Anthropogenic Radiofrequency Electromagnetic Fields as an Emerging Threat to Wildlife Orientation

Abstract

The rate of scientific activity regarding the effects of anthropogenic electromagnetic radiation in the radiofrequency (RF) range on animals and plants has been small despite the fact that this topic is relevant to the fields of experimental biology, ecology and conservation due to its remarkable expansion over the past 20years. Current evidence indicates that exposure at levels that are found in the environment (in urban areas and near base stations) may particularly alter the receptor organs to orient in the magnetic field of the earth. These results could have important implications for migratory birds and insects, especially in urban areas, but could also apply to birds and insects in natural and protected areas where there are powerful base station emitters of radiofrequencies. Therefore, more research on the effects of electromagnetic radiation in nature is needed to investigate this emerging threat.
Copyright © 2015 Elsevier B.V. All rights reserved.

Full text

Short communication
Anthropogenic radiofrequency electromagnetic fields as an emerging
threat to wildlife orientation
Alfonso Balmori
Consejería de Medio Ambiente, Junta de Castilla y León, C/ Rigoberto Cortejoso, 14, 47071 Valladolid, Spain
HIGHLIGHTS
•The growth of wireless telecommunication technologies causes increased electrosmog.
•Radio frequency fields in the MHz range disrupt insect and bird orientation.
•Radio frequency noise interferes with the primary process of magnetoreception.
•Existing guidelines do not adequately protect wildlife.
•Further research in this area is urgent.
abstractarticle info
Article history:
Received 5 J anuary 2015
Received in revised form 20 February 2015
Accepted 22 February 2015
Available online xxxx
Editor: P. Kassomenos
Keywords:
Ecological effect
Electromagnetic field exposure
Environmental pollution
Magnetic compass
Nonthermal effects
Orientation
The rate of scientific activity regarding the effects of anthropogenic electromagnetic radiation in the radiofre-
quency (RF) range on animals and plants has been small despite the fact that this topic is relevant to the fields
of experimental biology, ecology and conservation due to its remarkable expansion over the past 20 years.
Current evidence indicates that exposure at levels that are found in the environment (in urban areas and near
base stations) may particularly alter the receptor organs to orient in the magnetic field of the earth. These results
could have important implications for migratorybirds and insects, especially in urban areas, but could also apply
to birds and insects in natural and protected areas where there are powerful base station emitters of
radiofrequencies. Therefore, more research on the effects of electromagnetic radiation in nature is needed to
investigate this emerging threat.
© 2015 Elsevier B.V. All rights reserved.
Different animal groups are sensitive to low frequency electromag-
netic fields, and many species with receptor organs are provided with
important orientation cues from natural electric fields (Kalmijn, 1988).
Animals can use the direction of the magnetic field as a compass and
the intensity of the magnetic field as a component of the navigational
map, with light-dependent reactions in specialised photo-pigments
and reactions involving small crystals of magnetite, using one of these
systems, or both simultaneously, depending on the animal groups
(Kirschvink et al., 2001; Johnsen and Lohmann, 2005; Wiltschko et al.,
2007; Hsu et al., 2007; Ritz et al., 2009; Wajnberg et al., 2010).
Some insects, like bumblebees (Bombus terrestris), can interact with
floral electric fields and electric field sensing constitutes a potentially
important sensory modality. The perception of weak electric fields by
bees in nature, which should be considered alongside vision and
olfaction, may have an adaptive value (Clarke et al., 2013). An applied
static magnetic field affects circadian rhythms, magnetosensitivity and
orientation of insects throughcryptochromes, and a prolonged weaken-
ing of the geomagnetic field affects the immune system of rats (Roman
and Tombarkiewicz, 2009; Yoshii et al., 2009).
In the radiofrequency range, the rapid development and increased
use of wireless telecommunication technologies led to a substantial
change in the radio-frequency electromagnetic field (RF-EMF) exposure
(Levitt and Lai, 2010). This increased exposure was most consistently
observed in outdoor areas due to emissions from radio and mobile
phone base stations (Urbinello et al., 2014). Current evidence indicates
that exposure at levels found in the environment (in urban areas and
near base stations), may particularly alter the receptor organs to orient
in the magnetic field of the earth, although the species conservation
implications are unknown. Radio frequency fields in the MHz range dis-
rupt birds' orientation interfering directly with the primary processes of
magnetoreception and therefore disable the avian compass as long as
Science of the Total Environment 518–519 (2015) 58–60
E-mail addresses: balmaral@jcyl.es,abalmorimartinez@gmail.com.
http://dx.doi.org/10.1016/j.scitotenv.2015.02.077
0048-9697/© 2015 Elsevier B.V. All rights reserved.
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they are present (Wiltschko et al., 2014). Ritz et al. (2004 & 2009) re-
ported the sensitivity for orientation of European robins (Erithacus
rubecula) to radiofrequency magnetic fields. The orientation of migrato-
ry birds is disrupted when very weak high-frequency fields (broad-
band field of 0.1–10 MHz of 85 nT or a 1.315 MHz field of 480 nT) are
added to the static geomagnetic field of 46.000 nT (Thalau et al.,
2006). It was convincingly demonstrated that robins are unable to use
their magnetic compass in the presence of urban electromagnetic radio-
frequency noise in the frequency range of 2 kHz–5MHz(Engels et al.,
2014). Therefore, electrosmog scrambles birds' magnetic sense and
this finding could inform policies written to protect the habitats of en-
dangered species.
As with birds, radio frequency magnetic fields disrupt magneto-
reception in insects. The geomagnetic field reception in American
cockroach is sensitive to weak radio frequency field causing a disruptive
effect (Vacha et al., 2009), so these authors suggest that electromagnetic
smog will have to be taken more seriously in animal magnetoreception
experiments. In an experimentally-generated electromagnetic field of
about 1 V/m with a realistic (and even lower) power intensity similar
to those surrounding communication masts, the results and observa-
tions suggest that GSM (Global System for Mobile communications)
900 MHz radiation might have a severe impact on the nerve cells of
exposed ants, especially affecting the visual and olfactory memory,
causing the loss of their ability to use visual cues and suggesting that
electromagnetic radiation may have an impact on the orientation be-
haviour and navigation of animals that use magnetic fields to find
their way (Cammaerts et al., 2012, 2014). Honeybees are sensitive to
pulsed electromagnetic fields generated by mobile phones and observ-
able changes in the bee behaviour could be one explanation forthe loss
of colonies (Favre, 2011). Magnetoreception system in Monarch butter-
fly orientation (Guerra et al., 2014) may be also suffering interference
with anthropogenic radio frequency magnetic fields and this, together
with other factors (Brower et al., 2012), may be a cause of their popula-
tion decline.
Electromagnetic fields act via activation of voltage-gated calcium
channels (Pall, 2013). Changes in the size of the magnetic granules
upon applying additional magnetic field to the cells of Apis mellifera
were observed, and this size fluctuation triggered the increase of cal-
cium intracellular (Hsu et al., 2007). Therefore, we may hypothesise
that some of the disruptive effects of radio frequency fields on the
orientation of animals may be related to the interference with calcium
channels.
An aversive effect on bats has been found in habitats exposed to ra-
diofrequency radiation (1–4 GHz) when compared with matched sites
where no such radiation can be detected (Nicholls and Racey, 2009).
Cattle exposed to radiofrequency emissions (900 MHz) from nearby
base stations may suffer changes in the redox proteins and enzyme ac-
tivities. It was also found that some are sensitive to radiation, while
others are not (Hässig et al., 2014).
Exposure to low intensity radiation can have a profound effect on
biological processes (Bolen, 1994). Although there is a good degree of
evidence on the injurious effects of radiofrequency electromagnetic
fields on the immune system, pineal gland, circadian rhythm, oxidative
stress and teratogenicity, these topicsremain controversial (Lerchl et al.,
2008; Takahashi et al., 2009; Jinet al., 2012; Qin et al., 2012; Bilgici et al.,
2013; Tsybulin et al., 2013; Yakymenko et al., 2014; Cao et al., 2015).
Conversely, there is a scientific agreement regarding harmful effects of
radio frequency radiation on human reproduction (Adams et al.,
2014). Low-voltage electricity current-generated electromagnetic field
can produce a significantly negative effect on the breeding success of
birds (Ciconia ciconia) nesting directly on electricity lines (Vaitkuvienė
and Dagys, 2014) and these same results have been found in nests ex-
posed to radiofrequency radiation near phone masts (Balmori, 2005).
The health risk of electromagnetic fields to aquatic organisms
needs to be addressed (Lee and Yang, 2014). The potential interac-
tions between diadromous fishes of conservation importance and
the electromagnetic fields and subsea noise from marine renewable
energy developments are being studied (Gill et al., 2012).
In a systematic review of published scientific studies on the potential
ecological effects of radiofrequency electromagnetic fields (RF-EMF) in
the range of 10 MHz–3.6 GHz, about two thirds of the reviewed studies
show ecological effects of RF-EMF at high, as well as at low, dosages
(Cucurachi et al., 2013). The low dosages are compatible with real
field situations, and could be found under environmental conditions
(Cucurachi et al., 2013; Balmori, 2014). However, studies conducted in
real field situations must be made with a sufficient experimental expo-
sure time, since results with a short period of exposure are likely to be
ambiguous (e.g. 48 h in Vijver et al., 2013).
A limited number of studies have addressed the effects of radio-
frequency radiation on plants indicating that these effects depend
on the plant family, growth stage, exposure duration, frequency,
and power density, among other factors (Senavirathna and Takashi,
2013; Halgamuge et al., 2015). There are two papers warning on neg-
ative effects of radio frequencies from mobile phone masts on trees
(Balmori, 2004; Waldmann-Selsam and Eger, 2013) and researchers
have found very worrying effects in laboratory studies (Pesnya and
Romanovsky, 2013). The results of these preliminary findings indi-
cate that further research on this topic is extremely urgent.
Theseresultscouldhaveimportant implications for wildlife, es-
pecially in urban and suburban areas, but also in rural, natural and
protected areas where there are powerful base station emitters of
radiofrequencies (Bürgi et al., 2014). Such effects have not yet been
examined, but the consequences continue due to the fact that the
existing guidelines of public health protection only consider the effects
of short-term thermal exposure (Hyland, 2000) and do not adequately
protect wildlife. EMF safety standard should be based on the more
sensitive, natural biological response (Blank, 2014). Therefore, more
research on the effects of electromagnetic radiation in nature is needed
to investigate this emerging threat (Balmori, 2014).
Acknowledgements
The author is grateful to J.L. Telleria, D.O. Carpenter, R. Carbonell and
S. Wright for their help and advice. The author reports no conflicts of
interest.
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