations of microwave power density and duration under winter conditions at Monomet, MA, using birds from two additional flocks as controls, showed increased levels of aggression in some of the irradiated birds.
Other research indicated a range of effects capable of broad adverse environmental outcomes. Laboratory studies by Di Carlo et al. [256] found decreases in heat shock protein production in chick embryos. The researchers used 915-MHz RFR on domestic chicken embryos and found that exposure typical of some cell phone emissions reduced heat shock proteins (HSP-70) and caused heart attacks and death in some embryos. Controls were unaffected. In replicated experiments, similar results were found by Grigor’ev [257] and Xenos and Magras [258]. Batellier et al. [259] found significantly elevated embryo mortality in exposed vs. sham groups of eggs incubated with a nearby cell phone repeatedly calling a 10-digit number at 3-min intervals over the entire incubation period. Heat shock proteins help maintain the conformation of cellular proteins during periods of stress. A decrease in their production diminishes cellular protection, possibly leading to cancer, other diseases, heart failure, and reduction in protection against hypoxia and ultraviolet light.
Not all results are adverse. Tysbulin et al. [260, 261] investigated both short and prolonged GSM 900 MHz cell phone signal exposure on embryo development in Quail (Coturnix coturnix japonica), irradiating fresh fertilized eggs during the first 38 h and 14 days of incubation using a cell phone in connecting mode continuously activated through a computer system. Maximum intensity of incident radiation on the egg’s surface was 0.2 mW/cm2. Results found a significant (p<0.001) increase in differentiated somites in 38-h exposed embryos and a significant (p<0.05) increase in total survival of embryos in eggs after 14 days exposure. They also found the level of thiobarbituric acid (TBA) reactive substances was significantly (p 0.05–0.001) higher in the brains and livers of hatchlings from exposed embryos and hypothesized that a facilitating effect exists due to enhanced metabolism in exposed embryos via peroxidation mechanisms. They concluded low-level nonthermal effects from GSM 900 MHz to quail embryogenesis is possible and that effects can be explained via a hormesis effect induced by reactive oxygen species (ROS).
Signaling characteristics such as pulsing vs. continuous wave are also important. Berman et al. [262], in a multi-lab study of pulsed ELF magnetic fields found a highly significant incidence of abnormalities in exposed chick eggs vs. controls. And Ubeda et al. [263] found irreversible damage to chick embryos from weak pulsed ELF-EMF magnetic fields that are common in the environment today. Initial studies on freshly fertilized chicken eggs were exposed during the first 48 h of post-laying incubation to pulsed magnetic fields (PMFs) with 100 Hz repetition rate, 1.0 μT peak-to-peak amplitude, and 500 μs pulse duration. Two different pulse waveforms were used, with rise and fall times of 85 μs or 2.1 μs. A two-day exposure found significant increased developmental abnormalities. In follow-up research, after exposure, eggs were incubated for an additional nine days without PMFs. Embryos removed from eggs showed an excess of developmental anomalies in the PMF-exposed groups compared with the sham-exposed samples. There was a high rate of embryonic death in the 2.1 μs rise/fall time. Results indicate PMFs can cause irreversible developmental changes, confirming that a pulse waveform can determine embryonic response to ELF magnetic fields common today.
Between 1999 and 2005, Fernie et al. for the first time investigated various potential reproductive effects on a captive raptor species — the American Kestrel (Falco sparverius) — from ELF-EMF equivalent to that of wild nesting pairs on power transmission lines. In a series of studies, captive pairs were typically bred under control or EMF exposure over 1–3 breeding cycles. In 1999, Fernie et al. [264] investigated photo phasic plasma melatonin in reproducing adult and fledgling kestrels, finding that EMFs affected plasma melatonin in adult male kestrels, suppressing it midway through, but elevating it at the end of the breeding season. In long-term, but not short-term EMF exposure of adults, plasma melatonin was supressed in their fledglings too which could affect migratory success. Molt happened earlier in adult EMF-exposed males than in controls. EMF exposure had no effect on plasma melatonin in adult females. In avian species, melatonin is involved in body temperature regulation, seasonal metabolism, locomotor activity, feeding patterns, migration, and plumage color changes important for mate selection. Melatonin also plays a key role in the growth and development of young birds. The researchers concluded it is likely that the results are relevant to wild raptors nesting within EMF exposures.
In 2000 Fernie et al. [265] focused on reproductive success in captive American Kestrels exposed to ELF-EMF, again equivalent to that experienced by wild reproducing kestrels. Kestrels were bred one season per year for two years under EMF or controlled conditions. In some years but not others, EMF-exposed birds showed a weak association with reduced egg laying, higher fertility, larger eggs with more yolk, albumen, and water, but thinner egg shells than control eggs. Hatching success was lower in EMF pairs than control pairs but fledging success was higher than control pairs in one year. They concluded that EMF exposure such as what kestrels would experience in the wild was biologically active in a number of ways leading to reduced hatching success.
Also in 2000, Fernie et al. [266] further investigated behavioral changes in American Kestrels to ELF-EMF, again in captive birds comparable to nesting pairs that commonly use electrical transmission structures for nesting, perching, hunting, and roosting. The amount of EMF exposure time of wild reproducing American Kestrels was first determined at between 25 and 75% of the observed time. On a 24-h basis, estimated EMF exposure in wild species ranged from 71% during courtship, to 90% during incubation. Then effects of EMFs on the behavior of captive reproducing kestrels were examined at comparable exposures of 88% of a 24-h period. Additionally, captive kestrels were exposed to EMF levels experienced by wild kestrels nesting under 735-kV power lines. There appeared to be a stimulatory/stress effect. Captive EMF females were more active, more alert, and perched on the pen roof more frequently than control females during courtship. EMF females preened and rested less often during brood rearing. EMF-exposed male kestrels were more active than control males during courtship and more alert during incubation. The researchers concluded that the increased activity of kestrels during courtship may be linked to changes in corticosterone, but not to melatonin as found in earlier work [264], but said the behavioral changes observed were unlikely to result in previously reported effects in EMF-exposed birds as noted above. They added that behavioral changes of captive EMF-exposed kestrels may also be observed in wild kestrels, with uncertain results.
In 2001 Fernie and Bird [267] looked at ELF-EMF oxidative stress levels in captive American Kestrels using the same test parameters described above to see if ELF-EMF exposure elicited an immune system response. In captive male kestrels bred under control or EMF conditions equivalent to those experienced by wild kestrels, short-term EMF exposure (one breeding season) suppressed plasma total proteins, hematocrits, and carotenoids in the first half of the breeding season. It also suppressed erythrocyte cells and lymphocyte proportions, but elevated granulosa proportions at the end of the breeding season. Long-term EMF exposure (two breeding seasons) also suppressed hematocrits in the first half of the reproductive period. But results found that only short-term EMF-exposed birds experienced an immune response, particularly during the early half of the breeding season. The elevation of granulocytes and the suppression of carotenoids, total proteins, and melatonin [264] in the same kestrel species indicated that the short-term EMF-exposed male kestrels had higher levels of oxidative stress due to an immune response and/or EMF exposure. The researchers noted that long-term EMF exposure may be linked to higher levels of oxidative stress solely through EMF exposure. Oxidative stress contributes to cancer, neurodegenerative diseases, and immune disorders. And in 2005, Fernie and Reynolds [268] noted most studies of birds and EMF indicate changes on behavior, reproductive success, growth and development, physiology and endocrinology, and oxidative stress — with effects not always consistent or in the same direction under EMF conditions. The entire body of work by this research group has implications for all wild species that encounter a wide range of EMFs on a regular basis.
In field studies on wild birds in Spain, Balmori [269] found strong negative correlations between low levels of microwave radiation and bird breeding, nesting, roosting and survival in the vicinity of communication towers. He documented nest and site abandonment, plumage deterioration, locomotion problems, and death in Wood Storks (Mycteria americana), House Sparrows (Passer domesticus), Rock Doves (Columba livia), Magpies (Pica pica), Collared Doves (Streptopelia decaocto), and other species. While these species had historically been documented to roost and nest in these areas, Balmori [269] did not observe these symptoms prior to construction and operation of the cell phone towers. Results were most strongly negatively correlated with proximity to antennas and Stork nesting and survival. Twelve nests (40% of his study sample) were located within 656 ft (200 m) of the antennas and never successfully raised any chicks, while only one nest (3.3%), located further than 984 ft (300 m) never had chicks. Strange behaviors were observed at Stork nesting sites within 328 ft (100 m) of one or several cell tower antennas. Birds impacted directly by the main transmission lobe (i.e., electric field intensity > 2 V/m) included young that died from unknown causes. Within 100 m, paired adults frequently fought over nest construction sticks and failed to advance nest construction (sticks fell to the ground). Balmori further reported that some nests were never completed and that Storks remained passively in front of cell site antennas. The electric field intensity was higher on nests within 200 m (2.36 ± 0.82 V/m; 1.48 μW/cm2) than on nests further than 300 m (0.53 ± 0.82 V/m, 0.074 μW/cm2). RF-EMF levels, including for nests <100 m from the antennas, were not intense enough to be classified as thermal exposures. Power densities need to be at least 10 mW/cm2 to produce tissue heating of even 0.5 °C [270]. Balmori’s results indicated that RFR could potentially affect one or more reproductive stages, including nest construction, number of eggs produced, embryonic development, hatching and mortality of chicks and young in first-growth stages.
Balmori and Hallberg [271] and Everaert and Bauwens [272] found similar strong negative correlations among male House Sparrows (Passer domestics) throughout multiple sites in Spain and Belgium associated with ambient RFR between 1 MHz and 3 GHz at various proximities to GSM cell base stations. House Sparrow declines in Europe have been gradual but cumulative for this species once historically well adapted to urban environments. The sharpest bird density declines were in male House Sparrows in relatively high electric fields near base stations, indicating that long-term exposure at higher RFR levels negatively affected both abundance and/or behavior of wild House Sparrows. In another review, Balmori [25] reported health effects to birds that were continuously irradiated. They suffered long-term effects that included reduced territorial defense posturing, deterioration of bird health, problems with reproduction, and reduction of useful territories due to habitat deterioration.
Birds have been observed avoiding areas with high and low-intensity EMF, in daylight as well as nocturnally. An early study by Southern in 1975 [273] observed that gull chicks reacted to the U.S. military’s Project Sanguin ELF transmitter. Tested on clear days in the normal geomagnetic field, birds showed significant clustering with predicted bearing corresponding with migration direction, but when the large antenna was energized they dispersed randomly. He concluded that magnetic fields associated with such conductors were sufficient to disorient birds. Larkin and Sutherland [274] observed that radar tracking of individual nocturnal migrating birds flying over a large alternating-current antenna system caused birds to turn or change altitude more frequently when the antenna system was operating than when it was not. The results suggested that birds sense low-intensity alternating-current EMF during nocturnal migratory flight.
In a well-designed, multi-year avian study of magneto-disruption, Engels et al. [213] investigated environmental broadband electromagnetic ‘noise’ emitted everywhere humans use electronics, including devices and infrastructure. They found migratory birds were unable to use their magnetic compass in the presence of a typical urban environment today. European Robins (E. rubecula), exposed to the background electromagnetic ‘noise’ present in unscreened wooden huts at the University of Oldenburg campus, could not orient using their magnetic compass. But when placed in electrically grounded aluminum-screened huts, creating Faraday cages that attenuated electromagnetic ‘noise’ by approximately two orders of magnitude, their magnetic orientation returned. The researchers were able to determine the frequency range from 50 kHz to 5 MHz was the most disruptive. When grounding was removed, or additional broadband electromagnetic ‘noise’ was deliberately generated inside the screened and grounded huts, birds again lost magnetic orientation abilities. They concluded that RFR’s magneto-disruption effects are not confined to a narrow frequency band. Birds tested far from sources of EMFs required no screening to orient with their magnetic compass. This work documented a reproducible effect of anthropogenic electromagnetic ambient ‘noise’ on the behavior of an intact vertebrate. The magnetic compass is integral to bird movement and migration. The findings clearly demonstrated a nonthermal effect on European Robins and serves as a predictor for effects to other migratory birds, especially those flying over urban areas. Such fields are much weaker than minimum levels expected to produce any effects and far below any exposure standards.
Intensity windows in different species have also been found where effects can be more extreme at lower intensities than at higher ones due to compensatory mechanisms such as cell apotosis. Panagopoulos and Margaritas [34] found an unexpected intensity window at thermal levels around 10 mW/cm2 RFR — not uncommon near cell towers — where effects were more severe than at intensities higher than 200 mW/cm2. This window appeared at a distance of 8–12 in (20–30 cm) from a cell phone antenna, corresponding to a distance of about 66–98 ft (20–30 m) from a base station antenna. This could be considered a classic nonlinear effect and would apply to far-field exposures. Since cell base station antennas are frequently located within residential areas where birds nest, often at distances 20–30 m from such antennas, migratory birds, non-migratory avifauna, and other wildlife may be exposed up to 24-h per day.
Concerns also apply to impacts from commercial radio signals on migratory birds. The human anatomy is resonant with the FM bands so exposure standards are most stringent in that range. High intensity (>6,000 W) commercial FM transmitters are typically located on the highest ground available to blanket a wider area. Low powered FM transmitters (<1,000 W) can be placed closer to the human population. High intensity locations, which can be multi-transmitter sites (colloquially called “antenna farms”) for other services, also provide convenient perches and nest sites for migratory birds. FM digital signals, which simulate pulsed waves, pose additional health concerns to migratory birds. This creates a dangerous frequency potential for protected migratory birds such as Bald Eagles with wingspans that extend to about 6 ft (1.83 m) — a resonant match with the length of the FM signal — creating a potential full-body resonant effect for both humans and Bald Eagles. Birds could experience both thermal and non-thermal effects.
All migratory birds are potentially at risk, including Bald Eagles, Golden Eagles, birds of conservation concern [275], federal and/or state-listed bird species, birds nationally or regionally in peril, as well as birds whose populations are stable. Sadly, addressing these concerns — beginning with independent research conducted by scientists with no vested interest in the outcomes — has not been a priority for government agencies or the communications industry.
Insects and arachnids
Insects are the most abundant and diverse of all animal groups, with more than one million described species representing more than half of all known living species, and potentially millions more yet to be discovered and identified. They may represent as much as 90% of all life forms on Earth. Though some are considered pests to farm crops and others as disease vectors, insects remain essential to life and planetary health. Found in nearly all environments, they are the only invertebrates that fly, but adults of most insect species walk, while some swim. Because of these different environmental adaptations, different species will encounter different EMF exposures in varying degrees. For instance, ground-based walking insects may be more susceptible to effects from 60 Hz stray current while flying insects may be more susceptible to wireless exposures. However, all species tested have been affected across a range of the nonionizing electromagnetic bands.
Most insects have an exoskeleton, three-part body consisting of a head, thorax, and abdomen, three pairs of jointed legs, compound eye structures capable to seeing many more colors, widths, and images than humans, and one pair of antennae capable of sensing subtle meteorological changes and Earth’s geomagnetic fields. They live in close harmony with the natural environment for survival and mating purposes. The most diverse insect groups co-evolved with flowering plants, many of which would not survive without them. Most insect species are highly sensitive to temperature variations and climate alterations as they do not dissipate heat efficiently.
Nearly all insects hatch from eggs that are laid in myriad ways and habitats. Growth involves a series of molts and stages (called instars) with immature stages greatly differing from mature insects in appearance, behavior, and preferred habitat. Some undergo a four-stage metamorphosis (with a pupal stage) and others a three-stage metamorphosis through a series of nyphal stages.
While most insects are solitary, some — like bees, termites and ants — evolved into social networks, living in “cooperative” organized colonies that can function as one unit as evidenced in swarming behaviors. Some even show maternal care over eggs and young. They communicate through various sounds, pheromones, light signals, and through their antennae such as during the bees’ “waggle dance” (see below).
As far back as the 1800s, even though testing methods were primitive by today’s standards, researchers were curious about electromagnetism’s effect on insect development, particularly teratogenicity [276]. Research on EMF across frequencies and insect populations has been ongoing since at least the 1930s with an eye toward using energy as an insecticide and anti-contaminant in grain, typically at high intensity thermal exposures that would not exist in the natural environment. Mckinley and Charles [277] found that wasps die within seconds of high frequency exposure. But not all early work was strictly high intensity, or all effects observed due to thermal factors.
There were interesting theories introduced by early researchers regarding how energy couples with various insect species. Frings [278] found larval stages are more tolerant to heat than adult insects with appendages that can act as conducting pathways to the body, and that the more specialized the insect species, the more susceptible they appear to microwave exposure. Carpenter and Livingstone [279] studied effects of 10 GHz continuous-wave microwaves at 80 mW/cm2 for 20 or 30 min, or at 20 mW/cm2 for 120 min on pupae of mealworm beetles (Tenebrio molitor) — clearly within thermal ranges. In control groups, 90% metamorphosed into normal adult beetles whereas only 24% of exposed groups developed normally, 25% died, and 51% developed abnormally. Effects were assumed to be thermally induced abnormalities until they simulated the same temperature exposure using radiant heat and found 80% of pupae developed normally. They concluded that microwaves were capable of inducing abnormal effects other than through thermal damage.
Fruit flies
Insects at all metamorphic stages of development have been studied using RFR including egg, larva, pupa and adult stages. Much work has been done on genetic and other effects with fruit flies (D. melanogaster) because of their well-described genetic system, ease of exposure, large brood size, minimal laboratory space needed, and fast reproductive rates. Over several decades Goodman and Blank, using ELF-EMF on Drosophila models, found effects to heat shock proteins and several other effects ([201]; and see “Mechanisms” above). It is considered a model comparable to other insects in the wild approximating that size. D. melanogaster may be the most lab-studied insect on Earth, although honey and related bee species, due to their devastating losses over the last decade and significance to agriculture, are quickly catching up.
Michaelson and Lin [50] noted that RFR-exposed insects first react by attempting to escape, followed by disturbance of motor coordination, stiffening, immobility and eventually death, depending on duration of exposure and insect type. For example, D. melanogaster survived longer than 30 min while certain tropical insects live only a few seconds at the same field intensity. Also noted were concentration changes in many metabolic products and effects to embryogenesis — the period needed for a butterfly to complete metamorphosis — with accelerated gastrulation and larval growth [17]. Michaelson and Lin [50] cited several negative studies with D. melanogaster exposed with continuous-wave RFR between 25 and 2,450 MHz on larval growth [280, 281] and mutagenicity [282]. This was after Heller and Mickey [283] found a tenfold rise in sex-linked recessive mutations with pulsed RFR between 30 and 60 MHz. It was among the earliest studies that found pulsing alone to be a biologically active exposure.
As reported in Michaelson and Lin [50], Tell [284] looked at D. melanogaster’s physiological absorption properties and found that a group of 6-day old male wild-type flies, exposed to 2,450 MHz for 55 min at an intense field caused a dramatic 65% reduction in body weight. This was thought to be from dehydration. They then sought to calculate the fruit fly’s absorption properties in relation to plane electromagnetic waves and found that a fly has only a 1/1,000th effective area of its geometric cross section and thus is an inefficient test species for absorbed microwave radiation. However, they concluded that fruit flies were responsive to absorbed energy at thermal levels as a black body resonator at a power density of 1.044 × 104 mW/cm2, corresponding to a thermal flux density of 0.562 × 10−3 cal. These are levels found in close proximity to broadcast facilities and cell phone towers today.
More recent investigations of RFR by Weisbrot et al. [285] using GSM multiband mobile phones (900/1,900 MHz; SAR approximately 1.4 W/kg) on D. melanogaster during the 10-day developmental period from egg laying through pupation found that non-thermal radiation increased numbers of offspring, elevated heat shock protein-70 levels, increased serum response element (SRE) DNA-binding and induced the phosphorylation of the nuclear transcription factor, ELK-1. Within minutes, there was a rapid increase of hsp70, which was apparently not a thermal effect. Taken together with the identified components of signal transduction pathways, the researchers concluded the study provided sensitive and reliable biomarkers for realistic RFR safety guidelines.
Panagopoulos et al. [286] found severe effects in early and mid-stage oogenesis in D. melanogaster when flies were exposed in vivo to either GSM 900-MHz or DCS 1,800-MHz radiation from a common digital cell phone, at non-thermal levels, for a few minutes per day during the first 6 days of adult life. Results suggested that the decrease in oviposition previously reported [287], [288], [289] was due to degeneration of large numbers of egg chambers after DNA fragmentation of their constituent cells which was induced by both types of mobile phone radiation. Induced cell death was recorded for the first time in all types of cells constituting an egg chamber (follicle cells, nurse cells and the oocyte) and in all stages of early and mid-oogenesis, from germarium to stage 10, during which programmed cell death does not physiologically occur. Germarium and stages 7–8 were found to also be the most sensitive developmental stages in response to electromagnetic stress induced by the GSM and DCS fields. Germarium was also found to be more sensitive than stages 7–8. These papers, taken collectively, indicate serious potential effects to all insect species of similar size to fruit flies from cell phone technology, including from infrastructure and transmitting devices.
Fruit flies have also been found sensitive to ELF-EMF. Gonet et al. [290] found 50 Hz ELF-EMF exposure affected all developmental stages of oviposition and development of D. melanogaster females, and weakened oviposition in subsequent generations.
Savić et al. [291] found static magnetic fields influenced both development and viability in two species of Drosophila (D. melanogaster and D. hydei). Both species completed development (egg-to-adult), in and out of the static magnetic field induced by a double horseshoe magnet. Treated vials with eggs were placed in the gap between magnetic poles (47 mm) and exposed to the average magnetic induction of 60 mT, while control groups were kept far from the magnetic field source. They found that exposure to the static magnetic field reduced development time in both species, but only results for D. hydei were statistically significant. In addition, the average viability of both species was significantly weaker compared to controls. They concluded a 60 mT static magnetic field could be a potential stressor, influencing on different levels both embryonic and post-embryonic fruit fly development.
Beetles
Other insect species also react to both ELF-EMF and RF-EMF. Newland et al. [292] found behavioral avoidance in cockroaches (Periplaneta americana) to static electric fields pervasive in the environment from both natural and man-made sources. Such fields could exist near powerlines or where utilities ground neutral lines into the Earth. They found insect behavioral changes in response to electric fields as tested with a Y-choice chamber with an electric field generated in one arm of the chamber. Locomotor behavior and avoidance were affected by the magnitude of the electric fields with up to 85% of individuals avoiding the charged arm when the static e-field at the entrance to the arm was above 8–10 kV/m. Seeking to determine mechanisms of perception and interaction, they then surgically ablated the antennae and cockroaches were unable to avoid electric fields. They concluded that antennae are crucial in cockroach detection of electric fields that thereby helps them avoid such fields. They also noted that cockroach ability to detect e-fields is due to long antennae which are easily charged and displaced by such fields, not because of a specialized detection system. This leads to the possibility that other insects may also respond to electric fields via antennae alone.
Vácha et al. [208] found that cockroaches (P. americana) were sensitive to weak RFR fields and that the Larmor frequency at 1.2 MHz in particular had a “deafening effect” on magnetoreception. The parameter they studied was the increase in locomotor activity of cockroaches induced by periodic changes in geomagnetic North positions by 60°. The onset of the disruptive effect of a 1.2 MHz field was found between 12 and 18 nT whereas the threshold of a field twice the frequency (2.4 MHz) fell between 18 and 44 nT. A 7 MHz field showed no significant effect even at maximal of 44 nT. The results suggested resonance effects and that insects may be equipped with the same magnetoreception system as birds.
Prolić et al. [293] investigated changes in behavior via the nervous system of cerambycid beetles (Morimus funereus) in an open field before and after exposure to a 50 Hz ELF-MF at 2 mT. Experimental groups were divided into several activity categories. Results showed activity increased in the groups with medium and low motor activity, but decreased in highly active individuals. High individual variability was found in the experimental groups, as well as differences in motor activities between the sexes both before and after exposure to ELF‐MF. They assumed activity changes in both sexes were due to exposure to ELF‐MF. Only a detailed analysis of the locomotor activity at 1‐min intervals showed some statistically significant differences in behavior between the sexes.
Ants
Ants are another taxa found sensitive to EMF. Ants comprise between 15 and 25% of the terrestrial animal biomass and thrive in most ecosystems on almost every landmass on Earth. By comparison, the total estimated biomass (weight) of all ants worldwide equates to the total estimated biomass of all humans. Their complex social organization in colonies, with problem-solving abilities, division of labor, and both individual and whole colony communication via complex behavioral and pheromone signaling may account for their success in so many environments. Some ant species (e.g., Formica rufa-group) are known to build colonies on active earthquake faults and have been found to change behavior hours in advance of earthquakes [294], thus demonstrating predictive possibilities. Ants can modify habitats, influence broad nutrient cycling, spread seeds, tap resources, and defend themselves. Ants co-evolved with other species which led to many different kinds of mutual beneficial and antagonistic relationships.
Ants (e.g., Solenopsis invictus) are long known to be sensitive to magnetic fields both natural and manmade [295]. Ants (e.g., Atta colombica), like birds, have been found to be sensitive to the Earth’s natural fields and to use both a solar compass on sunny days as well as a magnetic compass when there is cloud cover [296]. Jander and Jander [297] similarly found that the weaver ant (Oecophylla spp) had a more efficient light compass orientation with a much less efficient magnetic compass orientation, suggesting that they switch from the former to the latter when visual celestial compass cues become unavailable. There is evidence from Esquivel et al. [298] that such magnetoreception is due to the presence of varying sized magnetite particles and paramagnetic resonance in fire ants (Solenopsis spp). But Riveros and Srygley [299] found a more complex relationship toward a magnetic compass rather than the presence of magnetite alone when leafcutter ants (Atta columbica) were subjected to a brief but strong magnetic pulse which caused complete disorientation regarding nest-finding. They found external exposures could interfere with ants’ natural magnetic compass in home path integration, which indicated evidence of a compass based on multi-domain and/or superparamagnetic particles rather than on single-domain particles like magnetite.
Acosta-Avalos et al. [300] found that fire ants are sensitive to 60 Hz alternating magnetic fields as well as constant magnetic fields, changing their magnetic orientation and magnetosensitivity depending on the relation between both types of magnetic fields. Alternating current had the ability to disrupt ant orientation, raising the question of effects to wild species from underground wiring and the common practice of powerline utility companies using the Earth as a neutral return pathway to substations, creating stray current along the way [99].
Camelitepe et al. [301] tested black-meadow ants’ (Formica pratensis) response under both natural geomagnetic and artificial earth-strength static EMFs (24.5 μT). They found that under the natural geomagnetic field, when all other orientational cues were eliminated, there was significant heterogeneity of ant distribution with the majority seeking geomagnetic north in darkness while under light conditions ants did not discriminate geomagnetic north. Under artificial EMF exposure, however, ant orientation was predominantly on the artificial magnetic N/S axis with significant preference for artificial north in both light and dark conditions. This indicated EMF abilities to alter ant orientation.
Ants are also shown to react to RFR [302, 303]. Cammaerts et al. [304] found that exposures to GSM 900 MHz at 0.0795 μW/cm2 significantly inhibited memory and association between food sites and visual and olfactory cues in ants (Myrmica sabuleti) and eventually wiped out memory altogether. Subsequent exposure, after a brief recovery period, accelerated memory/olfactory loss within a few hours vs. a few days, indicating a cumulative effect even at very low intensity. The overall state of the exposed ant colonies eventually appeared similar to that exhibited by honey bee (Apis mellifera) colony collapse disorder. Although the impact of GSM 900 MHz radiation was greater on the visual memory than on the olfactory memory, the researchers concluded that such exposures — common to cell phones/towers — were capable of a disastrous impact on a wide range of insects using olfactory and/or visual memory, including bees. Many ant species (e.g., Lasius neglectus, Nylanderia fulva, Camponotus spp, Hymenoptera formicidae, Solenopsis invicta, among others) are attracted to electricity, electronic devices, and powerlines, thereby causing short circuits and fires. One hypothesis [305] is that the accumulation of ants in electrical equipment may be due to a few foraging “worker ants” seeking warmth and finding their way into small spaces, completing electrical contacts which then causes a release of alarm exocrine gland pheromones that attract other ants, which then go through the same cycle. In their study, they found that workers subjected to a 120 V alternating-current released venom alkaloids, alarm pheromones and recruitment pheromones that elicited both attraction and orientation in ants as well as some other unknown behavior-modifying substances. But given how ants are affected by EMFs in general it is likely that an attractant factor is also involved, not just warmth and small spaces.
There is evidence that ants use their antennae as “antennas” in two-way electrochemical communications. Over 100 hundred years ago, Swiss researcher Auguste Forel [306] removed the antennae of different species of ants and put them together in one place. What would have normally evoked aggressive behaviors among the different species did not occur and they got along as if belonging to the same colony. To Forel this indicated an ability of ant antennae to help different ant species identify each other.
Two mechanisms in ants have long been known for chemical receptivity as well as electromagnetic sensitivity. Recently Wang et al. [307] found evidence that chemical signals located specific to antennae vs. other body areas drew more attention from non-nest mates. When cuticular hydrocarbons (CHCs) were removed by a solvent from antennae, non-nest mates responded less aggressively than to other areas of the body, indicating that antennae reveal nest-mate identity, conveying and receiving social signals. Regarding magnetoreception, magnetic measurements [308], [309], [310] found the presence of biogenic magnetite was concentrated in antennae and other body parts of the ant Pachycondyla marginata. De Oliveira et al. [311] also found evidence of magnetite and other magnetic materials imbedded in various locations of antennae tissue in P. marginata indicating that antennae function as magnetoreceptors. The amount of magnetic material appeared sufficient to produce a magnetic-field-modulated mechanosensory output and therefore demonstrated a magnetoreception/transduction sense in migratory ants.
Ticks
Ticks are members of the order Arachnida, shared with scorpions and spiders. Recent papers in a tick species (Dermacentor reticulates) mirrors an attraction to some frequencies but not others. Vargová et al. [312, 313] found that exposure to RFR may be a potential factor altering both presence and distribution of ticks in the environment. Studies were conducted to determine potential affinity of ticks for RFR using radiation-shielded tubes (RST) under controlled conditions in an electromagnetic compatibility laboratory in an anechoic chamber. Ticks were irradiated using a Double-Ridged Waveguide Horn Antenna to RF-EMF at 900 and 5,000 MHz; 0 MHz served as control. Results found that 900 MHz RFR induced a higher concentration of ticks on the irradiated arm of RST whereas at 5,000 MHz ticks escaped to the shielded arm. In addition, 900 MHz RFR had been shown to cause unusual specific sudden tick movements during exposure manifested as body or leg jerking [312]. These studies are the first experimental evidence of RFR preference and behavioral changes in D. reticulates with implications for RFR introduced into the natural environment by devices and infrastructure. In a further study, Frątczak et al. [314] reported that Ixodes ricinus ticks were attracted to 900 MHz RFR at 0.1 μW/cm2, particularly those infected with Rickettsia (spotted fever).
RFR may be a new factor in tick distribution, along with known factors like humidity, temperature and host presence, causing concentrated non-homogenous or mosaic tick distribution in natural habitats. Tick preference for 900 MHz frequencies common to most cell phones has possibly important ecological and epidemiological consequences. Increasing exposures from use of personal devices and infrastructure in natural habitats where ticks occur may increase both tick infestation and disease transmission. Further studies need to investigate this work, given the ubiquity of ticks today, their northward spread due to climate change in the Northern Hemisphere, and the increasing and sometimes life-threatening illnesses they transmit to humans, pets, and wildlife alike.
Monarch butterflies
The American Monarch butterfly (D. plexippus) has fascinated researchers for over 100 years as it is the only insect known to migrate in multi-generational stages [315], [316], [317], [318], [319], with the ability to find their exact birthplace on specific milkweed plants (Asclepias spp.) at great distances across land and oceans.
Monarchs (D. plexippus), found across Southern Canada, the United States, and South America, are generally divided by the Rocky Mountains into eastern and western migratory groups. Their population has precipitously declined by 99.4% since the 1980s (85% of that since 2017) and by 90% in the past two decades in both western and eastern populations [13, 15]. These steep declines are from numerous anthropogenic causes and may have already crossed extinction thresholds, thereby leaving us bereft not only of their beauty and inspiration, but also the perfect model for long-distance animal migration study in general.
Monarch butterflies are among North America’s most beloved invertebrates. They have for centuries navigated thousands of miles/kilometers in an iconic fall migration from southern Canada and the mid- and northeastern U.S. to a small area of about 800 square miles (2,072 square kilometers) in Central Mexico where they once wintered over in the millions in small remote oyamel fir forests. By the time they reach their final destination, some will have traveled distances exceeded only by some migratory seabird species. The monarch is the only insect known to migrate annually over 3,000 miles (4,828 km) at ∼ 250 miles (402 km) per day in the fall from the Canadian border to Mexico, and in the springtime back again. Similar to some bird species, it is the only butterfly known to have a two-way migration pattern. Monarchs are only followed by army cutworm moths (Euxoa auxiliaris) which may migrate several thousand kilometers to high elevation sites in the Rocky Mountains to escape lowland heat and drought.
But monarchs are more interesting than for this one amazing migrational feat alone. How they do this is a long-standing mystery since their entire lifecycle, including their two-stage spring return migration, is multi-generational indicating genetic factors in directional mapping since the final return fall migration south cannot be considered “learned.” Several multifaceted mechanisms must come into play, as well as little understood complexities in how those mechanisms cooperate and trade off with each other under different environmental circumstances. Monarchs also go from solitary insects during early developmental stages confined to specific locations, then exhibit social insect behaviors after the third generation has reached northern latitudes and turned south during the final fall migration. And all of this happens in a brain the size of a grain of sand.
Reppert et al. [320] published an excellent review in 2010 on the complexities of monarch migration, noting “…recent studies of the fall migration have illuminated the mechanisms behind the navigation south, using a time-compensated sun compass. Skylight cues, such as the sun itself and polarized light, are processed through both eyes and likely integrated in the brain’s central complex, the presumed site of the sun compass. Time compensation is provided by circadian clocks that have a distinctive molecular mechanism and that reside in the antennae. Monarchs may also use a magnetic compass, because they possess two cryptochromes that have the molecular capability for light-dependent magnetoreception. Multiple genomic approaches are being utilized to ultimately identify navigation genes. Monarch butterflies are thus emerging as an excellent model organism to study the molecular and neural basis of long-distance migration.” Reppert and de Roode [321] updated that information in 2018.
Although it has been known for some time that monarchs use a circadian rhythm time-compensated directional sun compass [316, 322], [323], [324], [325], [326], [327], [328], [329], [330], [331], [332], [333], [334], [335], [336], [337], [338], many questions remain about its dynamics and concerns regarding effects from radiation.
Monarch antennae are known to contain magnetite [339, 340] and cryptochromes [335, 336, 341, 342] — both understood to play a role in magnetoreception (see “Mechanisms”above). One early study by Jones and MacFadden [343] found magnetic materials located primarily in the head and thorax areas of dissected monarchs. More recently, Guerra et al. [16] found convincing evidence that monarchs use a magnetic compass to aid their longest fall migration back to Mexico. Those researchers used flight simulator studies to show that migrants possess an inclination magnetic compass to assist fall migration toward the equator. They found this inclination compass is light-dependent, utilizing ultraviolet-A/blue light between 380 and 420 nm and noted that the significance of light (<420 nm) for an inclination compass function had not been considered in previous monarch studies. They also noted that antennae are important for an inclination compass since they contain light-sensitive magnetosensors. Like some migratory birds, the presence of an inclination compass would serve as an orientation mechanism when directional daylight cues are impeded by cloudy or inclement weather or during nighttime flight. It may also augment time-compensated sun compass orientation for appropriate directionality throughout migration. The inclination compass was found to function at earth-strength magnetic fields, an important metric.
The question remains: Can the magnetic compass in monarchs be disrupted by anthropogenic EMF like it does with geomagnetic orientation in migratory birds [213]. There is some indication this is possible. Perez et al. [330] found monarchs completely disorient after exposure to a strong magnetic field (0.4-T MF for 10 s, or approximately 15,000 times the Earth’s magnetic field) immediately before release vs. controls. This is a high exposure but within range of man-made exposures today very close to powerlines.
Bees, wasps, and others
Pollinators, bees in particular, are keystone species without which adverse effects would occur throughout food webs and the Earth’s entire biome were pollinators to disappear. Because of their central role and accessibility for research, bee studies have created a wealth of information, including regarding anthropogenic EMFs.
Bees — especially honey and bumble bees — are another iconic insect species beloved for their role in pollination; honey, propolis, royal jelly and beeswax production; their critical importance to our food supply; and their crucial role in global ecological health and stability. Found on every continent except Anarctica wherever there are flowering plants requiring insect pollination, there are over 16,000 known species of bees in seven different biological families, consisting of four main branches. Some species live socially in colonies while others are solitary. The western honey bee (Apis mellifera) is the best known and most studied due in part to its central role in agriculture. Bees feed on nectar for energy and pollen for protein/nutrients, and have co-evolved with many plant species in astoundingly complex ways. They are also highly sensitive to both natural and anthropogenic EMFs. Beeswax itself has electrical properties [50].
Human apiculture has been practiced since the time of ancient Egyptian and Greek cultures and bees have been closely studied since the 1800s. Almost all bee species, including commercially raised and wild species, are under decades-long multiple assaults. These include from pesticides, herbicides, climate change, various bacterial/viral diseases, infestations from parasitic mite species — particularly Apis cerana, Varroa destructor and Varroa jacobsoni beginning in the mid-1980s — and predation from introduced species that attack bees directly (e.g., the invasive giant bee-eating hornet Vespa mandarinia), as well as alter plant ecology over time to adversely affect bee food supply. Some have suggested that vanishing bees may also have to do with premature aging due to environmentally caused shortened telomeres [344].
Whole colony collapse disorder (CCD) is the most dramatic manifestation of domesticated bee demise in which worker bees abruptly disappear from a hive without a trace, resulting in an empty hive with perhaps a remaining queen and a few worker bees despite ample resources left behind. Few, if any, dead bees are ever found near the hive. CCD was first described in the U.S. in 2006 in Florida in commercial western honey bee colonies. Van Englesdorp et al. [345] quantified bee losses across all beekeeping operations and estimated that between 0.75 and 1.00 million honey bee colonies died in the United States over the winter of 2007–2008. Up until that survey, estimates of honey bee population decline had not included losses occurring during the wintering period, thus underestimating actual colony mortality.
The same phenomenon had been described by beekeepers in France in 1994 [346] — later attributed to the timing of sunflower blooming and the use of imidacloprid (IMD), a chlorinated nicotine-based insecticide or “neonicotinoid” being applied to sunflowers for the first time there [347]. Similar to DDT but considered safer for mammals including humans, neonicotinoids are a slow-release class of neurotoxins that block insect nervous systems via acetylcholine receptors, interfering with neuronal signaling across synapses. Sublethal doses can interfere with bee navigation.
Since then similar phenomena have been seen throughout Europe [348] and some Asian countries. Causal hypotheses included all of the above factors with varying foci on pesticide classes like neonicotinoids and genetically modified crops, but no single agent adequately explains CCD. Bromenshenk et al. [349] however, identified pathogen pairing/co-infection with two previously unreported RNA viruses — V. destructor-1, and Kakugo viruses, and a new irridescent virus (IIV) (Iridoviridae) along with Nosema ceranae — in North American honey bees that were associated with all sampled CCD colonies. The pathogen pairing was not seen in non-CCD colonies. Later cage trials with IIV type-6 and N. ceranae confirmed that co-infection with those two pathogens was more lethal to bees than either pathogen alone. Still many questions remain.
There are two national surveying groups in the U.S. — the U.S. Department of Agriculture (USDA) which began surveying managed bee populations in 2015 but funding was cut in late 2019; and the Bee Informed Partnership (BIP), a non-profit that coordinates with research facilities and universities. Prior to USDA’s funding cuts, managed colonies decreased from CCD by 40% [350] with an additional 26% over the same quarter in 2019 [351]. BIP’s survey period for April 1, 2018 through April 1, 2019 found U.S. beekeepers lost an estimated 40.7% of their managed honey bee colonies. The previous year had similar annual losses of 40.1%. The average annual rate of loss reported by beekeepers since 2010–11 was 37.8% [352].
Also in the U.S., for the first time in 2016, seven species of Hawaiian yellow-faced bees (Hylaeus anthracinus, Hylaeus longiceps, Hylaeus assimulans, Hylaeus facilis, Hylaeus hilaris, Hylaeus kuakea, and Hylaeus mana) were added to the federal endangered species list, as well as the rusty patched bumble bee (Bombus affinis) which, prior to the late 1990s, had been widely dispersed across 31 U.S. states [353]. Mathiasson and Rehan [354] examined 119 species in museum specimens in New Hampshire going back 125 years and concluded that 14 species found across New England were on the decline by as much as 90%, including the lesser studied leafcutter and mining bees that nest in the ground, unlike honeybees that nest in commercial hives or in trees, shrubs, and rock crevices in the wild.
Worldwide, many bee and other pollinator populations have also declined over the last two decades. Managed honey bee (Apis mellifera) colonies decreased by 25% over 20 years in Europe and 59% over 58 years in North America, with many wild bumble bee populations in Europe and North America having gone locally extinct [355], [356], [357], [358]. But while dramatic range contractions have been seen, not all bees in all places are declining; some populations are growing depending on opportunistic and species-adaptability factors. For many species data are still insufficient, of poor quality, or nonexistent [359]. In addition, bee declines can affect flora survival. Miller-Struttmann et al. [360] recorded flower declines of 60% with 40 years of climate warming in alpine meadows — areas largely protected from land-use changes. Insects are highly sensitive to temperature changes.
A comprehensive UK survey of pollinator species [361] found that of 353 wild bee and hoverfly species across Britain from 1980 to 2013, 25% had disappeared from the places they had inhabited in 1980. Further estimates found a net loss of over 2.7 million in 0.6 mi (1 km) grid cells across all species. Declining pollinator evenness suggested losses were concentrated in rare species. Losses linked to specific habitats were also identified, with a 55% decline among wild upland species while dominant crop pollinators increased by 12%, possibly due to agricultural business interventions. The general declines found a fundamental deterioration in both wider biodiversity and non-crop pollination services.
There is no question that the huge diversity of pollinator species across the planet is suffering and that losses could be catastrophic with an estimated 90% of wild plants and 30% of world crops in jeopardy [362].
There is a likelihood that rising EMF background levels play a role. Bees have been known for decades to have an astute sense of the Earth’s DC magnetic fields [363, 364] and rely on that perception for survival. For centuries beekeepers had noticed curious movements in bee hives but Austrian ethologist Karl von Frisch finally interpreted that activity in the 1940s, winning the Nobel Prize in 1973 for what came to be known as the honey bee “waggle dance.” Through complex circles and waggle patterns, bees communicate the location of food sources to other members of the hive, using the orientation of the sun and the Earth’s magnetic fields as a gravity vector, “dancing” out a map for hive members to follow like nature’s own imbedded GPS. Bees also detect the sun’s direction through polarized light and on overcast days use the Earth’s magnetic fields, likely through the presence of magnetite in their abdominal area, and employ complex associative learning and memory [365].
Building on the earlier work of Gould et al. [119], Kobayashi and Kirschvink [52] noted that biogenic magnetite in honey bees is located primarily in the anterior dorsal abdomen. When small magnetized bits of wire were glued over those areas, it interfered with bees’ ability to learn to discriminate magnetic anomalies in conditioning experiments, while nonmagnetized wire used in controls did not interfere [366]. Kirschvink and Kobayashi [367] found that when pulse-remagnetization techniques were used on bees trained to exit from a T-maze, that north-exiting bees could be converted to a south-exiting direction similar to what was observed in magnetobacteria and artificial reorientation by Blakemore [113]. Honeybees could also be trained to respond to very small changes in the geomagnetic field intensity [368]. Valkova and Vacha [369] discussed the possibility that honey bees use a combination of both radical pair/cryptochromes and magnetite to detect the geomagnetic field and use it for direction like many birds.
Given these sensitivities, bees may be reacting negatively through muti-sensory mechanisms to numerous sources of anthropogenic multi-frequency interference. Bumble bees (Bombus terrestris), a solitary species, and honey bees (Apis mellifera), a social hive species, are known to detect weak electric fields in different behavioral contexts, using different sensory mechanisms. Bumble bee e-field detection is likely through mechanosensory hairs [370], [371], [372] while honey bees reportedly use their antennae [373] that are electro-mechanically coupled to the surrounding e-field, taking place in the antennal Johnston’s organ. Greggers et al. [373] found that honey bee antennae oscillate under electric field stimulation that can then stimulate activity in the antennal nerve. The latter occurs due to bees being electrically charged, and thus subject to electrostatic forces. Erickson [374] found different surface potentials in bees when leaving or entering hives, and Colin et al. [375] found seasonal variability between positive and negative charges in resting bees. It has also been shown that honey bees with removed or fixed antennae are less able to associate food reward with electric field stimuli and that bees emanate modulated electric fields when moving their wings (at about 230 Hz) and body (at about 16.5 Hz) during the waggle dance [373].
Electro-ecological interplay between flowers and pollinators has also been known since the 1960s and is critical to pollen transfer from flowers to bees [376], [377], [378]. It is known that as bees fly through the air, they accumulate a positive charge. Flowers, on the other hand, which are electrically grounded through their root systems, tend to have a negative charge in their petals created by surrounding air that carries around 100 V for every meter above ground. The accumulating positive charge around the flower induces a negative charge in its petals which then interacts with the positive charge in bees. In fact, bees do not even need to land on flowers for pollen transfer to occur; pollen can “jump” from the flower to the bee as the bee approaches due to charge differentials between the two. Thus, it appears that bees and flowers have been “communicating” via electric fields all along [379]. Bees can also learn color discrimination tasks faster when color cues are paired with artificial electric field cues similar to those surrounding natural flowers, but did not learn as readily in an electrically neutral environment [370].
This evidence points to floral e-fields being used in a co-evolutionary symbiotic relationship with bees. Clarke et al. [370, 371] even found that bumblebees can distinguish between flowers that give off different electric fields as floral cues to attract pollinators. Like visual cues, floral electric fields exhibit complex variations in pattern and structure that bumblebees can distinguish, contributing to the myriad complex cues that create a pollinator’s memory of floral food sources. And because floral electric fields can — and do — change within seconds of being visited by pollinators, this sensory ability likely facilitates rapid and dynamic “information exchange” between flowers and their pollinators. Bumblebees can even amazingly use electric field information to discriminate between nectar-rewarding and unrewarding flowers [370].
Bees, locusts: ELF-EMF
Bees are also known to be sensitive to anthropogenic ELF-EMF. In 1973,Wellenstein [380] found that high tension powerlines adversely affected honey bees in wooden hives. This in part prompted the Bonneville Power Administration, an American federal agency operating in the Pacific Northwest under the U.S. Department of Energy (U.S. DOE), to investigate in 1974 [381], [382], [383], [384] the effects of transmission lines on people, plants, and animals, including honey bees. The industry group, Electric Power Research Institute, also followed up on bee research [385, 386]. Both of those studies confirmed that transmission line electric fields can affect honey bees inside wooden hives as wood is a poor insulator and current can be induced when hives are placed in electric fields whether metal is present or not. The strength of the current inside the hive was influenced by the electric field strength, hive height, and moisture conditions with effects noticeable when induced current exceeded 0.02–0.04 mA. Depending on hive height, this occurred in field strengths between 2 and 4 kV/m. Effects included increased motor activity with transient increase in hive temperature, excessive propolis production (a resinous material used by bees as a hive sealer), decreased colony weight gains, increased irritability and mortality, abnormal production of queen cells, queen loss, decreased seal brood, and poor over-winter colony survival [387]. Impacts were most likely caused by electric shocks inside the hives [386, 388]. Effects were mitigated with grounded metal screen/shielding of hives [385]; however, bees appeared unaffected by magnetic fields which permeate metal shielding. The authors concluded that the shielding results indicated that bees were unaffected by flying through an external electric field up to 11 kV/m but noted that the study design could not reveal if subtle effects were occurring.
A more recent study of electric fields by Migdał [389] focused on honey bee behavioral effects on walking, grooming, flight, stillness, contact between individuals, and wing movement. They found that the selected frequency, intensity, and duration of exposure effects bees’ behavioral patterns. Bees were exposed for 1, 3 and 6 h to E-fields at 5.0 kV/m, 11.5 kV/m, 23.0 kV/m, or 34.5 kV/m (with controls under E-field <2.0 kV/m). Within the exposed groups, results showed that exposure for 3 h caused decreased time that bees spent on select behaviors as well as the frequency of behaviors, whereas after both 1 and 6 h, the behavioral parameters increased within the groups. The researchers concluded that a barrier allowing behavioral patterns to normalize for some periods was indicated although none of the exposed groups returned to reference values in controls which adhered to normal behavioral patterns. Bees may have compensatory windows that appear to be both time and intensity dependent for E-fields. The significance of this study is that bees must accomplish certain activities — like flight frequency and the honey bee ‘waggle dance’ noted above — that are critical for life expectancy and survival. Even slight sequential disturbances may have cascading effects.
In an early-1988 study, Korall et al. [390] also found effects to bees from magnetic fields (MF). Bursts comparable to some of today’s pulsed exposures of artificial MF at 250 Hz — the frequency of buzzing during the waggle dance — were applied parallel to natural EMF field lines and induced unequivocal ‘jumps’ of misdirection by up to +10° in bees during the waggle dance. This alone could cause directional confusion in hives. Continuous fields of 250 Hz with bursts perpendicular to the static MF however caused no effects. They concluded that a resonance relationship other than classic resonance models was indicated (see “Mechanisms” above). This early work has implications for subsequent digital pulsing and all wireless broadband technology.
More recent work on honey bees and ELF-EMF by Shepherd et al. [209] in 2018 found that acute exposure to 50 Hz fields at levels from 20–100 μT (at ground level underneath powerline conductors), to 1,000–7,000 μT (within 1 m of the conductors), reduced olfactory learning, foraging flight success toward food sources and feeding, as well as altered flight dynamics. Their results indicated that 50 Hz ELF-EMFs from powerlines is an important environmental honey bee stressor with potential impacts on cognitive and motor abilities.
Some wasp species have also been found sensitive to ELF-EMF. Pereira-Bomfim et al. [391] investigated the magnetic sensitivity of the social paper wasp (Polybia paulista) by analyzing wasp behavior in normal geomagnetic fields and in the presence of external magnetic fields altered by either permanent magnets (DC fields) or by Helmholtz coils (AC fields). They evaluated the change in foraging rhythm and colony behavior, as well as the frequency of departing/homeward flights and the behavioral responses of worker wasps located on the outer nest surface. They found that the altered magnetic field from the DC permanent magnet produced an increase in the frequency of departing foraging flights, and also that wasps grouped together on the nest surface in front of the magnet with their heads and antennae pointing toward the perturbation source, possibly indicating a response to a potential threat as a defense strategy. Controls showed no such grouping behavior. The AC fields created by the Helmholtz coils also increased foraging flights, but individuals did not show grouping behavior. The AC fields, however, induced wasp workers to perform “learning flights.” They concluded that for the first time, P. paulista demonstrated sensitivity to an artificial modification of the local geomagnetic field and that mechanisms may be due to both cryptochrone/radical pairs and magnetite.
Another flying insect model — desert locust (Schistocerca gregaria) — was found susceptible to entrainment by ELF-EMF. In a complex study, Shepherd et al. [392] analyzed acute exposure to sinusoidal AC 50 Hz EMF (field strength range: 10 to 10,000 μT) vs. controls on flights of individual locusts tethered between copper wire coils generating EMFs at various frequencies and recorded on high-speed video. Results found that acute exposure to 50 Hz EMFs significantly increased absolute change in wingbeats in a field-strength-dependent manner. Applying a range of ELF-EMF close to normal wingbeat occurance, they found that locusts entrained to the exact frequency of the applied EMF. They concluded that ELF exposure can lead to small but significant changes in locust wingbeats, likely due to direct acute effects on insect physiology (vs. cryptochrome or magnetite-based magnetoreception) and/or behavioral avoidance responses to molecular/physiological stress. Wyszkowska et al. [393] also found effects on locusts — exposure to ELF-EMF above 4 mT led to dramatic effects on behaviour, physiology and increased Hsp70 protein expression. Such higher exposures may be found near high tension lines.
Bees: RF-EMF
The effects of RF-EMF on bees is of increasing interest since that is the fastest rising EMF environmental exposure of the past 30 years [369]. Beginning in the early 2000s, studies of cell phones placed in the bottom of hives began to appear. Honey bees showed disturbed behavior when returning to hives after foraging and under various RFR exposures [394], [395], [396]. Early methodologies, however, were not well designed or controlled. For instance, Favre [397] found increased piping — a distress signal that honey bees give off to alert hive mates of threats and/or to announce the swarming process. Both active and inactive mobile phone handsets were placed in close proximity to honey bees with sounds recorded and analyzed. Audiograms and spectrograms showed that active phone handsets had a dramatic effect on bee behavior in induced worker piping. This study was criticized by Darney et al. [398] for using music in the active RFR exposure which may have introduced a variable capable of affecting bee piping in response to the added sound alone.
In a complex study, Darney et al. [398] tested high frequency (HF) and ultra high frequency (UHF) used in RFID technology in order to develop a method to automatically record honey bees going in and out of hives. They glued RFID tags onto individual bee dorsal surfaces that were detected at the hive entrance by readers emitting HF radio waves. They then looked for possible HF adverse effects on honey bees’ survival. Eight-day-old honey bees were exposed to HF 13.56 MHz or UHF 868 MHz RFR for 2 h split into ON and OFF periods of different durations. Dead bees were counted daily with cumulative mortality rates of exposed and non-exposed honey bees compared seven days after exposure. Two out of five experimental conditions found increased mortality, once after HF and once after UHF exposure, with OFF duration of 5 min or more, after which they recommended limiting honey bee exposure to RFR to less than 2 h per day. They also curiously concluded that the RFID parameters they used for monitoring hive activity presented no adverse effects but the multifrequency peak exposures and RFID attachments need further study in light of other works on RFID effects (see Part 1 for discussion of RFID.)
In another study using an active cell phone attached to hive frames, Odemer and Odemer [399] investigated RFR effects on honey bee queen development and mating success. Control hives had an inactive cell phone attached. After exposing honey bee queen larvae to GSM 900 MHz RFR during all stages of pre-adult development (including pupation), hatching of adult queens was assessed 14 days after exposure and mating success after an additional 11 days. They found that chronic RFR exposure significantly reduced honey bee queen hatching; that mortalities occurred during pupation but not at the larval stages; that mating success was not adversely affected by the irradiation; and that after exposure, surviving queens were able to establish intact colonies. They therefore determined that mobile phone radiation had significantly reduced the hatching ratio but not mating success if queens survived, and if treated queens successfully mated, colony development was not adversely affected. Even though they found strong evidence of mobile phone RFR damage to pupal development, they cautioned its interpretation, noting that the study’s worst-case exposure scenario was the equivalent of a cell phone held to a user’s head, not at a level found in typical urban or rural hive settings. They concluded that while no acute negative effects on bee health were seen in the mid-term, they also could not rule out effects on bee health at lower chronic doses such as found in ambient environments, and urgently called for long term research on sublethal exposures present in major city environments.
Sharma and Kumar [400] found similar abnormalities in honey bee behavior when they compared the performance of honey bees in RFR exposed and unexposed colonies. Two of four test colonies were designated and each equipped with two functional cell phones — a high exposure — placed on two different hive side walls in call mode at GSM 900 MHz. The average RFR power density was measured at 8.549 μW/cm2 (56.8 V/m, electric field). One control colony had a dummy phone; the other had no phone. Exposure was delivered in 15 min intervals, twice per day during the period of peak bee activity. The experiment was performed twice a week during February to April. It covered two brood cycles with all aspects of hive behavior observed, including brood area comprising eggs, larvae and sealed brood; queen proficiency in egg-laying rate; foraging, flight behavior, returning ability; colony strength including pollen storage; and other variables. Results included a significant decline in colony strength and egg laying and reduced foraging to the point where there was no pollen, honey, brood, or bees by the end of the experiment. One notable difference in this study was that the number of bees leaving the hive decreased following exposure. There was no immediate exodus of bees as a result of exposure — instead bees became quiet, still, and/or confused “…as if unable to decide what to do…” the researchers said. Such a response had not been reported before. The authors concluded that colony collapse disorder is related to cell phone radiation exposures.
Vilić et al. [401] investigated RFR and oxidative stress and genotoxicity in honey bees, specifically on the activity of catalase, superoxide dismutase, glutathione S-transferase, lipid peroxidation levels and DNA damage. Larvae were exposed to 900 MHz RFR at field levels of 10, 23, 41 and 120 V m−1 for 2 h. At a field level of 23 V m−1 the effect of 80% AM 1 kHz sinusoidal and 217 Hz modulation were also investigated. They found that catalase activity and the lipid peroxidation levels significantly decreased in larvae exposed to the unmodulated field at 10 V m−1 (27 μW/cm2) compared to the control. Superoxide dismutase and glutathione S-transferase activity in honey bee larvae exposed to unmodulated fields were not statistically different compared to the control. DNA damage increased significantly in larvae exposed to modulated (80% AM at 1 kHz) field at 23 V m−1 (140 μW/cm2) compared to control and all other exposure groups. Their results suggested that RFR effects in honey bee larvae manifested only after certain EMF exposure conditions. Interestingly, they found that increased field levels did not cause a linear dose-response in any of the measured parameters, while modulated RFR produced more negative effects than the corresponding unmodulated field. They concluded that while honey bees in natural environments would not be exposed to the high exposures in their experiments, the results indicated additional intensive research is needed in all stages of honey bee development since the cellular effects seen could affect critical aspects of bee health and survival.
Kumar et al. [402] also found biochemical changes in worker honey bees exposed to RFR. A wooden box was designed with glass on the front and back and wire gauze for ventilation on two sides for both exposed bees and controls. Cell phones (same make, model, and network connection) were kept in listen-talk mode for 40 min. At intervals of 10, 20 and 40 min, 10 exposed and 10 control bees were collected at the same times. Hemolymph was then extracted from the inter-segmental region of bee abdomens and analyzed. Results included increased concentration of total carbohydrates in exposed bees in the 10 min exposure period compared to unexposed bees. Increasing the exposure time to 20 min resulted in a further increase in the concentration, but exposure at 40 min had a reverse effect with declines in carbohydrate concentration although it was still higher than controls. Hemolymph glycogen and glucose content also showed the same exposure pattern — increase in content up to 20 min after which a slight decline that was still higher than controls. Changes in total lipids/cholesterol — the major energy reserves in insects — can affect numerous biological processes. Some lipids are crucial membrane structure components while others act as raw materials in hormones and pheromones. Changes in these parameters are significant to every biological activity, including reproduction. Also of interest in this study was that as exposure time increased, the bees appeared to have identified the source of disturbance. There was a large scale movement of workers toward the talk-mode (with higher RFR exposure during transmission function) but not the listening mode. Bees also showed slight aggression and agitation with wing beating. The researchers hypothesized that this increased activity could be responsible for increased energy use thereby accounting for the decrease in concentration of carbohydrates and lipids in the 40 min exposed sample. The researchers concluded that cell phone radiation influences honey bee behavior and physiology. Sharma [403] had also reported increased glycogen and glucose levels in exposed honey bee pupa.
It must be pointed out that the cell phone emission conditions used in some experiments are questionable, in particular where there was no detail regarding how the phones were activated to achieve emission.
Not all studies demonstrated adverse effects. Mall and Kumar [404] found no apparent RFR effects on brood rearing, honey production or foraging behavior in honey bees in hives with cell phones inside or near a cell tower; and Mixon et al. [405] also found no effects of GSM-signal RFR on increased honey bee aggression. They concluded that RFR did not impact foraging behavior or honey bee navigation and therefore was unlikely to impact colony health.
Although there are several anectodal reports of insect losses near communication towers, there are only a handful of ambient RFR field studies conducted on invertebrates thus far. In the first large survey of wild pollinating species at varying distances from cell towers, Lázaro et al. [406] found both positive and negative effects from RFR in a broad range of insects on two islands (Lesvos and Limnos) in the northeastern Aegean Sea near Greece. Measured ambient RFR levels included all frequency ranges used in cell communications; broadcast RFR is absent on the islands. RFR values did not significantly differ between islands (Lesvos: 0.27 ± 0.05 V/m; Limnos: 0.21 ± 0.04 V/m; v3 2 = 0.08, p=0.779) and did not decrease with the distance to the antenna, possibly, they hypothesized, because some sampling points near the antenna may have been outside or at the edge of the emission lobes. They measured RFR at four distances of 50, 100, 200 and 400 m (164, 328, 656, and 1,312 ft, respectively) from 10 antennas (5 on Lesvos Island and 5 on Limnos Island) and correlated RFR values with insect abundance (numbers of insects) and richness (general health and vitality) — the latter only for wild bees and hoverflies. The researchers conducted careful flowering plant/tree- and- insect inventories in several low-lying grassland areas, including for wild bees, hoverflies, bee flies, other remaining flies, beetles, butterflies, and of various types. Honey bees were not included in this study as they are a managed species subject to beekeeper decisions and therefore not a wild species. On Lesvos 11,547 insects were collected and on Limnos 5,544. Varied colored pan traps for both nocturnal and diurnal samples were used. Results found all pollinator groups except butterflies were affected by RFR (both positively and negatively) and for most pollinator groups effects were consistent on both islands. Abundance for beetles, wasps, and hoverflies significantly decreased with RFR but overall abundance of wild bees and bee flies significantly increased with exposure. Further analysis showed that only abundance of underground-nesting wild bees was positively related to RFR while wild bees nesting above ground were not affected. RFR effects between islands differed only on abundance of remaining flies. On species richness, RFR tended to only have a negative effect on hoverflies in Limnos. Regarding the absence of effects seen in butterflies, they hypothesized that the pan trap collection method is not efficient for collecting butterflies (butterflies accounted for only 1.3 % of total specimens), and that a different sampling method might produce a different result. They concluded that with RFR’s negative effects on insect abundance in several groups leading to an altered composition of wild pollinators in natural habitats, it was possible this could affect wild plant diversity and crop production. They further said the negative relationship between RFR on the abundance of wasps, beetles and hoverflies could indicate higher sensitivity of these insects to EMFs. Potentially more EMF-tolerant pollinators, such as underground-nesting wild bees and bee flies, may fill the vacant niches left by less tolerant species, thus resulting in their population increases. Another possible explanation is that EMFs may have particularly detrimental effects on more sensitive larval stages, and if so, larvae developing above ground (many beetles, wasps, hoverflies) may be more vulnerable than those developing underground since the former could be exposed to higher radiation levels.
In another field study, Taye et al. [407] placed five hives from December to May at varying distances of 1,000, 500, 300, 200 and 100 m (3,280, 1,640, 984, 656 and 328 ft, respectively) from a cell tower in India to measure flight activity, returning ability, and pollen foraging efficiency in honey bees (Apis cerana F). They found most effects closest to towers with the least returning bees at 100 m distance from the tower. Maximum foraging and return ability to the colonies was seen at 500 m, followed by 1,000 m and in descending order at 300 and 200 m, with the fewest returning bees at 100 m from the tower. The study also found that if bees returned, the pollen load per minute was not significantly affected.
Vijver et al. [408] however challenged the accuracy of distance from towers that is often used as a proxy for EMF gradients such as the study above. In a field study in The Netherlands, the researchers tested exposure to RFR from a cell base station (GSM 900 MHz) on the reproductive capacity of small virgin invertebrates during the most sensitive developmental periods spanning preadolescent to mating stages when reproductive effects would most likely be seen. Careful RFR field measurements were taken to determine null points in order to see if distance from emitters is a reliable RFR exposure model in field studies. They exposed four different invertebrate hexapod species. Springtails (Folsomia candida), predatory ‘bugs’ (Orius laevigatus), parasitic wasps (Asobara japonica), and fruitflies (D. melanogaster) were placed in covered pedestal containers within the radius of approximately 150 m of a 900 MHz mobile phone base station for a 48-h period. Six control groups were placed within 6.6 ft (2 m) of the treatment groups and covered in Farady cages. After exposure, all groups were brought to the laboratory to facilitate reproduction with resulting fecundity and number of offspring then analyzed. Results showed that distance was not an adequate proxy to explain dose-response regressions. After complex data synthesis, no significant impact from the exposure conditions, measures of central tendency, or temporal variability of EMF on reproductive endpoints were found although there was some variability between insect groups. As seen in other studies, distance is often used to create a gradient in energy exposures in studies but this study found the intensity of the transmitter and the direction of transmission to be more relevant, as did Bolte and Eikelboom [409, 410]. The direction and tilt of the transmitter determines whether the location of interest in field studies is in the main beam. In some instances, the closer promixity to the transmitter provided lower readings than further away, which they found between two locations. They also noted that the organisms selected in the study were small in size; springtails have a body length on average of 2 mm; wasps are about 3 mm, insect sizes from 1.4 to 2.4 mm, with the largest organisms tested being female fruit flies at about 2.5 mm length and males slightly smaller. Due to size, limited absorption and little energy uptake capacity, none of these insects are efficient whole-body receptors for 900 MHz waves with a wavelength of approximately 13 in (33 cm). But they further noted that this was a linear regression study and that biological effects are often non-linear. However, finding no distinct effects did not exclude physiological changes. They concluded that because of RFR exposure’s increasing ubiquity, urgent attention to potential effects on biodiversity is needed.
The issue of insect size, nonlinearity, and antenna tilt/direction are factors of critical importance with 5G radiation which will create extremely complex near- and- far-field ambient exposures to species in urban and rural environments alike, not only from a densification of small cell antennas close to the ground but also from increased satellite networks circling in low Earth orbits (see Part 1). The range of frequencies used for wireless telecommunication systems will increase from below 6 GHz (2G, 3G, 4G, and WiFi) to frequencies up to 120 GHz for 5G which, due to smaller wavelengths, is therefore a better resonant match for small insects. An alarming study by Thielens et al. [411], drawing on numerous robust studies of RFR’s decades-long use as a thermal insecticide, modeled absorbed RFR in four different types of insects as a function of frequency alone from 2 to 120 GHz. A set of insect models was obtained using novel Micro-CT (computer tomography) imaging and used for the first time in finite-difference time-domain electromagnetic simulations. All insects showed frequency-dependent absorbed power and a general increase in absorbed RFR at and above 6 GHz, in comparison to the absorbed RFR power below 6 GHz. Their simulations showed that a shift of 10% of the incident power density to frequencies above 6 GHz would lead to an increase in absorbed power between 3–370% — a large differential of serious potential consequence to numerous insect species.
Using a similar approach, Thielens et al. [412] focused on the western honey bee (Apis mellifera) with RF-EMF, using a combination of in-situ exposure measurements near bee hives in Belgium and numerical simulations. Around five honey bee models were exposed to plane waves at frequencies from 0.6 to 120 GHz — frequencies carved out for 5G. Simulations quantified whole-body averaged RFR absorbed as a function of frequency and found that the average increased by factors of 16–121 (depending on the specimen) when frequency increased from 0.6 to 6 GHz for a fixed incident electric field strength. A relatively small decrease in absorption was observed for all studied honey bees between 12 and 120 GHz due to interior attenuation. RFR measurements were taken at 10 bee hive sites near five different locations. Results found average total incident RFR field strength of 0.06 V/m; those values were then used to assess absorption and a realistic rate was estimated between 0.1 and 0.7 nW. They concluded that with an assumed 10% incident power density shift to frequencies higher than 3 GHz, this would lead to an RFR absorption increase in honey bees between 390 and 570% — a frequency shift expected with the buildout of 5G.
The two previous studies alone should give pause regarding environmental effects to invertebrates in these higher 5G frequency ranges.
Kumar [413] noted that RFR should be included as causal agents of bee CCD and that test protocols need to be standardized and established. Standardization is critical since many studies conducted with cell phones in hives are of very uneven quality and only indicative of potential effects. Placing cell phones in hives and assuming that RFR is the only exposure is inaccurate and misleading. ELF-EMFs are always present in all telecommunications technology, using pulsed and modulated signals [414]. All of these characteristics have been found to be highly biologically active apart from frequency alone. Such studies are likely capturing ELF effects without identifying them. All aspects of transmission, including transmission engineering itself from towers, need to be considered to determine accurate exposures and delineate causative agents. Vibration and heat must also be considered — cell phones in transmission mode could raise hive temperature quickly and bees are highly temperature sensitive. Due to “waggle dance” specifics in creating foraging “roadmaps,” bees should not be artificially relocated from hives to determine return ability after EMF exposure. They may be confused by relocation alone, adversely affecting their return abilities. Such tests also involve only one stressor when there are multiple stressors on insect species today. Understanding such co-factors is critical in determining accurate data and outcomes [415, 416]. Translating laboratory studies to field relevance has always been problematic but understanding EMF effects to insects has become urgent with ever increasing low-level ambient exposure from devices and infrastructure, especially in light of the new 5G networks being built. There are numerous variables that studies have yet to factor in. All of the above indicates a critical need to standardize experimental protocols and to take electro-ecology far more seriously, especially regarding aerial species in light of 5G.
Aquatic environments
There are fundamental electrical differences in conductivity (how well a material allows electric current to flow) and resistivity (how strongly a material opposes the flow of electric current) between air and water. Through water, EMF propagation is very different than through air because water has higher permittivity (ability to form dipoles) and electrical conductivity. Plane wave attenuation (dissipation) is higher in water than air, and increases rapidly with frequency. This is one reason that RFR has not traditionally been used in underwater communication while ELF has been. Conductivity of seawater is typically around 4 S/m, while fresh water varies but typically is in the mS/m range, thus making attenuation significantly lower in fresh water than in seawater. Fresh water, however, has similar permittivity as sea water. There is little direct effect on the magnetic field component in water mediums; propagation loss is mostly caused by conduction on the electric field component. Energy propagation continually cycles between electric and magnetic fields and higher conduction leads to strong attenuation/dissipation of EMF [98].
Because of these essential medium differences, electroreceptor mechanisms in aquatic species may be very different than those previously described in aerial species since air is a less conductive and resistive medium with less attenuation. That is why RFR travels more easily and directly through air. In aquatic species electroreception may be a result of transmission via water directly to the nervous system through unique receptor channels called Ampullae of Lorenzini [371]. In frogs, amphibians, fish, some worm species and others, receptor channels may be through the skin as well as via mechanisms more common in aerial species such as in the presence of magnetite (see “Mechanisms” above). There can be great variation in electroreceptive sensitivities in species inhabiting the two fundamentally different environments. Some amphibian species, however, have physical characteristics that span both mediums and therefore varied magnetoreception mechanisms.
Amphibians: frogs, salamanders, reptiles: regeneration abilities
Amphibians are the class of animals that include frogs, toads, salamanders, newts, some reptiles, and caecilians. The common term ‘frog’ is used to describe thousands of tailless amphibian species in the Order Anura. There are over 6,300 anuran species recorded thus far, with many more likely disappearing today due to climate change and other factors before we even knew they existed. Informal distinctions are made between frogs (thin-skinned species) and toads (thick, warty skins) but such distinctions are not used for taxonomic reasons. While the greatest concentration of diverse frog species is in tropical rainforests, they are widely found all over the world from the tropics to subarctic regions. Most adult frogs live in fresh water and/or on dry land while some species have adapted to living in trees or underground. Their skin varies in all manner of colors and patterns, from gray/green and brown/black to bright reds/yellows.
Frog skin is smooth and glandular — something of concern given nascent 5G technology (see Part 1) — and can secrete toxins to ward off predators. Frog skin is also semi-permeable which makes them highly susceptible to dehydration and pollutants. With radical weather shifts due to climate change and unpredictable swings between abnormal droughts followed by flooding in previously weather-stable regions, environmentally sensitive amphibians like frogs are considered bell-weather species. Frequently, time may be insufficient for some local/regional species to regenerate in between radical weather cycles, leading to population collapse.
Since the 1950s, there has been a significant decline in frog populations with more than one third of species today considered threatened with extinction while over 120 species are already believed to have gone extinct since the 1980s [10, 417, 418]. This amphibian decline is considered part of an ongoing global mass extinction, with population crashes as well as local extinctions creating grave implications for planetary biodiversity [419]. Amphibian extinction results are from climate change [420], [421], [422]; habitat loss/destruction [423, 424]; introduced species [425]; pollution [426]; parasites [423, 427]; pesticides, herbicides and fungicides [428], [429], [430]; disease [431], [432], [433], [434], [435]; and increased ultraviolet-B radiation [436], [437], [438], [439] among others. Anthropogenic sound pollution may also affect amphibian call rates and therefore impact reproduction [440] and artificial night lights affect male green frog (Rana clamitaus melanota) breeding [441]. Nonionizing electromagnetic fields may also play a role [442].
McCallum [443] calculated that the current extinction rate of amphibians could be 211 times greater than their pre-anthropogenic natural “background extinction” rate with the estimate rising 25,000–45,000 times if endangered species are also included in the computation. Today, declining amphibian populations are seen in thousands of species across numerous ecosystems, including pristine forested areas [418] and declines are now recognized among the most severe impacts of the anthropocene era [417, 442].
In addition, the number of frogs with severe malformations often incompatible with survival has risen sharply. Deformities are a complex issue related to physiology, anatomy, reproduction, development, water quality, changing environmental conditions, and ecology in general. Any time deformities are observed in large segments of wildlife populations there are indications of serious environmental problems [442]. Amphibian malformations are presumed due to an aggressive infectious fungal disease called Chytridiomycosisy, caused by the chytrid fungi Batrachochytrium dendrobatodis and Batrachochytrium salamandrivorans [432], [433], [434], [435], and by parasites like Ribeiroia ondatrae [427]. Chytridiomycosis has been linked to dramatic amphibian declines and extinctions in North, Central, and South America, across sections of Australia and Africa and on Caribbean islands like Dominica and Montserrat. First identified in the 1970s in Colorado, U.S., it continues to spread globally at an alarming rate. Some populations witness sporadic deaths while others experience 100% mortality. There is no effective measure to control the disease in wild populations. Herbicides like glyphosate used in Roundup™ and atrazine, an endocrine disruptor, have also been found to cause severe malformations in both aquatic and land amphibian species from farmland pesticide/herbicide/fungicide runoff [428], [429], [430].
Frogs are known to be highly sensitive to natural and manmade EMF. Much research into the electrophysiology of frogs has been conducted because they are good lab models for human nervous system research, readily available, and easily handled. As far back as 1780, the Italian physicist Luigi Galvani discovered what we now understand to be the electrical basis of nerve impulses while studying static electricity (the only kind then known) when he accidentally made frog leg muscles contract while connected to the spinal cord by two different metal wires [444]. Galvani thought he had discovered "animal magnetism” but had actually discovered direct current and what later became known as a natural “current of injury”— the process by which an injured limb, for instance, produces a negative charge at the injury site that will later turn to a positive charge at the same site in some species as discovered in the 1960s by Robert O. Becker [444], [445], [446], [447], [448], [449], [450], [451]. The earliest curiosity about natural current continued throughout the 1800s on various aspects of EMF and later throughout the 1920s to 1940s in pioneering researchers Elmer J. Lund [452], [453], [454] and Harold Saxon Burr [455], [456], [457] who worked to establish the first unified electrodynamic field theory of life, using hydra, frog, and salamander models among several others because of their morphogenic properties [458]. While frogs do not regenerate limbs the way salamanders do, both are so similar in taxonomy that curiosity was high in the early pioneers cited above throughout the 1960s to 1990s about what fundamentally allowed limb regeneration in one species, by not the other. Much was learned in the process about amphibian electrophysiology and cellular microcurrent in wound healing, as well as the electrophysiological properties of cellular differentiation, and eventually dedifferentiation pertinent to all contemporary stem cell research. Today the implications of this early work have gained new interest and targeted research regarding endogenous microcurrent and limb regeneration potential in humans, as well as dediffentiation/stem cell/morphogenesis in general for cancer treatment and other healing modalities. For a thorough review of studies on morphogenesis see Levin [459].
Ubiquitous low-level ambient EMFs today match some of the natural low-level microcurrent found critical to the fundamental processes of amphibian growth, reproduction, morphogenesis, and regeneration, lending new meaning to the early research that defined amphibian electrophysiology. We just need to make far better use of it to understand what role, if any, today’s ambient exposures may be contributing to amphibian losses. (To compare tables between rising ambient EMF levels and low level effects in wildlife, see Part 1, Supplement 1; and Part 2, Supplement 3.)
Amphibian and reptile magnetoreception
How amphibians perceive natural and manmade EMF is similar to other species reviewed above and for amphibian mechanism reviews see Phillips et al. [460, 461]. Like many bird and insect species, evidence indicates that amphibians perceive the Earth’s geomagnetic fields by at least two different biophysical magnetoreception mechanisms: naturally occurring ferromagnetic crystals (magnetite), and light-induced reactions via specialized photo-receptor cells (cryptochromes) that form spin-correlated radical pairs. Like birds, both mechanisms are present in some amphibians. Cryptochromes provide a directional ‘compass’ and the non-light-dependent magnetite provides the geographical ‘map.’
In a thorough discussion of many magnetoreception studies in anura and urodela species, Diego-Rasilla et al. [462] found evidence that Iberian green frog tadpoles (Pelophylax perezi) had a light-dependent magnetic compass, and Diego-Rasilla et al. [463] also found that tadpoles of the European common frog (Rana temporaria) are capable of using the Earth’s magnetic field for orienting along a learned y-axis. In these studies, they investigated if this orientation is accomplished using a light-dependent magnetic compass similar to that found in the earlier experiments with other species of frogs and newts [460, 462], [463], [464], [465], [466], [467], [468], [469], [470] or from some other factor. They concluded that the magnetic compass provided a reliable source of directional information under a wide range of natural lighting conditions. They also compared their findings to studies [470] that showed the pineal organ of newts to be the site of the light-dependent magnetic compass, as well as to recent neurophysiological evidence showing magnetic field sensitivity located in the frog frontal organ which is an outgrowth of the pineal gland. They hypothesized this work could indicate a common ancestor as long ago as 294 million years.
To determine if orientation using Earth’s magnetic fields changed according to seasonal migration patterns, Shakhparonov and Ogurtsov [471] tested marsh frogs (Pelophylax ridibundus) in the laboratory to see if frogs could determine migratory direction between the breeding pond and their wintering site according to magnetic cues. Adult frogs (n=32) were tested individually in a T-maze 127 cm long inside a three-axis Helmholtz coil system (diameter 3 m). Maze arms were positioned parallel to the natural migratory route and measured in accordance with the magnetic field. Frogs were tested in the breeding migratory state and the wintering state, mediated by a temperature/light regime. Frog choice in a T-maze was evident when analyzed according to the magnetic field direction. They moved along the migratory route to the breeding pond and followed the reversion of the horizontal component of the magnetic field. The preference was seen in both sexes but only during the breeding migratory state. They concluded that adult frogs obtained directional information from the Earth’s magnetic field.
Diego-Rasilla et al. [472] found similar evidence in two species of lacertid lizards (Podarcismuralis and Podarcis lilfordi) that exhibited spontaneous longitudinal body axis alignment relative to the Earth’s magnetic field during sun basking periods. Both species exhibited a highly significant bimodal orientation along the north-northeast and south-southwest magnetic axis. Lizard orientations were significantly correlated over a five-year period with geomagnetic field values at the time of each observation. This suggested the behavior provides lizards with a constant directional reference, possibly creating a spacial mental map to facilitate escape. This was the first study to provide spontaneous magnetic alignment behavior in free-living reptiles although studies of terrapins have also found such spontaneous magnetic alignment [92, 323, 473]. Nishimura et al. [474, 475] also found sensitivity to ELF-EMF sinusoidal 6 and 8 Hz, peak magnetic field 2.6 μT, peak electric field (10 V/m) in a lizard species (Pogona vitticeps) as demonstrated by significant increased tail lifting — a reproductive behavior. Interestingly, this tail-lifting response to ELF-EMF disappeared when the parietal eye was covered, suggesting that the parietal eye contributes to light-dependent magnetoreception and that exposure to ELF-EMFs may increase magnetic-field sensitivity in the lizards. A further experiment [476] showed that light at a wavelength lower than 580 nm was needed to activate the light-dependent magnetoreception of the parietal eye.
Amphibians: RF-EMF
Most frogs spend significant time on land but lay eggs in water where they hatch into tadpoles with tails and internal gills. However, some species bypass the tadpole stage and/or deposit eggs on land. Frogs are thus subject to exposures from both land-based and aquatic environments. A frog’s life cycle is complete when metamorphosis into an adult form occurs. Many adverse effects do not appear until after metamorphosis is completed but problems have been found throughout the entire life cycle after exposures to both ELF-EMF and RFR.
Most early research on frogs (other than the Becker et al. regeneration inquiries noted above) was conducted at high thermal levels rarely encountered in the environment but some are included here because they helped delineate amphibian electrophysiology with effects later supported in low-level research. Some early work did use frog models to investigate cardiac effects with lower intensity exposures. Levitina [477] found that intact frog whole-body exposure caused a decrease in heart rate, while irradiation of just the head caused an increase. Using VHF frequency RFR at a power density of 60 μW/cm2, A=12.5 cm, Levitina attributed the cardiac changes to peripheral nervous system effects but according to Frey and Siefert [478], because of the wavelengths used in that study, little energetic body penetration would be expected. They said a skin receptor hypothesis was therefore reasonable.
Following on Levitina’s work, Frey and Seifert [478] — using isolated frog hearts, UHF frequencies that penetrate tissue more efficiently and low intensity pulse modulation — found that pulsed microwaves at 1,425 GHz could alter frog heart rates depending on the timing of exposure between the phase of heart action and the moment of pulse action. Twenty-two isolated frog hearts were irradiated with pulses synchronized with the P-wave of the ECGs; pulses were of 10 s duration triggered at the peak of the P-wave. Two control groups were used without RFR exposures with no effects noted. They found heart rate acceleration occurred with pulsing at about 200 ms after the P-wave. But if the pulse occurred simultaneously with the P-wave, no increases were induced. Arrhythmias occurred in half the samples, some resulting in cardiac cessation. Clearly from this study, RFR affected frog heart rhythm and could cause death.
A more recent work by Miura and Okada [479] found severe vasodilation in frog foot webs from RFR. In a series of three experiments using 44 anesthetized frogs (X. laevis) at thermal and non-thermal intensities, researchers exposed foot webs to pulsed RFR in three parameters with the monitor coil set at 1 V peak-to-peak: 100 kHz 582-3 mG and 174.76 V cm− 1; 10 MHz 7.3 mG and 2.19 V cm− 1; 1 MHz 539 mG and 16.11 V cm− 1. They found not only dilated arterioles of the web which had already been re-constricted with noradrenaline, but also dilated arterioles under non-stimulated conditions. Vasodilatation increased slowly and reached a plateau 60 min after radiation’s onset. After radiation ceased, vasodilation remained for 10–20 min before slowly subsiding. Vasodilation was optimum when pulsation was applied 50% of the total time at a 10 kHz burst rate at 10 MHz. Effects were non-thermal. The pattern of vasodilation induced by warm Ringer solution was different from the vasodilatory effect of weak RFR, involving the level of intracellular Ca2+. They hypothesized that since Ca2+ ATPase is activated by cyclic GMP which is produced by the enzymatic action of guanylate cyclase, RF-EMF may activate guanylate cyclase to facilitate cyclic GMP production. They concluded the study indicates for the first time that RFR dilates peripheral resistance vessels by neither pharmacological vasodilator agents nor physical thermal radiation, but that the precise mechanisms of activation of guanylate cyclase by RFR at the molecular level required further study. Vasodilation and constriction affects every part of the body and can affect all organ systems.
Prior to this, Schwartz et al. [480] found changes in calcium ions in frog hearts in response to a weak VHF field that was modulated at 16 Hz. This would be an exposure common in the environment. Calcium ions are critical to heart function.
Balmori [24], [25], [26], [27], [28], [29], [30, 442] and Balmori and Hallberg [271] have focused widely on EMF effects to wildlife, with two papers on amphibians. Balmori [442], in a review, noted that RFR in the microwave range is a possible cause for deformations and decline of some amphibian populations, and Balmori [481] in 2010 found increased mortality in tadpoles exposed to RFR in an urban environment. In the 2010 study, tadpoles of the common frog (Rana temporaria) were exposed to RFR from several mobile phone towers at a distance of 459 ft (140 m). Two month exposures lasted through egg phase to advanced tadpole growth prior to metamorphosis. RF and MW field intensity between 1.8 and 3.5 V/m (0.86–3.2 μW/cm2) were measured with three different devices. Results determined that the exposed group (n=70) had low coordination of movements and asynchronous growth that resulted in both large and small tadpoles, as well as a disturbing 90% high mortality rate. In the control group (n=70) a Faraday cage was used under the same conditions. Controls found movement coordination to be normal and development synchronous with mortality rate at a low 4.2%. These results indicated that RFR from cell towers in a field situation could affect both development and mortality of tadpoles. Prior to this study, Grefner et al. [482] also found increased death in tadpoles (Rana temporaria L.) exposed to EMF, as well as higher mortality rates, and slower less synchronous development.
Mortazavi et al. [483] found changes in muscle contractions in frogs exposed to 900-MHz cell phone radiation for 30 min; gastrocnemimus muscles were then isolated and exposed to a switched on/off mobile phone radiation for three 10-min intervals. The authors reported RFR-induced effects on pulse height and latency period of muscle contractions. SARs of the nerve-muscle preparation were calculated to be 0.66 (muscle) and 0.407 (nerve) W/kg.
Rafati et al. [484] investigated the effects of RFR on frogs from mobile phone jamming equipment emitting RFR in the same frequencies as mobile phones. (Although illegal in many countries, jammers are nevertheless used to interfere with signals and stop communication.) The study sought to follow up on reports of non-thermal effects of RFR on amphibians regarding alterations of muscle contraction patterns. They focused on three parameters: the pulse height of leg muscle contractions, the time interval between two subsequent contractions, and the latency period of frog’s isolated gastrocnemius muscle after stimulation with single square pulses of 1 V (1 Hz). Animals in the jammer group were exposed to RFR at a distance of 1 m from the jammer’s antenna for 2 h while the control frogs were sham exposed. All were then sacrificed and isolated gastrocnemius muscles were exposed to on/off jammer radiation for three subsequent 10 min intervals (SAR for nerve and muscle of the different forms of jammer radiation was between 0.01 and 0.052 W/kg). Results showed that neither the pulse height of muscle contractions nor the time interval between two subsequent contractions were affected, but the latency period (time interval between stimulus and response) was statistically significantly altered in the RFR-exposed samples. They concluded the results supported earlier reports of non-thermal effects of EMF on amphibians including the effects on the pattern of muscle contractions. Control sham exposed samples showed no effects.
Amphibians, reptiles: ELF-EMF
Amphibians are highly sensitive to ELF-EMF. An early-1969 study by Levengood [485] using a magnetic field probe found increased high rates of teratogenesis in frogs (Rana sylvatica) and salamanders (Ambystoma maculatum). Two identical probes using different field strengths were employed — both operated in the kilogauss region with high field gradients. Amphibian eggs and embryos were exposed at various stages of development with gross abnormalities found in developing larvae vs. control. At the hatching stage severe abnormalities were noted in both anuran and urodele larvae from probe-treated eggs. Hatching abnormalities included microcephaly, altered development, and multiple oedematous growths. In probe-treated frogs there was a delay in the appearance of a high percentage of malformations until the climax stage of metamorphosis. Until that stage, the larvae were of the same appearance as control specimens, thus camouflaging the damage after just a brief treatment of early embryos. The frog abnormalities at metamorphosis differed from those in the hatching tadpoles and consisted mainly of severe subepidermal blistering and leg malformations including formation of multiple deformed limbs incompatible with life. Over 90% of the morphological alterations at metamorphosis climax were also found to be associated with deformed kidneys. The gastrula stages of development appeared to be the most sensitive in the delayed-effects category. While this was a high-field exposure experiment, it is an intensity that is found in some environments today especially near high tension lines and in abnormal ground current situations.
Neurath [486] also found strongly inhibited early embryonic growth of the common leopard frog (Rana pipiens) by a high static magnetic field with a high gradient (1T) — an exposure sometimes found in the environment — while Ueno and Iwasaka [487] found abnormal growth and increased incidence of malformations in embryos exposed to magnetic fields up to 8T but exposures that high are typically near industrial sites and rarely found in nature.
Severini et al. [488] specifically addressed whether weak ELF magnetic fields could affect tadpole development and found delayed maturation in tadpoles. Two cohorts of X. laevis laevis (Daudin) tadpoles were exposed for 60 days during immaturity to a 50 Hz magnetic field of 63.9–76.4 μT rms (root mean square, average values) magnetic flux density in a solenoid. Controls were two comparable cohorts remotely located away from the solenoid. The experiment was replicated three times. Results showed reduced mean developmental rate of exposed cohorts vs. controls (0.43 vs. 0.48 stages/day, p< 0.001) beginning from early larval stages; exposure increased the mean metamorphosis period of tadpoles by 2.4 days vs. controls (p < 0.001); and during the maturation period, maturation rates of exposed vs. control tadpoles were altered. No increases in mortality, malformations, or teratogenic effects were seen in exposed groups. The researchers concluded that relatively weak 50 Hz magnetic fields can cause sub-lethal effects in tadpoles via slowed larval development and delays in metamorphosis. Such exposures are found in the environment today in some locations and even though the changes were small, coupled with climate change, such sub-lethal effects may impact some wildlife populations in some environments.
In similar followup work, Severini and Bosco [489] found sensitivity to small variations of magnetic flux density (50 Hz, 22-day continuous exposure, magnetic flux densities between 63.9 and 76.4 µT) in tadpoles exposed to a stronger field vs. controls exposed to a weaker field. A significant delay in development of 2.5 days was found in exposed vs. controls. They concluded the delay was caused by the slightly different magnetic flux densities with results suggesting a field threshold around 70 µT in controlling the tadpole developmental rate.
Schlegel in 1997 found European blind cave salamanders (Proteus anguinus) and Pyrenean newts (Euproctus asper) to be sensitive to low level electric fields in water [490]. And Schlegel and Bulog [491] in followup work found thresholds of overt avoidance behavior to electric fields as a function of frequency of continuous sine-waves in water. Nine salamanders from different Slovenian populations of the urodele (P. anguinus) that included three specimens of its ‘black’ variety (P. anguinus parkelj) showed thresholds between 0.3 mV/cm (ca 100 nA/cm2) and up to 2 mV/cm (670 nA/cm2), with the most reactive frequencies around 30 Hz. Sensitivity included a total frequency range below 1 Hz (excluding DC) up to 1–2 kHz with up to 40 dB higher thresholds. These are ranges that may be found in the wild near high tension lines and utility grounding practices near water, by some underwater cabling, and by some RFR transmitters.
Landesman and Douglas in 1990 [492] found some newt species showed accelerated abnormal limb growth when pulsed electromagnetic fields were added to the normal limb regeneration process. While normal limb regeneration found normal regrowth patterns in 72% of specimens, 28% were abnormal. Abnormalities included loss of a digit, fused carpals, and long bone defects which occurred singly or in combination with one another. When exposure to a PEMF was added for the first 30 days postamputation, followed by a 3–4 month postamputation period, a group of forelimbs with unique gross defects increased by an additional 12%. Defects (singly or in combination) included the loss of two or more digits with associated loss of carpals, absence of the entire hand pattern, and abnormalities associated with the radius and ulna. The researchers offered no explanation. Exposure intensities were similar to those used to facilitate non-juncture fracture healing in humans.
Komazaki and Takano in 2007 [493] found accelerated early development growth rates with 50 Hz, 5–30 mT alternating current exposures in the fertilized eggs of Japanese newts (Cynops pyrrhogaster). The period of gastrulation was shortened via EMF-promoted morphogenetic cell movements and increased [Ca2+]i. They said their results indicated that EMF specifically increased the [Ca2]i of gastrula cells, thereby accelerating growth. This study only observed through the larval stages and they did not see any malformations under EMF exposures, which they attributed to possible differences in the intensity and mode of EMF.
With amphibians and some reptiles demonstrating high sensitivity to natural background EMF for important breeding and orientation needs, amphibians living in aquatic, terrestrial, and aerial environments (i.e. tree frog species) may be affected from multi-frequency anthropogenic EMF in ways we do not fully understand. There are potential effects — especially from 5G MMW that couple maximally with skin — to all aspects of their development and life cycles, including secondary effects.
Fish, marine mammals, lobsters, and crabs
Aquatic animals are exquisitely sensitive to natural EMF and therefore potentially to anthropogenic disturbance. The Earth’s dipole geomagnetic field yields a consistent though varying source of directional information in both land and aquatic species for use in homing behavior, orientation during navigation and migration. This information is used both as a ‘map’ for positional information as well as a ‘compass’ for direction [494], [495], [496], [497]. Aquatic species are known to be sensitive to static geomagnetic fields, atmospheric changes and sunspot activities [498]. For recent comprehensive reviews on magnetic field sensitivity in fish and effects on behavior, see Tricas and Gill [36] and Krylov et al. [33]. Some biological ‘magnetic maps’ may be inherited [499]. And for a recent extensive discussion of the Earth’s natural fields and magnetoreception in marine animals with a focus on effects from electromagnetic surveys that use localized strong EMFs to map petroleum deposits under seabeds, see Nyqvist et al. [498] and below.
As mentioned above, because of the difference in conductivity of water and other factors, the way some aquatic species sense EMF may rely on unique modes of physiological perception, as well as those employed by terrestrial animals. There may also be sensory combinations not yet understood in some aquatic and semi-aquatic species. For instance, what role does the neural conductivity of whiskers (vibrissae) in seals, sea lions and walrus play other than for food finding? Aquatic species’ dense network of whiskers is larger with greater blood flow than terrestrial species and can contain 1,500 nerves per follicle vs. cats at 200 per follicle. Seal whiskers also vary geometrically from terrestrial species and the largest part of the seal brain is linked to whisker function. Seals use whiskers to map the size, shape and external structure of objects and can find prey even when blindfolded. Their whiskers are also sensitive to weak changes in water motion [100]. But are they also using them as a location or directional compass in relation to the geomagnetic field? That has yet to be studied.
Unique sensory differences in aquatic species have long been documented. Joshberger et al. [500] noted that in 1,678 Stefano Lorenzini [501] was the first to describe a network of organs in the torpedo ray that became known as the Ampullae of Lorenzini (AoL). Its purpose was unknown for 300 years until Murray [502] measured AoL’s electrical properties in elasmobranch fish — sharks, rays and skates. Later work [101, 503], [504], [505], [506], [507], [508] confirmed and greatly added to this knowledge. Researchers now know that AoL is likely the primary mechanism that allows elasmobranch fish to detect and map a potential prey’s physiology via the very weak changes in electric fields given off by prey’s muscle contractions.
Individual ampullae are skin pores that open to the aquatic environment with a jelly-filled canal leading to an alveolus containing a series of electrosensing cells. Within the alveolus, the electrosensitive cells of the ampullae communicate with neurons and this integration of signals from multiple ampullae is what allows elasmobranch fish to detect electric field changes as small as 5 nV/cm [503, 506, 509, 510]. The AoL jelly has been reported as a semiconductor with temperature-dependence conductivity and thermoelectric behavior [500, 509, 510], as well as a simple ionic conductor with the same electrical properties as the surrounding seawater [503, 506]. Josberger et al. [500] attempted to clarify what AoL’s role is in electrosensing by measuring AoL’s proton conductivity. They found that room-temperature proton conductivity of AoL jelly is very high at 2 ± 1 mS/cm — only 40-fold lower than some current state-of-the-art manmade proton-conducting polymers. That makes AoL the highest conductive biological material reported thus far. They suggested that the polyglycans contained in the AoL jelly may contribute to its high proton conductivity.
Other aquatic magneto-sensory mechanisms more in harmony with terrestrial animals include the presence of ferromagnetic particles in magnetite — tiny naturally produced magnets that align with the Earth’s magnetic field, allowing for species’ direction and orientation. Magnetite appears to transmit necessary information through a connection with the central nervous system [340, 497, 511]. A magnetite-based system is plausible for cetaceans [512, 513] as magnetite has been found in the meninges dura mater surrounding the brains of whales and dolphins [514, 515]. There is also evidence that local variations/anomalies in the geomagnetic field in certain underwater topographies may play a role in live cetacean strandings [516, 517] which indicates a magnetic compass based on magnetite. And free-ranging cetaceans have shown evidence of magnetoreception-based navigation, e.g., Fin whale migration routes have been correlated with low geomagnetic intensity [513].
Recently, Granger et al. [518] found correlations in data between 31 years of gray whale (Eschrichtius robustus) strandings and sunspot activity, especially with RF ‘noise’ in the 2,800 MHz range. The 11-year sunspot cycle strongly correlates with the intense releases of high-energy particles known as solar storms which can temporarily modify the geomagnetic field, and in turn may modify orientation in magnetoreceptive species. Solar storms also cause an increase in natural broadband RF ‘noise’. They examined changes in both geomagnetic fields and RF ‘noise’ and found RF to be a determinant. Further, they hypothesized that increased strandings during high solar activity is more likely due to radical pair mechanisms which are more reactive with RFR than magnetite, which appears more reactive to ELF-EMF. Two previous studies also found correlations with cetacean strandings and solar activities [519, 520]. Both mechanisms may come into play under different circumstances or act in synergy.
Kremers et al. [512] investigated the spontaneous magnetoreception response in six captive free-swimming bottlenose dolphins (Tursiops truncates) to introduced magnetized and demagnetized devices used as controls. They found a shorter latency in dolphins that approached the device containing a strong magnetized neodymium block compared to a control demagnetized block identical in form and density and therefore indistinguishable with echolocation. They concluded that dolphins can discriminate on the basis of magnetic properties — a prerequisite for magnetoreception-based navigation. Stafne and Manger [521] also observed that captive bottlenose dolphins in the northern hemisphere swim predominantly in a counter-clockwise direction while dolphins in the southern hemisphere swim predominantly in clockwise direction. No speculation was offered for this behavior.
How salmon navigate vast distances — from their hatching grounds in freshwater river bottoms to lakes during juvenile growth, then the open ocean during maturity, and with a final return to their neonatal birthing grounds to spawn and die (for most anadromous salmonids) — has fascinated researchers for decades. Research indicates they may use several magneto-senses to accomplish this, including inherited mechanisms [522], imprinting [499, 522], a magnetic compass [499, 522, 523], and biomagnetic materials. Salmon have been found to have crystal chains of magnetite [524]. One recent study found that strong magnetic pulses were capable of disrupting orientation in salmon models [525], indicating a magnetite-based mechanism. In salmon, the migration process is complicated by the fact that the ability to sense geomagnetic fields can be altered by changes in salinity between fresh and salt water, thus pointing to multi-sensory mechanisms [499].
Speculation that salmon use the geomagnetic field in some capacity for their iconic migration goes back decades [526]. Quinn [527] found evidence that sockeye salmon (Oncorhynchus nerka) frey use both a celestial and magnetic compass when migrating from river hatching to lakes. Putman et al. [499], who have written extensively on this subject, focused on how salmon navigate to specific oceanic feeding areas — a challenge since juvenile salmon reach feeding habitats thousands of kilometers from natal locations. The researchers experimentally found that juvenile Chinook salmon (Oncorhynchus tshawytscha) responded to magnetic fields similar to latitudes of their extreme ocean range by orienting in directions that would lead toward their marine feeding grounds. They further found that fish use the combination of magnetic intensity and inclination angle to assess their geographic location and concluded that the magnetic map of salmon appears to be inherited since the fish had no prior migratory experience. These results, paired with findings in sea turtles (see below), indicate that magnetic maps are widespread in aquatic species and likely explain the extraordinary navigational abilities seen in long-distance underwater migrants [499].
It is less likely that light-sensing radical pair cryptochromes play much of a role in aquatic species though some hypothesize the possibility [528]. Krylov et al. [33], however, noted that there are no anatomical structures or neurophysiological mechanisms presently known for radical pair receptors in the brains of fish and that since light decreases with water depth and fish are capable of orienting in complete darkness using the geomagnetic field, their opinion was that it is too early to say fish have magnetoreception mechanisms based on free radicals, light-dependent or otherwise.
Fish, lobsters, crabs: ELF-EMF
For several reasons having to do with differences in conductivity in water vs. air (see above), RFR is of far less concern in aquatic environments at present than is ELF. With the ever-increasing number of underwater cables used for everything from transcontinental data/communications to power supplies for islands, marine platforms, underwater observatories, off-shore drilling, wind facilities, tidal and wave turbines among others, many new sources of both AC and DC electric current are being created in sea and freshwater environments alike. According to Ardelean and Minnebo writing in 2015 [529], almost 4,971 mi (8,000 km) of high voltage direct current (HVDC) cables were present on the seabed worldwide, 70% of which were in European waters, and this is only expected to grow dramatically as new sources of renewable energy are built to replace fossil fuels globally.
Curiosity about potential adverse effects from cable-generated ELF-EMF on all phases of fish life has also grown, especially in benthic and demersal species that spend significant time near cables in deeper bottom environments for egg laying, larvae growth, and development for most, if not all, of their adult lives.
Fey et al. [494, 495] and Öhman et al. [530] noted that there are two types of anthropogenic exposures created by cables: high voltage direct current (HVDC) that emits static magnetic fields, and three-phase alternating current (AC power transmission) that emit time-varying electromagnetic fields. The density of electric current near underwater cables on the sea floor can vary significantly depending on the type of cable and whether they are positioned on the sea bottom or buried [36, 530]. Noticeable magnetic field changes can occur within meters but generally not more than several meters from the cable. However, Hutchinson et al. [531], in a robust field study and extensive review, found surprisingly stronger and more complex exposures than anticipated (see below).
Since fish are highly sensitive to static magnetic fields (MF), it is important to delineate static fields from anthropogenic alternating current EMF in aquatic studies. In freshwater species under laboratory conditions, Fey et al. [494] found similar results to those of salmon studies (noted above) in northern pike (Esox lucius) exposed to a static magnetic field from DC cables (10 mT) during the embryonic phase and in the first six days of post-hatching. No statistically significant MF effect was seen on hatching success, larvae mortality, larvae size at hatching, and growth rate during the first six days of life. However, significant MF effects were seen on hatching time (one day earlier in a magnetic field than in control), yolk-sac size was smaller, and yolk-sac absorption rate was faster. They interpreted the faster yolk-sac absorption in a magnetic field as an indication of increased metabolic rate but added that even if some negative consequences were expected as a result, that the actual risk for increased northern pike larvae mortality seemed negligible. Though higher than 10 mT magnetic field values are hazardous for fish larvae, they added such values do not occur in the natural environment even along underwater cables.
But in follow-up work of longer duration the same general research group reached a different conclusion. Fey et al. [495] studied effects on eggs and larvae of rainbow trout (Oncorhynchus mykiss) exposed to a static magnetic field (MF) of 10 mT and a 50 Hz EMF of 1 mT for 36 days (i.e., from eyed egg stage to approximately 26 days post hatching). They found that while neither the static MF nor the 50-Hz EMF had significant effects on embryonic/larval mortality, hatching time, larval growth, or the time of larvae swim-up from the bottom, both fields did however enhance the yolk-sac absorption rates. While they said this was not directly related to a MF effect, it was shown that larvae with absorbed yolk-sacs by the time of swim-up were less efficient in taking advantage of available food at first feeding and gained less weight. They concluded that these exposures could negatively affect the yolk-sac absorption rate thereby hampering fish in important feeding activities needed for fast weight gain and increased survival. In an additional study, Fey et al. [532] observed that rainbow trout reared in a laboratory for 37 days and exposed to a static MF (10 mT) or a 50-Hz EMF (1 mT) showed defects in otolith of the inner ear which is responsible for hearing and balance in fish. The authors concluded that underwater construction and/or cables that emit a MF of 10 mT or higher can affect living organisms within a few meters distance, especially species like trout in settled life stages on the sediment bottom during early development.
Zebrafish (Danio rerio) are often used in EMF research in toxicology and developmental biology investigating effects on humans because the genomes are so similar. Li et al. [533] studied ELF-MF on the development of fertilized zebrafish embryos divided into seven groups. Embryos of experimental groups were continuously exposed to 50-Hz sinusoidal MF with intensities of 30, 100, 200, 400, or 800 μT for 96 h. The sham group was identical but without ELF-MF exposure. Results showed that ELF-MF caused delayed hatching and decreased heart rate at early developmental stages but no significant differences were seen in embryo mortality or abnormality. Acridine orange staining assays showed notable signs of apoptosis in the ventral fin and spinal column and transcription of apoptosis-related genes (caspase-3, caspase-9) was significantly up-regulated in ELF-MF-exposed embryos. They concluded that ELF-EMF demonstrated detrimental effects on zebrafish embryonic development, including on hatching, decreased heart rate, and induced apoptosis, although such effects were not a mortal threat. The lower range exposures of this study are found in some aquatic environments.
Sedigh et al. [534] investigated effects on zebrafish exposed to static magnetic fields. Exposures of 1-week acute and 3-week subacute exposures to different static magnetic fields at 2.5, 5, and 7.5 mT were measured on stress indices (cortisol and glucose), sex steroid hormones (17β-estradiol and 17-α hydroxy progesterone) and fecundity. They found a significant change in cortisol, glucose, 17β-estradiol (E 2) and 17-α hydroxy progesterone (17-OHP) levels with increased intensity and duration of exposure and concluded that static magnetic fields at higher intensities showed harmful effects on the reproductive biology of zebrafish during both acute and subacute exposures.
Recent laboratory research by Hunt et al. [535] used the transparent glass catfish (Kryptopterus vitreolus) found in slow moving waters in Southeast Asia as a model to investigate magnetoreception. The study used Y-maze chambers, animal tracking software and artificial intelligence techniques to quantify effects of magnetic fields on the swimming direction of catfish. They placed a permanent Neodymium Rare Earth Magnet (11.5 × 3.18 × 2.2 cm) with a horizontal magnetic flux of 577 mT at the magnet’s surface at 10 cm from the end of one of the Y-maze arms and found that catfish consistently swam away from magnetic fields over 20 μT. The catfish also showed adaptability to changing magnetic field direction and location. The magnetic avoidance was not influenced by school behavior. Sham exposures produced no avoidance. Such exposures might be found near some underwater cables.
To further elucidate findings of species reactions near underwater cables and fill in knowledge gaps since the 2011 Tricas and Gill review [36], Hutchinson et al. [531] conducted both field and laboratory modeling studies of both AC and DC fields on the American lobster (Homarus americanus) and the little skate (Leucoraja erinacea). They noted that in previous studies, while behavioral responses had been seen, findings were unable to determine if significant biological effects (e.g., population changes) occurred. The American lobster was modeled because it is a magnetosensitive species [536] and concern existed that EMF from cables might restrict movements and/or migration. Lobsters may migrate up to 50 mi (80 km) one way from deep waters to shallow breeding grounds. The little skate was used as a model for the most electro-sensitive taxa of the elasmobranchs, which may be attracted by/to the EMF of cables, particularly for benthic species, thereby altering their foraging or movement behavior. Both models were therefore thought indicative of potential EMF impacts. In this robust field study, the researchers found that the American lobster exhibited a statistically significant but subtle change in behavioral activity when exposed to the EMF of the HVDC cable (operated at a constant power of 330 MW at 1,175 Amps). The little skate exhibited a strong behavioral response to EMF from a cable powered for 62.4% of the study with the most frequently transmitted electrical current at 16 Amps (at 0 MW, 37.5% of time), 345 Amps (100 MW, 28.6%) and 1,175 Amps (330 MW, 15.2%). They concluded that for both species, the behavioral changes have biological relevance regarding how they will move around and are distributed in a cable-EMF zone, but they noted that the EMF did not constitute a barrier to movements across the cable for either species.
Of interest in this study were the actual field readings near cables. Unexpected significant AC magnetic and electric fields did not match computer models and were observed to be associated with both of the DC power cables studied. The maximum observed AC values along the cable axis were 0.15 μT and 0.7 mV/m for the magnetic and electric fields respectively for one cable, and 0.04 μT and 0.4 mV/m respectively, for the other cable. Also, the cross section of the EMF peaks exhibited by the DC subsea power cables were broader than anticipated at both studied. The DC and AC magnetic fields reached background levels on either side of the cable on a scale of c.a.5 and 10 m from the peak observed value respectively, whereas the AC electric fields reached background on a scale of 100 m (328 ft) from the peak value. Peak observed values occurred almost directly above the cable axis location; there was an offset of 3.3 ft (<1 m) where the cable was twisted. The researchers noted that this observation of AC fields, with broad areas of EMF distortion being associated with DC cables, increased the complexity of interpreting the studies of EMF’s biological effects from DC cables. The AC electric fields associated with the AC sea2shore cable (1–2.5 mV/m) were higher than the unanticipated AC electric fields produced by the DC cables (0.4–0.7 mV/m). The magnetic field produced by the AC sea2shore cable (range of 0.05–0.3 μT) was ∼10 times lower than modeled values commissioned by the grid operator, indicating that the three-conductor twisted design achieves significant self-cancellation. This entire aspect of the study indicates the need for accurate field assessment, not just computer modeling, and well-designed systems since anomalies occur.
Nyqvist et al. [498] in a thorough review, focused on marine mammals and the use of underwater electromagnetic surveys that map petroleum deposits in seabeds via strong induced EMFs in varied directional applications. They found that EMFs created during such active surveying were within the detectable ranges of marine animals and the fields can potentially affect behavior in electro-perceptive species, but they noted that effects should be limited to within a few kilometers as the electric and magnetic fields created attenuate rapidly. They added that in migrating marine animals, exposures are of short duration and most are close to naturally occurring levels but cautioned that lack of studies is a concern, especially for the most sensitive elasmobranchs at highest risk for disturbance to electric fields. They also noted that with induced magnetic fields, animals using magnetic cues for migration or local orientation during certain time-windows for migration, orientation, or breeding, could be most affected by this surveying technology.
Taorimina et al. [537] studied both static and time-varying magnetic fields on the behavior of juvenile European lobsters (Homarus gammarus). Using two different behavioral assays, day-light conditions to stimulate sheltering behavior and exposures to an artificial magnetic field gradient (maximum intensity of 200 μT), they found that juvenile lobsters did not exhibit any behavioral changes compared to non-exposed lobsters in the ambient magnetic field. No differences were noted on the lobsters’ ability to find shelter or modified their exploratory behavior after one week of exposure to anthropogenic magnetic fields (225 ± 5 μT) which remained similar to behavior in controls. They concluded that neither static nor time-varying anthropogenic magnetic fields at those intensities significantly impacted the behavior of juvenile European lobsters in daylight conditions, but they noted that evidence exists showing magnetosensitivity changes during different life stages in lobster species, and that since their modeling was on juveniles, their study was therefore an incomplete picture requiring further study.
Scott et al. [538] focused on ELF-EMF effects on commercially important edible/brown crab species (Cancer pagurus) and what they found was startling. In laboratory tanks, they simulated EMF (with Helmholtz coils, 2.8 mT evenly distributed, assessments during 24 h periods) that would be emitted from sub-sea power cables now commonly used at offshore renewable energy facilities. They measured stress related parameters (l-lactate, d-glucose, haemocyanin and respiration rate) along with behavioral and response parameters (antennal flicking, activity level, attraction/avoidance, shelter preference and time spent resting/roaming). They found that although there was no EMF effect on haemocyanin concentrations, respiration rate, activity level or antennal flicking rate, there were significant changes in haemolymph l-lactate and d-glucose natural circadian rhythms, indicating alterations in hormones. Crabs also showed an unusually high attraction to EMF-exposed shelter areas (69%) compared to control shelter areas (9%) and significantly reduced their time roaming by 21%, with adverse implications for food foraging, mating, and overall health. They noted that EMF clearly altered behavior. Crabs spent less time roaming around the tank and more time in a shelter in direct contact with the EMF source, indicating natural roaming/food-or-mate-seeking behavior had been overridden by attraction to EMF. In fact, crabs consistently chose an EMF-exposed shelter over a non-exposed one and were always drawn to the EMF. The results appear to predict that in benthic areas surrounding EMF-emitting cables, there will be an increase in the abundance of Cancer pagurus present. They noted that such potential crab aggregation around benthic cables and the subsequent physiological changes in l-lactate and d-glucose levels caused by EMF exposure, is a concern regarding feeding rates, mating, and especially egg incubation directly in increased EMF environments. They concluded that long term investigations are needed regarding chronic EMF exposure, especially on egg development, hatching success and larval fitness, and added that EMF emitted in marine environments from renewable energy devices must be considered as part of the study of cumulative impacts during the planning stages.
Clearly ELF-EMF can affect myriad aquatic species at intensity levels found in proximity to underwater cables at environmental intensities.
Fish: RF-EMF
As mentioned, RFR is of minimal environmental concern for fish since aquatic environments, while highly conductive mediums, also highly attenuate EMF at higher frequencies. This may change in the near future as new technologies now exist that may surpass these obstacles [98], thereby introducing for the first time novel new RFR exposures underwater. Longer wave wireless ELF with expanded ranges are used in anthropogenic sonar (sound navigation ranging), primarily for military applications. These travel easily through water and are known to adversely affect cetaceans and other species that rely on their natural sonar for communication, migration, reproduction and food finding. But sound waves are not considered “EMF” in the strict sense of the term; since the focus of this paper is EMF, sound waves are tangential here. But acoustic damage, especially to cetaceans from military and commercial applications, is well documented and ELF cables used for underwater military submarine communications can have significant EMF exposures near cables. Just because this paper does not address impacts from sound waves in detail does not mean they are without serious effects.
There are, however, three recent studies of RFR on zebrafish included here because it is plausible that such exposures could exist near shallow aquatic environments under some circumstances. Nirwane et al. [539] studied 900-MHz GSM RFR effects on zebrafish (D. rerio) neurobehavioral changes and brain oxidative stress as a model for human exposures to cell phones. Exposures were applied daily for 1 h, 14 days, with SAR 1.34 W/Kg. They found 900-MHz GSM radiation significantly decreased socialization and increased anxiety as demonstrated by significant increased time spent in bottom areas, freezing behaviors, and duration and decreased distance travelled, as well as decreased average velocity and number of entries to the upper half of the tank. Exposed zebrafish spent less time in the novel arm of a Y-Maze indicating significant impaired learning compared to the control group. Exposure also decreased superoxide dismutase (SOD) and catalase (CAT) activities while increased levels of reduced glutathione (GSH) and lipid peroxidation (LPO) were encountered indicating compromised antioxidant defense. Post-exposure treatment with melatonin in the water, however, significantly reversed the induced neurobehavioral and oxidative changes.
Piccinettia et al. [540] investigated in vivo effects on embryonic development in zebrafish at 100 MHz thermal and nonthermal intensities via a multidisciplinary protocol. Results found 100 MHz RFR affected embryonic development from 24 to 72 h post fertilization in all the analyzed pathways. Most notably at 48 h post fertilization, reduced growth, increased transcription of oxidative stress genes, onset of apoptotic/autophagic processes and a modification in cholesterol metabolism were seen. EMF affected stress by triggering detoxification mechanisms. At 72 h post fertilization, fish partially recovered and reached hatching time comparable to controls. The researchers concluded that EMF-RFR unequivocally showed in vivo effects at non-thermal levels.
Dasgupta et al. [541] used embryonic zebrafish models at 3.5 GHz SAR ≈ 8.27 W/kg and exposed developing zebrafish from 6 to 48 h post fertilization, then measured morphological and behavioral endpoints at 120 h post fertilization. Results found no significant impacts on mortality, morphology or photomotor response but noted a modest inhibition of startle response suggesting some levels of sensorimotor disruptions. They concluded that exposures at low GHz levels are likely benign but nevertheless entailed subtle sensorimotor effects. Such effects can affect fish survival in various ways, including inhibited response time to predators, among others. This study was done with an eye toward potential human bioeffects at frequencies used in 4 and 5G technology. It was also conducted at intensities higher than the focus of this paper.
If new technology overcomes the conductivity/attenuation limitations of aquatic environments and introduces more RFR to aquatic species, studies like those cited above may soon have more environmental relevance, even at higher intensities than explored here.
Turtles
Oceanic sea turtle migration joins that of other renowned long-distance migratory species like salmon and over-land monarch butterfly treks, spanning thousands of kilometers and traversing multiple complex environments throughout their life cycles. Sea turtles have long been known to use geomagnetic fields for orientation [542, 543]. Freshwater species (e.g., Chelydra serpentina) have also been shown to have a magnetic sense capable of artificial disruption [92] as do terrestrial box turtles (Terrapene carolina; [544]).
Sea turtles demonstrate natal homing behavior — the ability to return over great distances to their exact birth location to reproduce [89] and because of anthropogenic disruptions of nesting grounds along beaches, this reproductive homing drive imperils them today. The underlying mechanism is still imperfectly understood but involves ‘imprinting’ of the intensity and inclination angle of the geomagnetic field at the birth location [545]. The information is then later used in maturity to return to their place of origin.
Sea turtles are by far the most studied models for turtle magnetoreception, especially by the Lohmann Laboratory at the University of North Carolina, U.S. [323, 546], [547], [548], [549], [550], [551], [552], [553], [554], [555], [556], [557], [558].
Irwin and Lohmann [559] discussed the advantages and disadvantages of various research approaches used to investigate magnetic orientation behavior in turtles. These include the use of large magnetic coil systems in laboratory settings to generate relatively uniform fields over large areas [560] which allow the magnetic field to be artificially altered and carefully controlled to determine changes in behavioral orientation. This approach, however, is unsuited for manipulating exposures around animals in natural environments or for studying localized body magnetoreceptors, which in turtles are still a mystery. Another approach is to attach a small magnet or electromagnetic coil to an animal to disrupt magnetic orientation behavior — a far easier approach in hatchlings than in juvenile or mature free-swimming species. They note that if the imposed field from an attached magnet or coil is strong enough to interfere with the Earth’s field, behavioral orientation changes [116, 544, 561] and the performance of a conditioned response [367, 562] can be observed. This latter approach has been used in field studies for the purpose of blocking access to normal magnetic information [544, 561, 563], [564], [565] and to localize magnetoreceptors by disrupting the field around a specific terrapin body part [562]. This technique’s disadvantage, however, is that fields rapidly change with distance from the source, making it difficult to quantify the fields that the animal actually experiences.
Most sea turtle studies have involved large magnetic coil systems but Irwin and Lohmann [559] attached small magnets greater in strength than the Earth’s fields to two groups of loggerhead sea turtle hatchlings (Caretta caretta L.) under laboratory conditions in which turtles are known to orient magnetically [473, 546, 548], [549], [550]. They found that magnetic orientation behavior in hatchling turtles can be disrupted via small magnets attached to the carapace which then create exposures over the entire body. They concluded that such an approach can be used to finally determine local magnetoreceptors by varying the location of the magnet and using smaller, weaker magnets that alter the field only around specific anatomical target sites.
In loggerhead sea turtles, there is evidence of an inclination compass [473, 550] that is functionlly similar to the bird magnetic compass reported in European Robins [566, 567]. Lohmann and Lohmann [550] investigated an inclination compass in sea turtles and found it was a possible mechanism for determining latitude. Also investigated were detection of magnetic intensity [551]; natural regional magnetic fields used as navigational markers for sea turtles [557]; and sea turtle hatchlings’ mapping abilities [545]. Sea turtles are also known to have magnetite in their heads [104, 568]. Studies with young sea turtles have shown that a significant portion of their navigational abilities involve magnetoreception following hatching [569] — imprinting with the Earth’s magnetic field being one of several cues hatchlings use as they first migrate offshore [546, 554]. The magnetic fields that are unique to different areas at sea eventually serve as navigational markers to guide swimming direction to important migratory routes. As juveniles mature, they form topographical magnetic maps where they live that direct them to specific regions. But it has remained largely unknown if mature turtles, specifically nesting females, use such mechanisms in open-sea homing as this magneto-sense may change over time.
Field studies are notoriously difficult with large species at sea but Papi et al. [564] studied mature green turtles (Chelonia mydas) during their post-nesting migration over 1,243 mi (2,000 km) from their nesting grounds on Ascension Island in the middle of the Atlantic Ocean back to their Brazilian feeding grounds. They were investigating whether mature female turtles use an inclination compass and geomagnetic fields for direction, or by inference (once that sense is disturbed) by some other means as yet determined. Papi et al. [564] attached very strong DC magnets — significantly stronger than the Earth’s fields — to disturb and overcome natural magnetoreception, and thereby determine if they could still navigate back to Ascension Island. Controls had nonmagnetic brass bars attached and some had transmitters glued to their heads. All had tracking devices that communicated with satellites, thus creating strong multi-frequency static and pulsed RFR exposures. Seven turtles were each fitted with six powerful static magnets that produced variable artificial fields surrounding the whole turtle, making reliance on a geomagnetic map impossible. The study’s travel courses were very similar to those of eight turtles without magnets that had been tracked via satellite over the same period in the previous year. No differences between the magnetically exposed test turtles and untreated turtles were found regarding navigational performance and general course direction. They concluded that magnetic cues were not essential to turtles on the return trip and speculated that perhaps other factors such as smell or wave current direction may come into play.
Luschi et al. [563], like Papi et al. [564], also investigated the role of magnetoreception and homing in mature sea turtles but used a different design and found very different results. In a large field study in the Mozambique Channel, 20 mature pre-nesting green turtles were also equipped with both strong magnets and satellite tracking devices. The turtles were gathered at their nesting beach on Mayotte Island before egg-laying and transported to four open-sea sites 62–75 mi (100–120 km, respectively) away. There were five releases of four turtles each with three different treatments: turtles magnetically ‘disturbed’ only during transportation with magnets removed before release; those treated only during the homing trip with magnets attached just prior to release; and controls with nonmagnetic brass discs attached to their heads. Treated turtles had very strong moveable magnets attached to their heads to induce varying magnetic fields around them either at the nesting beach at the start of the relocation journey or on the boat just prior to release for the homing trip. All groups had satellite transmitters attached to their carapaces, thereby creating in the opinion of the authors of this paper, an additional exposure that was not considered as a variable. The researchers also included ocean currents in their assessments, estimated by using oceanographic remote sensing measurements. All but one turtle eventually returned to Mayotte to complete delayed egg-laying. But treated turtles, whether treated during transportation or homing, took significantly longer to reach the destination vs. controls — a surprising finding. Most homing routes showed very long circuitous curved and looping patterns before reaching their target. Control paths were direct. Both treated turtle groups were clearly impaired by the MF exposure, indicating significant recovery time needed between exposure and correcting positional behavior. The researchers hypothesized the existence of a navigational role for geomagnetic information being gathered by those turtles in the passive transportation group, as well as the possibility that magnetic disturbance during transportation may have persisted for some time after the removal of the magnets in that group, thus rendering the two treated groups functionally equivalent during their homing journeys. They also noted that exposures may have physically altered magnetite particles, thus creating a longer lasting effect but they said that since long-lasting after-effects of magnet application have not been described, this theory could neither be inferred nor dismissed.
Lohmann [323] reviewed both of the above studies and added that in addition to the two causal hypotheses of Luschi et al. [563] regarding their unexpected findings of turtle circuitous migration routes, another explanation would include the positioning of the satellite transmitters in the Papi et al. [564] study on turtle heads vs. on the carapace of the Luschi models. He added that since satellite transmitters also produce magnetic fields capable of disrupting magnetoreception, and since the Papi group also attached satellite transmitters on the heads of several control turtles, that re-analyzing the Papi study using only turtles with satellite transmitters placed on the carapace like the Luschi study could show evidence consistent with the hypothesis that adult turtles exploit magnetic cues in navigation. He concluded that sea turtles, like all other animals studied to date, likely exploit multiple cues for navigation since even with artificial magnetic disturbance causing impaired performance, the magnets in either study did not prevent turtles from eventually reaching their target beaches. This implies that turtles can also rely on other sources of information [570, 571] such as celestial compasses, wave direction [572], or olfactory cues like other species — a significant finding.
The sum total of the studies mentioned above is that sea turtle species are highly sensitive to Earth’s fields and are capable of adapting to subtle anthropogenic disruption.
Turtles: RF-EMF
Turtles may also be senstitive to RFR, especially during incubation while on land, and/or initial hatchling stages if they are exposed to anthopogenic RF-EMF that could distort the imprinting memory they use in later life to locate their birthsite beaches again. For example, if a radar or communications base station is installed on or near the beach of a nesting site, could that affect the initial “imprinting” process? Perhaps augment imprinting and make return easier? Or conversely overwhelm the subtle imprinting process at the start and make return impossible? If the latter is valid, such technology could lead to extinction of sensitive species since it interrupts the reproduction process. In the very least, in sensitive species, disorientation might result as discussed above.
To characterize the underlying compass mechanisms in turtles, Landler et al. [92] studied freshwater juvenile snapping turtles’ (Chelydra serpentine) ability for spontaneous magnetic alignment to the Earth’s geomagnetic fields. Using exposure to low-level RFR near the Larmor frequency (1.2 MHz) that is related to free radical pair formation, turtles were first introduced to the testing environment without the presence of RFR (“RF off, RF off”) and they were found to consistently align toward magnetic north. But when subsequent magnetic testing conditions were initially free of RFR, then included an introduced signal (“RF off, RF on”), they became disoriented. Thus, introduction of a RFR field could affect the turtles’ alignment response to the natural magnetic field. The RFR field used was only 30–52 nT (1.43 MHz). In the following reverse scenario, when the turtles were initially introduced to the testing environment with RFR present but then removed (“RF on, RF off”), they became disoriented when tested without RFR. And with RFR on in both cases (“RF on, RF on”), they aligned in the opposite direction toward magnetic south. Clearly test turtles were affected by the exposures. The researchers concluded that the sensitivity of the spontaneous magnetic alignment response of the turtles to RFR was consistent with a radical pair mechanism (see “Mechanisms” above). In addition, they concluded that the effect of RFR appeared to result from a change in the pattern of magnetic input, rather than elimination of magnetic input altogether. Their findings indicated that turtles, when first exposed to a novel environment, form a lasting association between the pattern of magnetic input and their surroundings, and that they may form a larger internal GPS-like mapping ability when they meet any new magnetic reference framework based on natural magnetic cues, from multiple sites and localities.
They also showed that RFR at or near the Larmor frequency (1.2–1.43 MHz) had the ability to disrupt snapping turtle natural orientation, establish its own novel orientation, and completely reverse a natural orientation, leading back to the complex questions asked above regarding imprinting and possible reproductive disruption. Although the Landler et al. study [92] was conducted in a freshwater, non-homing species, snapping turtles are long-lived with a low reproduction success rate. Even small disruptions to this species from anthropogenic sources could have an outsized population effect over time. If this freshwater species is any indication of potential RFR effects, researchers need to further investigate RFR in long-distance migrating turtle species that imprint on land. We simply do not know the full range of possible effects across frequencies with which turtle species come in contact at vulnerable points throughout development and lifetimes.
Nematodes and smaller biota
There are reports of sensitivity to EMF in lesser taxa as well. EMF is known to affect numerous other species including: nematodes (Earth and aquatic worms), mollusks (snails), amoeba (single-celled organisms), molds, algae, protozoans, yeast, fungi, bacteria, and viruses (to a limited extent) — with ramifications for creation of antibiotic resistant bacteria strains. Below are some representative examples of observed effects.
Nematodes
Common soil-based nematode species like C. elegans serve as a useful whole-organism model for genetic and multicellular organism investigations. They are routinely used as a research model to investigate key biological processes including aging, neural system functioning, and muscle degeneration, to name a few. This species’ genetic and phenotypic traits are extremely well documented and they can thus be used as important proxies for quantitative analyses [573]. Nematodes have a short lifespan, are hermaphrodites, and demonstrate effects quickly. As lab models they are used primarily for information that can be applied to humans but we can also glean important information and extrapolate to environmental exposures under certain circumstances. Healthy soil worm populations are critical to soil health upon which we all depend.
Hung et al. [574] investigated static magnetic field (SMF) effects on life span and premature aging in C. elegans. Nematodes were grown in SMFs varying from 0 to 200 mT. They found that SMF’s accelerated development and reduced lifespan in wild-type nematodes. They also found increases in heat shock proteins that were selective and dose dependent.
Vidal-Gadea et al. [66] investigated magnetic orientation in C. elegans to identify magnetosensory neurons and found that they orient to the Earth’s geomagnetic field during vertical burrowing migrations. Well-fed worms migrated up, while starved worms migrated down. Populations isolated from around the world were found to migrate at angles to the magnetic vector that would vertically translate to their native soil, with northern- and southern-hemisphere worms displaying opposite migratory preferences in conjunction with natural geomagnetic fields. They also found that magnetic orientation and vertical migrations required the TAX-4 cyclic nucleotide-gated ion channel in the AFD sensory neuron pair while calcium imaging showed that these neurons respond to magnetic fields even without synaptic input. They hypothesized that C. elegans may have adapted magnetic orientation to simplify their vertical burrowing migration by reducing the orientation task from three dimensions to one.
C. elegans have also demonstrated sensitivity to electric fields via electrotaxis (also known as galvanotaxis) which is the directed motion of living cells or organisms guided by an electric field or current and often seen in wound healing. Sukul and Croll [575] found that nematodes exposed to an electrical current (0.02–0.04 mA, potential differences 2–6 V) demonstrated a directional sensorily-mediated orientation toward the current at first, but at 2 mm from the electrode, individual worms increased reversing behaviors which then remained uniform as they moved in a constant direction parallel to the exposure. A few which did not reverse direction died (presumably from electrocution) at 6 V or 0.4 mA. They concluded that adult C. elegans move directionally at selected combinations of voltage and potential differences and that electrophoresis could be eliminated.
Gabel et al. [576] also investigated electric field effects on directionality on C. elegans with an eye toward better understanding how the nervous system transforms sensory inputs into motor outputs. They used time-varying electric fields modulated at 100 Hz across an agar surface with a defined direction and amplitude up to 25 V/cm. They found that the nematodes deliberately crawl toward the negative pole in an electric field at specific angles to the direction of the electric field in persistent forward movements with the preferred angle proportional to field strength. They also found that the nematodes orient in response to time-varying electric fields by using sudden turns and reversals (normal reorientation maneuvers). They also found that certain mutations or laser ablation that disrupt the structure and function of amphid sensory neurons also disrupted their electrosensory behavior and that specific neurons are sensitive to the direction and strength of electric fields via intracellular calcium dynamics among the amphid sensory neurons. This study showed that electrosensory behavior is crucial to how the C. elegans nervous system navigates and can be disrupted at some intensities found in the environment.
Maniere et al. [573] also found C.elegans was sensitive to electric fields and that when submitted to a moderate electric field, worms move steadily along straight trajectories. They hypothesized that imposing electric fields in research settings was an inexpensive method to measure worms’ crawling velocities and a method to get them to self-sort quickly by taking advantage of their electrotactic skills.
An early RFR study of C elegans by Daniells et al. [577] found this species to be a useful model for investigating stress-responses. In the majority of investigations, they used 750 MHz with a nominal power of 27 dBm; controls were shielded and all temperatures were strictly controlled. Stress responses were measured in terms of beta-galactosidase (reporter) induction above control levels. Response to continuous microwave radiation showed significant differences from 25 degrees C in controls at 2 and 16 h, but not at 4 or 8 h. Using a 5 × 5 multiwell plate array exposed for 2 h, the 25 microwaved samples showed highly significant responses compared with a similar control array. Experiments in which the frequency and/or power settings were varied suggested a greater response at 21 than at 27 dBm, both at 750 and 300 MHz indicating a nonlinear effect, although extremely variable responses were observed at 24 dBm and 750 MHz. Lower power levels tended to induce greater responses — the opposite of simple heating effects. They concluded that microwave radiation causes measurable stress to transgenic nematodes via increased levels of protein damage within cells at nonthermal levels.
Tkalec et al. [578] found oxidative and genotoxic effects in earthworms (Eisenia fetida) exposed in vivo to RFR at 900 MHz, at 10, 23, 41 and 120 V m(-1) for 2 h using a Gigahertz Transversal Electromagnetic (GTEM) cell. All exposures induced significant effects with modulation increasing such effects. Their results also indicated antioxidant stress response induction with enhanced catalase and glutathione reductase activity, indicating lipid and protein oxidative damage. Antioxidant responses and damage to lipids, proteins and DNA differed depending on EMF level, modulation, and exposure duration.
Aquatic and semi-aquatic worm species also show sensitivity to EMF. Jakubowska et al. [579] investigated behavioral and bioenergetic effects of EMF at 50 Hz, 1 mT fields (comparable to exposures near underwater cables) in polychaete ragworms (Hediste diversicolor) that live and burrow in the sand/mud of beaches and estuaries in intertidal areas of the North Atlantic. While they found no attraction or avoidance behavior to EMF, burrowing activity was enhanced with EMF exposure, indicating a stimulatory effect. Food consumption and respiration rates were unaffected but ammonia excretion rate was significantly reduced in EMF-exposed animals compared to control conditions at only geomagnetic fields. The mechanisms remained unclear. The authors said this was the first study to demonstrate effects of environmentally realistic EMF values on the behavior and physiology of marine invertebrates.
Van Huizen et al. [67] investigated effects of weak magnetic fields (WMF) on stem-cells and regeneration in an in vivo model using free-swimming flatworms (Planaria ssp) that are capable of regenerating all tissues including the central nervous system and brain. This regeneration ability is due to the fact that about 25% of all their cells are adult stem cells (ASC). Injury is followed by a systemic proliferative ASC response that initially peaks at ∼ 4 h, followed by ASC migration to the wound site over the first 72 h when a second mitotic peak occurs. Like salamander regeneration (see “Amphibians” above) this activity produces a blastema — a group of ASC cell growth that forms the core of new tissues. Full regeneration of damaged planaria tissues or organs occurs through new tissue growth and apototic remodeling/scaling of old tissues within 2–3 weeks. Following amputation above and below the pharynx (feeding tube), they exposed amputation sites to 200 μT WMF. At three days post-amputation, they found that 200 μT exposure produced significantly reduced blastema sizes compared to both untreated and earth-normal 45 μT field strength controls, indicating a WMF interference effect to regeneration. They also found that the 200 μT exposure was required early and had to be maintained throughout blastema formation to affect growth, and that shorter, single-day exposures failed to affect blastema size. In addition, they found weak magnetic fields produced field strength–dependent effects. These included significant reductions of blastema size observed from 100–400 μT, but conversely, a significant increase in outgrowth occurred at 500 μT. They hypothesized that WMF effects were caused by altered reactive oxygen species (ROS) levels, which peak at the wound site around 1-h post-amputation and are required for planarian blastema formation. This study shows that weak anthropogenic magnetic fields can affect stem cell proliferation and subsequent differentiation in a regenerative species, and that field strength can increase or decrease new tissue formation in vivo. This is a significant finding for regenerating species of all kinds, and may affect non-regenerating species as well. Sea lamprey eels (Petromyzon marinus), a fish species, are also known to regenerate even after multiple amputations [580].
Mollusks, amoeba, molds, algae, protozoans
Mollusks (marine versions are called chitons) are long known to manufacture magnetite in their teeth and to use fields weaker than the geomagnetic field for kinetic movement and direction [52, 117, 340, 524]. Lowenstam [118] first discovered that magnetite was the major mineral in the teeth of marine chitons, thought to give teeth their natural hardness. But Ratner [62] discovered chitons use magnetite as a magnetic compass when he found a number of chiton species have radulae (tongues) that are covered by ferro-magnetic (magnetite) denticles. The radulae of Acompapleura granulata and Chiton squamosis were also found to be ferro-magnetic but the shells were not. Live specimens of a chiton (Chaetopleura apiculata) that also have ferro-magnetic radulae were found to rotate more and move farther in a magnetic field weaker than in the Earth’s stronger geomagnetic field, indicating a nonlinear directionality. Ratner concluded that chitons are responsive to magnetic fields and demonstrate kinetic movements within them.
Some snails are sensitive to EMFs. Nittby et al. [581] observed analygesic effects in land snails (Helix pomatia) caused by GSM-1900 RFRs when snails lost sensitivity to pain on a hot plate test after nonthernal exposure to RFR.
Smaller organisms have also long shown effects from EMF. Goodman et al. [582] found delays in mitotic cell division in slime mold (Physarum polycephalum) with ELF-EMF exposures. Friend et al. [583] found perpendicular and parallel elongation of the giant amoeba Chaos chaos (Chaos carolinensis) in alternating electric fields over a wide frequency range (1 Hz–10 MHz) with characteristic changes as a function of frequency. Marron et al. [584] found effects on ATP and oxygen levels in another species of slime mold (P. polycephalum) after exposures to 60 Hz sinusoidal electric and magnetic fields. Luchien et al. [585] found a stimulating effect on the productivity of the algal biomass (Chlorella sorokiniana) for a magnetic field of 50 Hz but an inhibitory effect at 15 Hz in these microalgae.
Protozoans, thought to be more related to animals than microbes, also show sensitivity to EMF. Protozoans, as single-celled eukaryotes, are generally larger than bacteria which are classified as prokaryotes. The two organisms are structurally different: bacterial cells lack a nucleus while protozoa contain organelles such as mitochondria. Bacteria generally absorb nutrients through their cell walls while protozoa feed on bacteria, tissue, and organic matter and can be both infectious and parasitic. These protozoa include human parasites that cause diseases such as amoebic dysentery, malaria, giardiasis, leishmaniasis, trichomoniaisis, toxoplasmosis and others. Animal species are also affected by protozoans which can severely weaken and shorten their lifespans.
Rodriguez-de la Fuente et al. [586] tested ELF-EMF (60 Hz, 2.0 mT for 72 h) on two infectious protozoans, Trichomonas vaginalis and Giardia lamblia, and found growth alterations in both species which they attributed to alterations in cell cycle progression and cellular stress. Cammaerts et al. [587], used RFR (GSM 900-MHz at 2 W vs. control) on protozoans (Paramecium caudatum) and found individuals moved more slowly and sinuously than usual and that their physiology was affected. Paramecia became broader, pulse vesicles had difficulty expelling content to the outside of their cells, cilia moved less efficiently, and trichocysts became more visible — all effects that indicate poor functioning or cell membrane damage. They hypothesized that the first impact of RFR could be to cell membranes.
Clearly there are multiple effects at all levels documented in lower taxa from multi-frequency exposures that are now found in the environment.
Yeast and fungi
Yeast is often used in lab models, especially since 1996 when a complete genomic sequence of Saccharomyces cerevisiae was created. In fact it is now considered a “premier model” [588] for eukaryotic cell biology as well as having helped establish whole new fields of inquiry such as “functional genomics” and “systems biology” which focus on the interactions of individual genes and proteins to reveal specific properties of living cells and whole organisms.
EMF research is rich with studies using yeast models too numerous to fully analyze here. However we include a small sample of recent EMF research with potential significance to environmental exposures.
Lin et al. [589] investigated glucose uptake and transcriptional gene response to ELF-EMF (50 Hz) and RFR (2.0 GHz) on several strains of budding yeast (S. cerevisiae). Results determined that ELF-EMF and RFR exposure can upregulate the expression of genes involved in glucose transportation and the tricarboxylic acid (TCA) cycle, but not glycolysis pathways, thus showing that such exposures can affect energy metabolism which is closely related with cellular response to environmental stress. Glucose metabolism is fundamental to all living cells’ need for energy, with related significance to many disease states including most cancers.
In a magnetic field study by Mercado-Saenz et al. [590], premature aging and cellular instability were found in yeast (S. cerevisiae) exposed to low frequency, low intensity sinusoidal magnetic fields (SMF continuous exposure at 2.45 mT, 50 Hz) and pulsed magnetic fields (PMF 1.5 mT, 25 Hz, 8 h/day). Chronological aging was evaluated during 40 days and cellular stability was evaluated by a spontaneous mutation count and the index of respiratory competence (IRC). They found exposure to PMF produced accelerated aging while SMF did not, and decreased mitochondrial mutation during aging was also seen with PMF. No alterations in respiratory competence were observed for either SMF or PMF exposures. They concluded that exposure to PMF accelerated chronological aging and altered the spontaneous frequency of mitochondrial mutation during the aging process, whereas the SMF used had no effect, thus showing abnormal effects on cell activity from pulsed exposures.
Because yeast cells are known to be sensitive to magnetic fields, some industrial and therapeutic applications to human health have been investigated. These investigations serve to illuminate what we know about yeast and fungal reactions to EMF in general, as well as specific uses. For industrial applications, Wang et al. [591] investigated low level static magnetic fields (SMF) on mold (Aspergillus versicolor) growth which can have high impacts on metal corrosion in environmental conditions conducive to mold growth. This is especially problematic in fine electronic circuit boards produced today. Using a 10 mT static magnetic field (SMF) perpendicular to the surface of printed circuit boards, they found the magnetic field inhibited mold growth and surface corrosion which were slowed down, unlike control boards without applied magnetic fields where mold formed a spore-centered corrosion pit that then led to macroscopic regional uniform corrosion. This demonstrated changes in cell/spore growth at a low intensity exposure that can be found in the environment.
Also with an eye toward commercial possibilities, Sun et al. [592] found that a polysaccharide of Irpex lacteus (a white-rot fungus found widely in the environment which breaks down organic materials but also is commercially used to treat nephritis in humans) was sensitive to low-intensity ELF-EMF as demonstrated by increased biomass and polysaccharide content, as well as induced malformed twists on the sample cell surfaces. Polysaccharides are carbohydrates with a large number of sugar molecules used as energy sources in living cells. They identified varying changes in multiple differentially expressed genes after exposure to alternating current EMF (50 Hz, 3.5 mT, 3 h per day, for 4 days). They found initial sharp increases in growth rates in exposed samples that were then marked by significant declines in EMF’s influence over time, although there were also important lasting effects. Global gene expression alterations from EMF indicated pleiotropic effects (capable of affecting multiple proteins or catalyzing multiple reactions) were related to transcription, cell proliferation, cell wall and membrane components, amino acid biosynthesis and metabolism. Polysaccharide biosynthesis and metabolism were also significantly enriched in the EMF-exposed samples. They concluded that EMF significantly increased amino acid contents and was therefore deemed a suitable method for increasing fermentation of microorganisms, presumably for commercial use. However, the significance of this study to environmental exposures relates to the multiple ways that ELF alternating current common to electric power generation changed yeast gene expression. There is at least one clinical case of a different strain of I. lacteus taking on a rare infectious and dangerous quality in an immuno-compromised human [593]. The question is: can now-ubiquitous ELF-EMF contribute to potentially emerging new forms of yeast contagion?
The same question arises with Candida albicans and other pathogenic yeasts that have rapidly developed resistance to antifungal medications. C. albicans can live harmlessly in human microflora, but certain lifestyle circumstances or immunosuppression can turn it into an opportunistic pathogen. It can also infect some non-human animals. While chronic mucocutaneous candidiasis can infect the skin, nails, and oral and genital mucosae, under high host immunodeficiency C. albicans can enter the bloodstream and induce systemic infections with mortality between 30 and 80% [594]. There has been increasing resistance of C. albicans to traditional antifungal agents, such as fluconazole and amphotericin B [595, 596]. Resistance mechanisms include overproduction of membrane drug efflux transporters and/or changes in gene expression [597].
Two investigations in search of new therapeutic strategies were conducted using EMF. Sztafrowski et al. [594] investigated the use of static magnetic fields (SMF, 0.5 T) on C. albicans cultures in the presence of two commonly used antifungal medications. Their aim was to assess whether SMF had any impact on general viability of C. albicans hyphal transition and its susceptibility to fluconazole and amphotericin B. They found reduction of C. albicans hyphal length in EMF-exposed samples. They also found a statistically significant effect on C albicans viability when SMF was combined with amphotericin B. They hypothesized that this synergistic effect may be due to the plasma membrane binding effects of amphotericin B and that SMF could influence domain orientation in the plasma membrane. They concluded, with caution, that the use of a SMF in antifungal therapy could be a new supporting option for treating candidas infections.
Novickij et al. [598] also focused on therapeutic possibilities given the multi-drug resistance and side effects to antifungal therapies. Their aim was to optimize the electroporation-mediated induction of apoptosis using pulses of varied duration (separately and in combination with formic acid treatment) and to identify yeast apoptotic phenotypes. They focused on nonthermal nanosecond pulsed electric fields (PEF 3 kV, 100 ns – 1 ms squarewave; and 250, 500, 750 ns duration 30 kV/cm PEF, 50 pulses, 1 kHz) as a therapeutic alternative and/or to enhance effects in combination with conventional treatments. In three yeast models, S. cerevisiae (as control) and drug resistant Candida lusitaniae and Candida guilliermondii, they found that nanosecond PEF induced apoptosis in all three strains. Combining PEF with a weak formic acid solution improved induced apotosis and inactivation efficacy in the majority of the yeast population. Yeast cells showed DNA breaks and other changes. They concluded that PEF could be a useful new non-toxic protocol to treat some fungal diseases and minimize tissue damage.
Choe et al. [599] studied ion transportation and stress response on a yeast strain (K667) to ELF-EMF (60 Hz, 0.1 mT, sinusoidal or square waves), specifically investigating internal ionic homeostasis via the cell membrane involving metal ions and cation transports (cations are ionic species of both atoms and molecules with a positive charge). They found significantly enhanced intracellular cation concentrations as ELF-EMF exposure time increased, as well as other changes. This study has implications for soil health as yeast can be an integral aspect of how healthy organic soil matter is formed. They concluded that EMF and yeast could also play a role in the bioremediation processes in metal-polluted environments.
Lian et al. [600] studied effects of ELF-EMF (50 Hz, 0–7.0 mT) and RFR (2.0 GHz, 20 V/m, temperature at 30 °C, average SAR single cell/0.12 W/kg) on two budding yeast strains (NT64C and SB34) and prion generation/propagation. They found under both EMF exposures that de novo generation and propagation of yeast prions (URE3) were elevated in both yeast strains. The prion elevation increased over time and effects were dose-dependent. The transcription and expression levels of heat shock proteins and chaperones were not statistically significantly elevated after exposure but levels of reactive oxygen species (ROS), as well as superoxide dismutase (SOD) and catalase (CAT) activities were significantly elevated after short-term, but not long-term exposure. This work demonstrated for the first time that EMF exposure could elevate the de novo generation and propagation of yeast prions, supporting the researcher’s hypothesis that ROS may play a role in the effects of EMF on protein misfolding. ROS levels also mediate other broad effects of EMF on cell function. They concluded that effects of EMF exposure on ROS levels and protein folding may initiate a cascade of effects negatively impacting many biological processes.
The effects of EMF on protein folding cannot be overstated. Proteins must fold into proper three-dimensional conformations to carry out their specific functions — intact proteins are critical to the existence of all life. Misfolding not only impairs function but leads to disease. Folding inside of cells does not happen spontaneously but rather depends on molecular helpers called chaperones. Protein misfolding has been implicated in Alzheimer’s, Parkinson’s, and Huntington’s diseases, among others. The devastating Creutzfeldt–Jakob disease is caused by prion misfolding in the brain, which causes abnormal signaling in neurons that eventually leads to paralysis and death. Wildlife can also suffer from prion diseases such as chronic wasting in deer, elk, and other cervids, and cattle can suffer from so-called “mad-cow” disease. The two studies from above [599, 600] have implications for how such diseases are spread through soil with possible links to environmental EMFs.
It is clear from the above that ELF-EMF and RF-EMF, using multiple signaling characteristics, are biologically active in both temporary and permanent ways in yeast/fungi species with wide environmental implications across numerous taxa.
Bacteria
Strains of bacteria are known to be magnetotactic and use geomagnetic fields for direction. Blakemore [63] was the first to suggest in 1973 that bacteria in North American saltwater marsh muds use magnetite as a sensor when he discovered not only that bacteria were highly attracted to an external magnet but they also had magnetite crystals that caused them to align with the lines of the Earth’s magnetic fields. This was also discovered to be geo-location specific to the North Pole in northern samples and South Pole-seeking in southern species [52, 63, 511]. The bacteria showed “mud-up” and “mud-down” behavior along magnetic field gradients when mud was disturbed, indicating a magnetic compass. Since that early work, a whole new field called electromicrobiology has developed with discoveries that include some electro-active bacteria being responsible for magnetite formation, with others creating their own electric “wires” in mud flats with implications for new technologies [601].
Among the more troubling EMF effects are bacterial alterations with pressing implications for antibiotic resistance. Since the 1940s [602], nonthermal effects were documented in bacterial, viral, and tissue cultures with applied low-repetition 20-MHz pulses. Most studies spanning the 1940s though the 1980s focused on EMF’s ability to kill microbes and fungi in human food sources at high intensity, consequently most research was focused on thermal intensities. That work still continues today as microwaves have been shown to be an efficient means for killing microbes [50]. But microbes also react to much lower nonlethal intensities and recent work finds effects from both ELF and RFR.
The common bacteria Escherichia coli, which can live harmlessly in the gut of humans and many other animal species, can also turn virulent and kill through food-borne illnesses. E. coli comes in many strains, is well studied, and now considered the most genetically and physiologically characterized bacterium. E. coli encounter varied and numerous environmental stressors during growth, survival, and infection, including heat, cold, changes in Ph levels, availability of food/water supplies, and EMF. Along with other bacteria, they respond by activating groups of genes and heat shock proteins (see “Mechanisms” above) which can eventually lead to stress tolerance for survival purposes. But induced stress tolerance can also lead to increased virulence, as well as enhanced tolerance to other stressors that confer cross‐protection [603].
Salmen and colleagues [604, 605] published papers of EMF effects on bacterial strains documenting the growing investigation of microbes related to antibiotic resistance with many findings stressing responses to EMF [606], [607], [608], [609], [610]. Cellini et al. [611] investigated E. coli’s adaptability to environmental stress induced by ELF exposures to 50-Hz magnetic fields at low intensities (0.1, 0.5, 1.0 mT) vs. sham controls. They found exposed samples and controls displayed similar total and culturable counts, but increased cell viability was observed in exposed samples re-incubated for 24 h outside of the test solenoid compared to controls. Exposure to 50 Hz EMF (20–120 min) also produced a significant change in E. coli morphotype with a presence of coccoid cells aggregated in clusters after re-incubation of 24 h outside of the magnetic field-solenoid. Atypically lengthened bacterial forms were also noted, indicating probable alteration during cell division. Some differences in RNA-AFLP analysis were also seen for all intensities evaluated. They concluded that exposure to 50-Hz ELF-EMF is a bacterial stressor as evidenced by its immediate response in modifying morphology (from bacillary to coccoid) and inducing phenotypical and transcriptional changes. Despite this stressor effect, it was also seen that exposed samples significantly increased viability, suggesting the presence of VBNC cells. They concluded that further studies were needed to better understand ELF-EMF in bacterial cell organization. They did not extrapolate to the obvious — that E. coli was changed in an abnormal way but nevertheless strengthened in viability — a recipe for antibiotic resistance.
Crabtree et al. [612], in a small human study, investigated the biomic relationship of human bacteria exposed to both static magnetic fields (SMF) and RFR. Using laboratory culture strains and isolates of skin bacteria collected from the hand, cheek, and chin areas of four volunteers who had different (self-reported) cell phone use histories, they found varied growth patterns of E. coli, Pseudomonas aeruginosa, and Staphylococcus epidermidis under static magnetic fields on different bacterial species. Isolates of skin microbiota showed inconsistent growth among the test subjects, likely due to their differing cell phone usage histories (classified as heavy, medium and light) and other variables. The growth of Staphylococci was increased under RFR in certain individuals while in others growth was suppressed. This was complicated by the different body areas tested, some with higher chronic exposures such as the hands, as well as other variables when one test subject used an antibacterial face wash. Volunteers in the heavy use category showed less bacterial growth on the hands, possibly due to microbe habituation. Overall, and despite the small sample, they concluded RFR can disrupt the balance in skin microbiota, making it more vulnerable to infection by specific opportunistic and/or other foreign pathogens. They noted that both SMF and RF-EMFs have significant but variable effects on the growth of common human bacteria; that bacterial growth was either unaffected, increased, or suppressed depending on the species of bacteria; and that bacterial responses seemed to be determined by historic exposure to RF-EMF and life style. This study, even with inherent limitations, indicates changes in microbes with EMFs and may prove a novel way to study bacteria with significance for real-life exposures to humans and animals alike.
Salmen et al. [605] also found highly variable results from RFR (900 and 1,800 MHz) effects on DNA, growth rate, and antibiotic susceptibility in Staphylococcus aureus, Staphylococcus epidermidis, and P. aeruginosa. Using an active cell phone handset, they exposed bacteria to 900 and 1,800 MHz for 2 h, then injected samples into a new medium where growth rate and antibiotic susceptibility were evaluated. Regarding DNA, they found no differences in S. aureus and S. epidermidis when exposed to 900 and 1,800 MHz vs. controls, but P. aeruginosa showed changes in DNA band patterns following such exposures. Regarding growth rates, with the exception of a significant decrease after 12 h exposure to 900 MHz, no significant effects on growth of S. aureus and S. epidermidis were seen. But the growth of P. aeruginosa was significantly reduced following exposure for 10 and 12 h to 900 MHz, while no significant reduction in growth followed exposure to 1,800 MHz. Regarding antibiotic susceptibility, in the drugs studied (i.e., amoxicillin 30 mg, azithromycin 15 mg, chloramphenicol 10 mg, and ciprofloxacin 5 mg), with the exception of S. aureus treated with amoxicillin (30 mg), EMF-exposure had no significant effect on bacterial sensitivity to antibiotics. This study shows variability among bacterial species not only to different frequencies common in the environment today but also to changes in sensitivity to some antibiotics but not others. There may have been design problems with this study, however.
Several studies investigated WiFi signals on bacterial strains. Taheri et al. [610] assessed exposure to 900-MHz GSM mobile phone radiation and 2.4-GHz RFR from common WiFi routers to see if cultures of Listeria monocytogenes and E. coli resulted in altered susceptibility to 10 different antibiotics. They found narrow windows in which microbes became more resistant: For L. monocytogenes no significant changes in antibacterial activity between exposed and nonexposed samples — except for Tetracycline (Doxycycline) — were noted. For E. coli, however, there was a significant change in antimicrobial activities suggesting RFR exposures can influence antibiotic susceptibility of E. coli more than in Listeria. For window and pronounced effects, they found L. monocytogenes exhibited different responses to each antibiotic. For Doxycycline, the window occurred after 6 h exposure to WiFi and mobile phone-RFR. After 9 h of exposure to WiFi for Ciprofloxacin and Sulfonamide (Tremethoprin/sulfamethoxazole), bacteria tended to become more resistant. By contrast, the pattern for Levofloxacin and Penicillin (Cefotaxime/Deftriaxone) showed increased sensitivity. For E.coli, the pattern of the response to WiFi and mobile phone RFR was the same: maximum antibiotic resistance was seen between 6 and 9 h of exposure but after 12 h, a stress response lead to a return to preexposure conditions indicating an adaptive reaction. Taheri et al. [609] found similar nonlinear window effects and differences in growth rates in Klebsiella pneumonia, while Mortazavi et al. [613] found similar window effects in E coli. In addition, they saw significant increased growth rates after radiation exposures in both Gram-negative E. coli and Gram-positive L. monocytogenes. They concluded that such window effects can be determined by intensity and dose rate; that exposure to RFR within a narrow window can make microorganisms resistant to antibiotics; and that this adaptive phenomenon is a human health threat. The same can be inferred for many non-human species.
Said-Salman et al. [614] evaluated non-thermal effects of WiFi at 2.4 GHz for 24 and 48 h (using a WiFi router as the source) on the pathogenic bacterial strains E. coli 0157H7, S. aureus, and S. epidermis for antibiotic resistance, motility, metabolic activity and biofilm formation. Results found that WiFi exposure altered motility and antibiotic susceptibility of E. coli but there was no effect on S. aureus and S. epidermis. However, exposed cells (vs. unexposed controls) showed an increased metabolic activity and biofilm formation ability in E. coli, S. aureus and S. epidermis. They concluded that WiFi exposure acted as a bacterial stressor by increasing antibiotic resistance and motility of E. coli, as well as enhancing biofilm formation in all strains studied. They indicated the findings may have implications for the management of serious bacterial infections.
Movahedi et al. [615] also investigated antibiotic resistance, using short-term exposure to RFR from a mobile phone simulator (900 MHz, 24 h) on P. aeruginosa and S. aureus against 11 antibiotics. They found significant changes in structural properties and resistance to the numerous antibiotics studied. P. aeruginosa was resistant to all antibiotics after 24 h of exposure vs. non-exposed controls while S. aureus bacteria were resistant to about 50%. They also found structural changes in all exposed samples and increased cell wall permeability.
In a field study near cell towers, Sharma et al. [616] looked at changes in microbial diversity and antibiotic resistance patterns in soil samples taken near four different base stations with control samples taken >300 m away. Stenotrophomonas maltophilia, Chryseobacterium gleum, and Kocuria rosea were isolated and identified in soil samples collected near the exposed zones. They found greater antibiotic resistance in microbes from soil near base stations compared to controls, with a statistically significant difference in the pattern of antibiotic resistance found with nalidixic acid and cefixime when used as antimicrobial agents. They concluded that cell tower radiation can significantly alter the vital systems in microbes and make them multi-drug resistant.
Researchers have also investigated ELF-EMF effects on bacterial growth and antibiotic sensitivity. Segatore et al. [608] investigated 2 mT, 50 Hz exposures on E. coli ATCC 25922 and P. aeruginosa ATCC 27853 and found EMF significantly influenced the growth rate of both strains, notably at 4, 6, and 8 h of incubation. The number of cells was significantly decreased in exposed bacteria vs. controls. And at 24 h incubation, the percentage of cells increased (P. aeruginosa ∼ 42%; E. coli ∼ 5%) in treated groups vs. controls which suggested to the researchers a progressive adaptive response. However, they saw no remarkable change in antibiotic sensitivity. Potenza at al. [617] also found effects at high-intensity static magnetic fields at 300 mT on growth and gene expression in E.coli but that would be a high environmental exposure.
Viruses
There is a paucity of research on viral species and EMF, likely due to the fact that viruses lack ferromagnetic materials, are difficult to study, and don’t make good general lab models other than to investigate their direct impact on specific in vivo end points. Virology research thrives in its own specialized niche and has not been used for basic modeling like so many other living life forms as noted throughout this paper. There is long-standing debate on whether viruses are even alive.
However, one wide-ranging discussion by Zaporozhan and Ponomarenko [618] hypothesized a possible complex mechanistic link between influenza pandemics, natural sun spot cycles, and non-thermal effects of weak magnetic fields via cryptochromes/radical pairs, gene expression pathways, and stress-induced host immunological alterations favorable to influenza epidemics. Noting that most — though not all — major influenza epidemics occurred in time intervals starting 2–3 years before and ending 2–3 years after maximum solar activity, they hypothesized that solar cycles are able to both regulate and entrain processes of biological microevolution in viral species (among others), as well as influence human bio-rhythms in synergistic ways that could lead to influenza epidemics. Although others have also noted links between influenza pandemics and sunspot activity — possibly based on changes in migratory bird patterns as viral vectors [619], [620], [621]— and some have linked sun spots with other adverse human health events, these effects remain of interest but are still hypothetical. UV radiation, which is not covered in this paper, is known to suppress cell-mediated immunity and is therefore capable of adversely affecting the course of a viral infection in some mammal species. Ambient EMF in lower frequency ranges may also be reducing immune viability across species which can theoretically foster opportunistic virulence. Far more EMF research needs to be conducted on viruses; one fruitful approach might be synergistic investigations in virus-infected plant species.
The previous studies of microbes show a pattern of sensitivity in microorganisms to EMF with associations that encompass a wide range of critical changes, including consistent stress responses, alterations in growth and viability, cell membrane alterations, and clear patterns of how easily antibiotic resistance forms in microbial life to now ubiquitous EMF levels.
Plants (see Part 2, Supplement 4, for a table of flora studies: ELF, RFR)
Plants have evolved in highly sensitive ways to natural and manmade EMF in all phases of germination, growth and maturation [31]. Magnetoreception, which is well documented in animals such as birds, has also been described in plants [622] and plant species can respond to subtle changes in EMF in the environment, including in whole plant communities [623]. They may even ‘communicate’ and gather various kinds of ‘information’ via electrical signals in neuron-like cells in root tips and elsewhere [624]. Some hypothesize [625] that a form of vibrational and acoustic sensitivity around 220 Hz may play a role in plant life, although not everyone agrees [626].
Almost all vegetation is subject to complex multi-frequency fields due to their soil-based root systems and high water content, plus above-ground ambient RFR exposures makes plants uniquely susceptible to effects near transmission towers [623, 627]. Many EMF studies have found both growth stimulation as well as dieback. The presence of numerous RFR-emitters in the German and Swiss Alps is thought to have played a role in the deforestation there [628]. The ‘browning’ of treetops is often observed near cell towers, especially when water is near tree root bases [25]. Treetops, with their high moisture content and often thick vegetative canopy, are known RFR waveguides. In fact, military applications utilize this capability in treetops for communication signal propagation in remote areas and for guidance of low-flying weapons systems [629].
How flora interacts with EMF is still a mystery but a clear pattern has emerged in researching the database for this paper: static ELF-EMF has largely been found beneficial to plant and seed growth [630] while RFR is detrimental. Plants clearly have magnetoreception in their stationary condition. The normal ground state of magnetic fields for plants is the relatively constant natural geomagnetic field that averages between 25 and 65 μT depending on location and seasonal variations [631]. Atmospheric changes, such as thunderstorms and lightning, can cause intermittent changes in ambient magnetic fields. These activities are also generally associated with rainwater critical to virtually all plant life. Plants can detect these changes and prepare for growth using the upcoming rainfall. Trees are seen extending their branches skyward long before rain actually occurs and such changes match alterations in tree polarities [632].
There are many studies showing an increase in the growth rate in plants, such as studies of seed germination exposed to alternating magnetic fields. Plants also respond similarly to high intensity static magnetic fields. This may mean that the physiological mechanism in plants that causes magnetic field-induced growth is finely tuned to a certain intensity of magnetic flux. Any variation in intensity or shape of the ambient magnetic field could activate or hinder this growth mechanism.
Lightning, for instance, generates fast and intense electromagnetic pulses (EMP). EMP has consistently been shown to cause biological effects [633] with just one pulse. Plants may have mechanisms so sensitive that they can detect the energy of EMP from kilometers away. The pulse causes a transient change in the environmental magnetic field that may be detected by one or more of the mechanisms mentioned in the “Mechanisms” section above, as well as discussed below. EMP has been closely investigated for military applications for its ability at high intensities to disable electronics. While much of the military-supported research finds no biological effects from EMP exposure, non-military supported research does show effects. This parallels the same findings in industry vs. non-industry research patterns [165, 634].
There is a long history on the study of effects of EMF exposure on plant growth, notably, the work of the Indian scientist Sir Jagadish Bose (1858–1937) who proposed the electric nature of plant responses to environmental stimuli and studied effects of microwaves on plant tissues and membrane potentials [635]. Interestingly, Bose investigated the effects of millimeter waves [636] now applicable to 5G technology. Bose, arguably, was a pioneer of wireless communication.
Another early pioneer in EMF effects on plants was Harold Saxon Burr (1889–1973) at Yale University who investigated the electric potential of trees in two tree species (a maple and an elm) located on one property and another maple tree for comparison growing 40 miles (64 km) away. Measurements of numerous parameters were taken using embedded electrodes that recorded hourly from 1953 to 1961 [637]. Simultaneous records of temperature, humidity, barometric pressure, sunlight, moon cycles, sunspot activity, weather conditions, atmospheric-potential gradients, earth-potential gradients, and cosmic rays were correlated with tree potentials. Burr also installed equipment that measured the potential between electrodes in the Earth (about 10 miles apart) and the potential gradient of the air, and found that the air and Earth potentials fluctuated exactly with the phase of the tree potentials although the trees were not always synchronous. Burr ultimately found that the electrical environment correlated closely with tree potentials in a kind of entrainment to diurnal, lunar and annual cycles. Meteorological parameters did not correlate in any immediate way other than when passing thunderstorms elicited anomalous behavior in the trees in direct parallel to measurements with the Earth electrodes. This follows the theory noted above that plants can sense EMP and take immediate information from it.
There are no other long-term field studies as detailed as Burr’s of magnetic field effects on a plant species. However, another field study of RFR in Latvia [638] measured effects directly on trees near the Skrunda Radio Location Station, an early warning radar system that operated from 1971 to 1998. The system operated in the 156–162 MHz frequency range transmitting from four pulsed two-way antennas that had operated continuously for over 20 years by the time of the study. In permanent plots in pine forest stands, at varying distances from the radar station and in control areas, tree growth changes were measured and analyzed using retrospective tree ring data. They found a statistically significant negative correlation between the relative additional increment in tree growth and the intensity of the electric field with the radial growth of pine trees diminished in all plots exposed to RFR. The decreased growth began after 1970, which coincided with the initial operation of the station and was subsequently observed throughout the period of study. The effects of many other environmental and anthropogenic factors were also evaluated but no significant effects on tree growth were correlated. This may have been the first detailed field study of plants and RFR.
Many studies of EMF and plants are today conducted in laboratories and have often focused on growth promotion to create higher yields of food-producing plants. Effects of static EMF, pulsed EMF, ELF-EMF, and RF-EMF have been reported. There are, in fact, over 200 studies on plants and EMF alone — too numerous to review here. See Part 2, Supplement 4, for a Table of studies on plant seedlings and development based on the types of EMF’s tested.
As noted in Supplement 4 and in Halgamuge [627], frequently static and ELF-magnetic fields generally improve plant growth whereas RFR retards it. This is the opposite of results from animal and animal-cell culture experiments in which ELF-MF usually produces the same effects as RFR. It is interesting to note that Hajnorouzi et al. [639] and Radhakrishma et al. [640] proposed that MF decreases environmental stress in plants whereas Vian et al. [641, 642] considered RFR as a systemic stressor. A major morphological difference between animal and plant cells is that plant cells have a cell wall that is an active physiological organelle which regulates growth and cell division and controls cellular communications. The cell wall contains a considerable amount of water [643]. Is it possible that absorption of RFR by cell-wall water causes a micro-thermal effect that adversely affects plant cell functions and even causes cell death, whereas thermal effects are not likely to occur with ELF-EMF exposure.
Some plant roots have been found sensitive to both ELF and RFR. Belyavskaya [644] found a strong cytochemical reaction in pea root cells after exposure to low level magnetic fields. Kumar et al. [645] found cyto- and genotoxicity in root meristems of Allium cepa with 900-MHz and 1,800-MHz RFR. Chandel et al. [646] studied cytotoxic and genotoxic activity on DNA integrity in root meristems of A. cepa using 2,100-MHz RFR and found exposure caused DNA damage with a significant decrease in HDNA accompanied by an increase in TDNA while TM and OTM did not change significantly compared to controls. Biological effects were dependent on the duration of exposure with maximum changes seen at 4 h.
In a series of studies, Stefi et al. [647], [648], [649] investigated the effects of long term RFR exposure from the base units of common cordless DECT phone systems (pulsed transmission mode 1,882 MHz, 24 h/day, 7 d/week) on various plant species (Arabidopsis thaliana, Pinus halepensis, Gossypium hirsutum respectively) and found structural and biochemical alterations. Compared to controls in Faraday cages, exposed plant biomass was greatly reduced and leaf structure was only half as thick. Leaves were thinner and possessed greatly reduced chloroplasts which contributed to overall reduced vitality. Root systems were also adversely affected. They concluded that RFR is a stressor and noxious to plant life. A study of similar design [650] did not find the same effects on maize (Zea mays) which they attributed to that plant’s structural differences although chloroplasts were severely affected (see also Kumar et al. [651]).
Jayasanka and Asaeda [652] published a lengthy review that focused on microwave effects in plants. Studies indicate effects depend on the plant family and growth stage involved; and exposure duration, frequency, and power density, among other factors. They concluded that even for short exposure periods (<15 min to a few hours), nonthermal effects were seen that can persist for long periods even if initial exposures were very short. In addition, they noted that since base stations operate 24 h/day, neither short exposures nor recovery periods are possible in natural habitats as plants are continuously exposed throughout their life cycles. They said that variations in the power density and frequency of microwaves exert complex influences on plants, and that clearly diverse plant species respond differently to such factors. They concluded it is necessary to rethink the exposure guidelines that currently do not take nonthermal effects into consideration.
There are numerous reports of adverse RFR effects on mature flora. Waldman-Salsam et al. [653] reported leaf damage in trees near mobile phone towers/masts. In a detailed long-term field monitoring study from 2006 to 2015 in two German cities, they found unusual and unexplainable tree damage on the sides of trees facing the towers and correlated it to RFR measurements vs. control areas without exposures. They found that tree-side differences in measured values of power flux density corresponded to tree-side differences in damage. Controls, which consisted of 30 selected trees in low radiation areas without visual contact to any phone mast and power flux density under 50 μW/m2, showed no damage. They concluded that nonthermal RFR from mobile phone towers is harmful to trees and that damage that affects one side eventually spreads to the whole tree.
Vian et al. [642] published a review of plant interactions with high frequency RFR between 300 MHz and 3 GHz and noted that reports at the cellular, molecular, and whole plant scale included: numerous modified metabolic activities (reactive oxygen species metabolism, α- and β-amylase, Krebs cycle, pentose phosphate pathway, chlorophyll content, and terpene emission among others); altered gene expression (calmodulin, calcium-dependent protein kinase, and proteinase inhibitor); and reduced growth (stem elongation and dry weight) after nonthermal RFR exposure. They said changes occur in directly exposed tissues as well as systemically in distant tissues and proposed that high-frequency RFR be considered a genuine environmental factor highly capable of evoking changes in plant metabolism.
Halgamuge [627] also published a review that found weak non-thermal RFR affects living plants. The author analyzed data from 45 peer-reviewed studies of 29 different plant species from 1996 to 2016 that described 169 experimental observations of physiological and morphological changes. The review concluded that the data substantiated that RFR showed physiological and/or morphological effects (89.9%, p<0.001). The results also demonstrated that maize, roselle, pea, fenugreek, duckweeds, tomato, onions and mungbean plants are highly sensitive to RFR and that plants appear more responsive to certain frequencies between 800 and 1,500 MHz (p<0.0001); 1,500 and 2,400 MHz (p 0.0001); and 3,500 and 8,000 MHz (p=0.0161). Halgamuge [627] concluded that the literature shows significant trends of RFR influence on plants.
There is particular concern for impacts to flora and 5G since millions of small antennas mounted on utility poles, transmitting in MMW and other broadband frequencies, already are — or will soon be — in very close proximity to vegetation, creating both near- and -far field exposures. As noted in Halgamuge [627], the following are some studies investigating GHz frequencies already in use or planned for 5G that found significant effects on plants: Tanner and Romero-Sierra [654] on accelerated growth of Mimosa plant (10 GHz, 190 mW/cm2, 5–10 min); Scialabba and Tamburello [655] on reduced hypocotyls growth rate in radish (Raphanus sativus) (10.5 GHz, 8 mW or 12.658 GHz, 14 mW for 96 h); Tafforeau et al. [656] induced meristem (actively dividing group of cells) production in Linum usitatissimum (105 GHz for 2 h at 0.1 mW/cm2); and Ragha et al. [657] (9.6 GHz, 30 min) found germination depended on exposure parameters on Vigna radiata, Vigna aconitifolia, Cicer arietinum and Triticum aestivum plants. This is an area in immediate need of further investigation given the results from the previous studies.
A thorough review of RFR effects to trees and other plants was published by Czerwinski et al. [622] who reported that ecological effects on whole plant communities could occur at a very low exposure level of 0.01–10 μW/cm2 — certainly comparable to limits examined in this paper. They focused on frequencies between 0.7 and 1.8 GHz and included multiple complex indicators for plant types, biometrics, and environmental factors. It was the first comprehensive paper that extended beyond using narrower research methods. They noted that although the literature on the effects of RFR on plants is extensive, not a single field study had assessed the biological response at the level of a whole plant community, biome, or ecosystem, but rather focused mostly on short-term laboratory studies conducted on single species. They said, “…This dissonance is particularly striking in view of the fact that alterations in a plant community’s structure and composition have long been considered to be well founded, sensitive and universal environmental indicators.” The paper serves as a predictive model for complex future field studies on larger ecosystems.
Interesting EMF synergistic effects were found with static magnetic fields and bacteria in plants. Seeking non-chemical methods to improve seed germination after prolonged periods of storage when seed viability can deteriorate, Jovičić-Petrović et al. [658] studied the combined effects of bacterial inoculation (Bacillus amyloliquefaciens D5 ARV) and static magnetic fields (SMF, 90 mT, 5 and 15 min) on white mustard (Sinapis alba L.) seeds. Their results found that biopriming with the plant growth-promoting B. amyloliquefaciens increased seed growth by 40.43%. Seed response to SMF alone was dependent on treatment duration. While SMF at 5 min increased the germination percentage, exposure at 15 min lowered seed germination compared with the control. However, the negative effect at the longer exposure was neutralized when combined with the bacterial inoculation. Both germination percentages were significantly higher when SMF was combined with the bacteria (SMF, 5 min, + D5 ARV; and SMF, 15 min + D5 ARV; 44.68 and 53.20%, respectively) compared with control. They concluded that biopriming and SMF treatment gave better results than bacterial inoculation alone. The highest germination percentage — 53.20% of germinated seeds — was seen with the bacterium and 15 min exposure to 90 mT, demonstrating a synergistic effect. They concluded that such techniques can be used for old seed revitalization and improved germination.
Even aquatic plants have been found sensitive to artificial electric fields. Klink et al. [659] assessed electric field exposures on growth rates and the content of trace metals of Elodea canadensis. Plants were exposed in a laboratory to an electric field of 54 kV/m for seven days. Plant length and Fe, Mn, Ni, Pb, and Zn were measured. Results showed the applied electric fields slightly enhanced root growth. They also found changes in mineral absorption; Mn and Ni were significantly lower while Pb and Zn were significantly higher in exposed plants. Fe content did not differ between control and exposed plants. They concluded that electric fields had potential use for phytoremediation in trace metal contaminated waters. This study also has implications for long term aquatic plant health in general.
Also working with electric fields, Kral et al. [660] found fascinating regeneration in plant root tips in Arabidopsis at varying electric field exposures and time durations with the weaker exposures producing the most growth. They found that imposed electric fields can perturb apical root regeneration and that varying the position of the cut and the time interval between excision and stimulation made a difference. They also found that a brief pulse of an electric field parallel to the root could increase by up to two‐fold the probability of its regeneration, perturb the local distribution of the hormone auxin, and alter cell division regulation with the orientation of the root towards the anode or the cathode playing a role.
While mechanisms are still unclear regarding how EMFs affect plants, oxidative effects appear to play a significant role. Oxidative changes have been reported in many studies in plants after exposure to EMF [578, 639, 661], [662], [663], [664], [665], [666], [667], [668], [669], [670], [671]. EMF-related stress has been proposed by Vian et al. [641, 642], Roux et al. [672, 673], and Radhakrishma et al. [640]. Other mechanisms affecting plants such as ferromagnetism, radical-pairs, calcium ions and cryptochromes have also been proposed [674, 675].
It is apparent that plant growth and physiology — with their root systems anchored in the ground while their ‘heads’ manifest in the air — are affected by exposure to EMF in complex synergistic ways and that they are susceptible to multi-frequency exposures throughout their life spans.
Conclusion
Effects from both natural and man-made EMF over a wide range of frequencies, intensities, wave forms, and signaling characteristics have been observed in all species of animals and plants investigated. The database is now voluminous with in vitro, in vivo, and field studies from which to extrapolate. The majority of studies have found biological effects at both high and low-intensity man-made exposures, many with implications for wildlife health and viability. It is clear that ambient environmental levels are biologically active in all non-human species which can have unique physiological mechanisms that require natural geomagnetic information for their life’s most important activities. Sensitive magnetoreception allows living organisms, including plants, to detect small variations in environmental EMF and react immediately as well as over the long term, but it can also make some organisms exquisitely vulnerable to man-made fields. Anthropogenic EMF may be contributing more than we currently realize to species’ diminishment and extinction. Exposures continue to escalate without understanding EMF as a potential causative and/or co-factorial agent. It is time to recognize ambient EMF as a potential novel stressor to other species, design technology to reduce exposures to as low as reasonably achievable, keep systems wired as much as possible to reduce ambient RFR, and create laws accordingly — a subject explored more thoroughly in Part 3.
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Research funding: None declared.
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Author contributions: All authors have accepted responsibility for the entire content of this manuscript and approved its submission.
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Competing interests: Authors state no conflict of interest.
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Informed consent: Not applicable.
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Ethical approval: Not applicable.
Part 2: supplements
Supplement 1: Genetic Effects of RFR Exposure
Supplement 2: Genetic Effects at Low Intensity Static/ELF EMF Exposure
Supplement 3: Biological Effects in Animals and Plants Exposed to Low Intensity RFR
Supplement 4: Effects of EMF on plant growth
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