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Are Western European ospreys (Pandion haliaetus) shortening their migration distances? Evidence from trends of the wintering population in the Iberian Peninsula

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Here, we provide evidence that the number of Western European ospreys wintering in the Iberian Peninsula has been increasing over nearly two decades due to a reduction of the migration distances. We compared trends in wintering and breeding populations of ospreys in the Iberian Peninsula and western Europe, respectively, and we provide a detailed description of the present distribution and the numbers of ospreys wintering in the Iberian Peninsula. Observations of the species were collected as a citizen science project in January 2017. Based on the long-term data series from the Andalusian region (2004–2016) and from the Bay of Cadiz site (2000–2016), we estimated temporal trends in the population size of the ospreys wintering in these areas. Trends in the western European breeding population were derived from counts of ospreys migrating over the Strait of Gibraltar conducted by volunteers (1999–2016). All the trends were estimated by fitting a linear regression to the logarithm of the annual counts. For quantifying the origin of ospreys wintering in the Iberian Peninsula, we collected 204 confirmed field sightings of wintering ospreys in Spain and 155 in Portugal. We showed that the number of wintering ospreys has been increasing in southern Spain over the last 16 years. The magnitude of this increase is similar to the rate of change observed in the ospreys breeding across Western Europe. Recoveries of ringed birds in the Iberian Peninsula during winter indicate a reduction in the migration distances of Central and Northern European ospreys, making these birds winter at higher latitudes more than before. According to our results, this reduction in the migration distance was fairly uniform among different breeding populations in western Europe, but it did not affect all age classes equally, with juvenile birds more prone to winter at higher latitudes compared to adult birds. Our results showed that the overall number of ospreys which are shortening their migration distance, now over 3% of the total breeding population estimated for western Europe, is on an upward trend.
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ORIGINAL ARTICLE
Are Western European ospreys (Pandion haliaetus)shorteningtheir
migration distances? Evidence from trends of the wintering
population in the Iberian Peninsula
Beatriz Martín
1
&Carlos A. Torralvo
1
&Gonçalo Elias
2
&João Tomás
2
&Alejandro Onrubia
1
&Miguel Ferrer
3
Received: 7 October 2018 /Revised: 1 July 2019 /Accepted: 30 July 2019
#Springer-Verlag GmbH Germany, part of Springer Nature 2019
Abstract
Here, we provide evidence that the number of Western European ospreys wintering in the Iberian Peninsula has been increasing over
nearly two decades due to a reduction of the migration distances. We compared trends in wintering and breeding populations of ospreys
in the Iberian Peninsula and western Europe, respectively, and we provide a detailed description of the present distribution and the
numbers of ospreys wintering in the Iberian Peninsula. Observations of the species were collected as a citizen science project in January
2017. Based on the long-term data series from the Andalusian region (20042016) and from the Bay of Cadiz site (20002016), we
estimated temporal trends in the population size of the ospreys wintering in these areas. Trends in the western European breeding
population were derived from counts of ospreys migrating over the Strait of Gibraltar conducted by volunteers (19992016). All the
trends were estimated by fitting a linear regression to the logarithm of the annual counts. For quantifying the origin of ospreys wintering
in the Iberian Peninsula, we collected 204 confirmed field sightings of wintering ospreys in Spain and 155 in Portugal. We showed that
the number of wintering ospreys has been increasing in southern Spain over the last 16 years. The magnitude of this increase is similar
to the rate of change observed in the ospreys breeding across Western Europe. Recoveries of ringed birds in the Iberian Peninsula
during winter indicate a reduction in the migration distances of Central and Northern European ospreys, making these birds winter at
higher latitudes more than before. According to our results, this reduction in the migration distance was fairly uniform among different
breeding populations in western Europe, but it did not affect all age classes equally, with juvenile birds more prone to winter at higher
latitudes compared to adult birds. Our results showed that the overall number of ospreys which are shortening their migration distance,
now over 3% of the total breeding population estimated for western Europe, is on an upward trend.
Keywords Citizen science .Long-distance migrant .Mediterranean Basin .Monitoring .Raptor .Osprey .Pandion haliaetus
Introduction
Monitoring animal populations is required to define the conser-
vation status of species and to inform management decisions.
Among other needs, continuing monitoring is critical for identi-
fying long-term trends in populations related to environmental
changes (Martin et al. 2007). In this context, active public in-
volvement in scientific research (i.e., citizen science) can become
a key source of high-quality data for scientists and policymakers
(Irwin 2018). Particularly when a sustained investment in long-
term monitoring over wide areas is not possible, the use of vol-
unteers becomes a powerful tool to maintain cost-effective mon-
itoring programmes of species of conservation concern (e.g.,
Gouraguine et al. 2019). Long-term monitoring is of crucial im-
portance to understand population changes and to develop plans
for the adoption of proper conservation and management mea-
sures in long-lived species, such as raptors.
Osprey (Pandion haliaetus) is a long-lived, long-distance
migratory raptor widely distributed across the northern hemi-
sphere (Cramp and Simmons 1980) and Australasia. It was a
common breeding species throughout Europe before the
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s10344-019-1311-5) contains supplementary
material, which is available to authorized users.
*Beatriz Martín
bmartin@fundacionmigres.org
1
Fundación Migres, CIMA, ctra. N-340, Km. 85,
E-11380 Tarifa, Cádiz, Spain
2
Aves de Portugal, E-19016, 1991-901 Lisbon, Portugal
3
Applied Ecology Group, Doñana Biological Station, CSIC,
Seville, Spain
European Journal of Wildlife Research (2019) 65:72
https://doi.org/10.1007/s10344-019-1311-5
nineteenth century (Poole et al. 2017). During the mid-
twentieth century, however, the European breeding population
of the osprey suffered a considerable decrease, leading to its
extirpation in several countries, anditalmostcompletelydisap-
peared from the Mediterranean Basin, except for the Balearic
Islands, Corsica and northern African coasts of Morocco and
Algeria. Human-induced factors, such as hunting (Poole et al.
2017), the use of poisons and pesticides (Lensink 1997), and
the adverse consequences of habitat destruction and tourism
(Schmidt 1998) caused the extirpation of the species in many
parts of its range (Schmidt-Rothmund et al. 2014). The banning
of organochlorine pesticides (i.e., DDT) in the first half of the
twentieth century (Lensink 1997), together with the legal pro-
tection of the osprey in Europe between the 1920s and 1950s,
as well as other conservation measures, such as those imple-
mented to mitigate electrocution fatalities on power lines (Janss
and Ferrer 1999), have gradually led to an ongoing recovery of
the speciesrange and increase in population size (Poole 1989;
Schmidt-Rothmund et al. 2014).
Currently, osprey populations are large and show stable or
even positive trends in central and northern Europe (BirdLife
International 2017). In contrast, the species is still absent or
only present in small isolated populations in much of southern
Europe. The Iberian Peninsula is, however, an important pas-
sage and stopover area for migratory ospreys from western
Europe (Bernis 1980; Sanz 1997). These birds mainly winter
in West Africa, in contrast to easternmost European individ-
uals, which winter in eastern sub-Saharan Africa (Zwarts et al.
2009), occasionally as far south as South Africa (Österlöf
1977;Saurola2002).
Migratory ospreys spend over half of the year on migration
and at wintering sites in Africa (Hake et al. 2001;Alerstametal.
2006;Dennis2008; Bai and Schmidt 2012) and more recently
in southern Europe (Gil and Valenzuela 1997; Sanz 1997;
Casado and Ferrer 2005;Dennis2008; Sayago 2011). Events
during these stages through the life history annual cycle affect
individual survival and therefore may modulate the breeding
population trend (Klaassen et al. 2014; Monti et al. 2018).
Since adult ospreys usually return to the same wintering loca-
tion year after year (Poole 1989), the identification of sites used
by ospreys during winter should direct us to reduce threats that
represent a potential mortality risk for ospreys in those areas.
Many migratory birds have shortened their migration dis-
tances (e.g., Visser et al. 2009) as climate change and other
human activities have increased food availability at higher
latitudes in their wintering range. As a consequence, the win-
tering areas of many bird species are moving north (La Sorte
and Thompson 2007). This also appears to be the case of
ospreys as more and more ospreys are spending the winter
in the Iberian Peninsula (Gil and Valenzuela 1997;Sanz
1997;Dennis2008).
However, individuals of long-lived species, such as ospreys,
could be affected differently, since behavioural responses of
migrants to climate and other human-induced changes may vary
among different fractions of the overall population, such as age
classes (e.g., Martín et al. 2014; Martín et al. 2016a; Scholer et al.
2016). In this respect, identifying changes in the migration pat-
terns of different age classes within the population is crucial for
the proper understanding of how birds, and particularly ospreys,
may or may not persist under the current scenario of climate
change (Martín et al. 2016a).
The osprey is a clear example of a flagship species in the
framework of conservation management projects as well as in
projects for environmental protection (Muriel et al. 2010).
Ospreys frequently select conspicuous nest and perch sites,
it is easily identified and observed in the field, and it tolerates
well the presence of humans (Bierregaard et al. 2014), since
the potential disturbances of birds arising from human pres-
ence seem to be low in human-modified environments (e.g.,
Bird et al. 1996). For all these reasons, the osprey is a species
well suited to monitoring by citizen science projects.
In this study, we determined the present distribution and the
numbers of the ospreys wintering in the Iberian Peninsula by
means of the public participation of different organizations de-
voted to bird conservation from Portugal and Spain. Long-term
data counts available from southern Spain allowed us to quan-
tify the trend in the wintering osprey population over the last
16 years. Additionally, trends in migration counts are a broadly
accepted, cost-effective indicator of the breeding population
trend of a migratory species (Martín et al. 2016b). Long-term
data counts of migrating ospreys over the Strait of Gibraltar
from 1999 to 2016 conducted by volunteers were used to de-
termine the trends in the western European breeding population
of the osprey and to compare these trends with the observed
changes in the number of ospreys wintering in Iberia.
Our main aim was to provide evidence that the number of
wintering ospreys has been increasing in the Iberian Peninsula
over the years due to a shortening of migration distances and to
assess if these changes have been age- and population-specific.
Specifically, we compared trends in wintering and breeding
populations of ospreys in Iberia and western Europe, respec-
tively, and we identified the age and origin of the ospreys win-
tering in the Iberian Peninsula from recoveries of the ringed
ospreys. In addition, we provide a detailed description of the
present distribution and the numbers of ospreys wintering in the
Iberian Peninsula, which can be helpful for the conservation
and management of the species in Europe.
Methods
Study species
The osprey is a large, specialized fish-eating raptor inhabiting
freshwater lakes, reservoirs and rivers, as well as sea coasts,
estuaries and brackish water ecosystems. Ospreys breeding in
72 Page 2 of 13 Eur J Wildl Res (2019) 65:72
the Western Palearctic region (P. h. haliaetus; Linnaeus, 1758)
occur from the North African coast to the Arctic Circle (Poole
1989) but, due to more severe human disturbance south of the
northern populations, nowadays, most of the breeding popu-
lation is in the northern half of Europe. The Western Palearctic
osprey was extirpated in Portugal, mainland Spain and Turkey
in the 1980s and 1990s (Schmidt-Rothmund et al. 2014), al-
though a wild pair was recorded breeding in Portugal in 2015
(own unpublished data). In the Mediterranean region, only a
few small breeding populations (about 100 breeding pairs)
remain in Corsica, the Balearic and Chafarinas Islands, as well
as on the North African coast (i.e., Algeria and Morocco;
Monti 2015). This subspecies is also present in the Canary
and Cape Verde Islands and the Red Sea (Poole et al. 2017).
Because osprey populations are very large, and hence do not
approach the thresholds for Vulnerablebased on population
size, the species is globally classified as Least Concern
(BirdLife International 2017). In Spain and Portugal, howev-
er, ospreys are considered as Critically Endangered(Triay
and Siverio 2008;Cabraletal.2005; Equipa Atlas 2008).
After a reintroduction project started in 2003, almost 20 pairs
now breed in southern Spain (Muriel et al. 2010). A few more
pairs are found in Tuscany, Italy, as a result of the translocation
of juveniles from Corsica (Monti et al. 2014). A reintroduction
project is also ongoing in Portugal at the Alqueva reservoir
(Alentejo region). The project was started in 2011, and success-
ful breeding took place in the area for the first time in 2016,
after the translocation of 56 juveniles from Sweden and Finland
(Palma et al. 2019). Similarly, up to 70 juveniles were
translocated from Scotland to the Urdaibai Biosphere Reserve
(northern Spain) between 2013 and 2017 (Galarza 2019). In our
study, new established breeding individuals from the different
reintroduction projects have beenconsideredtobeanintegral
part of the ospreys breeding in Western Europe.
Although ospreys breeding in Europe mainly winter in sub-
Saharan Africa (Poole et al. 2017), ospreys breeding in the
Mediterranean islands and North Africa are frequently resi-
dent or short-distance migrants (Monti 2015; Monti et al.
2018) mostly traveling to wintering grounds in Spain and
Portugal (Monti et al. 2018). Ospreys wintering in the
Iberian Peninsula are the subject of the present study.
Data collection
Wintering distribution and population size in the Iberian
Peninsula
The censuses for data collection on the distribution and the
size of the osprey wintering population in Iberia were initially
promoted by the Birds of Portugalproject (Ave s de
Portugal;http://www.avesdeportugal.info/). These started in
January 2015 and provided a first estimate of the total number
of wintering ospreys in Portugal. In 2016, the public
participation network Friends of the Osprey(Amigos del
Águila Pescadora), led by the Migres Foundation
(Fundación Migres;http://www.fundacionmigres.org/
amigos-del-aguila-pescadora/) in Spain, joined the
Portuguese initiative, when wintering ospreys in Portugal
and the Andalusian region (southern Spain) were censused.
Within the framework of these two projects, 235 and 153
volunteers in Spain and Portugal, respectively (Fundación
Migres et al. 2017), representing more than 30 bird conserva-
tion organizations, were involved in an osprey wintering cen-
sus at the supranational scale on the Iberian Peninsula in the
20162017 winter. Volunteers were jointly coordinated by the
Birds of Portugal Project in Portugal and the Migres
Foundation in Spain.
Observations of wintering ospreys were carried out in
January 2017 over a variable number of days, depending on
the number of observers and the extent of the areas to be
covered in different provinces. Censuses covered the central
wintering period for the species (Casado 1999), which lasts
from mid-November until mid-March (Casado and Ferrer
2005). Observations were conducted from dawn to 13:00 h
GMT by professional ornithologists, bird watchers and bird
photographers initially contacted primarily through electronic
forums. Expert ornithologists coordinated the census at the
provincial level. Surveys covered those areas with osprey
presence previously reported as well as areas with suitable
habitat (i.e., water bodies with fish) that could be potentially
occupied by ospreys in Spain and Portugal(Casado and Ferrer
2005). Each coordinator was responsible to determine the
areas (i.e., water bodies) to be surveyed, ensuring that all the
water bodies where ospreys might potentially occur within a
province/district were surveyed. Although observers were
sometimes amateur ornithologists, all the survey teams were
led by an expert ornithologist having a good knowledge on the
study species.
Each water body was surveyed at least by 12 observers.
The only areas which were not surveyed were Guadalajara
and Albacete provinces, in Spain, due to the lack of volun-
teers. Ospreys usually use conspicuous perches (Ferguson-
Lees 1963), such as dead trees and artificial poles, facilitating
the sighting of the birds. Birds were recorded by direct obser-
vation from vantage points (Bibby et al. 1992) using binocu-
lars (10×) and telescopes (2060×). Both presence and ab-
sence data were recorded. To avoid double counting of birds,
local teams were coordinated and observers were in contact.
For each sighting, observers were required to provide location
(e.g., locality, departmentor province), date, geographic coor-
dinates (as precisely as possible) and the type of aquatic or
water system where the birds were observed (e.g., reservoirs,
rivers, lagoons, or marshes). Because osprey sex and age are
difficult to differentiate under field conditions (Poole 1989;
Blanco and Rodriguez-Estrella 1999) and even more difficult
for observers without previous experience, birds were not
Eur J Wildl Res (2019) 65:72 Page 3 of 13 72
classified by sex or age class. Counts of birds were conserva-
tive, reporting a minimum of observed birds to avoid duplica-
tions. All data collected at the provincial level were centralised
and reviewed by the research team applying a conservative
approach to set a minimum reliable number for observed os-
preys by preventing duplication of bird counts (i.e., birds ob-
served in nearby sites on consecutive dates) among provincial/
district censuses.
Wintering population trend in Andalusia (southern Spain)
Long-term data series of wintering ospreys for the whole of
the Iberian Peninsula are not available (Moreno-Opo 2012).
However, regional surveys of the wintering osprey population
were annually conducted in the Andalusian region (southern
Spain; Fig. 1) by professional ornithologists following a sim-
ilar methodology as described previously. Surveys in the
Andalusian region were carried out between 2004 and 2017
(CMAOT 2016; Fundación Migres et al. 2017). Additionally,
one of the largest osprey wintering population within the
Andalusian region (Bay of Cadiz, where around 28% of the
ospreys wintering in Andalusia are found; Jiménez and de las
Heras 2015;CMAOT2016) has been monitored since 2000;
so an even longer temporal data series is specifically available
for this site. Based on the overall long-term data series from
the Andalusian region and from the Bay of Cadizsite, we
estimated temporal trends in the population sizeof the ospreys
wintering in these areas accordingly.
Migratory population trends
Annual counts of ospreys migrating over the Strait of
Gibraltar have been recorded using standardized protocols
since 1999 (De la Cruz et al. 2011). From 1999 to 2016,
counts were conducted during the postnuptial migration be-
tween mid-July and mid-October. Numbers of migrants were
recorded on a daily basis at two different observatories
(Algarrobo 36°525N, 5°2902W and Cazalla 36°158N,
5°3436W). All observers were equipped with binoculars.
Main origins and age of wintering ospreys in Iberia
For quantifying the origin of ospreys wintering in the Iberian
Peninsula, we obtained information from 326 recoveries in
Spain for 19302014 provided by the SEO (Spanish
Ornithological Society) database and 11 recoveries in
Portugal up to 1999 (Catry et al. 2010) from birds ringed as
nestlings (i.e., known age at the time of the recovery). Using
these databases, we could identify the principal origins and the
age of wintering ospreys by selecting records of ospreys
Fig. 1 Location of the study area. Iberian Peninsula (Portugal and Spain), Andalusian region and Bay of Cádiz
72 Page 4 of 13 Eur J Wildl Res (2019) 65:72
ringed in their breeding grounds and subsequently recovered
in Spain and Portugal during winter. In this study, we refer to
migration distance as the linear distance between the breeding
and the wintering sites according to the recoveries of the
ringed birds.
Records were considered to reflect wintering if the birds
were recovered between 15th November and 31st January,
since, after this month, migratory ospreys returning from their
wintering grounds can also be observed in Iberia.
Data analysis
Population trends
Trends in wintering ospreys in Andalusia and the Bay of
Cadiz, as well as trends in the number of birds migrating over
the Strait of Gibraltar, were quantified. Because a trend may
be described by the geometric mean rate of population change
over time (Link and Sauer 1997), if the trend is linear, the
geometric mean rate of change can be estimated by fitting a
linear regression to the logarithm of the annual counts (Farmer
and Hussell 2008). We estimated the magnitude and signifi-
cance of the trends in wintering and migratory ospreys by
fitting log-linear models (Martín et al. 2016b) using general-
ized least squares (GLS) (package nlme in R; Pinheiro et al.
2017). GLS generalizes ordinary least squares to the case
where the residuals have a normal distribution with an arbi-
trary covariance matrix. In these extended linear models, the
errors are allowed to be correlated in such a way that we can
directly model temporal autocorrelation. Temporal autocorre-
lation (ACF) and partial temporal autocorrelation (PACF)
functions for all the models were inspected to identify the
form of the temporal autocorrelation structure. In case any
significant autocorrelation was detected, this autocorrelation
structure was specified in the GLS models; thus there was no
remaining autocorrelation in the residuals of the final models
(Box et al. 2008). The annual rate of change over the study
period was then measured from the coefficient of the year
variable in the regression models and multiplied by 100.
This result represents the annual percentage change in the
population and linear change in the log scale (Dunn and
Hussell 2009). We used Akaikes information criteria, AIC
(Akaike 1973), to identify the most robust and parsimonious
(avoiding over-fitting) among the different ARIMA models
(i.e., the model with the lowest AIC) that we tested. If several
models had low and similar AIC values (delta AIC < 2), then
we selected the model without temporal autocorrelation that
showed the lowest AIC (Burnham and Anderson 2002).
Main origins and age of wintering ospreys in Iberia
We analyzed differences in frequency of the ringed ospreys
recovered in Spain (SEO database) and Portugal (Catry et al.
2010) in relation to the grand totalsrecord of ringed ospreys
(EURING, accessed on 4th January 2018; https://euring.org/
data-and-codes/ringing-totals) per breeding country by means
of χ
2
test. To allow for correct approximation of χ
2
,we
grouped all the breeding countries with null recoveries in a
new group named others. Additionally, we used survival
rates reported by Wahl and Barbraud (2013)toestimatethe
age structure of a theoretical European breeding population of
osprey. Then,we compared this age structure with the propor-
tion of birds recovered during winter in Spain for each age
class by means of χ
2
test. We considered three different age
classes (< 1 yr, 12 yr, > 2 yr) that were meaningful according
to the life history of the species, i.e. juveniles, immature birds
and adult breeding birds (Wahl and Barbraud 2013). Although
these rates refer to a relatively new established population,
which may not represent all the other ospreys populations
across Europe due to density-dependence effects on survival,
this is the only available detailed analysis per age class on this
species in Europe.
All analyses were performed using R 3.4.1 (R Core
Development Team).
Results
Census results
During the census in January 2017, we detected the presence
of wintering ospreys at 28 Portuguese and 71 Spanish sites
(Fig. 2and Table 1; see also Table S1 and Fig. S1 in the
Supplementary Material). We collected a minimum of 204
confirmed field sightings of wintering ospreys in Spain and
155 in Portugal. These records were mostly observed (more
than 75% of the individuals) in the provinces of Cádiz, Huelva
and Seville (in Spain) and in the districts ofSantarém, Setúbal,
Faro, Aveiro and Lisbon (in Portugal). The Andalusian region
contained 77% of the ospreys wintering in Spain and 44% of
all the Iberian wintering birds. Main waterbodies selected by
ospreys for wintering in Spain were the Doñana Natural Site
(which includes a set of four interdependent water bodies i.e.,
Doñana, Isla Mayor, Isla Menor and Isla Minima; 45 birds;
see Table S1 in the Supplementary Information), the Bay of
Cadiz (36 birds) and Marismas del Odiel (14 birds).
Regarding wintering ospreys in Portugal, the Tejo River (56
birds) and the estuaries of Aveiro (29 birds), Formosa (23
birds), Sado (20 birds) and Tejo (14 birds) were the sites with
the largest number of birds, representing more than 75% of the
total birds recorded in Portugal. The wintering population of
ospreys in the Iberian Peninsula is distributed both in coastal
marshes and lagoons as well as in natural and artificial inland
water bodies. Up to 75% of the birds were observed at natural
water bodies whereas 25% of the ospreys were found at res-
ervoirs (Table S2, see the Supplementary Material).
Eur J Wildl Res (2019) 65:72 Page 5 of 13 72
Trends in wintering and migratory populations
The inspection of the temporal autocorrelation functions
(ACF and PACF) for the regression models showed no signif-
icant autocorrelation at any time lag for the time series of
wintering ospreys in Andalusia. However, we detected a tem-
poral dependency in the case of ospreys wintering in the Bay
of Cadiz, as well as for ospreys migrating over the Strait of
Gibraltar. The latter time series also showed evidence of non-
stationarity. An AR(1) autocorrelation structure was enough to
take into account the temporal autocorrelation in the Bay of
Cadiz wintering data. An autocorrelation structure of first or-
der AR(2) and three moving average terms MA(3) properly
modeled the autocorrelation structure and eliminated the non-
stationarity of the migratory population dataset (Tables 2and
3). All the studied osprey populations showed significantly
increasing trends (Fig. 3). There is considerable agreement
in the trends for the studied wintering populations (annual rate
of change for Andalusian osprey wintering population, 4.3%;
for Bay of Cadiz population, 5.6%) and the trend of those
birds migrating over the Strait of Gibraltar (annual rate of
change, 5.37%).
Ringed birds
Ringing recoveries on wintering ospreys came from 61
individuals in Spain and 11 in Portugal (Table 4).All
the birds except for a 6-yr-old female were ringed as
chicks at their nests. In accordance with the census re-
sults, most of the ringed birds recorded in Spain during
the winter were recovered in Cadiz (28%) and Huelva
(35%) provinces. The main origins of the birds were
Germany (41% of the recoveries), Sweden (24%) and
Great Britain (18%). According to the χ
2
test results,
the frequency of birds recovered from Finland and
Sweden, as well as from other countries (Belarus,
Denmark, Italy, Netherlands, Poland and Switzerland)
was lower than expected, whereas recoveries from
France, Germany, Norway, Spain and Great Britain were
more frequent (χ
2
= 215.33, df = 7, P< 0.0001; Fig. 4).
Since available data on grand totalsfrom birds ringed
inNorwayandFrancewerenotupdated(seeTableS3
in the Supplementary Material), results for these coun-
tries must be interpreted with caution. Based on the low
number of recoveries of ringed birds of known sex (N=
17), we did not detect differences in the frequency of
recovered males and females per country. Regarding the
age of the birds recovered in Spain, 49% of the ospreys
were younger than 1 year, 26% were immature birds
(12 year) whereas 25% were > 2 years. The theoretical
age structure estimated was consistent with data provid-
ed by other authors (Poole 1982;seeTableS4 in the
Supplementary Material). Comparisons between age
structure of the birds recovered during winter and age
structure of the breeding population showed that imma-
ture (12 yr) birds were recovered nearly as expected
according to the theoretical breeding population age
structure. In contrast, adult birds (> 2 yr) were less fre-
quently observed whereas juveniles were recovered in a
higher proportion than expected (χ
2
= 19.70, df = 2,
P< 0.0001; Fig. 5).
Table 1 Census results of wintering ospreys in the Iberian Peninsula in
January 2017. Counts recorded in the Bay of Cadiz (Bahia de Cádiz)
are included within the counts in the Andalusian region (see also Table S3
in the Supplementary Material)
Country Region Number of birds
Portugal Aveiro 23
Beja 3
Braga 3
Bragança 0
Castelo Branco 0
Coimbra 2
Évora 5
Faro 24
Guarda 0
Leiria 1
Lisboa 18
Portalegre 5
Porto 1
Santarém 39
Setúbal 29
Viana do Castelo 2
Vila Real 0
Viseu 0
Spain Andalucía 160
Asturias 4
Aragón 0
Cantabria 3
Castilla-La Mancha ?
Castilla-León 0
Cataluña 7
Extremadura 10
Galicia 14
La Rioja 0
Madrid 0
Murcia 0
Navarra 0
País Vasco 0
Valencia 6
Portugal 155
Spain 204
TOTAL 359
72 Page 6 of 13 Eur J Wildl Res (2019) 65:72
Discussion
In this study, we show that the number of wintering ospreys
has been increasing in southern Spain over the last 16 years.
The magnitude of this increase is similar to the rate of change
of Western European ospreys, as derived from annual counts
of ospreys migrating over the Strait of Gibraltar. Recoveries of
ringed birds in the Iberian Peninsula during winter indicate a
reduction in the migration distances of Central and Northern
European ospreys, making these birds winter at higher lati-
tudes more than before. According to our results, this
reduction in the migration distance was fairly uniform among
different breeding populations in western Europe, but it did
not affect all age classes equally, and we found that juvenile
birds were more prone to winter at higher latitudes compared
to adult birds.
Distribution numbers and trends
Wintering ospreys in the Iberian Peninsula, as with many win-
tering wading bird species from northern Europe (Domínguez
1990) occur mainly at locations on the Atlantic coast.
Although the Portuguese osprey wintering population is most-
ly distributed in coastal water bodies, an important number of
the Spanish wintering birds, specifically those ospreys
Fig. 2 Wintering osprey
population size and distribution in
the Iberian Peninsula (winter
20162017). All districts
(Portugal) and provinces (Spain)
were surveyed except for
Guadalajaraand Albacetein
Spain. Districts/provinces and lo-
cation of water bodies are shown
in the map
Table 2 Model selection among different ARIMA structures for
models with temporal autocorrelation in the residuals. (a) Migratory pop-
ulation over the Strait of Gibraltar; (b) wintering population in the Bay of
Cadiz. MA, moving average model; AR, autoregressive model. No sig-
nificant autocorrelation was found for the time series of wintering ospreys
in Andalusia. Best fit model without temporal autocorrelation pattern is
underlined
Df Log.lik AIC Delta AIC
(a)
Basic model 3 11.11 28.21 0.00
MA1AR1 6 8.18 28.36 0.15
MA1AR2 6 8.18 28.36 0.15
AR1 4 10.69 29.38 1.17
MA3AR2 86.78 29.56 1.35
AR2 5 10.31 30.63 2.42
MA2AR2 7 9.77 33.54 5.32
(b)
AR1 4 8.73 25.47 0.00
Basic model 2 10.93 27.86 2.40
Table 3 Log-generalized least-square models to the time series of the
(a) osprey wintering population in Andalusia; (b) in the Bay of Cadiz; and
(c) of the osprey migratory population over the Strait of Gibraltar. Best fit
models for ospreys through the Strait of Gibraltar and for ospreys winter-
ing in the Bay of Cadiz included temporal correlation and moving aver-
age structures (see Table 2)
Estimate Std. error tvalue Pvalue
(a)
(Intercept) 82.053 21.188 3.873 0.002
Year 0.043 0.011 4.085 0.002
(b)
(Intercept) 110.313 41.189 2.678 0.017
Year 0.056 0.021 2.752 0.014
(c)
(Intercept) 103.525 46.087 2.246 0.039
Year 0.054 0.023 2.337 0.033
Eur J Wildl Res (2019) 65:72 Page 7 of 13 72
wintering in Cadiz province, can be found at artificial reser-
voirs. Reservoirs are frequently occupied by ospreys in most
of their breeding range, but they are a relatively new ecosys-
tem for ospreys in Iberia (Casado and Ferrer 2005). Although
the destruction of the natural habitats available for the ospreys
in the Iberian Peninsula during the first half of the twentieth
century could have limited the occurrence of ospreys in
Portugal and Spain, artificial reservoirs offer new available
habitats for this species in Iberia, both for wintering and for
breeding individuals (Casado and Ferrer 2005).
Reservoirs contain an important stock of native and exotic
fish (Mancini et al. 2009); thus, they provide new feeding
opportunities for ospreys (Fuentes et al. 1998). Most of the
dams built in Spain (96%) were finished before 1999 and only
4% were built since 2000. Although habitat availability pro-
vided by reservoirs existed prior to the observed increases in
the osprey wintering population in Iberia, the use of artificial
impoundments may have contributed to the observed changes
in the migratory behaviour of the European ospreys.
Our counts largely exceed the most recent estimations of
ospreys wintering in the Iberian Peninsula (Moreno-Opo
2012). According to our results from the Andalusian region,
which encompassed more than the 40% of the Iberian winter-
ing osprey population, during the last 16 years, ospreys
regularly observed during winter have increased by around
4% if all the Andalusian region is considered, with an increase
of about 6% in Bay of Cadiz, one of the largest wintering
populations in Iberia, led only by the Doñana Natural Site.
The national censuses carried out in Portugal by Aves de
Portugal during the last three years also support a positive
trend in the numbers of ospreys wintering there (unpublished
data), although this increase is possibly related to a better
monitoring coverage of the country.
Increases in the European breeding population size of os-
preys observed in our results from migratory birds are sup-
ported by censuses conducted in different areas across Europe.
The decline of ospreys breeding in Europe in the 19th and
20th centuries, caused mainly by habitat loss and direct per-
secution, has been followed by population increases, both in
terms of population size and of spatial distribution (Dennis
2016). Compared to numbers from the 1980s, osprey breeding
pairs in Europe and the Middle East have almost doubled in
the early twenty-first century, although the largest European
populations (in Sweden, Finland and Russia) appear to be
stable, and negative trends were observed in Poland, as well
as in southeastern Europe and northern Africa (Schmidt-
Rothmund et al. 2014). According to our results from migra-
tory counts at the Strait of Gibraltar, the rate of change in the
0
50
100
150
1999 2002 2005 2008 2011 2014 2017
number of birds
year
Fig. 3 Trends in the wintering
population of osprey in Andalusia
(white dots); in the wintering
population of osprey in the Bay of
Cadiz (black dots); and in the
osprey migratory population
(grey dots). Trends are measured
as the back-transformed slope of
the log-generalized linear regres-
sion models to the time series of
annual osprey counts
Table 4 Summary of the ringing
recoveries on wintering ospreys
recovered in Spain and Portugal
Breeding
country
Number of recoveries in
Spain
Number of recoveries in
Portugal
Total n umb er of
recoveries
Finland 4 0 4
France 2 0 2
Germany 27 2 29
Norway 2 1 3
Spain 2 0 2
Sweden 12 5 17
Great Britain 10 3 13
72 Page 8 of 13 Eur J Wildl Res (2019) 65:72
number of wintering birds in southern Spain and the trends
observed in the breeding population of western Europe are of
similar magnitude (annual rate of 5%, in 19992016)
supporting a relationship between the recovery of the
European breeding population and the increases inthe number
of wintering birds. However, the rise in numbers of ospreys
breeding in western Europe has probably been underestimated
using migratory counts, because a growing number of ospreys
are shortening their migratory routes and no longer crossing
the Strait of Gibraltar (Link and Sauer 1997). In contrast,
released birds in the framework of the different reintroduction
projects across Iberia (Muriel et al. 2010; Palma et al. 2019;
Galarza 2019) have likely contributed to increase the counts of
ospreys migrating over the Strait of Gibraltar.
Although long-term data series of wintering ospreys are not
available for the whole of the Iberian Peninsula, it is widely
recognized that more and more ospreys spend the winter in the
Iberian Peninsula instead traveling further south to Africa
(Triay and Siverio 2008; Gil and Valenzuela 1997;Sanz
1997;Dennis2008). Occasional winter observations, mainly
of Swedish and Finnish ospreys, were detected in central and
southern Europe before 1973 (Österlöf 1977)althoughreal
wintering did not take place (Glutz von Blotzheim et al.
1971). Our results showed that a growing number of individ-
uals, currently about 3% of the total breeding population esti-
mated for western Europe (BirdLife International 2015), are
behaving as short-distance migrants, mostly traveling to win-
tering grounds in Spain and Portugal. Similarly, there is also a
continent-wide increase in osprey populations and a northerly
shift in the areas where ospreys overwinter in North America
(Bierregaard et al. 2016), supporting that the shortening of the
migration distances shown in our study is a global-scale
phenomenon.
As with other long-distance migrant species breeding in
temperate regions and specifically raptors, ospreys are short-
ening their migrations likely in relation to climate and other
land use changes (Martín et al. 2014,2016b). Shorter migra-
tion distance is expected to enhance the survival rates of indi-
viduals (Klaassen et al. 2014), therefore contributing to the
increase in the number of birds exhibiting this behaviour
and, in the long term, increasing the numbers of the ospreys
wintering in Iberia.
0%
20%
40%
60%
80%
100%
Fig. 4 Ratio between observed
(white bars) and expected
(black bars) frequencies of
recovered ospreys per age class
(χ
2
= 19.70, df = 7, P< 0.0001)
0%
20%
40%
60%
80%
100%
<1yr 1-2yr >2yr
Fig. 5 Ratio between observed
(black bars) and expected (white
bars) frequencies of recovered
ospreys per ringing country
(χ
2
= 215.33, df = 2, P< 0.0001).
< 1 yr, juveniles; 12yr,
immature; > 2 yr, adult birds
Eur J Wildl Res (2019) 65:72 Page 9 of 13 72
Age- and population-specific shortening
of the migration distance
Differences in the response of migratory birds among popula-
tions and among fractions within the same population (Cristol
et al. 1999) imply differential costs of climate change (Wood
and Kellerman 2015), leading to differential selection among
populations and groups within the same population.
Records of ospreys ringed at their breeding grounds and
subsequently recovered in Spain and Portugal during winter
showed that wintering birds in Iberia come from almost any
point of the species breeding range across western Europe
(BirdLife International 2017). Our results showed that most of
the birds wintering in Spain and Portugal breed in Germany,
GreatBritainandpossiblyinFrance.Ospreysringedatbreed-
ing sites from Finland and Sweden, however, were found less
frequently than expected in Iberia during winter. Ringed os-
preys breeding in Sweden and Finland are frequently recovered
in Spain during autumn migration (SEO/BirdLife 2012)be-
cause most Swedish birds and some Finnish individuals mi-
grate along the western migratory flyway (Österlöf 1977).
However, breeding birds in these countries may also migrate
through the central and eastern migratory flyways (Österlöf
1977), reaching Africa over the Strait of Messina in Italy and
over the Bosphorus, respectively (Porter and Beaman 1985).
Moreover, lower proportion of recoveries detected from other
countries(i.e., Belarus, Italy, Netherlands and Switzerland) is
likely related to the extirpation of the osprey from these coun-
tries during the mid-twentieth century. Therefore, in contrast to
results from other European raptor species showing a reduction
in migratory distances related to the latitude where the birds
breed (Martín et al. 2014), the observed reduction in the osprey
migration distance seems to be fairly uniform among different
breeding populations across western Europe.
European ospreys usually remain in their wintering areas in
Africa during their first and second years before returning to their
breeding areas once they reach two years old (Cramp and
Simmons 1980;Poole1989;Montietal.2018). However, ac-
cording to ringed birds recovered in Spain, ospreys wintering in
Iberia are mostly juvenile and immature birds, whereas adult
birds were observed in lower proportion than expected, suggest-
ing adult ospreys are responding differently to the ecological
conditions at their wintering grounds compared to juvenile birds.
Previous studies have shown the ability of juveniles of long-lived
and long-distance migrant species to alter their migratory patterns
according to environmental conditions, allowing these inexperi-
enced birds to respond to climate change (Martín et al. 2016a,b).
Adult and juvenile ospreys seem to follow a similar migration
pattern during autumn although juvenile birds appear to migrate
later (Österlöf 1977). It is known that juvenile birds tend to
migrate further south than adults in many raptor species.
However, this does not seem to be the case among ospreys,
and a comparison of the proportion of juvenile and adult birds
in western Africa during winter did not show differences between
age classes (Österlöf 1977). In contrast to adult birds of other
raptor species, which are shortening their migration distance
more than juveniles in response to climate change (Martín et al.
2014), according to our results, juvenile ospreys show a stronger
tendency to winter at higher latitudes than adult birds. One pos-
sible explanation for this could be related to the experienced
gained by older individuals. On the basis of their previous expe-
rience,ospreysusuallyreturntothesamewinteringlocationyear
afteryear(Poole1989). With no previous experience, juvenile
ospreys could try out a variety of stop-over sites before deciding
their preferred wintering location and, therefore, be more likely to
explore new wintering locations at higher latitudes.
Whatever the reason, most juvenile ospreys remain within
their wintering grounds in Africa throughout the year (Cramp
and Simmons 1980; Poole 1989; Monti et al. 2018). If the
juvenile birds wintering in Iberia also remain once winter is
over, they could play an important role in the future recovery
of the species in continental Spain and Portugal by means of
the reinforcement of the recently reintroduced breeding pop-
ulation through a conspecific attraction mechanism (Poole
1989;ThibaultandBretagnolle2001).
Other short-distance and non-migratory osprey
populations
Ospreys breeding in the Mediterranean basin number less than
100 breeding pairs distributed within Corsica, the Balearics,
Morocco and Algeria, and about 20 additional pairs belonging
to the recent reintroduction projects in the Iberian Peninsula
(Dennis 2016). Ospreys breeding in the Mediterranean islands
and North Africa are frequently resident or short-distance mi-
grants which mainly winter in the Mediterranean basin coasts
(Monti et al. 2018) thanks to the mild winter conditions and fish
availability in these areas (Poole 1989). In contrast, breeding
birds belonging to reintroduced populations in Spain and
Portugal showed a long-distance migratory pattern similar to
birds from the donor populations (in Finland, Germany,
Scotland and Sweden). Although some other individuals have
been found to be year-round residents after the reintroduction
(Muriel et al. 2010), from the 129 young ospreys reintroduced
in southern Spain, ringed and released between 2003 and 2009,
only six non-migratory young birds remained in the reintroduc-
tion areas, whereas the reintroduced breeders left the area after
the breeding (Muriel et al. 2010). It is probable that year-round
resident birds of the recently reintroduced breeding population in
continental Spain and Portugal are also contributing to increase
the wintering population of the ospreys in Iberia by attracting
new wintering birds that have originated in northern and central
Europe, as well as short-distance migrants from the
Mediterranean islands through a conspecific attraction mecha-
nism (Poole 1989; Thibault and Bretagnolle 2001). However,
the information provided by the recoveries of ringed ospreys
72 Page 10 of 13 Eur J Wildl Res (2019) 65:72
indicates that these Mediterranean populations play a minor, if
any role, in the observed trends in the number of wintering os-
preys in the Iberian Peninsula, because most of the wintering
birds originated in northern and central Europe and none of the
recoveries from birds ringed in the Mediterranean basin (i.e., two
adult ospreys ringed in Spain) belonged to birds that were born or
released in the framework of any reintroduction project in Spain
and Portugal. In addition, the main wintering areas in the Iberian
Peninsula identified in our study (i.e., water bodies located in
Cadiz and Huelva provinces) were also historical sites with high
densities of ospreys during winter before the reintroduction pro-
ject started in 2003, showing numbers about ten times higher
than average densities in other Spanish regions during winter
before 1990 (Ferrer and Casado 2014).Moreover, the wintering
distribution of ospreys in the Iberian Peninsula covers a wider
spatial range compared to the reintroduced breeding population.
Specifically regarding southern Spain, birds of the recently
established breeding population only occurred in six different
water bodies (Muriel et al. 2010), whereas wintering ospreys in
our study were observed in a total of 22 (data for year 2017).
Implications for osprey conservation
Ospreys usually return to the same wintering location year after
year (Poole 1989). Therefore, the identification of sites used by
ospreys during winter is of major importance to preserve those
areas from threats that represent a potential mortality risk, such
as habitat loss, pollution and direct persecution (Newton 1979).
Because osprey habitat requirements during winter appear to be
similar to those needed during the breeding period, the winter-
ing distribution here reported could also be a useful tool when
identifying new areas for future reintroduction projects (Casado
and Ferrer 2005) if required. Together with protection, habitat
management of these areas can also benefit the growing num-
ber of wintering ospreys as well as the increase and expansion
of the breeding population in the Iberian Peninsula.
The osprey is a conspicuous species, and its suitable habitat
is easily identifiable. In this context, public participation be-
comes an excellent tool to maintain a non-expensive monitor-
ing of the species covering the level of a large area, such as the
Iberian Peninsula. This long-term monitoring will allow us to
track the future changes in the population size and the migra-
tory behaviour of this species across western Europe.
Acknowledgements We are grateful to the volunteers and collaborators
who collected the information presented in this study (Fundación Migres
et al. 2017; Migres programme 19992016) as well as to the Board of the
Migres Foundation. We are also grateful to the Spanish Ornithological
Society (SEO) which made the recovery data available and to the many
ringers and ringing scheme staff who have gathered and prepared the data.
Special thanks to Andrew Paterson for his kind revision of the language
of the manuscript. Finally, we would like to thank the editor and two
anonymous referees for providing us with comments and suggestions that
greatly help to improve the manuscript.
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... At the Western Palearctic scale, northern and central European ospreys undertake longdistance migratory journeys up to ca. 6000 km towards sub-Saharan wintering grounds (Alerstam et al. 2006;Bai and Schmidt 2012;Østnes et al. 2019). There are also records of a few northern and central European ospreys wintering in Southern Spain and Italy, especially males from UK and Germany (MacKrill 2017; Bai and Schmidt 2012;Martín et al. 2019). Such numbers seem to be increasing, most likely in relation to climate warming effects and other land use changes (e.g. ...
... Such numbers seem to be increasing, most likely in relation to climate warming effects and other land use changes (e.g. Li et al. 2021;Valipour et al. 2021), although they represent only about 3% of the total breeding population estimated for Western Europe (Martín et al. 2019;Monti 2021). ...
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