8 Fea 7 e
8 Fea 7 e
8 Fea 7 e
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
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
Pedro M. Lourenço1
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
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Dietas das aves de Portugal baseadas em fóruns de fotografia online
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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 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
Anthus petrosus
1 Crustaceans (100%: Ligia oceanica) C Au
Rock Pipit
Anthus pratensis
1 Insects (100%: Lepidoptera larvae) N Wi
Meadow Pipit
Aquila pennata
3 Birds (100%: Columba livia and Larus fuscus) C Sp,Au
Booted Eagle
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Dietas das aves de Portugal baseadas em fóruns de fotografia online
SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE
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
Botaurus stellaris
2 Crustaceans (100%: Procambarus clarkii) C Wi
Eurasian Bittern
Burhinus oedicnemus
2 Insects (100%: Coleoptera, unidentified) S Su
Eurasian Thick-knee
Calidris alpina
1 Polychaetes (100%: unidentified) C Au
Dunlin
Cercotrichas galactotes
2 Insects (100%: Orthoptera) S Sp,Su
Rufous-tailed Scrub-robin
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Portuguese bird diets based on Internet photography forums
SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE
Charadrius hiaticula
6 Polychaetes (100%: unidentified) N,C Wi,Su,Au
Common Ringed Plover
Circaetus gallicus
2 Reptiles (100%: Rhinechis scalaris, Serpentes) C Sp,Su
Short-toed Snake-eagle
Cisticola juncidis
1 Insects (100%: Orthoptera) S Au
Zitting Cisticola
Coccothraustes coccothraustes
5 Seeds (100%: unidentified) C Sp,Su
Hawfinch
Corvus corone
1 Insects (100%: Odonata) C Su
Carrion Crow
Corvus monedula
2 Birds (100%: Delichon urbicumJ, Columba liviaJ) S Sp
Eurasian Jackdaw
Dendrocopus minor
5 Insects (100%: Myrmicidae, unidentified larvae) C,S Sp,Su
Lesser Spotted Woodpecker
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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
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 cirlus
3 Seeds (100%: Avena sp., unidentified) C,S Wi,Su,Au
Cirl Bunting
Emberiza citrinella
1 Insects (100%: Orthoptera) N Su
Yellowhammer
Falco columbarius
2 Birds (100%: Motacilla alba, Passeriformes) C Wi
Merlin
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
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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
Gelochelidon nilotica
1 Insects (100%: Odonata) C Su
Common Gull-billed Tern
Gyps fulvus
6 Mammals (100%: Ovis ariesn, Bos taurusn) S Wi,Su
Griffon Vulture
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
Larus audouinii
1 Crustaceans (100%: Procambarus clarkii) C Wi
Audouin’s Gull
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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
Limosa lapponica
1 Polychaetes (100%: unidentified) N Au
Bar-tailed Godwit
Loxia curvirostra
2 Seeds (100%: Pinus pinea) N Wi
Red Crossbill
Lullula arborea
2 Insects (100%: unidentified, unidentified larvae) N Su
Wood Lark
Miliaria calandra
5 Insects (100%: Orthoptera, Lepidoptera larvae) C,S Sp
Corn Bunting
Monticola saxatilis
1 Insects (100%: Gryllotalpa gryllotalpa) N Sp
Rufous-tailed Rock-thrush
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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
Muscicapa striata
1 Insects (100%: Lepidoptera) C Au
Spotted Flycatcher
Numenius arquata
1 Crustaceans (100%: unidentified crab) N Wi
Eurasian Curlew
Oenanthe hispanica
2 Insects (100%: Orthoptera, Coleoptera) S Sp
Black-eared Wheatear
Oenanthe oenanthe
1 Insects (100%: unidentified) N Sp
Northern Wheatear
Otus scops
1 Insects (100%: Lepidoptera) N Su
Eusarian Scops-owl
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Dietas das aves de Portugal baseadas em fóruns de fotografia online
SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE
Parus cristatus
1 Seeds (100%: Pinus pinea) C Wi
Crested Tit
Phalacrocorax aristotelis
1 Fishes (100%: Gobiidae) C Au
European Shag
Phylloscopus trochilus
2 Insects (100%: unidentified) N Su,Au
Willow Warbler
Pluvialis apricaria
2 Insects (100%: unidentified larvae) N,S Au
Eurasian Golden Plover
Pluvialis squatarola
5 Polychaetes (100%: unidentified) N,C Wi,Sp,Au
Grey Plover
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Portuguese bird diets based on Internet photography forums
SAMPLE
SPECIES FOOD ITEMS COVERAGE SEASON
SIZE
Porphyrio martinica
1 Amphibians (100%: Pelophylax perezi) C Au
Americn Purple Gallinule
Regulus ignicapillus
2 Insects (100%: Orthoptera) C Wi,Au
Firecrest
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
Sturnus vulgaris
1 Fruits (100%: Diospyros kaki) N Au
Common Starling
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
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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 ochropus
1 Crustaceans (100%: Atyaephyra desmarestii) S Su
Green Sandpiper
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.
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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.
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.
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Portuguese bird diets based on Internet photography forums
26
Censo deVOLUME
aves nos rios
26 Corubal2019
e Fefine, Guiné-Bissau
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).
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).
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)
1 seen outside
Ciconia microscelis African Woollyneck - -
transects
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
1 seen outside
Rostratula bengalensis Greater Painted-snipe - -
transects
1 seen outside
Tringa ochropus Green Sandpiper - -
transects
30
Censo de aves nos rios Corubal e Fefine, Guiné-Bissau
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
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Bissau. Report. Lisbon: Instituto para a
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32
VOLUME 26 2019
* 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.
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
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
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 Orthoptera 10.9 5.5 0.4 0.4 28.7 23.8 7.4 3.5 31.4 22.5
Orthoptera NI 2 0.4 0.4 124 28.4 23.6 15 7.4 3.5 99 31.0 22.3
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
Chlaenius olivieri 1 0.2 0.1 1 0.2 0.1 1 0.5 0.1 1 0.3 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 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
NF PB NF PB NF PB NF PB NF PB NF PB
N Nv N N N N
(%) (%) (%) (%) (%) (%) (%) (%) (%) (%) (%) (%)
Silphidae
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
Scarabaeidae
Melolonthidae
Tenebrionidae
Chrysomelidae
Chrysomela sp. 3 0.7 0.4 2 0.5 0.2 2 1.0 0.3 1 0.3 0.1
Curculionidae
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
39
Contribution of the Red Swamp Crayfish to the diet of the White Stork
CATAPEREIRO ROUBÃO
NF PB NF PB NF PB NF PB NF PB NF PB
N Nv N N N N
(%) (%) (%) (%) (%) (%) (%) (%) (%) (%) (%) (%)
Class Mammalia 5.5 47.1 0.2 1.6 0.5 4.4 2.5 15.7 0.3 2.1
Order Rodentia 3.6 12.8 0.2 1.6 1.5 12.9 0.3 2.1
N pellets 10 33 33 5 18 23
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
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-
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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:
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