Recent changes on migratory behaviour of the White stork (Ciconia ciconia) in Portugal: towards the end of migration?

Abstract

Historically, the White stork (Ciconia ciconia) was almost entirely migratory in Europe, but
recently increasing numbers of individuals started wintering in their Iberian breeding grounds. We
performed a survey in 2015 to estimate the number of wintering storks in Portugal and assess the
last two-decade trend based on results from seven previous surveys performed between 1995 and
2008. The number of wintering storks increased from 1,187 individuals in 1995 to 14,434 in 2015.
Although the breeding population showed a considerable boost during the same period, the proportion
of resident individuals increased substantially in the last two decades (from 18% to 62%),
suggesting a sound change in the migratory behaviour of this species towards fully residency.

Full text

Changes on the migratory behaviour of the White Stork
28
Recent changes on migratory behaviour of the
White stork (Ciconia ciconia) in Portugal:
Towards the end of migration?
Alterações recentes do comportamento
migratório da Cegonha-branca (Ciconia
ciconia) em Portugal: O fim da migração?
Inês Catry1,2,3*, Vítor Encarnação4, Carlos Pacheco5,
Teresa Catry6, Paulo Tenreiro7, Luís P. da Silva8,
Fernando L eão9, Filipe Bally10, Sara Roda10, Si lvério
Lopes11, Carlos Capela11, Hany Alonso2,12, Sérgio
Saldanha13, Otília Urbano13, Jorge Saraiva14, Paulo
Encarnação15, Nuno Sequeira16, Miguel Mendes17,
Paulo Monteiro18, Gonçalo Elias19 & Francisco
Moreira1,2
1 Centro de Ecologia Aplicada “Prof. B aeta Neves” & InBio – Rede de Investigação em Biodiversidade e Biologia Evolutiva, Instituto Sup erior
de Agronomia, Universidade de Lisboa, Tapada da Ajuda, 1349-017 Lisboa, Por tugal . 2 REN Biodiversity Chair, CIBIO/InBIO - Rede de
Investiga ção em Biodiversida de e Biologia Evolutiva, Uni versidade do Porto, Campus Agrári o de Vairão, 4485-601 Vairão, P ortugal. 3 School
of Environment al Sciences, University of East Anglia, Norwich, NR4 7TJ, United Kingdom. 4 Instituto da Conservação da Natureza e das
Floresta s, IP, Divisão de Conser vação da Biodiver sidade, Centro de Estud os de Migrações e Proteção de Aves, 2890 -015 Alcochete , Portugal.
5 Rua João de Freitas Branco, nº. 38 - 2º Dto. 1500-359 Lisboa. 6 Centro de E studos do Ambiente e do Mar (CESAM), Departamento de
Biologia Animal, Faculdade de Ciências da Univer sidade de Lisb oa, 1749-016 Lisboa, Portugal. 7 Rua 25 de Abril, 16 - 3020 575 Brasfemes,
Portugal. 8 Centro de Ciências do Mar e do Ambiente (MARE) e Centro de Ecologia Funcional (CEF), Departamento de Ciências da Vida,
Universidade de Coimbra, 3000-456 Coimbra, Por tugal. 9 Núcleo Regional de Aveiro da Quercus - A.N.C.N., Apartado 363, 3811-905 Aveiro,
Portugal. 10 Divisão de Ambiente, Município de Portimão, Largo 1º de Maio, 8500 -543 Portimã o, Portugal. 11 Instituto da Conservação da
Natureza e das Florestas, IP, Departamento de Conserva ção da Natureza e Florestas do Algarve, Parque Natural da Ria Form osa, Divisão
de Gestão Operacional e Fiscalização, CEAM, Quinta de Marim, Quelfes, CP - 8700-194 Olhão, Portugal. 12 CIBIO/InBio-UE, Centro de
Investiga ção em Biodiversid ade e Recursos Genéti cos, Pólo de Évora, Univ ersidade de Évora, Nú cleo da Mitra, Aparta do 94, 7002-554, Évora,
Portugal. 13 Quinta da Fonte, Caixa nº 4505, 6200 -065 Covilhã, Portugal. 14 Rua 26, Lote 533, Marquesa I, 2950 -680 Qta do Anjo, Palmela,
Portugal. 15 Estação Ornitológica Nacional Monte do Outeirão, Apartado 139, 7500-014 Vila Nova de Santo André, Portugal. 16 Quercus,
Centro Associativo do Calhau, Bairro do Calhau, 1500-045 Lisboa, Portugal. 17 Rua David Teixeira nº 226 2º Dto 8100 Loulé, Por tugal. 18
Instituto da Conservação da Natureza e das Florestas, IP, Reserva Natural do Sapal de Castro Marim e Vila Real de Santo António, Sapal de
Venta Moinhos , Apartado 7, 8951-909 Castro Marim , Portugal. 19 Apartado 19016, 1991-901 Lisboa, Portugal.
VOLUME 24 2016 | 2017
Historically, the White stork (Ciconia ciconia) was almost entirely migratory in Europe, but
recently increasing numbers of individuals started wintering in their Iberian breeding grounds. We
performed a survey in 2015 to estimate the number of wintering storks in Portugal and assess the
last two-decade trend based on results from seven previous surveys performed between 1995 and
2008. The number of wintering storks increased from 1,187 individuals in 1995 to 14,434 in 2015.
Although the breeding population showed a considerable boost during the same period, the pro-
portion of resident individuals increased substantially in the last two decades (from 18% to 62%),
suggesting a sound change in the migratory behaviour of this species towards fully residency.
ABSTRACT
* Corresponding author: inescatry@gmail.com
Keywords: census, migration, Portugal, wintering population, White Stork.

Changes on the migratory behaviour of the White Stork
29
Nas últimas décadas, um número crescente de Cegonhas-brancas (Ciconia ciconia) passa
o inverno na Península Ibérica, em vez de migrar para África. Em 2015 foi realizado um
censo nacional para determinar o número de indivíduos invernantes em Portugal e com-
parar com a tendência registada nas últimas duas décadas, baseado em sete censos realiza-
dos entre 1995 e 2008. O número de Cegonhas-brancas invernantes aumentou de 1,187
indivíduos em 1995 para 14,434 contabilizados em 2015. Embora este aumento seja em
parte justificado pelo aumento do efectivo reprodutor nas últimas duas décadas, a pro-
porção de indivíduos residentes aumentou substancialmente no mesmo período (de 18%
para 62%), sugerindo uma alteração no comportamento migratório da espécie que poderá,
no futuro próximo, tornar-se residente.
The migratory behaviour of birds is
changing in response to global environ-
mental change. Many migratory species
are modifying their migratory phenology
by advancing spring arrival to the breeding
areas (Cotton 2003, Jonzén et al. 2006),
shifting their breeding and wintering ranges
and shortening their migration distances by
wintering closer to the breeding grounds
(Visser et al. 2009, La Sorte & Jetz 2010).
In recent decades, even more profound and
fascinating changes to migratory behaviour
have occurred, with individuals from migra-
tory species abandoning migration com-
pletely (Newton 2008). In southern Europe,
particularly in the Iberian Peninsula, previ-
ously fully migratory species have recently
established non-migratory populations
(Berthold 2001, SEO/Birdlife 2012).
The iconic White stork (Ciconia ciconia)
is a very adaptable, opportunistic species.
After a sharp decline of the western Euro-
pean populations recorded in the mid-20th
century, likely due to the prolonged Suda-
no-Sahelian drought and locust control pro-
grams in this area (Dallinga & Schoenmak-
ers 1989), the Iberian population started to
recover in the mid-1980s. Increased food
availability and milder temperatures in
winter have enabled an increasing number
of residents, i.e., individuals that choose to
stay in Iberia rather than migrate to Africa.
Residency, coupled with changes in drought
conditions in the Sahel were thought to be
important in reversing the strong popula-
tion decline in Europe (Tortosa et al. 2002).
In Portugal, the recovery of the White stork
population also started in the mid-1980s.
The breeding population increased contin-
uously from 1,533 pairs in 1984 to 3,302
in 1994, 7,684 in 2004 and 11,691 in 2014
(Encarnação 2015). Although considered
traditionally a fully migratory species, some
authors refer the presence of small num-
bers of wintering storks in the rst half of
the 20th century and the existence of small
ocks during the decades of 1960 and 1970
(Tait 1924, Coverley c. 1945, Cary 1973).
This paper aimed at estimating the cur-
rent number of wintering storks in Portugal
and assessing the last two-decade trend of
resident storks based on results from seven
previous surveys performed between 1995
and 2008.
Introduction
RESUMO
Palavras-chave: Cegonha-branca, censo, migração, população invernante, Portugal.

Changes on the migratory behaviour of the White Stork
30
Methods
A program to monitor the number of winter-
ing white storks was launched in 1995, but the
last out of the seven census occurred in 2008
(Rosa et al. 2009). In 2015, between 5 and 10
October, we surveyed the wintering popula-
tion of white storks in Portugal to describe the
trend of the wintering population comparing
with data from seven previous surveys (1995
to 2008). The same survey was used to assess
the proportion of resident individuals, i.e., indi-
viduals that stay in Portugal all year-round.
After breeding, most migratory individuals
cross the Strait of Gibraltar towards their Afri-
can wintering grounds till the end of August
(Fernández-Cruz 2005). Migratory storks can
start their pre-nuptial migration very early,
but not before the end of October (Fundación
MIGRES, pers. comm.). From mid September
to mid November, the number of emigrants
and immigrants is residual (Rosa et al. 1998,
pers. obs.). Therefore, we considered the win-
tering birds counted during the survey period
as resident ones, although acknowledging that
these gures might be slightly overestimated by
the inclusion of birds from northern breeding
areas. Surveys included all areas where the spe-
cies is known to winter regularly, giving special
attention to areas with known high winter food
availability, such as landll sites and rice elds,
where the birds tend to concentrate (Figure 1).
1
2
35
67
8
129
4
10
11
1. Ria de Aveiro
2. Baixo Mondego
3. Vale do Tejo
4. Vale do Sorraia
5. Avis landll
6. Sado
7. Évora landll
8. Beja landll
9. Barlavento landll
10.Sotavento landll
11. Ria Formosa
12.Castro Marim
Figure 1 - Main wintering sites of white storks (Ciconia
ciconia) in Portugal surveyed between 1995 and 2015
(Rosa et al. 2009 and this study).
Figura 2 - Principais áreas de invernada de Cegonha-
branca (Ciconia ciconia) em Portugal entre 1995 e
2015 (Rosa et al. 2009 e presente estudo).

Changes on the migratory behaviour of the White Stork
31
Results
The number of wintering white storks in
Portugal has increased signicantly from
1,187 individuals in 1995 to 14,434 in
2015 (Table 1, Figure 2). Most birds con-
centrated in areas of rice elds (68%) and
landll sites (21%) where birds likely rely
on the guaranteed year-round food supply,
namely Red-swamp Craysh (Procambarus
clarkii) and anthropogenic food. The most
important areas for wintering storks were
the Tejo, Sorraia and Sado valleys holding
approximately 65% of the surveyed storks,
followed by Baixo Mondego and Ria de
Aveiro (12%) and the Algarve (8%; Table
1). The recorded northward range expan-
sion of breeding birds (Encarnação 2015)
seems to also occur during the non-breed-
ing period: the proportion of storks win-
Table 1 - Number of wintering white storks (Ciconia ciconia) counted in each surveyed area in Portugal between 1995 and
2015 (Rosa et al. 2009 and this study).
Tabela 1 - Efectivos de Cegonha-branca (Ciconia ciconia) contados em cada área de invernada em Portugal entre 1995 e 2015
(Rosa et al. 2009 e presente estudo).
1995 1996 1997 1998 1999 2006 2008 2015
Ria Aveiro nc 14 30 1 nc 79 163 422
Baixo Mondego 22 28 40 53 109 377 763 1342
Vale do Tejo 2 7 100 219 405 308 545 3339
Vale do Sorraia 9 31 19 67 nc 610 1145 1317
Avis Landll x x x x x 245 628 0
Évora Landll x x x x x 135 900 571
Sado 272 520 433 1368 2813 4238 3717 4792
Beja Landll x x x x x 873 1100 550
Sotavento
Landll 95 150 124 340 750 0 0 0
Barlavento
Landll x x x x x 585 800 790
Ria Formosa 168 156 197 52 37 30 10 106
Castro Marim 522 266 550 176 45 13 8 13
Other sites 97 253 215 149 42 450 241 1192
TOTA L 1187 1425 1708 2425 4201 7943 10020 14434
(nc) not counted, (x) landll site not built at survey date

Changes on the migratory behaviour of the White Stork
32
Number of storks
1187 1425 1708
2425
4201
7943
10020
14434
15000
10000
5000
0
1995 1996 1997 1998 1999 2006 2008 2015
Proportion of resident storks
18.0
1994/1995 2004/2006 2014/2015
51.6
61.7
100
80
60
40
20
0
Figure 2 - Population trend of wintering white storks (Ciconia ciconia) in Portugal between 1995 and 2015 (Rosa et al. 2009
and this study).
Figura 2 - Evolução do efectivo populacional invernante de Cegonha-branca (Ciconia ciconia) em Portugal entre 1995 e
2015 (Rosa et al. 2009 e presente estudo).
Figure 3 - Evolution of the White stork (Ciconia ciconia) resident population in Portugal in the last two decades as estimated
by the ratio between the number of breeding and wintering individuals. Breeding and wintering population were assessed in
the breeding season of 1994, 2004 e 2014 (n= 3302, 7684 and 11691 breeding pairs, respectively; Encarnação 2015) and
during winter surveys in 1995, 2006 (Rosa et al. 2009) and 2015 (this study).
Figura 3 - Evolução da população residente de Cegonha-branca (Ciconia ciconia) em Portugal nas últimas duas décadas,
estimada como a proporção entre o número de indivíduos reprodutores e o número de indivíduos migradores. As
estimativas da população reprodutora e invernante referem-se aos censos nacionais realizados nas primaveras de 1994,
2004 e 2014 (n= 3302, 7684 e 11691 casais reprodutores, respectivamente; Encarnação 2015) e aos censos de inverno
realizados em 1995, 2006 (Rosa et al. 2009) e 2015 (presente estudo).

Changes on the migratory behaviour of the White Stork
33
tering north of the Tejo River increased
from approximately 2% in 1995 to 14%
in 2015. Besides the high increase in the
number of wintering storks in coastal areas
in the centre of the country (Baixo Mon-
dego and Ria de Aveiro), we should high-
light the high number recorded in the Cas-
telo Branco district, where 200 birds were
counted at the Fundão landll site (included
in “other sites”, Table 1). Overall, although
the long-term positive trend in the number
of breeding birds could partially explain the
observed increase in the wintering popula-
tion numbers, our results unveil a change in
the migratory behaviour of white storks, as
the proportion of resident individuals in the
population steeply increased from 18% in
1994/1995 to 62% in 2014/2015 (Figure 3).
Discussion
Bird migratory behaviour can be highly
exible. Migration is likely to be advan-
tageous whenever there is sufcient envi-
ronmental variation to benet individu-
als that move to exploit spatial variation
in resource availability or quality (Boyle
2008, Newton 2008). Changes to envi-
ronmental conditions can thus alter the
selection pressures operating on migratory
behaviour. If winter conditions improve,
species may alter their migratory strategy
and stay closer to their breeding areas. This
saves them the costs of migration in terms
of time, energy and mortality and ensures
the benets of early arrival to the breed-
ing grounds (Visser et al. 2009). Climate
change may thus not only result in strong
shifts of phenology but also in changes in
the primary migratory decision (to migrate
or not migrate). A recent study showed
that rising winter temperatures in the last
decades have promoted an overall increase
in climatic similarity between the Iberian
Peninsula overwintering areas and African
wintering grounds of six bird species with
recent established overwintering popula-
tions in Iberia, including the White stork
(Correia 2014). Additionally, year-round
food availability from anthropogenic
sources, including rubbish dumps and land-
ll sites (Gilbert et al. 2016), and the intro-
duction of the invasive red-swamp craysh
in the 1970s (Ramos & Pereira 1981) likely
enabled the establishment of overwintering
populations of white storks in Iberia. In
Spain, national winter census performed in
1995 and 2004 showed a large increase in
the number of wintering storks, from 7,594
to 31,229 individuals (Molina & Del Moral
2005). Comparison with surveys of breed-
ing numbers (1994 and 2004, Molina &
Del Moral 2005) suggest an increase in the
resident Spanish population from 23% to
47%, matching well the ndings recorded
for Portuguese resident storks in the same
period (18% and 52%, respectively).
The migratory status of the White
stork is changing substantially and in
the mid-term, if environmental con-
ditions continue to favour non-mi-
gratory individuals, the population is
likely to change towards full residency.
Acknowledgements
Thanks are due to all volunteers that
participated in the census. We thank the
landll sites for their interest in our proj-
ect and for kindly permitting us to count
storks on their premises: Aterros Sani-
tários do Fundão (RESISTRELA), Coim-
bra e Aveiro (CITVRSU), Avis (VALNOR),
Palmela e Seixal (AMARSUL), Évora
(GESAMB), Vila Ruiva (AMCAL), Ermi-
das do Sado (AMBILITAL), Beja (RESI-
ALENTEJO), Barlavento e Sotavento
(ALGAR). IC (SFRH/BPD/102637/2014)
and LPS (SFRH/BD/77746/2011) bene-
ciated from post-doctoral and doctoral
grant from Fundação para a Ciência e
Tecnologia, respectively. We thank Rui
Lourenço and one anonymous referee
for helpful comments on the manuscript.

Changes on the migratory behaviour of the White Stork
34
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