UNIVERSIDADE DE LISBOA
FACULDADE DE CIÊNCIAS
DEPARTAMENTO DE BIOLOGIA ANIMAL
WINTERING AND MIGRATING POPULATIONS OF DUNLIN
CALIDRIS ALPINA USING THE TAGUS ESTUARY:
FORAGING ECOLOGY, BEHAVIOUR AND DISTRIBUTION
RICARDO JORGE PAIS DA COSTA LEAL MARTINS
DOUTORAMENTO EM BIOLOGIA
(ECOLOGIA)
2015
UNIVERSIDADE DE LISBOA
FACULDADE DE CIÊNCIAS
DEPARTAMENTO DE BIOLOGIA ANIMAL
WINTERING AND MIGRATING POPULATIONS OF DUNLIN
CALIDRIS ALPINA USING THE TAGUS ESTUARY:
FORAGING ECOLOGY, BEHAVIOUR AND DISTRIBUTION
RICARDO JORGE PAIS DA COSTA LEAL MARTINS
TESE ORIENTADA PELO PROFESSOR DOUTOR JORGE MANUEL MESTRE MARQUES
PALMEIRIM E PELO DOUTOR JOSÉ PEDRO OLIVEIRA GRANADEIRO, ESPECIALMENTE
ELABORADA PARA A OBTENÇÃO DO GRAU DE DOUTOR EM BIOLOGIA (ECOLOGIA)
2015
Notas prévias
A presente tese inclui artigos científicos já publicados ou submetidos para publicação
(capítulos 2 a 5). Uma vez que estes trabalhos foram realizados em colaboração, de acordo
com o previsto no nº 1 do artigo 45º do Regulamento de Estudos Pós-Graduados da
Universidade de Lisboa, publicado no Diário da República, 2ª série, nº 65, de 30 de março de
2012, o candidato esclarece que participou integralmente na conceção dos trabalhos,
obtenção dos dados, análise e discussão dos resultados, bem como na redação dos
manuscritos.
Este estudo foi financiado pela Fundação para a Ciência e a Tecnologia (FCT), através de
uma Bolsa de Doutoramento (SFRH/BD/44871/2008) e dos projetos de investigação
“MigraTagis – Aves limícolas invernantes e migradoras como indicadores da qualidade de
ambientes estuarinos (PTDC/MAR/66319/2006)” e “Elos invisíveis – desvendando a origem de
aves limícolas migradoras através de marcadores biogeoquímicos (PTDC/MAR/119920/2010)”.
À Ana
Ao Miguel e à Catarina
“In my hand I held the most remarkable of all living things, a creature
of astounding abilities that elude our understanding of extraordinary,
even bizarre senses, of stamina and endurance far surpassing anything
else in the animal world. (…) I held that truly awesome enigma, a bird.”
A. C. Fisher 1979
(in Gill, F. 2007. Ornithology 3rd
Ed. WH Freeman and Company, New York.)
Table of Contents
Agradecimentos .......................................................................................................................... 13
Abstract ....................................................................................................................................... 17
Resumo ........................................................................................................................................ 19
CHAPTER 1. General Introduction ................................................................................................. 29
1.1. Waders: long-distance travellers ..................................................................................... 31
1.2. Estuarine environments as habitats for waders during the non-breeding season .......... 34
1.3. Wintering versus migrating birds: different ecological contexts ..................................... 37
1.4. Threats to wader populations in non-breeding areas and conservation concerns ......... 39
1.5. Tagus estuary: characterization and relevance for waders ............................................. 40
1.6. Dunlin: the model-species ................................................................................................ 43
1.7. Thesis main aims and outline ........................................................................................... 45
CHAPTER 2. Seasonal variations in the diet and foraging behaviour of dunlins Calidris alpina in a
South European estuary: improved feeding conditions for northward migrants ............ 47
2.1. Abstract ............................................................................................................................ 49
2.2. Introduction ..................................................................................................................... 49
2.3. Methods ........................................................................................................................... 51
2.4. Results .............................................................................................................................. 57
2.5. Discussion ......................................................................................................................... 61
CHAPTER 3. Contrasting estuary-scale distribution of wintering and migrating waders: the
potential role of fear ......................................................................................................... 65
3.1. Abstract ............................................................................................................................ 67
3.2. Introduction ..................................................................................................................... 67
3.3. Materials and methods .................................................................................................... 69
3.4. Results .............................................................................................................................. 73
3.5. Discussion ......................................................................................................................... 77
3.6. Conclusions ...................................................................................................................... 81
CHAPTER 4. Discriminating geographic origins of migratory waders at stopover sites: insights
from stable isotope analysis of toenails ........................................................................... 83
4.1. Abstract ............................................................................................................................ 85
4.2. Introduction ..................................................................................................................... 85
4.3. Materials and methods .................................................................................................... 87
4.4. Results .............................................................................................................................. 89
4.5. Discussion ......................................................................................................................... 92
CHAPTER 5. Crossbow-netting: a new method for capturing shorebirds ..................................... 95
5.1. Abstract ............................................................................................................................ 97
5.2. Introduction ..................................................................................................................... 97
5.3. Methods ........................................................................................................................... 98
5.4. Results ............................................................................................................................ 102
5.5. Discussion ....................................................................................................................... 103
CHAPTER 6. General Discussion................................................................................................... 105
6.1. Wintering and migrating dunlin populations using the Tagus estuary .......................... 107
6.2. New methodological approaches for wader research ................................................... 110
6.3. Major conservation implications .................................................................................... 111
6.4. Indications for future research....................................................................................... 113
References ................................................................................................................................. 115
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Agradecimentos
São muitas as pessoas e instituições que contribuíram de alguma forma para esta tese,
pelo que aqui deixo um sincero agradecimento a todas elas.
Aos meus orientadores, Professor Doutor Jorge Palmeirim e Doutor José Pedro
Granadeiro, por terem aceitado a orientação deste trabalho e por toda a experiência,
conhecimento e apoio disponibilizados aos longo destes anos, sem os quais nunca teria sido
possível vencer este desafio. Ao Zé Pedro, pelo acompanhamento ativo e interessado em todas
as fases, desde o planeamento à escrita, passando pela análise estatística e algumas tarefas de
campo, e também pela constante energia positiva e boa disposição, que muito ajudaram. Ao
Prof. Palmeirim pelo apoio mais prático que também disponibilizou em vários momentos, mas
também pela grande acessibilidade, que muito facilitou a discussão frutuosa dos trabalhos.
Ao Centro de Ecologia Evolução e Alterações Ambientais (cE3c) e ao Museu Nacional de
História Natural e da Ciência (MUHNAC), como instituições de acolhimento, por terem
aceitado integrar este projeto no âmbito das suas atividades de investigação.
À Teresa Catry, por ter desempenhado um verdadeiro papel de co-orientação (não-
formal) desta tese, pela dinâmica, disponibilidade e determinação sempre patentes na
participação, colaboração ou mesmo liderança da equipa de investigação e também pelo
companheirismo, simpatia e troca de ideias sobre os mistérios das limícolas do Tejo ao longo
de muitas horas de campo.
Aos muitos voluntários que ajudaram nas inúmeras tarefas de campo, grande parte
delas bem exigentes, potencialmente aborrecidas e em terreno muito difícil, por exemplo a
recolha de amostras de sedimento e crivagem da lama, capturas de aves, incluindo durante a
noite e a montagem e desmontagem de antenas de telemetria: Maria Dias, Miguel Lecoq, Ana
Almeida, Hany Alonso, Inês Catry, Rui Rebelo, David Rodrigues, Luís Rosa, Cristina Maldonado,
David Santos, José Alves, João P. Pio, Elena Garcia, Ana Leal, Pedro Andrade, João Moura,
Raquel Martins e Nuno Alves. A todos eles muito obrigado pela fantástica contribuição! A
special thanks is acknowledged to Hilger Lemke for its enthusiastic help during a full month of
fieldwork in the Tagus estuary.
À Sara Pardal, Marta Ferreira, Ioana Posa e Cristina Maldonado pela preciosa ajuda no
laboratório, nas triagens e identificação de invertebrados.
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Ao David Santos, pelo grande apoio inicial com os truques para filmar os pilritos em
alimentação, pelo companheirismo e também pela partilha de ideias sobre as limícolas e sobre
o estuário.
À Maria Dias, umas das pessoas com quem comecei no mundo das limícolas, ainda no
estágio de licenciatura, pela disponibilidade em ajudar regularmente em diversas atividades de
campo, algumas bem chatas, mas sobretudo pela grande amizade desde aqueles tempos.
Ao Miguel Lecoq, pela importante ajuda nas capturas de limícolas, em especial nos
desafios do “método da besta” e experiência transmitida, por exemplo na anilhagem, mas
muito pelo que contribuiu desde há muito para o meu fascínio pelas aves, incluindo limícolas,
com o seu enorme entusiasmo e conhecimento nesta área.
A toda a equipa do MigraTagis, liderada pelo José Pedro (e com um papel muito
relevante da Teresa), incluindo mestrandos, bolseiros e outros colaboradores, nomeadamente
David Rodrigues, Luís Rosa, José Alves, Sara Pardal, Maria Dias, David Santos, Rui Rebelo e
Filipa Peste, que, em conjunto com os inúmeros voluntários acima referidos, constituíram uma
extraordinária força humana, indispensável para corresponder às enormes ambições do
projeto. Foi um privilégio fazer parte desta equipa de espírito dinâmico e contribuir
ativamente para colocar ainda mais altos os limites do que já foi alguma vez feito na
investigação das limícolas no estuário do Tejo.
À Ana Rainho, pela ajuda preciosa e paciência em desenterrar do baú as instruções e
fotografias que permitiram a construção de antenas de telemetria direcionais, bem como na
ajuda nos testes dos emissores em pintos.
À Susana Rosa, que tendo terminado o doutoramento no tema das limícolas no estuário
do Tejo pouco antes de eu começar este projeto, em conjunto com as teses do David e da
Maria constituíram uma espécie de modelos nesta área, sem dúvida importantes para me
guiar em vários aspetos.
À Reserva Natural do Estuário do Tejo, por ter facilitado as suas instalações nas Hortas
para acondicionamento de material, como suporte para crivagens de sedimento e também
pela autorização de instalação temporária de uma antena de telemetria no topo da torre de
observação.
Ao CEMPA/ICNF pelas credenciais relativas à captura de limícolas e autorizações para
recolha de amostras biológicas e colocação de emissores nos pilritos.
15
À Fundação Gonçalves Júnior, pela autorização para realização de trabalhos na salina do
Brito, nomeadamente capturas de aves e colocação de uma estação automática de telemetria
e em especial ao Sr. Manel (e companheiros), pelas facilidades logísticas no acesso ao local.
À Fundação das Salinas do Samouco pela permissão de acesso e recolha de dados na
área e pela autorização para a instalação de duas antenas de telemetria.
Ao Sport Lisboa e Benfica, pela autorização para colocação de uma estação automática
de telemetria no centro de estágios do Seixal, junto a um refúgio de preia-mar para limícolas.
Ao Sr. Joaquim José (Monte de Pancas), ao Sr. Eduardo (Monte de Bate Orelhas) e ao Sr.
Almiro de Sousa (Salinas de Vasa Sacos) pela facilidade de acesso às zonas de Pancas e Vasa
Sacos, bem como permissão para colocação de antenas de telemetria.
To the Royal Netherlands Institute for Sea Research and to Dr. Theunis Piersma, for
loaning ten Automatic Radio-Telemetry Stations for MigraTagis project and to the Dutch
colleagues that facilitated all the logistics and provided support, namely Jos Hooijmeijer and
Bernard Spaans. Although the data collected using this material has not been directly used in
the papers included in this thesis, it contributed to the general knowledge of the ecology of
dunlins in the Tagus estuary.
To the Pete Potts’ team (Farlington Ringing Group) for some cannon-netting captures
directed to colour-ring dunlins in the Tagus estuary and its advice on the attachment of radio-
tags on birds.
To the ones that collected samples of nails from living dunlins for isotope analyses,
namely Jutta Leyrer and Theunis Piersma (Mauritania), Ricardo Lopes, Hamid Idrissi and Latifa
Joulami (Morocco) and also to Dr. Mark Adams and Dr. Robert Prys-Jones, curators from the
Natural History Museum of London, for kindly providing samples from UK museum specimens.
To Gary Ritchison, Chiyeung Choi and several anonymous referees for helpful comments
on the manuscripts accepted by scientific journals.
Ao Paulo Catry, pelos comentários e revisão a um dos artigos (capítulo 4).
Aos colegas da sala dos bolseiros (e outros vizinhos) do Museu, com quem pude
partilhar muitas das alegrias e dificuldades deste doutoramento, pelo companheirismo e
amizade, principalmente Miguel, Ana e Hany, Susana Pereira, Pedro Andrade, Bruno Pinto,
Paulo Marques, Pedro Lourenço e Daniel Magalhães.
Aos colegas da sala “dos doutorandos terminais” (e outros relacionados) da Faculdade,
onde estive na parte final da elaboração desta tese, pela solidariedade e apoio moral nesta
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luta, nomeadamente Ana, Nuno e Tatá, Miguel, Inês, Sérgio, Sara, Mafalda, Fernando, William,
Ricardo R e Ricardo C.
A muitos dos meus amigos, David e Catarina, Sérgio e Sofia, Ana e Hany, Ricardo e
Teresa, Susana e Pedro, Maria D., Miguel L., Paulo e Inês, Joana C., Susana e Luís, Maria João e
Nuno, Joana A., Sílvia, Diana, Dulce, Lélia e Daniel, Joana O. e Dirceu, pela amizade e pelo
convívio mais ou menos regular, sempre importantes para manter a sanidade mental.
Aos meus pais por todo o apoio ao longo da minha formação académica, e em particular
à minha mãe, pela disponibilidade constante em ajudar, em especial na fase pós-bolsa de
doutoramento.
Aos meus irmãos e aos meus sogros pelo acompanhamento interessado na elaboração
desta tese, principalmente nas etapas finais de escrita.
À minha querida Ana, pela contribuição concreta em muitos aspetos da tese, como a
ajuda no campo e a revisão de textos, mas principalmente por todo o apoio, amor e
compreensão ao longo destes anos, elementos que foram essenciais para enfrentar os
desafios do doutoramento. Obrigado também pelos dois produtos “extra-científicos” desta
tese, Miguel e Catarina, e pelas admiráveis capacidades de super-Mamã, mas também pelo
enorme privilégio de ser Pai e pelo que isso ajuda a calibrar a importância relativa das coisas
da vida!
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Abstract
Waders typically perform long-distance migrations between breeding and wintering
areas, depending on a network of stopover sites to refuel along their flyway. Most wetlands
act both as wintering and stopover areas for different wader populations and their distinct
ecological constrains might lead them to different patterns of resource use, which is important
information to plan conservation.
The main aim of this thesis was to investigate the foraging ecology, behaviour and
distribution of wintering and northward migrating dunlins Calidris alpina in the Tagus estuary,
Portugal. These populations contrasted in diet, foraging behaviour and distribution.
Differences in diet and foraging behaviour were explained by marked seasonal variations in
prey availability. The improved feeding conditions for migrants presumably enabled high
fattening rates, which highlight the good quality of the foraging habitats of the Tagus estuary
for waders in stopover. In terms of distribution, unlike wintering dunlins, migrants avoided the
areas of the estuary with higher perceived (but not real) risk of predation, despite their higher
abundance of invertebrates. The distinct ecological constrains of these populations (e.g. in
time and knowledge of the estuary) likely explains this pattern, as migrants are especially
conservative in terms of predation risk when selecting foraging areas.
In this thesis, the temporal overlap of wintering and migrating dunlins using the estuary
in late winter/spring was investigated. This was done by determining departure dates of
wintering birds, with radio-tracking, and through the innovative analysis of stable isotopes
from toenails to unveil the wintering origins of birds using the estuary in migratory periods.
This method confirmed the Banc d’Arguin, Mauritania, as the prime wintering area of birds
that stopover at the Tagus estuary. To assist these studies, a new method to capture
shorebirds was developed, where a crossbow is used to pull a mist-net over flocks of roosting
birds.
Keywords: Waders; Migration; Stopover ecology; Foraging behaviour; Predation risk; Stable
isotopes; Capture techniques.
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Resumo
Capítulo 1. Introdução Geral
As limícolas são um grupo de aves muito diverso, com mais de 200 espécies
amplamente distribuídas por todo o mundo. A grande maioria destas espécies são migradoras
de longa distância, realizando movimentos regulares entre as áreas de reprodução, sobretudo
na tundra ártica e regiões sub-árticas, e as áreas de invernada, principalmente em estuários e
outros habitats costeiros de zonas temperadas e tropicais de ambos os hemisférios. As
limícolas migradoras têm diversas adaptações morfológicas e fisiológicas que lhes permitem
fazer voos de longa distância, por vezes de milhares de quilómetros sem parar. No entanto, a
maioria das espécies necessita de efetuar paragens para restabelecimento energético
(stopover) nos movimentos entre áreas de reprodução e de invernada, pelo que dependem da
existência de locais com habitat adequado ao longo da sua rota migratória.
Durante o período não-reprodutor (durante o inverno e períodos migratórios, de
primavera e de outono), as limícolas alimentam-se tipicamente nas zonas intertidais, durante a
baixa-mar, onde consomem invertebrados bentónicos, sobretudo bivalves, gastrópodes,
poliquetas e crustáceos. Durante a preia-mar, tendem a concentrar-se, por vezes formando
bandos de milhares de indivíduos, em locais de refúgios, onde podem descansar.
Ao longo do gradiente de latitudes que atravessam nas suas rotas migratórias, as
limícolas utilizam zonas intertidais com diferente composição e disponibilidade de presas. Para
além disso, em zonas temperadas, a abundância e biomassa de invertebrados bentónicos pode
variar sazonalmente, de forma acentuada, sendo a disponibilidade de alimento para as aves
normalmente maior na primavera ou verão. Assim, as limícolas tendem a mostrar alguma
flexibilidade na sua dieta e comportamento alimentar, respondendo tanto a variações
geográficas (ao longo da rota migratória) como a variações temporais da composição e
disponibilidade de presas, e como tal, aves que usam a mesma área em diferentes períodos do
ano podem apresentar diferenças importantes na sua dieta e comportamento alimentar.
A disponibilidade de presas (e fatores relacionados, como o tipo de sedimento) tem sido
identificada como um dos fatores mais determinantes da distribuição de aves limícolas em
áreas estuarinas. No entanto, o risco de predação (maioritariamente por aves de rapina) é
também reconhecido como um fator importante na seleção de áreas de alimentação por parte
das limícolas. Desta forma, a configuração do habitat envolvente é frequentemente usada
como um indicador de perigo, nomeadamente a distância à linha de costa, onde a vegetação e
20
outras estruturas podem ser usadas como obstáculos visuais, facilitando ataques-surpresa por
predadores aéreos, especialmente falcões.
Muitas zonas húmidas costeiras de regiões temperadas e subtropicais das rotas
migratórias funcionam como áreas de invernada e também de stopover para diferentes
populações de limícolas, pelo que aves invernantes e migradores de passagem
frequentemente co-ocorrem nesses locais entre o inverno e os períodos de migração. Tanto
para uma efetiva conservação das aves limícolas como para o estudo da sua ecologia, é
essencial a identificação de diferentes populações que utilizam em simultâneo determinada
zona húmida, bem como conhecer os diferentes locais usados por cada população. No
entanto, pode ser muito difícil distinguir morfologicamente diferentes populações da mesma
espécie, mesmo quando estas pertencem a diferentes subespécies. Uma forma de alcançar tal
distinção é através da determinação das datas de partida e chegada de diferentes populações
numa área de invernada/stopover. O radio-seguimento é uma das técnicas que permite obter
esse tipo de dados, tendo sido utilizada nesta tese para determinar as datas de partida dos
pilritos-de-barriga-preta invernantes no estuário do Tejo (Capítulo 3). Uma outra técnica que
tem sido crescentemente usada para estudar a origem geográfica de alimentação de aves
migradoras é a análise de isótopos estáveis (principalmente de carbono e azoto). Os tecidos
mais frequentemente usados para esse efeito são as penas e o sangue, mas ambos
apresentam limitações para uma grande parte das limícolas migradoras. As unhas das aves
apresentam um crescimento estável e incorporam informação da dieta da ordem das semanas
a poucos meses anteriores à amostragem. Assim, a análise dos isótopos estáveis de unhas de
limícolas em passagem migratória pré-nupcial, num local de stopover, tem potencial para
revelar a sua área de invernada, podendo por isso ser utilizada para diferenciar migradores de
passagem das invernantes desses mesmos locais (Capítulo 4).
Durante a migração, as limícolas em stopover apresentam elevados requisitos
energéticos, uma vez que necessitam de acumular rapidamente reservas para os voos
migratórios, o que contrasta com a situação verificada em pleno inverno em que as
necessidades envolvem essencialmente os custos de termorregulação e procura de alimento.
Para além disso, as variações sazonais na abundância de invertebrados resultam
habitualmente em melhores condições alimentares para limícolas nos períodos migratórios,
relativamente ao inverno. Assim, estes fatores podem promover diferentes formas de explorar
os recursos alimentares por parte de limícolas invernantes e migradoras de passagem
(Capítulo 2).
A abundância de alimento e a segurança relativamente a ataques de predadores são
dois fatores conhecidos como determinantes na distribuição das limícolas. No entanto, o peso
21
relativo desses fatores é dependente da situação em que as aves se encontram, como a idade
e a experiência em determinada área ou a capacidade (física) de fuga a predadores aéreos.
Desta forma, estes fatores podem promover diferenças nos padrões de distribuição à escala
estuarina entre populações de limícolas invernantes e migradoras de passagem na sua
utilização de uma mesma zona húmida (Capítulo 3).
O estuário do Tejo é a zona húmida de maior importância de Portugal para aves
aquáticas e um dos maiores estuários da Europa Ocidental. A zona intertidal tem quase 100
km2 e é circundada sobretudo por praias e sapais, sendo os habitats terrestres em redor
dominados por zonas agrícolas e área urbana. Na preia-mar as aves limícolas no estuário do
Tejo utilizam sobretudo sapais e antigos complexos de salinas como sítios de refúgio. Nestes
locais a concentração de aves funciona frequentemente como atrativo para aves de rapina que
podem predar limícolas, como o Falcão-peregrino Falco peregrinus, a Águia-calçada Hieraaetus
pennatus ou a Águia-sapeira Circus aeruginosus.
O estuário do Tejo é considerado um local de importância internacional para aves
limícolas que utilizam a Rota Migratória do Atlântico Este, quer como área de invernada quer
como local de stopover, durante os períodos migratórios, sendo as espécies mais abundantes o
Pilrito-de-barriga-preta Calidris alpina, o Milherango Limosa limosa e a Tarambola-cinzenta
Pluvialis squatarola. Parte da área do estuário está classificada como Zona de Proteção
Especial, dentro da qual se inclui também uma área de Reserva Natural.
O Pilrito-de-barriga-preta é uma limícola de pequena dimensão que apresenta uma
ampla distribuição mundial. Está entre as espécies mais abundantes da Rota Migratória do
Atlântico Este, mas também no estuário do Tejo, que alberga uma população invernante de
cerca de 10 000 indivíduos, sobretudo reprodutores da Escandinávia e Rússia (subespécie C. a.
alpina). Nos picos de migração pré- e pós-nupcial contam no estuário do Tejo em média cerca
de 12 000 e 6000 pilritos, respetivamente, pertencendo a maioria destes sobretudo à
população nidificante na Islândia (subespécie C. a. schinzii) e que inverna na África Ocidental,
nomeadamente na Mauritânia. O Pilrito-de-barriga-preta foi escolhido como espécie-modelo
para este estudo porque (1) partilha com muitas outras espécies de limícolas tanto presas
como predadores, (2) é bastante abundante no estuário, o que facilita a recolha de dados e (3)
é mais fácil de capturar que outras espécies maiores e mais sensíveis à presença humana (mas
ver Capítulo 5).
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Capítulo 2. Variações sazonais na dieta e comportamento alimentar do Pilrito-de-barriga-
preta Calidris alpina num estuário Sul Europeu: melhores condições alimentares para
migradores de passagem pré-nupcial
O principal objetivo deste estudo foi examinar as diferenças no comportamento
alimentar e dieta de pilritos-de-barriga-preta invernantes e em passagem migratória no
estuário do Tejo e investigar em que medida esses padrões são influenciados pela abundância
e disponibilidade de presas. Este trabalho incluiu a gravação de vídeos de aves em
alimentação, a análise de dejetos e a amostragem de invertebrados-presa para análise da sua
abundância, biomassa e disponibilidade para as aves à superfície do sedimento. Foram
calculadas as taxas de consumo energético obtidas pelas aves em cada estação e interpretadas
à luz dos seus requisitos energéticos, de forma a compreender a significância do típico
aumento primaveril na disponibilidade alimentar para os pilritos em passagem migratória.
Os pilritos-de-barriga-preta invernantes e em passagem migratória pré-nupcial
apesentaram diferenças marcadas no comportamento alimentar e dieta. No inverno, os
pilritos adotaram sobretudo técnicas de procura de alimento táteis (bicadas profundas no
sedimento), principalmente para ingerir pequenos bivalves inteiros, alternando com técnicas
visuais (bicadas superficiais) para capturar gastrópodes e sifões de bivalves, ambos disponíveis
à superfície do sedimento. Em contraste, as aves em passagem migratória usaram geralmente
técnicas visuais de procura de presas, principalmente para consumir poliquetas (anelídeos),
mas também sifões de bivalves e pequenos camarões. Do inverno para a primavera, verificou-
se um forte aumento tanto na biomassa das presas no sedimento como na disponibilidade de
sifões e poliquetas à superfície do sedimento. A combinação destes dois fatores, juntamente
com o aparecimento de pequenos camarões, na primavera, explicam muito provavelmente as
diferenças observadas no comportamento alimentar e na dieta dos pilritos. Tirando partido
deste aumento sazonal na disponibilidade de presas, os migradores de passagem obtiveram
taxas de consumo energético 65% mais elevadas do que as aves invernantes. Tendo em
consideração os requisitos energéticos diários conhecidos para esta espécie, estima-se que os
pilritos em stopover consigam obter elevadas taxas de acumulação de gordura (fundamental
para os voos migratórios), o que indica que o estuário do Tejo fornece ótimas condições de
alimentação para aves limícolas em passagem. Assim, este estudo reforça a importância desta
zona húmida como local de stopover para aves limícolas no contexto da Rota de Migração do
Atlântico Este.
23
Capítulo 3. Diferenças na distribuição à escala estuarina de limícolas invernantes e em
passagem migratória: o potencial efeito do medo de predação
Neste estudo foram reanalisados dados previamente publicados sobre o número de
limícolas em refúgios de preia-mar para avaliar as variações sazonais na distribuição do Pilrito-
de-barriga-preta por dois grandes sectores do estuário do Tejo (norte e sul, considerando a
latitude do Montijo como divisória) que apresentam diferenças marcadas na forma e
dimensão das áreas intertidais. Para uma correta interpretação das referidas variações
sazonais de distribuição das aves, pretendeu-se clarificar a sobreposição temporal que se sabe
existir na utilização do estuário pelas populações de invernantes e de migradores de passagem
pré-nupcial. Para tal, recorreu-se à radio-seguimento para determinar as datas de partida da
população invernante do estuário e posterior análise desta informação em relação às
variações na abundância das aves em pleno período migratório. De forma a compreender os
padrões de distribuição dos pilritos invernantes e em migração, foram efetuadas análises
comparativas dos sectores norte e sul do estuário em termos de disponibilidade de alimento e
também de indicadores da pressão de predação, comportamento das limícolas e perceção do
risco de predação.
A análise de dados publicados, de contagem de limícolas em refúgios, salientou as
diferenças claras na distribuição do Pilrito-de-barriga-preta à escala estuarina: enquanto que
no inverno as aves mostraram uma preferência pelo sector sul do estuário, em ambos os
períodos migratórios os pilritos concentram-se quase exclusivamente no sector norte. No
sector sul do estuário a disponibilidade de invertebrados foi significativamente maior do que
no sector norte, em ambas as estações. Por outro lado, as áreas de alimentação do sector sul
inserem-se em braços do estuário relativamente fechados, comparativamente com a extensa e
contínua zona intertidal do sector norte, pelo que estas últimas tendem em geral a ser
percecionadas pelas limícolas como sendo mais seguras relativamente à presença de
predadores aéreos, devido a um menor efeito de orla. No entanto, os indicadores de pressão
de predação indicaram que a zona sul não acarreta maior risco real que a zona norte (os dados
sugerem mesmo a tendência contrária).
Assim, os resultados deste estudo sugerem que os pilritos em passagem migratória
evitaram a zona sul do estuário do Tejo devido ao seu risco aparente (e não real) de predação,
tendo com isso desaproveitado as áreas com mais alimento, o que contrastou com o
observado nas aves invernantes. Presumivelmente, as aves invernantes têm um melhor
conhecimento do estuário, incluindo os seus riscos reais de predação, o que lhes permite
aproveitar as melhores oportunidades alimentares. As aves em migração, por utilizarem as
24
suas áreas de stopover durante períodos de tempo relativamente curtos, devem ter um
conhecimento mais limitado desses locais, tendendo a selecionar as suas áreas de alimentação
sobretudo com base em indicadores indiretos do risco de predação, tais como a distância à
linha de costa, onde a vegetação ou outro tipo de estruturas podem funcionar como ataques
surpresa por parte de predadores aéreos. Este estudo ilustra como o risco de predação pode
afetar a distribuição das aves limícolas à escala estuarina, mas também como esse tipo de
efeito é “dependente de estado”, uma vez que diferentes populações da mesma espécie
(invernante versus migradora de passagem), sujeitas a distintos contextos ecológicos,
responderam de modo diferente relativamente a este fator.
Capítulo 4. Discriminação da origem geográfica de aves limícolas migratórias em locais de
stopover a partir da análise de isótopos estáveis de unhas
Este estudo pretendeu testar o potencial da análise de isótopos estáveis de unhas para
revelar a origem geográfica de invernada de pilritos-de-barriga-preta em áreas que funcionam
simultaneamente como de invernada e de paragem migratória. Esta informação foi
posteriormente utilizada para desvendar os calendários migratórios das populações invernante
e migradora de passagem pré-nupcial que se misturam no estuário do Tejo no fim do inverno /
primavera. Para tal, primeiro determinaram-se as assinaturas isotópicas de carbono (δ13C) e
azoto (δ15N) estáveis de unhas de pilritos a invernar em diferentes locais referência ao longo
da Rota Migratória do Atlântico Este: Mauritânia, Marrocos, Portugal e Reino Unido.
Subsequentemente, foram determinados os locais de invernada dos pilritos amostrados na
primavera (i.e., no período de migração) no estuário do Tejo com base nos respetivos valores
de isótopos estáveis.
As unhas de pilritos de diferentes áreas de invernada apresentaram valores de δ13C e
δ15N significativamente diferentes, apesar de ter havido alguma sobreposição nas assinaturas
isotópicas de carbono entre as aves de Marrocos, Portugal e Reino Unido. Nos pilritos
amostrados durante a migração pré-nupcial no estuário do Tejo, verificou-se um padrão bi-
modal nos valores de carbono, o que permitiu uma distinção entre os migradores de passagem
vindos da Mauritânia (valores mais altos de δ13C) e as aves invernantes no estuário do Tejo
(valores mais baixos de δ13C). Os primeiros migradores vindos da Mauritânia foram detetados
no estuário do Tejo no fim de março, mas os picos de passagem ocorreram na segunda metade
de abril e início de maio.
Este estudo comprovou que as assinaturas isotópicas de unhas podem desempenhar um
papel importante na determinação das origens de inverno de pilritos-de-barriga-preta em
25
passagem migratória, nos seus locais de stopover. Assim, as unhas, em vez de penas, podem
ser o tipo de tecido mais recomendável para se amostrar em estudos com aves limícolas,
permitindo colmatar a falhas de conhecimento sobre a conectividade migratória entre áreas
usadas em diferentes fases do ciclo de vida das limícolas.
Capítulo 5. Crossbow-netting: um novo método de captura de aves limícolas
Alguns dos métodos utilizados nesta tese, tais como a radio-seguimento ou a análise de
amostras de tecido, requerem a captura dos indivíduos. No entanto, capturar limícolas em
período não-reprodutor pode ser bastante difícil uma vez que estas aves se dispersam muito
nas áreas de alimentação e são bastante sensíveis à perturbação humana quando se
concentram nos locais de refúgio. Existem atualmente vários métodos disponíveis para
capturar limícolas, todos apresentando vantagens e desvantagens. No âmbito da investigação
desenvolvida no estuário do Tejo era necessário capturar pilritos-de-barriga-preta de forma
regular mas nenhum dos métodos era perfeitamente adequado às condições específicas das
áreas de estudo.
Assim, foi desenvolvido um novo método de captura de limícolas (e outras aves
costeiras), que consiste na utilização de uma besta como método de propulsão de uma seta
modificada (mais pesada) de forma a puxar uma rede por cima de bandos de aves em
descanso. Esta técnica foi testada em quatro tipos de habitat (salinas, sapais, praias e zonas
intertidais de lama) no estuário do Tejo, tendo-se capturado, no total, 300 pilritos-de-barriga-
preta e mais 84 aves de outras sete espécies de limícolas.
As principais vantagens e desvantagens desta técnica, relativamente a outros métodos
já existentes (e.g. redes-japonesas, clap-nets, whoosh-nets e redes-canhão), incluem: (1)
elevada portabilidade, (2) facilidade de montagem, (3) perturbação mínima junto da área de
captura e (4) a não utilização de materiais explosivos. Estes resultados mostram que a técnica
de captura crossbow-netting é um método seguro e útil, especialmente adequado para
estudos que requerem a captura de um número reduzido de indivíduos numa base regular.
Capítulo 6. Discussão Geral
A investigação realizada no âmbito desta tese, focando-se nas populações invernante e
de passagem migratória do Pilrito-de-barriga-preta no estuário do Tejo, contribuiu em geral
para o conhecimento da ecologia de aves limícolas migradoras e sua conservação. Para além
26
disso, foram desenvolvidas ou melhoradas algumas técnicas de estudo em ornitologia, com
utilidade para outros investigadores.
Através de dois métodos distintos (radio-seguimento e análise de isótopos estáveis de
unhas) foi clarificada a sobreposição temporal de pilritos-de-barriga-preta invernantes e
migradores de passagem na utilização deste estuário na primavera, tendo-se identificado o
período entre fim de março a fim de abril como aquele em que ambas as populações se
misturam no estuário. Para além disso, confirmou-se a Mauritânia como a principal área de
invernada dos pilritos que usam o Tejo como local de stopover.
O facto de o estuário do Tejo funcionar como área de invernada e também de stopover
constituiu uma oportunidade para se demonstrar que os padrões de utilização de recursos por
parte das aves limícolas, nomeadamente a dieta, comportamento alimentar e a distribuição à
escala estuarina, estão fortemente condicionados pelo contexto ecológico em que elas se
encontram, i.e., os seus constrangimentos energéticos, a disponibilidade alimentar em
diferentes períodos e o tempo que têm para explorar determinada zona húmida.
A população invernante de Pilrito-de-barriga-preta, ao utilizar o estuário numa fase em
que as oportunidades alimentares são menores (em relação à primavera), tendeu a
concentrar-se mais no sector sul do estuário do Tejo, que tem maior abundância de
invertebrados (em comparação com o sector norte). A aparência de maior risco de predação
por rapinas da zona sul do estuário (devido ao maior efeito de orla, associado ao formato mais
fechado das suas áreas de alimentação) não foi corroborada pela comparação dos indicadores
do risco real/pressão de predação nos dois sectores do estuário. Esse facto sugere que as aves
invernantes tenderam a fazer as escolhas aparentemente mais ajustadas relativamente às
condições ecológicas do estuário. Na migração pré-nupcial, os pilritos-de-barriga-preta em
stopover também mostraram ajustar-se bem às condições do estuário do Tejo no que respeita
à alimentação, tirando proveito em termos energéticos do aumento da disponibilidade de
invertebrados na primavera (relativamente ao inverno). No entanto, não se verificou um
ajustamento equivalente nos padrões de distribuição à escala estuarina, uma vez que as aves
em migração desaproveitaram as áreas intertidais com mais alimento para evitar o maior risco
aparente de predação associado a essas áreas. Este facto é ilustrativo da forma como as
limícolas em migração, provavelmente por possuírem um conhecimento mais limitado dos
locais de stopover, tendem a adotar medidas “automáticas” de minimização do risco de
predação, na seleção do habitat, que podem influenciar fortemente a sua distribuição.
Muitas espécies de limícolas, a nível global, têm sofrido declínios populacionais, devido
a vários tipos de ameaças, nomeadamente a degradação ou destruição de habitat e a
perturbação humana. Os dados recolhidos para esta tese contribuíram com informação útil
27
para a conservação de aves limícolas, através da formulação de recomendações acerca da
proteção e gestão dos seus habitats. No Capítulo 2 mostrou-se o importante papel ecológico
desempenhado pela comunidade de invertebrados nos ecossistemas estuarinos, bem como a
importância das variações sazonais na sua abundância para a adequada recuperação
energética das aves em passagem migratória nos locais de stopover. A degradação das
condições de alimentação em locais importantes de paragem migratória pode causar
alterações nas rotas migratórias de populações inteiras de limícolas, com potenciais
consequências negativas para o seu sucesso reprodutor. Nesse sentido é essencial garantir que
a boa-qualidade das áreas de alimentação para limícolas em locais de stopover, como se
verificou ser o caso do estuário do Tejo, não é afetada pela pressão das atividades humanas.
Da análise da distribuição do Pilrito-de-barriga-preta no estuário do Tejo (Capítulo 3)
resultaram duas preocupações principais relativamente à conservação desta espécie (e de
outras, que apresentam padrões semelhantes de distribuição). A primeira é o facto de uma
parte considerável (cerca de metade) da população invernante utilizar o sector sul do estuário,
ou seja, maioritariamente áreas não abrangidas por qualquer estatuto de proteção legal. A
segunda resulta da concentração de quase toda a população migradora de passagem no sector
norte do estuário. Embora este sector esteja totalmente abrangido pela Zona de Proteção
Especial (ZPE) do estuário do Tejo, aquela concentração faz com que uma esmagadora maioria
das migradoras de passagem no estuário dependam de apenas um ou dois refúgios de preia-
mar. A este facto, que acarreta, por si só, alguns riscos de conservação, acresce ainda a
pressão que se tem verificado nos últimos anos em antigos complexos de salinas, para
produção de camarinha nestes locais (mesmo dentro da ZPE), o que reduz drasticamente a sua
qualidade como refúgios de preia-mar para as aves. Assim, seria recomendável (1) estender os
limites da ZPE, para que esta inclua as principais áreas de alimentação e de refúgio de preia-
mar do sector sul do estuário, e (2) melhorar a proteção dos refúgios mais importantes do
estuário e implementar medidas efetivas de gestão para assegurar e/ou melhorar a sua
qualidade para limícolas. Tais medidas beneficiariam tanto as populações invernantes como as
migradoras de passagem nesta zona húmida de importância internacional para aves limícolas.
Palavras-chave: Pilrito-de-barriga-preta; Aves limícolas; Comportamento alimentar; Invernada;
Migração; Ecologia de stopover; Distribuição; Risco de predação; Estuário do Tejo; Isótopos
estáveis; Técnicas de captura.
29
CHAPTER
General Introduction
HAPTER 1
General Introduction
Chapter 1. General Introduction
31
1. General Introduction
1.1. Waders: long-distance travellers
Waders form a very diverse and widespread group of birds across the globe, with more
than 200 species, organized in 12 families included in the order Charadriiformes (Perrins 2003).
Four families – Charadriidae (plovers and lapwings), Scolopacidae (sandpipers, snipes,
phalaropes and allies), Recurvirostridae (avocets and stilts) and Haematopodidae
(oystercatchers) – include 86% of all species (Perrins 2003) and represent the typical wader,
i.e. the long-legged birds associated with wetlands and coastal environments. The term
“shorebirds” is also commonly used to refer to the group of waders, though it may include
birds from other families.
Most wader species are strongly migratory, performing long-distance movements
between their breeding areas, mainly in the Arctic tundra and subarctic regions, and their
wintering grounds, mainly estuarine and other coastal habitats of tropical and temperate
regions of both hemispheres (Delany et al. 2009). Breeding takes place during the short boreal
summer, mainly June-July in the Arctic but starting much earlier in lower latitudes. Southward
and northward migratory journeys to/from wintering areas occur in spring (mostly March-
May) and late summer-autumn (July-October), respectively. Many species of waders travel
more than 10 000 km each year between their nesting and wintering grounds. There are
several examples of longer migrations, the most extreme being described for a particular
population of the Bar-tailed Godwit Limosa lapponica baueri, that completes 29 000 km each
year (Gill et al. 2014). Some wader species perform non-stop flights for distances of 3000 km
or more (Battley et al. 2003; Hedenstrom 2010; Battley et al. 2012); the Bar-tailed Godwit flies
more than 11 000 km, crossing the Pacific Ocean from Alaska to New Zealand in just eight
days, the most extreme endurance flight known in birds (Gill et al. 2009).
Waders possess several morphological and physiological adaptations for long-distance
migratory flights. Their narrow and pointed wings (high aspect ratio) provide an efficient and
fast flight (usually 50-70 km/h), which is powered by large flight muscles and hearts (van de
Kam et al. 2004). The long flapping flights are fuelled by high loads of subcutaneous fat
(frequently up to 30% of the total body mass) accumulated before departing for migration
(Piersma and van Brederode 1990; Zwarts et al. 1990b). Other noticeable physiological
changes occur in internal organs. For instance, flight muscles increase in size during the
fattening period and especially before departure, whereas stomach, liver and intestines
Chapter 1. General Introduction
32
initially increase while fattening but then decrease just before departure, to reduce weight and
thus energy expenditure during migratory flights (Piersma and Gill 1998). These abdominal
organs can be quickly restored when birds stop to refuel (Piersma et al. 1999).
Although some species perform non-stop flights between breeding and wintering areas
(Gill et al. 2005), most waders use a network of stopover areas, i.e. wetlands (usually coastal
but also interior) where they stop for periods extending from few days to few weeks (e.g.
Warnock et al. 2004; Verkuil et al. 2010; Norling et al. 2012) to rest and refuel before resuming
migration (van de Kam et al. 2004). These are also commonly called staging areas, although
this term is more adequate to refer to the largest areas, where substantial proportions of a
whole population strategically stop to refuel, usually for longer periods than in less important
sites (Warnock 2010).
Different wader species and populations of a certain region of the globe tend to share,
at least partly, the same stopover and/or wintering areas, as well as the migration routes used
to link these areas to breeding grounds, which together are termed flyways (Boere and Stroud
2006). Despite the substantial overlap between the different global flyways (Figure 1.1; Boere
and Stroud 2006), this is a very useful concept for conservation, providing an integrative
perspective of different sites used by wader populations along the year cycle. The East Atlantic
Flyway is used by several millions of waders and is one of the best studied migration routes.
Birds using this flyway breed over a large range, from North Eastern Canada to Central Siberia
(Figure 1.1). Many populations spend the winter in estuaries and other coastal areas of the
Western Europe, while others use this region only to stopover during their migratory
movements to/from wintering sites in West Africa, some reaching South Africa (Delany et al.
2009). In the East Atlantic Flyway there are 44 key sites, spread over 16 countries from
Northern Europe to South Africa, holding internationally important numbers (>1% of a
population, according with Ramsar Convention) of at least five wader species (Delany et al.
2009). The Wadden Sea (extending from The Netherlands to Denmark) and the Banc d’Arguin
(Mauritania) are the two most important sites during the non-breeding season, with ca. 4 and
2.4 millions of waders, respectively (Hagemeijer et al. 2004; Blew and Sudbeck 2005).
Chapter 1. General Introduction
33
Figure 1.1. The eight most important flyways used by waders (adapted from Boere and Stroud 2006).
Waders can move between wintering and breeding areas using different strategies
(Figure 1.2; Piersma 1987). Some species, such as Red Knot Calidris canutus and Bar-tailed
Godwit, travel from Banc d´Arguin to Siberia, in spring, with just two long-distance flights and a
single but prolonged stop to refuel in the Wadden Sea (“jump” strategy). In contrast, other
species, such as Redshank Tringa totanus and Curlew Numenius arquata perform several
short-distance flights and stopover at many different sites along the route (“hop” strategy).
Dunlin Calidris alpina show an intermediate pattern of migration, taking medium-length
journeys at each time to reach their destiny (“skip” strategy). Given the importance of arriving
to breeding areas at the right time, i.e. not too early to avoid the freezing grounds and the lack
of invertebrate prey but early enough to ensure a breeding territory and a mate (Hotker 2002;
Gunnarsson et al. 2006) and in good body condition (Marra et al. 1998), these strategies during
the northward migration must take into account several other ecological factors. On one hand,
“jumpers” can complete migration quickly and take fewer risks associated with finding suitable
habitats to feed and rest safely in many different small stopover sites, as they usually rely on
very few (but predictable) staging areas (Warnock 2010). On the other hand “hoppers” have
the most energetically efficient migration (Piersma 1987), as they do not need to accumulate
and carry large fat loads to fuel the flight, which would implicate high abundances of food or a
long preparation for migration in wintering areas (Zwarts et al. 1990b).
Chapter 1. General Introduction
34
Figure 1.2. Main migratory strategies of waders travelling from their wintering grounds, in Western
Africa, to breeding areas, in Northern Europe (adapted from Piersma 1987).
Waders can spend the winter in a wide range of latitudes, thus experiencing very
different climatic and ecological conditions, such as air temperature and food availability
(Meltofte 1996). These conditions can affect bird survival at wintering grounds but also in
subsequent stages of the year-cycle (e.g. through low body condition), impacting for instance
migratory performance (Marra et al. 1998; Bearhop et al. 2004) and breeding success (Norris
et al. 2004; Alves et al. 2012a). Therefore, the decisions on where to spend the winter shown
by different populations are of great importance, as they can affect bird fitness (Alves et al.
2013), and involve also other aspects of the migratory strategy. For instance, waders wintering
in the Wadden Sea (53° N) face much harsher conditions than in the Banc d’Arguin (20° N),
which requires high energy use due to thermoregulatory costs and the accumulation of fat
reserves during winter (Meltofte 1996), given the possibility of temporary unavailability of
foraging areas due to snow or ice. On the other hand, for an arctic breeding wader, spending
the winter in North Western Europe requires much shorter migratory movements than
wintering in Western Africa; this involves not only less energy expenditure (and time) in
migratory flights (and associated risks) but also less time fattening before migration and/or
less dependence on intermediate stopover sites to refuel (Drent and Piersma 1990).
1.2. Estuarine environments as habitats for waders during the non-
breeding season
During the non-breeding season, i.e. winter and (autumn and spring) migratory periods,
many waders tend to congregate in estuarine areas, where they play an important ecological
role in local food webs (e.g. Moreira 1997). Waders typically forage in intertidal areas during
the low tide, where they capture benthic invertebrates, mostly bivalves, gastropods,
Hop Skip Jump
Chapter 1. General Introduction
35
polychaetes and crustaceans that live buried or at the surface of the sediment (BWPi 2006).
During high tide, when foraging areas are unavailable, waders concentrate in dense flocks in
roosting sites, i.e. supra-tidal areas which are mostly used to rest (Rogers 2003; Rosa et al.
2006), although foraging may also occur at some circumstances (e.g. Luis et al. 2002).
Most waders are extremely well adapted to forage in intertidal areas, with long legs to
walk in flooded grounds, and among species there are different sizes of feet (proportionally)
for a wide range of sediment types and a variety of bill forms to capture a large diversity of
invertebrate prey, using different foraging techniques. Plovers (Charadrius sp. and Pluvialis sp.)
have very large eyes and relatively short bills, typically using visual foraging strategies (sit and
wait technique) to capture mobile prey at the sediment surface (e.g. Barbosa 1995). Species
from the family Scolopacidae have long bills to penetrate deep in the sediment and flexible
tips of mandibles to adopt tactile foraging (e.g. Mouritsen and Jensen 1992), in some cases
with the help of high densities of sensors (Herbst corpuscles) on the bill tip, that allow the
remote detection of buried prey, mainly bivalves (e.g. Red Knot and other sandpipers; Piersma
et al. 1998; Nebel et al. 2005). Other waders have particular bill morphology, such as the
avocets Recurvirostra sp. which sweep the top layer of the wet mud to collect tens of tiny
polychaetes at once (Moreira 1995b; c) or the Western Sandpiper Calidris mauri, possessing
tongue adaptations to consume biofilm (Elner et al. 2005; Kuwae et al. 2008). These
evolutionary specializations in morphology and foraging methods contribute to reduce inter-
specific competition and allow waders to successfully explore a wide range of ecological niches
(van de Kam et al. 2004).
Across the latitudinal gradient of the migration route, waders have to find food in
intertidal sediments with different prey composition and environmental conditions (Piersma et
al. 1993a). Furthermore, in temperate regions prey abundance and biomass show strong
seasonal variations usually peaking during the warmer periods of the year (Zwarts et al. 1992;
Scheiffarth and Nehls 1997). Therefore waders generally show a considerable plasticity in
foraging behaviour and diet, responding both to geographical changes (along the flyway;
Beninger et al. 2011; MacDonald et al. 2012) and seasonal variations in the composition and
abundance of prey (Zwarts and Wanink 1989; Zwarts et al. 1992). Many scolopacids, such as
the Redshank or the Dunlin, although morphologically adapted for tactile foraging, are
particularly able to adjust their foraging behaviour in response to environmental changes. They
are able to switch between tactile and visual foraging modes to optimize intake rates
(Lourenço et al. 2008; Kuwae et al. 2010; Santos et al. 2010b; Dwyer et al. 2012).
In tidal flats only a fraction of the buried living invertebrates is available for waders,
depending on their bill length and burring depth of prey (Zwarts et al. 1992; Zwarts and
Chapter 1. General Introduction
36
Wanink 1993). Furthermore, the largest individuals may not be ingestible and the smallest may
not be profitable, i.e., are ignored if the rate of energy intake while handling this prey is below
the current overall average intake rate during feeding, according with the optimal foraging
theory (van de Kam et al. 2004). The fraction of prey that is not too small, not too large and
not too deep – the harvestable fraction – varies seasonally mainly due to changes in burry
depth (higher in winter) and activity at the sediment surface (lower in winter; Esselink and
Zwarts 1989; Zwarts and Wanink 1989). Such variations in availability, together with changes in
invertebrate abundance and/or biomass, can promote differences in the diet and foraging
behaviour of birds using the same estuarine area in distinct periods (e.g. Nehls and Tiedemann
1993).
The way waders are distributed in estuarine areas has been the focus of intensive
research and many environmental factors were identified as affecting habitat choice at
different spatial scales. Among factors acting at the medium to large (wetland) scale, the
availability of prey (and related features, such as the sediment type), have been traditionally
identified as drivers of bird distribution (e.g. Goss-Custard et al. 1977; Yates et al. 1993;
Granadeiro et al. 2007). Waders in general show a very dynamic use of space when foraging in
tidal flats (Granadeiro et al. 2006). Therefore, they are able to relatively quickly assess patch
quality, concentrating in higher densities or spending more time where their intake rates are
higher (van Gils et al. 2006). While assessing the quality of foraging areas, waders must also
weigh predation risk, particularly by raptors (Accipitriformes and Falconiformes; Cresswell
2008). Their gregarious behaviour, together with an accurate vision and good flight capacities,
can, to some extent, reduce the individual chance of being captured. This can be achieved
through an early detection of predators, by frequently scanning the sky when foraging or
resting (Barbosa 1995), or through coordinated flight manoeuvres when escaping from
predator attacks (Michaelsen and Byrkjedal 2002). However, waders also reduce the risk of
predation by selecting areas with specific habitat features (Cresswell 2008). For example, they
often prefer to forage in open areas, far from the shore, where vegetation or other structures
can be used by raptors as a cover to launch surprise attacks (Cresswell and Whitfield 1994;
Pomeroy et al. 2006). Therefore, distance to cover is known to affect the estuary-scale
distribution of waders, both in winter and migratory periods (e.g. Sprague et al. 2008;
Cresswell et al. 2010).
Chapter 1. General Introduction
37
1.3. Wintering versus migrating birds: different ecological contexts
Discriminating overlapping populations
Many coastal wetlands in intermediate latitudes of the migratory flyways act both as
wintering and stopover areas for different populations (Delany et al. 2009). Due to different
migratory schedules, wintering birds and passage migrants often occur in the same wetland at
the same time during the transitions between winter and migratory periods. Both for the study
of the ecology and for the effective conservation of waders it is essential to identify the
different populations using the most important wetlands, as well as to establish the link
between sites along their flyways. However, different populations of the same species may be
difficult to distinguish through plumage patterns and morphological measurements, even
when different subspecies are involved (Prater et al. 1977). Complementary methods can be
used to distinguish between wintering and migrating wader populations using the same area,
thus clarifying their migratory schedule. For example, individually marked birds with colour-
rings, can provide useful data clarifying departure/arrival rates of different groups of birds
from/to a certain wetland (Alves et al. 2013). However, this technique requires a huge effort
capturing and subsequently searching for marked birds. Genetic markers can also be used but
often lack power to discriminate between different populations of the same species (Lopes et
al. 2006). Radio-tracking with VHF transmitters has been used in wader research for decades
(e.g. Wood 1986; Iverson et al. 1996; Warnock 1996) and can also contribute to identify
migratory schedules of different populations (see Chapter 3) as it allow the detection of birds
in relatively large areas of open habitats. It can be used in small-sized species (Iverson et al.
1996), which are usually more difficult to follow with individual colour marks. Nonetheless, the
costs involved in radio-tracking, both in equipment and human resources, and the relatively
short duration of batteries (at least in small waders) usually restrict this technique to relatively
small sample sizes (e.g. Leyrer et al. 2006; Conklin et al. 2008).
Stable isotope analysis is a technique that relies on intrinsic signatures of animal tissues
and provides information on the provenance of feeding in a period prior to sampling, as long
as isotopic composition of their food varies with geographical area (Hobson 1999). Therefore,
stable isotope analysis (mainly carbon and nitrogen) has been increasingly used to track
movements of migratory birds across isotopic gradients (Atkinson et al. 2005). The most
frequently sampled tissues in birds are blood and feathers (Hobson 1999) but both present
limitations to unveil the geographic origin of wader populations. Blood incorporates an
isotopic signature that reflects a period before sampling that is too short for such purpose, and
Chapter 1. General Introduction
38
feathers provide geographical information of the moulting grounds, but those are often
unknown given the complex moulting cycles of these birds. Toenails of birds grow continuously
and integrate information on their diet from weeks to few months prior to sampling (Bearhop
et al. 2003). Therefore, this tissue has great potential to reveal the wintering origin of
migratory birds (Clark et al. 2006; Yohannes et al. 2010) and thus to clarify the temporal
overlap between wintering and migrating wader populations of a single species using the same
estuarine area. This issue is investigated on Chapter 4.
Ecological contexts of different populations and expected effects on resource use
During migratory periods and particularly during stopovers, waders have to quickly build
up their fat reserves to resume migration, whereas during winter they strive to ensure
thermoregulation and avoid the risk of starvation (van de Kam et al. 2004). These different
energetic requirements of wintering and migrating birds may lead to distinct ways of exploiting
food resources in the same wetland, such as diet preferences and foraging behaviour.
Moreover, temporal variations in availability of invertebrate prey may result in increased
foraging opportunities for waders during migratory periods in relation to winter (Zwarts and
Wanink 1993). Therefore, studying the foraging ecology of wintering and migrating waders
under distinct requirements and constraints can contribute for the understanding of the
proximate behavioural mechanisms allowing birds to respond to temporal variations in prey
availability. Furthermore, given the importance of stopover areas for migratory waders
(Warnock 2010), it is interesting to assess how migrants benefit from the improved feeding
conditions that are usually found in temperate estuaries during migratory periods, in relation
to winter (van Gils et al. 2005). These issues are explored in Chapter 2.
Food abundance and safety from predator attacks are among the most important
factors driving the distribution of waders within a wetland (Piersma et al. 1993b; van Gils et al.
2006). However, the relative weight of these factors is known to be state-dependent, being
influenced for instance by the age/experience of birds in a certain area (Dierschke 1998; van
den Hout et al. 2014) or by their capacity to escape from predators (Ydenberg et al. 2002;
Nebel and Ydenberg 2005). In comparison with wintering birds, that generally spend long
periods in the same wetland, migrants usually stay for short periods at each stopover site (e.g.
Warnock et al. 2004). Therefore they are likely to have a poor knowledge of local habitat
characteristics, such as of real predation risk (Yasué 2006; Sprague et al. 2008), which might be
difficult to evaluate (Lima and Dill 1990). Furthermore, the additional weight of fat reserves
carried by migrating birds is a disadvantage when escaping from aerial predators (Piersma et
Chapter 1. General Introduction
39
al. 2003; Nebel and Ydenberg 2005). Therefore these factors may promote differences in
habitat selection and distributional patterns between wintering and migrating wader
populations using the same wetland. These points are investigated in Chapter 3.
1.4. Threats to wader populations in non-breeding areas and
conservation concerns
Wader populations are declining worldwide, which is a matter of international
conservation concern (IWSG 2003). The reasons behind this decline are diverse and partly
unknown, but anthropogenic pressure is a widespread threat. Most of the arctic breeding
grounds such as the Siberian Tundra, have not (yet) been suffering from intense human
pressure (van de Kam et al. 2004). However, several wader populations breeding further
south, in temperate regions, have been dramatically affected by human activities, mostly
involving habitat loss, degradation and disturbance (e.g. Beintema and Muskens 1987; Cayford
1993; Goss-Custard et al. 1995; Sutherland et al. 2012).
During the non-breeding period many wader populations suffer high direct human
pressure, because coastal and estuarine habitats are usually surrounded by densely-populated
urban areas, especially in the temperate regions of the northern hemisphere (Rosa et al. 2003;
Martín et al. 2015). Despite the legal protection of the most important sites along each flyway
(see Delany et al. 2009), waders continue to be threatened by loss and deterioration of both
intertidal flats and high-tide roosts (Goss-Custard and Yates 1992; Yates et al. 1996; Dias et al.
2006) and by direct human disturbance (West et al. 2002; Rogers et al. 2006; Yasué 2006). An
additional recent threat is the rise in sea level, which is expected to reduce the availability of
feeding and roosting areas for waders (Galbraith et al. 2002).
The direct loss of intertidal habitat through large-scale impacting activities, such as the
construction of barriers or dams and sediment dredging, forces waders to forage in alternative
areas. This may increase the density of foraging birds in non-affected areas (e.g. Schekkerman
et al. 1994), and thus the competition for resources (Goss-Custard et al. 2004), or cause a raise
in their energetic costs due to longer flights between roosting sites and foraging areas (Dias et
al. 2006). The dense urban occupation around many estuaries and intensive agricultural/
industrial activities can also impact the quality of feeding areas for waders, e.g. through the
pollution with toxic chemicals, such like heavy metals (França et al. 2005) or eutrophication of
intertidal areas (Sutherland et al. 2012). However, the abundance of some invertebrates may
locally increase in response to discharges of organic material (Ait Alla et al. 2006). The
Chapter 1. General Introduction
40
commercial exploitation of shellfish using mechanical systems can also dramatically reduce
bivalves and other non-target populations (Ferns et al. 2000), hence affecting the availability of
food for waders.
High-tide roosting sites are particularly vulnerable to human pressure. The destruction
of saltmarshes and the convertion of saltpans to aquacultures are examples of loss of roosting
habitat (Goss-Custard and Yates 1992; Catry et al. 2011), and direct disturbance reduces their
suitability for waders (Rogers 2003; Yasué 2006). Impacts on roosting sites can also negatively
affect the use of adjacent intertidal flats by waders, due to the spatial interdependence
between roosts and foraging areas (Piersma et al. 1993b; Dias et al. 2006).
Overall, anthropogenic pressure has a strong potential to reduce the quality of estuarine
ecossystems and thus impact wader populations. For example, it may reduce the probability of
survival during the non-breeding season (Durell et al. 2006), especially when climatic
conditions are unfavourable, e.g. during the cold periods common in the northermost
wintering areas (Davidson and Evans 1982). The reduction of habitat quality for waders in
estuarine areas may also limit their carrying capacity during non-breeding season (Goss-
Custard et al. 2002) and thus affect birds in their subsequent stages of the year-cycle. A poor
body condition or a late arrival at breeding areas (Hotker 2002; Gunnarsson et al. 2006) are
examples of negative consequences that waders can bring from poor-quality wintering and
stopover areas (Marra et al. 1998; Bearhop et al. 2004), which are known to limit their
breeding success (Norris et al. 2004). The long term deterioration of feeding conditions in
stopover sites may also promote large-scale changes in migratory pathways of entire
populations (Verkuil et al. 2012), highlighting the importance of maintaining networks of good-
quality stopover sites linking wintering and breeding areas.
1.5. Tagus estuary: characterization and relevance for waders
The Tagus estuary (Figure 1.3) is one of the largest estuaries in Western Europe,
covering a total area of 320 km2 (Costa 1999), and it is the most important Portuguese wetland
for waterbirds (Costa et al. 2003). Its tides are semi-diurnal, with amplitudes ranging from 1 to
3.8 m in neap and spring tides, respectively. During low water of spring tides (bellow 0.6 m) ca.
97 km2 of intertidal flats become exposed. The shape and size of intertidal areas of the estuary
are notoriously diverse (Figure 1.3); in the northern side (north of the latitude of Montijo)
intertidal flats are large and form a vast uninterrupted open area (total of ca. 71 km2), whereas
the remaining estuary (southern areas) encompasses several small mudflats in enclosed bays
Chapter 1. General Introduction
41
(totalizing ca. 26 km2). The composition of intertidal sediments are variable, from mud
(particles < 63 μm) to coarse sand (particles > 500 μm), but mud is the dominant type of
substrate (Rodrigues et al. 2006; Figure 1.3A). There are also large dead oyster banks near the
main navigation channels (Rodrigues et al. 2006; Figure 1.3A).
The benthic community of the Tagus estuary is dominated in abundance by small
annelids, while the biomass is largely dominated by the bivalve Scrobicularia plana (Rodrigues
et al. 2006). Other abundant species known as important prey for waders include the
polychaete Hediste diversicolor, the gastropod Hydrobia ulvae and the isopod Cyathura
carinata (Moreira 1995a; Silva et al. 2006). They are also important food items for fishes that
feed in intertidal flats during the high-tide, such as gobies Pomatoschistus spp. and soles Solea
spp. (Cabral 2000; Salgado et al. 2004).
Intertidal flats of the Tagus estuary are bordered mostly by beaches and saltmarshes
(Figure 1.3) and the surrounding land is mainly used for agriculture or urbanization. The
northern half of the left margin of the river (north of Alcochete) is dominated by extensive
farmland and pastures, with low human occupation (Figure 1.3B). In contrast, the right margin
Figure 1.3. (A) Main habitats used by waders in the Tagus estuary and limits of protected areas, and (B)
density of human population in surrounding land, by civil parish (data from INE 2011).
Chapter 1. General Introduction
42
of the river and the southern half of the left margin (south to Montijo) are densely populated
(Figure 1.3B) and mostly urban or industrial. Around the estuary there are many saltpans
(Figure 1.3A), remnants of the salt exploitation that declined after the 70s (Rufino and Neves
1992), which have been abandoned or converted in tanks for aquaculture. The largest saltpan
complex (Samouco) is actively managed for waterbirds.
During the high-tide, waders using this estuary roost mainly in saltpans or saltmarshes
(e.g. Alves et al. 2011). However, in some areas they prefer to roost in mudflats that do not
flood during neap (high) tides, presumably to avoid the higher risks of predation from aerial
predators that are found in habitats bordering the estuary (Rosa et al. 2006). Common aerial
predators include the Peregrine-falcon Falco peregrinus, Marsh-harrier Circus aeruginosus and
Booted-eagle Hieraaetus pennatus.
The Tagus estuary is considered a key site for migratory waders in the East Atlantic
Flyway, holding internationally important numbers of seven species, during the winter and
migration periods (Delany et al. 2009). The Dunlin, Black-tailed Godwit Limosa limosa, Avocet
Recurvirostra avosetta and Grey Plover Pluvialis squatarola are the most abundant species of
the estuary during the winter (Catry et al. 2011), representing a large fraction of the ca. 50 000
waders counted in the 1990s by Instituto para a Conservação da Natureza e Florestas – ICNF
(Dias 2008; Catry et al. 2011).
The total number of migrant waders using the estuary is unknown for most species,
because such estimation requires frequent counts and knowledge of local turnover rates. An
exception is the Black-tailed Godwit, for which it has been estimated that 15-25% of the
continental European population (subspecies L. l. limosa) uses the Tagus estuary as a staging
area (Lourenço and Piersma 2008). High numbers of waders regularly counted in the spring
and autumn migrating periods (Alves et al. 2011; Catry et al. 2011; Alves et al. 2015) suggest
that this wetland, strategically located between the West African wintering areas and key
estuaries in the North western Europe, plays a relevant role as a stopover site for many other
species (Delany et al. 2009).
Over the past three decades significant declines of wintering populations in the Tagus
estuary were detected in three of the five most abundant species (Catry et al. 2011): Dunlin,
Grey Plover and Redshank. The increasing human pressure around the estuary (Rosa et al.
2003) is a likely reason for such long term declines, in particular on roost sites, due to the
human activities causing their loss and degradation, such as abandonment or conversion of
saltpans into aquacultures (Dias 2008; Catry et al. 2011).
The legal protection of the Tagus estuary started in 1976 with the classification of part of
the wetland (ca. 142 km2) as Nature Reserve (Reserva Natural do Estuário do Tejo - RNET;
Chapter 1. General Introduction
43
Figure 1.3). A Special Protected Area for Birds (SPA) was defined in 1994 (the limits were
slightly extended in 1997) covering actually a total of ca. 450 km2 of intertidal areas and
surrounding land, which includes all the RNET area (Figure 1.3). Both RNET and SPA are
managed by the ICNF. The Tagus estuary is also considered a wetland of international
importance for waterbirds under the Ramsar Convention (1980).
Previous research in the Tagus estuary focused diverse aspects of wader ecology, at
different scales, such as their distribution across intertidal areas and association to sediment
types (Moreira 1993; Granadeiro et al. 2004; Granadeiro et al. 2007), diet and foraging
behaviour (Moreira 1995a; Lourenço et al. 2005; Santos et al. 2005; Dias et al. 2009; Catry et
al. 2012b), selection of roosting sites (Rosa et al. 2006) and the use of the estuary in the
context of the flyway (Alves et al. 2013). Despite the importance of the estuary during
migratory periods, the great majority of these studies focused wintering populations, so there
is still little information on local stopover ecology for many wader species (Lourenço and
Piersma 2008).
1.6. Dunlin: the model-species
Figure 1.4. (A) Detail of a dunlin in wintering plumage, (B) a dunlin flock foraging on intertidal mudflats
in spring and (C) a few hundreds of dunlins mixed with other wader species roosting in a saltpan.
C
A B
Chapter 1. General Introduction
44
The Dunlin (Figure 1.4) is a small-sized wader with a globally widespread distribution and
10 recognized sub-species (BWPi 2006). It breeds mainly in sub-arctic and low Arctic regions of
Europe, Asia and North America, extending into temperate and high Arctic latitudes in parts of
its range (Delany et al. 2009). This species spends the non-breeding season in temperate and
sub-tropical estuarine and coastal areas of the northern hemisphere (Delany et al. 2009),
where it feeds in intertidal mudflats upon invertebrates, mostly polychaetes, bivalves,
gastropods and crustaceans (BWPi 2006). It is the most abundant wader of the East Atlantic
Flyway (van de Kam et al. 2004), which is used by five breeding populations: C. a. alpina – from
Northern Scandinavia to Western Siberia; three different populations of C. a. schinzii – from
Iceland, British Isles and the Baltic; and C. a. arctica – from Northeast Greenland (Delany et al.
2009).
The Tagus estuary holds about 10 000 wintering dunlins (Alves et al. 2011; Catry et al.
2011; Alves et al. 2015), most of which breed in Scandinavia and Russia (Lopes et al. 2006). The
total number of dunlins using the estuary as stopover area is unknown, but average counts in
the peak of migration reach around 12 000 individuals in spring and 6000 in autumn (Alves et
al. 2011; Catry et al. 2011; Alves et al. 2015). Most of these belong to the Icelandic-breeding
population that winters mainly in Mauritania (Delany et al. 2009). Therefore, the Tagus estuary
is adequate to compare how different populations of the same species vary in their use of
estuarine resources.
Although the Dunlin is a relatively well studied species, most of the research on the East
Atlantic Flyway populations took place in northern Europe. Therefore, baseline information
from estuaries of southern Europe and along the African coast is still relatively scarce,
particularly during migratory periods.
Wader species vary in their ecology, so none of them is fully representative of all the
species in the group. Nevertheless, the Dunlin is a good model species to study the overall
wader community of the Tagus estuary, because:
• It shares with many other wader species both their main prey (e.g. Moreira 1995a)
and predators (e.g. Rosa et al. 2006), especially with species preferring the same
types of sediment (Granadeiro et al. 2007);
• It shows plasticity in terms of foraging behaviour and diet (Nehls and Tiedemann
1993; Santos et al. 2005), which makes it suitable to compare foraging responses to
different environmental conditions;
• It is quite abundant and widespread in the estuary (Granadeiro et al. 2006;
Granadeiro et al. 2007; Catry et al. 2011), which facilitates the collection of data;
Chapter 1. General Introduction
45
• It is less difficult to capture than other larger-sized (and more wary) species (but see
Chapter 5).
1.7. Thesis main aims and outline
This thesis aimed at comparing the foraging ecology, behaviour and distribution of
wintering and migrating dunlins at the Tagus estuary, as these populations can be investigated
in different periods under very distinct ecological constraints. This research also aimed to
unveil the geographic origins of dunlins using the estuary as a stopover, and to investigate the
overlap of wintering and migrating birds that mix there between winter and migratory periods.
The main conservation implications of the findings are also addressed.
The thesis is organised as a set of relatively independent chapters, and it ends with a
general discussion of the results obtained (Chapter 6). Chapters 2, 3, 4, and 5 were prepared as
manuscripts, which have been submitted to scientific journals or are already published. The
specific aims of each paper are described below, along with the main methodological
approaches.
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins Calidris alpina in
a South European estuary: improved feeding conditions for northward migrants
The main aim of this study was to examine the differences in foraging behaviour and
diet of wintering and northward migrating dunlins in the Tagus estuary and investigate the
extent to which these differences are influenced by seasonal variations in prey abundance and
availability. It included the video-recording of foraging birds, the analysis of their droppings,
and the sampling of prey abundance, to estimate biomass available for dunlins in winter and
spring. Energy intake rates achieved by dunlins in each season were calculated and interpreted
in the light of their energetic demands to understand the significance of the improved feeding
conditions provided by the estuary as a stopover site for migrants.
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the
potential role of fear
In this study, previously published data on wader numbers at high-tide roosts of Tagus
estuary were re-analysed to assess seasonal variations in the distribution of dunlins in two
major (northern and southern) sectors of the estuary. These sectors present marked
differences in shape and size of intertidal areas. Departure rates of wintering dunlins from
both sectors of the estuary were investigated, using radio-tracking, to clarify to which extent
Chapter 1. General Introduction
46
they co-occur with northward migrants in the estuary in late winter-early spring. Food
availability and predation risk for dunlins were evaluated in both sectors of the estuary,
respectively through sediment sampling and observation sessions to count raptors and record
wader behaviour. These data, together with indicators of perceived risk of predation in each
sector, were used to identify the main drivers of the spatial distribution of wintering and
migrating birds.
Chapter 4. Discriminating geographic origins of migratory waders at stopover sites: insights
from stable isotope analysis of toenails
This study aimed at testing the potential use of stable isotope analysis from toenails to
reveal the geographic wintering origin of dunlins in areas that act both as wintering and
stopover sites. This information was further used with the purpose of deriving migratory
schedules of dunlins at the Tagus estuary during spring migration. This was carried out by
determining the stable carbon (δ13C) and nitrogen (δ15N) isotope signatures of toenails of
dunlins wintering in several sites along the East Atlantic Flyway. Subsequently, dunlins sampled
at the Tagus estuary in spring were assigned to their wintering grounds, according to their
stable isotope values.
Chapter 5. Crossbow-netting: a new method for capturing shorebirds
Many of the methods used in this thesis to study waders, such as radio-tracking and
analysis of tissue samples, require the capture of individuals. However, capturing waders
during the non-breeding season can be challenging (Stroud and Davidson 2003) because they
are usually scattered in wide-open foraging areas and are sensitive to human disturbance at
the roosts, where they gather during high tide. Several techniques are currently available for
capturing waders, under different circumstances, and all have their strengths and weaknesses
(e.g. Johns 1963; Thompson and DeLong 1967; Hicklin et al. 1989; Doherty 2009). The wader
research at the Tagus estuary required the capture of dunlins on a regular basis and none of
the existing techniques was well suited for the particular conditions of the study areas. This
chapter describes the development of a new method to capture waders and other shorebirds,
where a crossbow is used to pull a mist-net over flocks of roosting birds. The main advantages
and disadvantages of this technique are discussed in comparison with other methods.
47
CHAPTER 2
Seasonal variations in the diet and foraging
behaviour of dunlins Calidris alpina in a South
European estuary: improved feeding conditions
for northward migrants
Martins, R. C., T. Catry, C. D. Santos, J. M. Palmeirim & J. P. Granadeiro. 2013
Plos One 8(12): e81174
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
49
2. Seasonal variations in the diet and foraging behaviour of
dunlins Calidris alpina in a South European estuary: improved
feeding conditions for northward migrants
2.1. Abstract
During the annual cycle, migratory waders may face strikingly different feeding
conditions as they move between breeding areas and wintering grounds. Thus, it is of crucial
importance that they rapidly adjust their behaviour and diet to benefit from peaks of prey
abundance, in particular during migration, when they need to accumulate energy at a fast
pace. In this study, we compared foraging behaviour and diet of wintering and northward
migrating dunlins in the Tagus estuary, Portugal, by video-recording foraging birds and
analysing their droppings. We also estimated energy intake rates and analysed variations in
prey availability, including those that were active at the sediment surface. Wintering and
northward migrating dunlins showed clearly different foraging behaviour and diet. In winter,
birds predominantly adopted a tactile foraging technique (probing), mainly used to search for
small buried bivalves, with some visual surface pecking to collect gastropods and crop bivalve
siphons. Contrastingly, in spring dunlins generally used a visual foraging strategy, mostly to
consume worms, but also bivalve siphons and shrimps. From winter to spring, we found a
marked increase both in the biomass of invertebrate prey in the sediment and in the surface
activity of worms and siphons. The combination of these two factors, together with the
availability of shrimps in spring, most likely explains the changes in the diet and foraging
behaviour of dunlins. Northward migrating birds took advantage from the improved feeding
conditions in spring, achieving 65% higher energy intake rates as compared with wintering
birds. Building on these results and on known daily activity budgets for this species, our results
suggest that Tagus estuary provides high-quality feeding conditions for birds during their
stopovers, enabling high fattening rates. These findings show that this large wetland plays a
key role as a stopover site for migratory waders within the East Atlantic Flyway.
2.2. Introduction
Each year, millions of waders undertake long distance migratory movements between
high-latitude breeding areas and temperate or tropical wintering grounds (Delany et al. 2009).
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
50
During these periods, most species depend on a network of wetlands along their flyways
(Delany et al. 2009), where they stopover to rebuild their reserves and roost (Warnock 2010).
As most migratory taxa, waders have to cope with the challenge of finding food in a
variety of habitats, experiencing dramatically different environmental conditions. Feeding
resources, in particular, show high variability in composition and availability across the
latitudinal gradient of breeding, stopover and wintering areas used by waders (Piersma et al.
1993a).
In estuarine and coastal wetlands, prey availability also varies seasonally, with prey
biomass usually peaking during the warmer periods of the year (Scheiffarth and Nehls 1997). In
order to adapt to these rather short-termed variations in prey abundance and accessibility,
waders generally show a strong behavioural plasticity, allowing them to explore a wide range
of feeding resources during their annual cycle (e.g. Beninger et al. 2011; MacDonald et al.
2012).
The Dunlin Calidris alpina is a migratory wader, with circumpolar breeding range and a
wide wintering distribution along temperate and subtropical coastlines of the Northern
hemisphere (Delany et al. 2009). As other calidrid species, dunlins possess very sensitive bills
adapted for tactile foraging (Nebel et al. 2005), mainly on polychaetes, molluscs and
crustaceans (BWPi 2006). However, they have been traditionally classified as mixed foragers,
being able to alternate between visual and tactile foraging modes in response to variable
environmental conditions. Indeed, previous studies on dunlins documented shifts in their diet
and/or foraging strategy in response to factors such as sediment penetrability (Mouritsen and
Jensen 1992; Santos et al. 2005; Kuwae et al. 2010), light conditions (Mouritsen 1993;
Lourenço et al. 2008; Santos et al. 2010b) and prey availability (Rands and Barkham 1981; Clark
1983; Nehls and Tiedemann 1993; Dierschke et al. 1999; Lourenço et al. 2005; Santos et al.
2009; Santos et al. 2010a). Dunlins are then expected to take advantage of seasonal peaks of
food abundance, in particular if such changes occur during periods of higher energetic
demand, such as during migratory periods. Some authors have reported seasonal variations in
the diet of dunlins (Ferns and Worrall 1984; Worrall 1984; Nehls and Tiedemann 1993; Moreira
1995a), but the proximate factors of such variations are still poorly understood. Furthermore,
no studies have focused on the role that changes in prey availability, in particular at the
sediment surface, can have both in foraging strategies and diet and in the energy intake rates
obtained by dunlins with different energetic constrains, such as wintering and passage migrant
birds using the same intertidal flats.
The Tagus estuary, Portugal, holds internationally important numbers of wintering
dunlins (more than 1% of the population; Delany et al. 2009), with an overwintering
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
51
population of ca. 10 000 individuals (Catry et al. 2011). It is also a relevant stopover area for
dunlins migrating along the East Atlantic Flyway, harboring an average of about 15 000 birds in
the peak of northward migration (Catry et al. 2011). Dunlins wintering in Tagus estuary include
birds that breed in Scandinavia (C. a. alpina) and in the Baltic region and in the UK (both C. a.
schinzii) (Lopes et al. 2006; Delany et al. 2009). Northward migrants are thought to originate
mostly from Mauritania, using the Tagus as stopover area when travelling to breeding grounds
in Iceland (C. a. schinzii) (Delany et al. 2009; Catry et al. 2012a). Wintering dunlins are in the
estuary mainly from November to early-April, while most northward migrants arrive in large
numbers in the second half of April (Catry et al. 2012a).
Despite its importance as a stopover area, the great majority of the studies in the Tagus
estuary have focused in wintering populations (e.g. Santos et al. 2005; Dias et al. 2006;
Lourenço et al. 2008), so there is little information about wader foraging behaviour and
feeding conditions during migratory periods (Moreira 1995a).
In this study we aimed to (1) examine the differences in foraging behaviour and diet of
wintering and northward migrating dunlins in the Tagus estuary and (2) investigate the extent
to which these are influenced by seasonal variations in invertebrate availability. Additionally,
we (3) calculated the energy intake rates achieved by dunlins in each season in light of their
expected energetic demands and (4) discuss the significance of the improved feeding
conditions provided by this temperate estuary for northward migrants in the context of the
East Atlantic Flyway.
2.3. Methods
Ethics statement
Although our study area is included in a Special Protected Area for birds (Zona de
Protecção Especial do Estuário do Tejo), the fieldwork carried out in this study did not require
any legal permission from the Nature Reserve authorities, as it did not involve capture or
manipulation of birds. Furthermore, the observation of birds, at a distance, did not cause any
disturbance and Dunlin is not an endangered species. It is considered a “species of Community
interest” according to the Portuguese law (DL 49/2005, that transposes the European Birds’
Directive) and has the conservation status of “Least Concern” according to both the Red Book
of the Vertebrates of Portugal (Cabral et al. 2005) and the IUCN Red List of Threatened Species
(IUCN 2012).
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in
Study area
This study was carried out in the Tagus estuary, Portugal (38
which covers a total area of ca. 13
oyster beds and sandy flats (Granadeiro et al. 2007
Our study area was located in the southern margin of the estuary (Figure
two sectors of intertidal mudflat were selected near the shoreline (ca. 200 m). Western and
eastern sectors had an exposure period of approxima
(amplitude >2.7 m) and cover 4.5 and 18 ha, respectively.
(>95% of particles <63 µm; Rodrigues et al. 2006
recorded in the study area during winter and spring were of 5.6 ± 1.2 (SE) and 3.4 ± 2.5 (SE)
birds/ha (n= 8 and 6 counts), respectively. These sectors are representative of the intertidal
areas commonly used by dunlins in the Tagus estuary
procedures were replicated in both sectors.
Figure 2.1. Map of the Tagus estuary, showing the location of the study area.
represent the selected sectors of intertidal mudflat.
intertidal area and dark grey
Bird observations
Haphazardly chosen dunlins were video
tide peak) in winter (Jan-Feb of 2009 and 2010) and spring (mid
while foraging in the study area. Recordings were carried
DS15, Panasonic) with a 20x optical zoom, equipped with a 1.4x adapter. Birds were filmed at
close distances (from 8 to 30 m, mean ± SD= 17.7 ± 5.5 m, n= 155). In general, birds were
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
52
rried out in the Tagus estuary, Portugal (38°45’N, 09°
which covers a total area of ca. 13 000 ha, largely dominated by mudflats, but also including
Granadeiro et al. 2007).
Our study area was located in the southern margin of the estuary (Figure
two sectors of intertidal mudflat were selected near the shoreline (ca. 200 m). Western and
eastern sectors had an exposure period of approximately three and five hours in spring tides
m) and cover 4.5 and 18 ha, respectively. The sediment consisted of mud
>95% of particles <63 µm; Rodrigues et al. 2006) and the mean low tide densities of dunlins
recorded in the study area during winter and spring were of 5.6 ± 1.2 (SE) and 3.4 ± 2.5 (SE)
6 counts), respectively. These sectors are representative of the intertidal
areas commonly used by dunlins in the Tagus estuary (Granadeiro et al. 2007
ted in both sectors.
Map of the Tagus estuary, showing the location of the study area.
represent the selected sectors of intertidal mudflat. Light grey shading represent
dark grey areas represent saltmashes.
Haphazardly chosen dunlins were video-taped during diurnal low tides (± 2
Feb of 2009 and 2010) and spring (mid-Apr-May of 2009 and 2010)
while foraging in the study area. Recordings were carried out with a digital camcorder (NV
DS15, Panasonic) with a 20x optical zoom, equipped with a 1.4x adapter. Birds were filmed at
close distances (from 8 to 30 m, mean ± SD= 17.7 ± 5.5 m, n= 155). In general, birds were
� �
a South European estuary
00’W; Figure 2.1),
000 ha, largely dominated by mudflats, but also including
Our study area was located in the southern margin of the estuary (Figure 2.1), where
two sectors of intertidal mudflat were selected near the shoreline (ca. 200 m). Western and
tely three and five hours in spring tides
The sediment consisted of mud
and the mean low tide densities of dunlins
recorded in the study area during winter and spring were of 5.6 ± 1.2 (SE) and 3.4 ± 2.5 (SE)
6 counts), respectively. These sectors are representative of the intertidal
Granadeiro et al. 2007). All field work
Map of the Tagus estuary, showing the location of the study area. Black dots
rey shading represents the
taped during diurnal low tides (± 2 h from low
May of 2009 and 2010)
out with a digital camcorder (NV-
DS15, Panasonic) with a 20x optical zoom, equipped with a 1.4x adapter. Birds were filmed at
close distances (from 8 to 30 m, mean ± SD= 17.7 ± 5.5 m, n= 155). In general, birds were
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
53
numerous and moved in the same direction along the shoreline. Therefore, it is highly unlikely
that pseudoreplication (i.e. filming the same individual more than once) affected our dataset
and conclusions to any significant extent. A total of 99 and 56 one-minute good-quality videos
were obtained, respectively in winter and spring (recordings of poor quality were discarded).
Sampling periods were chosen to ensure that birds recorded in winter belong to the local
wintering population and those sampled in spring belong mainly to the African-wintering
populations that stopover in Tagus estuary during their northward migration.
Foraging behaviour
Video recordings of foraging dunlins were examined in slow-motion to quantify the
number of steps and number of pecks per minute. Three different types of pecks were
considered: (1) superficial pecks – when only the tip of the bill (< 5 mm) is inserted in the
sediment; (2) probes – when more than 5 mm of the bill is inserted in the sediment; and (3)
sweeps – essentially used as a visual technique, comprising a very fast sequence of opening
and closing movements of the flexible tip of the bill (> 5 cycles/sec) while making small range
(< 3 cm) radial movements of the neck. Sweeps were usually performed in the water film for
capturing shrimps. No evidence of biofilm grazing was observed in the videos (Kuwae et al.
2012).
Characterization and quantification of diet
Prey identity and consumption rates were assessed from video recordings and
complemented with dropping analyses. Analysis of video recordings allowed the accurate
distinction between filiform (worms and siphons of bivalves) and non-filiform prey items
(crustaceans, bivalves and gastropods), as filiform prey are usually pulled out of the sediment
and are visible even when extracted by deep probing.
The specific identification of filiform prey was possible in a subset of recordings (ca. 20%
in each season) obtained at a short distance, and revealed that birds were consuming the
polychaete Hediste diversicolor and siphons of the bivalve Scrobicularia plana, in both seasons.
Therefore, prey-specific consumption rates of filiform prey were calculated for all video
recordings assuming the relative occurrence of S. plana siphons or H. diversicolor in this subset
of recordings, in each season.
Among non-filiform prey, isopodes can also be identified in video recordings (Santos et
al. 2010a), as well as shrimps, whose capture by dunlins involves a specific and easily
recognizable behaviour (see also Nehls and Tiedemann 1993). However, the consumption of
entire bivalves and gastropods could not be well assessed even with the best quality
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
54
recordings. Although consumption of whole bivalves by dunlins results in the typical
swallowing movements, these prey are difficult to be confirmed in recordings because they are
often ingested during continuous probing. Gastropods consumed by dunlins in the study area
(Hydrobia ulvae) live on the sediment surface but due to their small size they are quickly
collected with superficial pecks and ingested without the typical swallowing movement (see
also Santos et al. 2010a) and consequently can not be detected in video recordings.
Furthermore, dunlins also use superficial pecks to capture (e.g.) retractable prey available at
sediment surface (worms and bivalve siphons) and we were often unable to distinguish
unsuccessful attempts to capture such retractable prey from captures of H. ulvae.
Due to these difficulties, the quantification of the consumption of bivalves and
gastropods was supported by the analysis of 80 and 148 dunlin droppings, collected in winter
(Jan-Feb 2010, in eight sessions) and spring (mid-Apr-May 2010, in 14 sessions) periods,
respectively. Droppings were collected in the study area immediately after video recording
foraging birds, and at least 30 minutes after a flock arrived in the area. Dunlin droppings could
be easily identified in the sediment by their size and shape, and there were no other similar-
sized species in the study area that could cause identification issues. Whole droppings were
carefully collected from the sediment surface, stored in individual containers and frozen at -18
ºC prior to analysis. In the laboratory, droppings were examined with a stereomicroscope, and
prey species were identified using diagnostic remains.
We assumed that all ingested items classified in video recordings as unidentified non-
filiform prey were entire S. plana. This is supported mainly by the fact that the capture of
these items resulted exclusively from probing and that droppings did not contain remains of
any other non-filiform buried-living prey. Accordingly, the seasonal differences in the
occurrence of shell fragments of S. plana in droppings (73.8% in winter and 19.6% in spring)
were similar to those found in the consumption rate of those unidentified non-filiform items in
recordings (see results).
The quantification of H. ulvae in the diet of dunlins was based only in dropping analyses
and is expressed as a frequency of occurrence.
Prey sampling and availability
The density of benthic prey was determined in the study area by randomly taking 100
and 114 sediment cores (86.6 cm2, 30 cm deep) in late winter (early March 2010) and spring
(end of May 2010), respectively. The upper 5 cm of each core was sieved through a 0.5 mm
mesh (to ensure that small prey in the top layer could be quantified), whereas a 1 mm mesh
was used to sieve the remaining sediment. Shrimps available at the surface water film were
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
55
unlikely to be adequately sampled with sediment cores. Therefore we used a wood enclosure
(75x75 cm wide and 20 cm high) that was randomly thrown to the surface of the sediment, 40
and 47 times during the winter and spring periods, respectively. The whole area of the
enclosure was then carefully sieved with a square-shaped landing net with a mesh of 1 mm,
collecting all shrimps in the sediment surface and water film. Invertebrates collected with both
techniques were stored in 70% alcohol and later identified using stereomicroscope, and their
densities were calculated.
Prey biomass (expressed in AFDW/m2) was estimated by measuring their body/structure
size and then using published relationships between size and biomass for each species (Table
2.1). Some H. diversicolor were not intact and therefore we estimated the total body length
using published relationship between mandible and body lengths (Table 2.1). The length of S.
plana siphons was estimated from regressions with shell size, following Zwarts et al. (1994)
(Table 2.1).
There is no detailed information on seasonal variations in size-biomass relationships for
all dunlin prey in the Tagus estuary. However, Guerreiro (1991), in a study with S. plana in
Portuguese estuaries, showed minor winter to spring variations in such relationship in
comparison of those obtained in higher latitudes (Zwarts 1991). Furthermore, Guerreiro (1991)
also showed that the smaller sizes of S. plana (corresponding to the sizes consumed by
dunlins) are virtually not affected by seasonal variations in size-biomass relationships.
Therefore, assuming that this also applies to other prey, it is unlikely that our estimates of
invertebrate biomass are significantly affected by such effect.
Table 2.1. Equations used to calculate biomass (ash free dry weight, AFDW) of Dunlin
invertebrate prey.
Equation Source
Hediste diversicolor TL=40.173ML-3.4225 (Masero et al. 1999)
AFDW=10(2.53LOG(TL)-5.94)x0.771x1000 (Moreira 1995a)
Scrobicularia plana AFDW=10(2.49LOG(APL)-4.57)x0.795x1000 (Moreira 1995a)
Siphons of S. plana SLS=0.9APL+1.4 (Zwarts et al. 1994)
AFDW=SLSx0.00014APL1.69 (Zwarts et al. 1994)
Hydrobia ulvae AFDW=0.0154SL2.61 (Santos et al. 2005)
Crangon crangon AFDW=0.2((TL+1.1295)/4.7906)3.0725 (Viegas et al. 2007)
TL- total length (mm); ML- mandible length (mm); AFDW- biomass, expressed as ash free
dry weight (mg); APL- antero-posterior length of the shell (mm); SLS- siphon length at
surface (mm); SL- shell length.
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
56
We considered that all invertebrates present in the upper 5 cm of core samples (plus
shrimps) were available for dunlins, with the exception of bivalves and polychaetes larger than
13 and 66 mm, respectively, as they are not consumed by dunlins (Santos et al. 2005). We also
considered that all polychaetes less than 66 mm long and the siphons of bivalves present in
the lower portion of the core were available, as their surface activity (Esselink and Zwarts
1989; Zwarts and Wanink 1989) makes them accessible to dunlins (Moreira 1995a; Santos et
al. 2005).
The availability of H. diversicolor and siphons of S. plana at the surface of the sediment
(nr. of active items/m2) was further quantified with video recordings, in winter and spring. A
digital camcorder (NV-DS15, Panasonic) was used to record invertebrate activity in 50 x 50 cm
areas of exposed sediment, during 6 min, within 2 h from the low tide. A total of 17 and 56
recordings were obtained in winter (Jan-Feb 2010) and spring (Apr-May 2010), respectively.
Each video recording was analysed in a computer and the number of S. plana siphons
and H. diversicolor visible at the surface in each sampling square were counted at intervals of
0.5 min. In all videos, we excluded the first 2 min and the last 1.5 min of the recordings, to
avoid any observer effect. We recorded the highest count of each prey item in each video
recording, and then averaged these values across all videos, as an estimate of surface prey
availability. The biomass of S. plana siphons and H. diversicolor available at the surface was
estimated by multiplying the average number of visible items (obtained from video recordings,
in items/m²), by the season-specific average biomass of each prey, obtained from core
sampling.
Energy intake rates of dunlins
Energy intake rates of dunlins were obtained by multiplying the number of items
consumed per minute (estimated from video recordings) by their specific average energetic
content. The ingestion of individual H. ulvae could not be detected in video recordings (see
above) and therefore we estimated their consumption rate in each season by multiplying the
rate of superficial pecks identified in video recordings as potential captures of H. ulvae by the
frequency of occurrence of this prey in droppings.
The average energy content of each prey was calculated using published information
relating structural size with biomass (Table 2.1) and then considering that one gram of ash free
dry weight (AFDW) of each prey corresponds to about 23 Kj (van de Kam et al. 2004).
Average sizes of consumed S. plana and H. ulvae were obtained from Santos et al.
(Santos et al. 2005) (Table 2.2) as we confirmed that the size distribution of these two prey
species in our study is very similar of that obtained by those authors, within the size classes
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
57
consumed by dunlins (Santos et al. 2005). The size of H. diversicolor, the shrimp Crangon
crangon and siphons of S. plana consumed by dunlins was estimated in relation to culmen
length, from our best-quality videos, when these items were held by the tip of the bill
immediately before ingestion (Table 2.2). Average culmen length of dunlins in the Tagus
estuary is 32.3 mm (SD= 2.9) and 30.8 mm (SD= 2.8) for wintering and northward migrating
birds, respectively (authors’ unpublished data).
Table 2.2. Mean sizes (± SD, sample sizes in parenthesis) and mean individual energy
content of prey consumed by dunlins in winter and spring. Consumed sizes of S. plana and
H. ulvae were obtained from Santos et al. (2005). Size of S. plana refers to antero-
posterior length of the shell. Size of siphons refers to siphon length at surface. Size of H.
ulvae refers to shell length.
Size (mm) Energy content (J)
Winter Spring Winter Spring
H. diversicolor 15.4 ± 4.7 (4) 24.6 ± 9.9 (18) 20.7 67.4
C. crangon --- 13.5 ± 2.4 (11) --- 142.2
Siphons of S. plana 21.1 ± 10.8 (19) 44.1 ± 10.5 (5) 28.2 46.8
S. plana 7.1 ± 0.4 (169) --- 64.8 ---
H. ulvae 1.8 ± 1.5 (216) --- 1.64 ---
Statistical analyses
Most of the data failed to meet the assumption of normality and homocedasticity (even
after transformation) and therefore we used Mann-Whitney tests to compare diet and
behavioural parameters, as well as prey availability in winter and spring periods.
2.4. Results
Foraging behaviour and diet of dunlins
Foraging dunlins showed a significantly lower step rate in winter than in spring (134 ± 6.0 (SE)
steps/min in winter and 163 ± 6.1 (SE) steps/min in spring; Mann-Whitney test: U= 1952.5,
p<0.01). The total number of pecks (superficial pecks, probes and sweeps) did not vary
between seasons (74.0 ± 2.8 (SE) pecks/min in winter and 72.3 ± 5.5 (SE) in spring; Mann-
Whitney test: U= 3089.5, p= 0.238). However, we found significant differences in the type of
feeding techniques used from winter to spring (Figure 2.2). In fact, superficial pecking rate
increased significantly in spring, whereas the opposite trend was observed for probing (Figure
2.2). Sweeping was only observed in spring. These differences were also significant when each
sampling year was analysed separately (Mann-Whitney tests, all p< 0.001).
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
58
Figure 2.2. Mean rate of superficial pecks, probes and sweeps of foraging dunlins in winter
and spring. Values represent mean ± SE. Differences between seasons were tested with
Mann-Whitney test (*** p<0.001).
The diet of dunlins also differed significantly between seasons (Figure 2.3). In winter,
dunlins consumed mainly H. ulvae and S. plana (small entire individuals and siphons), whereas
in spring the main prey was H. diversicolor, and to a lesser extent S. plana siphons. The shrimp
C. crangon was consumed only in spring and at a relatively low rate (Figure 2.3A).
Figure 2.3. Diet of Dunlin in winter and spring assessed by (A) field observations and (B)
dropping analyses. A: Consumption rate (prey/min) of main prey. B: Occurrence of shell
remains of H. ulvae in Dunlin droppings. Values represent mean ± SE. Differences between
seasons were tested with (A) Mann-Whitney (B) and Chi-squared tests (* p<0.05; ***
p<0.001).
0
10
20
30
40
50
60
70
Superficial Pecks
Probes Sweeps
Pe
cks/
min
Winter (n=99)
Spring (n=56)
***
***
***
0
0.5
1
1.5
2
2.5
3
3.5
4
H. diversicolor Siphons S. plana C. crangon
Co
nsu
me
d p
rey
/m
in
Winter (n=99)
Spring (n=56)***
*
***
***
0%
10%
20%
30%
40%
50%
60%
70%
80%
90%
H. ulvae
Occ
urr
en
ce i
n d
rop
pin
gs
Winter (n=80)
Spring (n=148)
***
Siphons
A B
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
59
Prey availability
H. ulvae was the most abundant prey species in the study area, but the harvestable
biomass for dunlins was dominated by H. diversicolor, especially in spring (Table 2.3). S. plana,
siphons of S. plana, and H. ulvae had similar contributions to the available biomass and C.
crangon was virtually irrelevant (Table 2.3).
There was a noticeable increase (>2.5x) in the overall harvestable biomass from winter to
spring (Table 2.3). This was mostly due to increases in the size of H. diversicolor and (juvenile)
S. plana and in the number of adult S. plana (which are inaccessible to dunlins but provide
larger siphons at the surface).
The availability of H. diversicolor and S. plana siphons at the sediment surface also
increased significantly from winter to spring (Table 2.4). Although such increases were similar
in terms of numerical importance between these two prey items (12.5x in S. plana siphons and
15.5x in H. diversicolor), the corresponding biomass values were of rather different magnitude:
10x in S. plana siphons and 44x in H. diversicolor.
Table 2.3. Seasonal variation in harvestable density and biomass of main Dunlin prey
species in winter and spring. Means are represented ± SE. Relative contribution of each
prey for the total biomass in each season is shown between brackets. Differences
between seasons were tested with Mann-Whitney test (M-W test). Data were obtained
from 100 core samples in winter and 114 in spring, except for Crangon crangon, which
resulted from 40 and 47 sampling squares, respectively (see methods for further details).
Density (indiv./m2) Biomass (g of AFDW/m
2)
Winter Spring M-W test Winter Spring M-W test
H. ulvae 1947 ±
153
3768 ±
263
U=3362
p<0.001
0.25 ± 0.02
(15%)
0.27 ± 0.02
(6%)
U=5300
p=0.377
S. plana1 367 ± 51 304 ± 41
U=5787
p=0.845
0.20 ± 0.03
(12%)
0.49 ± 0.07
(11%)
U=3945
p<0.001
Siphons of S.
plana2
89.5 ±
11.6
181.6 ±
11.7
U=3187.5
p<0.001
0.26 ± 0.03
(16%)
0.43 ± 0.03
(10%)
U=4070
p<0.001
H. diversicolor3 310 ± 32 381 ± 31
U=4868
p=0.06
0.94 ± 0.10
(57%)
3.34 ± 0.27
(73%)
U=2734
p<0.001
C. crangon 0.04 ±
0.04
11.5 ±
5.4
U=5.5
p<0.001
<0.01 ± <0.01
(0%)
0.05 ± 0.01
(1%)
U=5
p<0.001
Total Biomass 1.65 4.58
1 Juvenile individuals, considered to be reachable and ingestible (whole) by dunlins, as
they lay in the upper sediment fraction (0-5 cm deep) and are small (<13 mm). 2 Siphons of
the individuals that are out of reach of a Dunlin’s bill, as they lay in the lower sediment
fraction (5-30 cm deep), corresponding mostly to large (>30 mm) and adult individuals. 3
Individuals longer than 66 mm were excluded.
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
60
Table 2.4. Seasonal variations in the surface availability of Hediste diversicolor and siphons
of Scrobicularia plana and their corresponding biomass. Means are represented ± SE.
Differences between seasons were tested with Mann-Whitney test (M-W test). Biomass
was estimated by multiplying the surface availability by the mean individual biomass of
each prey in each season (obtained from core sampling).
Surface availability (indiv./m2) Biomass (mg of AFDW/m
2)
Winter
(n=17)
Spring
(n=56) M-W test Winter Spring
H. diversicolor 0.4 ± 0.4 6.4 ± 2.2 U=354
p<0.05 1.2 ± 1.2 53.4 ± 19.2
Siphons of S.
plana 1.1 ± 0.7 13.7 ± 3.1
U=201
p<0.001 3.2 ± 1.9 32.3 ± 7.2
Energy intake rates of dunlins
In spring dunlins achieved energy intake rates 65% higher than wintering birds (Figure
2.4; Mann-Whitney test: U=1877, p<0.001). In winter, whole S. plana was clearly the main
source of energy whereas H. diversicolor was the least important. In contrast, in spring H.
diversicolor contributed the most energy while whole S. plana played a relatively minor role
(Figure 2.4).
Figure 2.4. Mean energy intake rates achieved by foraging dunlins in winter and spring
(J/min). Relative contribution of different prey is shown, as percentage. Error bars
represent the SE for pooled prey.
0
50
100
150
200
250
300
350
400
Winter (n=99) Spring (n=56)
En
erg
y i
nta
ke r
ate
(J/
min
)
H. diversicolor
Siphons
S. plana
C. crangon
H. ulvae22%
62%
13%
2%
65%
12%4%
19%
1%
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
61
2.5. Discussion
Foraging behaviour and diet of wintering and northward migrating dunlins
In this study we found clear differences between the foraging behaviours and diets of
the Dunlin populations wintering in the Tagus estuary and those using it in spring, during their
northward migration. In winter, birds predominantly adopted a tactile foraging technique
(probing), mainly used to search for juvenile S. plana. The lower step rate observed during this
period results from the prolonged searching times associated with the probing technique
(Nehls and Tiedemann 1993). Visual methods (superficial pecking) were also used in winter, to
collect the gastropod H. ulvae and siphons of adult S. plana. In contrast, in spring dunlins
generally used a visual foraging strategy (superficial pecking and sweeps), mostly to consume
H. diversicolor, but also S. plana siphons and C. crangon. The higher step rate of foraging birds,
observed in spring, is characteristic of visual techniques, as it increases the encounter rate and
capture success of retractable items available at the surface (Zwarts and Esselink 1989).
Diet composition of dunlins recorded in this study is mostly in accordance with other
studies in northern and southern European estuaries. In fact, the prey most frequently
reported in the literature include polychaetes (mainly H. diversicolor but also Nephtys sp. and
other taxa), bivalves (S. plana, Cerastoderma edule and Macoma baltica) and the widespread
and abundant gastropod H. ulvae (Davidson 1971; Goss-Custard et al. 1977; Ferns and Worrall
1984; Worrall 1984; Durell and Kelly 1990; Moreira 1995a; Lopes et al. 1998; Santos et al.
2005). Seasonal shifts in dietary regimes have been previously described for dunlins, namely
the higher predation upon H. diversicolor and crustaceans (like C. crangon) during migratory
periods (Nehls and Tiedemann 1993; Dierschke et al. 1999). In particular, the increase of H.
diversicolor consumption between winter and spring, concurrently with a decrease in the
intake of gastropods and bivalves, observed in our study, were previously reported by Worral
(1984) and Moreira (1995a).
The influence of seasonal variation in food availability in the diet and foraging behaviour of
dunlins
In this study we found a substantial increase in the harvestable prey biomass for waders
from winter to spring, as described in previous studies carried out in temperate estuaries
(Zwarts 1991; Zwarts and Wanink 1993). This variation resulted from a combined effect of
increased densities (siphons of S. plana) and larger size of individual prey (in juvenile S. plana
and H. diversicolor).
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
62
We found a very marked seasonal increase in the surface availability of S. plana siphons
and H. diversicolor (12.5x and 15.3x, respectively), mostly due to a much higher surface activity
in spring, and to lesser extent to variation in densities, which increased quite modestly (only
2.0x and 1.2x, respectively). Our study revealed important seasonal variations in surface
behaviour in these two species, which imply a higher exposition to predation by birds. The
increase in activity probably resulted from a higher prevalence of deposit feeding mode in S.
plana (Zwarts and Wanink 1989) and an intensification of foraging activity of H. diversicolor,
due to higher temperatures (Esselink and Zwarts 1989).
These observations pooled together strongly suggest that seasonal variations in biomass
and activity of invertebrate key prey played a critical role in shaping the diet and foraging
behaviour of wintering and northward migrating dunlins; feeding opportunities were much
greater for the latter. The combined effect of the seasonal increase in surface activity and
individual size of H. diversicolor resulted in a very strong surge in their biomass available at the
sediment surface, certainly changing their profitability in relation to other prey. The shrimp C.
crangon also represented an important addition to the diet of northward migrating dunlins,
contributing with 19% of the total energy intake, despite its low abundance and modest
contribution to the overall available biomass (ca. 1%). The apparent preference for this prey
seems to be mainly explained by their high individual energetic content (Nehls and Tiedemann
1993; Viegas et al. 2007) (Table 2.2).
The spring increase in the availability of H. diversicolor, S. plana siphons and C. crangon at
the sediment surface and its water film was likely responsible for the visual feeding behaviour
observed in northward migrating dunlins, as these prey represented ca. 96% of both the
consumed prey and energy intake rates in this season (Figure 2.4).
Our results support the idea that dunlins have a high foraging plasticity, efficiently
exploiting a wide range of food resources while aiming at the most profitable prey. In this
context, it should be noted that the dietary changes observed in our study do not seem to be a
consequence of a decline in the availability of the prey preferred during the winter towards
spring. Indeed, the preferred prey in winter (H. ulvae, S. plana and siphons) were mainly
ignored by dunlins in spring, although their abundance remained stable or even increased.
Dunlins are well adapted to tactile predation, holding high densities of sensory pits in the bill
(Nebel et al. 2005). Nonetheless, evidence from studies comparing daytime and night-time
foraging behaviour of dunlins suggests that visual predation tends to be the preferred foraging
mode whenever conditions allow birds to use visual clues (Mouritsen 1993; Lourenço et al.
2008; Santos et al. 2010b), as found in our study.
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
63
Energy intakes and stopover importance of the Tagus estuary
In the Tagus estuary, northward migrating dunlins do not seem to be more constrained
by feeding resources in relation to wintering birds. Due to higher prey availability at the
sediment surface in spring, migrating birds achieved energy intake rates that were 65% higher
than those wintering in the same estuary (353 J/min and 213 J/min, in spring and winter,
respectively). But is this increment likely to meet the high energy demands of migrating birds
(van de Kam et al. 2004) and is it enough to allow for a quickly refuelling?
Dunlins have an average body mass of 46 g and an estimated daily energy expenditure
(DEE) in the temperate zone of ca. 139 Kj/day (assuming that DEE corresponds to 3x the basal
metabolic rate; Kersten and Piersma 1987). This requires a gross intake of 163 Kj/day,
assuming a digestive efficiency of 85% (Kersten and Piersma 1987). As dunlins in the Tagus
estuary forage moving through the intertidal mudflats since the higher areas exposed until
they cover again (Granadeiro et al. 2006), they are able to feed for 7.5 h/tide. Therefore,
wintering dunlins at the intake rate of 213 J/min (estimated in this study) obtain ca. 96 Kj in
each diurnal tide, which corresponds to 59% of their daily requirements. Nocturnal energy
intake rates are not known but dunlins are well adapted to tactile feeding (Nebel et al. 2005)
and usually forage at night (Mouritsen 1994; Lourenço et al. 2008; Santos et al. 2010b).
Therefore, it is likely that they are able to obtain a significant part of their energy requirements
during the night, as found in others waders wintering in the Tagus estuary (Lourenço et al.
2008). To fulfil their daily energy requirements (assuming similar diurnal and nocturnal intakes
rates), they would need to forage for 4.5 h of the 7.5 h of sediment exposure during a typical
night time tidal cycle. Therefore, it seems that wintering dunlins can fulfil their energetic
requirements in the intertidal area, and thus do not need to feed in supratidal areas during
high-tide periods, such as the saltpans where they usually roost during these periods (Luis et
al. 2002; Rosa et al. 2006).
The energy requirements of dunlins during northward migration are poorly known, as
fattening rates vary according to their migration strategies and schedules (Goede et al. 1990;
Zwarts et al. 1990b). The maximum theoretic and empirical rates of weight gain calculated for
most waders are around 4-5% of weight gain per day (Zwarts et al. 1990b) and the highest
rates obtained by dunlins in stopover areas are ca. 3.9% (Steventon 1977). Fattening rates of
this magnitude correspond to a weight gain of 1.8 g/day in dunlins, requiring an additional 82
Kj above maintenance levels, i.e. a total of 245 Kj/day (considering that each g of weight gain
requires 45.7 Kj/day above maintenance costs; Kersten and Piersma 1987). Assuming the
intake rate estimated for migrating dunlins in this study (353 J/min), birds can obtain about
159 Kj during diurnal tides. Therefore, to achieve the highest fattening rates during stopover,
Chapter 2. Seasonal variations in the diet and foraging behaviour of dunlins in a South European estuary
64
dunlins need an extra 86 Kj each night (245-159 Kj), or only 4.1 h/day of nocturnal feeding (out
of 7.5 h). This value is less than that required by wintering birds to fulfil their energy
requirements. These crude estimations suggest that the activity budgets of northward
migrating dunlins are quite similar to those of wintering birds and therefore they seem to be
able to achieve high fattening rates in the intertidal areas of the Tagus estuary, without the
need to feed during high tide. In fact, shorebird fattening rates in temperate areas tend to be
higher than in the tropics (Steventon 1977; Pienkowski et al. 1979; Goede et al. 1990; Zwarts
et al. 1990b; Piersma et al. 2005), due to the seasonal peaks in food availability, which are
typical of temperate areas (Wolff and Smit 1990; Zwarts 1991; Piersma et al. 1993a; Zwarts
and Wanink 1993; Scheiffarth and Nehls 1997) and are coincident with migratory periods (this
study, Zwarts et al. 1992).
Migratory wader populations are suffering a global decline (IWSG 2003) and the success
of their migration relies on a network of high-quality stopover sites in-between breeding and
wintering areas (Baker et al. 2004; van Gils et al. 2005; Smith et al. 2012), where they can
rapidly rebuild their condition and pursue their journey. The available evidence from regular
wader counts suggests that the Tagus estuary plays a critical role as a stopover area for
thousands of birds within the East Atlantic Flyway (Delany et al. 2009; Catry et al. 2011),
representing an important link between the wetland-rich northwestern Europe and the distant
(albeit very large) wintering areas of the western coast of Africa, such as the Banc d’Arguin
(Mauritania) and Guinea-Bissau. Our results indicate that Tagus estuary provides high-quality
feeding areas for dunlins and probably other waders during northward migration. The long-
term deterioration of feeding conditions for waders in stopover sites can cause changes in
their migratory paths and timings (Verkuil et al. 2012) and consequently adversely affect the
reproductive success of individuals (Baker et al. 2004), through carry-over effects. From a
conservation stand-point it is crucial that large-scale impacting activities (such as extensive
sediment dredging or reworking, infrastructure expansion into intertidal areas, roost/habitat
degradation or over-shellfishing) are carefully controlled, to ensure that the quality of feeding
conditions for migratory waders is not affected in this internationally important wetland.
65
CHAPTER 3
Contrasting estuary-scale distribution
of wintering and migrating waders:
the potential role of fear
Martins, R. C., T. Catry, R. Rebelo, S. Pardal, J. M. Palmeirim & J. P. Granadeiro
Manuscript submitted to Hydrobiologia
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
67
3. Contrasting estuary-scale distribution of wintering and
migrating waders: the potential role of fear
3.1. Abstract
In estuaries hosting both wintering and migrating populations of waders of the same
species, the distinct ecological constraints of these birds may result in different criteria to
select foraging habitats. We analysed the distribution patterns of dunlins Calidris alpina in the
Tagus estuary, Portugal, during the non-breeding season and investigated the roles of prey
availability and predation risk to explain those patterns. The narrower flats of the southern
estuary may induce greater fear of predation in waders than the open northern flats, although
our data suggests that the real risk was similar. Prey availability was lower in the northern
estuary. Migrating birds avoided the southern estuary, favouring areas perceived as safer over
better feeding opportunities. In contrast, wintering dunlins favoured the southern flats,
despite their proximity to cover. Presumably, wintering waders have a better knowledge of the
estuary, including its real predation risks, taking advantage of the best foraging areas. Without
such knowledge, waders in short stopovers have to base their choice of foraging areas on
indirect indicators of predation risk, such as distance to cover. This study illustrates the
importance of incorporating specificities of habitat preferences by wintering and migrating
wader populations in conservation planning for large estuaries.
3.2. Introduction
The intertidal flats of many temperate and sub-tropical estuaries are of prime
importance for millions of waders that use them as foraging grounds during the non-breeding
season. In these habitats waders feed on benthic macro-invertebrates, which have patchy
distributions determined by physical and chemical characteristics of the sediment (e.g.
Rodrigues et al. 2006). Prey availability is a key factor determining the large-scale distribution
of waders in estuarine and costal environments during the non-breeding season (Goss-Custard
et al. 1977; Piersma et al. 1994; Kelly 2001; Harrington et al. 2010). However, waders are also
very responsive to the presence of aerial predators, which influences their preferences of
foraging and roosting areas (Ydenberg et al. 2004), as well as their behaviour (Cresswell and
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
68
Whitfield 1994). Therefore, fear of predation is also important in shaping site-selection by
waders at both estuary (e.g. Yasué 2006; Sprague et al. 2008; Ydenberg et al. 2010) and flyway-
scales (Lank et al. 2003; Nebel and Ydenberg 2005). Despite the potentially high mortality
caused by raptors on waders (Whitfield 1985; Cresswell and Whitfield 1994), predation
impacts their distribution mostly through non-lethal effects (Cresswell 2008), such as
behavioural and physiological (e.g. stress) responses induced by the perception of predation
risk (e.g. Barbosa 1997; Michaelsen and Byrkjedal 2002).
Intertidal areas with higher food availability are often more dangerous (Pomeroy 2006;
Pomeroy et al. 2008) and this trade-off between food and safety can promote state-dependent
choices. Therefore, groups of individuals within a given species may show disparate
preferences according, for instance, to age/experience (Dierschke 1998; van den Hout et al.
2014), escape performance (Ydenberg et al. 2002; Nebel and Ydenberg 2005) and starvation
risk (Hilton et al. 1999). In areas where wintering and migrating waders congregate, i.e. in
estuaries acting both as wintering and stopover areas, different population segments of the
same species may show distinct decisions regarding such balance. Migrating birds may
primarily select richer foraging areas during stopover (Ydenberg et al. 2002) to replenish their
fat stores before resuming migration (van de Kam et al. 2004), but they are strongly
constrained by time and usually stay for short periods in stopover areas (e.g. Warnock et al.
2004). As a consequence, migrants have less time to gather knowledge on local habitat
characteristics (Yasué 2006; Sprague et al. 2008) than wintering birds that spend the full winter
in the same wetland. Therefore, during migration birds are expected to select foraging habitats
at a larger (landscape) scale (Farmer and Parent 1997; Albanese et al. 2012) based on general
rules related with perceived predation risk (Lima 1998; Rogers 2003; Pomeroy et al. 2006;
Sprague et al. 2008). The presence of shoreline vegetation, which may promote cover that
facilitates surprise attacks from aerial predators, is one such factor. Empirical evidence
demonstrated that in foraging waders shorter distances to cover are often associated with
high real or perceived predation risk, potentially affecting spatial distribution of both wintering
(Dekker and Ydenberg 2004; van den Hout et al. 2008; Cresswell et al. 2010) and migrating
birds (Ydenberg et al. 2004; Pomeroy et al. 2008; Sprague et al. 2008) whithin an estuary.
The Tagus estuary in the western coast of Portugal holds internationally important
numbers of several species of waders using the East Atlantic Flyway, both during winter and
migratory periods (Delany et al. 2009; Catry et al. 2011; Catry et al. 2012a). Recent studies
reported significant seasonal variation in the spatial distribution of waders in the estuary:
during the winter birds are dispersed across the entire estuary, whereas in autumn and spring
they are mostly concentrated in its northern half (Alves et al. 2011; Catry et al. 2011; Alves et
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
69
al. 2015). This pattern is particularly clear in the Dunlin Calidris alpina, the most abundant
species in the Tagus estuary, which was selected as our model species.
There are two groups of dunlins using this estuary: the wintering population, including
mainly birds that breed in Scandinavia (Lopes et al. 2006; Delany et al. 2009), and passage
migrants, thought to belong mostly to the Icelandic-Mauritanian population (Delany et al.
2009; Catry et al. 2012a). These two groups co-occur in the estuary during the transitions
between winter and migratory periods. It is thus difficult to determine if the observed seasonal
variations in dunlin numbers in different parts of the estuary are mostly due to shifts in the
areas used by the same birds or to different preferences of the two groups. The driving factors
of such large-scale changes in the distribution of waders in the Tagus estuary remain unknown,
even though this phenomenon has important implications for management and conservation.
In this study, we first examine the magnitude of the differences between winter and
migratory periods in the large-scale distribution of dunlins in the Tagus estuary and clarify if
these patterns can be attributed to different preferences of wintering and migrating dunlin
populations. Secondly, we investigate the potential roles of food availability and predation risk
to explain the spatial distribution of those birds and interpret them in light of their distinct
ecological contexts.
3.3. Materials and methods
Study area
This study was carried out in the Tagus estuary, Portugal (38°45’N, 9°00’W; Figure 3.1),
which comprises an intertidal area of ca. 97 km2, largely dominated by mudflats, but also
including oyster beds and sandy flats (Granadeiro et al. 2007). For the purposes of this study
we consider the estuary divided in two sections, corresponding roughly to its northern and
southern halves (Figure 3.1). The northern sector comprises large and open intertidal mudflats
(ca. 71 km2), mainly surrounded by wide saltmarshes, saltpans and agricultural fields. In
contrast, the southern sector encompasses smaller mudflats in enclosed bays (totalizing ca. 26
km2), surrounded by narrower saltmarshes and a stronger human occupation (INE 2011). As a
consequence of these differences, mudflats in the southern sector are usually much closer to
the coast line than in the upper estuary (Figure 3.1). A significant part of the Tagus estuary is
under legal protection, due to the Nature Reserve (RNET) and a Special Protected Area (SPA),
but these are almost exclusively in the northern sector (Figure 3.1).
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
70
Figure 3.1. Map of the Tagus estuary showing the northern and southern sectors
considered in this study. Intertidal areas (in spring low-tides) are shown from light to dark
grey according with increasing distances to coast, in 400 m bands.
Seasonal variation in the spatial distribution of dunlins
We analysed monthly counts of waders in the main high-tide roosts of the estuary
between 2007 and 2011 (data compiled from Alves et al. 2010a; Alves et al. 2011; Catry et al.
2011; Alves et al. 2015) to compare year-round dunlin abundance in northern and southern
sectors of the Tagus estuary. The approximate densities of birds using intertidal foraging areas
were estimated by dividing the number of birds counted in the high-tide roost counts in each
sector by the total area of mud to muddy-sand sediments (ca. 54 km2 and 18 km2 for the
northern and southern sectors, respectively). These types of sediments are positively selected
by dunlins in the Tagus estuary (Santos et al. 2005; Granadeiro et al. 2007).
In order to interpret correctly seasonal variations in distributional patterns we
contributed to clarify to which extent wintering birds co-occur with northward migrants in the
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
71
estuary in late winter / early spring. To do so we estimated the departure dates of wintering
dunlins from the estuary and interpreted them against the variation of bird abundance in that
period. To estimate the departure dates of wintering dunlins and detect possible differences
between birds from northern and southern sectors of the estuary we used radio-tracking.
Between 1 and 19 March 2011, 14 and 16 dunlins were captured by crossbow-netting (Martins
et al. 2014) in the northern and southern sectors of the estuary, respectively, and fitted with
VHF radio transmitters (Biotrack, UK). Tags weighing 1.5 g were fixed to back feathers with
super-glue (Warnock and Warnock 1993), and represented on average 3.1% of birds’ body
mass (range: 2.4-3.7%). Radio-marked dunlins belonged to the local wintering population,
given that passage migrants are virtually absent from the estuary in the first half of March
(Catry et al. 2012a). Between 21 of March and 26 of April all roost sites in both sectors of the
estuary were screened for tag presence every three days. Scans were carried out by two
observers using two-element portable yagi antennas and receivers (Telonics, USA), within ± 2 h
of high water. Birds were tracked at their roosts rather than at the intertidal foraging areas
because the latter are often too distant from the coast line to allow radio-tracking. However,
there is strong evidence that the great majority of dunlins forage close to their roosting sites
(Dias et al. 2006; authors’ unpublished data). Therefore, we assumed that radio-tagged birds
usually foraged in the sector of the estuary where they were detected while roosting during
high-tide. Battery life of transmitters surpasses seven weeks, largely exceeding the maximum
period between tag deployment and signal disappearance from the estuary.
Food availability
Abundance of invertebrate species known to be important prey for dunlin (Santos et al.
2005; Martins et al. 2013) was estimated in the north and south sectors of the estuary, in both
winter and spring. In winter we used data from two sampling schemes involving the collection
of sediment cores (86.6 cm2, 30 cm deep) in early March of 2010 (for details see Catry et al.
2012b; Martins et al. 2013). We analysed a total of 110 cores from three stations in the north
of the estuary and 40 cores from four stations in the south (Figure 3.1). In spring (mid-April
2011), two stations were defined in mudflats used by foraging dunlins of both sectors of the
estuary (Figure 3.1) and 15 cores were collected in each station. The upper (<5 cm deep) and
lower (5-30 cm) fractions of cores were sieved through 0.5 and 1 mm mesh size, respectively.
All prey were immediately preserved in alcohol 70% and later identified and counted in the
laboratory. We estimated the size of at least 30 individuals per species, randomly selected
from samples from each sector of the estuary. Published relationships between structural size
and biomass (see Martins et al. 2013) were then used to estimate available prey biomass (in
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
72
ash free dry mass). To quantify the biomass available for dunlins, we included all invertebrates
present in the upper 5 cm of core samples, with the exception of bivalves and polychaetes
larger than 13 and 66 mm, respectively, which are too large to be consumed by the species
(Santos et al. 2005). In addition, we included all polychaetes smaller than 66 mm and the
siphons of bivalves in the lower portion of the core, because they are active at the sediment
surface and are thus accessible (Moreira 1995a; Santos et al. 2005; Martins et al. 2013).
Predation risk
We estimated predator presence during the winter of 2010/2011 (Nov-Mar) by
conducting nine 2-h observation periods to count raptors and record dunlin behaviour during
high-tide at each of three refuges: Vasa Sacos, in the northern sector, and Alhos Vedros and
Seixal in the southern sector (Figure 3.1). Vasa Sacos is an old saltpan complex that harboured
an average of ca. 3000 dunlins in the winter of 2010-2011, representing 50% of the dunlins
present in the northern sector of the estuary in that period (Alves et al. 2011; Alves et al.
2015). Alhos Vedros and Seixal are refuges in saltmarsh and held on average ca. 1500 and 700
dunlins, respectively, during the winter of 2010-2011, representing 44% of the dunlins in the
southern sector (Alves et al. 2011; Alves et al. 2015). Observations took place at roosting sites
given that aerial predators tend to concentrate their activity near the high-tide periods (e.g.
Dekker and Ydenberg 2004) and we considered predation risk at high-tide roosts as a proxy for
the risk in adjacent intertidal areas.
During each observation period we recorded the following parameters: (1) number and
identity of all raptors flying over the roost; (2) number of alarm flights caused by raptors, i.e.
all situations when more than 25% of the dunlins present in the roost suddenly flew, even if
they returned to the original location; (3) proportion of dunlins in vigilance behaviour. For the
latter, we randomly selected flocks of 100-200 dunlins (mean= 170), once every 30 minutes in
each observation period, and counted the number of birds with raised head (scanning, as a
proxy of vigilance behaviour) and those with bill under the wing (sleeping), using a telescope
(20-60x).
We did not quantify predation risk and associated dunlin behaviour in spring because
bird abundance in the southern area of the estuary was very low during this season (see
results) which generally results in a decrease in the local abundance of predators (Cresswell
and Whitfield 1994; Sprague et al. 2008).
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
73
Statistical analyses
We used generalized linear mixed models (GLMM) to compare densities of dunlins in
both sectors of the estuary in three different periods (Autumn Migration: July-September;
Winter: November-February; Spring Migration: April-May), between 2007 and 2011. To
account for temporal correlation among counts carried out in successive months (within the
same year) we defined a random factor to compute these variance components separately. To
compare the rate at which radio-tagged birds left the estuary as the season progressed, we
used a cox-proportional hazard model. This type of survival analysis has the advantage of not
requiring the baseline survival function to be defined a priori, as the parameter estimation can
be solved for any arbitrary hazard function (Pollock et al. 1989). This fact, together with the
analytical simplicity, makes this method particularly suited for analyzing the effects of
covariates on hazard functions. We modeled bird departures between 21 March (after all birds
were already tagged) and 27 April 2011 (when no more tags could be detected in the estuary)
and we used the sector (northern and southern) as a fixed factor. All calculations were carried
out with the library “survival” (Therneau 2014), running under R software (R Core Team 2013).
We used Mann-Whitney tests to analyse statistical differences between the two sectors of the
estuary in terms of invertebrate availability, numbers of raptors/h in roosts and dunlin
behaviour, given that this data failed to meet the assumptions of normality and
homocedasticity (even after transformation).
3.4. Results
Seasonal variation in the spatial distribution of dunlins
The analyses of the monthly counts carried out between 2007 and 2011 in the Tagus
estuary revealed a clear temporal variation in the spatial distribution of dunlins at the
estuarine scale (Figure 3.2). During winter (November-February) the total number of dunlins is
similar in the northern and southern sectors of the estuary (ca. 4000 individuals), while in
autumn and spring birds are mostly concentrated in the northern sector (Figure 3.2A). When
these numbers are expressed as densities (i.e., in relation to the foraging area available in each
sector of the estuary, Figure 3.2B) it becomes clear that the southern flats support a
significantly higher density of foraging birds in winter whereas the northern sector show
higher densities during the spring and autumn migratory periods (GLMM: interaction between
area and phase of the year cycle: F2,24= 40.8, p< 0.001).
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
74
Figure 3.2. Seasonal variation in (A) the mean abundance of dunlins counted in high-tide
roosts of the northern and southern sectors of the Tagus estuary between 2007 and 2011
and (B) the expected density of birds in northern and southern foraging areas. Vertical
lines represent SE. Data sources: Alves et al. (2010a; 2011; 2015) and Catry et al. (2011).
Radio-tracking data showed a fairly regular departure of wintering dunlins from the
estuary between late March and late April, with no significant differences in departure rates
between sectors (effect of sector: Z= 0.191, p= 0.85; Figure 3.3). Overall, 90% (27/30) of radio-
tagged birds departed for migration directly from the sector of estuary where they were
captured.
Figure 3.3. Variation in the proportion of wintering radio-tagged dunlins from the
northern (n=14) and southern (n=16) sectors of the Tagus estuary detected in a systematic
monitoring scheme through the estuary during the pre-migration period (21st
March – 26th
April 2011).
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18-A
pr
20-A
pr
22-A
pr
24-A
pr
26-A
pr
Pro
po
rtio
n o
f b
ird
s
Northern birds
Southern birds
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
75
Food availability
The southern sector of the estuary had significantly higher biomass of invertebrate prey
harvestable for dunlins than the northern sector, both in winter (M-W test: U=1407, p<0.001)
and spring (M-W test: U= 95, p< 0.001) (Figure 3.4). The polychaete Hediste diversicolor
comprised the majority of the total biomass and showed significant differences between
estuary sectors (higher in the south), in both seasons (M-W tests: U= 1698.5, p< 0.05 in winter
and U= 215, p< 0.001 in spring). In the southern sector the available biomass of the gastropod
Hydrobia ulvae was higher in winter (M-W test: U= 969.5, p< 0.001), while that of the bivalve
Scrobicularia plana was higher in spring (M-W test: U= 86, p< 0.001) (Figure 3.4).
Figure 3.4. Comparison of prey biomass availability (Ash Free Dry Weight /m2) between
northern and southern sectors of the estuary during winter (A) and spring (B). Significant
differences between sectors are presented for each prey (Mann-Whitney tests; * p<0.05;
*** p<0.001). The number of core samples (n) is presented for each sector and season.
Predation risk
Seven raptor species were observed flying over wader roosts during high-tide in winter,
but only four species caused alarm flights in dunlins (Table 3.1). Marsh Harriers Circus
aeruginosus and Peregrine Falcons Falco peregrinus were the most frequent predators in
roosts (Table 3.1), causing alarm flights on 64% (n= 14) and 100% (n= 5) of their roost visits,
respectively. The number of raptors visiting roost sites was marginally higher in the northern
sector, both considering all raptors or only those species that caused dunlins’ alarm flights
(Table 3.1; M-W tests: U= 115.5, p= 0.063 and U= 116.5, p= 0.052, respectively). Marsh harrier
was the only raptor showing significant differences between sectors (M-W test: U= 127.5,
p< 0.01; Table 3.1), being more frequent in the northern sector.
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
North (n=110)
South (n=40)
Bio
mas
s (g
of A
FD
W/m
2) H. ulvae***
Siphons
S. plana
H. diversicolor*
0
2
4
6
8
10
12
14
16
18
20
North (n=30)
South (n=30)
H. ulvae
Siphons***
S. plana***
H. diversicolor***
A B
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
76
Table 3.1. Number of raptors per hour (mean ± SE) flying over roost-sites of the northern
and southern sectors of the estuary in winter (n= total observation time).
Species North
(n=16.6 h)
South
(n=35.3 h)
Marsh Harrier Circus aeruginosus a 0.56 ± 0.13 0.17 ± 0.10
Peregrine Falcon Falco peregrinus a 0.06 ± 0.06 0.15 ± 0.09
Common Kestrel Falco tinnunculus a 0.06 ± 0.06 0.07 ± 0.05
Osprey Pandion haliaetus a 0 0.03 ± 0.03
Hen Harrier Circus cyaneus 0.06 ± 0.06 0
Black Kite Milvus migrans 0.06 ± 0.06 0
Common Buzzard Buteo buteo 0 0.03 ± 0.03
Species that caused alarm-flights (a) 0.68 ± 0.18 0.42 ± 0.23
All species 0.79 ± 0.22 0.45 ± 0.23 a Raptor species triggering alarm flights of dunlin flocks
The frequency of alarm flights caused by raptors did not differ between the two sectors
(M-W test: U= 98.5, p= 0.297; Figure 3.5A), but dunlins were found to be more vigilant in
northern than southern roosts (M-W tests for scanning and sleeping behaviours: U= 1506,
p< 0.05 and U= 599, p< 0.001, respectively; Figure 3.5B). None of the observed predator
attacks was successful.
Figure 3.5. Comparison of dunlin behaviour in roosting sites of the northern and southern
sectors of the Tagus estuary in winter: (A) frequency of alarm flights (number of flights per
hour) of dunlin flocks disturbed by raptors (n= total observation time) and (B) proportion
of birds in sleeping and scanning behaviour (n= number of observations). Vertical lines
represent SE. Differences between sectors were tested with Mann-Whitney tests for these
three parameters (* p<0.05; *** p<0.001).
0%
20%
40%
60%
80%
100%
North (n=33)
South (n=70)
Sleeping***Scanning*
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
North (n=16.6h)
South (n=35.3h)
Ala
rm f
ligh
ts /
h
A B
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
77
Although we could not assess predation risk during spring, non-systematic data on
predator occurrence in three of the most important high-tide roosts of the Tagus estuary
collected in April-May of 2009-2011 suggest that the southern sector does not hold more
predators than the northern area during spring (0.40 raptors/h in northern roosts vs 0.29
raptors/h in southern roosts; n= 8.25 and 8.17 h of observation, respectively; R. Martins, T.
Catry and P. Fernandes, unpublished data).
3.5. Discussion
Distribution of wintering and migrating dunlins
In this study we demonstrated that the broad distribution of dunlins in the Tagus
estuary shows a predictable variation along the non-breeding period (July to May). While in
winter the dunlin population is roughly equally divided between northern and southern
sectors of the estuary, during both autumn and spring migration periods dunlin numbers are
much greater in the northern sector (Moreira 1995a; Alves et al. 2010a; Alves et al. 2011; Catry
et al. 2011; Alves et al. 2015). Furthermore, the analysis of bird densities in foraging areas
(instead of number of birds) showed that in winter dunlins are not evenly distributed,
suggesting that they prefer the southern sector.
Radio-tracking results showed that by mid-April, when the number of birds in the
northern sector usually peaks (Figure 3.2), most of the wintering population already left the
estuary. This is true for both birds that wintered in the north and south sectors. Consequently,
the high abundance of birds observed at this time of the year in the northern sectors cannot
be explained by a concentration of wintering birds. Therefore, that increase can only be
explained by a strong preference for that area by incoming migrants.
Although we have not confirmed if the variation in numbers observed in Summer-
Autumn also corresponds mostly to a distinct site-selection by migrating dunlins, there is
evidence pointing in that direction. Dunlins that winter in the Tagus estuary are thought to
arrive only after September (Lopes et al. 2006), which mean that birds using the northern
estuary from July to September (ca. 3000-6000) are mostly in migration towards their NW-
African wintering areas. On the other hand, the increase in dunlin numbers in the southern
sector begins in late October/early November, which coincides with the expected arrival of the
birds that winter at the Tagus estuary.
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
78
The roles of food availability and predation risk in the distribution of dunlins
Previous studies reporting differences (unrelated with age or sex) in the spatial
distribution of distinct populations of a wader species within an estuary (or landscape)
explained such patterns with factors like specialization on different prey (Alves et al. 2010b;
Harrington et al. 2010), avoidance of foraging competition (Cohen et al. 2010) or temporal and
spatial variations in invertebrate availability (Piersma et al. 1994).
In the Tagus estuary, southern intertidal mudflats provide more food for dunlins than
the northern ones, both in winter and spring, so food availability cannot explain the
contrasting spatial distribution between wintering and migrating dunlin populations. While
wintering birds occurred at higher densities where food is more abundant, spring migrants did
not take advantage of the better feeding opportunities available in the southern sector. One
may argue that food available in the northern areas of the estuary is sufficient to sustain the
high fattening rates required by migrants, as suggested in another study (Martins et al. 2013).
This might indicate that these birds are not forced to find other foraging areas in the estuary,
but it does not explain the fact that they clearly avoided the southern sector.
Predation risk is an alternative explanation to justify the differences in the selection of
north and south sectors of the estuary by spring migrants, but we did not find any evidence of
major differences in predation risk between the two sectors. If anything, there is a slight
indication that birds in the north sector, where migrants concentrate, are under a stronger
predatory pressure. This indicates that the avoidance of the southern estuary by migrants may
not be related to actual predation risk.
Birds can evaluate predator abundance and the frequency of attacks and change their
behaviour accordingly (Cresswell and Whitfield 1994), but the exact magnitude of the risk of
predation is difficult to assess (Lima and Dill 1990). Therefore, animals often have to make
decisions based on the perception of predation risk, which may be substantially different from
the actual existing risks (Cresswell 2008). This perception (or the fear of predation) can be
mediated by habitat characteristics, such as the distance to potential cover for predators
(Lindstrom 1990; Lima 1998; Cresswell 2008). Previous studies found evidence that the
perceived risk of predation is an important determinant of stopover site selection in migrating
waders (e.g. Sprague et al. 2008). Some species avoid to forage in areas close to shore (e.g.
Pomeroy et al. 2006) and may even skip small potential stopover sites along migratory routes
due to the high edge effect of such sites (Ydenberg et al. 2004; Taylor et al. 2007; Pomeroy et
al. 2008).
In the southern sector of the Tagus estuary, the narrower intertidal flats reduce the
distance between foraging areas and the shoreline, where vegetation and human-made
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
79
structures often limit the visual field of wading birds. They may thus perceive that these areas
entail a greater risk of attack by aerial predators than areas in the northern estuary. There is
therefore a trade-off between food availability and perceived predation risk, and ultimately
migrant dunlins seem to choose the minimization of predation risk. In avoiding areas with
higher perceived predation risk, they actually fail to take advantage of the best feeding
opportunities provided by southern areas, a phenomenon that is similar to that observed in
other studies (e.g. Sprague et al. 2008).
If the perception of predation risk shapes the distribution of migrant dunlins to the point
of overlooking rich foraging areas, why does the same phenomenon not occur with wintering
birds? Two main hypotheses might be involved in explaining the difference. The first assumes a
possible mismatch between perceived and real predation risk (Pomeroy 2006; Cresswell 2008;
Sprague et al. 2008). The fact that wintering dunlins spend less time in vigilance in the
southern sector of the Tagus estuary and the tendency for higher raptor abundance in the
northern area support this idea. Wintering waders probably have a more accurate knowledge
of the estuary than migrants, as the former had more leeway to explore different areas in
terms of feeding opportunities (Shepherd and Lank 2004) and predation, enabling them to
assess whether risk-perception matches real risk (Lima and Dill 1990). In contrast, migrants are
particularly constrained by time when exploring stopover areas and thus less informed and
more compelled to be conservative in terms of predation risk (Sprague et al. 2008). Hence,
they are more prone to select their habitats at a broader landscape scale (Farmer and Parent
1997; Albanese et al. 2012) and rely on more general and less accurate rules based on the
perception of predation risk (Lima 1998; Rogers 2003; Pomeroy et al. 2006; Cresswell 2008).
Differences in body weight of wintering and migrating populations may also play a role
in explaining their contrasting spatial preferences. Spring migrants in stopover at the Tagus
estuary are generally heavier than wintering birds because they carry extra fat required for
migration (size-corrected mass 13% higher, on average; n= 353 and 324 birds in winter [Nov-
Feb] and spring [Apr-May], respectively; authors’ unpublished data). This extra weight may
reduce escape performance and consequently increase vulnerability to aerial predatory
attacks (Lank and Ydenberg 2003). Therefore, migrating dunlins are probably more vulnerable
to predation than wintering birds, making them less tolerant to predation risk (Ydenberg et al.
2002).
Implications for conservation
Most wader species are in decline worldwide (IWSG 2003) and maintaining a network of
good-quality stopover sites and wintering areas is key for the survival of most populations
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
80
(Baker et al. 2004; van de Kam et al. 2004). Virtually all major wetlands, like the Tagus estuary,
are under pressure due to land reclamation (e.g. Yang et al. 2011), direct human disturbance
(Rogers et al. 2006; Yasué 2006) and sea level rise (Galbraith et al. 2002). In this context, a
thorough understanding of the processes driving the spatial distribution of waders within a
wetland is very important to inform conservation action.
In this study we demonstrated that wintering and migrating populations of dunlins show
very distinct distributions within this large estuary, a pattern that has also been observed in
other wader species (Catry et al. 2011). A conservation concern rising from our results is that a
large proportion of the wader populations wintering at the Tagus estuary now reside in the
southern sector, i.e. outside protected areas. This insufficiency is presumably due to the fact
that the limits of the protected area were established without taking into consideration that
different wader populations may depend on distinct areas of the estuary. In any case, the
assumption that gazetting a substantial part of an estuary results in the protection of an
important proportion of the foraging areas of all the wader populations using the wetland
does not hold. In the studied case, migrating dunlins use mostly protected areas but roughly
half of the wintering population is particularly under pressure, as in the southern sector of
Tagus estuary mudflats are always close to the shore, much of which is occupied by urban
areas. Similar situations of conservation insufficiency may occur in other wetlands that act
both as wintering and stopover sites and includes large sectors without legal protection.
The fact that migrating dunlins concentrate almost only in the northern sector of the
estuary is also an issue of conservation concern; although the mudflats in the sector are vast,
waders usually depend on very few high tide roosting sites (e.g. a single roost held >80% of all
dunlins of the estuary in half of the migratory periods between 2007 and 2011; Catry et al.
2011). Although these roosts in the northern estuary are included in the SPA, they have been
affected by conversion of the original saltpans into fish or shrimp aquacultures (Dias et al.
2006; Catry et al. 2011). Finally, our results highlight the need to (1) extend the limits of the
actual SPA of Tagus estuary to include the main intertidal areas and roosting sites of the
southern sector, (2) take effective measures to contain urbanization and disturbance around
the foraging areas in the southern sector, and (3) to enhance the protection of high tide
roosting sites, especially in the northern sector. These measures would greatly benefit the
populations of multiple species of waders wintering and migrating along the East Atlantic
Flyway.
Chapter 3. Contrasting estuary-scale distribution of wintering and migrating waders: the potential role of fear
81
3.6. Conclusions
We confirmed that wintering and migrating waders of the same species can use
different criteria for selecting foraging habitat, within the same estuary. In fact, we concluded
that in the Tagus estuary the observed seasonal changes of abundance of dunlins in different
sectors of the wetland are explained by different habitat choices made by wintering and
passage migrants. These choices are different presumably because wintering waders, which
spend several months in the estuary each winter, have a better knowledge of the real
predation risk than the waders in stopover. The latter forego using the food rich areas of the
southern estuary because they perceive them as risky due to a generalized proximity to the
shoreline, where the vegetated margins can be used as cover by predators. They instead
concentrate in the less rich but wide open flats of the northern estuary. In contrast, wintering
birds learn from experience that, in spite of this cover, predation pressure is not any higher in
the south, so they prefer to forage on its prey rich flats. Therefore, our results confirm the
potential role of predation risk shaping the spatial distribution of waders in estuarine
environments and highlight the state-dependent character of the balance between food
abundance and fear of predation, as wintering and migrating dunlins, under distinct time and
energy constraints, used different criteria for selecting habitat within the same wetland.
Finally, this study illustrates the importance of incorporating specificities of habitat
preferences by wintering and migrating wader populations in conservation planning for large
estuaries.
83
CHAPTER 4
Discriminating geographic origins of migratory
waders at stopover sites: insights from stable
isotope analysis of toenails
Catry, T., R. C. Martins & J. P. Granadeiro. 2012
Journal of Avian Biology 43: 79-84
Chapter 4. Discriminating geographic origins of migratory waders at stopover sites: insights from isotope analysis
85
4. Discriminating geographic origins of migratory waders at
stopover sites: insights from stable isotope analysis of toenails
4.1. Abstract
In this study we test the potential of stable isotope analysis to reveal wintering origins of
waders mixing at stopover sites, using the Dunlin Calidris alpina as a case study. We
determined stable carbon (δ13C) and nitrogen (δ15N) isotope signatures of toenails of dunlins
captured during winter at reference sites along the East-Atlantic Flyway, from Mauritania to
the United Kingdom. Afterwards, during spring migration, dunlins were sampled at the Tagus
estuary, Portugal, and assigned to their wintering grounds according to their stable isotope
signatures. Toenails from wintering dunlins at different sites had significantly different δ13C
and δ15N signatures, despite some overlap in isotopic carbon ratios of birds from Morocco,
Portugal and the UK. Among birds sampled during migration in Portugal, we found a clear
bimodal pattern in δ13C values, corresponding to passage migrants from Mauritania (enriched
δ13C values) and wintering birds from the Tagus estuary (depleted δ13C values). The first
passage migrants from Mauritania appeared at the Tagus estuary by the end of March, with
peak numbers during late April and early May. Our study provides evidence that isotopic
signatures of toenails can play a determinant role in tracing the wintering origins of migrant
dunlins at their stopover areas. Toenails, instead of feathers, can be the powerful and
innovating tissue to sample in wader studies, allowing to bridge the gap in the field of
migratory connectivity between sites used in different phases of the life cycle of waders.
4.2. Introduction
Bird migration has always attracted scientific attention and the need to monitor
seasonal movements of individuals and populations has promoted the continuous
development of methods and techniques to investigate such behaviour (Wernham 2002).
Tracing the movement of birds allows a deeper understanding of connectivity among breeding,
wintering and stopover sites throughout migratory flyways, which has important ecological,
evolutionary and conservation implications (Webster et al. 2002). However, tracing the links
Chapter 4. Discriminating geographic origins of migratory waders at stopover sites: insights from isotope analysis
86
among these areas is particularly difficult in species that show both broad geographic
distribution and significant mixing among populations.
Waders perform some of the longest migratory flights amongst all birds and despite the
relatively narrow latitudinal span in breeding distributions, most species show extensive
wintering ranges and also use, along their migratory routes, numerous sites that act as
refuelling stops – stopover areas. Here, populations of different wintering and breeding origins
frequently overlap. In addition, several of these areas hold their own wintering populations
that mix with passage populations of the same species during migratory periods (Delany et al.
2009). Among waders, geographically distinct populations or subspecies are often difficult to
discriminate: morphological and plumage characteristics usually show extensive overlap,
ringing recoveries provide few and often biased data, and genetic markers often lack
discriminant power (Lopes et al. 2006). These circumstances prevent an accurate estimation
and interpretation of several migration-related parameters, such as migratory schedules of
different wader populations at their stopover areas.
Stable isotope analysis of bird tissues has been increasingly used to track movements of
birds across isotopic gradients and thus assess their breeding or wintering origins (Hobson
1999; Atkinson et al. 2005). The choice of chemical elements and tissues is crucial to achieve
the correct conclusions. Carbon and nitrogen have been mainly used to examine the relative
contribution of terrestrial and marine-derived nutrients (Hobson 1999). Amongst birds,
feathers and blood are the most commonly sampled tissues. Blood is a metabolically active
tissue yielding an isotopic record that represents a short temporal window ranging from days
to a few weeks from collection date (Hobson 1999). For this reason, blood is inappropriate to
trace origins and migration patterns of animals (Bearhop et al. 2002). Feathers, being
metabolically inert, show fixed signatures after synthesis (Hobson 1999) and thus provide
geographical information of the moulting grounds. However, for species such as waders, with
unknown or complex moulting cycles (showing suspended or arrested moult), feather isotopic
signatures are extremely difficult to interpret and can hardly provide accurate information on
the geographical origins of sampled individuals.
Recently, stable isotope signatures of avian toenails were successfully used to infer diet,
habitat use (Bearhop et al. 2003; Bearhop et al. 2004; Yohannes et al. 2010) and geographic
origins (Clark et al. 2006) of different species. Toenails possess two important attributes not
found in other avian tissues: they are metabolically inert but grow continuously and they
integrate information on the diet of birds over a medium temporal scale prior to sampling,
varying from weeks to few months (Bearhop et al. 2003). Therefore, toenails of migrants at
Chapter 4. Discriminating geographic origins of migratory waders at stopover sites: insights from isotope analysis
87
stopover sites will invariably yield information from their pre-migratory grounds (Bearhop et
al. 2003; Clark et al. 2006).
The Dunlin Calidris alpina is a migratory wader with a circumpolar breeding distribution
which winters along temperate and subtropical coastlines north of the equator (Delany et al.
2009). The Tagus estuary, Portugal, is one of the large European wetlands where wintering and
passage migrant dunlins mix during migratory periods (Catry et al. 2011). Wintering dunlins
include birds from the subspecies C. a. alpina (breeding mostly in northern Scandinavia) and C.
a. schinzii (belonging to Baltic and probably to British and Irish breeding populations; Lopes et
al. 2006; Delany et al. 2009). Spring migrants are thought to be mostly C. a. schinzii originating
from Mauritania, and travelling north to their breeding grounds in Iceland.
In this study we investigate the power of stable isotope analysis (in toenails) to unveil
the geographic origin of migratory dunlins at wetlands that act both as wintering and stopover
sites. We also examine migratory schedules of dunlins at the Tagus estuary during spring
migration in relation to phenological patterns described for the most important wintering
wetland for waders within the East Atlantic Flyway, the Banc d’Arguin, Mauritania (Piersma et
al. 1990).
4.3. Materials and methods
Sample collection
Dunlins were captured with mist-nets at Banc d’Arguin, Mauritania and Sidi Moussa,
Morocco, during the winter (December to February), and at the Tagus estuary, Portugal, during
both winter (as above) and spring periods (March to May; Table 4.1). We measured culmen
length (nearest 0.05 mm), wing length (nearest 1 mm) and body mass (nearest 0.5 g). Fat was
scored in a 0-8 scale according to Kaiser (1993) and muscle in a 0-3 scale following Bairlein
(1995).
Between 1 and 2 mm of nail were clipped from three to four toes of each bird using
sharp scissors and stored in individual plastic bags. Toenails were also obtained from 13 dunlin
specimens held at the Natural History Museum of London, collected during the winter at three
British estuarine areas (Table 4.1). These samples were meant to represent the isotopic
signature of dunlins wintering at the UK, to broaden the scope of our analysis within the East
Atlantic Flyway.
Chapter 4. Discriminating geographic origins of migratory waders at stopover sites: insights from isotope analysis
88
Table 4.1. Location, sampling period, number of capture events and number (n) of dunlins
sampled for stable isotope analysis. Numerical digits after the month initials correspond to
the first (1) or second (2) half of each month (e.g. Mar2 = second half of March). Samples
from the UK are from museum specimens.
Location Sampling period Capture events n
Wintering Banc d’Arguin, Mauritania Dec 2009 1 9 Sidi Moussa, Morocco Feb 2010 1 9 Rochford, Kilnsea and Emsworth estuaries, UK
Jan and Dec 1897
unknown 13
Tagus Estuary, Portugal Feb 2009 1 1 Dec 2009 1 6 Jan 2010 1 4
Migration Tagus Estuary, Portugal Mar2 2010 3 11 Apr1 2010 2 9 Apr2 2010 4 30 May1 2010 1 7
Total 99
Stable isotope analysis
Toenails were washed in double baths of 0.25 N sodium hydroxide solution alternated
with baths of double distilled water to remove adherent contamination, and then dried at 50º
C for 48 h. Between 0.30 and 0.40 mg of toenails were stored in tin cups for stable-carbon and
nitrogen isotope assays. Isotopic ratios were determined by continuous-flow isotope-ratio
mass spectrometry (CF-IRMS). Results are presented conventionally as δ values in parts per
thousand (‰) relative to the Pee Dee Belemnite (PDB) for δ13C, and atmospheric nitrogen (N2)
for δ15N.
Data analysis
In order to investigate differences in toenail isotopic signatures of dunlins sampled at
the four wintering study sites, we used a linear discriminant analysis and evaluated the
accuracy of predicted group memberships by cross-validation. Carbon and nitrogen isotopic
values were log (x + 18) transformed prior to analysis to meet the assumptions of normality
and homocedasticity. A second discriminant analysis was carried out excluding samples from
the UK, in order to assign the origins of dunlins captured at Tagus during spring migration.
Each sample was allocated to one of the wintering sites (Mauritania, Morocco and Tagus
estuary) according to the highest probability of group membership. All samples that had a
value of either canonical variable greater than 2.58 from any group mean were not classified,
as we assumed them to have less than 1% chance of belonging to any particular group. The
critical value of 2.58 represents the number of standard deviations away from the group mean
Chapter 4. Discriminating geographic origins of migratory waders at stopover sites: insights from isotope analysis
89
above which group membership is predicted to be less than 1% (Atkinson et al. 2005). A
discriminant analysis was also used to investigate the ability of body measurements (wing and
culmen length) and physiological parameters (body mass, muscle and fat scores) to classify
dunlins during spring migration as wintering (local) or as passage migrants (from Mauritania).
A generalized linear model (GLM) with a binomial error distribution and a logit link
function was used to investigate the probability of occurrence of passage migrant dunlins at
the Tagus estuary as function of date.
All analyses were carried out with R v.2.11.1 (R Core Team 2010).
4.4. Results
Isotopic signatures of wintering reference populations
Carbon isotopic ratios of dunlins from Mauritania were significantly different from those
of Tagus, Morocco and the UK, which formed an uniform group (F3,39 = 16.66, p< 0.001, n= 42,
followed by post-hoc Tukey tests; Figure 4.1). In contrast, all wintering sites showed
statistically distinct δ15N signatures (F3, 39 = 54.11, p< 0.001, followed by post-hoc Tukey tests).
The discriminant analysis correctly classified all samples from Mauritania, but
percentage of correct assignment was considerably lower within the other sites (55.6%. for
Morocco, 83.3% for Tagus estuary, 84.6% for UK). When excluding the samples from the UK,
the discriminant analysis correctly predicted group membership in 90% of cases, showing
100% correct classification for Mauritania, 88.9% for Morocco and 83.3% for the Tagus
estuary.
Assigning dunlins to their wintering grounds during spring migration
Overall, the 57 samples collected during the migration period (second half of March to
early May) at the Tagus estuary did not fit well within the three reference sites (UK excluded),
with approximately 40% of all individuals falling outside the 1% criteria of group membership.
In addition, a high proportion of birds assigned to Morocco (50%, n= 10) and to the Tagus
estuary (17%, n= 6) had low (< 75%) classification probabilities. Indeed, δ13C and specially δ15N
signatures from dunlins captured during spring migration show a larger variance compared
with that of individuals sampled during the winter at reference sites (Figure 4.1). However, we
Chapter 4. Discriminating geographic origins of migratory waders at stopover sites: insights from isotope analysis
90
Figure 4.1. Carbon (δ13
C) and nitrogen (δ15N) stable isotope signatures of dunlins (toenails)
sampled during winter in Mauritania, Morocco, Tagus estuary (Portugal) and United
Kingdom (mean ± SD), and during spring migration (March-May) at the Tagus estuary.
Marginal histograms represent δ13C (upper) and δ15
N (right side) frequencies of dunlins
sampled during spring migration at the Tagus estuary.
did not find a significant correlation between δ15N values of local wintering dunlins during
spring migration and their sampling date (Spearman correlation: r= 0.11, p= 0.608, n= 23).
There was a bimodal pattern in δ13C signatures: one group showed enriched δ13C values,
more closely related with Mauritania signatures, and another group exhibited lower δ13C
values, more similar to those from the Tagus estuary and Morocco (Figure 4.1). For the
purpose of the following analysis, birds with δ13C> -8‰ will be referred to as “passage
migrants”, representing birds that spent the winter in Mauritania. Birds with δ13C< -12‰ will
be considered to belong to the Tagus estuary wintering population.
Wintering and passage migrants revealed an almost complete overlap in body
measurements (wing and culmen length) and physiological parameters (body mass, muscle
and fat scores; Table 4.2). In fact, a discriminant analysis using these variables was able to
correctly classify only 66.1% of the birds in these two groups, and 16% of these had posterior
probabilities <60%.
Chapter 4. Discriminating geographic origins of migratory waders at stopover sites: insights from isotope analysis
91
Table 4.2. Mean ± SD values of body measurements and physiological parameters of
dunlins captured during spring migration at the Tagus estuary, classified as “wintering”
(n=23) and “passage migrants” (n=34) according to their isotopic signature.
Wintering Passage migrants
Mean ±±±± SD Range Mean ±±±± SD Range
Wing length (mm) 118.2 ± 4.0 111 - 127 116.1 ± 3.0 112 - 125
Culmen length (mm) 31.4 ± 2.9 27.3 - 37.4 28.9 ± 2.7 24.7 – 36.8
Body mass (g) 51.1 ± 7.3 39.0 - 67.4 47.3 ± 5.9 36.0 - 61.9
Muscle 2.0 ± 0.6 1 - 3 1.8 ± 0.6 1 - 3
Fat 3.7 ± 2.3 1 - 7 4.4 ± 1.9 0 - 7
Migratory patterns of dunlins as revealed by stable isotopes
The first two passage migrants from Mauritania were captured at the Tagus estuary on
the 24th and 31st of March, corresponding to 18% of the birds sampled during the second half
of this month (n= 11). There was a significant increase in the proportion of passage migrants
with date (z= 3.61, p< 0.001, n= 68, Figure 4.2). According to the model, and assuming equal
capture probability between wintering and passage migrants, 50% of the dunlin present at the
Tagus estuary by the end of the first half of April originate from Mauritania, and represent
> 80% of all birds during the last week of April and early May (Figure 4.2).
Figure 4.2. Predicted probability of occurrence of passage migrant dunlins at the Tagus
estuary fitted by a logistic regression (solid line). Histograms represent the distribution of
capture events with migrant (top) and wintering (bottom) dunlins.
Chapter 4. Discriminating geographic origins of migratory waders at stopover sites: insights from isotope analysis
92
4.5. Discussion
Despite being among the best studied avian groups, waders have seldom been used as
model species for stable isotope studies, mostly for two reasons: first, wader moulting
processes are poorly understood and highly variable (Prater et al. 1977) limiting the use of
feathers to assign individual birds to geographic populations. Second, there are no clear
isotopic gradients in wader habitats across large geographical scales, which prevent modelling
isotope ratios as a function of latitude (Wunder et al. 2005). Our study shows, however, that
stable isotopes help assigning dunlins to their wintering grounds, as long as a suitable tissue is
selected for sampling. Although isotopic reference values of wintering dunlins may show
seasonal and inter-annual variations, the magnitude of these variations is unlikely to mask the
clear segregation in carbon signature among groups. These findings are likely to be applicable
in many areas where wintering and passage birds co-occur during migration.
Tracing wintering origins of dunlins using stable isotope analysis
Isotopic signatures of dunlins from Mauritania are very distinct from those of European
and Moroccan birds, these later presenting considerable overlap mainly in δ13C values. The
more enriched δ13C values found in Banc d’Arguin, Mauritania, could partly be explained by the
low freshwater influence (Hobson 1999) and by the large extent of seagrass beds (Connolly et
al. 2005) compared with European estuaries. Nonetheless, given the magnitude of the
differences found, also in comparison with samples from the saline environment of Sidi-
Moussa, Morocco, it is more likely that the differences are due to distinct baseline values in
the particulate organic matter of each site.
On the other hand, the significantly lower δ15N values found in dunlins from Mauritania
could be due to differences in diet composition. Although prey consumed by dunlins is not
considerably different among sites (Goss-Custard et al. 1977; Zwarts et al. 1990c; Santos et al.
2005), dunlins at Banc d’Arguin eat remarkably smaller prey than elsewhere (Zwarts et al.
1990c). Given that prey size is often positively correlated with δ15N signatures (Ménard et al.
2007), the consumption of smaller prey could lead to lower δ15N values. However, several
other mechanisms, such as the degree of freshwater and/or terrestrial influence and the
amount of anthropogenic inputs, may affect nitrogen isotopic ratios in intertidal areas (Hobson
1999; Ogden et al. 2005). Thus, the large differences found among some of the study sites
suggest that the sources of nitrogen are very distinct and site-specific, as proposed in previous
studies (Atkinson et al. 2005).
Chapter 4. Discriminating geographic origins of migratory waders at stopover sites: insights from isotope analysis
93
During spring migration the Tagus estuary acts as a stopover site for several thousand
migrating dunlins that mix with the local wintering population (Catry et al. 2011). South of
Tagus, there are only two important areas for wintering dunlins: Mauritania, holding the
largest populations across West Africa (1 030 000 dunlins; Hagemeijer et al. 2004) and with
much lower importance, Morocco (40 000 dunlins; Dakki et al. 2001). During spring migration
at Tagus estuary two groups of individuals were clearly segregated by their δ13C values,
strongly suggesting that dunlins with enriched δ13C signatures (> -8‰) belong to the wintering
population of Mauritania. Most individuals with lower δ13C values (< -12‰) fall well within the
range obtained for wintering Moroccan and Portuguese dunlins, but the existing evidence
suggest that these birds mostly belong to the Tagus wintering population. Indeed, the large
majority of these dunlins were captured before mid April, whilst numbers of wintering birds in
Morocco only drop significantly in the second half of April (El Hamoumi and Dakki 2010),
suggesting later departure dates.
Overall, the reduction in the proportion of birds with depleted versus enriched δ13C
values fits well with bird counts carried out in the Tagus estuary. Count data reveal a peak of
passage migrants in the second half of April (Catry et al. 2011). In addition, telemetry studies
have shown that part of the wintering dunlin population do not leave the estuary before late
April, largely mixing with passage migrants (author’s unpublished data).
Nitrogen isotope ratios of dunlins sampled during spring migration were generally lower
and showed larger variation than those found in wintering populations of both Mauritania and
the Tagus estuary. The temporal mismatch in sample collection between the two periods
(which varied from 1.5 to 4.5 months) might explain the differences found in δ15N values. The
period of information integration of stable isotopes in toenails varies according to species and
nail growth rate. Deposition of keratin is a continuous process and thus the nail tip probably
has a combination of old and new keratin, providing information over a medium temporal
scale, from weeks to few months (Bearhop et al. 2003). As a consequence, samples collected
during the winter might integrate information from the early winter, whilst samples collected
in spring most probably integrate information from late winter. Important seasonal variations
in the availability of benthic invertebrates are common and shorebirds are known to vary their
diet accordingly (e.g. Zwarts and Wanink 1993). However, the lack of a significant correlation
between δ15N values of local wintering dunlins during spring migration and their sampling
date, meaning that the temporal mismatch could only partially explain the variation obtained.
Morphometrics, mainly bill length, have been used to trace dunlin migratory routes,
linking breeding to wintering grounds (Pienkowski and Dick 1975; Hallgrimsson 2010).
Chapter 4. Discriminating geographic origins of migratory waders at stopover sites: insights from isotope analysis
94
However, our data indicates that body measurements and physiological parameters alone are
overall inappropriate to efficiently segregate dunlins by wintering origin.
Migratory patterns of dunlins as revealed by stable isotopes
The first migrant dunlin from Mauritania was recorded at the Tagus estuary on the 24th
of March, but the bulk of migrants arrived during late April and early May. These schedules
match with the departing period recorded by Piersma et al. (1990) in Mauritania (24 March –
13 May; average date 29 April). The wide temporal window of migratory passage at the Tagus
estuary also reinforces the hypothesis of intraspecific differences in departure timings of
dunlins from their wintering grounds at Banc d’Arguin, which can be related to (1) sex
differences in the optimal arrival time at the breeding grounds and (2) differences in breeding
destinations (Piersma et al. 1990). Although dunlins were not sexed, bill length of early
migrants covers a large range (26.0-36.75 mm), suggesting that both male and female dunlins
are involved in early migratory movements. As for the differences in breeding destinations,
although most dunlins wintering in Mauritania belong to the Icelandic C. a. schinzii breeding
population (Pienkowski and Dick 1975; Delany et al. 2009), at least part of the C. a. schinzii
populations breeding in Britain and Ireland and in the Baltic region also winter in West Africa,
namely in Mauritania (Wernham 2002; Thorup et al. 2009). The UK and Baltic populations,
breeding at lower latitudes, might leave first their African wintering grounds in comparison
with the Icelandic population, resulting in the observed bimodal pattern in timing of departure
from Banc d’Arguin (Piersma et al. 1990) and also in the timing of stopover at the Tagus
estuary.
95
CHAPTER 5
Crossbow-netting: a new method
for capturing shorebirds
Martins, R. C., T. Catry & J. P. Granadeiro. 2014
Journal of Field Ornithology 85(1): 84-90
Chapter 5. Crossbow-netting: a new method for capturing shorebirds
97
5. Crossbow-netting: a new method for capturing shorebirds
5.1. Abstract
Capturing shorebirds during the non-breeding season can be challenging because they
are usually scattered over wide-open intertidal areas while foraging and are sensitive to
human disturbance at roosts where they gather during high tide in large vigilant flocks. Several
techniques are available for capturing shorebirds, but, for a study of stopover ecology, we
needed a method that would allow us to capture dunlins Calidris alpina on a regular basis at
high-tide roosts during the day (ruling out mist-nets), did not require the use of gun-powder
(ruling out cannon-nets), and that would deploy a net faster than clap nets, whoosh nets, and
wilsternets. Therefore, we developed a new method to capture shorebirds where a crossbow
is used to pull a mist-net over flocks of roosting birds. We tested this technique in four habitats
(saltpans, salt marshes, beaches, and mudflats) in the Tagus estuary, Portugal, and captured
over 380 birds representing eight different species. Advantages of this technique compared to
other methods (e.g., mist nets, clap- and whoosh nets, and cannon-nets) include (1)
portability, (2) ease of set up, (3) minimal disturbance of birds near the capture area, and (4)
no explosive materials are needed. Our results suggest that crossbow-netting is a safe and
useful capture technique, especially for studies requiring the capture of small numbers of birds
on a regular basis.
5.2. Introduction
Capturing shorebirds during the non-breeding season can be challenging (Stroud and
Davidson 2003) because they are usually widely dispersed over wide-open intertidal areas
while foraging and are sensitive to human disturbance at roosts where they gather during high
tide in large vigilant flocks. However, several different capture techniques have been described
(Low 1935; Gerstenberg and Harris 1976; Hicklin et al. 1989; Mehl et al. 2003; Lindstrom et al.
2005; Doherty 2009; Edwards and Gilchrist 2011). One way to capture wintering shorebirds is
to use mist-nets at night (in roosting areas and, less frequently, foraging areas; Johns 1963;
Gerstenberg and Harris 1976). Although logistically simple, the effectiveness of mist-nets
depends on the amount of ambient light and favourable weather conditions (especially low
wind), and also requires prior knowledge of the location of nocturnal roost sites, which often
Chapter 5. Crossbow-netting: a new method for capturing shorebirds
98
differ from those used during the day (Johns 1963; Gerstenberg and Harris 1976; Sutherland et
al. 2004; pers. obs.). Active trapping techniques, where a net is rapidly deployed over a flock of
birds, are sometimes more successful in foraging and roosting areas. Such techniques include
cannon-nets, clap nets, whoosh nets, wilsternets, and drop-nets (Thompson and DeLong 1967;
Gerstenberg and Harris 1976; Sutherland et al. 2004; Doherty 2009).
During a recent study of stopover duration and roost-site selection by spring-migrant
dunlins Calidris alpina, we needed to capture birds at several high-tide roosts, some of which
were used by birds exclusively during the day so mist-nets could not be used. Moreover, we
wanted a capture method that would not require the use of gun-powder (which requires legal
permission to handle, store, and transport and, in Portugal, can only be used within a 50-km
radius of an official gun-powder storehouse), ruling out the use of cannon-nets. We also
wanted to use an active trapping method, but one where the net could be deployed faster,
and thus potentially be more effective in capturing birds than nets pulled by elastics, such as
those used in clap nets, whoosh nets, and wilsternets. Thus, we developed a new method for
capturing shorebirds (mainly small species such as Calidris spp. and Charadrius spp.) that
involved use of a crossbow to pull a mist-net over flocks of roosting birds.
5.3. Methods
Our study was conducted at the Tagus estuary, Portugal (38°45’ N, 09°50’ W), during the
winter (December-February) and spring-migration (March-April) seasons of 2009-2013.
Intertidal areas comprise ≈ 97 km2 of mudflats with small sandy areas. Salt marshes and
saltpans are the main high-tide roosts of shorebirds. The Tagus estuary regularly harbours
> 30 000 shorebirds during the winter and spring-migration periods (Catry et al. 2011).
Our capture device consists of a crossbow, a heavy arrow, and a modified mist-net. The
crossbow (Horton Tacoma, Horton Manufacturing Co., Tallmadge, OH; draw weight = 68 kg)
shoots an arrow attached to the leading edge of the net. We modified a standard mist-net (11
m long, 20-mm mesh size) by removing shelf strings and cutting it in the shape of a trapezium
(11 m at the base, 4 m at the leading edge, and 5 m maximum width; Figure 5.1). A 2-mm
string was sewed around the net perimeter and an extension of the string was used to tie the
arrow to the leading edge of the net at three points (Figure 5.1). The length of these strings
was carefully adjusted by stretching the three strings simultaneously so that the single-point
traction provided by the arrow is transmitted to the maximum extent at the leading edge.
Initial trials revealed that standard (carbon) arrows (28 g) did not provide enough momentum
Chapter 5. Crossbow-netting: a new method for capturing shorebirds
99
Figure 5.1. Overview of the crossbow-net design showing the net completely open. A
modified trapezium-shaped mist-net was used and attached to an arrow heavy enough
(280 g) to pull the 400-g net. Black dots in the front of the net represent the points where
the extension of the arrow-string was attached.
to pull the net (400 g). Therefore, we conducted several tests with modified arrows of
increasing weight (28 - 610 g) and concluded that a 280-g arrow was the lightest arrow able to
pull the net to its maximum length, thus providing the fastest full-net deployment possible.
Arrow weight was increased by removing its metal point and filling the hollow carbon body
with 2-mm lead spheres (210 g) and then attaching (with cable-ties and strong tape) a 70-g
iron rod (40 cm long, 8-mm diameter) to the arrow (Figure 5.2).
The crossbow was firmly fixed to the ground behind the capture area, using three
wooden poles and a board (Figure 5.2). The height of the poles (≈ 80 cm in the example of
Figure 5.2, with the crossbow set above water) was chosen to ensure that the crossbow was at
the level of the capture area. The back side of the crossbow was fixed to one of the poles using
a metal wire (≈ 2-mm thick) and the front side (cocking stirrup) of the crossbow was also
attached to a board (supported by two poles) with wire (see Figure 5.2). The crossbow was set
with a slight (≈ 10°) upward angle relative to the horizontal (Figure 5.2) to ensure that, when
shot, the arrow passed safely above roosting birds and the net would not be caught by any
vegetation or other debris on the ground. A 10-m-long plastic gutter (Figure 5.2; composed by
five 2-m sections) was fixed on the ground, together with the bottom edge of the net (with
stakes at five different points). The plastic gutter hid the net from birds and also kept it free of
loose vegetation or other debris.
Chapter 5. Crossbow-netting: a new method for capturing shorebirds
100
Figure 5.2. Photograph of the crossbow-net device set in a saltpan in the Tagus estuary,
Portugal. The crossbow is fixed over the water on a wooden structure, and the net is
placed in a plastic gutter.
To fire the crossbow, we developed a mechanism that included (1) a radio receiver, (2)
four 1.5-volt batteries, (3) one servo, (4) a rat trap (10 x 15 cm), and (5) a radio control (Figure
5.3; radio control, radio receiver, servo, and battery support come in a package, model T2ER,
Robbe Futaba, Futaba Corporation, Mobara, Japan). The servo, activated by radio control, was
used to release the spring of the rat trap (with a string) that in turn pulled the crossbow trigger
(again using a string). The spring of the rat trap was used as a power-amplification mechanism
because the servo was not strong enough to pull the trigger of the crossbow. The radio control
was generally operated from a distance of ≈ 100 m (but could be operated at distances up to
200 m).
We used the crossbow-net device in four different habitats (saltpans, salt marshes,
beaches, and mudflats), targeting roosting shorebirds during high-tide periods. Several
exploratory visits and our prior knowledge of shorebird abundance and behaviour at different
roosting sites were crucial in selecting the best capture locations. Observation of birds during
high tide on days prior to capture attempts allowed us to identify the most frequently used
locations at each roost site.
Chapter 5. Crossbow
Figure 5.3. Crossbow remote
include (1) a radio receiver, (2) four 1.5 V batteries, (3) one servo, (4) a rat trap, and (5) a
radio control. In this system, the servo is
(with a string), which in turn pulls the crossbow trigger (again with a string). The spring of
the rat trap was used because the servo was not strong enough to pull the trigger of the
crossbow directly.
Most capture attempts (21 of 26 attempts, 80.8%) were on saltpans. On many of these
man-made structures, shorebirds frequently roosted on the dikes that separate water ponds
(Figure 5.2) and, therefore, to capture birds on these flat 5
(and hidden net) at the edge of the dike with the crossbow behind it and above the water
(Figure 5.2). The crossbow-net was also used three times at a small mudflat, once on a beach,
and once in a salt marsh. At the salt marsh, we used wood
above the vegetation so the net would not be caught in the vegetation while in flight.
When setting up the crossbow
with the net usually set to be pulled downwind
deployed seemed to be affected by wind
Chapter 5. Crossbow-netting: a new method for capturing shorebirds
101
Crossbow remote-firing mechanism. The main components of the mechanism
include (1) a radio receiver, (2) four 1.5 V batteries, (3) one servo, (4) a rat trap, and (5) a
radio control. In this system, the servo is responsible for releasing the spring of a rat trap
(with a string), which in turn pulls the crossbow trigger (again with a string). The spring of
the rat trap was used because the servo was not strong enough to pull the trigger of the
Most capture attempts (21 of 26 attempts, 80.8%) were on saltpans. On many of these
made structures, shorebirds frequently roosted on the dikes that separate water ponds
(Figure 5.2) and, therefore, to capture birds on these flat 5-m-wide dikes, we pl
(and hidden net) at the edge of the dike with the crossbow behind it and above the water
net was also used three times at a small mudflat, once on a beach,
and once in a salt marsh. At the salt marsh, we used wooden poles to elevate the plastic gutter
above the vegetation so the net would not be caught in the vegetation while in flight.
When setting up the crossbow-net, wind speed and direction were taken into account,
the net usually set to be pulled downwind because the speed with which the net
deployed seemed to be affected by wind, falling slower than normal when shot against strong
firing mechanism. The main components of the mechanism
include (1) a radio receiver, (2) four 1.5 V batteries, (3) one servo, (4) a rat trap, and (5) a
responsible for releasing the spring of a rat trap
(with a string), which in turn pulls the crossbow trigger (again with a string). The spring of
the rat trap was used because the servo was not strong enough to pull the trigger of the
Most capture attempts (21 of 26 attempts, 80.8%) were on saltpans. On many of these
made structures, shorebirds frequently roosted on the dikes that separate water ponds
wide dikes, we placed the gutter
(and hidden net) at the edge of the dike with the crossbow behind it and above the water
net was also used three times at a small mudflat, once on a beach,
en poles to elevate the plastic gutter
above the vegetation so the net would not be caught in the vegetation while in flight.
wind speed and direction were taken into account,
the speed with which the net
when shot against strong
Chapter 5. Crossbow-netting: a new method for capturing shorebirds
102
winds (> 30 km/h) and potentially reducing the likelihood of capturing shorebirds. Although
the effect of wind was not systematically evaluated, the effect of wind was apparent during
initial test shots and during capture attempts when we shot the net against the wind because
wind speed and direction changed after we had already set up the crossbow-net.
We set up the crossbow-net during low tide when birds were dispersed in foraging
areas, ensuring that the capture area was undisturbed when birds started arriving to roost
sites (2-3 h before high-tide peak). To minimize the likelihood of shorebirds avoiding the
capture area, we camouflaged the crossbow and plastic gutter by painting them with natural
(ground) colours. At the roost site (saltpan) where most capture attempts occurred, supporting
structures for the crossbow were set up at two different locations and left in place between
capture attempts with dummy (wooden) crossbows to habituate birds to the apparatus.
Decoys of dunlins (twice) and ruddy turnstones (once) were used non-systematically (≈ 10% of
all capture attempts), but we did not test the possible influence of dummy crossbows or bird
decoys on the number of shorebirds landing in capture areas.
5.4. Results
We successfully captured shorebirds in four representative types of high-tide roosting
habitat in Tagus estuary (saltpan, beach, mudflat and salt marsh), but most birds were
captured in saltpans. Captured birds included dunlins (N= 300), sanderlings Calidris alba (N=
11), little stints Calidris minuta (N= 8), curlew sandpipers Calidris ferruginea (N= 7), ruddy
turnstones Arenaria interpres (N= 2), ringed plovers Charadius hiaticula (N= 30), Kentish
plovers Charadrius alexandrinus (N= 15) and grey plovers Pluvialis squatarola (N= 11).
We did not determine the capture efficiency of the crossbow-net because we did not
systematically count the number of birds present in capture areas before shooting the
crossbow, preventing us from quantifying factors that might affect capture success.
Nonetheless, our observations suggest that the number of birds captured in a single shot, in
addition to the obvious influence of flock size in the area of capture, depended mainly on wind
direction and velocity and on the level of awareness of the birds before shooting. When
shooting against strong winds (> 30 km/h), the net fell more slowly and was not pulled to its
maximum length, increasing the likelihood of birds avoiding capture. In addition, we generally
captured more birds when most birds in the capture area were resting on the ground or with
their heads under their wings than when most birds were alert. Birds within 2-3 m of the
gutter were also more likely to be captured than those near the leading edge of the net.
Chapter 5. Crossbow-netting: a new method for capturing shorebirds
103
We usually captured < 20 birds, but once captured 115 dunlins in a single shot (mean =
14.8 ± 25.2 [SD], range = 1-115, N= 26 capture attempts when the crossbow was fired). In a
few cases (≈ 5, or ≈ 20% of all trials), the crossbow was not fired either because birds did not
enter the capture area or because the flock was disturbed (by aerial predators or human
activities) while we were waiting for birds to settle in sufficient numbers and reduce their
vigilance levels. The crossbow was typically fired 1-3 h after birds start arriving at a roost site.
On six occasions (i.e., ≈ 25% of all capture events), we re-set the crossbow and net after
the first shot and were able to make another capture attempt during the same high-tide
period. We captured additional birds with a second shot on three occasions (mean number
captured: second shot = 14.0 ± 10.0, range = 4-24; first shot = 14.0 ± 13.0, range = 6-29; mean
interval between shots = 126.7 ± 40.4 min). Second shots were sometimes possible because,
when disturbed by the fired crossbow, some birds moved to other parts of the roost site (e.g.
other dikes of the saltpan), but most remained in the area and returned to their usual roosting
spots (where our crossbow was usually set) after we re-set the crossbow and net. The decision
to re-set the net depended on the number of birds captured in the first attempt (relative to
the number of birds we wanted to radio-tag each day), the time elapsed since high tide
(because birds would start leaving roosts to visit foraging areas), and the number of birds
remaining at a roost after the first shot.
After each shot, captured birds were covered with a light cloth (≈ 8×4 m) to keep them
calm until they were extracted from the net. Birds were kept in large cardboard boxes while
waiting to be processed. No birds were killed or injured during capture attempts.
5.5. Discussion
Our crossbow-netting technique proved to be a useful method to capture shorebirds at
roost sites during the day, especially because, as in other studies (e.g. Catry et al. 2012a), we
only need to capture small numbers of birds on a regular basis over an extended period rather
than a large number in a short period of time. Advantages of our crossbow-net system relative
to other capture methods (e.g., mist nets, clap- and whoosh nets, and cannon-nets) include (1)
portability, (2) ease of set up (one person could set up the equipment in ≈ 45 min, but a
minimum of two trained people is advisable for extracting and processing birds), (3) minimal
disturbance of birds near capture areas, and (4) no explosive materials are required.
Moreover, compared to elastic-powered devices, such as whoosh and clap nets, we believe
Chapter 5. Crossbow-netting: a new method for capturing shorebirds
104
that the crossbow system deploys a net faster, which can be critical for capturing attentive,
fast-flying species such as shorebirds. Another advantage of this method is that the firing event
is silent. We found that most birds usually remained at roost sites after the first shot (and after
removal of captured birds from the net), allowing us, on six occasions, to make two capture
attempts during the same high-tide period. In addition, as with other capture methods,
attracting more shorebirds to capture areas may be possible using decoys and tape-lures (Clark
and Austin 2005; McGowan and Simons 2005). Baiting might also be useful (Edwards and
Gilchrist 2011) and could extend the use of the crossbow-net to foraging areas.
Although the crossbow technique requires training to handle birds captured in nets,
permission from banding authorities, and safety precautions to avoid injury (to people and
birds), it does not require the intensive training of cannon-netting (Bub 1991; FAO 2007). Also,
in several countries, use of a crossbow does not require licensing or additional permission such
as those needed to store, handle, and transport gun-powder. Nonetheless, the legal status of
crossbows varies among countries and states and should be carefully investigated by anyone
planning to construct and use a crossbow-net.
The main disadvantage of the crossbow-net is the relatively small size of the net (≈ 38
m2). However, use of either a stronger crossbow or a synchronized firing mechanism with two
crossbows would allow use of larger nets. Another disadvantage of the crossbow-net is that,
with the crossbow and lightweight net used in our study, strong wind and the presence of
vegetation can reduce the likelihood of capturing birds, by making the net to fall slower than
normal or preventing a full-net deployment.
Ethical issues regarding the safety of shorebirds during capture events are a matter of
concern for the research community and legal authorities, and thus a key issue when using the
crossbow-net. Although we cannot totally rule out the possibility of injury to birds, the
likelihood of the arrow hitting a bird is small. Nevertheless, the upward angle of the crossbow
should be adjusted based on the size of the target species. The upward angle can be increased
(at the expense of increasing the time needed for the net to hit the ground) and still allow
capture of slower-moving species, e.g., whimbrels Numenius phaeopus and curlews Numenius
arquata, with the further benefits of reducing the already low likelihood of the arrow hitting a
bird and making it less likely that the net will get stuck on vegetation. In addition, the net
strings along the net perimeter are light and do not move as fast as a cannon-net so are
completely harmless to the birds. Therefore, based on our experience, we believe that the
crossbow-net is a safe method of capturing shorebirds (and possibly other flocking species).
105
CHAPTER
General Discussion
HAPTER 6
General Discussion
Chapter 6. General Discussion
107
6. General Discussion
In the previous chapters (2-5) several aspects of the ecology of wintering and migrating
dunlin populations using the Tagus estuary were addressed, and the specific objectives and
conclusions of each study have been presented in detail. This chapter highlights and integrates
the most important findings, the new methodological approaches and the main conservation
implications that resulted from those studies. In addition, some questions that were left open
in this thesis for future research are also addressed.
6.1. Wintering and migrating dunlin populations using the Tagus estuary
Clarifying temporal overlaps
Many of the coastal wetlands located along migratory flyways act both as wintering and
stopover area for different wader populations, which therefore co-occur at these sites
between winter and migratory periods (Delany et al. 2009). For an effective conservation of
waders it is essential to identify the different populations overlapping in the same wetland
during migration, but this is generally difficult when they belong to the same species (BWPi
2006). This is the case of wintering and migrating dunlin populations using the Tagus estuary,
and this thesis set out to clarify the observed overlap between the two populations in late
winter/early spring, using different methods. By radio-tracking wintering dunlins (Chapter 3), it
was shown that this population departed progressively from the estuary from late March to
late April, with less than 20% of wintering birds remaining after mid April. This represents a
small proportion of all dunlins using the estuary at that time, as dunlin abundance usually
peaks in the second half of April (Chapter 3). These data are consistent with the information
obtained from the analysis of stable isotopes of dunlin nails using the estuary in spring (which
revealed their wintering origin), as it showed that most northward migrants coming from
Mauritania and stopping over in the Tagus estuary mostly occur in the second half of April,
although a few pass earlier (Chapter 4).
The clarification of the migratory schedules of wintering and migrating populations of
the same species using a certain wetland is very important for conservation managers and
provides relevant information for interpreting temporal variations of their local patterns of
use.
Chapter 6. General Discussion
108
Ecological contexts of different populations affected the patterns of resource use
The fact that the Tagus estuary acts as wintering and stopover area provides a good
opportunity to assess how the patterns of resource use by distinct wader populations are
influenced by their distinct ecological contexts, such as differences in energetic constrains,
feeding opportunities and time to explore the wetland. In this thesis, this opportunity was
used to compare wintering and migrating dunlins to examine how birds adjust their diet and
foraging behaviour in response to variations in prey availability (Chapter 2) and to investigate
the relative importance of the perceived risk of predation on wader distribution at the estuary
scale (Chapter 3).
Waders usually respond to variations in environmental conditions, such as sediment
type and prey availability, changing their behaviour and diet to obtain the best energetic profit
while foraging (e.g. Zwarts and Esselink 1989). However, the factors driving such changes were
still poorly understood in small-sized species (but see Kuwae et al. 2010), as their fast foraging
behaviour can limit its study (e.g. Lourenço et al. 2008). The clear winter to spring increase in
prey availability for dunlins in the Tagus estuary, was identified as the main determinant of the
marked differences between wintering and migrating birds in terms of diet and foraging
behaviour (Chapter 2). In particular, it was found that the increase in the surface activity and
biomass of the polychaete Hediste diversicolor is a key ecological factor for migrants as they
adopted mostly visual foraging methods to catch this prey on the sediment surface. During
stopover, such behaviour resulted in an energetic intake that allowed high fattening rates,
which highlights the potential importance of this estuary for waders during migratory periods.
Food abundance and predation risk are among the most important factors driving the
distribution of waders within wetlands (Piersma et al. 1993b; van Gils et al. 2006). However,
the relative weight of these factors is known to be state-dependent (Hilton et al. 1999;
Ydenberg et al. 2002) and therefore the distinct ecological contexts of wintering and migrating
waders using the same area may affect their distribution patterns at the estuary-scale. In the
Tagus estuary, previous studies detected a seasonal variation in the distribution of waders
(Alves et al. 2011; Catry et al. 2011; Alves et al. 2015), but the reasons behind such patterns
were poorly understood. In Chapter 3, it was shown that wintering dunlins prefer the southern
sector of the estuary, where food is more abundant (in both seasons), whereas migrants
mostly concentrate in the northern sector. The perceived (but not actual) risk of predation,
which is higher in the enclosed mudflats of the southern sector, was pointed out to be the
cause of these distribution patterns, because this factor is known to be particularly important
for passage migrants, due to their poor knowledge of stopover areas (Lima and Dill 1990;
Sprague et al. 2008). Also, migrants are on average heavier than wintering birds, due to the fat
Chapter 6. General Discussion
109
load for migration, which increases their susceptibility to perceived risk of predation, by
affecting the escape performance (Lank and Ydenberg 2003), and this factor probably also play
a role.
A few general conclusions can be drawn from the integration of Chapters 2 and 3.
Wintering dunlins of the Tagus estuary faced poorer feeding opportunities than migrants, as
the natural seasonal cycles in intertidal areas of temperate regions usually dictates lower
invertebrate availability for waders during winter (Zwarts et al. 1992; Scheiffarth and Nehls
1997). In accordance with this, wintering birds preferred the estuary sector with higher prey
availability, despite their apparent risk of predation for waders due to the shorter distance
between foraging areas and the shoreline. However, this apparent risk does not seem to
correspond to actual predation risk; the abundance of aerial predators in the southern sector
of the estuary is relatively low and dunlins do not engage in more intense vigilance behaviour
or more alarm flights than in the northern sector. This evidence suggests that, overall,
wintering birds tended to take the most adjusted options of foraging habitat selection to
explore the ecological conditions of the estuary. Furthermore, wintering dunlins are
apparently able to fulfil their daily energetic requirements without major efforts, possibly due
to the mild climate conditions found in this estuary, which decrease thermoregulation costs
and often delivers higher prey availability (Piersma et al. 1993a; van de Kam et al. 2004).
Therefore, wintering in southern Europe, despite it implicates longer migratory journeys, might
represent an advantage for dunlins in relation to other population segments that winter in
northern estuaries with harsher climatic conditions (Santos 2009), as recently shown for the
Icelandic population of Black-tailed Godwit Limosa limosa limosa (Alves et al. 2012a; Alves et
al. 2013).
This thesis also contributed to the study of stopover ecology of waders in the Tagus
estuary, by analysing the diet, behaviour and estuary-scale distribution of dunlins during spring
migration. Most of the migrants that stopover at the Tagus estuary have wintered in the Banc
d’ Arguin, Mauritania. It has been demonstrated that the standing stocks of invertebrates in
this wetland are very low in relation to the number of waders wintering in it (Wolff and Smit
1990; Piersma et al. 1993a), estimated at over 2 million birds (Hagemeijer et al. 2004). While
wintering at the Banc d’Arguin, dunlins feed on very small invertebrate prey (Altenburg et al.
1982; Zwarts et al. 1990a). Such diet contrasts with that recorded at the Tagus during
stopover, where they found larger prey and adopted foraging behaviours particularly adequate
to benefit energetically from the seasonally improved feeding conditions. This contrast
confirms the behavioural foraging flexibility of migratory waders, important because they
usually face very distinct ecological conditions when travelling along their flyways (e.g.
Chapter 6. General Discussion
110
Beninger et al. 2011; MacDonald et al. 2012). However, when deciding where to forage at the
scale of a stopover area, migrating waders may not adjust so well to the local conditions. The
fact that migrating dunlins in the Tagus estuary missed the areas with higher prey availability
presumably to avoid their high apparent risk of predation illustrates well the high importance
of safety rules for waders in active migration (Lima and Dill 1990; Sprague et al. 2008).
Although in some circumstances migrants are forced to take the risk of foraging in dangerous
areas (Dierschke 1998; Ydenberg et al. 2002), such general safety rules often influence how
waders use wetlands, both at the local and flyway scales (Ydenberg et al. 2004; Pomeroy 2006;
Sprague et al. 2008).
6.2. New methodological approaches for wader research
In this thesis very diverse methods were used to investigate wintering and migrating
dunlin populations using the Tagus estuary, but two of these deserve to be highlighted due to
their novelty and potential utility in studies of avian ecology.
Discriminating the winter origin of dunlins using stable isotopes in toenails
The knowledge on connectivity among breeding, wintering and stopover areas used by
migratory birds is essential for their conservation, but such information is often difficult to
obtain. Stable isotope analysis (mainly carbon and nitrogen) has been increasingly used to
track their migratory movements across isotopic gradients (Hobson 1999). In birds, the most
frequently sampled tissues are blood and feathers (Hobson 1999) but both present limitations
specifically to unveil the geographic origin of waders. In this thesis the analysis of stable
isotopes (carbon δ13C and nitrogen δ15N) from toenails was used to reveal the geographic
wintering origin of dunlins using the Tagus estuary during late winter/spring migration period.
The distinct values of δ13C and δ15N obtained from dunlins wintering at different reference
sites of the East Atlantic Flyway, in particular those from Mauritania, allowed the identification
of this wintering area as the main source of dunlins that stopover at the Tagus estuary during
northward migration. Therefore, this study provided evidence that toenails constitute a
suitable biological structure to investigate migratory connectivity in waders.
Chapter 6. General Discussion
111
Crossbow-netting: a new method to capture shorebirds
Obtaining samples of tissue and biometric data from live birds is essential for many
studies in ecology and conservation. However, catching waders during the non-breeding
season can be particularly challenging (Stroud and Davidson 2003), due to the “openness” of
intertidal flats (i.e. lack of natural features or man-made structures that can conceal the
trapping devices) and to their sensitivity to disturbance while gathering at roosting sites.
Several techniques are available for capturing waders, and yet none of them was perfectly
suited for the particular requirements and limitations for the specific conditions found in the
Tagus estuary. Therefore, a novel method to capture waders and other shorebirds was
developed. It consists of using a crossbow, activated at distance by remote control, to shoot a
special (heavy) arrow that in turn pulls a hidden mist-net over flocks of roosting birds. This
technique was tested in four habitats (saltpans, saltmarshes, beaches, and mudflats) in the
Tagus estuary and it successfully captured over 380 birds of eight different species. The main
advantages of this method include high portability, set up simplicity, minimal disturbance to
birds near the capture area, and the non-use of explosive materials. Therefore, the crossbow-
netting is a safe and useful capture technique, especially for researchers requiring the capture
of small numbers of shorebirds on a regular basis.
6.3. Major conservation implications
Data collected during this thesis contributed with important information for the
conservation and management of waders. Many wader populations are suffering long-term
declines due to a variety of threats (IWSG 2003). Like many other wetlands, the Tagus estuary
is partly surrounded by major urban areas. This has affected the estuary, despite the legal
protected status of part of the area. The wintering populations of three out of the five most
abundant wader species of the estuary are declining in the long-term (Catry et al. 2011), which
includes the Dunlin. Considering the stability of the C. a. alpina populations at the flyway-scale
(Delany et al. 2009), the observed declines of dunlins in the Tagus estuary (where that
subspecies is the most represented in winter) were mostly attributed to local causes, in
particular to the degradation of roosts, rather than food abundance in intertidal areas (Catry et
al. 2011). In this thesis, the relative easiness of wintering dunlins to fulfil their energetic
requirements (Chapter 2), together with the high availability of prey in the southern flats of
the Tagus estuary (Chapter 3), indicates that wintering wader populations of this wetland are
not constrained by food.
Chapter 6. General Discussion
112
Chapter 3 highlights that a significant part of the wintering dunlin population forage in
the southern sector of the estuary, i.e. outside protected areas, which is also true for other
species (Catry et al. 2011). Given the increasing pressure of urbanization around the estuary,
these birds might be at risk of suffering further habitat degradation. This is particularly likely to
occur at roosting sites, where the human pressure is higher, including by direct disturbance
(Rogers 2003; Yasué 2006). This highlights the need to extend the limits of the existing Special
Protected Area in the Tagus estuary, to include the main intertidal areas and roosting sites of
the southern sector, and take effective measures to control urbanization and disturbance.
By studying the departure of wintering dunlins from the Tagus (Chapter 3) and detecting
the presence of passage migrants from Mauritania (Chapter 4), the timing of use of this
estuary by those populations was clarified. Furthermore, their distinct estuary-scale
distribution patterns were described (Chapter 3). This thesis thus provided accurate
information to help decision makers deciding where and when to act, adapting management
practices to the alternate presence of wintering or migrating wader populations.
A network of good-quality stopover areas, providing adequate conditions to rest and
refuel, is essential to ensure habitat connectivity for migratory waders (van de Kam et al.
2004). This thesis also showed how seasonal variations in the invertebrate community of
intertidal flats of the Tagus estuary ensured good quality feeding conditions for migrating
dunlins, during spring stopover (Chapter 2). The deterioration of feeding conditions for waders
in stopover sites can cause changes in their migratory paths and timings (Verkuil et al. 2012)
and potentially reduce their breeding success through carry-over effects (Baker et al. 2004). It
is thus crucial that activities with potential impacts on foraging areas of the Tagus estuary are
carefully controlled, to ensure that the quality of feeding conditions for migratory waders is
not affected. Such long term objective is facilitated by the fact that migrants clearly prefer to
stopover in the northern sector of the Tagus estuary (Chapter 3), which is covered by the
Special Protected Area (both intertidal flats and roosting sites). However, this legal protection
has not been sufficient to prevent important damage to roosting sites, such as the conversion
of saltpans into fish or shrimp aquacultures (Dias et al. 2006; Catry et al. 2011), which reduces
or entirely eliminates their suitability for roosting waders. Furthermore, the concentration of
migrants in just part of the estuary poses an additional threat, which is their reliance on very
few roosting sites. This highlights the need to enhance the protection of the most important
roosting sites of the Tagus estuary and implement effective management measures to increase
their quality for waders (Velasquez 1992; Warnock et al. 2002). Such improvement would
benefit both wintering and migrating wader populations using this internationally important
wetland.
Chapter 6. General Discussion
113
6.4. Indications for future research
In Chapter 3 it was shown that mudflats of the southern sector of the estuary are richer
in prey for waders than those of the northern sector. This is probably related to the higher
urban occupation around the southern mudflats of the estuary and the untreated sewage
discharges in recent decades, which cause an organic enrichment of the sediments, thus
promoting the abundance of invertebrates like the polychaete Hediste diversicolor
(Ravenscroft and Beardall 2003; Ait Alla et al. 2006; Alves et al. 2012b). These untreated
discharges in the estuary cessed completely by 2011, after the completion of a network of
wastewater treatment stations (Águas de Portugal 2011). It would now be important to
monitor possible ongoing changes of the invertebrate community and investigate their
consequences on the foraging ecology of waders and their wintering distribution across the
estuary.
The Dunlin wintering population of the Tagus estuary is equally divided between its
northern and southern sectors, even though density is higher in the smaller sediment flats of
the latter (Chapter 3). Data collected in the estuary in recent years (e.g. Dias et al. 2006; and
non-published information from dunlin colour-ringing and radio-tracking) are in general
consistent with the site fidelity usually observed in waders at the wetland-scale (e.g. Warnock
and Takekawa 1996; Leyrer et al. 2006; Conklin and Colwell 2007). These data suggest that
those two wintering dunlin groups may remain spatially segregated throughout the winter,
despite the short distance between northern and southern sectors. The fact that the latter
provides higher food availability (both in winter and spring) indicates that these two groups
face different conditions for accumulating fat quickly during the pre-migratory period.
However, it was shown that they departed from the estuary for northward migration at similar
rates (Chapter 3). Therefore, it would be interesting to compare northern and southern
wintering dunlins regarding the duration of their fattening period and their body condition at
departure. In addition, it would be also interesting to study if possible differences between
these groups are later reflected in their migratory strategies along the flyway and in the
location of their breeding grounds.
Much information concerning the migratory periods is still missing. Regular wader
counts at the scale of the estuary provide strong indication of the importance of this
strategically located wetland in the context of the East Atlantic Flyway, for different species
(e.g. Alves et al. 2011; Catry et al. 2011). However, the total numbers of individuals of each
wader species/population that stopover in the estuary are mostly unknown (but see Lourenço
and Piersma 2008). To obtain such information, the knowledge on stopover length and further
Chapter 6. General Discussion
114
estimation of turnover rates in the estuary is essential. These issues of stopover ecology
deserve to be the focus of future studies, which would provide a far more accurate evaluation
of the importance of this wetland for waders during migration and an improved knowledge
base to support their conservation.
Finally, in this thesis it was shown that stable isotope analysis (carbon δ13C and nitrogen
δ15N) of toenails of dunlins can successfully reveal their wintering areas. Given the importance
of understanding the connectivity between wintering areas and stopover sites for the
conservation of migratory waders (Delany et al. 2009), this technique should be further
developed. Potential paths to be explored include (1) applying this methodology to other
wader species stopping over in the Tagus estuary, (2) test the applicability of the method in
other European wetlands (3) compile reference isotopic signatures from other important
wintering areas in the western coast of Africa (e.g. Guinea-Bissau) and (4) test different
biochemical markers (stable isotopes of deuterium, oxygen and/or sulphur, heavy metals,
trace elements) in order to increase the specificity of the local food-web signatures and thus
refine the geographic origin of waders.
References
115
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