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ORIGINAL PAPER
Bearded vultures (Gypaetus barbatus) prefer fatty bones
Antoni Margalida
Received: 8 April 2008 / Revised: 18 August 2008 / Accepted: 18 August 2008 / Published online: 6 September 2008
#Springer-Verlag 2008
Abstract In animal species, prey processing and the
provisioning of nutrients are subject to several constraints
related with finding, ingesting and processing food. In most
bird species, these constraints are obvious as a consequence
of food morphology. In the case of the bearded vulture
(Gypaetus barbatus), in comparison with other species, its
behavioural and physiological adaptations apparently allow
this vulture to ingest bone remains irrespective of their
morphology. Here, by comparing bones delivered to the
nest to be consumed (selected) and remains found at an
experimental feeding station and at bone-breaking sites or
ossuaries (rejected), I tested whether bearded vultures are
capable of choosing from among the various anatomical
parts of an animal carcass in relation to their fatty acid
content (nutrient concentration hypothesis), their size
(width-reduction hypothesis) or both. The results suggest
that bearded vultures prefer the fatty anatomical parts (with
a high percentage of oleic acid) of an animal carcass
regardless of bone length, although bone morphology as a
consequence of handling efficiency or the ingestion process
may also play a secondary role in food selection. The close
association between the bones selected and their high fat
value implies an optimisation of foraging time and of the
increased energy gained from the food. This is in line with
selective foraging to redress specific nutritional imbalances
(nutrient concentration hypothesis) and, secondarily, the
width-reduction hypothesis.
Keywords Bone .Feeding preferences .Foraging theory .
Gypaetus barbatus .Nutrient concentration .
Width-reduction
Introduction
In the optimal foraging theory, the energy nutrient intake
has been used as a surrogate for fitness, although several
studies have found little support for such a relationship
when fitness and energy intake maximisation are subject to
constraint (Illius et al. 2002).
Although vertebrate carnivores optimise the rate of prey
capture rather than the nutritional balance of their prey
(Stephens and Krebs 1986), herbivores and omnivores
adjust their food selection behaviour to regulate the intake
of multiple nutrients (Raubenheimer and Simpson 1997;
Berthound and Seely 2000). Invertebrate predators can also
forage selectively for potential lipids in order to redress
specific nutritional imbalances (Mayntz et al. 2005). In bird
species, the costs and benefits of foraging behaviour differ
when an individual ingests all the acquired food or when
the resources are delivered to a mate, catch-site or to
offspring (Ydenberg 1988). The costs associated with
feeding are activities of food acquisition and the mainte-
nance of the energy reserve once secured (Cuthill and
Houston 1998). Prey processing allows to prepare food in
ingestible portions, and to remove inedible parts that could
hinder digestion, waste energy or affect the forager through
toxicity or mechanical damage to the digestive tract to be
removed (Davies 1977; Kaspari 1991). In central-place
foragers obliged to transport a prey item rather than
consume it at the place of capture, another benefit is the
removal of excess mass, reducing the costs involved in
carrying the prey (Ydenberg 1988).
Behav Ecol Sociobiol (2008) 63:187–193
DOI 10.1007/s00265-008-0649-6
Communicated by E. Korpimäki.
A. Margalida (*)
Bearded Vulture Study and Protection Group,
Apdo. 43,
E-25520 El Pont de Suert, Lleida, Spain
e-mail: margalida@inf.entorno.es
Prey handling and the provisioning of nutrients are
subject to several constraints associated with the finding,
ingesting and processing of food (Schoener 1971;
Kaspari 1991). However, for bearded vultures (Gypaetus
barbatus; Accipitridae), the use of bone-breaking sites or
ossuaries to prepare their specialised food (Margalida and
Bertran 2001), and the high concentration of acid-
secreting cells in their stomach allow them to ingest and
digest bones repeatedly within a 24-h period (Houston and
Copsey 1994). Unlike other vultures, this species carries
prey remains to the nest in its feet and bill and does not
feed its young by regurgitation (Brown and Plug 1990;
Margalida and Bertran 2000a).Theadaptivebehavioural
and physiological differences with respect to other species
suggest that the morphology, preparation and ingestion of
bones cannot be considered as important constraints for
bearded vultures. Recently, the study of remains found in
ossuaries suggested an alternative explanation to bone
storage, related to a possible rejection of some bone
remains as a consequence of their low nutritive value
(Margalida 2008). Nevertheless, in this study, it was
suggested that the time and energy spent on their
preparation (handling efficiency) may also play a second-
ary role in food selection. Two hypotheses that are not
mutually exclusive may explain the selection of bone
remains in the bearded vulture. According to the width-
reduction hypothesis, prey preparation increases the ability
to swallow prey. In addition, the nutrient concentration
hypothesis posits that the removal of parts of prey
maximises the rate at which nutrients are concentrated in
the remaining food (Kaspari 1991). I hypothesise that if a
nutritive selection of bones exists (bone-nutritive selec-
tion) in the bearded vulture, remains present in ossuaries
and feeding stations should be the bones with the lowest
fat content. On the contrary, bones selected to be delivered
(and consumed) to the nest should be those with highest
fat content. On the other hand, according to the width-
reduction hypothesis, if anatomical parts are selected
according to their size (bone-morphology hypothesis),
remains present in ossuaries and feeding stations (not
selected) should be the largest. On the contrary, bones
selected to be consumed (i.e. delivered to the nest) should
be small.
Here, by comparing bones (i.e. anatomical parts selected)
delivered to the nest to be consumed of a medium-sized
ungulate (sheep Ovis aries, considered the ideal prey item)
and remains found in an experimental feeding station and
ossuaries (i.e. anatomical parts rejected), I test whether
bone selection among the various anatomical parts of an
animal carcass may be explained by their fat content
(nutritive value), their size (morphological selection) or
both.
Materials and methods
The study species
The bearded vulture is a long-lived territorial vulture with a
wingspan of 255–270 cm and a weight of 4–6 kg (Hiraldo
et al. 1979; personal observation). This species nests on
rocky cliffs and territorial adults’have main foraging areas
of 250–700 km
2
(Brown 1988, Margalida, unpublished
data) although home ranges may reach 7,468 km
2
(Brown
1988).
Clutch size is usually two eggs, but only one chick
survives as a consequence of sibling aggression (Margalida
et al. 2004). In monogamous pairs, both sexes invest
equally in rearing the offspring, although males take a more
active part in nest building and territorial defence, while
tending the nest is more pronounced in females (Margalida
and Bertran 2000a,b; Margalida and Bertran 2005). This
species is the only vertebrate with a bone-dominated diet
that can ingests bones up to 280 mm long and 40 mm wide
without difficulty. The bearded vulture resolves the problem
of ingesting large bones by the use of bone-breaking sites
or ossuaries. These sites are rocky surfaces where the birds
throw the remains from the air until they become sufficiently
fragmented or disjointed to be swallowed (Boudoint 1976;
Margalida and Bertran 2001). Unlike other vultures, this
species carries prey remains to the nest in its feet and bill
and does not feed its young by regurgitation (Brown and
Plug 1990; Margalida and Bertran 2000a). Its diet is
based on mammals (93%), birds (6%) and reptiles (1%;
Margalida et al. 2009). Medium-sized mammals constitute
61% of their diet. The bearded vulture’s diet seems to be
based mainly on the bones of wild and domestic ungulates
(Margalida et al. 2007,2009). The bones have a mean
water content of 32% and dry bone weight was made up of
54% mineral content and 46% organic content (Houston
and Copsey 1994). Due to their high fat content, mammal
bones have a higher energy content than muscle tissue (6.7
vs 5.8 kJ/g respectively, Brown 1988).
Study area, data collection and observation methods
The study was carried out in the Pyrenees (NE Spain).
Between October 2003 and May 2004, I placed 39 sheep
carcasses in an experimental feeding station. I observed the
abandoned bone remains consumed by other scavenger
species such as Eurasian griffon vultures (Gyps fulvus),
Egyptian vultures (Neophron percnopterus) and common
ravens (Corvus corax). Because bones can remain un-
touched for several months and bearded vultures may select
old bones as a consequence of the low water content and of
how easy they are to digest (Brown and Plug 1990), I
188 Behav Ecol Sociobiol (2008) 63:187–193
collected bones 30 months after their consumption by
vultures in October 2006. Carrion consumed by Eurasian
griffon vultures and other scavenger species allows the
bearded vulture (breeding and non-breeding population) to
take different anatomical parts without apparent difficulty
(and sometimes the entire carcass is brought to the
ossuaries where the bones are selected afterwards). I
estimated the proportion of bones found in relation to the
expected number (e.g., two scapulas and one skull is
expected from each sheep) in order to standardise the data.
As a second source of bone selection, I considered that the
bones present in the ossuaries were those rejected by
bearded vultures. Between 1994 and 2000, samples from
ten bone-breaking sites (n=5 pairs) were collected after
breeding. Each pair uses one or two ossuaries regularly
despite having various ossuaries available to them in the
territory (Margalida and Bertran 2001). As bone splinters
were difficult to identify and occasionally ingested by
Eurasian griffon vultures as a source of calcium (Bertran
and Margalida 1997) or by other species such as carnivores
(personal observation), only bone remains >5 cm were
taken into consideration (see Margalida 2008). To avoid
biases related with the overestimation of large bones
remains, the minimum number of individuals present for
each prey item was calculated (Poplin 1976). After deter-
mining bone characteristics at the feeding station and bone-
breaking sites between 2000 and 2006, we video-monitored
12 breeding attempts (although data were available for six
different pairs due to breeding failures or image interrup-
tion, Margalida et al. 2006) to document the diet of bearded
vultures as a measure of selected bone-types.
Data obtained in bone-breaking sites (1994–2000) and
prey items delivered to the nest observed (2000–2006) were
not paired, because the pairs studied were different. Thus,
the two sample sources analysed are independent, avoiding
the possibility that remains present in the ossuaries were
also brought to the nest.
To test whether bearded vultures choose the most
nutritive/fatty bones, I compared the percentage of oleic
acid that each bone contains (see white columns of Fig. 1)
with the proportion of sheep bones available at a feeding
station, at ten bone-breaking sites and brought to six nests.
As quantitative analyses of bone tissue from different
anatomical parts of sheep showed differences in the
percentage of oleic acid (white bone grease content), I
used this grease index value as a measurement of its
nutritive content (see Binford 1978). Bone grease is the
term used for the fat and grease contained in the bone
tissue itself (Binford 1978). To do this, the Binford (1978)
calculations were used for skeletal elements of a 90-month-
old sheep in which samples of tissue were extracted from
the cancellous zone and a quantitative analysis was
performed also analysing bone-marrow samples. The
analysis was reported as the percentage of oleic acid in
the sample’s total fat content. In the Pyrenees, sheep may
constitute >50% of their diet. I selected the 12 most
representative bones that form the sheep’s skeleton and
those that were observed in their diet, to compare bone
selection with the proportion of oleic acid the bones
contain. Because there are differences between the fat
content in distal and proximal parts of long bones, I
calculated the average of each large bone summing two
proportions of the distal part and the proximal divided by
three. For example, the grease value of a proximal humerus
is 39% and for a distal humerus 40% (Binford 1978), thus I
used 39.7% as the average value. In the case of the vertebral
column, I had to also calculate an average value due to the
differences in oleic acid contents. For this item, because it
was considered as a unit and values are similar (34% for
lumbar, 29% for cervical and 34% for thoracic vertebrae) the
average of the three values (32.33%) was considered as the
total value. In the case of bones delivered to the nest, because
bearded vultures may select specific items among the
different remains, each bone item was considered as an
independent sample. Thus, a posterior extremity delivered to
the nest was considered as two independent items: the
average of the three phalanges (77.67% of oleic acid because
the first phalange contains 79%, the second 80% and the
third 74%) and one tarsal (73%).
On the other hand, I measured the maximum length and
width of each anatomical part hypothesising that if size is
an important factor for bone selection (bone-morphology
hypothesis), larger bones (with respect to their length and
width) should be present in ossuaries and feeding stations
and, on the contrary, small bones should be selected and
delivered to the nests. As length and width measures were
strongly correlated (r
s
=0.77, P=0.0017, n= 12), and
yielded qualitatively similar results in the analyses, only
length results are presented. The lengths of bone remains
found in the feeding station were measured and, in addition,
biometric data were obtained in the literature (Gállego et al.
1992).
Statistical analyses
The means of means for bone remains found and observed
at each bone-breaking site and nest, respectively, from each
territory were used as a sample unit to avoid pseudorepli-
cation problems. The Spearman rank correlation coefficient
was used to test the relationship between the proportion of
rejected bone-types (i.e. found at ossuaries and at the
feeding station) or of selected bone-types (i.e. delivered to
nests) and their oleic acid content. Partial correlation values
taking into account bone length were calculated in
Behav Ecol Sociobiol (2008) 63:187–193 189
accordance with Sokal and Rohlf (1995) to discard the
effect of bone morphology in the selection of different
anatomical parts. Afterwards, observed frequencies of the
four main categories selected (tibia, tarsal, metacarpal/
metatarsal and phalanges) or avoided (skull, mandible,
scapula and vertebrae) were compared with Chi-square
contingency tables (Sokal and Rohlf 1995). To implement
this test avoiding pseudoreplication problems, before, I
tested whether interterritorial differences among the four
categories existed (each collection of bones obtained in
ossuaries and prey items delivered to the nest from a
territory was considered as a sample unit). Because no
significant differences were found among samples obtained
from the nests and from the ossuaries (chi-square P>0.05
for all of the samples considered), data was pooled.
Results
Between October 2003 and May 2004, I placed 39 sheep
carcasses at the feeding station and collected the bones that
were not consumed 2.5 years later. The proportion of
skeletal parts found (n=189) and hence not selected by
bearded vultures was significantly and negatively correlated
with the oleic acid content (r
s
=−0.86, P=0.00016, n=12;
Fig. 1a). Partial correlation between the skeletal parts found
and the percentage of oleic acid content, while controlling
for the length of the bones was also significant (r
s
=−0.76,
P=0.002, n=12). However, there was a negative relation-
ship between bone size and oleic acid content (r
s
=−0.67,
P=0.0085, n=12), suggesting that small (length) bones
have more fatty acid content.
As some bones may be removed from the feeding station
by other species such as mammals, the second source of
evidence to demonstrate that bearded vultures choose the
most nutritive bones was provided by the remains (n= 95)
found in bone-breaking sites (n= 10). These sites are rocky
surfaces where bearded vultures deliberately and repeatedly
drop remains from the air until they become fragmented or
disjointed. The negative and significant relationship (r
s
=
−0.75, P=0.0025, n=12) of bone remains found with the
percentage of oleic acid, suggests again a reluctance by the
bearded vulture to eat bones with low fat content (Fig. 1b).
Partial correlation between skeletal parts found and the
percentage of oleic acid content, while controlling for the
length of the bones, was also statistically significant (r
s
=
−0.53, P=0.05, n=12).
I confirmed fatty bone selection by bearded vultures by
installing micro-cameras in nests. Of the bone remains (n=
544) delivered to nests (n=6), bearded vultures positively
and significantly selected the bones with the highest fat
content (r
s
=0.64, P=0.012, n=12; Fig. 1c). Partial corre-
lation between skeletal parts observed delivered to the nest
and the percentage of oleic acid content, while controlling
for the length of the bones was also significant (r
s
=0.66,
P=0.0097, n=12).
The four most abundant bones found at bone-breaking
sites (skull, mandible, scapula and vertebrae), which
accounted for 65.9% of the sample, were less nutritious
and differed significantly from the proportion of the same
bones brought to the nest (χ
2
=13.73, df=3, P=0.003). On
the contrary, the four most abundant bones brought to the
nest (tibia, tarsal, metacarpal/metatarsal and phalanges),
which accounted for 86.8% of the sample, were the most
nutritious and differed significantly from the proportion of
0
20
40
60
80
100
Feeding station (%)
a
0
20
40
60
80
100
Bone breaking sites (%)
b
0
20
40
60
80
100
Nests (%)
c
Skull
Tarsals
Tibia
Radio-cubitus
Femur
Humerus
Pelvis
Vertebrae
Scapula
Mandible
Phalanges
Metacarpal/metatarsal
Fig. 1 a Proportion of the anatomical parts found in the feeding
station with respect to the number of bones remaining as a percentage
of those initially available. bPercentage (±1 s.d.) of bone remains
found in bone-breaking sites. cPercentage (±1 s.d.) of bone remains
brought to the nest. White bars show the percentage of oleic acid that
each fresh bone contains (Binford 1978)
190 Behav Ecol Sociobiol (2008) 63:187–193
the same bones found at bone-breaking sites (χ
2
=53.95,
df=3, P<0.0001).
Discussion
This is the first examination of the bearded vulture’s
preferred feeding habits which takes into account the
anatomical part selection of remains of a medium-sized
ungulate (sheep), which is considered to be the most
suitable prey to be swallowed by this species (Margalida
et al. 2007,2009). The results reveal a close association
between selected bone-types and their nutritive value (fat
content) regardless of bone size, although handling effi-
ciency may also play a secondary role in this selection. In
this respect, bearded vultures positively select bone
remains of medium-sized ungulates (Brown and Plug
1990; Margalida et al. 2009). Skeletal parts of larger
species (e.g., Bos taurus,Equus caballus) are probably
discarded as a consequence of the costs of transporting (to
the nest or ossuaries) and handling efficiency. In addition,
temporal variation in food quality during the chick-rearing
period seems to occur (Margalida and Bertran 2001) and
this is related to the chick’s limited ingestive capacity
during the first month. Thus, among the bone remains
selected to be delivered to the nest, meat content (for
example in the skulls) may also influence this selection.
Although ossuaries are also used to store food, being a
differentiating and advantageous trait with respect to
feeding behaviour developed by other meat scavengers
(Margalida and Bertran 2001), the results suggest a
negative relationship between bone remains present and
their nutritive content regardless of bone morphology.
These results coincide with the analyses carried out at
ossuaries considering all mammal remains and 31 different
anatomical parts studied, suggesting that the presence of
bones in ossuaries may be explained by a nutritive rejection
rather than storage function (Margalida 2008).
The bearded vulture is a central-place forager that
inhabits mountainous regions with low temperatures, which
increases basal metabolic expenditure. Their diet, based on
spatio-temporally unpredictable bone remains, implies costs
associated with the time and effort involved in searching for
food with apparently negligible nutritional content. Never-
theless, for every 100 g of bone, this species would absorb
387 kJ compared to 440 kJ on a purely meat-based diet,
suggesting that a bone-based diet (due to its high fat
content) is energetically almost as valuable as a meat-based
diet (Houston and Copsey 1994). Thus, processing and
selecting a food item before bringing it to the nest optimises
foraging time and increases the amount of energy gained
from the food. So, as has been suggested in other species
(Mayntz et al. 2005), bearded vultures forage to gain a
balanced nutrient intake, rather than maximising the energy
intake subject to constraints (Simpson and Raubenheimer
2001; Simpson et al. 1994). In this respect, the diversity of
prey items delivered to the nest in this species (e.g., small
mammals, micromammals, birds, reptiles, see Thibault et
al. 1993, Margalida et al. 2009) supports this prediction. In
addition, given that there is a risk of kleptoparasitism by
conspecifics and heterospecifics that visit feeding stations
and ossuaries (Margalida and Bertran 2003), prey prepara-
tion and the selection of the more fatty remains would
influence the transport costs and decisions of central-place
foragers (Cuthill and Kacelnik 1990; Rands et al. 2000),
reducing the costs that this food strategy implies.
This is in line with the idea of selective foraging aimed
at redressing specific nutritional imbalances through ex-
traction of specific nutrients from a single prey item
(Manytz et al. 2005). It also supports the nutrient con-
centration hypothesis, which posits that partial prey
removal maximises the rate at which nutrients are concen-
trated in the remaining prey (Sherry and McDade 1982;
Kaspari 1991). However, the existence of a negative
relationship between bone size and fatty acid content make
it hard to interpret the relations between these variables and
the selection. In this sense, although bone morphology may
also explain feeding preferences, the adaptive behavioural
(use of ossuaries) and physiological characteristics of this
species suggest that the ingestion of bones cannot be
considered as important constraints. Thus, the width-
reduction hypothesis probably plays a secondary role in
food selection.
Finally, it seems necessary to point out that the results
are conservative and the selection of nutritious bones is
probably much stronger than the results obtained. This is
due to two factors: firstly, if carnivorous or other birds take
bones from the feeding place it is reasonable to assume that
Fig. 2 Bearded vulture choice a leg of sheep in a feeding station of
the Spanish Pyrenees (© Antoni Margalida)
Behav Ecol Sociobiol (2008) 63:187–193 191
these bones will be the most nutritive. For this reason, the
availability of fatty bones for the bearded vulture would be
less than is supposed. Secondly, some of the nutritive bones
found in ossuaries may be consumed by bearded vultures
after the visits to collect samples.
These results have interesting conservation applications
for the management of wild and captive populations of this
threatened species, showing the significance of behavioural
ecology for conservation biology (Caro 1998). The estab-
lishment of supplementary feeding points (Fig. 2) for the
management of bearded vulture populations has been used
in the Pyrenees (Heredia 1991) and Southern Africa
(Brown 1990). However, these conservation measures have
been undertaken without any previous analysis regarding
the potential differences in the nutritive quality of the
food. Because the conservation efforts for the population
dynamics of bearded vultures should facilitate the geo-
graphic expansion (Margalida et al. 2008), the management
of feeding stations could facilitate the dispersion of non-
breeding individuals increasing the value of demographic
parameters (Carrete et al. 2006) and favouring the mainte-
nance of a metapopulation structure. In the future, supple-
mentary feeding programmes to increase breeding success
and facilitate geographic expansion could be optimised,
with the most nutritive bones being delivered. In this
respect, anatomical parts as tibias, tarsals, and extremities
seem to be the most appropriate for the species.
Acknowledgments I thank Gary R. Bortolotti, José A. Donázar,
Fabrizio Sergio and an anonymous reviewer for discussions and
critical reading of the manuscript. I thank Joan Bertran, Diego García
and Rafael Heredia for their help during field work and Sheila Hardie
for the review of the English. I acknowledge Departament de Medi
Ambient i Habitatge of Generalitat de Catalunya and Dirección
General del Medio Natural of Ministerio de Medio Ambiente for
financial support.
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