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Electromagnetic Biology and Medicine, 26: 63–72, 2007
DOI: 10.1080/15368370701205693
The original publication is available at www.informaworld.com
A Possible Effect of Electromagnetic Radiation
from Mobile Phone Base Stations on the Number
of Breeding House Sparrows (Passer domesticus)
JORIS EVERAERT
AND
DIRK BAUWENS
Research Institute for Nature and Forest, Brussels, Belgium
A possible effect of long-term exposure to low-intensity electromagnetic radiation from mobile
phone (GSM) base stations on the number of House Sparrows during the breeding season was
studied in six residential districts in Belgium. We sampled 150 point locations within the 6 areas
to examine small-scale geographic variation in the number of House Sparrow males and the
strength of electromagnetic radiation from base stations. Spatial variation in the number of House
Sparrow males was negatively and highly significantly related to the strength of electric fields
from both the 900 and 1800MHz downlink frequency bands and from the sum of these bands
(Chi²-tests and AIC-criteria, P < 0.001). This negative relationship was highly similar within each
of the six study areas, despite differences among areas in both the number of birds and radiation
levels. Thus, our data show that fewer House Sparrow males were seen at locations with
relatively high electric field strength values of GSM base stations and therefore support the
notion that long-term exposure to higher levels of radiation negatively affects the abundance or
behavior of House Sparrows in the wild.
Keywords Antenna; Bird; Electromagnetic radiation; GSM base station; Non thermal effect.
Address correspondence to Joris Everaert, Research Institute for Nature and Forest,
Kliniekstraat 25, B-1070 Brussels, Belgium; E-mail: joris.everaert@inbo.be
Introduction
Mobile phones, also called cellular phones or handies, are now an integral part of modern life.
The widespread use of mobile phones has been accompanied by the installation of an increasing
number of base station antennas on masts and buildings. GSM base stations emit electromagnetic
fields at high frequencies in the 900 and 1800 MHz range (= downlink frequency bands), pulse
modulated in low frequencies (Hyland, 2000). In recent years, increased public awareness and
scientific research have questioned to what extent the non thermal exposure to low-intensity
electromagnetic fields may affect the health, reproduction, well-being and behaviour of humans
and other organisms. There is an active and, as yet, unsettled controversy about current safety
standards. Some researchers and national committees advised more stringent safety standards,
based on experimental data with reported biological effects from (chronic) non thermal exposures
(Hyland, 2000; Belyaev, 2005a, b).
There are studies showing frequency-specific biological effects, and studies demonstrating
that a high frequency signal modulated at certain low frequencies, or a signal that is pulsed, has
more harmful effects than an unmodulated, steady carrier. These so-called ‘window effects’
greatly complicate any attempt to understand the relationship between electromagnetic radiation
and health (Adey, 1981; Hyland, 2000; Lai, 2005; Belyaev, 2005a).
Public and scientific concern were also raised by results of some epidemiologic studies that
examined the effects of long-term exposure on humans living near mobile phone base stations. A
growing number of studies point to the existence of effects, ranging from changes in cognitive
performance and sleep disturbances to serious illness and disablement, with even higher cancer
rates (Santini et al., 2002; Navarro et al., 2003; Bortkiewicz et al., 2004; Eger et al., 2004; Wolf
and Wolf, 2004; Hutter et al., 2006; Abdel-Rassoul et al., 2006).
Short-term laboratory experiments used mice, rats, chickens and other birds as study models
to better understand the possible implications of electromagnetic fields on organismal
functioning. In many studies however, ‘mobile communication-like’ signals were investigated
that in fact were different from the real exposures in such aspects as intensity, carrier frequency,
modulation, polarisation, duration and intermittence (Belyaev, 2005a, b; Lai, 2005).
Studies of the effects of exposure to electromagnetic fields on populations of wild birds can
provide further insights into the potential impacts on animal and human health (Fernie and
Reynolds, 2005). Birds are candidates for being good biological indicators for low-intensity
electromagnetic radiation: they have thin skulls, their feathers can act as dielectric receptors of
microwave radiation, many species use magnetic navigation, they are very mobile and possible
psychosomatic effects are absent (Bigu-del-Blanco and Romero-Sierra, 1975; Balmori, 2005).
Field studies of wild populations can also reveal possible effects of long-term exposure to
radiation from GSM base stations. In addition, species like the House Sparrow (Passer
domesticus) are especially of interest because a large proportion of the birds use higher breeding
height locations like roof spaces (Wotton et al., 2002) where potentially higher levels of base
station radiation are present.
Here we report results of a preliminary study that explored putative effects of electromagnetic
radiation emitted by mobile phone base stations on the number of House Sparrows during the
breeding season. Specifically, we examined small-scale geographic variation within each of six
study areas in both the number of birds and the strength of electromagnetic radiation. If
electromagnetic fields from GSM base stations have adverse effects on bird populations, this
should result in a decreasing number of House Sparrows with increasing levels of radiation.
Materials and Methods
Data collection
We determined, during the spring of 2006, the number of House Sparrow males and the strength
of electromagnetic radiation from mobile phone (GSM) base stations at 150 locations that were
distributed over six residential areas in the region of Gent – Sint-Niklaas (province of East
Flanders, Belgium). The study areas were similar in overall appearance, with abundant hedges,
bushes and other vegetation between the houses, and with one or more GSM base stations nearby.
The 150 study locations were selected in advance as points on a map (ArcGIS). All locations
were situated along small roads within the residential areas and were at variable distances from
the nearest GSM base station (mean = 352 m, range = 91 - 903 m, about 90% at 100 - 600 m).
The number of locations, and study dates, within each area were: Lokeren - Eksaarde (N = 19;
April 9), Lokeren - Spoele (N = 27, April 15), Lokeren - Bergendries (N = 17, April 17), Sint
Niklaas - Clementwijk (N = 25, April 20), Gent- Wondelgem (N = 38, April 25) and Gent -
Mariakerke (N = 24, April 26).
At each location, a point count of five minutes (see ‘point transect count’ in Bibby et al., 2000;
Hustings et al., 1985) was made of the number House Sparrow males that were singing or
otherwise visible within a distance of ca. 30 m. Sightings of birds were done with binoculars
(Swarovski EL 10x42). Counts were restricted to the morning hours (7-11h), when male House
Sparrows are most active (Hustings et al., 1985; Van Dijk, 2004), on days with favourable
weather conditions (no rain, little wind, sunny, normal temperatures).
Simultaneously, we measured the maximum value (peak hold) of the electric field strength (in
V/m) from the downlink frequencies of GSM 900 MHz (925-960 MHz) and GSM 1800 MHz
(1805-1880 MHz) base station antennas. Measurements at each location were made during two
minutes for each frequency band. The electric field strength was measured using a portable
calibrated high-frequency spectrum analyser (Aaronia Spectran HF-6080; typ. accuracy ± 3 dB)
with calibrated EMC directional antenna (HyperLOG 6080; logarithmic-periodic). To measure
the maximum radiation values, the EMC antenna was turned around in all directions.
Additional antennas for the new UMTS-system are now being installed on several existing
base stations in Belgium. Therefore, at several locations within each study area, the electric field
strength from the downlink frequencies of UMTS antennas (2110-2170 MHz) was also checked,
but no significant signals were found. Consequently, the UMTS variable was not taken into
account for further analysis.
Data analyses
The sum (Egsm) of the measured GSM 900 MHz (Egsm900) and 1800 MHz (Egsm1800) electric
field strength values was calculated using the formula: Egsm = Egsm900² + Egsm1800²
(Electronic Communications Committee, 2003). Prior to all analyses, the electric field strength
variables were logarithmically transformed to achieve normality of their frequency distributions.
We explored relations between the number of House Sparrow males (dependent variable) and
each of the three electric field strength variables. As the dependent variable consists of count data
and is hence discontinuous, standard regression (or correlation) techniques are inappropriate.
Instead, we used Poisson regressions (i.e., generalized linear models) with a log link function to
examine putative relationships. Preliminary analyses indicated that significant variation among
the six study areas was present for all variables (ANOVA, P < 0.001). Therefore we included
“area” as a categorical factor in all models and considered it to be a proxy for all unknown, and
hence unmeasured variables causing among area variation in the number of House Sparrows
(e.g., habitat characteristics, food availability, temporal differences among censuses). Statistical
analyses were done with S-PLUS v. 6.2.
Results
The number of House Sparrow males varied between zero and four at the different locations. The
measured electric field strengths were seldom higher than 1 V/m, and most often well below that
value (Table 1).
To explore the putative effects of area, electric field strength and their interaction on the
number of House Sparrows, we performed separate analyses for each of the three radiation
variables. As no significant interaction effect between area and electric field strength was
detected in any of the three analyses (Chi²-tests and AIC-criteria, P > 0.20), we excluded the
interaction term from further treatments. The final regression models were highly similar for the
three electric strength variables. They revealed significant variation among study areas (Chi²-
tests, P < 0.001), and a highly significant negative effect of electric field strength on the number
of House Sparrow males (Chi²-tests and AIC-criteria, P < 0.001; Figure 1). Estimates of the
scaled deviance (1.06 – 1.14) were very close to 1, and examination of the regression residuals
revealed no clear patterns or deviations from normality. These observations indicate an adequate
fit of the models to the data.
Table 1
Summary statistics (mean, 95% confidence interval, range) of the number of House Sparrow
males and electric field strength variables in the six study areas. Means and confidence limits of
the radiation variables were calculated after back-transformation of the logarithmically
transformed data; the confidence intervals are therefore asymmetrical around the mean
Study area
Number of
House Sparrow
males
E
gsm900
(V/m)
E
gsm1800
(V/m)
E
gsm
(V/m)
1: Lokeren - Eksaarde mean 1.5 0.153 0.075 0.193
95% CI 0.8 – 2.2 0.108 - 0.216 0.046 - 0.123 0.139 - 0.270
Min - Max 0 – 4 0.036 - 0.494 0.015 - 0.333 0.052 - 0.505
2: Lokeren - Spoele mean 1.9 0.084 0.083 0.130
95% CI 1.5 – 2.3 0.059 - 0.120 0.058 - 0.120 0.091 - 0.183
Min - Max 0 – 4 0.008 - 0.327 0.013 - 0.394 0.016 - 0.412
3: Lokeren - Bergendries mean 0.8 0.245 0.017 0.247
95% CI 0.3 - 1.3 0.186 - 0.323 0.009 - 0.031 0.187 - 0.327
Min - Max 0 - 3 0.052 - 0.537 0.004 - 0.125 0.052 - 0.551
4: Sint Niklaas - Clementwijk mean 1.0 0.130 0.056 0.148
95% CI 0.6 - 1.4 0.098 - 0.173 0.039 - 0.082 0.111 - 0.197
Min - Max 0 - 3 0.019 - 0.412 0.009 - 0.231 0.021 - 0.469
5: Gent - Wondelgem mean 1.3 0.109 0.040 0.121
95% CI 0.9 - 1.6 0.079 - 0.151 0.030 - 0.054 0.089 - 0.165
Min - Max 0 - 4 0.016 - 1.006 0.009 - 0.321 0.022 - 1.056
6: Gent - Mariakerke mean 0.8 0.043 0.080 0.160
95% CI 0.3 - 1.2 0.024 - 0.078 0.049 - 0.130 0.107 - 0.240
Min - Max 0 - 4 0.006 - 1.022 0.017 - 0.824 0.040 - 1.023
Figure 1. Scatterplots of the observed number of House Sparrow males as a function of the sum
(Egsm) of GSM 900 MHz and GSM 1800 MHz electric field strength values (logarithmic scale)
at the different locations within each of the six study areas. Regression lines were obtained by
Poisson regressions and incorporated the effects of area and radiation intensity (see text).
We further explored the separate effects of electromagnetic radiation at the two frequencies by
modelling the number of House Sparrow males as a function of area, electric field strength at 900
MHz, electric field strength at 1800 MHz, and their interactions. The final model retained
included highly significant effects of area and the two electric field strengths (Chi²-tests and AIC-
criteria, P < 0.001) and a marginally significant interaction effect between both field strengths
(Chi²-test, P = 0.02). This strongly suggests that the electromagnetic radiations at both
frequencies have complex additive effects on the number of House Sparrow males.
Overall, analyses indicated that the strength of all three radiation variables decreased with
increasing distance to the nearest base station (F-tests, P < 0.001). We therefore examined
whether the negative relation between the number of birds and strength of radiation was induced
by variation among sampling locations in the distance to GSM base stations. Upon adding
distance to the nearest base station as an additional factor to the regression models that included
area and electric field strength, distance did not account for a significant portion of the residual
variation (Chi²-tests and AIC-criteria, P > 0.50). Conversely, when we forced distance as the first
factor into the regression equations, both area and radiation strength were subsequently selected
as highly significant factors (Chi²-tests and AIC-criteria, P < 0.001).
Discussion
Our results indicate that spatial variation among sampling locations in the number of House
Sparrow males was negatively related to the strength of electric fields emitted by GSM base
stations. Importantly, this relation was highly similar among the six study areas, as evidenced by
the non-significant interaction effects between area and electric field strength, despite differences
among areas in both the number of birds and radiation levels. Moreover, the negative association
was detected for electric field strengths from both the 900 and 1800 MHz frequency bands and
from the sum of these frequency bands. Our analyses also revealed that the negative relation
between the number of birds and strength of radiation was not a simple consequence of
differences among sampling locations in distances to the nearest GSM base station. This can
probably be attributed to variations in the orientation, position and number of antennas and to the
shielding effects and multiple reflections from structures like buildings and trees, which affect
local levels of exposure to electromagnetic radiation. Thus, our data show that fewer House
Sparrow males were seen at locations with relatively high electric field strength values of GSM
base stations and therefore support the notion that long-term exposure to higher levels of
radiation negatively affects the abundance or behaviour of House Sparrows in the wild.
Nevertheless, our study should be considered as preliminary for several reasons. First,
sampling locations were each visited only once, such that counts of the number of House
Sparrow males and measurements of electric field strength are subject to some variation and
estimation error. However, it is most likely that these errors are randomly distributed among
locations. We also note that a single visit during the peak of the breeding season (April – May) is
considered to be adequate to locate House Sparrow breeding territories (Hustings et al., 1985;
Van Dijk, 2004). Second, because of the short study period, we ignore whether differences in bird
counts reflect variation in abundance of breeding birds or in short-term behavioural responses
like the tendency to sing. However, a decrease in singing intensity will result in a decrease of
reproductive success and ultimately a decline of population size. Third, only the radiation from
GSM base station antennas was measured. Probably, the distribution of possible other significant
electromagnetic signals will be random, but due to the lack of measurements in other frequency
bands (except for UMTS), this remains an object of further study. Fourth, as with all descriptive
field studies, we cannot provide evidence for a causal relationship between radiation levels and
the number of birds. Nevertheless, the fact that we found a highly similar pattern in each of the
six study areas strengthens the possibility that the relationship is not a spurious one.
There are several unpublished and anecdotal reports about birds and mobile phone base
stations, but we know of only one other published study that examined the effects of
electromagnetic radiation from mobile phone base stations on wild bird populations. Balmori
(2005) found a significantly lower number of White Stork (Ciconia ciconia) fledglings in nests
exposed to relatively high electromagnetic radiation (2.36 ± 0.82 V/m) than in nests receiving
lower levels of radiation (0.53 ± 0.82 V/m). Together with observations on aberrant behaviours of
the adult birds, these results suggest that electromagnetic radiation interferes with reproduction in
this wild population.
What could be the underlying mechanisms of the (putative) negative effects of radiation from
GSM base stations on wild bird populations? Because all measured electric field strength values
were far below what is required to produce heating as low as 0.5 °C (i.e., 10 mW/cm² or ca. 194
V/m; Bernhardt, 1992), the effects should be considered as non thermal at very low intensities.
Non thermal effects of microwaves on birds were reported already 40 years ago (Tanner,
1966; Tanner et al., 1967). Most studies indicate that exposure of birds to electromagnetic fields
generally changes, but not always consistently in effect or in direction, their behaviour,
reproductive success, growth, development, physiology, endocrinology, and oxidative stress
(Wasserman et al., 1984; Grigor’ev et al., 2003; Fernie and Reynolds, 2005). Of special relevance
within the context of our research are laboratory studies that demonstrate negative effects of
electromagnetic radiation from mobile phones on the development and survival of bird embryo’s
(Farrel et al., 1997; Youbicier-Simo and Bastide, 1999; Grigoriew, 2003).
Bird feathers are known to act as dielectric receptors of high frequency electromagnetic fields
and some experiments indicate that audiofrequency pulse-modulated high frequency fields may
induce piezoelectric effects in the feathers (Bigu-del-Blanco and Romero-Sierra, 1975a, b). These
results are important in view of the fundamental role that feathers play in the life of birds and in
the influence of environmental factors on bird behaviour. Experiments also indicated that
microwave radiation can have the same averse effects on birds in flight as those observed in
caged birds (Romero-Sierra et al., 1969).
Several bird species also use magnetic navigation (Liboff and Jenrow, 2000; Muheim et al.,
2006) and can become disorientated when exposed to weak (< 1/50 of geomagnetic field
strength) high frequency magnetic fields (Ritz et al., 2004; Thalau et al., 2005). The available
evidence concerning magnetoreception suggests that birds use a radical pair mechanism for a
chemical compass, and a mechanism based on magnetite particles (Wiltschko and Wiltschko,
2005; Mouritsen and Ritz, 2005). Magnetite is an excellent absorber of microwave radiation at
frequencies between 0.5 and 10.0 GHz through the process of ferromagnetic resonance
(Kirschvink, 1996), so that interaction with electromagnetic fields from mobile phone base
stations might be possible.
In an experiment with Zebra Finches (Taenopygia guttata) that were temporary (10 minutes)
stimulated with a pulsed electromagnetic field similar to the signal produced by mobile phones
with carrier frequency 900 MHz, significant non thermal changes in the amount of neural activity
by more than half of the brain cells were detected (Beasond and Semm, 2002). The effect did not
appear tot be limited to magnetic sensory cells, but occurred in any part of the brain. The authors
postulate that similar neural responses to different frequencies point toward a common
mechanism of low frequency modulation, perhaps at the cell membrane. Such a stimulus might
mimic a natural mechanism involved in cell communication. Although the peak electric field
strength used in that experiment (0.1 mW/cm² = approx. 19 V/m; Beasond and Semm, 2002) was
higher than the values measured in our study, results from other studies indicate that a long-term
exposure at low intensities can produce the same effects as a short-term exposure at higher
intensity (D’Andrea et al., 1986a, b; Lai, 2005; Belyaev, 2005a). This suggests that the non
thermal effects of relatively weak electromagnetic radiation from mobile phone base stations can
accumulate over time and have significant implications, as detected by several pilot
epidemiological studies on humans (see Introduction).
Radiation from GSM base stations may also affect the local abundance of insects or other
invertebrates and thereby indirectly influence the number of House Sparrows. Although adult
House Sparrows are mainly seed-eaters, they need insects and other invertebrates to feed their
young, such that it is likely that they will prefer areas with high abundance of invertebrates at the
beginning of the breeding period. Several researchers have postulated that the lack of
invertebrates might be an important factor in the reported decline of House Sparrow populations
in urban areas (Wotton et al., 2002; Summers-Smith, 2003). Short-term exposure of pulsed
mobile phone radiation with carrier frequency 900 MHz resulted in a 50-60 % decrease of the
reproductive capacity of insects (Panagopoulos et al., 2004). Similar results were also found with
microwave radiation at other frequencies (Bol’shakov et al., 2001; Atli and Unlu, 2006).
The results of our study suggest that long-term exposure to low-intensity (pulsed)
electromagnetic radiation from GSM base stations may have significant effects on populations of
wild birds. The exact mechanisms of these effects are as yet poorly understood. Given the
potential importance that such effects may have on aspects of biodiversity and human health,
more detailed studies in both the laboratory and the field are urgently needed to corroborate our
results and to uncover the underpinning mechanistic relationships.
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