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ABSTRACT
Electricity, the interaction between electrically charged objects, is widely known to be fundamental to the functioning of living systems. However, this appreciation has largely been restricted to the scale of atoms, molecules, and cells. By contrast, the role of electricity at the ecological scale has historically been largely neglected, characterised by punctuated islands of research infrequently connected to one another. Recently, however, an understanding of the ubiquity of electrical forces within the natural environment has begun to grow, along with a realisation of the multitude of ecological interactions that these forces may influence. Herein, we provide the first comprehensive collation and synthesis of research in this emerging field of electric ecology. This includes assessments of the role electricity plays in the natural ecology of predator–prey interactions, pollination, and animal dispersal, among many others, as well as the impact of anthropogenic activity on these systems. A detailed introduction to the ecology and physiology of electroreception – the biological detection of ecologically relevant electric fields – is also provided. Further to this, we suggest avenues for future research that show particular promise, most notably those investigating the recently discovered sense of aerial electroreception.
I. INTRODUCTION
Electromagnetism is one of the four fundamental forces of the universe. Therefore, electromagnetic interactions inevitably influence the biotic world in a multitude of ways. There are two primary manifestations of electromagnetism: the magnetic field (magnetism), and the electric field (electricity); which when oscillating in synchronicity produce electromagnetic waves, i.e. light (Maxwell, 1865). For a summary and definition of the key electric and magnetic terminology used within this review, see Table 1. Whilst electromagnetic waves, and to some extent magnetic fields, have in many ways driven the rise and evolution of life on Earth, the influence of electric fields alone should not be understated.
Electricity, the interaction between electrically charged objects, is widely known to be fundamental to the functioning of living systems. However, this appreciation has largely been restricted to the scale of atoms, molecules, and cells. By contrast, the role of electricity at the ecological scale has historically been largely neglected, characterised by punctuated islands of research infrequently connected to one another. Recently, however, an understanding of the ubiquity of electrical forces within the natural environment has begun to grow, along with a realisation of the multitude of ecological interactions that these forces may influence. Herein, we provide the first comprehensive collation and synthesis of research in this emerging field of electric ecology. This includes assessments of the role electricity plays in the natural ecology of predator–prey interactions, pollination, and animal dispersal, among many others, as well as the impact of anthropogenic activity on these systems. A detailed introduction to the ecology and physiology of electroreception – the biological detection of ecologically relevant electric fields – is also provided. Further to this, we suggest avenues for future research that show particular promise, most notably those investigating the recently discovered sense of aerial electroreception.
I. INTRODUCTION
Electromagnetism is one of the four fundamental forces of the universe. Therefore, electromagnetic interactions inevitably influence the biotic world in a multitude of ways. There are two primary manifestations of electromagnetism: the magnetic field (magnetism), and the electric field (electricity); which when oscillating in synchronicity produce electromagnetic waves, i.e. light (Maxwell, 1865). For a summary and definition of the key electric and magnetic terminology used within this review, see Table 1. Whilst electromagnetic waves, and to some extent magnetic fields, have in many ways driven the rise and evolution of life on Earth, the influence of electric fields alone should not be understated.
see https://onlinelibrary.wiley.com/doi/full/10.1111/brv.12804 for table of terms
II. SOURCES OF ECOLOGICALLY RELEVANT ELECTRIC FIELDS
(1) Abiotic electric field sources
It is first important to consider the presence of electric fields of abiotic origin. Arguably, the primary abiotic electric field source experienced by terrestrial organisms on Earth is the atmospheric potential gradient (APG) (Hunting et al., 2021c). The APG is an electric field oriented vertically in the Earth's atmosphere, such that, within the vast majority of biologically inhabited altitudes (Imshenetsky, Lysenko & Kazakov, 1978; Womack, Bohannan & Green, 2010), the electric potential increases with altitude (Wilson, 1903). Near to the Earth's surface, in fair-weather conditions, the strength of the APG is on the order of 100 V m−1, but can increase by an order of magnitude, or even invert, during certain meteorological conditions, most notably thunderstorms (Wilson, 1903; Bennett & Harrison, 2007). The APG is largely created by a potential difference between the ionosphere and the Earth's surface and is constantly maintained by the global atmospheric electric circuit, wherein thunderstorms generate electric current upwards in the atmosphere, towards the ionosphere; this current is simultaneously counteracted elsewhere on the planet in fair-weather regions by gradual currents flowing back down to the ground (Rycroft, Israelsson & Price, 2000; Rycroft et al., 2012).
It is also worth mentioning the electrical charges of atmospheric precipitation. Individual raindrops generally carry non-negligible electrostatic charges (Wilson, 1903). These charges vary in polarity, even within the same rainfall, but negative charges appear to be marginally more common (Wilson, 1903; Chalmers & Pasquill, 1938; Chauzy & Despiau, 1980; Bennett & Harrison, 2007). The magnitude of charge carried is also highly variable but is typically in the region of 0.1–1000 pC, depending on meteorological conditions and the size of the raindrop (Banerji & Lele, 1932; Chalmers & Pasquill, 1938; Smith, 1955; Chauzy & Despiau, 1980). Snowflakes and hailstones have also been shown to carry electrostatic charges (Chalmers & Pasquill, 1938; Latham, Mason & Blackett, 1961).
In the aquatic environment, a major abiotic source of electric fields is the Earth's geomagnetic field. Whilst the geomagnetic field itself is not an electric field, any time-varying magnetic field will induce an electric field (Faraday, 1832; Maxwell, 1865). Therefore, because the geomagnetic field varies spatially, when water or animals move through the geomagnetic field, this can be viewed as a temporal variation in magnetic field from the reference point of the moving object, and therefore electric currents are electromagnetically induced in the water or animal (Kalmijn, 1974). The magnitudes of these motion-induced electric fields are not negligible, with a fish moving at 1 m s−1 likely to induce electric fields as strong as 0.4 μV cm−1, and electric fields induced by water motion typically measuring around 0.05–0.25 μV cm−1 (Barber & Longuet-Higgins, 1948; Kalmijn, 1974). By the same electromagnetic principles, temporal variations in the ambient magnetic field, for example those caused by magnetic storms, will similarly induce electric fields in the Earth's crust and mantle, including the oceans (Kalmijn, 1974). These are generally referred to as telluric, or Earth currents, and in coastal or continental shelf waters (where oceanic telluric currents are at their highest), they are typically on the order of 0.01 μV cm−1 in magnitude (Kalmijn, 1974).
(2) Electric fields around plants
Plants are known to be electrically conductive (Corbet, Beament & Eisikowitch, 1982; Gora & Yanoviak, 2015). Therefore, because they are connected into the ground, but protrude above it, the vertical electric field of the APG will cause accumulation of negative charges within the plant via electrostatic induction. This results in most plants usually exhibiting a negative surface potential relative to the surrounding air, and thus electric fields will be present around most plants exposed to the APG in typical conditions; a prediction backed up by measurements (Maw, 1962). The strength and shape of these electric fields is dependent largely on the morphology, height, and conductance of the plant, as well as the local atmospheric conditions and the structure of the nearby abiotic and biotic landscape. Typically, however, electric field magnitudes on the order of 1–100 kV m−1 within centimetres of the plant surface are likely (Bowker & Crenshaw, 2007b). Notably, plant parts with a high geometrical aspect ratio, such as reproductive floral structures, will exhibit the greatest local electric field strengths (Dai & Law, 1995; Vaknin et al., 2001), potentially reaching 1 MV m−1 or more within a few millimetres of the plant surface (Bowker & Crenshaw, 2007b). Furthermore, because of their electrical conductivity, plants, especially tall trees and vegetation, will shield large portions of their surroundings from the vertical APG, effectively nullifying, greatly reducing, or even inverting the electric field strength underneath their canopy (Arnold, Pierce & Whitson, 1965; Williams, Markson & Heckman, 2005; Clarke, Morley & Robert, 2017; Hunting, England & Robert, 2021b).
Individual pollen grains also carry electric charge (Vercoulen et al., 1992; Bowker & Crenshaw, 2007a). Available measurements suggest a typical magnitude of roughly 1 fC, with some pollen grains reaching charges as high as 40 fC (Bowker & Crenshaw, 2007a). Both positive and negative polarities of charge are reportedly common on pollen grains (Bowker & Crenshaw, 2007a), however, other studies have found negative pollen charges to be far more prevalent (Vercoulen et al., 1992).
Plants, especially those found in the aquatic environment, will additionally be electric field sources due to transmembrane potentials resulting from differences in electrochemical concentrations between the inside of the plant and its external surroundings. This is discussed in detail in Section II.4.
(3) Electrostatic charges of animals
Any electrically insulated object, including an animal, is likely to accumulate charge as it moves through its environment, via a mechanism known as triboelectrification, or the triboelectric effect. The triboelectric effect describes the phenomenon wherein the separation of two materials formerly in contact with each other results in an anti-symmetrical deposition of charge on their surfaces. Whilst this effect is usually small, with repetition such as when rubbing two materials against each other, significant differences in charge can be created. The same principle applies to animals walking across and brushing past objects in their environment, including friction with the air when in flight. As such, one would expect many, if not the majority of, animals in the terrestrial environment to carry non-negligible electric charges. This has long been noted in many taxa, but most comprehensively in insects, which tend to accumulate charges whilst in flight (Edwards, 1960a, 1962b; Erickson, 1975; Gan-Mor et al., 1995; Clarke et al., 2013), walking (McGonigle & Jackson, 2002; McGonigle, Jackson & Davidson, 2002; Jackson & McGonigle, 2005), or otherwise in contact with a surface (Edwards, 1962a; Colin, Richard & Chauzy, 1991). These charges are generally, but not exclusively, positive, which places insects near to the top of the triboelectric series (Edwards, 1962a; Clarke et al., 2017), meaning that they will almost always be electron donors in triboelectric interactions. Measures of the electric charge carried by an object or animal are given either as total charge, measured in Coulombs (C), or as surface potentials, measured in Volts (V). Comparison or conversion between the two quantities requires knowledge of the capacitance of the object or animal, measured in Farads (F). The typical electrostatic charges of insects range between 1 and 1000 pC (Fig. 1). Of note is the observation that the amount of charge carried by insects is generally higher in field measurements as compared to laboratory measurements (Montgomery, Koh & Robert, 2019).
Fig. 1
Ranges of net electrostatic charge measured on animals, taken from existing literature. From top to bottom: bumblebees, Bombus terrestris, N = 798 (Clarke et al., 2013; Montgomery, 2020); Anna's hummingbird, Calypte anna, N = 194 (Badger et al., 2015); red mason bee, Osmia bicornis, N = 85 (Montgomery, 2020); wintering honeybees, Apis mellifera, N = 352 (Colin et al., 1992); European peacock butterfly, Aglais io, N = 72 (S.J. England & D. Robert, in preparation); queen honeybee, N = 1, two replicates (Colin et al., 1992); foraging honeybees, N = 339 (Colin et al., 1992); housefly, Musca domestica, N = 10 (McGonigle & Jackson, 2002); common wasp, Vespula vulgaris, N = 18 (Montgomery, 2020); stingless bee, Scaptotrigona subobscuripennis, N = 144 (S.J. England & D. Robert, in preparation); paper wasp, Mischocyttarus spp., N = 22 (S.J England, X. Miranda & D. Robert, in preparation); European peacock caterpillar, N = 44 (S.J. England & D. Robert, in preparation); stingless bee, Tetragonisca angustula, N = 157 (S.J. England & D. Robert, in preparation); silverleaf whitefly, Bemisia tabaci, N = 40 (Lapidot et al., 2020); cinnabar caterpillar, Tyria jacobaeae, N = 5 (S.J. England & D. Robert, in preparation). Where exact minimum and maximum values were not provided in the source text, estimates of these values were extracted from figures.
Outside of insects, charges have been measured on hummingbirds as high as +800 pC (Badger et al., 2015). Furthermore, reptiles also build up significant positive charges (Vonstille & Stille III, 1994; Izadi, Stewart & Penlidis, 2014), with surface potentials purportedly on the order of 100–1000 V (Vonstille & Stille III, 1994). Electrostatic charges of mammals or amphibians have not been well characterised; however, it is known that the fur of cats and rabbits lies very near to the top of the triboelectric series (Clarke et al., 2017), meaning it readily accumulates positive charge. This likely applies to most mammalian taxa with keratinous fur. Amphibians are unlikely to accumulate significant electrostatic charge due to the presumably high conductivity of their moist skin, and the generally wet or very humid environments that they inhabit. Similarly, for fully aquatic fauna, accumulating electrostatic charge is challenging due to the higher electrical conductivity of the surrounding water, which allows for much faster dissipation of charge than in air.
(4) Transmembrane potentials, myogenic potentials, and electrogenesis
As a result of the biophysics and chemistry of the eukaryotic body, almost all animals and plants will be sources of electric fields irrespective of the triboelectric charging of their surfaces. These electric fields have two primary sources; transmembrane potentials, and myogenic potentials. Transmembrane potentials, defined here as the potential difference between the interior and exterior of an organism, exist around almost all living organisms, due to differences in electrochemical concentrations between the inside of the organism and its environment (Kalmijn, 1974). These electrochemical potentials largely arise from the active transport of ions through the outer wall of the organism, in the pursuit of maintaining internal homeostasis. Ultimately, these transmembrane potentials result in DC electric fields being emitted from most animals and plants. Generally, the magnitude of transmembrane potentials is low enough such that, due to the high resistivity of air, the resultant electric currents in the terrestrial environment are too weak to propagate over distances that would be considered ecologically relevant in most conceivable circumstances. However, the conductivity of water is sufficiently high to allow even very small potentials to generate notable electric currents within the surrounding water, and thus these electrical cues can propagate at higher magnitudes for greater distances in the aquatic environment. Transmembrane potentials, measured within 1 mm of the skin of a variety of vertebrate and invertebrate taxa, are typically on the order of 100 μV (Kalmijn, 1974; Wilkens & Hofmann, 2005), resulting in electric field strengths of around 100 μV cm−1 within 1 cm of the animal, decreasing to around 0.1 μV cm−1 at about 10 cm away (Kalmijn, 1974). The magnitude of transmembrane potentials is greatly increased around openings of the body cavity, such as the mouth, gills, and anus, as well as open wounds (Kalmijn, 1974). Of particular note is the order of magnitude increase in transmembrane potential observed in wounded crustaceans versus unwounded counterparts, rising to as high as 1250 μV, measured at 1 mm (Kalmijn, 1974). The electric field resulting from the transmembrane potential of animals will exhibit very low frequency modulations (typically less than 5 Hz), caused by body movement of the animal, as well as opening and closing of body cavity entrances, such as the gills (Kalmijn, 1974; Wilkens & Hofmann, 2005).
The second primary intrinsic source of electric fields around most eumetazoans is myogenic nervous activity. Specifically, the firing of action potentials within the muscles of animals produces electric fields that leak out into the surrounding environment. These external myogenic potentials are usually of slightly lower magnitude, but higher frequency, than transmembrane potentials; typically on the order of 10–100 μV with frequencies generally greater than 10 Hz (Kalmijn, 1974; Wilkens & Hofmann, 2005). Therefore, like transmembrane potentials, myogenic potentials do not produce significant currents in air, due to its low conductivity, but are able to propagate well in the aquatic environment.
In addition to these incidental electric fields produced by animals and plants, some fish actively generate electric fields with specialised organs. This is known as electrogenesis. There are two main types of electrogenic fish, the strongly electric fish, and the weakly electric fish. Strongly electric fish produce electric potentials from around 10 V up to 860 V (Bennett, 1971a; Zupanc & Bullock, 2005; de Santana et al., 2019), whereas the weakly electric fish generally produce potentials on the order of 100–1000 mV (Bennett, 1971a; Zupanc & Bullock, 2005). Electrogenesis in both strongly and weakly electric fish is performed by modified muscle and nerve tissues, known as the electric organ (Bennett, 1971a). The potentials produced by the electric organ are referred to as electric organ discharges (EODs) and originate from the cumulative contribution of many electrocytes; specialised cells that produce electric potentials by actively transporting large quantities of ions across their membranes (Bennett, 1971a; Crampton, 2019). Whilst the transmembrane potentials produced by electrocytes are not markedly different from other cells, it is their structural arrangement and synchronicity in firing that is largely responsible for the remarkable external potentials produced by the electric organ in its entirety. The EODs of strongly electric fish are of high enough magnitude such that they can constitute a stunning or startling function (discussed in Section III.2), whereas in the weakly electric fish, they facilitate active electroreception and communication (discussed in detail in Section IV.2). The category of weakly electric fish can be further divided into pulse-type and wave-type varieties. Pulse-type animals produce EODs in pulses, which are relatively brief in comparison to the length of electrical silence between them. On the other hand, wave-type fish generate EODs in a quasi-sinusoidal pattern, in which pulses and silences are of comparable length to each other (Zupanc & Bullock, 2005). A small number of fish species are capable of producing both strongly and weakly electric EODs, with separate electric organs (Bennett, 1970, 1971a).
(5) Anthropogenic electric field sources
As with almost all aspects of ecology in the modern day, it is also important to discuss the presence and impact of anthropogenic factors, and therefore anthropogenic electric field sources warrant discussion. Electric fields of human origin have increased exponentially since the industrial revolution, with almost every electrical appliance, device, or infrastructure component emitting electric fields into the environment to some degree. The most significant anthropogenic electric field source is high-voltage power cables and transmission lines, both above ground and sub-marine. In the terrestrial environment, overhead transmission lines are typically held at voltages on the order of 100 kV, higher than 750 kV in some cases, and as such can produce electric fields in excess of 30 kV m−1 at ground level (Repacholi & Greenebaum, 1999; Gonen, 2011). Some household appliances are also capable of producing electric field strengths of this magnitude at very short distances, but more typically these fields are on the order of 100 V m−1 (Repacholi & Greenebaum, 1999). In the aquatic environment, subsea cables are emerging as an increasingly prevalent anthropogenic electric field source due to the acceleration in development of offshore energy production. Whilst the cables are usually insulated and shielded to prevent current and electric field leakage, magnetic fields produced by the current in the cable are still emitted into the surrounding water, which subsequently can create electric fields in the water via electromagnetic induction. These induced electric fields are thought to have magnitudes between 0.5 and 100 μV m−1 (Gill, Bartlett & Thomsen, 2012), which although seemingly small compared to values in the terrestrial environment, are well within the detection ranges of most aquatic electroreceptive organisms (Peters, Eeuwes & Bretschneider, 2007).
In the context of anthropogenic electric field sources, it is also worth mentioning the triboelectric properties of synthetic materials. Generally speaking, synthetic materials and fibres sit at very extreme ends of the triboelectric series, meaning that they often build up negative or positive charges at much greater magnitudes than naturally occurring materials (Henniker, 1962; Zou et al., 2019). The consequence of this is that the electric fields around clothed humans, as well as many anthropogenic structures, are likely to be much higher in magnitude than those around similarly sized animals or natural structures.
III. THE PHYSICAL ECOLOGY OF ELECTRIC FIELDS
The presence of electric fields around organisms and in the environment has many potential ecological consequences. Whilst electroreception provides some of the more complex and well-studied examples of the influence of electric fields at the ecological scale, there are many more underappreciated facets of electric ecology that do not involve the biological detection of electric fields. Instead, these functional aspects relate to physical electrical interactions between organism(s) and their environment; termed here the ‘physical ecology’ of electric fields. An overview of our current knowledge of this physical, non-sensory, ecology is provided herein.
(1) Electrostatics in pollination and seed dispersal
This publication is very long and thorough those interested can continue reading the published paper at: https://onlinelibrary.wiley.com/doi/full/10.1111/brv.12804 free of charge.
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