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Inter-insular variation of the diet of Osprey Pandion haliaetus in the Canarian archipelago

Wiley
Wildlife Biology
Authors:
  • Canary Islands’ Ornithology and Natural History Group (GOHNIC)
  • Canary Islands' Ornithology and Natural History Group (GOHNIC)
  • Museo Natural de Ciencias Naturales CSIC
  • Canary Islands’ Ornithology and Natural History Group (GOHNIC)

Abstract and Figures

We studied the diet of the osprey Pandion haliaetus in the Canary Islands during 1997-2008 using prey remains under perches and nests, and direct observations. We collected data both in breeding territories and in non-breeding areas. We counted a minimum of 307 fish individuals as prey remains (both during breeding and non-breeding seasons), and identified another 78 during 433 hours of field observations. According to our results, ospreys consumed at least 15 taxa belonging to 12 families. We found slight differences in the spatial (both intra and inter insular) and temporal diet composition. During the breeding season, the main prey species were flying fishes (belonging to the family Exocoetidae) and needlefishes (belonging to the family Belonidae) according to the two employed methods (i.e. prey remains and direct observations). In the non-breeding period, the diet was composed primarily of non-autochthones freshwater fishes such as common carp Cyprinus carpio and goldfish Carassius auratus. In general, the diet diversity was similar to the diversity reported in other breeding populations of subtropical areas, and being less diverse than those of tropical areas. More precise studies evaluating the effect of fish availability in marine reserves, overfishing areas or fish farms on the demographic parameters are necessary for the management and conservation of threatened Canarian ospreys.
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Original article
Wildl. Biol. 17: 240-247 (2011)
DOI: 10.2981/10-004
ÓWildlife Biology, NKV
www.wildlifebiology.com
Inter-insular variation of the diet of osprey Pandion haliaetus in the
Canarian archipelago
Manuel Siverio, Beneharo Rodrı
´guez, Airam Rodrı
´guez & Felipe Siverio
We studied the diet of the osprey Pandion haliaetus in the Canary Islands during 1997-2008 using prey remains under
perches and nests, and direct observations. We collected data both in breeding territories and in non-breeding areas. We
counted a minimum of 307 fish individuals as prey remains (both during breeding and non-breeding seasons), and
identified another 78 during 433 hours of field observations. According to our results, ospreys consumed at least 15 taxa
belonging to 12 families. We found slight differences in the spatial (both intra and inter insular) and temporal diet
composition. During the breeding season, the main prey species were flying fishes (belonging to the family Exocoetidae)
and needlefishes (belonging to the family Belonidae) according to the two employed methods (i.e. prey remains and
direct observations). In the non-breeding period, the diet was composed primarily of non-autochthones freshwater
fishes such as common carp Cyprinus carpio and goldfish Carassius auratus. In general, the diet diversity was similar to
the diversity reported in other breeding populations of subtropical areas, and being less diverse than those of tropical
areas. More precise studies evaluating the effect of fish availability in marine reserves, overfishing areas or fish farms on
the demographic parameters are necessary for the management and conservation of threatened Canarian ospreys.
Key words: Belonidae, Canary Islands, diet, direct observations, Exocoetidae, osprey, Pandion haliaetus, prey remains
Manuel Siverio, Constitucio
´n 17-3, E-38410 Los Realejos, Tenerife, Canary Islands, Spain - e-mail: mansiverio@
telefonica.net
Beneharo Rodrı´guez, La Malecita s/n, E-38480 Buenavista del Norte, Tenerife, Canary Islands, Spain - e-mail:
benerguez@terra.es
Airam Rodrı´guez, Department of Evolutionary Ecology, Estacio
´n Biolo
´gica de Don
˜ana (CSIC), Avda. Ame
´rico Vespucio
s/n, E-41092 Seville, Spain - e-mail: airamrguez@ebd.csic.es
Felipe Siverio, Los Barros 21, E-38410 Los Realejos, Tenerife, Canary Islands, Spain - e-mail: felipe.siverio@telefonica.net
Corresponding author: Beneharo Rodrı´guez
Received 12 January 2010, accepted 2 May 2011
Associate Editor: Anne Loison
The osprey Pandion haliaetus is a top predator spe-
cialised on fish. Its diet composition is greatly in-
fluenced by seasonal and geographical fish prey
distributions (Poole 1994). Several methods have
been employed to assess its diet worldwide: direct or
video recording observations of foraging birds or
fish deliveries to the nests (Ha
¨kkinen 1977, Edwards
1988, Eriksson 1988, Chubbs & Trimper 1998,
Glass & Watts 2009), identification of prey remains
collected under nests or feeding perches (Ha
¨kkinen
1978, Swenson 1978, Carss & Brockie 1994, Gil-
Sa
´nchez 1995, Fisher et al. 2001, Cartron & Molles
2002, Clancy 2005) or the combination of both
(McKlein & Byrd 1991, Carss & Godfrey 1996). As
only flesh and easily broken bones are ingested,
pellets are not useful for assessing osprey diet
(Francour & Thibault 1996).
Breeding sites of osprey in the Macaronesian
archipelagos (i.e. in the northeastern Atlantic) are
currently limited to the Canary and the Cape Verde
Islands, where 14 and ca 80 pairs occur, respectively
(Palma et al. 2004, Siverio 2008). Despite its delicate
conservation status (catalogued as Critically En-
dangered by the Red List of Spanish birds; Triay &
Siverio 2004), specific ecological aspects of the
Canarian population remain poorly known, with
240 ÓWILDLIFE BIOLOGY 17:3 (2011)
only a few surveys conducted regarding status,
distribution and breeding parameters (Siverio &
Rodrı
´guez 2007 and references therein). The avail-
able quantitative information on the food habits of
osprey in Macaronesia is limited to the Cape Verde
population (de Naurois 1987, Den Hartog 1990,
Ontiveros 2003, Martins 2006), with a few isolated
observations on the subject from the Canarian
population (Martı
´n & Lorenzo 2001). In our study
we quantify, for the first time, composition and
inter-insular variation of the osprey diet in the
Canary Islands, mainly during the nesting period.
We do this by prey remains analysis (PRA) com-
pared with direct observations (DO) on foraging
birds and birds delivering fish to the nests.
Material and methods
The Canarian archipelago (278-298N and 138-188W)
is located 96-100 km from the northwestern Atlantic
coast of Africa. It is composed of seven major
islands and some small islets and rocks. The current
osprey breeding distribution comprises the islands
of Lanzarote (including its related islets Montan
˜a
Clara and Alegranza belonging to the Chinijo
archipelago), Tenerife, La Gomera and El Hierro
(Fig. 1). Some individuals are regularly observed in
the remaining islands, but no successful breeding
attempts have been recorded there (Siverio & Ro-
drı
´guez 2007).
We assessed diet composition during breeding
(i.e. January-July; Siverio 2006) in 2003-2007, by vi-
Figure 1. Current breeding distribution of osprey in the Canarian archipelago (occupied islands are shown in black and the numbers of
breeding pairs are also given according to Siverio 2008). The histogrammes show the prey frequencies and sample sizes (N) on the three
studied islands.
ÓWILDLIFE BIOLOGY 17:3 (2011) 241
siting 22 perch or nest sites (five in Chinijo islets in
North Lanzarote, 12 on Tenerife and five on La
Gomera; see Fig. 1) of 12 of the 14 current breeding
territories of the archipelago (Siverio 2008), and by
collecting prey remains. To avoid disturbances, we
mainly collected prey remains during July-August,
just after fledglings leave the nests. We also collected
material at non-breeding sites (one on Gran Ca-
naria and two on Tenerife), where local breeding
adults were regularly sighted, but also European
visitors (colour-ringed) have been recorded (M.
Siverio & B. Rodrı
´guez, pers. obs.). This non-
breeding season material was presented and ana-
lysed independently. We placed emphasis on key
fish parts that provided taxonomic identification,
and we considered only fresh prey remains (i.e.
estimated to be ,2 months old). We assessed the
minimum number of fish individuals in prey
remains based on the most commonly found fins,
whole tails, jaws, different bones or body parts
representing an individual (Marti et al. 2007).
Whenever possible, we identified prey items at the
species level using a reference collection and fish
guides (Whitehead et al. 1986, Fischer et al. 1987,
Gonza
´lez et al. 2000, Brito et al. 2002, Miranda &
Escala 2002). We estimated sizes and weights of
common carp Cyprinus carpio according to formu-
las relating opercula size and the measurements
published by Gil-Sa
´nchez (1995) referred to a pop-
ulation of the Iberian Peninsula. For the other prey
species identified in our study, similar formulas were
not available in the literature. We also tried to
identify all fishes delivered to nests and being carried
by flying birds, using binoculars and telescopes (10-
60 magnifications), during the 1997-2008 breeding
seasons. For this phase of our study, we employed a
total of 433 observation hours at different breeding
territories and its nearest feeding areas (mainly
located on Tenerife and La Gomera). As it has been
reported that estimating length size from direct
observations entails important biases (Carss &
Godfrey 1996), we did not consider this direct
method to estimate the size of prey. Niche breath
and diet diversity were calculated using the stan-
dardised Levin’s (B
sta
) and Shannon (H) indexes
(Krebs 1999) applied to the items consumed. The
Levin’s index formula is:
B¼1=Xp2
i;
where p
i
is the frequency of each food category
consumed. The standardised Levin’s index formu-
la is:
Bsta ¼B-1
Bmax -1;
where B is the Levin’s index and B
max
is the total
number of food categories recognised (lowest
niche breadth ¼0 and greatest niche breadth ¼1).
The Shannon index (in which higher values refer
to higher diversity) formula is:
H¼-Xpilogpi:
We measured the diet overlap between islands using
percentage of food items through the Pianka’s index
(O):
Ojk ¼X
n
i¼1
pijpik
ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
X
n
i¼1
p2
ij X
n
i¼1
p2
ik
s;
where p
i
is the percentage of prey item iin the diet
of islands jand k. Pianka’s index varies between 0
(total separation) and 1 (total overlap).
To study insular variation of the most important
prey (belonging to the families Exocoetidae and
Belonidae), we applied likelihood ratio tests (G-
tests), comparing a certain prey item with the total
number of the remaining prey items. We conducted
analyses using SPSS (version 17.0).
Results
During the breeding season, we counted a minimum
of 262 and 78 fish individuals in prey remains and
direct observation, respectively, including at least 15
taxa (belonging to 12 families; Table 1). The most
frequently consumed prey was flying fishes (belong-
ing to the family Exocoetidae; 42.7 and 19.2%
according to PRA and DO, respectively) and nee-
dlefish (belonging to the family Belonidae; 38.5 and
6.4% according to PRA and DO, respectively). At
least six species were represented by only one in-
dividual in the PRA and DO (see Table 1). We found
some remains of red rock crabs Grapsus grapsus at
two feeding perches on Tenerife, but they were not
considered in the analysis as we were not confident
that they were consumed by ospreys. Diet compo-
sition varied slightly between the islands (La Go-
mera: B
sta
¼0.35 and H¼0.53, Tenerife: B
sta
¼0.21
and H¼0.59 and Chinijo: B
sta
¼0.42 and H¼0.63;
see Fig. 1). Only on Tenerife, fresh-water fishes were
caught, and the percentage of captures of flying
242 ÓWILDLIFE BIOLOGY 17:3 (2011)
fishes (belonging to the family Excoetidae) in Chi-
nijo was lower than on La Gomera and Tenerife (see
Fig. 1). Diet overlap (O), expressed as Pianka’s in-
dex, between La Gomera and Tenerife was 0.99, be-
tween Tenerife and Chinijo 0.66 and between Chi-
nijo and La Gomera 0.68. The two most important
groups of prey showed different patterns. Thus, the
species belonging to the family Exocoetidae were
significantly more consumed on Tenerife and La
Gomera than in Chinijo (G
2
¼20.85, P ,0.001), but
for species belonging to the family Belonidae it did
not vary between the islands (G
2
¼2.33, P ¼0.31).
In the non-breeding areas (all associated with large
artificial ponds), all identified prey was freshwater
fishes. Of a total of 45 fish individuals, the common
carp (belonging to the family Cyprinidae; 71.1%,
N¼32) was the most common species followed by
goldfish Carassius auratus (belonging to the family
Cyprinidae; 8.9%, N ¼4), tilapia Oreochromis
mossambicus (belonging to the family Cichlidae;
6.7%, N ¼3) and large mouth bass Micropterus
salmoides (belonging to the family Centrarchidae;
2.2%, N ¼1), whereas the rest remainded uniden-
tified (11.1%, N ¼5). Estimated mean size and
weight of common carp (N¼35) captured by osprey
were 25.9 cm 62.6 (range: 21.5-32.3) and 223.3 g 6
43.4 (range: 147.4-329.3), respectively (Fig. 2).
Discussion
We found only small differences between prey re-
main analysis and direct observations (see Table 1),
so both methods could be considered complemen-
tary, though some limitations and biases are present
(see Marti et al. 2007). Direct observation is time
consuming, and the percentage of correct identifi-
cations is highly biased and related to several factors
such as size, colour and morphology of the fish, and
by the distance of the observation (Carss & Godfrey
1996). Fish identification is also impeded, because
often fish are partially eaten when observations
commence. In the case of prey remains analysis,
some biases are associated with identifiable, con-
spicuous and lasting body pieces, so usually the
smallest fish are more prone to be undetected
compared to bigger fish (Carss & Brockie 1994).
The presence of scavengers that may affect the
durability of larger prey remains, could represent a
Table 1. Breeding diet composition of osprey in the Canary Islands according to prey remains analysis (PRA) and direct observations
(DO) during the periods 2003-20 07 and 1997-2008, respectively (see details in text). MNI ¼Minimum number of individuals.
Prey taxa PRA DO
Family Species MNI % MNI %
Marine fish
Cupleidae Unidentified 1 4 - -
Mugilidae Unidentified 1 4 1 1.3
Belonidae Tylosurus acus* 96 366 5 6.4
Belonidae Unidenfied 5 19 - -
Exocoetidae Cheilopogon heterurus* 112 427 15 19.2
Aulostomidae Aulostomus strigosus - - 1 1.3
Moronidae Dicentrarchus labrax - - 1 1.3
Carangidae Trachinotus ovatus 5 19 2 2.6
Sparidae Sparus auratus 4 15 2 2.6
Sparidae Diplodus sp. 2 8 - -
Scaridae Sparisoma cretense 415- -
Sphyraenidae Sphyraena viridensis 14--
Freshwater fish
Cichlidae Oreochromis mossambicus 14--
Cyprinidae Carassius auratus - - 7 9.0
Cyprinidae Cyprinus carpio 10 38 - -
Unidentified Unidentified 20 76 44 56.4
Total 262 78
B
sta
0.15 0.38
H’ 0.55 0.70
* includes primarily this species but possibly others too.
ÓWILDLIFE BIOLOGY 17:3 (2011) 243
small bias in our study as we collected remains at the
end of the nesting season. In this sense, we noticed
that some prey remains were probably moved into
cracks by the black rat Rattus rattus. Furthermore,
yellow legged gull Larus michahellis and common
raven Corvus corax usually occur in the vicinity of
the osprey feeding perches or nests, apparently
searching for food (M. Siverio & B. Rodrı
´guez, pers.
obs.).
Taking into account the quantitative data from
our study and the addition of saddled seabream
Oblada melanura (belonging to the family Spari-
dae), quoted as an occasional item (Martı
´n&
Lorenzo 2001), the diet of osprey in the Canary
Islands is composed of a minimum of 16 fish taxa
(belonging to 12 families). This diet diversity is
comparable to reports from other Palearctic popu-
lations, but lower than reported in tropical waters
such as the southern Red Sea or Cape Verde (Table
2). Reviewing osprey dietary studies during breed-
ing in the western Palearctic, northern populations
feed mainly on freshwater fishes, while southern
populations feed mainly on marine fishes, and it
seems that diet diversity increases in a latitudinal
gradient southward (see Table 2). It has been
suggested that sea surface temperature is the main
proximate factor affecting surface fish availability
(both factors related positively), and consequently,
osprey feeding behaviour selection into marine or
freshwater environments (Marquiss et al. 2007).
However, the proportion of marine items in the
osprey diet must also be influenced by local factors
such as availability of foraging areas (e.g. freshwa-
ter body masses are scarce and small on the Canary
Islands) and human disturbances. In this sense, it is
well-known that ospreys are generalist and oppor-
tunistic foragers on fish, depending greatly on
locally available resources (Poole 1994, Martins
2006). This behaviour also explains the observed
spatial differences within the Canarian archipelago.
According to the Pianka’s index, the diets of ospreys
from La Gomera and Tenerife overlap more (0.99)
than the osprey diet from Chinijo compared with La
Gomera (0.68) or Tenerife (0.66). These differences
are probably related to fish availability as Canarian
coastal fish assemblages vary greatly within and
between the islands according to the particular
habitat features and human pressure (Falco
´n et al.
1996, Tuya et al. 2004, Clemente et al. 2010).
During the breeding season, freshwater fishes
(belonging to the families Cichlidae and Cyprinidae)
were only consumed in low numbers on Tenerife (see
Figure 2. Estimated size (A) and weight (B)
of common carps (N ¼35) consumed by
osprey on the Canary Islands based on the
opercula size according to equations de-
scribed in Gil-Sa
´nchez (1995).
244 ÓWILDLIFE BIOLOGY 17:3 (2011)
Fig. 1), and thus the relative high level of diet diversity
there (H¼0.59) could be related to their consump-
tion. Both on Tenerife and La Gomera, although
more abundant on Tenerife (Siverio et al. 2008, M.
Siverio & B. Rodrı´guez, pers. obs.), the breeding
territories are situated close to water ponds used for
agriculture. Many of these reservoirs contain domes-
ticated fishes which make up potential prey for
ospreys. However, according to our observations on
Tenerife, the domesticated fishes seem to be con-
sumed mainly during the non-breeding season or by
non-breeding or migratory birds. Given the lack of
native freshwater fish in the Canary Islands, the
artificial fish source may be crucial when weather
conditions (strong winds or rough sea) impede fishing
at sea (Grubbs 1977). It is known that birds also
forage on fish farms of gilthead seabream Sparus
auratus and European seabass Dicentrarchus labrax
(M. Siverio & B. Rodrı
´guez, pers. obs.), of which
some are close to nesting sites of Tenerife.
Although several non-fish prey have been re-
ported worldwide (see Wiley & Lohrer 1973), in the
Canaries only lizards (two Caesar’s lizard Gallotia
caesaris individuals captured on El Hierro; Dı
´az et
al. 1986) and crabs (without any more information;
Martı
´n & Lorenzo 2001) have been recorded.
Curiously, recent observations have indicated that
some ospreys ingested algae (Rhizoclonium sp.
belonging to the family Cladophoraceae) and slime
near the banks of an agricultural water reservoir,
but the reason for this behaviour remains un-
known (Siverio et al. 2008).
The estimated mean length (25.9 cm) and weight
(223.3 g) of the common carp consumed by ospreys
in the Canaries are within the range recorded
elsewhere (Ha
¨kkinen 1978, Poole 1989, Francour
& Thibault 1996). It has been observed that the size
and weight of fish captured by ospreys vary ac-
cording to its availability, and it has been sug-
gested that neither species nor size are selected for
by this raptor (Swenson 1978, Poole 1989, Carss &
Godfrey 1996, Francour & Thibault 1996).
Our study indicates that during the breeding
season, the osprey diet in the Canaries is mainly
composed of flying fishes (belonging to the family
Exocoetidae) and needlefish (belonging to the
family Belonidae), species whose abundance is
probably related to their very low commercial
fisheries value (G. Gonza
´lez-Lorenzo, pers. com.).
The slightly higher diet diversity observed in the
Chinijo islets compared to Tenerife and La
Gomera could be influenced by the fact that the
former present a better conservation state of
coastal fish assemblages as they were declared as
a Marine Reserve by the Spanish Government in
1986. At this site, protection measures against
overfishing have contributed to the increase and/or
the maintenance of the populations of certain
heavily exploited species, such as for example the
parrot fish Sparisoma cretense (Garcı
´a-Charton et
al. 2008). The differences in the management re-
Table 2. Comparison of diet of selected osprey breeding populations across the western Palearctic based on prey remains. The Behaviour/
main foraging ground abbreviations are M-Fe¼migratory and freshwater environment and S-Me ¼sedentary and marine environment.
Location Latitude Longitude
Behaviour/main
foraging ground N8prey Species/taxa B
sta
HSource
Finland (inland) 60.58N 23.88E M-Fe 716 12 0.13
a
0.58
a
Ha
¨kkinen (1978)
Finland (coastal) 60.38N 21.38E M-Fe 198 10 0.33
a
0.71
a
Ha
¨kkinen (1978)
Scotland (north) 56.68N 3.68W M-Fe 104 6 0.63 0.67 Carss & Brockie (1994)
Scotland (south) 54.98N 4.48W M-Fe 239 9 0.36 0.69 Marquiss et al. (2007)
Germany (north-east) 51.58N 13.58E M-Fe 562 6 0.47 0.22 Mu
¨ller et al. (2005)
France (south)
b
47.18N 2.58E M-Fe 90 14 0.60 1.02 Thiollay & Wahl (1998)
Corsica (inland)
c
41.88N 8.78E S-Me 258 12 0.46 0.87 Francour & Thibault (1996)
Portugal (south)
d
37.18N 8.68W S-Me 49 9 0.21 0.62 Cancela & Palma (1984)
Canary Islands 28.28N 15.38W S-Me 262 13
e
0.15 0.55 Our study
Red Sea (south) 16.88N 42.08E S-Me 688 56 0.30
f
- Fisher et al. (2001)
Cape Verde Islands 16.18N 22.88W S-Me 1264 32 0.20 1.01 Martins (2006)
a
calculated using number of key bones per species;
b
study based on direct observation;
c
considering also some direct observations;
d
currently extinct population;
e
16 considering prey remains analysis, direct observations and bibliographic sources (Martı
´n & Lorenzo 2001);
f
mean value of four studied islands.
ÓWILDLIFE BIOLOGY 17:3 (2011) 245
gimes could be affecting the diet composition of
osprey in Chinijo (a marine reserve) vs Tenerife
and La Gomera (unprotected and overfishing ar-
eas). More precise studies to assess the effect of
availability of fish (under natural conditions such
as marine protected areas, or at artificial sources
such as water ponds or fish farms) on the breeding
success and demographic parameters of popula-
tions are necessary for the management and con-
servation of threatened Canarian ospreys.
The use of fish farms as artificial sources of food
by osprey could also represent an additional source
of mortality as ospreys may entangle in the nets that
cover the cages (Siverio & Rodrı
´guez 2007). As it is
suspected that the maintenance staff of these farms,
to avoid legal problems, may easily hide dead birds
if found, competent authorities should inspect these
installations to detect and correct potential risks to
the raptor species.
Acknowledgements - we are very grateful to Francisco M.
Gonza
´lez for his interest in our study and for allowing us
access to some otherwise inaccessible locations using his
boat. We also thank Aurelio Acevedo, Leandro De Leo
´n
and Jaime Ginove
´s who helped us collect prey remains.
Special thanks go to Alejandro Sancho, Jose
´Carlos
Herna
´ndez and Alberto Brito of the Department of
Zoology (La Laguna University), and Rafael Miranda of
the Department of Zoology (Navarra University) for their
help in the identification of prey remains. Furthermore,
Juan Curbelo, Jose
´G. Martı
´n, Jose
´J. Herna
´ndez, Manuel
Pe
´rez and Rosme
´n Ramos provided fish for our reference
collection. The 2004-2005 surveys in Tenerife were
partially funded by Oficina de Gestio
´n del Parque Rural
de Teno (Cabildo de Tenerife). In addition, the Canarian
delegation of SEO/BirdLife supported us by covering
some of the field expenses. Mikael Hake and Daniel
Schmidt provided valuable information of osprey diet in
Sweden and Germany, respectively. Finally, Greg. P.
Clancy (University of New England, Armidale, NSW
Australia), Charles J. Henny (USGS, Forest and Range-
land Ecosystem Science Center, Oregon) and an anony-
mous referee provided valuable comments and improved
the English version of earlier drafts of the manuscript.
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ÓWILDLIFE BIOLOGY 17:3 (2011) 247
... A few blue crab (Portunus segnis) remains could be attributed to osprey predations since this species cannot be encountered out of the water. Similarly, red rock crabs (Grapsus grapsus) were identified by Siverio et al. (2011) at two perches on Tenerife Island (Canarian Archipelago) but they were not considered consumed by ospreys by the latter authors. A few fragments of isopod exoskeletons were also found. ...
... In this sense, Francour and Thibault (1996: tab. 1) found that mullet opercles and preopercles constitute almost 80% of the collected remains in Corsica (South-East France). Similarly, opercle bones are also among the dominant remains found in Finland, Latvia, and the Canarian Archipelago (Häkkinen, 1978;Siverio et al., 2011;Kalvans & Bajinskis, 2016). Prevost (1982: 87) indicates that opercles of even the smallest fish caught were removed in Senegal. ...
Article
The Osprey Pandion haliaetus is one of the most widely distributed raptor species in the world, present on all continents except Antarctica. Since its diet is mainly based on fish, this raptor is typically encountered close both to marine and fresh waters. Ospreys are well represented in the Arabian Peninsula where remote islands are the location for some of their key breeding sites. On Marawah Island (Emirate of Abu Dhabi, United Arab Emirates), ospreys have been reported to build nests on top of abandoned man-made structures, including archaeological sites. The discovery of fish remains associated with numerous bird bones and eggshell fragments in archaeological deposits raises the question of the potential contamination of ancient faunal accumulations by birds of prey. To date, the possible impact of ospreys on zooarchaeological assemblages has been little considered and the taphonomic signature of this fish-eating raptor has never been described. However, ospreys are effective competitors to traditional and small-scale fisheries and should be considered as potential accumulators of fish remains on archaeological sites located close to water bodies. Indeed, zooarchaeological analyses demonstrate that fish had always played a major role in the daily subsistence of the ancient inhabitants of Marawah Island since the first traces of occupation dating back some 8000 years. The present study will enable researchers working in the region as well as in other geographical area to determine if ospreys are accumulation agents for fish remains on archaeological sites. The present diet assessment of ospreys allows us to specify the taphonomic signature of this raptor: targeted species are mainly medium to large-sized fish swimming just beneath the surface (e.g. needlefish and queenfish) and slow benthic fish occurring in shallow waters such as tripodfish, emperors, and groupers. Bone accumulations are almost entirely composed of skull elements, indicating specific discarding behaviours. Certain traces left on jaw bones, in particular maxillae, can also help to differentiate osprey accumulations from archaeological ones.
... populations also occur in the south, scattered over some Mediterranean islands, the north and north-east shore of Africa and the Atlantic archipelagos of Cape Verde and the Canaries (Thibault, Bretagnolle & Dominici, 2001). Some aspects of osprey ecology in the South, such as the fact they are resident, the natural substrate where they build their nests (usually on top of pinnacles, coastal cliff ledges or on the ground; Naurois, 1987;Fisher et al., 2001;Thibault, Bretagnolle & Dominici, 2001;Triay & Siverio, 2008) and prey consumed (essentially marine fish species; see a review in Siverio et al., 2011), considerably differ from those in higher latitudes, where the birds are migratory and tree nesters (Saurola, 1997), and feed mainly on freshwater fish species (see Siverio et al., 2011). In general, southern resident populations are rare and severely threatened (some of them even extinct) mostly because of human persecution and habitat degradation, or habitat loss due to coastal developments (Schmidt, 1998;Palma, 2001;Triay & Siverio, 2004;Siverio & Rodr ıguez, 2005). ...
... populations also occur in the south, scattered over some Mediterranean islands, the north and north-east shore of Africa and the Atlantic archipelagos of Cape Verde and the Canaries (Thibault, Bretagnolle & Dominici, 2001). Some aspects of osprey ecology in the South, such as the fact they are resident, the natural substrate where they build their nests (usually on top of pinnacles, coastal cliff ledges or on the ground; Naurois, 1987;Fisher et al., 2001;Thibault, Bretagnolle & Dominici, 2001;Triay & Siverio, 2008) and prey consumed (essentially marine fish species; see a review in Siverio et al., 2011), considerably differ from those in higher latitudes, where the birds are migratory and tree nesters (Saurola, 1997), and feed mainly on freshwater fish species (see Siverio et al., 2011). In general, southern resident populations are rare and severely threatened (some of them even extinct) mostly because of human persecution and habitat degradation, or habitat loss due to coastal developments (Schmidt, 1998;Palma, 2001;Triay & Siverio, 2004;Siverio & Rodr ıguez, 2005). ...
Article
Between 2004 and 2007, we studied density, habitat features and breeding parameters of the osprey (Pandion haliaetus) population in Boa Vista Island (Cape Verde). A total of 79 nest structures were identified, 37 of which were occupied for at least 1 year during the study period. The osprey population ranged between 14 and 18 pairs, and the mean density and distance between neighbouring occupied nests were 2.58 pairs per 100 km2 and 3089 m, respectively. Occupied nests were found to be significantly further from the coastline and roads than unoccupied nests, but the distances from villages were similar. The majority (81.1%) of the 37 occupied nests were easily accessible to humans. Mean clutch size was 2.59, average productivity was 0.76 young/active nest, and breeding success was 58.8% [Correction added on 13 May 2013, after first online publication: the average productivity was changed from 0.72 to 0.76]. Density in Boa Vista was higher than that in other sedentary island populations in the Western Palearctic, whereas the productivity was the lowest of this region. Clutch size did not vary among Western Palearctic populations, but the differences observed in productivity were likely influenced by local factors that in Boa Vista are attributed to nest depredation by the brown-necked raven (Corvus ruficollis) and to direct human persecution.
... Many osprey populations are closely dependent on the marine environment for fishing, especially in archipelagos (Francour and Thibault, 1996;Martins et al., 2011;Siverio et al., 2011). Currently, coastal insular ecosystems are highly threatened by climate change, introduction of exotic species or human pressure (Graci and Dodds, 2010;Hernández-Delgado, 2015;Spatz et al., 2017). ...
Article
The use of anthropogenic debris as nest-building materials may affect nest function. We study ospreys (Pandion haliaetus) on an island with scarce vegetation and high availability of beached marine debris. We describe the anthropogenic debris in osprey nests, evaluate the factors affecting its prevalence and abundance, and test its potential effects on breeding parameters. We also quantify plastic entanglements among adults and nestlings. Of the 36 studied nests, 92 % included non-natural items, with plastic being the most frequent material (88.9 %). Nests that were bigger and closer to the coast had more anthropogenic items. The abundance of anthropogenic items in nests did not correlate with osprey breeding parameters. We recorded two live entangled adult females, which represent 3.9 % of the adult population. Monitoring the abundance of anthropogenic debris and its effects on wildlife is necessary to guarantee long-term viability of coastal wildlife.
... Los peces beloniformes («maraos») también resultan presas usuales en la dieta de las águilas pescadoras, dada su costumbre de nadar o permanecer estáticos cerca de la superficie, siendo fáciles de divisar y capturar (safRiel et al. 1985); tanto es así que en otras regiones, como California, en el litoral pacífico norteamericano, y en las islas Canarias y el archipiélago Cabo Verde, en el océano Atlántico africano, señalan la preferencia del Águila Pescadora por especies de este orden (MaRtins et al. 2011;siveRio et al. 2011). En las costas del golfo de California, caRtRon & Molles (2002) informaron que las presas preferidas de las águilas pescadoras fueron peces de las familias Mugilidae y Belonidae. ...
Article
Full-text available
RESUMEN: El Águila Pescadora (Pandion haliaetus), de hábitos estrictamente piscívoros, es el único representante de la familia Pandionidae. Es una especie migratoria, con una distribución cosmopolita. A pesar de su presencia habitual en humedales litorales venezolanos, en el país no existe un estudio sobre la variación estacional de su dieta. Esta investigación se llevó a cabo de abril hasta mayo (temporada de sequía) y de junio hasta septiembre (temporada de lluvia), en el complejo lagunar Chacopata-Bocaripo, península de Araya, estado Sucre, mediante la identificación de peces recolectados en las perchas de alimentación, que luego fueron identificados taxonómicamente. Su dieta estuvo constituida por seis especies de peces, agrupadas en cinco familias; en orden de abundancia: Ariidae > Mugilidae > Hemiramphidae > Batrachoididae > Belonidae. Al contrario de lo determinado en estudios de otros países, los bagres (Cathorops spixii) constituyeron el renglón de mayor importancia en la dieta (64,00%), lo cual llama la atención dado el carácter demersal de los Ariidae, y la preferencia alimentaria generalizada del Águila Pescadora por peces epipelágicos. Mugil curema y M. liza (25,84 %) son especies usuales en las lagunas costeras; a pesar de sus hábitos bentófagos, eventualmente realizan desplazamientos en cardúmenes en aguas subsuperficiales que hacen a sus individuos muy accesibles para las águilas pescadoras. Los beloniformes (Hemiramphus brasiliensis y Tylosurus acus) también fueron parte de la dieta, dada su costumbre de nadar cerca de la superficie siendo fáciles de divisar y capturar. Esta rapaz está categorizada como vulnerable en gran parte de su ámbito distribucional. Palabras clave: Ariidae, ave migratoria, especie vulnerable, peces pelágicos y demersales ABSTRACT: The Osprey (Pandion haliaetus), a specialist fish eater, is the only member of Pandionidae. The Osprey is a long-distance migratory raptor distributed worldwide. Despite its usual presence in venezuelan coastal wetlands, no comprehensive studies their diet composition have been carried out in our country. The present study was conducted in Chacopata-Bocaripo lagoon complex, peninsula of Araya, state of Sucre, and it described the seasonal variation in diet of ospreys. We collected fish remains, recovered in perch sites that were later identified taxonomically by keys. In total, six fish species were identified in the diet; the most numerous families were: Ariidae > Mugilidae > Hemiramphidae > Batrachoididae > Belonidae, in that order of abundance. Unlike other studies carried out in other countries, catfishes (Cathorops spixii) accounted for 64,0% of fish diet items identified, it is noteworthy given the demersal condition of Ariidae and the preference of the Osprey for epipelagic preys. Mullets (Mugil curema y M. liza) are common species in coastal lagoons, in spite of its benthic feeding habits its shoal movements in subsuperficial waters make them catchable preys. Beloniformes fishes (Hemiramphus brasiliensis and Tylosurus acus) were also prey due to their behavior of swimming near the surface, being easy to detect and capture. This raptor is classified as vulnerable largely through its distribution range. INTRODUCCIÓN El Águila Pescadora (Pandion haliaetus L. 1758), único representante de la familia Pandionidae, es un ave rapaz exclusivamente piscívora, de unos 52 a 71 cm de longitud total y una envergadura alar entre 150-170 cm; sin embargo, su peso oscila entre 1,4-1,7 kg. Habita a lo largo de las costas, lagos y ríos. Dispone de diversas adaptaciones anatómicas como reversibilidad del dedo exterior delantero (zigodactilia) (sustaita et al. 2109), lo que le permite agarrar a los escurridizos peces con dos dedos hacia adelante y dos hacia atrás; éstos presentan prominencias cutáneas, y uñas largas y curvadas para evitar el deslizamiento de las presas; los tarsos son alargados y las alas relativamente largas; poseen válvulas nasales que ayudan en las zambullidas y un largo intestino delgado, probablemente para facilitar la digestión (Poole 1994). Esta rapaz, de una distribución cosmopolita, excepto la Antártida, puede viajar entre 1.900 y 8.700 km, encontrándose la mayor parte de la población en el norte de Europa, la cual se ha estimado entre 8.000 a 10.000 parejas (Poole 1994); sin embargo, en EE.UU se ubica la mayor concentración poblacional de individuos reproductivos del mundo distribuidas en tres poblaciones que se ubican en la costa oeste, la región del medio occidente y la costa este de Norteamérica Bol. Inst. Oceanog. Venez. 58(2): 122-129 (2018) 1 Fig., 3Tabs.
... Los peces beloniformes («maraos») también resultan presas usuales en la dieta de las águilas pescadoras, dada su costumbre de nadar o permanecer estáticos cerca de la superficie, siendo fáciles de divisar y capturar (safRiel et al. 1985); tanto es así que en otras regiones, como California, en el litoral pacífico norteamericano, y en las islas Canarias y el archipiélago Cabo Verde, en el océano Atlántico africano, señalan la preferencia del Águila Pescadora por especies de este orden (MaRtins et al. 2011;siveRio et al. 2011). En las costas del golfo de California, caRtRon & Molles (2002) informaron que las presas preferidas de las águilas pescadoras fueron peces de las familias Mugilidae y Belonidae. ...
Article
Full-text available
RESUMEN: El Águila Pescadora (Pandion haliaetus), de hábitos estrictamente piscívoros, es el único representante de la familia Pandionidae. Es una especie migratoria, con una distribución cosmopolita. A pesar de su presencia habitual en humedales litorales venezolanos, en el país no existe un estudio sobre la variación estacional de su dieta. Esta investigación se llevó a cabo de abril hasta mayo (temporada de sequía) y de junio hasta septiembre (temporada de lluvia), en el complejo lagunar Chacopata-Bocaripo, península de Araya, estado Sucre, mediante la identificación de peces recolectados en las perchas de alimentación, que luego fueron identificados taxonómicamente. Su dieta estuvo constituida por seis especies de peces, agrupadas en cinco familias; en orden de abundancia: Ariidae > Mugilidae > Hemiramphidae > Batrachoididae > Belonidae. Al contrario de lo determinado en estudios de otros países, los bagres (Cathorops spixii) constituyeron el renglón de mayor importancia en la dieta (64,00%), lo cual llama la atención dado el carácter demersal de los Ariidae, y la preferencia alimentaria generalizada del Águila Pescadora por peces epipelágicos. Mugil curema y M. liza (25,84 %) son especies usuales en las lagunas costeras; a pesar de sus hábitos bentófagos, eventualmente realizan desplazamientos en cardúmenes en aguas subsuperficiales que hacen a sus individuos muy accesibles para las águilas pescadoras. Los beloniformes (Hemiramphus brasiliensis y Tylosurus acus) también fueron parte de la dieta, dada su costumbre de nadar cerca de la superficie siendo fáciles de divisar y capturar. Esta rapaz está categorizada como vulnerable en gran parte de su ámbito distribucional. Palabras clave: Ariidae, ave migratoria, especie vulnerable, peces pelágicos y demersales ABSTRACT: The Osprey (Pandion haliaetus), a specialist fish eater, is the only member of Pandionidae. The Osprey is a long-distance migratory raptor distributed worldwide. Despite its usual presence in venezuelan coastal wetlands, no comprehensive studies their diet composition have been carried out in our country. The present study was conducted in Chacopata-Bocaripo lagoon complex, peninsula of Araya, state of Sucre, and it described the seasonal variation in diet of ospreys. We collected fish remains, recovered in perch sites that were later identified taxonomically by keys. In total, six fish species were identified in the diet; the most numerous families were: Ariidae > Mugilidae > Hemiramphidae > Batrachoididae > Belonidae, in that order of abundance. Unlike other studies carried out in other countries, catfishes (Cathorops spixii) accounted for 64,0% of fish diet items identified, it is noteworthy given the demersal condition of Ariidae and the preference of the Osprey for epipelagic preys. Mullets (Mugil curema y M. liza) are common species in coastal lagoons, in spite of its benthic feeding habits its shoal movements in subsuperficial waters make them catchable preys. Beloniformes fishes (Hemiramphus brasiliensis and Tylosurus acus) were also prey due to their behavior of swimming near the surface, being easy to detect and capture. This raptor is classified as vulnerable largely through its distribution range. INTRODUCCIÓN El Águila Pescadora (Pandion haliaetus L. 1758), único representante de la familia Pandionidae, es un ave rapaz exclusivamente piscívora, de unos 52 a 71 cm de longitud total y una envergadura alar entre 150-170 cm; sin embargo, su peso oscila entre 1,4-1,7 kg. Habita a lo largo de las costas, lagos y ríos. Dispone de diversas adaptaciones anatómicas como reversibilidad del dedo exterior delantero (zigodactilia) (sustaita et al. 2109), lo que le permite agarrar a los escurridizos peces con dos dedos hacia adelante y dos hacia atrás; éstos presentan prominencias cutáneas, y uñas largas y curvadas para evitar el deslizamiento de las presas; los tarsos son alargados y las alas relativamente largas; poseen válvulas nasales que ayudan en las zambullidas y un largo intestino delgado, probablemente para facilitar la digestión (Poole 1994). Esta rapaz, de una distribución cosmopolita, excepto la Antártida, puede viajar entre 1.900 y 8.700 km, encontrándose la mayor parte de la población en el norte de Europa, la cual se ha estimado entre 8.000 a 10.000 parejas (Poole 1994); sin embargo, en EE.UU se ubica la mayor concentración poblacional de individuos reproductivos del mundo distribuidas en tres poblaciones que se ubican en la costa oeste, la región del medio occidente y la costa este de Norteamérica Bol. Inst. Oceanog. Venez. 58(2): 122-129 (2018) 1 Fig., 3Tabs.
... Differences in the extent of shallow platforms in front of recently active and randomly selected cliffs could also be related to human presence because, at a small scale (just in front of the nest), sea characteristics may affect the likelihood of human activities such as anchoring, scuba diving or spear-fishing. On the other hand, the likely higher availability of pelagic fishes (Exocoetidae and Belonidae) in such sites, which constitute the main Osprey prey in the Canary Islands (Siverio et al. 2011a), could be also influencing habitat choice. No local studies of the population dynamics of these pelagic fishes are available, but benthic species are much influenced by habitat degradation and over-fishing (Tuya et al. 2004). ...
Article
We studied nesting habitat selection of the endangered non-migratory Osprey Pandion haliaetus population of the Canary Islands and evaluated the effect of human expansion in recent decades. Compared with randomly selected potential nest-sites, Osprey nests were more frequently found on taller, southwest-facing cliffs, char-acterized by lower human pressure and closer to Yel-low-legged Gull Larus michahellis colonies and Barbary Falcon Falco pelegrinoides breeding sites. Furthermore, changes in some breeding habitat features have been detected in recent decades. According to our predictive models, large areas of suitable habitat are available but unoccupied in the Canaries, and human activities are probably limiting the settlement and dispersion of new pairs.
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The analysis of metals in different tissues of raptors has been an important tool for assessing metal pollution. Several studies using a range of sentinel raptor species have been carried out in Portugal and Spain since the 1980s to identify the adverse effects in the animals themselves and on their populations, to identify the contamination of the food chain, to determine the levels of environmental contamination and to estimate human health risks. The aim of this work is to provide synthesized information of the studies carried out in Portugal and Spain in the direct biomonitoring of metals and metalloids using raptors, through a systematic search of the published literature. The information is summarized taking into account specific issues, such as monitored raptor species, sampling periods, monitored areas, type of samples, analytical techniques used in the determination of the metals and metalloids, the analysed metals and metalloids, and overall analysis of the concentrations obtained. There is a striking difference between the number of studies performed in Portugal and Spain, and most of them have been carried out in Spain. The eagle owl, black kite, and common buzzard were the species from which the greatest number of individuals have been analysed. Among the most analyzed biological samples, the blood and liver samples were used to measure the concentrations of all studied metals, while bone was mainly collected to evaluate chronic exposure to lead and feathers to evaluate exposure to mercury during feather growth. Atomic absorption spectrometry has been the most frequently performed technique to determine the majority of metals and arsenic. In general, the concentrations of metals detected in raptor samples from Portugal and Spain are low and insufficient to produce toxic side effects. Only lead, in certain cases, can be related with toxic side effects. However, particular attention should be given to mercury due to its high toxicity, its transport from an aquatic environment to the adjacent terrestrial food web, and because the mercury toxicity threshold has yet to be established for raptors. This work confirms the need for further biomonitoring studies of metals with raptors, especially in Portugal; the establishing of national programs to conduct long-term studies; and creating a network between Portugal and Spain to study environmental contamination using raptors.
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The Teno range of mountains, located in the northwest Tenerife, Canary Islands, is still a refuge for the flora and fauna of the island. Until now, at least four native species of reptiles, 232 of birds (both breeding and migrant), and six mammals have been recorded for that site. For some of these animals, such as Canarian Spotted Lizard (Gallotia intermedia), Manx Shearwater (Puffinus puffinus), Osprey (Pandion haliaetus), Rock Sparrow (Petronia petronia) and Northern Raven (Corvus corax), these cliffs, gorges, tablelands or forests hold a good part or all of their insular populations. This illustrated and annotated checklist synthesizes and updates the available information on terrestrial vertebrates for the entire northwestern area of Tenerife. A current and comprehensive list of extant species supports effective management strategies and conservation projects as well as the efficient dissemination of information regarding this Natural Heritage. More info at http://www.gohnic.org/noticias/nuevas-publicaciones-gohnic/
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In situ visual surveys using a hierarchical sampling design were carried out at 36 sublittoral rocky locations along the central-east Atlantic Canarian Archipelago to find relationships among (1) benthic primary producers, (2) the demographic structure of the herbivorous sea urchin Diadema antillarum Phillipi and (3) the trophic structure of coastal fish communities. Our correlation approach displayed a relationship between the lack of large macroinvertebrate-eating predatory fish and the increase in density of sea urchins, in addition to a decrease in fish richness. In contrast, increases in fast-growing plankton feeding fish species were detected. The size structure of D. antillarum is dominated by small-to-intermediate sized sea urchins in environments with a high density of individuals, whereas low sea urchin density locations are characterized by the dominance of large sized individuals. The physical complexity of the substrate seems to play an important role in determining the local patchiness of D. antillarum. Finally, a non-linear decrease in the percentage of fleshy macroalgal cover with increasing density of D. antillarum was observed. We therefore propose D. antillarum as a key herbivorous species, which plays an important role in determining the structure of shallow, hard-substratum, infralittoral benthic communities throughout the Canary Islands.
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In 1998 and 1999, we carried out a systematic survey of the Osprey (Pandion haliaetus) in the Cape Verde Islands, to evaluate its population and conservation status. Some poorly surveyed areas were revisited in the summer of 2001 to complete our status assessment. We found an estimated 72-81 pairs on the archipelago, of which 94% were concentrated in the northern Barlavento (windward) islands group. In this area the species is common and seems to be recovering from a presumed decline, probably caused by a long-term overharvesting of eggs and nestlings by humans during past decades. On the contrary, in the southern Sotavento (leeward) islands the species is currently scarce, seemingly still on the decline and already extirpated in the southwesternmost islands. The high percentage of abandoned near-shore nests in the eastern ''flat'' islands is probably associated with the increasing tourism activities. ESTADO ACTUAL DEL A ´ GUILA PESCADORA PANDION HALIAETUS EN LAS ISLAS DE CABO VERDE RESUMEN.-Durante el año 1998 y la primavera de 1999 se hizo una prospección sistemática del a ´guila pescadora (Pandion haliaetus) en las islas de Cabo Verde con la intención de actualizar la información sobre su estado poblacional y de conservación. Algunas a ´reas peor prospectadas fueran visitadas en el verano de 2001 para confirmar datos anteriores. Se obtuvo como estimación más probable el nú mero de 72-81 parejas reproductoras en todo el archipiélago, largamente (94%) concentradas en el grupo de islas septentrionales del Barlavento. En este a ´rea, la especie es bastante común y parece estar recu-perándose de un presunto declive durante las décadas pasadas, como resultado probable de un contínuo expolio de huevos y pollos para la alimentación humana. Al contrario, en las islas del grupo sureño del Sotavento, la especie es actualmente muy escasa y sigue aparentemente en declive y incluso ya extinguida en las islas del extremo suroccidental. El incremento del turismo costero constituye una amenaza adi-cional para los nú cleos poblacionales de las islas ''llanas'' orientales al echar la especie de sus sitios vulnerables de nidificación costera, como lo indica el alto porcentaje de nidos abandonados a lo largo del litoral. [Traducción de los autores]
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The first successful breeding attempt of an Osprey, Pandion halieatus, in contnental France since several decades, occurred in 1985 in the Orleans Forest, 90 km south of Paris. The population has grown steadily to 6 pairs in 1997 and an additional pair is now breeding 65 km SW of the nearest site in the Orleans Forest. The overall breeding success was 1.20-1.83 fledgling/pair/year and 2.26 per successful pair. Fishing occurred both on forest ponds and on River Loire. Nests were built in old pine forest stands, 4.5-16 km from the river and 30-800 m from the nearest pond. The first breeders arrived in early March and laid eggs between 1-15 April. Fledglings dispersed away from nest after 15 August. Foraging trips were usually 8-25 km long and foraging ranges extended over 40-180 km2. Most prey were Cyprinid fishes. The mean number of fishes brought daily to nest (100% by male) increased from 1.3 during incubation to 4.15 in the late fledging period. From 1995 to 1997, 28 fledglings were banded but none of them has yet been resighted. Three banded breeding adults in 1997 had been ringed as nestlings in Eastern Germany in 1988-92. The population is now expected to expand in France and new pairs are settling as far as Lorraine. Conservation measures are suggested for the management and growth of the French population of breeding Ospreys.
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We examined the diet of nesting Ospreys (Pandion haliaetus) along the Naskaupi River in Labrador during 1995 and 1996. Observations of Ospreys feeding on identifiable prey species provided an indication of available food supply and summer diet for this population. Mammals and birds may constitute important food sources. Prey consumption dropped from 7.5% and 5.0% for mammals and birds, respectively, in 1995 to 0% in 1996, coinciding with a regional crash in the small mammal population. Inclement weather during 1996 also may have been a factor in lowering productivity.
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