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AIRO 26

Sociedade Portuguesa para o Estudo das Aves

VOLUME 26 | Ano 2019


SOCIEDADE PORTUGUESA PARA O ESTUDO DAS AVES
PORTUGUESE SOCIETY FOR THE STUDY OF BIRDS

Avenida Columbano Bordalo Pinheiro, 87, 3º Andar.


1070-062 Lisboa – Portugal
T. +351 213 220 430 | F. +351 213 220 439
[email protected] | www.spea.com

DIRECÇÃO NACIONAL
NATIONAL BOARD

Presidente
Graça Lima

Vice-presidente
Paulo Travassos

Tesoureiro
Peter Penning

Vogais
Alexandre Leitão
Martim Pinheiro de Melo

COMISSÃO EDITORIAL
EDITORIAL BOARD

Editor Principal
Teresa Catry

ILUSTRAÇÕES
ILLUSTRATIONS

PAG. 03-27-33
Birdlife International
ANO / YEAR 2019
VOLUME 26 2019

CONTENTS
03 Internet photography forums as sources of avian dietary data:
bird diets in Continental Portugal
Pedro M. Lourenço

27 Results from an avifaunal survey along the Corubal and Fefine


rivers, Guinea-Bissau
Paulo Catry, Miguel Lecoq, Mohamed Henriques, Pierre Campredon
& José Pedro Granadeiro

33
Diet of the White Stork (Ciconia ciconia) in a heterogeneous
Mediterranean landscape: the importance of the invasive Red
Swamp Crayfish (Procambarus clarkii)
Eduardo M. Ferreira, Filipa Grilo, Raquel C. Mendes, Rui Lourenço,
Sara M. Santos & Francisco Petrucci-Fonseca

ÍNDICE

03 Fóruns de fotografia na Internet como fontes de dados de dieta de aves:


dietas de aves de Portugal Continental
Pedro M. Lourenço

27 Resultados de um censo de aves realizado ao longo dos rios Corubal


e Fefine, Guiné-Bissau
Paulo Catry, Miguel Lecoq, Mohamed Henriques, Pierre Campredon & José Pedro Granadeiro

33 Dieta da Cegonha-branca (Ciconia ciconia) numa paisagem Mediterrânica


heterogénea: a importância de uma espécie invasora, o Lagostim-vermelho-
-do-Louisiana (Procambarus clarkii)
Eduardo M. Ferreira, Filipa Grilo, Raquel C. Mendes, Rui Lourenço, Sara M. Santos
& Francisco Petrucci-Fonseca
Dietas das aves VOLUME
de Portugal26
baseadas em fóruns de fotografia online
2019

Internet photography forums as sources of avian


dietary data: bird diets in Continental Portugal

Fóruns de fotografia na Internet como


fontes de dados de dieta de aves: dietas
de aves de Portugal Continental

Pedro M. Lourenço1

1 Centro de Estudos do Ambiente e do Mar (CESAM)


/ Departamento de Biologia Animal, Faculdade de
Ciências da Universidade de Lisboa, 1749-016 Lis-
boa, Portugal.

* Corresponding author: [email protected]

ABSTRACT
Knowing animal diets is key ecological information, required for understanding the dynamics
of ecosystems as a whole, as well as the ecology of individual species. However, for many species/
regions such information is not available. Here I explore the potential use of internet photog-
raphy forums to describe the diet composition of birds by analysing photographs posted on the
“Aves de Portugal Continental” Facebook page.
A total of 909 photographs were found to show identifiable food items being taken by 144 dif-
ferent avian species. These included 78 regularly occurring species for which there were no avail-
able dietary data for Portugal according to Catry et al. (2010). The photographs were obtained
in 262 different locations, covering all the 18 districts of Continental Portugal. They exhibited
a total of 206 different food item categories, their taxonomic rank ranging from species (n=97)
to class (n=3), as well as some non-taxonomic groupings such as unidentified berry or human
refuse. The avian species with the most dietary information were European Bee-eater Merops
apiaster (n=68), Osprey Pandion haliaetus (n=59) and Common Kingfisher Alcedo atthis (n=40).
Although this type of data are affected by several biases, namely a geographic bias in favour
of areas closer to human settlements and human-altered habitats, and a possible bias favouring
larger food items that are more easily identifiable in photographs, it could provide an invalu-
able source of avian dietary data. In the future, these data could be gathered through an open
web-enabled platform which would include photographers and biologists who would provide
identifications of the food items being taken.

Keywords: Alcedo atthis, diet composition, Facebook, Merops apiaster, photography, Turdus merula, Upupa epops

03
Portuguese bird diets based on Internet photography forums

RESUMO
O conhecimento das dietas dos animais é essencial para compreender as dinâmicas dos
ecossistemas, assim como a ecologia de espécies individuais. Contudo, para muitas espécies/
regiões, esse tipo de informação não está disponível. Nesta contribuição, exploro o potencial
dos fóruns de fotografia na Internet como fontes de informação sobre dietas de aves, analisando
as fotografias publicadas na página de Facebook “Aves de Portugal Continental”.
Um total de 909 fotografias continham imagens de aves a consumir itens alimentares
identificáveis, cobrindo 144 espécies diferentes de aves. Estas incluíram 78 espécies de
ocorrência regular em Portugal para as quais, segundo Catry et al. (2010), não existiam
quaisquer dados publicados relativos às suas dietas no país. Estas fotografias foram obtidas em
262 locais distintos, cobrindo todos os 18 distritos de Portugal Continental. Elas apresentavam
206 categorias diferentes de alimentos que, em termos taxonómicos, iam desde o nível da
espécie (n=97) até ao nível da classe (n=3). As espécies de aves para as quais foi obtida mais
informação alimentar foram o Abelharuco Merops apiaster (n=68), a Águia-pesqueira Pandion
haliaetus (n=59) e o Guarda-rios Alcedo atthis (n=40).
Embora este tipo de dados tenha alguns problemas de enviesamento, nomeadamente um
enviesamento geográfico a favor de áreas mais próximas de povoações e de habitats com maior
influência humana, e um provável enviesamento a favor de itens alimentares maiores que são
mais facilmente identificáveis em fotografias, podendo ser uma fonte valiosa de informação
ecológica. No futuro estes dados poderiam ser recolhidos através de uma plataforma online
que incluiria fotógrafos e biólogos capazes de identificar os itens alimentares consumidos.

Palavras-chave: Alcedo atthis, dieta, Facebook, Merops apiaster, fotografia, Turdus merula, Upupa epops

Introduction
The diet of a species is key ecological widely studied vertebrates, ecological studies
information, required for understanding frequently rely on dietary information based
its position in trophic webs, its interactions on observations in different geographic
with other species and often its habitat areas, habitats or seasons, which fails to
preferences and seasonal routines (e.g. Pimm address the issue that diet can greatly vary
et al. 1991, Piersma 2012). Information on throughout a species range (e.g. Bojarska &
the many links and interactions among prey Selva 2011, Terraube & Arroyo 2011).
and predators within an ecosystem is an The Portuguese avifauna is a good example
important starting point for exploring the of such lack of detailed dietary information.
dynamics of ecosystems as a whole, as well Despite its relatively small size, the geographic
as the population dynamics of individual location and varied landscape of Portugal
species (Thébault & Loreau 2003, Olff et grants it one of the richest avifaunas in
al. 2009). However, such information is Europe with roughly 300 regularly occurring
often not available. Even for common and bird species in Continental Portugal (Catry

04
Dietas das aves de Portugal baseadas em fóruns de fotografia online

et al. 2010). However, detailed ecological Method


data is still lacking for many of these species
within the Portuguese territory. In terms of The “Aves de Portugal Continental”
dietary information, “Aves de Portugal”, the Facebook page (https://www.facebook.
most up to date monograph on Portuguese com/groups/121307984660183/) is a
ornithology, provides diet information for large forum for bird photographers and
286 species. However, for 193 (67%) of bird enthusiasts in general, focusing on
these species, this diet information refers to the avifauna that occurs in Continental
other parts of their range. Specific dietary Portugal. As of October 2018, the page has
data for Portugal, which is some cases is only over 25000 members and its archives store
anecdotal, is only available for the remaining over 12000 photographs, with tens of new
93 species (33%; Catry et al. 2010). For a photographs being added every week. I
few species, these data have become available went through all the archived photographs,
since the publication of that monograph, as well as monitoring the new photographs
examples being Sanderling Calidris alba being posted (until 8 October 2018), in
(Lourenço et al. 2015) and European Roller order to select every case where it was
Coracias garrulus (Catry et al. 2018), but for possible to identify a food item being taken
the vast majority the situation remains the by a given bird species (see Appendix 1 for
same. some examples).
In recent years, the development of web- I only used photographs in which the
enabled networks for citizen science and bird could be unquestionably identified
globally accessible unified databases (e.g. to specific level (the only exception being
Sullivan et al. 2009) have allowed scientists Phylloscopus ibericus and P. collybita
to have access to a plethora of data on which cannot be reliably identified based
species distributions, phenological patterns, on photographs and were lumped together)
habitat associations, and even variations and where the bird was either actively eating
in numbers, productivity and survival a food item or, in the case of raptors, was
(Greenwood 2007, Rubolini et al. 2007) that holding a prey in its talons. Photographs
would otherwise be very difficult to collect without information on location, date
through traditional research and monitoring and authorship were also excluded as this
endeavours. Moreover, such web-based information was used to exclude potential
initiatives contain information similar in pseudo-replicates, such as two photos by the
quality to that from standardized monitoring same author of the same species consuming
programmes (Munson et al. 2010, Tiago the same food type on the same day. Finally,
et al. 2017a). Another potential source of I also exclude photographs of birds eating
valuable ecological data are internet nature food items that were likely used as lure by
photography forums, which may provide data the photographer, such as sunflower seeds
on consumed food items, morphology (e.g. (when the birds was not actively removing
plumage variability in birds) or occurrence of the seed from the flower), canary grass seeds
specific behaviours. and mealworms, but cannot completely
Here I explore the potential value of such rule out the possibility than other prey
internet photography forums by compiling items identified in photographs were also
data on the diets of bird species in Continental placed by photographers as lure.
Portugal through the analysis of photographs Prey items were then identified to the
published on the “Aves de Portugal lowest possible taxonomic rank, using
Continental” Facebook page, aiming to use identification keys (e.g.Chinery 1993,
these data to describe the diet composition of MacDonald & Barret 1993, Ferrand de
as many avian species as possible. Almeida et al. 2001) and in some cases

05
Portuguese bird diets based on Internet photography forums

through the help of experts (e.g. for of photographs per species ranged from 1
fishes, insects, reptiles and fruits). Often (for 31 species) to 68 (for European Bee-
the photographers also provided valuable eater Merops apiaster; Table 1).
information that helped with food item The photographs were obtained in 262
identification. Food items were then divided different locations which cover all districts
into groups, mostly referring to animal of Continental Portugal (Fig. 1). Lisboa
classes, but also to fruits, seeds and other (n=168 photographs), Setúbal (n=116),
groupings such as human refuse. For each Porto (n=99) and Beja (n=86) were the
avian species I calculated the proportion of districts with more photographs, while
food items from each group. I also provide Viseu (n=9), Viana do Castelo (n=13),
information on the seasons and geographic Castelo Branco (n=13) and Guarda (n=14)
areas in which each species was photograph, were the districts with fewer photographs.
for the latter dividing Portugal in three Overall, and despite photograph locations
regions (North, including the districts of being more concentrated along the more
Braga, Viana do Castelo, Porto, Vila Real, densely populated coast, and around the
Bragança, Aveiro, Viseu and Guarda; main coastal wetlands that attract more
Centre, including the districts of Coimbra, birdwatchers, there is a wide coverage of
Castelo Branco, Leiria, Lisboa, Santarém, the whole territory (Fig. 1).
Portalegre and the Setúbal Peninsula; and It was possible to detect 206 different
South, including the districts of Évora, Beja, food item categories (Table 1), their
Faro and the remainder of Setúbal district). taxonomic rank ranging from species
For species with over 15 photographs, diets (n=97) to class (n=3), as well as some non-
were analysed in more detail, including the taxonomic groupings such as unidentified
proportion of lower rank food item groups berry or human refuse. The most commonly
and any apparent geographic or seasonal found food items were unidentified fishes
patterns. (n=75, present in the diet of 15 species),
mullets (Mugilidae, n=44, present in the
diet of 10 species), unidentified insect larvae
Results and discussion (n=40, present in the diet of 16 species),
and unidentified insect (n=37, present in
A total of 909 photographs, covering the diet of 28 species). Among lower rank
144 avian species and obtained between taxonomic categories, the Red-swamp
January 2003 and October 2018, were Crayfish Procambarus clarkii (n=28, present
found to provide dietary information (Table in the diet of 12 species), the European Eel
1, Appendix 1). These include 78 regularly Anguilla anguilla (n=18, present in the diet
occurring species for which there was no of 7 species), the European Mole Cricket
available dietary data for Portugal, even Gryllotalpa gryllotalpa (n=15, present in
if anecdotal (Catry et al. 2010), for which the diet of 8 species), the Iberian Green Frog
there were 359 photographs. There were Pelophylax perezi (n=15, present in the diet
also four species that do not regularly of 8 species), and Quercus sp. acorns (n=15,
occur in Portugal (Falco vespertinus, present in the diet of 3 species) stand out as
Larus hyperboreus, Pluvialis dominica most commonly taken food items. However,
and Porphyrio martinica). The recording the importance of the latter may results both
of several hundred food items for such a from their importance in avian diets or from
large number of species clearly evidences being easier to identify in photographs.
the potential value of this method for
obtaining data on avian diets. The number

06
Dietas das aves de Portugal baseadas em fóruns de fotografia online

Fig. 1- Map with the 262 locations (black camera icons) where the 909 photographs used to analyse avian diets were obtained.

Fig. 1 - Mapa com os 262 locais (símbolos pretos) onde foram obtidas as 909 fotografias usadas para estudar dietas de aves.

07
Portuguese bird diets based on Internet photography forums

Table 1- Consumed food items detected in photographs of Portuguese birds published on the “Aves de Portugal Continental”
Facebook page. For each bird species I present the proportion of food items represented by each main group (mostly at the
Class taxonomic rank, but also distinguishing fruits and seeds) and within each group, between brackets, all the lower rank
identifications that were possible. I also present the number of photos used (sample size), the geographic coverage dividing
Continental Portugal in North (N), Centre (C) and South (S; see Methods), and the seasons when photos were taken (Wi:
winter, Sp: spring, Su: summer, Au: autumn). n: necrophagy; J: juvenile or hatchling; e: egg.

Tabela 1 - Itens alimentares consumidos por aves em Portugal, de acordo com fotografias publicadas na página de Facebook
“Aves de Portugal Continental”. Para cada espécie de ave é apresentada a proporção de itens pertencentes a cada grupo
alimentar (sobretudo ao nível taxonómico de Classe, mas também distinguindo frutos e sementes), assim como a lista de todos
os itens identificados até níveis taxonómicos inferiores. É também apresentada o número de fotografias utilizadas (tamanho
da amostra), a cobertura geográfica dividindo Portugal em Norte (N), Centro (C) e Sul (S; ver Métodos) e as estações do ano
em que as fotografias foram obtidas (Wi: inverno, Sp: primavera, Su: verão, Au: outono). n: necrofagia; J: presa juvenil; e: ovo.

SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE

Accipiter gentilis Birds (100%: Carduelis carduelis


2 C,S Su,Au
Northern Goshawk and Anas platyrhynchos)

Accipiter nisus
1 Birds (100%: Passer domesticus) N Sp
Eurasian Sparrowhawk

Acrocephalus arundinaceus
2 Insects (100%: Lepidoptera larvae and Diptera) S Sp,Au
Great Reed Warbler

Aegithalus caudatus Fruits (33%: Diospyrus kaki); Insects (33%:


3 N,C Su,Au
Long-tailed Tit Coleoptera larvae); Arachnids (33%: Araneae)

Fishes (75%: Anguilla anguillaJ,


Cobitis paludica, Cyprinidae, Mugilidae
Alcedo atthis and unidentified); Crustaceans Wi,Sp,
Common Kingfisher 40 N,C,S
(20%: unidentified shrimp and Procambarus Su,Au
clarkiiJ); Amphibians (2.5%: Pelophylax perezi);
Reptiles (2.5%: Timon lepidusJ)

Anthus campestris Arachnids (67%, Araneae);


3 S Su
Tawny Pipit Insects (33%: Lepidoptera larvae)

Anthus petrosus
1 Crustaceans (100%: Ligia oceanica) C Au
Rock Pipit

Anthus pratensis
1 Insects (100%: Lepidoptera larvae) N Wi
Meadow Pipit

Aquila fasciata Birds (50%: Columba livia); Mammals (50%:


2 N,S Wi,Su
Bonelli’s Eagle Oryctolagus cuniculus)

Aquila pennata
3 Birds (100%: Columba livia and Larus fuscus) C Sp,Au
Booted Eagle

Fishes (80%: Anguilla anguilla, Barbus barbus,


Belone belone, Cyprinus carpio, Dicentrarchus
labrax, Solea solea, Trachurus trachurus,
Ardea cinerea Cyprinidae, Mugilidae, Petromyzontidae
Wi,Sp,
Grey Heron 39 and unidentified); Mammals (7.5%: Rattus N,C,S
Su,Au
sp.); Crustaceans (5%: Procambarus clarkii);
Amphibians (2.5%: Pleurodeles waltl);
Cephalopods (2.5%: Sepia officinalis); Insects
(2.5%: Odonata)

Ardea purpurea Amphibians (50%: Pelophylax perezi); Fishes


4 N,C Wi,Sp,Su
Purple Heron (25%: unidentified); Reptiles (25%: Natrix maura)

08
Dietas das aves de Portugal baseadas em fóruns de fotografia online

SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE

Ardeola ralloides Amphibians (67%: Pelophylax perezi, Ranidae);


6 C Wi,Su
Squacco Heron Crustaceans (33%: Procambarus clarkii)

Arenaria interpres Gastropods (100%: Patella vulgata,


2 N,S Sp,Su
Ruddy Turnstone Phorcus lineatus)

Asio flammeus
1 Mammals (100%: Rattus sp.) C Wi
Short-eared Owl

Asio flammeus
4 Mammals (100%: Apodemus sylvaticus, Muridae) C Sp,Su,Au
Short-eared Owl

Insects (43%: Gryllotalpa gryllotalpa, Coleoptera,


Athene noctua
7 Lepidoptera larvae); Mammals (43%: Muridae); N,C,S Sp,Au
Little Owl
Reptiles (14%: Lacerta schreiberi)

Botaurus stellaris
2 Crustaceans (100%: Procambarus clarkii) C Wi
Eurasian Bittern

Reptiles (25%: Timon lepidus, Chalcides striatus,


Serpentes); Mammals (25%: Talpa occidentalis,
Bubulcus ibis Rattus norvegicus); Insects (17%: Gryllotalpa Wi,Sp,
12 N,C,S
Cattle Egret gryllotalpa, unidentified); Amphibians (17%: Su,Au
Pelophylax perezi); Arachnids (8%: Araneae);
Crustaceans (8%: Procambarus clarkii)

Burhinus oedicnemus
2 Insects (100%: Coleoptera, unidentified) S Su
Eurasian Thick-knee

Mammals (34%: Rattus norvegicus, Muridae,


Soricidae); Amphibians (22%: Ranidae, Hyla
Buteo buteo
9 arborea); Crustaceans (22%: Procambarus N,C,S Wi,Sp,Au
Eurasian Buzzard
clarkii); Reptiles (11%: Serpentes); Birds
(11%: Limosa limosa)
Bivalves (20%: unidentified); Polychaetes
Calidris alba (20%: unidentified); Crustaceans
5 N,C,S Wi,Sp,Su
Sanderling (20%: Amphipoda); Fishes (20%: Mugilidaen);
Insects (20%: unidentified larvae)

Calidris alpina
1 Polychaetes (100%: unidentified) C Au
Dunlin

Calidris canutus Bivalves (50%: unidentified);


2 N,S Wi,Sp
Red Knot Polychaetes (50%: unidentified)

Carduelis carduelis Seeds (83%: Cynareae, unidentified);


6 C,S Wi,Sp,Au
European Goldfinch Fruits (17%: Arbutus unedo)

Carduelis chloris Seeds (50%: Helianthus sp., unidentified); Fruits


4 N,C,S Wi,Sp,Au
European Greenfinch (50%: unidentified berry)

Carduelis spinus Seeds (80%: Betula celtiberica, Platanus sp., Pinus


5 N,C Wi,Au
Eurasian Siskin pinea); Fruits (20%: Arbutus unedo)

Cercotrichas galactotes
2 Insects (100%: Orthoptera) S Sp,Su
Rufous-tailed Scrub-robin

09
Portuguese bird diets based on Internet photography forums

SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE

Certhia brachydactyla Insects (80%: Forficulidae, Lepidoptera);


5 N,C,S Wi,Sp,Au
Short-toed Treecreeper Arachnids (20%: Araneae)

Charadrius hiaticula
6 Polychaetes (100%: unidentified) N,C Wi,Su,Au
Common Ringed Plover

Chlidonias niger Fishes (50%: unidentified); Insects


2 C Su,Au
Black Tern (50%: Blattoidea)

Ciconia ciconia Crustaceans (67%: Procambarus clarkii);


3 C,S Wi,Sp,Su
White Stork Mammals (33%: Oryctolagus cuniculus)

Cinclus cinclus Insects (100%: Odonata, Odonata larvae and


13 N,C Sp
White-throated Dipper nymphs, Ephemeroptera, unidentified larvae)

Circaetus gallicus
2 Reptiles (100%: Rhinechis scalaris, Serpentes) C Sp,Su
Short-toed Snake-eagle

Circus aeruginosus Amphibians (50%: Anura); Birds (25%: Anas


4 N,C Sp,Au
Western Marsh-harrier platyrhynchos); Insects (25%: unidentified)

Circus pygargus Reptiles (50%: Serpentes); Mammals


2 S Sp,Su
Montagu’s Harrier (50%: Muridae)

Cisticola juncidis
1 Insects (100%: Orthoptera) S Au
Zitting Cisticola

Insects (100%: Lymantria dispar larvae,


Clamator glandarius
8 Thaumetopoea pityocampa larvae, Lepidoptera C,S Sp,Su
Great Spotted Cuckoo
larvae, Lepidoptera, unidentified larvae

Coccothraustes coccothraustes
5 Seeds (100%: unidentified) C Sp,Su
Hawfinch

Insects (60%: Gryllotalpa gryllotalpa,


Coracias garrulus
5 Orthoptera, Tipulidae); Centipedes (20%: C,S Sp,Su
European Roller
Scolopendromorpha); Mammals (20%: Muridae)

Corvus corone
1 Insects (100%: Odonata) C Su
Carrion Crow

Corvus monedula
2 Birds (100%: Delichon urbicumJ, Columba liviaJ) S Sp
Eurasian Jackdaw

Cuculus canorus Insects (100%: Thaumetopoea pityocampa larvae,


6 N,C,S Sp,Su
Common Cuckoo Lepidoptera larvae, unidentified larvae)

Fruits (57%: Prunus sp., Olea europaea,


Cyanopica cyanus
7 Eriobotrya japonica); Insects (43%: C,S Sp
Azure-winged Magpie
Coleoptera, unidentified

Dendrocopus major Insects (67%: Lepidoptera larvae, unidentified


3 C,S Wi,Sp,Su
Great Spotted Woodpecker larvae); Seeds (33%: unidentified)

Dendrocopus minor
5 Insects (100%: Myrmicidae, unidentified larvae) C,S Sp,Su
Lesser Spotted Woodpecker

10
Dietas das aves de Portugal baseadas em fóruns de fotografia online

SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE

Egretta alba
2 Fishes (100%: Cyprinidae, Lepomis gibbosus) C Wi,Au
Great White Egret

Fishes (63%: Anguilla anguilla, Solea solea,


Lepomis gibbosus, Gobiidae, Mugilidae,
Egretta garzetta
16 unidentified); Crustaceans (25%: Carcinus N,C,S Wi,Su,Au
Little Egret
maenas, Procambarus clarkii); Polychaetes
(6%: unidentified); Insects (6%: Odonata)

Elanus caeruleus Mammals (92%: Mus sp., Rattus sp., Microtus Wi,Sp,
13 N,C,S
Black-winged Kite sp., Muridae); Birds (8%: Motacilla alba) Su,Au

Emberiza cia Insects (50%: unidentified larvae);


2 S Sp
Rock Bunting Arachnids (50%: Araneae)

Emberiza cirlus
3 Seeds (100%: Avena sp., unidentified) C,S Wi,Su,Au
Cirl Bunting

Emberiza citrinella
1 Insects (100%: Orthoptera) N Su
Yellowhammer

Insects (29%: unidentified larvae);


Erithacus rubecula Oligochaetes (29%: Lumbricidae); Fruits
7 N,C Wi,Sp,Au
European Robin (29%: Pistacia lentiscus, Rubus sp.);
Polychaetes (13% unidentified)

Falco columbarius
2 Birds (100%: Motacilla alba, Passeriformes) C Wi
Merlin

Insects (56%: Orthoptera); Mammals (22%:


Falco naumanni
9 Muridae); Reptiles (11%: Chalcides sp.); S Sp,Su
Lesser Kestrel
Centipedes (11%: Scolopendra cingulata)

Falco peregrinus Birds (100%: Streptopelia decaocto,


5 C,S Wi,Sp
Peregrine Falcon Columba livia, Calidris alpina)

Falco subbuteo Birds (50%: Passer domesticus);


2 N,C Sp
Eurasian Hobby Insects (50%: unidentified)

Mammals (44%: Mus sp., Muridae);


Amphibians (28%: Pelophylax perezi, Anura);
Falco tinnunculus Wi,Sp,
18 Birds (22%: Passer domesticus, Sturnus N,C,S
Common Kestrel Su,Au
unicolor, Columba livia, Carduelis chloris);
Reptiles (6%: Tarentola mauritanica)

Falco vespertinus
1 Insects (100%: Orthoptera) C Sp
Red-footed Falcon

Ficedula hypoleuca
2 Insects (100%: Pararge aegeria, Coleoptera larvae) N Au
European Pied Flycatcher

Fringilla coelebs
1 Insects (100%: Lepidoptera larvae) N Su
Eurasian Chaffinch

Fringilla montifringilla
1 Fruits (100%: unidentified berry) C Au
Brambling

11
Portuguese bird diets based on Internet photography forums

SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE

Galerida cristata
3 Insects (100%: Orthoptera, unidentified) C,S Sp
Crested Lark

Gallinago gallinago
2 Oligochaetes (100%: Lumbricidae) C Wi
Common Snipe

Fruits (70%: Quercus sp., Eryobotrya japonica,


Juglans regia, Ficus carica); Insects
Garrulus glandarius
23 (17%: Orthoptera, Diptera, unidentified); N,C,S Wi,Sp,Au
Eurasian Jay
Birds (9%: Sylvia atricapillaJ, Turdus merulae);
Seeds (4%: unidentified)

Gavia immer Fishes (50%: Anguilla anguilla); Crustaceans


2 N Wi,Au
Common Loon (50%: Carcinus maenas)

Gelochelidon nilotica
1 Insects (100%: Odonata) C Su
Common Gull-billed Tern

Glareola pratincola Insects (100%: Gryllotalpa gryllotalpa,


6 C Sp,Su
Collared Pratincole Crocothemis sp., Odonata, unidentified)

Gyps fulvus
6 Mammals (100%: Ovis ariesn, Bos taurusn) S Wi,Su
Griffon Vulture

Haematopus ostralegus Bivalves (67%: Solen marginatus, unidentified);


3 N,C,S Wi,Au
Eurasian Oystercatcher Gastropods (33%: Gibbula umbilicalis)

Hippolais polyglotta Insects (100%: Forficulidae, Hymenoptera,


3 C Sp,Su
Melodious Warbler unidentified)

Hirundo rustica
3 Insects (100%: unidentified) N,C,S Sp.Su
Barn Swallow

Jynx torquilla
5 Insects (100%: Myrmicidae, unidentified) C,S Sp,Su,Au
Eurasian wryneck

Lanius collurio Insects (67%: Orthoptera, unidentified);


3 N Sp,Su
Red-backed Shrike Arachnids (33%: Araneae)

Insects (60%: Orthoptera, Coleoptera, Odonata);


Lanius meridionalis
5 Mammals (20%: Muridae); Reptiles N,C,S Wi,Sp
Iberian Grey Shrike
(20%: Podarcis bocagei)

Insects (67%: Gryllotalpa gryllotalpa, Orthoptera,


Lanius senator Coleoptera, Odonata, Lepidoptera larvae,
12 N,C,S Wi,Sp,Su
Woodchat Shrike unidentified); Centipedes (16.5%: Scolopendra
sp.); Arachnids (16.5%: Araneae)

Larus audouinii
1 Crustaceans (100%: Procambarus clarkii) C Wi
Audouin’s Gull

Crustaceans (45.5%: Procambarus clarkii,


Carcinus maenas, unidentified crab); Fishes
Larus fuscus
11 (45.5%: Mugil cephalus, Halobatrachus N,C Wi,Su,Au
Lesser Black-backed Gull
didactylus, Anguilla anguilla, Mugilidae,
unidentified); Birds (9%: Columba livia)

12
Dietas das aves de Portugal baseadas em fóruns de fotografia online

SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE

Larus hyperboreus
1 Fishes (100%: Merluccius merluccius) N Wi
Glaucous Gull

Birds (25%: Columba livia, Anas platyrhynchosJ);


Cephalopods (12.5%: Sepia officinalis); Barnacles
Larus michahellis (12.5%: Pollicipes pollicipes); Starfishes (12.5%: Wi,Sp,
8 N,C,S
Yellow-legged Gull unidentified); Fishes (12.5%: Scyliorhinus Su,Au
caniculaJ); Mammals (12.5%: Rattus sp.);
Human refuse (12.5%)

Fishes (50%: Diplodus sargus, Silurus glanis);


Larus ridibundus
4 Polychaetes (25%: unidentified); Algae (25%: N,C,S Su,Au
Black-headed Gull
Ulva sp.)

Limosa lapponica
1 Polychaetes (100%: unidentified) N Au
Bar-tailed Godwit

Limosa limosa Polychaetes (50%: unidentified); Bivalves (50%:


2 N,C Wi,Su
Black-tailed Godwit Scrobicularia plana)

Loxia curvirostra
2 Seeds (100%: Pinus pinea) N Wi
Red Crossbill

Lullula arborea
2 Insects (100%: unidentified, unidentified larvae) N Su
Wood Lark

Insects (99%: Apis melifera, Bombus terrestris,


Xylocopa violacea, Vespa crabro, Vespula vulgaris,
Boyeria irene, Cordulegaster boltonii, Orthetrum
chrysostigma, Sympetrum fonscolombii,
Merops apiaster
68 Hippotion celerio, Papilio machaon, Maniola N,C,S Sp,Su
European Bee-eater
jurtina, Vanessa atalanta, Vespidae, Sphingidae,
Cicadidae, Coleptera, Diptera, Orthoptera,
Hemiptera, Odonata, Plecoptera, unidentified);
Crustaceans (1%: Uca tangeri)

Miliaria calandra
5 Insects (100%: Orthoptera, Lepidoptera larvae) C,S Sp
Corn Bunting

Fishes (55%: Micropterus salmoides, Mugilidae,


Cyprinidae, unidentified); Insects (9%:
Milvus migrans
11 Orthoptera); Amphibians (9%: Pelophylax N,C Sp,Su
Black Kite
perezi); Reptiles (9%: Serpentesn); Mammals
(9%: Rattus sp.); Birds (9%: Tringa totanus)

Monticola saxatilis
1 Insects (100%: Gryllotalpa gryllotalpa) N Sp
Rufous-tailed Rock-thrush

Insects (47%: Bombus terrestris, Gryllotalpa


gryllotalpa, Coleoptera, Hymenoptera,
Monticola solitarius unidentified larvae); Centipedes
15 N,C,S Sp
Blue Rock-thrush (26.5%: Scolopendra cingulata); Reptiles
(25.5%: Psammodromus algirus, Tarentola
mauritanica, Chalcides bedriagai)

13
Portuguese bird diets based on Internet photography forums

SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE

Morus bassanus
3 Fishes (100%: Belone belone, unidentified) N,C,S Wi,Au
Northern Gannet

Motacilla alba
3 Insects (100%: Hymenoptera, unidentified) N,S Sp,Su,Au
White Wagtail

Insects (50%: Ephemeroptera, unidentified


Motacilla cinerea Wi,Sp,
6 larvae); Fishes (33%: unidentified); Crustaceans N,C,S
Grey Wagtail Su,Au
(17%: Palaemon sp.)

Motacilla flava Insects (75%: Dytiscidae, Diptera, Lepidoptera


4 N Sp
Yellow Wagtail larvae); Oligochaetes (25%: Lumbricidae)

Muscicapa striata
1 Insects (100%: Lepidoptera) C Au
Spotted Flycatcher

Numenius arquata
1 Crustaceans (100%: unidentified crab) N Wi
Eurasian Curlew

Crustaceans (80%: Carcinus maenas, Uca


Numenius phaeopus
5 tangeri, unidentified crab); Bivalves (20%: N,S Wi,Sp,Au
Whimbrel
Cerastoderma edule)

Fishes (90%: Anguilla anguilla, Carassius auratus,


Nycticorax nycticorax
10 Mugil cephalus, Chondrostoma sp., Mugilidae, C Sp,Su
Black-crowned Night-heron
Cyprinidae); Reptiles (10%: Natrix maura)

Oenanthe hispanica
2 Insects (100%: Orthoptera, Coleoptera) S Sp
Black-eared Wheatear

Oenanthe oenanthe
1 Insects (100%: unidentified) N Sp
Northern Wheatear

Oriolus oriolus Fruits (86%: Ficus carica, Morus alba, Prunus


7 N,C,S Sp,Su
Eurasian Golden Oriole sp.); Insects (14%: Cicadidae)

Otus scops
1 Insects (100%: Lepidoptera) N Su
Eusarian Scops-owl

Fishes (100%: Liza ramada, Mugil cephalus,


Pandion haliaetus Dicentrarchus labrax, Sparus aurata, Carassius Wi,Sp,
59 N,C,S
Osprey auratus, Barbus barbus, Cyprinus carpio, Su,Au
Mugilidae, unidentified)

Parus ater Insects (50%: Coleptera); Arachnids


2 N Sp
Coal Tit (50%: Araneae)

14
Dietas das aves de Portugal baseadas em fóruns de fotografia online

SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE

Insects (50%: Lepidoptera larvae, unidentified


Parus caeruleus larvae, unidentified); Fruits (25%: Diospyrus kaki,
12 N,C,S Wi,Sp
Blue Tit Prunus sp.); Arachnids (17%: Araneae); Seeds
(8%: unidentified)

Parus cristatus
1 Seeds (100%: Pinus pinea) C Wi
Crested Tit

Insects (55%: Lepidoptera larvae, unidentified);


Parus major Fruits (23%: Quercus sp., unidentified berry);
9 N,C,S Sp,Au
Great Tit Arachnids (11%: Araneae); Seeds (11%:
unidentified)

Passer domesticus Seeds (70%: Helianthus sp., unidentified); Insects


10 N,C,S Sp,Su
House Sparrow (30%: Coleptera, Hemiptera, unidentified larvae)

Passer montanus Seeds (50%: unidentified); Insects (50%:


2 N Sp,Su
Eurasian Tree Sparrow unidentified larvae)

Phalacrocorax aristotelis
1 Fishes (100%: Gobiidae) C Au
European Shag

Fishes (100%: Anguilla anguilla, Solea solea,


Phalacrocorax carbo Conger conger, Scorpaena scrofa, Micropterus
21 N,C,S Wi,Sp,Au
Great Cormorant salmoides, Silurus glanis, Cyprinus carpio, Barbus
sp., Mugilidae, Pleuronectiformes, unidentified)

Insects (89%: Tipulidae, Tettigonidae,


Phoenicuros ochruros Lepidoptera, Lepidoptera larvae, Diptera,
9 N Sp,Su,Au
Black Redstart Hymenoptera, unidentified larvae), Arachnids
(11%: Araneae)

Insects (57%: Xanthogramma sp., Diptera,


Phylloscopus collybita ibericus
7 unidentified, unidentified larvae); Fruits (29%: C,S Wi,Au
Common/Iberian Chiffchaff
Diospyrus kaki); Nectar (Aloe sp.)

Phylloscopus trochilus
2 Insects (100%: unidentified) N Su,Au
Willow Warbler

Pica pica Insects (50%: Lepidoptera larvae), Birds (25%:


4 N,C,S Wi,Sp,Au
Eurasian Magpie unidentified egg); Fruits (25%: Quercus sp.)

Platalea leucorodia Fishes (80%: Mugilidae, Pleuronectiformes,


5 N,C Wi,Sp,Au
Eurasian Spoonbill unidentified); Crustaceans (Procambarus clarkii)

Crustaceans (75%: Procambarus clarkii);


Plegadis falcinellus
8 Amphibians (25%: Pelophylax perezi, Pleurodeles C,S Wi,Sp,Au
Glossy Ibis
waltl)

Pluvialis apricaria
2 Insects (100%: unidentified larvae) N,S Au
Eurasian Golden Plover

Pluvialis dominica Polychaetes (67%: unidentified); Crustaceans


3 N Au
American Golden Plover (33%: unidentified crab)

Pluvialis squatarola
5 Polychaetes (100%: unidentified) N,C Wi,Sp,Au
Grey Plover

15
Portuguese bird diets based on Internet photography forums

SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE

Podiceps cristatus Fishes (100%: Solea solea, Conger conger,


3 S Sp,Su
Great Crested Grebe unidentified)

Porphyrio martinica
1 Amphibians (100%: Pelophylax perezi) C Au
Americn Purple Gallinule

Fruits (100%: Celtia australis, Melia azedarach,


Psittacula krameri Wi,Sp,
6 Cupressus lusitanica, Eryobotria japonica, C
Ring-necked Parakeet Su,Au
Morus sp., Acacia sp.)

Regulus ignicapillus
2 Insects (100%: Orthoptera) C Wi,Au
Firecrest

Insects (85%: Gomphidae, Odonata, Coleoptera,


Saxicola rubicola Orthoptera, Diptera, Lepidoptera larvae, Wi,Sp,
13 N,C
European Stonechat unidentified, unidentified larvae); Centipedes Su,Au
(7.5%: unidentified); Reptiles (7.5%: Podarcis sp.)

Insects (50%: Coleoptera, Lepidoptera larvae,


Sitta europaea
6 unidentified); Seeds (50%: Pinus pinea, N,C,S Wi,Sp,Su
Wood Nuthatch
unidentified)

Sterna albifrons
1 Fishes (100%: unidentified) C Sp
Little Tern

Sterna sandvicensis
3 Fishes (100%: Ammodytes tobianus, unidentified) N,C,S Wi,Au
Sandwich Tern

Insects (43%: Gryllidae, Diptera, unidentified


Sturnus unicolor
7 larvae); Fruits (43%: Ficus carica, Prunus sp., N,C,S Sp,Au
Spotless Starling
Rubus sp.); Oligochaetes (16%: Lumbricidae)

Sturnus vulgaris
1 Fruits (100%: Diospyros kaki) N Au
Common Starling

Fruits (90%: Arbutus unedo, Eriobotrya japonica,


Sylvia atricapilla Diospyros kaki, Pyracantha sp., Aracacea,
10 N,C,S Wi,Sp,Au
Blackcap unidentified berry); Gastropods
(10%: unidentified snail)

Sylvia borin
1 Fruits (100%: Ficus carica) C Su
Garden Warbler

Sylvia cantillans
1 Insects (100%: Vespidae) S Au
Subalpine Warbler

Sylvia communis
3 Fruits (100%: Rubus sp., unidentified berry) N,S Su,Au
Common Whitethroat

Fruits (50%: Pyracantha sp., Rubus sp.,


Sylvia melanocephala Wi,Sp,
6 Diospyros kaki); Insects (33%: Lepidoptera N,C,S
Sardinian Warbler Su,Au
larvae); Arachnids (17%: Araneae)

Sylvia undata Insects (67%: Tipulidae, Orthoptera); Arachnids


3 N,C,S Sp,Su
Dartford Warbler (33%: Araneae)

16
Dietas das aves de Portugal baseadas em fóruns de fotografia online

SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE

Tachybaptus ruficollis
1 Crustaceans (100%: unidentified shrimp) C Wi
Little Grebe

Tringa nebularia Crustaceans (67%: Carcinus maenas, unidentified


3 N,C Wi,Su
Common Greenshank crab); Polychaetes (33%: unidentified)

Tringa ochropus
1 Crustaceans (100%: Atyaephyra desmarestii) S Su
Green Sandpiper

Troglodytes troglodytes Insects (100%: Clytus arietis, Odonata,


8 N,C Wi,Sp
Eurasian Wren Lepidoptera, unidentified larvae, unidentified)

Oligochaetes (50%: Lumbricidae); Fruits


(24%: Ficus carica, Diospyros kaki, Citrus
sinensis, Prunus sp., Cotoneaster sp.,
Turdus merula Wi,Sp,
30 unidentified berry); Insects (17%: unidentified N,C,S
Common Blackbird Su,Au
insect, unidentified larvae); Gastropods (3%:
unidentified snail); Amphibians (3%: Anura);
Arachnids (3%: Araneae)

Turdus philomelus Gastropods (50%: unidentified snail); Oligochaetes Wi,Sp,


6 N,C
Song Thrush (33%: Lumbricidae); Fruits (17%: Diospyros kaki) Su,Au

Tyto alba Mammals (100%: Rattus norvegicus, Apodemus


17 C Wi,Su,Au
Barn Owl sylvaticus, Rattus sp. Muridae)

Insects (92%: Gryllotalpa gryllotalpa,


Upupa epops Thaumetopoea pityocampa larvae, Blattoidea, Wi,Sp,
26 N,C,S
Common Hoopoe Lepidoptera larvae, unidentified larvae, Su,Au
unidentified), Arachnids (8%: Araneae)

Fig. 2- Diet composition of the twelve best sampled species, based on the analysis of photographs posted on the “Aves de
Portugal Continental” Facebook page. Sample sizes: Common Kingfisher, n=40; Grey Heron, n=39; Little Egret, n=16;
Common Kestrel, n=18; Eurasian Jay, n=23; European Bee-eater, n=68; Blue-rock Thrush, n=15; Osprey, n=59; Great
Cormorant, n=21; Common Blackbird, n=30; Barn Owl, n=15; and Eurasian Hoopoe, n=26.

Fig. 2 - Composição da dieta das doze espécies melhor amostradas, de acordo com a análise de fotografias publicadas na
página de Facebook “Aves de Portugal Continental”. Número de amostras: Guarda-rios, n=40; Garça-real, n=39; Garça-
branca-pequena, n=16; Peneireiro-comum, n=18; Gaio, n=23; Abelharuco, n=68; Melro-azul, n=15; Águia-pesqueira, n=59;
Corvo-marinho-de-faces-brancas, n=21; Melro-preto, n=30; Coruja-das-torres, n=15; e Poupa, n=26.

17
Portuguese bird diets based on Internet photography forums

18
Dietas das aves de Portugal baseadas em fóruns de fotografia online

Common Kingfisher Alcedo atthis ary (Moreira 1992), were seldom or never
Kingfishers fed mainly on fish (75%) and observed in the analysed photographs. Such
crustaceans (20%), with two cases of pre- differences could arise from a bias caused by
dation on amphibians and reptiles (Fig. 2). the difficulty in identifying smaller prey in
The diet of this species had not been previ- photographs.
ously studied in Portugal (Catry et al. 2010).
Although kingfishers are known to routinely
consume non-fish prey (e.g. Snow & Perrins Common Kestrel Falco tinnunculus
1998), the present data suggested a much On the 18 analysed Common Kestrel pho-
higher proportion of crustaceans than that tographs, the most common prey were mam-
observed elsewhere in Europe (e.g. Reynolds mals (44%), amphibians (28%) and birds
& Hinge 1996, Vilches et al. 2012, Čech & (22%). Particularly, murid rodents, Iberian
Čech 2015), which may be related to the Green Frog and passerines represented 83%
consumption of the introduced Red-Swamp of identified prey (Fig. 2). The importance of
Crayfish that has become an important prey rodents and passerines for common kestrels
for several mammals and birds in Portugal in Portugal had already been described (Fon-
and southern Spain (Correia 2001). seca 1994), but that study also indicated that
insects, which were absent from the analysed
photographs, represented 38% of prey found
Grey Heron Ardea cinerea in pellets collected around Lisboa. Although
Grey Herons predominantly took fish frogs had been previously recorded as Com-
(80%), with a wide variety of secondary prey mon Kestrel prey in other parts of their range
such as rats Rattus sp., Red-Swamp Crayfish, (e.g. Korpimäki 1985), they typically repre-
Iberian Ribbed Newt Pleurodeles waltl, Com- sent a very small proportion of the diet. The
mon Cuttlefish Sepia officinalis and dragon- large proportion of frogs in the analysed pho-
flies (Odonata, Fig. 2). Similarly to what had tographs was most likely due to a geographic
been described for the Tejo estuary (Moreira bias as these frogs were found exclusively on
1992) and Santo André lagoon (Catry 1993), photographs taken at Ponta da Erva, an agri-
the most common fish prey that could be cultural area north of the Tejo estuary where
identified were mullets (31%) and European they seem to be an important prey for the
Eel (10%, Fig. 2). Although the Red-Swamp Common Kestrel (71% of prey, n=7 photo-
Crayfish has been described as a frequent graphs).
prey for Grey Herons (e.g. Catry 1993, Cor-
reia 2001), it only occurred twice in the 39
photographs that were analysed. Eurasian Jay Garrulus glandarius
Eurasian Jays fed predominantly on plants,
including both fruits (70%) and seeds (4%,
Little Egret Egretta garzetta Fig. 2). Insects (17%) and passerine eggs and
Little Egrets fed mainly upon fish (63%) nestlings (9%) were also observed in the pho-
and crustaceans (25%), with polychaetes tographs. The most frequently recorded fruits
and dragonflies as secondary prey (Fig. 2). were oak Quercus sp. acorns (57%), but jays
Previous work in the Tejo estuary (Moreira were also photographed taking figs Ficus car-
1992) and Boquilobo marsh (Cardoso 1994) ica, walnuts Juglans regia and loquats Erio-
also highlighted the importance of fish and botrya japonica. Although there was no pre-
crustaceans for this species. However some vious published data on their diet in Portugal
prey such as gobies Pomatoschistus sp. and (Catry et al. 2010), jays are also known to
Brown Shrimp Crangon crangon, which were be omnivorous and rely heavily on Quercus
described as common prey in the Tejo estu- sp. acorns in other parts of their range (e.g.

19
Portuguese bird diets based on Internet photography forums

Patterson et al. 1991, Clayton et al. 1996), photographs range from north (Peso da
while being often reported as predators of Régua) to south (Tavira) of the country, the
passerine nests (e.g. Moreira & Mota 1998, majority (87%, n=15) originate from just
Weidinger 2009). two areas, Peso da Régua and Arouca, so
these results may be biased for prey availabil-
ity in those regions. Although there was no
European Bee-eater Merops apiaster previous published information on the diet
The diet of European Bee-eaters consisted of Blue Rock-thrush in Portugal (Catry et
almost exclusively of insects (99%, Fig. 2), al. 2010), insects and other invertebrates, as
with one case of a bird eating the claw of a well as small reptiles and amphibians are also
Fiddler Crab Uca tangeri. Among insects, the reported in their diet in other parts of their
most important were Hymenoptera (46%), range (Snow & Perrins 1998).
but Honey Bees Apis melifera only repre-
sented 19% of prey (Fig. 2). This large relative
importance of Hymenoptera had also been Osprey Pandion haliaetus
reported in various parts of their breeding Osprey was the second most common bird
range (Costa 1991, Inglisa et al. 1993, Kris- species in the analysed photographs (n=59).
tin 1994, Galeotti & Inglisa 2001). However, Unsurprisingly, all photographed Ospreys
this species is also reported to exhibit high were taking fish (Fig. 2). Most of the fish were
diet diversity (e.g. Kristin 1994) with hun- not possible to identify (53%), but mullets
dreds of different insect species listed as prey represented at least 37% of their diet (Fig. 2)
of European Bee-eater (Kristin 1994, Galeotti and are likely to be also a large proportion of
& Inglisa 2001). The analysed photographs the unidentified specimens. The importance
evidence the consumption of at least eight of mullets for Ospreys had already been
insect orders, the most relevant after Hyme- noted in a previous study performed along
noptera being Odonata (13%, including the south-western coast of Portugal (Palma
Boyeria irene, Cordulegaster boltonii, Orth- et al. 1986). However, that study suggested
etrum chrysostigma and Sympetrum fonsco- European Carps Cyprinus carpio were also a
lombii) and Lepidoptera (10%, including key prey for Ospreys, while the present data
Hippotion celerio, Maniola jurtina, Papilio suggested they represent less than 5% of all
machaon and Vanessa atalanta), which dif- taken prey (Fig. 2). Such a difference may
fers from a previous study indicating Coleop- arise from the large proportion of Osprey
tera and Diptera as the main secondary prey photographs obtained in and around estu-
for European Bee-eaters in Portugal (Costa arine areas (83%, n=59), where mullets are
1991). The importance of Honey Bees in bee- very abundant (e.g. Costa & Bruxelas 1989).
eater diet varies depending on the abundance However, estuaries are in fact the most com-
of bee hives (e.g. Costa 1991, Galeotti & monly used habitat by Ospreys wintering in
Inglisa2001), so the prevalence of this prey in Portugal (Torralvo et al. 2018), so the present
the present data set was most likely related to data is likely to reflect the true importance of
the proportion of photographs taken in areas mullets for this piscivorous predator, at least
with and without apiculture. along the Portuguese coast.

Blue Rock-thrush Monticola solitarius Great Cormorant Phalacrocorax carbo


Blue Rock-thrushes fed on insects (47%), Great Cormorants fed exclusively on fish
centipedes (26.5%) and reptiles (26.5%), the (Fig. 2), mainly species found in salt and
most important individual prey being Scol- brackish water (62%), but also fresh water
opendra cingulata (26.5%, Fig. 2). Although species (24%) and European Eels (14%)

20
Dietas das aves de Portugal baseadas em fóruns de fotografia online

which are catadromous migrants. The pro- barn owls occasionally also take birds,
portion of fresh water fishes reflects the pro- amphibians and insects (Catry et al. 2010),
portion of photographs taken in inland water all 15 analysed photographs exhibited rodent
bodies versus those obtained in estuarine prey, 67% of which were rodents from the
areas and along the coast. In salt and brack- family Muridae while the remaining 33%
ish water environments, Great Cormorants were rats (Fig. 2). Voles and shrews were
fed mainly on mullets (29%), eels (14%) absent from the photographs, despite being
and Common Sole Solea solea (10%, Fig. important prey for barn owls in some areas
2), which were also important prey in previ- (e.g. Tomé 1994, Vale-Gonçalves & Cabral
ous studies performed in the Algarve (Grade 2003), but I believe this was not caused by
& Granadeiro 1997), Santo André lagoon identification issues as several photographs
(Catry 1993) and the Sado estuary (Grana- with murids were shown to a micromammal
deiro et al. 2013). Although this species is expert.
widely regarded as an aquaculture pest (e.g.
Garcia 2000), the two most common aqua-
culture fishes in Portugal, European Sea Bass Eurasian Hoopoe Upupa epops
Dicentrachus labrax and Gilthead Seabream Photographed hoopoes were mostly eating
Sparus aurata were not observed in any of the insects, both larvae (50%) and adults (42%),
21 analysed photographs. as well as a few spiders (8%, Fig. 2). The most
frequently recorded adult insects were Euro-
pean Mole Crickets (31%, Fig. 2). The major-
Common Blackbird Turdus merula ity of larvae were impossible to identify, but
Blackbirds relied heavily on earthworms, all identified larvae were Lepidoptera, includ-
which represented 50% of all food items ing one individual of Pine Processionary Tha-
observed in photographs (Fig. 2). Fruits umetopoea pityocampa, a troublesome pest
(23%) and insects (17%) were also observed for pine plantations in Portugal (e.g. Gatto
frequently, with single records of a spider, an et al. 2009). Large insects and their larvae,
anuran and a snail also being taken (Fig. 2). including European Mole Crickets, also form
The diet of this species had not been previ- the bulk of hoopoe diets elsewhere in Europe
ously studied in Portugal, but in other parts (e.g. Snow & Perrins 1998, Fournier & Arlet-
of their range they are known to feed mainly taz 2001) and they have been reported as
on earthworms and insects during spring and important predators of pine processionary
summer, with a higher frequency of fruits and in Italy (Battisti et al. 2000). Although there
berries during autumn and winter (Snow & were no previous detailed studies in Portugal,
Perrins 1998). Similarly, in the present data Catry et al. (2010) already mentioned anec-
set fruits represented 60% of the diet in dotal evidence for the importance of mole
autumn and winter (n=5 photographs), but crickets for hoopoes in Portugal.
just 20% during spring and summer (n=25
photographs).
Biases and other issues of the method,
and way forward
Barn Owl Tyto alba Although photographs posted on inter-
The diet of this species had already been net forums are clearly a valuable source of
widely studied in Portugal (e.g. Buckley dietary data, such data also suffers from sev-
1976, Tomé 1994, Catry et al. 2010, Vale- eral types of biases. Despite the wide terri-
Gonçalves & Cabral 2014), evidencing the torial coverage of the analysed photographs,
importance of small rodents and, to a lesser they tend to be concentrated near human
extent, shrews in barn owl diets. Although settlements. Also, human influenced habitats,

21
Portuguese bird diets based on Internet photography forums

such as urban parks, agricultural areas and lures were still included in this analysis. This
beaches, are much more likely to be sampled may well be the case of micromammal in the
through this method than other less accessi- diets of European Rollers and Lesser Kestrel
ble habitats. In fact, opportunistic data from for although these birds do occasionally con-
citizen science typically suffer from such spa- sume small mammals (Snow & Perrins 1998),
tial biases, the most important factor being they are not as widely consumed as the pres-
path density (Tiago et al. 2017b). This means ent data would suggest (e.g. Catry et al. 2018,
that prey types being photographed are more Rodríguez et al. 2010).
often those that these avian species consume Despite these biases, and the fact that secre-
in human-altered environments. Since there tive species or those that specialize in very
is no control over where the photographs small prey are unlike to be sampled through
are originating from, the dataset can also be this method, I believe internet photogra-
biased in favour of prey that are only com- phy could be an invaluable source of avian
mon in a specific location from which there dietary data. This could best work through
are a disproportionate number of photo- an open web-enabled platform which would
graph, such as the case of frogs in common include both nature photographers and biol-
kestrel diet that was discussed above. How- ogists. Nature photographers could post their
ever, in a larger dataset such issues could be photographs of foraging birds, and these
solved by sub-sampling photographs with a could be later screened by biologists who
geographic stratification. would provide identifications of the prey
Another potential issue, especially in the items being taken. The development of such a
case of scarce species, is that photographers platform would originate an ever increasing
may consistently photograph the same indi- dataset of casuistic observations covering an
vidual, because it is particularly easy to increasing number of avian species. If photo-
access. In that way, data may not accurately graphs could be coupled with data on time,
express the diet of the species, but only of date, location and also habitat, the dataset
that specific individual in a specific location. would be increasingly robust against biases
Data from photographs are also more likely and provide each day a more reliable picture
to be biased in favour of larger prey, which are of avian diets in Portugal as a whole, in spe-
more likely to be identifiable in a photograph. cific regions and also of how diets vary sea-
Although such prey will also likely be more sonally and spatially. This could potentially
important in terms of consumed biomass, it be done through existing biodiversity data-
is possible that the importance of small but bases who already couple random observers
highly frequent prey will be underestimated. and experts to obtain reliable data on the dis-
If such prey are mostly consumed in a spe- tribution and seasonal occurrence of wildlife.
cific season, or through a specific behaviour,
such as during nest provisioning when birds
are more likely to carry prey instead of con- Acknowledgements
suming it on the spot, this may lead to sea-
sonal or behavioural biases. Such biases are I would like to thank the many photogra-
common to most other methods of diet anal- phers and nature lovers who posted the pho-
ysis as there are always prey that will be less tographs that were here used to access avian
likely to be detected by any given method (e.g. diets. The full list would include 300 names,
Rosenberg & Cooper 1990, Pierce & Boyle so I won’t thank each photographer individ-
1991). Additionally, and although I excluded ually, but special thanks are due to Armando
photographs with prey items they were likely Caldas and José Frade who manage the page
provided as lure by photographers, it is and together produced 59 of the photographs
impossible to rule out completely that some that were used. I would also like to thank sev-

22
Dietas das aves de Portugal baseadas em fóruns de fotografia online

eral experts who helped identify food items, Čech, M. & Čech, P. 2015. Non-fish prey
namely Filipe Ribeiro, Israel Silva, Joaquim in the diet of an exclusive fish-eater: the
Tapisso, Miguel Porto, Renato Barragão and common kingfisher Alcedo atthis. Bird
Roland van Steen, as well as two reviewers Study 62: 457-465.
who provided useful comments to an earlier
version of this paper. Chinery, M. 1993. Insects of Britain and
northern Europe. 3rd edition. Harper
Collins Publishers, London.
References
Clayton, N.S., Mellor, R. & Jackson, A. 1996.
Battisti, A., Bernardi. M. & Ghiraldo, C. 2000. Seasonal patterns of food storing in the jay
Predation by the hoopoe (Upupa epops) Garrulus glandarius. Ibis 138: 250-255.
on pupae of Thaumetopoea pityocampa
and the likely influence of other natural Correia, A.M. 2001. Seasonal and
enemies. Biocontrol 45: 311-323. interspecific evaluation of predation by
mammals and birds on the introduced
Bojarska, K. & Selva, N. 2011. Spatial red swamp crayfish Procambarus clarkii
patterns in brown bear Ursus arctos diet: (Crustacea, Cambaridae) in a freshwater
the role of geographic and environmental marsh (Portugal). Journal of Zoology 255:
factors. Mammal Review 42: 120-143. 533-541.

Buckley, J. 1976. Barn owl (Tyto alba) pellets Costa, L.T. 1991. Apiculture and the diet
from Portugal. Boletim da Sociedade of breeding European bee-eater Merops
Portuguesa de Ciências Naturais 16: 133- apiaster. Airo 2: 34-40.
136.
Costa, M.J. & Bruxelas, A. 1989. The
Cardoso, A.C. 1994. Uso do habitat e sucesso structure of fish communities in the Tagus
alimentar dos ardeídeos do Paul do estuary, Portugal, and its role as a nursery
Boquilobo. BSc thesis. Faculty of Sciences for commercial fish species. Scientia
of the University of Lisboa, Lisboa. Marina 53: 561-566.
Catry, I., Sampaio, A., Silva, M.C., Moreira,
F., Franco, A.M.A. & Catry, T. 2018. Ferrand de Almeida, N., Ferrand de Almeida,
Combining stable isotope analysis and P., Gonçalves, H., Sequeira, F., Teixeira, J.
conventional techniques to improve & Ferrand de Almeida, F.. 2001. Anfíbios
knowledge of the diet of the European e répteis de Portugal. FAPAS, Porto.
roller Coracias garrulus. Ibis doi 10.1111/
ibi.12625. Fonseca, J.P. 1994. Aspectos da ecologia
trófica e da biologia da reprodução do
Catry, P. 1993. A avifauna da lagoa de peneireiro-de-dorso-malhado (Falco
Santo André. Caracterização, impacto tinnunculus, Linnaeus, 1758). BSc thesis.
das actividades humanas e propostas de Faculty of Sciences of the University of
gestão. BSc thesis. Faculty of Sciences of Lisboa, Lisboa.
the University of Lisboa, Lisboa.
Fournier, J. & Arlettaz, R. 2001. Food
Catry, P., Costa, H., Elias, G. & Matias, R. provision to nestlings in the hoopoe Upupa
2010. Aves de Portugal. Ornitologia do epops: implications for the conservation
território continental. Assírio & Alvim, of a small endangered population in the
Lisboa. Swiss Alps. Ibis 143: 2-10.

23
Portuguese bird diets based on Internet photography forums

Galeotti, P. & Inglisa, M. 2001. Estimating Lourenço, P.M., Alves, J.A., Catry, T. &
predation impact on honeybees Apis Granadeiro, J.P. 2015. Foraging ecology
melifera L. by European bee-eaters Merops of sanderlings Calidris alba wintering
apiaster L. Revue d’Écologie 56: 373-388. in estuarine and non-estuarine intertidal
areas. Journal of Sea Research 104: 33-40.
Garcia, G.M.D. 2000. A população de corvos-
marinhos-de-faces-brancas Phalacrocorax MacDonald, D. & Barret, P. 1993. Mammals
carbo na Reserva Natural do estuário do of Britain and Europe. Harper Collins
Sado. BSc thesis. Instituto de Conservação Publishers, London.
da Natureza, Setúbal.
Moreira, F. 1992. Aves piscívoras em
Gatto, P., Zocca, A., Battisti, A., Barrento, ecossistemas estuarinos: a dieta da garça-
M.J., Branco, M. & Paiva, M.R. 2009. branca pequena Egretta garzetta e da
Economic assessment of managing garça-real Ardea cinerea num banco de
processionary moth in pine forests: A case- vasa no estuário do Tejo. Airo 3: 9-12.
study in Portugal. Journal of Environmental
Management 90: 683-691. Moreira, M. & Mota, P.G. 1998. Nest
predation in the serin Serinus serinus (Aves:
Grade, N. & Granadeiro, J.P. 1997. Fringillidae) and predator identification
Cormorant wintering in Portugal: the case using artificial nests. Acta Ethologica 1:
o Ria Formosa Natural Park. Supplemento 81-87.
alle Ricerche di biologia della Selvaggina
26: 465-468. Munson, M.A., Caruana, R., Fink, D.,
Hochachka, W.M., Iliff, M., Rosenberg,
Granadeiro, J.P., Catry, T., Catry, P., Pereira, S. K.V., Sheldon, D., Sullivan, B.L., Wood,
& Campos, A. 2013. Distribuição e impacto C. & Kelling, S. 2010. A method for
do corvo-marinho-de-faces-brancas sobre measuring the relative information
as comunidades ictiológicas do estuário do content of data from different monitoring
Sado. Unpublished report. Tróia-Natura protocols. Methods in Ecology and
S.A., Setúbal. Evolution 1: 263-273.

Greenwood, J.J.D. 2007. Citizens, science and Olff, H., Alonso, D.A., Berg, M.P., Eriksson,
bird conservation. Journal of Ornithology B.K., Loreau, M., Piersma, T. & Rooney,
148: Suppl.77–124. N. 2009. Parallel ecological networks in
ecosystems. Philosophical Transactions
Inglisa, M., Galeotti, P. & Taglianti, A.V. 1993. of the Royal Society of London B 364:
The diet of a costal population of European 1755−1779.
bee-eater (Merops apiaster) compared to
prey availability (Tuscany, central Italy). Palma, L., Fonseca, L. & Beja, P. 1986.
Bolletino di Zoologia 60: 307-310. A população residual de Pandion
haliaetus em Portugal de 1979-1986 -
Korpimäki, E. 1985. Diet of the kestrel Falco fenologia, produtividade, regime trófico e
tinnunculus in the breeding season. Ornis conservação. V Conferência Internacional
Fennica 62: 130-137. sobre Rapinas Mediterrâncias, Évora.

Kristin, A. 1994. Breeding biology and diet of Patterson, I.J., Cavallini, P. & Rolando, A.
the bee-eater (Merops apiaster) in Slovakia. 1991. Density, range size and diet of the
Biologia, Bratislava 49: 18-23. European jay Garrulus glandarius in the

24
Dietas das aves de Portugal baseadas em fóruns de fotografia online

Maremma Natural Park, Tuscany, Italy, in Sulivan, B.L., Wood, C.L., Iliff, M.J., Bonney,
summer and autumn. Ornis Scandinavica R.E., Fink, D. & Kelling, S. 2009. eBird:
22: 79-87. a citizen-based bird observation network
in the biological sciences. Biological
Pierce, G.J. & Boyle, P.R. 1991. A review of Conservation 142: 2282-2292.
methods for diet analysis in piscivorous
marine mammals. Oceanography and Terraube, J. &Arroyo, B. 2011. Factors
Marine Biology, an Annual Review 29: influencing diet variation in a generalist
409-486. predator across its range distribution.
Biodiversity and Conservation 20: 2111-
Piersma, T. 2012. What is habitat quality? 2131.
Dissecting a research portfolio on
shorebirds. In: Fuller, R.J. (ed) Birds Thébault, E. & Loreau, M. 2003. Food-web
and habitat: relationships in changing constraints on biodiversity−ecosystem
landscapes. Cambridge University Press, functioning relationships. Proceedings
Cambridge, pp. 383−407. of the Natural Academy of Sciences 100:
14949−14954.
Pimm, S.L., Lawton, J.H. & Cohen, J.E. 1991.
Food web patterns and their consequences. Tiago, P., Pereira, H.M. & Capinha, C. 2017a.
Nature 350: 669−674. Using citizen science data to estimate
climatic niches and species distributions.
Reynolds, S.J. & Hinge, M.D.C. 1996. Foods Basic and Applied Ecology 20: 75-85.
brought to the nest by breeding kingfishers
Alcedo atthis in the New Forest of southern Tiago, P., Ceia-Hasse, A., Marques, T.A.,
Englang. Bird Study 43: 96-102. Capinha, C. & Pereira, H.M. 2017b. Spatial
distribution of citizen science casuistic
Rodríguez, C., Tapia, L., Kieny, F. & observations for different taxonomic
Bustamante, J. 2010. Temporal changes groups. Scientific Reports 7: 12832.
in the lesser kestrel (Falco naumanni) diet
during the breeding season in southern Tomé, R. 1994. A coruja-das-torres (Tyto
Spain. Journal of Raptor Research 44: alba) no estuário do Tejo: fenologia,
120-128. dinâmica populacional, utilização do
espaço e ecologia trófica. BSc thesis.
Rosenberg, K.V. & Cooper, R.J. 1990. Faculty of Sciences of the University of
Approaches to avian diet analysis. Studies Lisboa, Lisboa.
in Avian Biology 13: 80-90.
Torralvo, C.A., Martín, B., Elias, G., Tomás, J.,
Rubolini, D., Møller, A.P., Rainio, K. Onrubia, A., González-Broco, C. & Ferrer,
& Lehikoinen, E. 2007. Intraspecific M. 2018. Increase of the wintering osprey
consistency and geographic variability population in the Iberian Peninsula. III
in temporal trends of spring migration International Congress on Bird Migration
phenology among European bird species. and Global Change, Tarifa.
Climate Research 35: 135-146.
Vale-Gonçalves, H.M. & Cabral, J.A. 2014.
Snow, D.W. & Perrins, C.M. 1998. The birds New records on the distribution of three
of the Western Palearctic. Concise Edition. rodent species in NE Portugal from barn
Oxford University Press, London & New owl (Tyto alba) diet analysis. Galemys 26:
York. 100-104.

25
Portuguese bird diets based on Internet photography forums

Vilches, A., Miranda, R. & Arizaga, J.


2012. Fish prey selection by the common
kingfisher Alcedo atthis in Northern
Iberia. Acta Ornithologica 47: 169-177.

Weidinger, K. 2009. Nest predators of woodland


open-nesting songbirds in Central Europe.
Ibis 151: 352-360.

26
Censo deVOLUME
aves nos rios
26 Corubal2019
e Fefine, Guiné-Bissau

Results from an avifaunal survey


along the Corubal and Fefine
rivers, Guinea-Bissau
Resultados de um censo de aves
realizado ao longo dos rios Corubal
e Fefine, Guiné-Bissau

Paulo Catry1*, Miguel Lecoq²,


Mohamed Henriques³, Pierre
Campredon4, José Pedro Granadeiro3

1 MARE, Marine and Environmental Sciences Centre,


ISPA-Instituto Universitário, Rua Jardim do Tabaco 34,
1149-041 Lisbon, Portugal.

2 Rua Barão de Sabrosa, n.º 29 – 1.º, 1900-087 Lisbon,


Portugal

3 CESAM & Departamento de Biologia Animal, Facul-


dade de Ciências da Universidade de Lisboa, Campo
Grande, 1749-016 Lisbon, Portugal

4 53, Rua V. Costa – Bissau, Guinea-Bissau

* Corresponding author: paulo.catry@gmail,com

ABSTRACT
A waterbird survey was carried out along 122 km of the Corubal and Fefine rivers, eastern
Guinea-Bissau, on 6-12 December 2018. Several river specialists were recorded, such as Pel’s
Fishing Owl Scotopelia peli, White-backed Night Heron Calherodius leuconotus, Egyptian Plo-
ver Pluvianus aegyptius and White-headed Lapwing Vanellus albiceps. Other noteworthy river
species present in the area include White-crested Tiger Heron Tigriornis leucolopha and Rock
Pratincole Glareola nuchalis. Some wetland and coastal birds that are common elsewhere in the
country were surprisingly rare or absent (for example African Fish Eagle Haliaeetus vocifer and
Osprey Pandion haliaetus were both completely absent).

Keywords: Boé, Dulombi, Guinea-Bissau, Pluvianus, Scotopelia

27
Bird survey in the rivers Corubal and Fefine, Guinea-Bissau

RESUMO
Foi realizado um censo de aves aquáticas ao longo de 122 quilómetros dos rios Corubal e
Fefine, no leste da Guiné-Bissau, de 6 a 12 de Dezembro de 2018. Foram detetadas várias aves
típicas de rios, como o Corujão-pesqueiro Scotopelia peli, a Garça-noturna-de-dorso-branco
Calherodius leuconotus, a Ave-do-crocodilo Pluvianus aegyptius e o Abibe-de-gola-branca
Vanellus albiceps. Outras aves especialistas de rios que ocorrem na zona incluem a Garça-tigre
Tigriornis leucolopha e a Perdiz-do-mar-de-colar-branco Glareola nuchalis. Várias espécies
típicas de zonas húmidas, nomeadamente de zonas costeiras, que são comuns no resto do país,
revelaram-se surpreendentemente raras ou ausentes (por exemplo, não se registou a presença
de qualquer exemplar de Pigargo-africano Haliaeetus vocifer ou de Guincho/Águia-pesqueira
Osprey Pandion haliaetus).

Palavras-chave: Boé, Dulombi, Guiné-Bissau, Pluvianus, Scotopelia

Introduction
Guinea-Bissau is a small country in West Corubal) mostly within the Boé National
Africa (36,125 km2) but harbours some Park, and also partly within the Dulombi
interesting ornithological values. Its coastal National Park, using three small and light
wetlands provide one of the major wader boats with 8CV engines (Fig. 1). Where
wintering grounds in the East Atlantic the river was broader, we always had at
Flyway, as well as a habitat for many other least one boat sailing close to each of the
waterbirds such as herons, waterfowl two margins, to maximise the probability
and migratory terns (Dodman et al. 2004, of detecting birds. There were always two
Dodman & Sá 2005, Correia et al. 2019). observers fully dedicated to counting birds,
The country is also noted for its important while a third recorded habitat characteristics.
populations of globally endangered vultures These observers were free from tasks
(Henriques et al. 2017, 2018). The avifauna related to manoeuvring and navigation.
of freshwater systems in the interior of Counts were carried out while sailing
Guinea-Bissau has been scarcely surveyed downstream in the Corubal and upstream
(but see Araújo 1994, Dodman et al. 2004), in the Fefine. Sampling outside transects was
which contrasts with numerous studies for opportunistic, mostly around campsites. The
the rich coastal systems (Dodman & Sá rainy season had occurred between mid-
2005). The aim of the present study was to May and mid-November and water levels
bring more information on the river bird were high, with less than 0.1% of the river
fauna of two important rivers of the interior margins presenting sand banks or exposed
of the country. rocks. Marginal vegetation was dense and
tall everywhere, dominated by trees or tall
bushes, with branches generally overhanging
Methods the water. Water flow was generally slow and
in-water visibility between 0.5 and 1.5 m.
From 6 to 12 December 2018, we Bird numbers were low (see Table 1), but
navigated 90 km of the Corubal River in the speed of travel (generally c.10 km.h-
the regions of Cabuca and Tchetche and 32 1
) and the dense vegetation meant that
km of the lower Fefine (a tributary of the species that predominantly hide in the

28
Censo de aves nos rios Corubal e Fefine, Guiné-Bissau

vegetation (most kingfishers Alcedinidae, overlooked. Birds that typically perch in the
some herons Ardeidae, African Finfoot open (including on treetops or side branches)
Podica senegalensis) must have been largely were probably efficiently surveyed.

Figure 1- Eastern Guinea-Bissau, with the surveyed sectors of the Corubal and Fefine rivers indicated in red. The Fefine
runs towards the northwest, meeting the Corubal where the two red lines join.

Figura 1 - O leste da Guiné-Bissau, com os setores dos rios Corubal e Fefine que foram recenseados assinalados
a vermelho. O Fefine corre em direção ao noroeste, desaguando no Corubal onde as duas linhas vermelhas se juntam.

Table 1- Waterbirds recorded along the Corubal and Fefine river transects (Guinea-Bissau), 6-12 December 2018, with total
numbers and, in parentheses, the number per km of surveyed river.

Tabela 1 - Aves aquáticas recenseadas ao longo dos rios Corubal e Fefine (Guiné-Bissau) entre 6 e 12 de Dezembro de 2018,
com números totais e, entre parêntesis, o número por quilómetro de rio percorrido.

CORUBAL FEFINE
SPECIES COMMON NAME TOTAL
(90 Km) (32 Km)

Podica senegalensis African Finfoot 3 (0.03) 3 (0.09) 6 (0.05)

1 seen outside
Ciconia microscelis African Woollyneck - -
transects

Bostrychia hagedash Hadada Ibis 8 (0.09) 17 (0.5) 25 (0.20)

2 seen outside
Calherodius leuconotus White-backed Night Heron - -
transects

29
Bird survey in the rivers Corubal and Fefine, Guinea-Bissau

CORUBAL FEFINE
SPECIES COMMON NAME TOTAL
(90 Km) (32 Km)

3 seen outside
Nycticorax nycticorax Black-crowned Night Heron - -
transects

Ardea cinerea Grey Heron 4 (0.04) 0 (0.00) 4 (0.03)

Ardea melanocephala Black-headed Heron 2 (0.02) 0 (0.00) 2 (0.02)

Ardea purpurea Purple Heron 0 (0.00) 1 (0.03) 1 (0.01)

Bubulcus ibis Cattle Egret 17 (0.19) 4 (0.13) 21 (0.17)

Butorides striata Green-backed Heron 1 (0.01) 0 (0.00) 1 (0.01)

Egretta gularis Western Reef Egret 2 (0.02) 0 (0.00) 2 (0.02)

Scopus umbretta Hamerkop 4 (0.04) 0 (0.00) 4 (0.03)

Microcarbo africanus Long-tailed Cormorant 22 (0.24) 1 (0.03) 23 (0.19)

Anhinga rufa African Darter 6 (0.07) 0 (0.00) 6 (0.05)

Burhinus senegalensis Senegal Thick-knee 9 (0.10) 0 (0.00) 9 (0.07)

Pluvianus aegyptius Egyptian Plover 5 (0.06) 0 (0.00) 5 (0.04)

Vanellus albiceps White-headed Lapwing 7 (0.08) 0 (0.00) 7 (0.06)

1 seen outside
Rostratula bengalensis Greater Painted-snipe - -
transects

Actitis hypoleucos Common Sandpiper 9 (0.1) 3 (0.09) 12 (0.10)

1 seen outside
Tringa ochropus Green Sandpiper - -
transects

Gypohierax angolensis Palm-nut Vulture 16 (0.18) 0 (0.00) 16 (0.13)

Scotopelia peli Pel’s Fishing Owl 1 (0.01) 1 (0.03) 2 (0.02)

Alcedo quadribrachys Shining-blue Kingfisher 2 (0.02) 4 (0.13) 6 (0.05)

Ceryle rudis Pied Kingfisher 1 (0.01) 0 (0.00) 1 (0.01)

Corythornis cristatus Malachite Kingfisher 3 (0.03) 1 (0.03) 4 (0.03)

Halcyon malimbica Blue-breasted Kingfisher 12 (0.13) 4 (0.13) 16 (0.13)

Megaceryle maxima Giant Kingfisher 5 (0.06) 4 (0.13) 9 (0.07)

30
Censo de aves nos rios Corubal e Fefine, Guiné-Bissau

Results crested Tiger Herons Tigriornis leucolopha,


another river specialist, although this incon-
The results of our surveys are presented spicuous species is known to occur near
in Table 1. Tchetche (H. Monteiro pers. comm.).
Palm-nut Vultures Gypohierax ango-
lensis, which are very common elsewhere
Discussion in the country (Carneiro et al. 2017, Hen-
riques et al. 2017) were scarce (but nests
Although apparently not rich in num- and nest building were observed), which
bers of species and individuals, our results might be linked to the very low density of
revealed a bird community with some palms Elaeis guineensis (estimated at <1 per
interesting features. Some specialised river ha). Nevertheless, as transects were often
species were observed, and may be more carried out in the middle of the day, we may
numerous than the few records suggest, as have missed some individuals hidden in the
they often keep well hidden. At least four canopy and actual densities may be slightly
different Pel’s Fishing Owls Scotopelia peli higher. Waders were very scarce, which is
were found along the Fefine (three outside not surprising given the almost complete
transects), and one other individual along absence of exposed rock, sand or mud. Pos-
the Corubal. Only two White-backed Night sibly some increase in number later in the
Herons Calherodius leuconotus were seen season. For example, we have seen Egyptian
(in the evening, outside the transect), but Plovers Pluvianus aegyptius at the Tch-
they must have been largely overlooked etche ferry landing point previously, but
because they are nocturnal birds and may be none were recorded there this time. Herons
relatively common (we have also seen them and egrets were similarly scarce, and may
a few kilometres downstream the study area, increase in numbers before the following
at Saltinho). We did not detect any White- raining season. Of note was the complete

Figure 2- Pel’s Fishing Owl Scotopelia peli, lower Fefine, Guinea-Bissau, 7 December 2018 (credits Paulo Catry).

Figura 2 - Corujão-pesqueiro Scotopelia peli no baixo Fefine, Guiné-Bissau, em 7 de Dezembro de 2018 (crédito Paulo Catry).

31
Bird survey in the rivers Corubal and Fefine, Guinea-Bissau

absence of African Fish Eagles Haliaee- Carneiro, C., Henriques, M., Barbosa,
tus vocifer and Ospreys Pandion haliaetus, C., Tchantchalam, Q., Regalla, A.,
which are common along the coast (Hen- Patrício, A. R. & Catry, P. 2017. Ecology
riques et al. 2017) and also occur at some and behaviour of palm-nut vultures
freshwater lakes. Another river species that Gypohierax angolensis in the Bijagós
was not detected is the Rock Pratincole Archipelago, Guinea-Bissau. Ostrich 88:
Glareola nuchalis, which regularly breeds 113–121.
further down the Corubal, in the Saltinho–
Cusselinta area (pers. obs.). Correia E, Granadeiro JP, Mata VA, Regalla
Despite extensive signs of slash-and-burn A, Catry P 2019. Trophic interactions
agriculture and fishing activities, the sur- between migratory seabirds, predatory
veyed sections of the river are still relatively fishes and small pelagics in Coastal West
wild and well conserved, and seven species Africa. Marine Ecology Progress Series
of primates were detected, including 3-4 622: 177-189.
groups of chimpanzees Pan troglodytes,
numerous baboons Papio papio and colobus Dodman, T., Barlow, C., Sá, J. & Robertson,
Piliocolobus badius and Colobus polyko- P. 2004. Important Bird Areas in Guinea-
mos. Therefore, human presence or habitat Bissau. Dakar: Wetlands International &
degradation are presumably not responsible Bissau: Gabinete de Planificação Costeira.
for the low number of birds recorded. More
studies are needed, with counts along the Dodman, T. & Sá, J. 2005. Monitorização
annual cycle (and perhaps different method- de aves aquáticas no Arquipélago dos
ologies, such as nocturnal listening stations), Bijagós, Guiné-Bissau. Dakar: Wetlands
to further clarify to what extent the scarcity International & Bissau: Gabinete de
of birds reported in our study is typical of Planificação Costeira.
these ecosystems, and the true status of the
most interesting river specialists. Henriques, M., Lecoq, M., Monteiro, H.,
Regalla, A., Granadeiro, J. P. & Catry, P.
2017. Status of birds of prey in Guinea-
Acknowledgements Bissau: first assessment based on road
surveys. Ostrich 88: 101–111.
We thank Instituto da Biodiversidade e das
Áreas Protegidas, namely Justino Biai (Direc- Henriques M, Granadeiro JP, Monteiro H,
tor), Abílio Rachid Said (Coordinator of the Nuno A, Lecoq M, Cardoso P, Regalla A,
Program) and Aissa Regalla (Coordinator of Catry P 2018. Not in wilderness: African
the Department for the Conservation of Bio- vulture strongholds remain in areas with
diversity) for permits and encouragement. high human density. PLoS ONE 13(1):
Laurent Durris and his team are thanked e0190594.
for the logistical support and for sharing his
expertise on the river.

References
Araújo, A. 1994. A importância ornitológica
da Região da Cufada na Guiné-
Bissau. Report. Lisbon: Instituto para a
Conservação da Natureza.

32
VOLUME 26 2019

Diet of the White Stork (Ciconia ciconia) in


a heterogeneous Mediterranean landscape:
the importance of the invasive Red Swamp
Crayfish (Procambarus clarkii)
Dieta da Cegonha-branca (Ciconia ciconia) numa paisagem
Mediterrânica heterogénea: a importância de uma espécie invasora,
o Lagostim-vermelho-do-Louisiana (Procambarus clarkii)

Eduardo M. Ferreira1*, Filipa Grilo2,


Raquel C. Mendes2, Rui Lourenço3, Sara
M. Santos1, Francisco Petrucci-Fonseca2

1 UBC – Conservation Biology Lab, Department of Biol-


ogy, University of Évora, Núcleo da Mitra, Apartado 94,
7002-554, Évora, Portugal

2 Centre for Ecology, Evolution and Environmental


Changes (cE3c), Faculdade de Ciências, Universidade
de Lisboa, 1749-016 Lisboa, Portugal

3 Instituto de Ciências Agrárias e Ambientais Mediter-


rânicas, Laboratório de Ornitologia, Universidade de
Évora, Núcleo da Mitra, Apartado 94, 7002-554, Évora,
Portugal

* Corresponding author:
[email protected]

ABSTRACT
Limited quantitative data are available on food habits of the White Stork (Ciconia ciconia)
in Mediterranean environments, particularly in ricefields where a relatively new food resource,
the invasive Red Swamp Crayfish (Procambarus clarkii), is abundant. We studied the diet of the
White Stork in a heterogeneous landscape (Central Portugal) in order to compare the importance
of the Red Swamp Crayfish as a food resource in a dominant agricultural/ricefield area in rela-
tion to a predominant woodland/agricultural area. White Storks´ diet was analysed spatially (two
sites) and seasonally (winter, spring, summer) using pellets (n = 122) collected between December
2012 and July 2013. Overall, from 1570 prey items identified, crayfish was the second most
frequent and abundant prey in the diet (frequency of occurrence, FO = 79.5%; numerical fre-
quency, NF = 22.9%, respectively), only surpassed by coleopterans (FO = 94.3%; NF = 57.7%).
However, in terms of consumed biomass (global PB) crayfish dominated the diet (PB = 44.0%),

33
Contribution of the Red Swamp Crayfish to the diet of the White Stork

representing 1.8 times the consumed biomass of coleopterans (PB = 24.2%). Consumption of
crayfish was higher in the site with highest abundance of ricefields (NF: 32.0% vs. 17.7%; PB:
51.3% vs. 38.4%). Although no significant seasonal variations were detected in terms of the
number of crayfish consumed by storks, consumed crayfish biomass was significantly higher in
summer in relation to other seasons. Our findings suggest that in Mediterranean heterogeneous
areas the White Stork feeds upon a wide range of prey taxa though, when available, coleopterans
along with Red Swamp Crayfish dominate the diet.

Keywords: Feeding ecology, Mediterranean, pellet analysis, Red Swamp Crayfish, White Stork

RESUMO
O estudo dos hábitos alimentares da Cegonha-branca (Ciconia ciconia) em ambientes medi-
terrânicos carece de informação quantitativa, particularmente em áreas de arrozais onde um
recurso alimentar relativamente novo, o Lagostim-vermelho-do-Louisiana (Procambarus clar-
kii), é abundante. Analisámos a dieta da Cegonha-branca numa paisagem heterogénea no centro
de Portugal com o intuito de comparar a importância desta espécie de lagostim invasor como
recurso alimentar numa área dominada por culturas agrícolas e arrozais em relação a uma área
predominantemente florestal/agrícola. A dieta da Cegonha-branca foi analisada espacialmente
(dois locais) e sazonalmente (inverno, primavera e verão) a partir da análise de regurgitações (n
= 122) recolhidas entre Dezembro de 2012 e Julho de 2013. De um total de 1570 presas iden-
tificadas, o Lagostim-vermelho-do-Louisiana foi o segundo recurso alimentar mais frequente e
abundante na dieta (frequência de ocorrência, FO = 79.5%; frequência numérica, NF = 22.9%,
respectivamente), unicamente excedido pelos coleópteros (FO = 94.3%; NF = 57.7%). Con-
tudo, em termos de biomassa o lagostim dominou a dieta (PB = 44.0%) representando 1.8
vezes a biomassa consumida dos coleópteros (PB = 24.2%). O consumo de Lagostim-verme-
lho-do-Louisiana foi significativamente maior no local com maior percentagem de cobertura de
arrozais (NF: 32.0% vs. 17.7%; PB: 51.3% vs. 38.4%). Embora não tenham sido detectadas
variações sazonais significativas no consumo do lagostim em termos numéricos, o lagostim teve
uma contribuição para a biomassa consumida significativamente maior no verão face às outras
estações. Os resultados deste trabalho sugerem que nesta área mediterrânica heterógena, a Cego-
nha-branca alimenta-se de um vasto leque de presas, porém, quando disponíveis, os coleópteros
e o Lagostim-vermelho-do-Louisiana dominam a dieta.

Palavras-chave: regurgitações, Cegonha-branca, ecologia alimentar, Lagostim-vermelho-do-Louisiana, Mediterrâneo

Introduction
The White Stork (Ciconia ciconia) is 1991, Hancock et al. 1992). This species is
a large migratory species, being widely considered a generalist and opportunistic
distributed and inhabiting a variety of open predator and its diet has been well
and agricultural habitats (Alonso et al. documented throughout its distributional

34
Contribuição do Lagostim-vermelho-da-Lousiana para a dieta da Cegonha-branca

range in Europe (Mužinić & Rašajski 1992, Portugal, in a freshwater marsh located in
Antczak et al. 2002, Tsachalidis & Goutner the Tagus river basin, White Storks show
2002). Several studies revealed that the a high consumption of crayfish, which is
White Stork feeds upon a wide range of prey available all over the year (Correia 2001).
including invertebrate and vertebrate species In Spain, the crayfish is also an important
(Melendro et al. 1978, Antczak et al. 2002, prey item in White Storks’ diet in ricefield
Kosicki et al. 2006, Cheriak et al. 2014). areas (Negro et al. 2000, Tablado et al.
Earthworms, orthopterans, coleopterans, 2010, Sanz-Aguilar et al. 2015), a typical
and small mammals (predominantly voles habitat where this invasive species is often
in Eastern Europe) seem to be primary food abundant (Anastácio et al. 2009). However,
resources throughout the breeding range available information is still insufficient
of the White Stork. On the other hand, to fully understand the relationship
small fish, birds, reptiles, amphibians, and between White Storks and crayfish, namely
molluscs are sporadically consumed, being concerning a quantitative assessment of
referred as complementary food resources crayfish contribution to White Stork’s diet
(Antczak et al. 2002, Tsachalidis & Goutner considering simultaneously the contribution
2002, Vrezec 2009, Catry et al. 2010). The of other food resources.
diet of White Storks seems to be shaped by Here, we aimed to describe and compare
landscape use, prey availability and climatic the diet of the White Stork at two sites
conditions of each geographical region within a Mediterranean area characterized
(Johst et al. 2001, Tsachalidis & Goutner by a heterogeneous landscape: one site
2002, Ciach & Kruszyk 2010, Chenchouni dominated by woodland with agricultural
et al. 2015, Chenchouni 2017). patches, and the other dominated by
Recently, the appearance of new food mixed agricultural habitats, with a high
resources, such as rubbish dumps, has percentage occupied by ricefields (another
produced considerable shifts in the feeding site). Specifically, we aimed to (1) quantify
habits (e.g. foraging behaviour; Tortosa et the proportion and biomass contribution
al. 2002, Ciach & Kruszyk 2010, Gilbert of crayfish in the diet of White Storks in
et al. 2016) and diet composition of White relation to other food resources and (2)
Storks (Peris 2003). Likewise, the spread evaluate possible spatial-seasonal variations
of the invasive Red Swamp Crayfish of crayfish consumption by White Storks.
(Procambarus clarkii; hereafter referred
as “crayfish”) has been suggested to be
an important driver of observed dietary Methods
changes of the White Stork (Correia 2001, Study area
Tablado et al. 2010), as well as a major
cause for the establishment and increase The study was carried out in Charneca do
of White Stork wintering populations Infantado (Figure 1), within the estate “Com-
in the Iberian Peninsula (Tablado et al. panhia das Lezírias S.A”, which is the largest
2010, Catry et al. 2017). This invasive Portuguese agroforestry farmstead (38° 52’
crayfish was introduced in southwestern N, 08° 51’ W; Central Portugal), located on
Europe from North America in the 1970s, the left margin of the Tagus River. The area
and is now widespread in wetlands (e.g. is characterized by a landscape mosaic with
ricefields) across Portugal and Spain, where high abundance of cork oak woodlands,
it became an abundant new food resource pine forests and agricultural lands, such as
exploited by White Storks. For example, in ricefields and pastures.

35
Contribution of the Red Swamp Crayfish to the diet of the White Stork

The diet of the White Stork was assessed by dominant land use comprises broad-leaved
analysing pellets collected underneath nests in forest (25.9%) – mainly cork oak woodland –
two sites, Catapereiro and Roubão, separated mixed agricultural areas (21.9%), forest and
by 8.4 km (Figure 1). The nests were located semi natural areas (18.2%) and arable land
on the top of transmission electricity pylons: (18.1%). Here, the percentage of ricefields is
18 nests in seven pylons at Catapereiro and low (3.6%). The Roubão nest site is mainly
12 nests in six pylons at Roubão. Land use characterized by arable land (30.9%), mixed
around nest sites was assessed and character- agricultural areas (29.0%) and ricefields
ized in a buffer of 6.5 km (maximum distance (20.3%). Here, the percentages of broad-
of a foraging flight recorded in the area by leaved forest (2.3%) and forest and semi nat-
visual estimation; E. Ferreira unpubl. data) ural areas (10.4%) are low. The remaining
around each nest site centroid by using the land use types (artificial surfaces, wetlands
Corine land cover 2006 information (Cae- and water bodies) accounted individually for
tano et al. 2009). In Catapereiro, the pre- less than 10% of the land use at each nest site.

Figure 1 - Study area (“Charneca do Infantado”) in Central Portugal showing details on the location of the sampled nest sites,
feeding areas and main land use types.

Figura 1 - Localização da área de estudo (“Charneca do Infantado”) em Portugal com destaque para a localização dos locais
de ninhos amostrados, áreas de alimentação e principais classes de uso do solo.

36
Contribuição do Lagostim-vermelho-da-Lousiana para a dieta da Cegonha-branca

Pellet Collection orthopterans, coleopterans, other insects,


reptiles, birds, small mammals, and lago-
and Prey Identification
morphs. Diet composition was expressed as
During the first visit to the study area the frequency of occurrence (FO), numerical
we surveyed both nest sites and removed frequency (NF) and the percentage of con-
old pellets, which were not included in diet sumed biomass (PB). FO was calculated for
analyses. Afterwards, pellet collection took each main prey category as the number of
place once a month, from December 2012 pellets containing a prey item i / total num-
to July 2013 (except March 2013), cover- ber of pellets × 100 – being only determined
ing the presence of the White Stork in nest- for the global data set (data from the two
ing areas during the whole breeding period. sites across the three seasons combined).
Only intact and fresh pellets found under NF was calculated for each prey item iden-
the pylons with nests were collected. In the tified as the minimum number of individuals
laboratory, pellets were soaked in water and (MNI) of a given prey item i / total number
washed through a 2 mm mesh sieve to dis- of prey items N × 100 (Chenchouni et al.
aggregate their content. Afterwards, food 2015). PB was calculated for each prey item
remains were identified using a binocular identified as the mean biomass of a given
stereomicroscope with the help of identifica- prey item i / total consumed biomass of all
tion keys, reference collections, and special- prey items × 100 – using mean individual
ist consultation. Mammals were identified live weights of the consumed prey as a proxy
through microscopic hair analysis (Pinto for ingested biomass (Supporting informa-
1978, Teerink 1991) and reptiles by the pres- tion, Table S1). NF and PB were determined
ence of scales and bone remains. Bird iden- for the global data set and then by site (Cat-
tification was based on microscopic analysis apereiro and Roubão) and season (winter:
of feathers (Brom 1986) and insects from the from December to February; spring: from
presence of different body parts (e.g. heads, April to May; summer: from late June to
mandibles, legs, elytra and thorax) accord- July), wherein seasons represent different
ing to Chinery (1997). The crayfish – the phases of a single breeding season. Consid-
only malacostraca species detected – was ering the relatively low number of pellets
identified through fragments of body parts, per site (Table 1), we carried out seasonal
namely grastroliths, uropods, rostrum and analyses combining data from both sites.
propodites of the chelae (Beja 1996, Correia Chi-square tests for independence (x2) with
2001). Prey item remains were identified to Bonferroni correction for multiple compari-
the lowest possible taxonomic level and then sons were used to test the significance of NF
the minimum number of individuals (MNI) and PB differences in each consumed prey
was quantified for each prey taxa. We esti- category between sites and seasons. Diet
mated MNI by counting the number of frag- diversity was determined using the Shannon
ments/items recovered in each pellet corre- index (H’ = − Σpixlog pi where pi represents
sponding to different individuals of a same the proportion of each prey taxa in the diet;
given prey taxa (Chenchouni et al. 2015). Shannon & Weaver 1949) at the family
level, i.e. the most precise taxonomic level,
Data Analysis since not all prey items could be identified
to species level. All statistical analyses were
Prey items were grouped into the follow- performed in the software R 3.4.3 (R Core
ing eight main prey categories: crayfish, Development Team 2017).

37
Contribution of the Red Swamp Crayfish to the diet of the White Stork

Table 1- Diet composition of the White Stork (Ciconia ciconia) in the two study sites (Catapereiro and Roubão) throughout
the study period (winter, spring and summer). N: number of individuals; NF (%): numerical frequency of prey in diet; PB (%):
percentage of consumed biomass; N total: total number of individuals; N pellets: number of pellets collected from each site
and per season; H’: diet diversity according to Shannon index.

Tabela 1 - Composição da dieta da Cegonha-branca (Ciconia ciconia) descrita por local de estudo (Catapereiro e Roubão) e
por estação do ano (inverno, primavera, verão). N: número de indivíduos; NF (%): frequência numérica de presas na dieta; PB
(%): percentagem de biomassa consumida; N total: somatório do número de indivíduos; N pellets: número de regurgitações
recolhidas por local de amostragem e estação do ano; H’: valor do nicho trófico (índice de Shannon).

CATAPEREIRO ROUBÃO

winter spring summer winter spring summer


PREY TAXA

NF PB NF PB NF PB NF PB NF PB NF PB
N Nv N N N N
(%) (%) (%) (%) (%) (%) (%) (%) (%) (%) (%) (%)

Class Malacostraca 21.8 28.9 13.6 34.9 20.9 45.3 32.6 68.9 37.3 46.5 28.5 53.7

Order Decapoda

Procambarus clarkii 24 21.8 28.9 62 13.6 34.9 91 20.9 45.3 15 32.6 68.9 76 37.3 46.5 91 28.5 53.7

Class Insecta 71.8 23.2 84.4 48.0 78.2 47.8 67.4 31.1 59.3 17.7 69.9 38.4

Order Odonata 0.2 0.2

Odonatata NI 1 0.2 0.2

Order Orthoptera 10.9 5.5 0.4 0.4 28.7 23.8 7.4 3.5 31.4 22.5

Gryllotalpa gryllotalpa 12 10.9 5.5 1 0.2 0.2 1 0.3 0.2

Orthoptera NI 2 0.4 0.4 124 28.4 23.6 15 7.4 3.5 99 31.0 22.3

Order Hemiptera 0.4 0.4 0.5 0.2

Hemniptera NI 2 0.4 0.4 1 0.5 0.2

Order Coleoptera 60.9 17.6 82.0 45.9 47.5 22.5 67.4 31.1 51.5 14.0 38.6 15.8

Carabidae

Calosoma maderae 6 5.5 1.6

Carabus lusitanicus 1 0.2 0.1

Carabus melancholicus 8 1.8 1.0 4 0.9 0.4 2 0.6 0.3

Carabus sp. 5 1.1 0.6 1 0.2 0.1 1 0.5 0.1

Chlaenius olivieri 1 0.2 0.1 1 0.2 0.1 1 0.5 0.1 1 0.3 0.1

Cicindela campestris 3 0.7 0.4 1 0.5 0.1

Poecilus kugelanni 1 0.2 0.1

Scarites cyclops 5 1.1 0.6 2 0.5 0.2 2 1.0 0.3 1 0.3 0.1

Carabidae NI 3 2.7 0.8 64 14.1 7.9 1 2.2 1.0 13 6.4 1.7 17 5.3 2.2

Dytiscidae 31 7.1 3.4

Dytiscidae NI 1 0.9 0.3 46 10.1 5.7 24 5.5 2.6 1 2.2 1.0 25 12.3 3.3 17 5.3 2.2

Histeridae

Histeridae NI 1 0.9 0.3 4 0.9 0.5 2 0.5 0.2 2 1.0 0.3 1 0.3 0.1

38
Contribuição do Lagostim-vermelho-da-Lousiana para a dieta da Cegonha-branca

CATAPEREIRO ROUBÃO

winter spring summer winter spring summer


PREY TAXA

NF PB NF PB NF PB NF PB NF PB NF PB
N Nv N N N N
(%) (%) (%) (%) (%) (%) (%) (%) (%) (%) (%) (%)

Silphidae

Silpha puncticollis 3 0.7 0.4 1 0.3 0.1

Silphidae NI 30 27.3 7.9 30 6.6 3.7 4 0.9 0.4 7 3.4 0.9 7 2.1 0.9

Dynastidae

Oryctes nasicornis 3 2.7 0.8

Scarabaeidae

Bubas bison 2 1.8 0.5 4 8.7 4.0

Bubas sp. 3 0.7 0.4

Copris hispanus 1 2.2 1.0

Onthophagus sp. 1 2.2 1.0

Scarabaeidae NI 9 19.6 9.0

Melolonthidae

Melolontha papposa 1 0.2 0.1 9 19.6 9.0 12 5.9 1.6

Tenebrionidae

Akis sp. 1 0.2 0.1 13 4.1 1.7

Blaps sp. 1 0.2 0.1 1 0.3 0.1

Erodius sp. 2 0.5 0.2

Pimelia sp. 3 0.7 0.3

Sepidium sp. 6 1.3 0.7 7 1.6 0.8 4 1.3 0.5

Tenebrionidae NI 43 9.5 5.3 73 16.7 7.9 4 2.0 0.5 47 14.7 6.1

Chrysomelidae

Chrysomela sp. 3 0.7 0.4 2 0.5 0.2 2 1.0 0.3 1 0.3 0.1

Chrysomelidae NI 1 0.2 0.1 2 0.5 0.2

Curculionidae

Curculionidae NI 2 0.4 0.2 3 0.9 0.4

Coleoptera NI 21 19.1 5.5 143 31.4 17.6 47 10.8 5.1 5 10.9 5.0 35 17.2 4.7 7 2.2 0.9

Insect larvae NI 6 1.3 1.1 9 2.1 1.5

Class Reptilia 0.9 0.7 1.8 15.5 0.5 2.5 1.3

Order Squamata 0.9 0.7 1.8 15.5 0.5 1.2 1.3

Chalcides striatus 4 0.9 5.6 1 0.2 1.2 2 0.6 2.9

Psammodromus sp. 1 0.9 0.7

Colubridae NI 4 0.9 9.8

Reptilia NI 1 0.2 1.2 2 0.6 2.9

39
Contribution of the Red Swamp Crayfish to the diet of the White Stork

CATAPEREIRO ROUBÃO

winter spring summer winter spring summer


PREY TAXA

NF PB NF PB NF PB NF PB NF PB NF PB
N Nv N N N N
(%) (%) (%) (%) (%) (%) (%) (%) (%) (%) (%) (%)

Class Aves 1.0 20.0

Order Anseriformes 1.0

Anatidae NI 2 1.0 20.0

Class Mammalia 5.5 47.1 0.2 1.6 0.5 4.4 2.5 15.7 0.3 2.1

Order Insectivora 0.9 1.4 0.5 4.4 1.0 2.8

Crocidura russula 1 0.9 1.4 1 0.5 0.7

Talpa occidentalis 1 0.2 2.7

Insectivora NI 1 0.2 1.7 1 0.5 2.1

Order Rodentia 3.6 12.8 0.2 1.6 1.5 12.9 0.3 2.1

Microtus sp. 1 0.5 2.1 1 0.3 2.1

Mus sp. 1 0.9 2.5

Rattus sp. 1 0.5 9.1

Rodentia NI 3 2.7 10.3 1 0.2 1.6 1 0.5 1.7

Order Lagomorpha 0.9 32.9

Lagomorpha NI 1 0.9 32.9

N total 110 455 436 46 204 319

N pellets 10 33 33 5 18 23

Shannon index (H’) 1.97 1.97 1.9 1.46 1.99 1.74

Results
From a total of 122 White Stork pellets (NF = 22.9%), only surpassed by coleopter-
analysed, we identified and quantified 1570 ans (NF = 57.7%). Indeed, the crayfish rep-
prey items comprising 46 taxa belonging to resented 1.4 times the consumption of ortho-
5 classes, 10 orders and 21 families (Table pterans (NF = 16.2%) and 6.9 times the sum
1). Coleopterans (FO = 94.3%), crayfish (FO of other insects (NF = 1.2%), reptiles (NF =
= 79.5%) and orthopterans (FO = 27.9%) 1.0%), small mammals (NF = 0.9%), birds
were the prey categories more frequently (NF = 0.1%) and lagomorphs (NF = 0.1%)
found in pellets. Other prey categories, together. In terms of biomass (global PB),
namely reptiles (FO = 11.5%), small mam- crayfish (PB = 44.0%) dominated the diet of
mals (FO = 8.2%), and other insects (FO = White Storks representing 1.8 times the PB
4.9%) had a moderate frequency in pellets. of coleopterans (PB = 24.2%), 3.7 times the
Birds (FO = 1.6%) and lagomorphs (FO = PB of orthopterans (PB = 11.9%) and 2.2
0.8%) were the least represented prey in pel- times the sum of PB of small mammals (PB
lets. Regarding the numerical frequency of = 6.5%), reptiles (PB = 5.3 %), birds (PB =
prey in diet (global NF %), the crayfish was 4.0 %), lagomorphs (PB = 3.3%), and other
the second most consumed prey category insects (PB = 0.8%) together.

40
Contribuição do Lagostim-vermelho-da-Lousiana para a dieta da Cegonha-branca

Spatial Analysis
The crayfish was the second most consumed PB at each site. We found significant between-
prey taxa (NF) at both sites, accounting for site differences both on NF and PB mainly for
32.0% of all prey consumed at Roubão and the most consumed prey categories, with cray-
17.7% at Catapereiro (Figure 2). The cole- fish being significantly more consumed and
opterans dominated the diet at both sites, rang- represented in terms of biomass at Roubão,
ing from 45.5% at Roubão to 64.6% at Cat- while coleopterans and other insects were more
apereiro, whereas the orthopterans, the third consumed and had a larger contribution to the
most important prey category, represented consumed biomass at Catapereiro (Chi-square
20.2% of the diet at Roubão and 13.9% at Cat- pairwise tests with Bonferroni correction sig-
apereiro. However, in terms of biomass (PB), nificance at P < 0.006; Table 2). For the ortho-
crayfish represented the most important prey pterans, only significant spatial differences in
category at both sites (PB = 51.3% at Roubão; terms of NF were detected, wherein this prey
PB = 38.4% at Catapereiro), while coleopter- was more common in the diet at Roubão. No
ans were ranked second (PB = 30.6% at Cata- significant between-site differences on NF were
pereiro; PB = 15.9% at Roubão), followed by found for reptiles, birds, small mammals, and
orthopterans (PB = 12.4% at Roubão; PB = lagomorphs. Nevertheless, the contribution of
11.5% at Catapereiro; Figure 2). The propor- these prey (evidenced as secondary and occa-
tion of the other prey categories (other insects, sional food items by NF) to the consumed bio-
reptiles, birds, small mammals and lago- mass varied significantly between sites (Table
morphs) varied among sites, however, together 2). Diet diversity was higher at Catapereiro
represented a low fraction of the diet: less than (H’ = 2.20) than at Roubão (H’ = 2.07), with
5% of NF at each site; and, individually, each species richness values of 43 and 34 prey taxa,
prey category accounted for less than 10% of respectively (Table 1).

Table 2- Comparison of the main prey consumed by White Storks (Ciconia ciconia) between study sites and seasons. Results refer
to the chi-square tests (X²) with Bonferroni correction for multiple comparisons testing the differences in numerical frequency
and percentage of consumed biomass of each consumed prey category (*: significant results (p < 0.006); NA: Not applicable.

Tabela 2 - Comparação do consumo das principais categorias de presas encontradas em regurgitações de Cegonha-branca
(Ciconia ciconia) entre locais de estudo e estações do ano. São apresentados os resultados dos testes de qui-quadrado (X²) com
correcção de Bonferroni para comparações múltiplas para a frequência numérica e percentagem de biomassa consumida. *:
diferenças significativas (p < 0.006); NA: Não aplicável.

Catapereiro vs. Roubão winter vs. spring winter vs.summer spring vs. summer
PREY
NF PB NF PB NF PB NF PB
CATEGORY
X² p X² p X² p X² p X² p X² p X² p X² p

Crayfish 42.1 <0.001* 124.5 <0.001* 1.2 0.269 3.3 0.071 0.1 0.813 42.8 <0.001* 2.0 0.156 49.4 <0.001*

Orthopterans 10.7 0.001* 1.3 0.249 9.6 0.002* 18.2 <0.001* 32.8 <0.001* 172.1 <0.001* 183.8 <0.001* 652.2 <0.001*

Coleopterans 54.3 <0.001* 216.0 <0.001* 5.7 0.017 37.6 <0.001* 19.0 <0.001* 0.5 0.503 119.4 <0.001* 108.5 <0.001*

Other insects 8.0 0.005* 34.0 <0.001* 2.4 0.122 9.3 0.002* 1.9 0.171 7.7 0.006 0.3 0.596 0.5 0.476

Reptiles 0.6 0.438 69.8 <0.001* 0.4 0.538 68.3 <0.001* 0.04 0.841 27.4 <0.001* 0.6 0.427 46.5 <0.001*

Birds 3.5 0.061 406.3 <0.001* 0.5 0.491 94.5 <0.001* NA NA NA NA 2.3 0.130 341.6 <0.001*

Small mammals 0.3 0.605 30.2 <0.001* 5.0 0.026 7.3 0.007 11.7 <0.001* 97.5 <0.001* 1.5 0.226 76.6 <0.001*

Lagomorphs 0.6 0.451 199.0 <0.001* 4.2 0.040 867.0 <0.001* 4.9 0.028 938.0 <0.001* NA NA NA NA

41
Contribution of the Red Swamp Crayfish to the diet of the White Stork

Figure 2 - Proportion of the main prey categories in the diet of the White Stork (Ciconia ciconia) by site, expressed as the
numerical frequency of prey in diet (NF) and percentage of consumed biomass (PB). Dark grey: Catapereiro; light grey:
Roubão.

Figura 2 - Contribuição dos principais grupos de presas para a dieta da Cegonha-branca (Ciconia ciconia) nos dois locais de
estudo, em termos da frequência numérica de presas na dieta (NF) e percentagem de biomassa consumida (PB). Cinzento-
escuro: Catapereiro; cinzento-claro: Roubão.

Figure 3 - Proportion of the main prey categories in the diet of the White Stork (Ciconia ciconia) by season, expressed as the
numerical frequency of prey in diet (NF) and percentage of consumed biomass (PB). The three levels of grey (from light to
dark) represent winter, spring and summer, respectively.

Figura 3 - Contribuição dos principais grupos de presas para a dieta da Cegonha-branca (Ciconia ciconia) por estação do
ano, em termos da frequência numérica de presas na dieta (NF) e percentagem de biomassa consumida (PB). Os três níveis de
cinzento (do mais claro para o mais escuro) representam o inverno, a primavera e o verão, respectivamente.

42
Contribuição do Lagostim-vermelho-da-Lousiana para a dieta da Cegonha-branca

Seasonal analysis

Crayfish was regularly consumed by the and, additionally, a higher contribution in


White Stork throughout the study period terms of PB was detected in spring than in
(Figure 3), being the second most important summer. No significant seasonal variations
prey taxa in winter (NF = 25.0%) and spring regarding NF were found for other insects,
(NF = 20.9%), and the third in summer reptiles, birds and lagomorphs. However, the
(NF = 24.1%). Coleopterans were the most contribution of these prey (secondary and
consumed prey across the three periods (NF occasional prey in terms of NF) to the bulk
ranging between 43.7% in summer to 72.5% of consumed biomass varied significantly
in spring), while orthopterans were the second among seasons (Table 2). The diversity of diet
most important prey in summer (NF = 29.8%) seasonally decreased (H’ = 2.11, H’ = 2.10
and the third in winter and spring (NF = and H’ = 1.86 for winter, spring and summer,
7.7% and 2.6% respectively). Regarding the respectively), while species richness showed
consumed biomass, crayfish was the most no seasonal trend (19, 34 and 29 prey taxa,
representative prey category across all studied respectively for winter, spring and summer;
seasons (PB ranging from 37.3% in winter to Table 1).
49.2% in summer; Figure 3). Coleopterans
and orthopterans were the second most Discussion
important prey categories in spring (PB
= 30.6%) and summer (PB = 23.2%), White Storks in our study area feed upon
respectively. Lagomorphs and small mammals a relatively wide range of prey, though a few
recorded noteworthy PB values during specific food resources constitute the bulk of
the winter (PB = 26.1% and PB = 11.3%, the diet. Regardless of the study site and sea-
respectively). The remaining prey categories son, coleopterans, crayfish, and orthopterans
(other insects, reptiles, and birds) were not were the most consumed prey categories. Our
consumed across all seasons and represented results are similar to those from other dietary
a low fraction of the diet: together, accounted studies (based on pellet analysis) conducted
for less than 5% of NF in each season; and in Europe, where insects (primarily cole-
individually, each prey category accounted opterans and orthopterans) were found to be
for less than 10% of PB in each season. the most frequent consumed prey (>80%),
No significant differences were detected on whereas vertebrates constituted only a small
crayfish consumption (NF) among seasons fraction (<10%) of the diet (Antczak et al.
(Chi-square pairwise tests with Bonferroni 2002, Tsachalidis & Goutner 2002, Miraglia
correction significance at P < 0.006; Table et al. 2008, Vrezec 2009). On the other hand,
2). There were, however, significant seasonal in terms of consumed biomass, crayfish turn
differences in terms of PB, with crayfish out to be the most representative prey among
having a larger contribution to the consumed sites and across the studied seasons, whereas
biomass in summer in relation to spring and insects became less prominent on diet.
winter. The proportion of orthopterans in diet Following the introduction in Spain in
and its contribution to the bulk of biomass the 1970s, craysfishes quickly spread across
was significantly different among all seasons, wetlands in the Iberian Peninsula, including
peaking in summer. For coleopterans, a ricefields (Geiger et al. 2005), becoming an
significantly higher consumption occurred in abundant new food resource exploited by
winter and spring in relation to summer, while White Storks (Negro et al. 2000, Correia
in terms of PB a significant higher contribution 2001). The consumption of this new prey
to the diet was detected in spring in relation promoted not only dietary changes but it also
to winter and summer. The proportion on shaped the foraging behaviour of the White
diet of small mammals (both NF and PB) was Stork in southwestern Europe (Correia 2001,
significantly higher in winter than in summer, Barbraud et al. 2002, Tablado et al. 2010,

43
Contribution of the Red Swamp Crayfish to the diet of the White Stork

Sanz-Aguilar et al. 2015). In our study area, areas (Sanz-Aguilar et al. 2015). The spatial
the crayfish was the second most important exploitation of the crayfish may also be influ-
prey category for the White Stork in terms of enced by the availability of other important
number of individuals consumed and the most prey in accordance to land use types. Spe-
predominant in terms of biomass, being reg- cifically, coleopterans and orthopterans are
ularly consumed throughout the year. This is abundant in arable land, mixed agricultural
consistent with previously studies, suggesting areas and broad-leaved forests, mainly cork
that crayfish, where available, is an important oak woodland (Alonso et al. 1991, Galante et
dietary prey for White Storks. al. 1995, Tsachalidis & Goutner 2002, Silva
Linking prey consumption with abundance et al. 2008). In fact, these habitats, which are
and availability of prey is key to deepen on also used by storks (Alonso et al. 1991, Johst
spatial-temporal diet variations and how et al. 2001, Catry et al. 2010), presented
predators exploit the available prey (e.g. Beja the highest difference in terms of land cover
1996, Correia 2001). Regrettably, in this abundance between the two sites.
study, diet analysis was not complemented Regarding the seasonal consumption of
with the assessment of ecological factors crayfish by the White Stork, the continuous
most likely to influence the diet of the White exploitation of this prey throughout all stud-
Stork, particularly the abundance and avail- ied seasons is consistent with the few studies
ability of prey (e.g. Correia 2001), which hin- conducted in the Iberian Peninsula (Correia
der and limit the extension of interpretations 2001, Tablado et al. 2010). Results of prey bio-
of the results. Nevertheless, the differences mass consumption suggest that crayfish had a
detected on crayfish consumption between more important role in summer in relation to
sites, as well as its regular seasonal use by other seasons. However, in terms of numerical
White Storks may be related to landscape frequency our results indicate a regular sea-
structure and composition at each sampled sonal pattern of consumption of crayfish, con-
site, though further investigation is required trasting with the results from Correia (2001),
to test the potential effects of abundance which found seasonal differences on crayfish
and availability of prey on spatial-temporal consumption by storks, with a lower preda-
diet variations. For instance, spatially, cray- tion intensity in winter and higher in summer.
fish consumption is likely to be linked with These patterns probably depend on crayfish
the presence of ricefields, a major habitat abundance and availability to predators in
for crayfish (Anastácio et al. 2009, Ramalho accordance to hydrological cycle and water
& Anastácio 2015). Specifically, the highest temperature of habitat types, which may be
consumption of crayfish was recorded at different between natural marshlands (found
Roubão, which is the site with higher abun- in Correia 2001) and ricefields – such as the
dance of ricefields nearby (20.3%), against case of this study – (Correia 1998, Anastácio
3.6% of ricefields at Catapereiro. Similar et al. 2009, Ramalho & Anastácio 2015).
results were found by Tablado et al. (2010) Additionally, crayfish consumption may also
in Guadalquivir marshes, in southwestern be driven by the cost-benefit relation of for-
Spain. Accordingly, a greater presence of aging on other highly available food, partic-
crayfish in the White Stork´s diet (expressed ularly insects (as evidenced by the seasonal
as percentage of crayfish in dietary samples) consumption of this prey). Notice, for exam-
was recorded in areas mainly occupied by ple, that the White Stork apparently shifted
ricefields, rather than in natural marshland from a diet mostly comprised by coleopterans
areas (Tablado et al. 2010). Although the in spring to a combined consumption of cole-
White Stork is a generalist predator that can opterans and orthopterans in summer, which
explore a variety of freshwater habitats, it may be associated with peak density of these
tends to forage crayfish mainly in ricefields two prey taxa (Loureiro et al. 2009).

44
Contribuição do Lagostim-vermelho-da-Lousiana para a dieta da Cegonha-branca

The establishment of crayfish populations Anastácio, P.M., Leitão, S.A., Boavida M.J. &
has influenced the diet of several species of Correia, A.M. 2009. Population dynam-
predators (e.g. Lutra lutra; Beja 1996, Bar- ics of the invasive crayfish (Procambarus
rientos et al. 2014), including the White clarkii Girard, 1852) at two marshes with
Stork, resulting in dietary changes (Correia differing hydroperiods. Annales de Lim-
2001, Tablado 2010), behavioural changes nologie - International Journal of Limnol-
(e.g. increase of wintering population of ogy 45: 247-256.
storks; Catry et al. 2017) and demographic
shifts (e.g. increase of local abundance of Antczak, M., Konwerski, S., Grobelny, S. &
storks; Tablado et al. 2010). Moreover, the Tryjanowski, P. 2002. The food composi-
response of crayfish predators in relation tion of immature and non-breeding White
to crayfish availability will likely continue Storks in Poland. Waterbirds 25: 424-428.
to be strong in the absence of restrictive
factors (e.g. nesting-site areas; Tablado et Barbraud, C., National, F. & Karine, D.
al. 2010). Thus, it is of great relevance to 2002. Recent changes in the feeding diet
increase our knowledge on the potentially of White Stork (Ciconia ciconia) chicks in
key role of the crayfish, considering the par- Charente Maritime (West France). Alauda
adox trade-off of its positive effects vs. neg- 70: 437-444.
ative impacts on ecosystems (e.g. as a pred-
ator of amphibians and vector of diseases), Barrientos, R., Merino-Aguirre, R., Fletcher,
as well as the driver of complex cascading D.H. & Almeida, D. 2014. Eurasian otters
effects on foods webs (Geiger et al. 2005). modify their trophic niche after the intro-
Specifically, broad-scale studies on this duction of non-native prey in Mediterra-
interaction, which assess the availability of nean fresh waters. Biological Invasions 16:
prey species, may help to evaluate to which 1573-1579.
degree crayfish availability can lead to sig-
nificant changes on populations of White Beja, P.R. 1996. An analysis of otter Lutra
Stork and other predators. lutra predation on introduced American
crayfish Procambarus clarkii in Iberian
streams. Journal of Applied Ecology 33:
Acknowledgements 1156-1170.

We would like to thank administration Brom, T.G. 1986. Microscopic identification


of Companhia das Lezírias for providing us of feathers and feather fragments of pale-
facilities and for allowing us to work in the artic birds. Bijdragen Tot de Dierkunde
study area. We also would like to thank San- 56: 181-204.
dra Alcobia, André Silva and Bruno Silva for
their technical help. Caetano, M., Nunes, V. & Nunes, A. 2009.
CORINE Land Cover 2006 for Continen-
tal Portugal. Technical Report, Instituto
References Geográfico Português, Lisboa.

Alonso, J.C., Alonso, J.A. & Carrascal, L.M. Catry, I., Encarnação, V., Pacheco, C., Catry,
1991. Habitat selection by foraging White T., Tenreiro, P., da Silva, L.P., Leão, F., Bally,
Storks, Ciconia ciconia, during the breed- F., Roda, S., Lopes, S., Capela, C., Alonso,
ing season. Canadian Journal of Zoology H., Saldanha, S., Urbano, O., Saraiva, J.,
69: 1957-1962. Encarnacao, P., Sequeira, N., Mendes, M.,

45
Contribution of the Red Swamp Crayfish to the diet of the White Stork

Monteiro, P., Elias, G. & Moreira, F. 2017. Galante, E., Mena, J. & Lumbreras, C. 1995.
Recent changes on migratory behaviour of Dung beetles (Coleoptera: Scarabaeidae,
the White stork (Ciconia ciconia) in Por- Geotrupidae) attracted to fresh cattle dung
tugal: towards the end of migration? Airo in wooded and open pasture. Environmen-
24: 28-35. tal Entomology 24: 1063-1068.

Catry, P., Costa, H., Elias, G. & Matias, R. Geiger, W., Alcorlo, P., Baltanás, A. & Mon-
2010. Aves de Portugal. Ornitologia do ter- tes, C. 2005. Impact of an introduced
ritório continental. Assírio & Alvim, Lisboa. Crustacean on the trophic webs of Med-
iterranean wetlands. Biological Invasions
Chenchouni, H. 2017. Variation in White 7: 49-73.
Stork (Ciconia ciconia) diet along a cli-
matic gradient and across rural-to-urban Gilbert, N.I., Correia, R.A., Silva, J.P.,
landscapes in North Africa. International Pacheco, C., Catry, I., Atkinson, P.W., Gill,
Journal of Biometeorology 61: 549-564. J.A. & Franco, A.M.A. 2016. Are white
storks addicted to junk food? Impacts
Chenchouni, H., Si Bachir, A. & AlRashidi, of landfill use on the movement and
M. 2015. Trophic niche and feeding strat- behaviour of resident white storks (Cico-
egy of the White Stork (Ciconia ciconia) nia ciconia) from a partially migratory
during different phases of the breeding population. Movement Ecology 4: 7.
season. Avian Biology Research 8: 1-13.
Hancock, J., Kushlan, J.A., Kahl, P., Harris,
Cheriak, L., Barbraud, C., Doumandji, S. A & Quinn, D. 1992. Storks, Ibises and
& Bouguessa, S. 2014. Diet variability in Spoonbills of the World. Academic Press
the White Stork Ciconia ciconia in eastern Limited, London.
Algeria. Ostrich - Journal of African Orni-
thology 85: 201-204. Johst, K., Brandl, R. & Pfeifer, R. 2001. For-
aging in a patchy and dynamic landscape:
Chinery, M. 1997. Guía de campo de los human land use and the White Stork. Eco-
insectos de España y de Europa. Ediciones logical Applications 11: 60-69.
Omega 5ª, Barcelona.
Kosicki, J. Z., Profus, P., Dolata, P.T. &
Ciach, M. & Kruszyk, R. 2010. Foraging Tobółka, M. 2006. Food composition
of White Storks on rubbish dumps on and energy demand of the White Stork
non-breeding grounds. Waterbirds 33: Ciconia ciconia breeding population. Lit-
101–104. erature survey and preliminary results
from Poland. In: Tryjanowski, P., Sparks,
Correia, A.M. 1998. Seasonal and circadian T.H. & Jerzak, L. (eds) The White Stork
foraging activity of Procambarus clarkii in Poland: studies in biology, ecology and
(Decapoda, Cambaridae) in Portugal. conservation, pp. 169-183. Poznań: Bogu-
Crustaceana 71: 158-166. cki Wydawnictwo Naukowe.

Correia, A.M. 2001. Seasonal and interspe- Loureiro, F., Bissonette, J.A., Macdonald,
cific evaluation of predation by mammals D.W. & Santos-Reis, M. 2009. Temporal
and birds on the introduced red swamp variation in the availability of Mediter-
crayfish Procambarus clarkii (Crustacea, ranean food resources: do badgers Meles
Cambaridae) in a freshwater marsh (Por- meles track them? Wildlife Biology 15:
tugal). Journal of Zoology 255: 533-541. 197-206.

46
Contribuição do Lagostim-vermelho-da-Lousiana para a dieta da Cegonha-branca

Melendro, J., Gisbert, J. & Rodríguez, A. Shannon, C.E. & Weaver, W. 1949. The
1978. Datos sobre la alimentación de mathematical theory of communication.
Ciconia ciconia. Ardeola 24: 207-209. Univ. Illinois Press, Urbana, IL.

Miraglia, G., Aloise, G., Godino, G., Santo- Silva, P.M., Aguiar, C.A.S., Niemelä, J., Sousa,
paolo, R. & Gustin, M. 2008. New data J.P. & Serrano, A.R.M. 2008. Diversity
on the diet of White Stork Ciconia ciconia patterns of ground-beetles (Coleoptera:
in Calabria (southern Italy). Acrocephalus Carabidae) along a gradient of land-use
29: 185-186. disturbance. Agriculture, Ecosystems &
Environment 124: 270-274.
Mužinić, J. & Rašajski, J. 1992. On food and
feeding habits of the White Stork, Ciconia Tablado, Z., Tella, J.L., Sanchez-Zapata,
c. ciconia, in the Central Balkans. Ecology J.A. & Hiraldo, F. 2010. The paradox of
of Birds 14: 211-223. the long-term positive effects of a North
American crayfish on a European commu-
Negro, J.J., Tella, J.L., Blanco, G., Forero, nity of predators. Conservation Biology
M,G. & Garrido-Fernández, J. 2000. 24: 1230-1238.
Diet explains interpopulation variation of
plasma carotenoids and skin pigmentation Teerink, B. J. 1991. Hair of West-European
in nestling White Storks. Physiological and mammals: atlas and identification key.
Biochemical Zoology 73: 97-101. Cambridge University Press, Cambridge.

Peris, S. J. 2003. Feeding in urban refuse Tortosa, F. S., Caballero, J.M. & Reyes-
dumps: ingestion of plastic objects by the López, J. 2002. Effect of rubbish dumps
White Stork (Ciconia ciconia). Ardeola 50: on breeding success in the White Stork in
81-84. southern Spain. Waterbirds 25: 39-43.

Pinto, M. V. 1978. Estudo morfológico dos Tsachalidis, E.P. & Goutner, V. 2002. Diet of
pêlos dos mamíferos portugueses: chaves the White Stork in Greece in relation to
para a sua determinação. Unpublished habitat. Waterbirds 25: 417-423.
report, University of Lisbon, Lisbon.
Vrezec, A. 2009. Insects in the White Stork
R Develeopment Core Team. 2017. R: A Ciconia ciconia diet as indicators of its
language and environment for statistical feeding conditions: the first diet study in
computing. R Foundation for Statistical Slovenia. Acrocephalus 30: 25-29.
Computing, Vienna, Austria.

Ramalho, R.O. & Anastácio, P.M. 2015.


Factors inducing overland movement of
invasive crayfish (Procambarus clarkii)
in a ricefield habitat. Hydrobiologia 746:
135-146.

Sanz-aguilar, A., Jovani, R., Melián, C.J.,


Pradel, R. & Tella, J.L. 2015. Multi-event
capture– recapture analysis reveals indi-
vidual foraging specialization in a general-
ist species. Ecology 96: 1650-1660.

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