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ORIGINAL ARTICLE
Artificial lights and seabirds: is light pollution a threat
for the threatened Balearic petrels?
Airam Rodrı
´guez
1,2,3
•David Garcı
´a
4
•Beneharo Rodrı
´guez
3
•
Esteban Cardona
4
•Lluı
´s Parpal
5
•Pere Pons
6
Received: 18 January 2015 / Revised: 16 April 2015 / Accepted: 4 May 2015
ÓDt. Ornithologen-Gesellschaft e.V. 2015
Abstract Petrels are among the most threatened group of
birds. On top of facing predation by introduced mammals
and incidental bycatch, these seabirds have to deal with an
emerging threat, light pollution, which is increasing glob-
ally. Fledglings are disoriented and attracted to artificial
lights in their maiden night flights from their nests to the
sea. Once grounded, they are exposed to multiple threats
leading to high mortality. We report on numbers of three
petrel species (Balearic shearwater Puffinus mauretanicus,
Scopoli’s shearwater Calonectris diomedea, and European
storm-petrel Hydrobates pelagicus) rescued on the Balearic
Islands, Mediterranean Sea, in the period 1999–2013. We
assessed the proportion of grounded fledglings in the
population and colonies impact based on radiance levels
measured from a nocturnal satellite image. We also cal-
culated the radius of light pollution impact. At least 304
fledgling birds were found stranded due to attraction to
artificial lights, fatally affecting 8.5 % of them. The pro-
portion of grounded fledglings ranged between 0.13 and
0.56 % of the fledglings produced annually. The body mass
of Balearic and Scopoli’s shearwater fledglings decreased
with rescue date. Light-induced mortality increased during
the fledging period for Scopoli’s shearwaters. Birds were
rescued at a mean distance of 4833 m from the nearest
colony, and between 30 and 47 % of colonies were ex-
posed to light-polluted areas. Although impact seems to be
low for all species, urban development and, consequently,
the increase in light pollution in the proximity of the
colonies should be taken into account to reduce as much as
possible this emerging source of mortality.
Keywords Artificial lights Attraction Balearic
Islands Disorientation Illumination Light pollution
Mortality Seabird
Zusammenfassung
Ku
¨nstliches Licht und Seevo
¨gel: Stellt Lichtver-
schmutzung eine Bedrohung fu
¨r gefa
¨hrdete Sturmvo
¨gel
auf den Balearen dar?
Sturmvo
¨gel geho
¨ren zu den am sta
¨rksten gefa
¨hrdeten Vo-
gelgruppen. Diese Seevo
¨gel sind nicht nur der Pra
¨dation
durch eingefu
¨hrte Sa
¨ugetiere ausgesetzt und verenden in
Fischereinetzen als unbeabsichtigter Beifang, sondern sie
mu
¨ssen nun auch noch mit einer weiteren Bedrohung fertig
werden, die weltweit zunimmt – Lichtverschmutzung. Auf
ihren na
¨chtlichen Jungfernflu
¨gen vom Nest zur See sind die
Flu
¨gglinge desorientiert und werden von ku
¨nstlichem Licht
Communicated by C. Barbraud.
&Airam Rodrı
´guez
airamrguez@ebd.csic.es
1
Department of Evolutionary Ecology, Estacio
´n Biolo
´gica de
Don
˜ana (CSIC), Avda. Ame
´rico Vespucio s/n, 41092 Seville,
Spain
2
Research Department, Phillip Island Nature Parks,
P.O. BOX 97, Cowes, VIC 3922, Australia
3
Canary Islands’ Ornithology and Natural History Group
(GOHNIC), La Malecita s/n, Buenavista del Norte,
38480 Tenerife, Canary Islands, Spain
4
Islands Biodiversity Research Initiative (IRBI), C/Son
Borra
´s, 14, Alaro
´, 07340, Mallorca, Balearic Islands, Spain
5
Consorci per a la Recuperacio
´de la Fauna de les Illes Balears
(COFIB), Ctra. Sineu km 15, Santa Eugenia, Mallorca,
Balearic Islands, Spain
6
Balearic Ornithology Group (GOB-Minorca), Molı
´del Rei.
Camı
´des Castell, 53, Mao
´-Maho
´n, 07702 Menorca,
Balearic Islands, Spain
123
J Ornithol
DOI 10.1007/s10336-015-1232-3
angezogen. Sobald sie zu Boden gegangen sind, sind sie
vielfachen Gefahren ausgesetzt, die zu hoher Mortalita
¨t
fu
¨hren. Wir berichten, wie viele Individuen dreier Stur-
mvogelarten (Balearensturmtaucher Puffinus mauretanicus,
Sepiasturmtaucher Calonectris diomedea und Sturm-
schwalbe Hydrobates pelagicus) auf den Balearischen
Inseln im Mittelmeer von 1999 bis 2013 gerettet wurden.
Wir haben den Anteil der zu Boden gegangenen Flu
¨gglinge
in der Population und die Folgen der Helligkeit in den
Kolonien (basierend auf einem na
¨chtlichen Satellitenbild)
abgescha
¨tzt. Außerdem haben wir den Radius der
Lichtverschmutzung berechnet. Mindestens 304 Flu
¨gglinge
wurden gefunden, die von ku
¨nstlichem Licht angezogen
gestrandet waren; 8,5 % davon tot. Der Anteil zu Boden
gegangener Flu
¨gglinge lag zwischen 0,13 und 0,56 % der
ja
¨hrlich produzierten Flu
¨gglinge. Die Ko
¨permasse der
Flu
¨gglinge von Balearen- und Sepiasturmtaucher war umso
niedriger, je spa
¨ter diese gerettet wurden. Lichtinduzierte
Mortalita
¨t nahm fu
¨r Sepiasturmtaucher wa
¨hrend der Aus-
fliegephase zu. Die Vo
¨gel wurden in einer mittleren Ent-
fernung von 4833 m zur na
¨chsten Kolonie gerettet, und 30
bis 47 % der Kolonien waren Lichtverschmutzung ausge-
setzt. Obwohl die Auswirkungen fu
¨r alle Arten gering zu
sein scheinen, sollte die urbane Entwicklung und folglich
die Zunahme der Lichtverschmutzung in der Na
¨he der
Kolonien so erfolgen, dass diese aufkommende Todesur-
sache so weit wie mo
¨glich reduziert wird.
Introduction
Light pollution, i.e. the alteration of natural light levels at
night as consequence of human structures, is increasing
worldwide and it has been recently recognized as a threat
for biodiversity (Ho
¨lker et al. 2010a,b). One of the nega-
tive effects of light pollution on animals is disorientation in
their movements, with consequences for their fitness and
survival (Longcore and Rich 2004; Gaston et al. 2014).
Land-breeding marine animals, such as sea turtles and
seabirds, are strongly affected by lights when hatchlings or
fledglings direct toward the sea for the first time in their
lives (Rich and Longcore 2006). These events can cause
high mortality in one of the most endangered groups of
birds, the petrels (order Procellariiformes; Croxall et al.
2012), as fledglings are grounded in lit areas and suscep-
tible to collisions with human infrastructures or vehicles,
predation by introduced predators, starvation, or dehydra-
tion (a phenomenon called fallout; Reed et al. 1985; Telfer
et al. 1987; Ainley et al. 2001; Le Corre et al. 2002; Ro-
drı
´guez and Rodrı
´guez 2009; Miles et al. 2010; Fontaine
et al. 2011; Rodrı
´guez et al. 2014). Because petrels are
long-lived birds, population dynamics are especially
sensitive to adult survival. However, light pollution af-
fecting mainly fledglings has been recognized as an im-
portant mortality source, which, in addition to other threats,
could endanger the survival of petrel populations (Ainley
et al. 2001; Fontaine et al. 2011; Griesemer and Holmes
2011). Apart from attracting fledglings to lit areas, light
pollution could also modify the behaviour of predators of
nocturnal colony-visiting petrels. Burrow-nesting petrels
visit colonies at night apparently to avoid predators (Miles
et al. 2013), and thus an increase in light levels at colonies
as a consequence of light pollution can increase the pre-
dation by diurnal predators (Oro et al. 2005).
The Balearic Islands are among the most popular
touristic destinations in the Mediterranean Sea, highly
populated, and have increasing light pollution levels
(IBESTAT 2014; de Miguel et al. 2014). Despite high
anthropogenic transformation of the archipelago, four
threatened procellariiform species breed there still,
relegated to the most inaccessible places, mainly islets,
marine rocks, and coastal cliffs. Among the species af-
fected, as the most significant values, are the endemic and
critically endangered Balearic shearwater Puffinus maure-
tanicus and the largest populations of European storm-pe-
trels Hydrobates pelagicus in the western Mediterranean
(Madron
˜o et al. 2004).
In this study, we evaluate the effect of light pollution as
a source of mortality for fledglings of the three most
abundant petrel species breeding on the Balearic Islands:
the critically endangered Balearic shearwater, as well as
the regionally endangered Scopoli’s shearwater Calonec-
tris diomedea and European storm-petrel (Madron
˜o et al.
2004). These three species differ in size, abundance,
breeding period, and distribution among islands. In addi-
tion, the Balearic Islands constitute a different scenario
from other locations where fallout has been studied (e.g.
Azores, Canary Islands, Hawaii, La Reunion Island, or
Phillip Island), as light pollution levels are higher than
reported elsewhere (maximum radiance value 197.3 vs.
103.6 nW/sr cm
2
on Tenerife Island—the highest value
where fallout has been studied; see Table 2 in Rodrı
´guez
et al. 2014 for a comparison) and distribution of colonies
are mainly located on coastal areas. In this regard, petrel
colonies can be located inland on typical oceanic islands,
such as Azores, Canaries, Hawaii, or La Reunion. Thus, the
Balearic Islands are an exceptional scenario to study a
crucial conservation question in the human–wildlife con-
flict of light pollution and seabirds. It has been proposed
that fledglings could be attracted to lights once they suc-
cessfully reach the ocean (Podolsky et al. 1998). This
means that fledglings from dark colonies are also vul-
nerable to light attraction because they can be attracted
back to land (Troy et al. 2011,2013). However, the pro-
portion of fledglings attracted in this way does not seem to
J Ornithol
123
be considerable according to GPS-tracked and banded birds
from known colonies at the Canaries (Rodrı
´guez et al.
2015). Given the coastal distribution of the breeding
colonies at the Balearic Islands (mainly on islets and
marine rocks), the majority of birds grounded by lights
must have flown over the sea. Thus, if the proportion of
affected birds in relation to annually produced fledglings is
high, this means that fledglings can be attracted back to
land lights. On the other hand, if the proportion of affected
birds is low, the numbers of birds attracted back to land
would not be significant for the phenomenon of petrel at-
traction to artificial lights.
Our specific aims are: (1) to estimate the proportion of
fledglings grounded by artificial lights with respect to the
total fledglings annually produced by the population; (2) to
study body condition and fatality in relation to rescue date;
(3) to calculate the radius of light pollution impact by as-
signing birds to the nearest breeding colony and compare
with data coming from ringing programs conducted on two
colonies of Scopoli’s shearwaters; and (4) to evaluate light
pollution levels in the breeding colonies proximity to
quantify alterations of breeding habitats due to this
emerging pollution.
Materials and methods
Study area
The Balearic Islands, western Mediterranean Sea, comprise
four major islands (Majorca, Minorca, Ibiza, and For-
mentera) and several islets and rocks. More than one mil-
lion people inhabit the archipelago, the majority
concentrated along the coast, and approximately 13 million
tourists per year visit the archipelago (IBESTAT 2014).
According to the analyses of satellite imagery, light pol-
lution levels have increased during recent years (de Miguel
et al. 2014).
Species
The Balearic shearwater P. mauretanicus is the most
threatened seabird in Europe (1750–2125 breeding pairs,
Sauleda 2006), the most critical threats being predation by
introduced mammals and fishery bycatch (Arcos 2011).
Other threats, including light pollution, have been men-
tioned in the Balearic shearwater conservation action plan,
but limited information regarding their effects on popula-
tions has been provided (Arcos 2011). In addition, some
events of predation by peregrine falcons have been
recorded at night at the breeding colonies, which could be
related to an artificial increase of light levels (Garcı
´a2009;
Wynn et al. 2010).
The Scopoli’s shearwater C. diomedea is the largest and
the most abundant of the Balearic procellariiforms
(100–125 cm wingspan and around 11,000 breeding pairs).
Some references indicate that this species is grounded by
light pollution in some Mediterranean islands (Baccetti
et al. 2005; Raine et al. 2007; Laguna et al. 2014), although
no information on scientific literature is available for the
Balearic Islands.
The European storm-petrel H. pelagicus is the smallest
petrel breeding on the Mediterranean basin (36–39 cm
wingspan). The Balearic archipelago holds the largest
populations in the western Mediterranean (2916–4046
breeding pairs, Sauleda 2006). This species can be affected
by light pollution in two different ways: (1) attraction and
disorientation of juveniles (Laguna et al. 2014); and (2)
increase of predation rates by gulls in light polluted colo-
nies (Oro et al. 2005).
A small, mixed population of Yelkouan shearwater
Puffinus yelkouan and Balearic shearwater is breeding on
Minorca. Despite several morphological and genetic studies,
taxonomic status of these birds is controversial (see Arcos
2011; Genovart et al. 2012). For this reason, we considered
all Puffinus fledglings as Balearic shearwater specimens.
Rescue and ringing campaigns
Data on rescued birds come from three wildlife reha-
bilitation centres located on the three main islands (Ma-
jorca, Minorca, and Ibiza) and sponsored by the regional
government (Consorci per a la Recuperacio
´de la Fauna de
les Illes Balears, Govern de les Illes Balears). The study
period extends from 1999 to 2013. Birds were collected by
the public or personnel of the wildlife rehabilitation centres
and examined by qualified staff for identification, ringing,
assessment of condition and health status, and release into
the wild, if possible. Injured birds were admitted and held
for rehabilitation or euthanized. In contrast to other islands
where petrels are severely affected by lights (Telfer et al.
1987; Le Corre et al. 2002; Rodrı
´guez and Rodrı
´guez 2009;
Fontaine et al. 2011; Rodrigues et al. 2012), no public
dissemination of rescue campaigns is conducted by local
administrations to mitigate light pollution mortality on the
Balearic Islands. Thus, data presented here on the number
of grounded birds should be interpreted as minimum
numbers, as some birds could be found by people unaware
of the light pollution-seabird problem.
As part of a long-term programme for monitoring
breeding success and recruitment rate of Scopoli’s shear-
waters, nestlings of two colonies (Illot Pantaleu, Majorca
and Illa d’Aire, Minorca) are ringed at their nests before
fledging. We used ringing data from these colonies to es-
timate the rate of birds grounded by lights. A total of 190
J Ornithol
123
nestlings were ringed on Illa d’Aire in the 2002–2006,
2009–2010, and 2012–2013 breeding seasons. On Illot
Pantaleu, 1084 nestlings were ringed in the 2000–2009 and
2011–2012 seasons.
Impact on the populations
To estimate roughly the impact of artificial light attraction
at fledging and compare with other studies, we followed
formulas given by Le Corre et al. (2002). We first de-
termined the total number of fledglings annually produced
by the population of the three species. We multiplied
productivity (proportion of pairs laying an egg that pro-
duced a fledgling) by breeding population size, taking into
account the probability of reproduction skipping
(Table 1). Then, we divided the number of annually
grounded birds by the number of fledglings produced by
the population for each species. Finally, we calculated
95 % confidence intervals for the smaller estimated
population sizes.
We used population size and productivity from the lit-
erature (Table 1), and we assumed they were constant
among years. Estimating breeding population size of bur-
row-nesting petrels is challenging, and some of them could
be overestimated (e.g. the European storm-petrel; see
Madron
˜o et al. 2004). Some grounded fledglings could
never be found by rescuers. Fledglings look for hiding
places during daylight hours, could ground in or reach not-
frequented places, or may be unreported by unaware peo-
ple. Thus, our estimates should be interpreted with caution
and as minimal numbers. Despite constraints (i.e. as-
sumptions on constant population size and productivity,
and the presumably underestimated numbers of grounded
birds), estimates give us a rough idea of the magnitude of
the problem and allow comparison with other studies
which follow the same methodology (see Table 2 in Ro-
drı
´guez et al. 2014).
Environmental information and variables
Information on spatial distribution of species was taken
from BioAtles, Govern de les Illes Balears (available at
http://bioatles.caib.es). Resolution was based on a
191 km grid size. Light pollution levels were taken from
a cloud-free composite of VIIRS nighttime lights corre-
sponding to April and October of 2012 and produced by the
Earth Observation Group, National Oceanic and Atmo-
spheric Administration (NOAA) National Geophysical
Data Center (available at http://ngdc.noaa.gov/eog/viirs/
download_monthly.html). VIIRS imagery with a spatial
resolution of 742 9742 m and no saturation constitutes an
improvement to the previous DMSP satellite imagery
(Elvidge et al. 2013).
Table 1 Affection levels of light pollution on annually produced fledglings and colonies for three petrel species on the Balearic Islands during the period 1999–2013
Species English name Conservation status Breeding
population size
c
Productivity Probability of
skipping
% of grounded
fledglings (95 % CI)
Light pollution levels at colonies
IUCN
a
National
b
Colonies with
mean values [1
Colonies with max
values [10
n
Puffinus
mauretanicus
Balearic
shearwater
Critically
endangered
Critically
endangered
1,750–2,125 0.61
d
0.26
d
0.46–0.56
(0.381–0.733)
2512
Calonectris
diomedea
Scopoli’s
shearwater
Least
concern
Endangered 10,000–11,000 0.42
e
0.15
f
0.34–0.37
(0.256–0.488)
4715
Hydrobates
pelagicus
European
storm-petrel
Least
concern
Vulnerable 2,912–4,046 0.50
g
*0
h
0.13–0.18
(0.093–0.265)
2310
a
BirdLife International (2015)
b
Madron
˜o et al. (2004)
c
Sauleda (2006)
d
Oro et al. (2004)
e
Amengual and Aguilar (1998)
f
Sanz-Aguilar et al. (2011)
g
Tavecchia et al. (2008)
h
Sanz-Aguilar et al. (2008)
J Ornithol
123
Geographical analyses to obtain distances from colonies
to rescue location and light pollution levels of colonies and
rescue locations were conducted in QGIS version 2.0.1
(Open Source Geospatial Foundation Project, http://qgis.
osgeo.org). Because the majority of rescued birds were not
ringed at their colonies, we assumed that birds were
coming from the nearest colony, following Rodrigues et al.
(2012). To determine light pollution levels at colonies we
used centroids of 1 91km
2
cells having a colony of at
least one species. We report the single value of the pixel
intersected with the centroids, but also the mean and
maximum values in a 4 km radius buffer centred at the
centroid of the 1 91 km cells representing a breeding
colony.
Statistical analysis
To test the effect of rescue date (explanatory variable) on
the status of birds (response variable with two levels:
released vs. dead), we used generalized linear models
(GLM) with binomial error structure and logit link func-
tion for each species. The significance of the model was
assessed by a likelihood ratio test, comparing deviance
with the null model (comprising only the intercept). We
run Pearson’s correlations to test for relationships be-
tweenbodymassanddateofrescue for the Balearic and
Scopoli’s shearwaters (data on storm-petrel body mass
were unavailable). To test for differences in distances to
colonies and light pollution levels among species, we
conducted linear models. Variables were transformed to
meet normality and homoscedasticity assumptions. ‘Dis-
tance to nearest colony’ and ‘light pollution level’ were
log [i.e. ln(x ?1000)] and square root-transformed,
respectively.
Statistical analyses were conducted in R version 3.0.3 (R
Foundation for Statistical Computing, Vienna, Austria).
Results
Magnitude and timing of fallout
A total of 304 fledgling birds were found stranded due to
attraction to artificial lights on the Balearic Islands in the
period 1999–2013. The most abundant species was the
Scopoli’s shearwater (199 birds), followed by the Balearic
shearwater (66 birds) and the European storm-petrel (39
birds). The percentage of fledglings grounded by artificial
lights was lower than 1 % for the three species (Table 1).
Despite of the lower breeding population size, the critically
endangered Balearic shearwater was the most affected
species. The highest number of grounded birds was reached
in Minorca (147 birds), followed by Ibiza (92), Majorca
(61), and Formentera (4). The birds were rescued mainly in
the periods 13–20 October, 4–14 July, and 20 August–5
September for Scopoli’s shearwater, Balearic shearwater,
and European storm-petrel, respectively, coinciding with
the fledging season of each species (1st and 3rd quartiles;
Fig. 1).
Mortality and body condition
Twenty-six (8.5 %) out of 304 birds were fatally affected
by lights. No differences in mortality frequency were de-
tected between species (v
2
=3.364, df =2, P=0.186).
Only the GLM explaining the relationship between prob-
ability to die and rescue date for Scopoli’s shearwater was
significant as compared to the null model (likelihood ratio
test: v
2
=11.484, P\0.001), and it showed that the
Fig. 1 Frequency distribution of petrel fledglings found grounded in
the Balearic Islands during the period 1999–2013: Balearic shearwa-
ter Puffinus mauretanicus, Scopoli’s shearwater Calonectris diome-
dea, and European storm-petrel Hydrobates pelagicus
J Ornithol
123
probability to die increased with the fledging season (es-
timate ±SE 0.205 ±0.053; v
2
=3.887, P\0.001). The
remaining GLMs for the Balearic shearwater and the
European storm-petrel were not significantly better than
their respective null models (likelihood ratio tests:
v
2
=0.004, P=0. 949 and v
2
=0.608, P=0.435, re-
spectively). The body mass of Balearic and Scopoli’s
shearwater fledglings decreased with rescue date
(r=-0.762, P\0.002, n=13; and r=-0.501,
P\0.001, n=45, respectively).
Distances from rescue locations to colonies
Birds were rescued at a mean distance of 4833 m from
the nearest colony (median 4206, 1st and 3rd quar-
tiles =1581 and 5644 m, n=303; Figs. 2,3). Mean
distances were different between species
(F
2, 300
=5.438, P=0.005), rescuing Scopoli’s shear-
water at closer locations (4219 ±6701 m, mean ±SD)
than the other two species (5943 ±7094 m for the
Balearic shearwater and 6075 ±5413 m for the Euro-
pean storm-petrel). However, information from Scopoli’s
shearwater rings indicates that they flew shorter distances.
Only 10 out of the 1274 Scopoli’s shearwater fledglings
ringed at their natal colonies were recaptured, and all
within a 4 km radius from colonies (eight and two birds
from Pantaleu and Illa d’Aire colonies, respectively; see
inset in Fig. 2). In addition, one ringed Balearic shear-
water fledgling was recovered at a distance of 1581 m
from its natal colony, Mola de Mao
´,Minorca.
Light pollution levels at rescue locations
and colonies
Light pollution levels at rescue locations ranged between
0.2 and 123.4 nW/sr cm
2
(mean 24.6, median 21.0, 1st and
3rd quartiles 5.2 and 38.1 nW/sr cm
2
,n=303) and no
significant differences were detected between species
(F
2, 300
=2.522, P=0.082; Figs. 2,3). In general, colo-
nies were exposed to low light pollution levels, only 2–4
out of the 10–15 colony buffers (depending on species)
showed mean radiance values higher than 1 nW/sr cm
2
.
However, a higher proportion (30–47 %) of colonies
showed areas with high levels of light pollution, i.e. higher
than 10 nW/sr cm
2
, within a 4 km radius (Table 1). One
hundred and ninety-eight birds (65 % out of the total
fallout) were assigned to colonies exposed to radiance
values higher than 10 nW/sr cm
2
within a radius of 4 km.
Fig. 2 Histograms of distances
and light pollution levels. Inset
corresponds to distances from
natal colonies to rescue
locations of ringed Scopoli’s
shearwater. Distances
correspond to the length in a
straight line between rescue
locations and the nearest
colonies. Light pollution levels
correspond to radiance values
taken from a nocturnal satellite
image produced by the Earth
Observation Group, NOAA
National Geophysical Data
Center at rescue locations (see
text)
J Ornithol
123
No significant differences were observed between the light
pollution levels at colonies of the three species (mean
values: F
2, 34
=0.163, P=0.850; max. values:
F
2, 34
=0.471, P=0.629; log-transformed variables).
Discussion
Magnitude of fallout
Our study provides baseline information on the light-induced
mortality of three petrel species on the Balearic Islands, in-
cluding the critically endangered Balearic shearwater. The
numbers reported here are low in comparison to those from
other islands and species, where thousands of fledglings are
involved in a single fledging season (e.g. Day et al. 2003;
Fontaine et al. 2011; Rodrı
´guez et al. 2012b). This figure
seems to be general in the Mediterranean Sea where low
affection rates have been recorded (Baccetti et al. 2005;
Raine et al. 2007; Laguna et al. 2014). Distribution of
colonies seems to play a crucial role in the fallout numbers.
In the Balearic Islands, as in many other Mediterranean is-
lands, breeding colonies are mainly located on islets and
rocks offshore or on coastal sectors at low altitudes, and thus
many fledglings successfully reach the ocean. According to
this, petrel fledglings are not massively attracted back to land
lights (but see Troy et al. 2013). A similar case occurs with
other species mainly breeding at coastal sectors, such as the
wedge-tailed shearwater Ardenna pacifica on La Reunion,
Indian Ocean (Le Corre et al. 2002), or the short-tailed
shearwater Ardenna tenuirostris on Phillip Island, Australia
(Rodrı
´guez et al. 2014), where a small proportion of annually
produced fledglings are grounded by lights. However, on
islands where fledglings from inland colonies must fly over
cities to reach the ocean, the rate of grounded birds by lights
is higher (Rodrı
´guez et al. 2014).
Mortality and body condition
Without human intervention (rescuing), all grounded birds
would die because most probably any would have reached
the sea for themselves (Le Corre et al. 2002). Mortality rate at
rescue was similar to other studies conducted elsewhere,
which ranges between 4 and 14 % of rescued birds (Ro-
drı
´guez et al. 2014). However, we have to note that light-
induced mortality is underestimated because (1) an unknown
number of the grounded birds are never found, and (2) rescue
campaigns based on the collaboration of the general public
Fig. 3 Rescue locations and breeding colonies of three seabird
species on the Balearic Islands, Mediterranean Sea. Light pollution
levels correspond to radiance values (nW/sr cm
2
) taken from a
satellite image from National Geophysical Data Center. Lines
represent a 4 km buffer around breeding colonies
J Ornithol
123
are biased toward the collection of live birds, i.e. lay people
do not report (or collect) dead birds (Podolsky et al. 1998;
Rodrı
´guez et al. 2014). Thus, if an active rescue patrol for
dead and live birds had been conducted in the Balearic Is-
lands, the mortality rate would have increased as recorded for
the Newell’s shearwater Puffinus newelli or the short-tailed
shearwater A. tenuirostris (assuming no species-specific
differences in attraction to light; Ainley et al. 2001; Ro-
drı
´guez et al. 2014).
As previously recorded for Cory’s shearwaters
Calonectris borealis (Rodrı
´guez et al. 2012a), we found that
both the probability of releasing a rescued bird back to the
wild and the body mass decreased with the date of admis-
sion at the rehabilitation centre. Given that body mass at
fledging seems crucial for recruitment into the breeding
population (Mougin et al. 2000), an effort should be made to
rescue the birds as soon as possible, reducing the probability
of dying and improving their fitness. In this sense, rescued
fledglings of the endangered Newell’s shearwater are ad-
mitted for rehabilitation and feeding if they fall below a
minimum body mass threshold (Griesemer and Holmes
2011). A similar action could be undertaken with those
birds rescued late at the fledging season, especially for the
critically endangered Balearic shearwater.
Distances and light pollution levels
The distances observed in the Balearic Islands are similar to
those reported for GPS-tracked Cory’s shearwaters on
Tenerife, Canary Islands (mean distance 5108 m for birds
with a known origin; Rodrı
´guez et al. 2015), but longer than
mean distance (2387 m) estimated in Sao Miguel, Azores
(Rodrigues et al. 2012). The higher light pollution levels of the
Balearic Islands and Tenerife could explain these differences,
as the higher the intensity of light pollution, the further away
the birds are attracted from (Rodrı
´guez et al. 2015). In addi-
tion, the higher spread distribution of colonies at Sao Miguel
in comparison to the confined colonies on Balearic Islands
could also explain the differences in distances.
In general, colonies showed low mean light pollution
levels, but 30–47 % of them were exposed to radiance
values higher than 10 nW/sr cm
2
(percentages vary on
species; Table 1). That is a very conservative estimate of
light pollution affecting colonies because of the cut-off
points used: (1) more than a third of birds are grounded in
areas with radiance values lower than 10 nW/sr cm
2
(104
out of 304 found birds); and (2) 54 % of birds were rescued
farther away than 4 km from the nearest colony (163 out of
304 found birds). Despite this conservative threshold,
colonies exposed to radiance values higher than 10 nW/
sr cm
2
were the main contributors to the fallout (65 % of
rescued birds were assumed to be born at these colonies),
which points to the validity of our approach.
Finally, we should note that light-induced mortality is
not limited to coastal cities. Fledglings can also be attracted
to lights of ships or oil platforms, extending the problem of
light pollution at sea (Wiese et al. 2001; Merkel and Jo-
hansen 2011; Glass and Ryan 2013). In this sense, the in-
crease of recreational vessels and cruise ships, which are
currently an important touristic resource for the archipe-
lago, and oil-drilling plans of the Spanish Government
around Balearic waters, will not only increase the mortality
of birds by light attraction, but also due to the inevitable oil
spills and marine litter from ships (Ronconi et al. 2014).
Recommendations and conclusions
Although numbers of birds grounded by lights are not high,
reducing mortality by anthropogenic causes should be a
priority for the management and conservation of these
threatened species. To mitigate light-induced mortality and
to have a better idea of its effect, we recommend estab-
lishing a rescue campaign during the fledging seasons,
especially for the Balearic shearwater. Rescue campaigns
should at least focus on the nearest urban areas to breeding
colonies. Educational campaigns to make the general
public aware of the economic, environmental, and health
consequences of light pollution should accompany rescue
campaigns. Regional governments should legislate to pre-
serve the natural night sky, reducing light pollution levels
as low as possible, especially in the proximity of colonies.
These measures would help to save limited economic re-
sources, but also to preserve the natural and crucial
fledging processes of nocturnal seabirds.
Acknowledgments We are deeply thankful to all the anonymous
people who kindly helped rescue the birds, to Manolo Sua
´rez and
Rau
¨l Escandell for providing ringing data of fledglings at colonies,
and to Cristo
`fol Mascaro
´and Nieves Negre for their help in the
fieldwork and information gathering. We are also indebted to the
personnel of the wildlife rehabilitation centres for their help and
collaboration. Ana Sanz-Aguilar, Andie Filadoro and two anonymous
reviewers provided interesting comments on earlier drafts. The sup-
port given by the species protection service of the counselling envi-
ronment of the Balearic Islands’ Government and by a Marie Curie
International Outgoing Fellowship within the 7th European Com-
munity Framework Programme (No. 330655 FP7-PEOPLE-2012-
IOF) was crucial to conduct this research.
References
Ainley DG, Podolsky R, Nur N, Deforest L, Spencer GA (2001)
Status and population trends of the Newell’s Shearwater on
Kauai: insights from modelling. Stud Avian Biol 22:108–123
Amengual JF, Aguilar JS (1998) The impact of the black rat (Rattus
rattus) on the reproduction of Cory’s shearwater Calonectris
diomedea in the Cabrera National Park, Balearic Islands, Spain.
In: Walmsley JG, Goutner V, El Hili A, Sultana J (eds) Ecologie
des oiseaux marins et gestion inte
´gre
´e du littoral en
J Ornithol
123
Me
´diterrane
´e. 4e
´me symposium me
´diterrane
´en des oiseaux
marins, Hammamet, 11–16 April 1995. Arc Editions, Rades,
pp 94–121
Arcos JM (2011) International species action plan for the Balearic
shearwater, Puffinus mauretanicus. SEO/BirdLife & BirdLife
International
Baccetti N, Sposimo P, Giannini F (2005) Artificial lights and
mortality of Cory’s shearwater Calonectris diomedea on a
Mediterranean island. Avocetta 29:89–91
BirdLife International (2015) IUCN Red List for birds. http://www.
birdlife.org. Accessed 27 Mar 2015
Croxall JP, Butchart SHM, Lascelles B, Stattersfield AJ, Sullivan B
et al (2012) Seabird conservation status, threats and priority
actions: a global assessment. Bird Conserv Int 22:1–34
Day RH, Cooper BA, Telfer TC (2003) Decline of Townsend’s
(Newell’s) shearwaters (Puffinus auricularis newelli) on Kauai,
Hawaii. Auk 120:669–679
de Miguel AS, Zamorano J, Go
´mez Castan
˜o J, Pascual S (2014)
Evolution of the energy consumed by street lighting in Spain
estimated with DMSP-OLS data. J Quant Spectrosc Radiat
Transf 139:109–117
Elvidge CD, Baugh K, Zhizhin M, Hsu FC (2013) Why VIIRS data
are superior to DMSP for mapping nighttime lights. Proc Asia-
Pac Adv Netw 35:62–69
Fontaine R, Gimenez O, Bried J (2011) The impact of introduced
predators, light-induced mortality of fledglings and poaching on
the dynamics of the Cory’s shearwater (Calonectris diomedea)
population from the Azores, northeastern subtropical Atlantic.
Biol Conserv 144:1998–2011
Garcı
´a D (2009) Predation on the endemic Balearic Shearwater
Puffinus mauretanicus by Peregrine Falcon Falco peregrinus.
Alauda 77:230–231
Gaston KJ, Duffy JP, Gaston S, Bennie J, Davies TW (2014) Human
alteration of natural light cycles: causes and ecological conse-
quences. Oecologia 176:917–931
Genovart M, Juste J, Contreras-Dı
´az H, Oro D (2012) Genetic and
phenotypic differentiation between the critically endangered
Balearic shearwater and neighboring colonies of its sibling
species. J Hered 103:330–341
Glass JP, Ryan PG (2013) Reduced seabird night strikes and mortality
in the Tristan rock lobster fishery. Afr J Mar Sci 35:589–592
Griesemer AM, Holmes ND (2011) Newell’s shearwater population
modeling for habitat conservation plan and recovery planning.
Technical Report 176. The Hawaii Pacific Island Cooperative
Ecosystem Studies Unit and Pacific Cooperative Studies Unit,
Honolulu, HI, USA
Ho
¨lker F, Moss T, Griefahn B, Kloas W, Voigt CC et al (2010a) The
dark side of light: a transdisciplinary research agenda for light
pollution policy. Ecol Soc 15:13
Ho
¨lker F, Wolter C, Perkin EK, Tockner K (2010b) Light pollution as
a biodiversity threat. Trends Ecol Evol 25:681–682
IBESTAT (2014) Institut d’Estadı
´stica de les Illes Balears. Consel-
leria d’Economia I Competitivitat, Govern de les Illes Balears.
http://ibestat.caib.es/ibestat/inici. Accessed 26 Aug 2014
Laguna JM, Barbara N, Metzger B (2014) Light pollution impact on
‘‘tubenose’’ seabirds: an overview of areas of concern in the
Maltese Islands. BirdLife Malta. http://www.birdlifemalta.org/
photos/otherfiles/5922.pdf. Accessed 1 Dec 2014
Le Corre M, Ollivier A, Ribes S, Jouventin P (2002) Light-induced
mortality of petrels: a 4-year study from Re
´union Island (Indian
Ocean). Biol Conserv 105:93–102
Longcore T, Rich C (2004) Ecological light pollution. Front Ecol
Environ 2:191–198
Madron
˜o A, Gonza
´lez C, Atienza JC (2004) Libro rojo de las aves de
Espan
˜a. Direccio
´n General para la Conservacio
´n de la Biodi-
versidad-SEO/BirdLife, Madrid, Spain
Merkel FR, Johansen KL (2011) Light-induced bird strikes on vessels
in Southwest Greenland. Mar Pollut Bull 62:2330–2336
Miles W, Money S, Luxmoore R, Furness RW (2010) Effects of
artificial lights and moonlight on petrels at St Kilda. Bird Study
57:244–251
Miles WTS, Parsons M, Close AJ, Luxmoore R, Furness RW (2013)
Predator-avoidance behaviour in a nocturnal petrel exposed to a
novel predator. Ibis 155:16–31
Mougin J-L, Jouanin C, Roux F, Zino F (2000) Fledging weight and
juvenile survival of Cory’s shearwater Calonectris diomedea on
Selvagem Grande. Ring Migr 20:107–110
Oro D, Aguilar JS, Igual JM, Louzao M (2004) Modelling demog-
raphy and extinction risk in the endangered Balearic shearwater.
Biol Conserv 116:93–102
Oro D, De Leo
´n A, Minguez E, Furness RW (2005) Estimating
predation on breeding European storm-petrels (Hydrobates
pelagicus) by yellow-legged gulls (Larus michahellis). J Zool
Lond 265:421–429
Podolsky R, Ainley D, Spencer G, Deforest L, Nur N (1998)
Mortality of Newell’s shearwaters caused by collisions with
urban structures on Kauai. Colon Waterbirds 21:20–34
Raine H, Borg JJ, Raine A, Bariner S, Cardona MB (2007) Light
pollution and its effect on Yelkouan shearwaters in Malta; causes
and solutions. Malta: Life Project Yelkouan Shearwater. Bird-
Life Malta. http://www.birdlifemalta.org/photos/otherfiles/370.
pdf. Accessed 1 Aug 2014
Reed JR, Sincock JL, Hailman JP (1985) Light attraction in
endangered procellariiform birds: reduction by shielding upward
radiation. Auk 102:377–383
Rich C, Longcore T (eds) (2006) Ecological consequences of artificial
night lighting. Island Press, Washington, USA
Rodrigues P, Aubrecht C, Gil A, Longcore T, Elvidge C (2012)
Remote sensing to map influence of light pollution on Cory’s
shearwater in Sa
˜o Miguel Island, Azores Archipelago. Eur J
Wildl Res 58:147–155
Rodrı
´guez A, Rodrı
´guez B (2009) Attraction of petrels to artificial
lights in the Canary Islands: effect of the moon phase and age
class. Ibis 151:299–310
Rodrı
´guez A, Rodrı
´guez B, Curbelo A, Pe
´rez A, Marrero S, Negro JJ
(2012a) Factors affecting mortality of shearwaters stranded by
light pollution. Anim Conserv 15:519–526
Rodrı
´guez A, Rodrı
´guez B, Lucas MP (2012b) Trends in numbers of
petrels attracted to artificial lights suggest population declines in
Tenerife, Canary Islands. Ibis 154:167–172
Rodrı
´guez A, Burgan G, Dann P, Jessop R, Negro JJ, Chiaradia A
(2014) Fatal attraction of short-tailed shearwaters to artificial
lights. PLoS ONE 9:e110114
Rodrı
´guez A, Rodrı
´guez B, Negro JJ (2015) GPS tracking for mapping
seabird mortality induced by light pollution. Sci Rep 5:10670
Ronconi RA, Allard KA, Taylor PD (2014) Bird interactions with
offshore oil and gas platforms: review of impacts and monitoring
techniques. J Environ Manag 147:34–45
Sanz-Aguilar A, Tavecchia G, Pradel R, Minguez E, Oro D (2008)
The cost of reproduction and experience-dependent vital rates in
a small petrel. Ecology 89:3195–3203
Sanz-Aguilar A, Tavecchia G, Genovart M, Igual JM, Oro D (2011)
Studying the reproductive skipping behavior in long-lived birds
by adding nest inspection to individual-based data. Ecol Appl
21:555–564
Sauleda CV (2006) Libro Rojo de los vertebrados de las Baleares, 3rd
edn. Conselleria de Medi Ambient, Govern de les Illes Balears
Tavecchia G, Minguez E, de Leo
´n A, Louzao M, Oro D (2008) Living
close, doing differently: small-scale asynchrony. Ecology 89:77–85
Telfer TC, Sincock JL, Byrd GV, Reed JR (1987) Attraction of
Hawaiian seabirds to lights: conservation efforts and effects of
moon phase. Wildl Soc Bull 15:406–413
J Ornithol
123
Troy JR, Holmes ND, Green MC (2011) Modeling artificial light
viewed by fledgling seabirds. Ecosphere 2:109
Troy JR, Holmes ND, Veech JA, Green MC (2013) Using observed
seabird fallout records to infer patterns of attraction to artificial
light. Endanger Species Res 22:225–234
Wiese FK, Montevecchi WA, Davoren GK, Huettmann F, Diamond
AW, Linke J (2001) Seabirds at risk around offshore oil platforms
in the north-west Atlantic. Mar Pollut Bull 42:1285–1290
Wynn RB, Rodrı
´guez-Molina A, McMinn-Grive
´M (2010) The
predation of Balearic shearwaters by peregrine falcons. Br Birds
103:350–356
J Ornithol
123