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ORIGINAL ARTICLE
The flight feather moult pattern of the bearded vulture
(Gypaetus barbatus)
In
˜
igo Zuberogoitia
1
•
Juan Antonio Gil
2
•
Jose
´
Enrique Martı
´
nez
3
•
Birgit Erni
4
•
Bakartxo Aniz
5
•
Pascual Lo
´
pez-Lo
´
pez
6
Received: 27 February 2015 / Revised: 15 June 2015 / Accepted: 29 June 2015 / Published online: 14 July 2015
Ó Dt. Ornithologen-Gesellschaft e.V. 2015
Abstract Moult is an extremely time-consum ing and
energy-demanding task for large birds. In addition, there is
a trade-off between the time devoted to moulting and that
invested in other activities such as breeding and/or territory
exploration. Moreover, it takes a long time to grow a long
feather in large birds, and large birds that need to fly while
moulting cannot tolerate large gaps in the wing, but only
one or two simultaneously growing feathers. As a conse-
quence, large birds take several years to complete a full
moult cycle, and they resume the moult process during
suboptimal conditions. A clear example of this pattern is
the Bearded Vulture (Gypaetus barbatus), which needs
2–3 years for changing all flight feathers. Here we describe
the sequence, extent, and timing of moult of 124 Bearded
Vultures in detail for the first time. We found that extent
and timing of flight feather moult was different between
age classes. Subadults (from 3rd to 5th calendar year)
started moult, on average, in early March, whereas adults
only started moult, on average, in late April, possibly due
to breeding requirements. Second calendar year individuals
delayed onset of moult until the middle of May. In general,
the moult lasted until November, and although adults
started to moult later than subadults, they moulted more
feathers. Subadults needed 3 years for moulting all flight
feathers, whereas adults normally completed it in 2 year s.
Keywords Bearded Vulture Gypaetus barbatus Moult
sequence Underhill–Zucchini model
Zusammenfassung
Die Flugfedermauser beim Bartgeier
Die Mauser ist ein extrem zeit- und energieaufwa
¨
ndiger
Vorgang fu
¨
r große Vo
¨
gel. Daru
¨
ber hinaus gibt es einen
Konflikt zwischen der Zeit, die fu
¨
r die Mauser aufgebracht
wird und derjenigen, die in ander e Aktivita
¨
ten investiert
werden kann, so wie Bru
¨
ten oder territoriale Exploration.
Außerdem braucht das Wachstum einer langen Feder bei
großen Vo
¨
geln lange; und große Vo
¨
gel, die darauf ange-
wiesen sind wa
¨
hrend der Mauser zu fliegen, ko
¨
nnen sich
keine gro
¨
ßeren Lu
¨
cken in den Flu
¨
geln leisten, sondern nur
ein oder zwei gleichzeitig nachwachsende Federn. Als
Konsequenz braucht es mehrere Jahre, bis große Vo
¨
gel
einen vollen Mauserzyklus vollendet haben, und sie neh-
men die Mauser unter suboptimalen Bedingungen wieder
auf. Ein deutliches Beispiel fu
¨
r dieses Muster ist der
Bartgeier (Gypaetus barbatus), der zwei bis drei Jahre
braucht fu
¨
r einen kompletten Wechsel sei ner Flugfedern.
Hier beschreiben wir zum ersten Mal im Detail die
Abfolge, das Ausmaß und das Timing der Mauser von 124
Bartgeiern. Wir fanden, dass Ausmaß und Timing der
Communicated by F. Bairlein.
& In
˜
igo Zuberogoitia
zuberogoitia@icarus.es
1
Estudios Medioambientales Icarus S.L. C/San Vicente, 8. 6
a
Planta, Dpto 8, Edificio Albia I, 48001 Bilbao, Bizkaia, Spain
2
Fundacio
´
n para la Conservacio
´
n del Quebrantahuesos, Plaza
San Pedro Nolasco 1, 4u F, 50001 Zaragoza, Spain
3
Bonelli
´
s Eagle Study and Conservation Group, Apdo,
4009, 30080 Murcia, Spain
4
Department of Statistical Sciences, Centre for Statistics in
Ecology, Environment and Conservation, University of Cape
Town, Rondebosch 7701, South Africa
5
Pl Dra Juana Garcı
´
a Orcoyen 5, 31012 Pamplona, Spain
6
Vertebrates Zoology Research Group, University of Alicante,
Apdo. 99, 03080 Alicante, Spain
123
J Ornithol (2016) 157:209–217
DOI 10.1007/s10336-015-1269-3
Flugfedermauser sich zwischen Altersklassen unterschied.
Subadulte (vom dritten bis fu
¨
nften Kalenderjahr) begannen
die Mauser, im Durchschnitt, im fru
¨
hen Ma
¨
rz, wa
¨
hrend die
Mauser der Adulten im Durchschnitt erst im spa
¨
ten April
begann, mo
¨
glicherweise aufgrund von Zwa
¨
ngen im
Zusammenhang mit der Brut. Individuen im zweiten
Kalenderjahr verzo
¨
gerten den Beginn der Mauser bis Mitte
Mai. Generell dauerte die Mauser bis November, und
obwohl Adulte mit der Mauser spa
¨
ter begannen als Sub-
adulte, mauserten sie mehr Federn. Subadulte brauchten
drei Jahre zur Mauser sa
¨
mtlicher Flugfedern, wa
¨
hrend
dagegen Adulte normalerweise in zwei Jahren fertig waren.
Introduction
Large birds take a long time to complete a full cycle of life-
history stages. Normally, each stag e requires high amounts
of energy that determine mutual ly exclusive activities (e.g.
breeding, migration, and flight feather moult, Hedenstro
¨
m
2006). In birds, the time required to raise young increases
with body size (Calder 1984), leaving large birds with less
time in their annual cycle for other activities (Rohwer et al.
2011). In long-distance migrants, flight feather moult rarely
overlaps with breeding or migration, but some species start
moulting during the last part of the bree ding season and
stop before migration, resuming the moult in winter
grounds (Herremans 2000; Chandler et al. 2010), whereas
others only moult once in the wintering areas (Barshep
et al. 2013). In contrast, sedentary large species can extend
the time devoted to moult, but suspend moult in winter to
save energy, in order to survive during adverse weather
periods and to obtain enough reserves to start reproduction
early (Zuberogoitia et al. 2013a). Hence, the more time
spent rearing young, the less time for moult, and, recip-
rocally, a longer moult that clears worn feather s from the
wing may make breeding in the next season impossible
(Rohwer et al. 2011).
Non-breeding birds have more time available for
moulting. However, for immature birds, time devoted to
moult is constrained by their inexperience (a poor knowl-
edge of the home range and thus decreased feeding effi-
ciency). On the other hand, experienced breeders take
advantage of their better knowledge of the territory,
allowing them to obtain resources more efficiently than
young birds (Espie et al. 2000; Daunt et al. 2007;
Zuberogoitia et al. 2013b; Penteriani et al. 2013). Hence,
adults optimize time and resources and, as a result, they can
moult more flight feathers in a given moult period and
quicker than inexperienced birds (Dietz et al. 2013;
Zuberogoitia et al. 2013a).
In some of the biggest flying birds, such as vultures,
condors, storks, and albatrosses, each moult cycle las ts
more than a year, but may be interrupted during difficult
periods, such as chick rearing, migration, or times of food
shortage, such as midwinter in high latitudes or during
extended droughts (Mundy 1982; Edelstam 1984; Clark
2004; Newton 2009). The moulting process places addi-
tional energy demands on birds (Hemborg and Lundberg
1998) in order to: (1) produce replacement plumage; (2)
regulate body temperature while feather insulation is
reduced; and (3) maintain efficient flight despi te gaps in the
wing due to dropped or growing feathers (Ginn and Mel-
ville 2000).
Feather growth rate in large birds is not much higher
than in small birds, but because feathers are much longer, it
takes longer to grow a long feather. Rohwer et al. (2009)
suggest that feather growth rate does not increase propor-
tional to feather size, but is constrained by one-dimensional
follicle size. Moreover, many large birds that depend on
flight for feed ing during moult, shed only a part of their
flight feathers annually and require two, and sometimes
three, years to complete moult (Rohwer et al. 2009). They
cannot tolerate large gaps in the wing, but can only tolerate
one or two simultaneously growing feathers. The replace-
ment of two or three adjacent remiges in quick succession
can lea ve large gaps in the wings inhibiting flight, so most
of these species have evolved strategies in which remiges
at different locations are replaced at the same time, pro-
ducing multiple smaller gaps while maintaining the wing’s
surface integrity and the bird’s ability to fly (Pyle 2006).
Moult duration is mainly determined by the number of
simultaneously growing feathers (Rohwer and Rohwer
2013). This strategy for replacing remiges among large
birds is known as ‘‘stepwise’’ or ‘‘serial’’ moult, and it is
also called ‘‘Staffelmauser’’ (Stresemann and Stresemann
1966).
The Bearded Vulture, as other vultures, is a classic
example of a bird that has a serial/stepwise moult
(Staffelmauser; Houston 1975; Clark 2004; Zuberogoitia
et al. 2013a ). The moult pattern of the Bearded Vulture
(Gypaetus barbatus) has received little attention despite its
endangered status (see Margalida 2011). The species is
currently listed as ‘‘priority species’’ in the conservation
strategies of the European Union (Birds Directive, Anne x
I) and is listed as ‘‘endangered’’ in Spain (Antor et al.
2005). Hiraldo et al. (1979) documented a first approxi-
mation to the moult and later Adam and Llopis (2003)
described the flight feather moult in captive birds and in
free-ranging birds using photographs in flight. Later, Sese
´
(2011) published a summary of the moult pattern of
Bearded Vultures. Therefore, the aim of this paper is to
describe the moult pattern of the flight feathers of Bearded
210 J Ornithol (2016) 157:209–217
123
Vultures and analyse differences in the onset and duration
of moult between age groups.
Methods
A total of 153 Bearded Vultures of different ages [87
nestlings, 34 2nd calendar year (cy), 18 subadults, and 14
adults] and both sexes (86 males, 58 females, nine
unknown sex) were trapped, ringed, and tagged with wing-
tags from 1987 to 2014. Tags included an alphanumeric
code allowing individual identification at distance with
spotting scopes. This work took place as part of a long-term
conservation and research program conducted by FCQ
(‘‘Fundacio
´
n para la Conservacio
´
n del Quebrantahuesos’’
in Spanish) in the central Pyrenees (Gil et al. 2010, 2014).
The number of trapped Bearded Vultures was limited
due to the small population size of the species in the
Pyrenees (i.e. 105 breeding units in Spain in 2010, Mar-
galida 2011; Gil 2012). Moreover, the endangered status of
this bird restricted the time devoted to obtain a correct
moult pattern because we were not allowed to hold them
long enough to score the moult of all trapped birds. Out of
the 66 completed moult sheets, we used 24 in the analysis.
The rest were excluded because we could not validate their
moult sheets with adequate photos. Moul t scores from six
dead, marked birds of known age from wildlife rehabili-
tation centres were also obtained.
In addition, 94 moult cards were obtained from high
definition (HD) and high quality pictures of wild birds taken
by wildlife photographers (see Snyder et al. 1987, Fig. 1, see
acknowledgements for photo credits). We compared series
of photos of each individual and used individual marks in
order to improve information about the moult.
Summarizing, we used 124 complete moult sheets: 11
1st cy, 25 2nd cy, 21 3rd cy, 15 4th cy, 18 5th cy, and 34
adults.
Number of feathers
The birds in hand were inspected following a standardized
protocol by one trained researcher (JAG). All birds were
photographed, and these pictures and those of the other non-
handled birds were inspected by a second trained researcher
(IZ, see Zuberogoitia et al. 2013a). We recorded a moult card
for both wings of each individual, identifying feather gen-
eration by wear, shape, colour, age pattern, and growth of the
remiges (i.e. primaries and secondaries) and rectrices. This
gave us data for 10 primaries (PP) and 19–20 secondaries
(SS) for each wing, and 12 rectrices (RR). For the moult
analysis, we only included the first 16 SS because we
observed that not all individuals had the expected 20 SS
(Adam and Llopis 2003): in four dead Bearded Vultures (two
first calendar year birds and two adults) with no active moult
in winter, the two juven ile birds had 19 SS, whilst the adults
had 20 SS, confirmed by removing all feathers to count the
insertion marks of SS in the ulna (forewing bone; Cieslak and
Bolestaw 2006). These results suggest an individual differ-
ential number of SS, possib ly due to the lack of one of the
innermost SS. Primaries were numbered in descending order
(from inside to outside), SS were numbered in ascending
order (from outside to inside) and RR were numbered cen-
trifugally (from the central feathers outwards).
Moult score
Following Ginn and Melville (2000) and Newton (2009)
we followed a standard recording system according to the
stage of growth of primaries and secondaries: old feathers
were scored as 0, fully grown new ones as 5, and growing
ones as 1–4 for intermediate stages of feather development.
These individual moult scores were then summed to give
an overall moult score between 0 and 50 (for 10 PP) and 0
and 80 (for 16 SS). Following Zuberogoitia et al. (2013a),
feathers scored as 0 were also recorded as A (juvenile), K
(moulted in the previous moult season), M (moulted
2 years ago), and O (moulted 3 years ago).
The extent of the moult at different age stages
In order to determine the extent of the moult for each age
class, we used birds checked at the end of the year, with no
active moult (some from the last days of November and
December), from which we considered all the feathers
scoring as ‘‘5’’ and birds from the first months of the year
before the onset of the moult, considering all the feathers
scoring as ‘‘K’’.
Fig. 1 Example of HD picture from which a moult pattern can be
derived moult (picture by Bakartxo Aniz). This is a 4 cy bird recorded
on 18th November 2011. This bird had completed the moult of all the
flight feathers in 3 years. During 2011 it moulted P3, P4, P5, P9, and
P10 from both wings, S1, S4, S7-13 from the right wing, S1, S7-10,
S13-15 from the left wing and R3 and R5 from the tail feathers,
including R2 right, which was growing
J Ornithol (2016) 157:209–217 211
123
Symmetry
To calculate the symmetry of the moult process between
wings, we superimposed both wings and compared each
corresponding primary, secondary, and rectrix. We
assigned ‘‘1’’ when both feathers were at the same moult
level and ‘‘0’’ in those cases where the feathers were at a
different stage. We then summed up the scores of PP and
SS and calculated the perc entage of symmetry for the flight
feathers by comparing the sum to the total (see also
Zuberogoitia et al. 2005).
Timing of moult
We analysed timing of primary and secondary moult using
the models of Underhill and Zucchini (1988) and Underhill
et al. (1990), implemented in the ‘‘moult’’ package (Erni
et al. 2013) for R (R Core Team 2014). These models give
estimates of moult duration and average start date (from
which average end date can be calculated) and also the
standard deviation of the start date. Because the number of
feathers moulted in a season differed between individuals,
it was not possible to calculate the proportion of feather
mass grown (the moult index used in the Underhill–Zuc-
chini models) in the current season. For this reason we used
the moult data type 1 (Underhill and Zucchini 1988),
requiring only the information whether an individual has
not yet started, is in moult, or has completed moult, coded
as 0, 0.5, and 1, respectively, only using the current year’s
moulting feathers for analyses. We used Julian day (Jan-
uary 1 = 1) as time scale in the analyses and graphs. We
classified individuals into three age groups: (1) Second cy:
birds in the second calendar year (cy) during their first
moulting season; (2) subadults: birds from 3cy to 5cy that
are still non-breeders (Lo
´
pez-Lo
´
pez et al. 2013); and (3)
adults: birds from 6cy onwards with adult plumage (Sese
´
2011). Differences in start and duration of moult were
expected between the age groups. This was tested by
including age as a covariate on start and duration.
We ran three sets of models to estimate timing of moult
in PP, SS, and PP and SS combined. We compared models
using AIC, assuming models within two AIC units of the
best model to have similar support as the best model
(Burnham and Anderson 2002).
Results
Modelling start and duration of moult
According to Underhill and Zucchini’s Models, the best
model for PP and PP&SS was M5 (Table 1). Models
improved when ‘‘age’’ was considered as covariate. Start of
moult and standard deviation in start clearly differed
between age classes, and possibly duration differed
between ages when considering PP and SS combined
(model M4 was wi thin two units of AIC of the best model
M5). Most 2nd cy did not moult secondaries (Fig. 2).
Therefore, for secondaries, we fitted the moult models to
data including 2nd cy and then excluding 2nd cy.
Excluding 2nd cy, the null model was within two AIC units
of the best model (M2), showing that start and duration of
moult of SS did not clearly differ between subadults and
adults, although adults moult ed on average more SS than
subadults (Fig. 2).
Estimated average start of moult for subadult Bearded
Vultures was 3rd of March [Table 2 (PP&SS); Fig. 3],
whereas adults started on average on 26th of April. Second
cy birds delayed onset of moult until the 10th of May. The
duration of moult also differed between age groups. The
moult of PP finished before the SS (Table 2). In general,
the moult lasted until November (Fig. 3). Subadults had the
longest moult period (8 months) whilst 2nd cy were
moulting on average over a period of 6 months (Table 2).
Moult pattern
Second calendar year (2cy)
Bearded Vultures started moulting in their second cy. We
did not find evidence of flight-feather moult in any of the
11 first cy Bearded Vultures analysed between the fledging
season and the end of the year. There was no evidence of
moult in 2cy Bearded Vultures before May (n = 6), and
50 % of the analysed birds in May (n = 6) and 100 % of
birds in June (n = 5) had just dropped the P1. From then
until December, 2cy Bearde d Vultures moulted on average
4.32 inner primaries of each wing (SD = 1.25; range 3–6;
n = 25, Fig. 4). When the fourth primary was moulted, by
October, 2cy Bearded Vultures started to moult SS, nor-
mally S1, and rectrices, normally R1. Second cy Bearded
Vultures moulted on average only 0.58 SS (SD = 0.71;
range 0–2; n = 26, Fig. 4) of each wing and 0.56 RR
(SD = 0.71; range 0–3; n = 25) of each side of the tail.
The moulting process at this age showed a high degree of
symmetry (96.8 % in PP, 99.5 % in SS, and 96.67 % in
RR).
Third calendar year (3cy)
Bearded Vultures continued moulting PP, beginning
where they had left off in December of the previous
year, mainly P5, P6, and P7. We also detected 35 % of
birds beginning a new wave from P1. During the third
cy they replaced on average 3.75 PP of each wing
(SD = 0.97; range 2–5; n = 20). The moult of SS and
212 J Ornithol (2016) 157:209–217
123
RR started 2 or 3 weeks after start of primary moult.
During this period, 3cy birds moulted on average 5.78
SS (SD = 2.95; range 1–11; n = 19) and 2.55 RR of
each side of the tail (SD = 1.25, range 1–5, n = 18).
The moult of SS showed three foci: in S1, the starting
focus, which continued inwards in an orderly manner, in
S5 inwards, and in S15 towards both sides (Fig. 4).
These foci were observed in birds that showed the
neighbour feathers in sequential growing stages and
different birds showing the overlapping sequence (one
feather growing on the side of another new feather). Tail
feather moult als o showed different foci, starting in R1
outwards and following R6 inwards. We detected these
two foci in rectrices active at the same time in some
birds. The moulting process during the 3 cy still showed
a high degree of symmetry in PP (92.5 %), but sym-
metry was lower than in 2nd cy birds in SS (88.3 %)
and RR (82.5 %).
Table 1 Results of multi-
model evaluation applied to the
moult index of the Bearded
Vulture
Model Duration | start | SD Type K AIC PP AIC SS AIC SS* AIC PP&SS
M1 1 | 1 | 1 1 3 (2) 139.4 206.0 142.3 136.0
M2 Age | 1 | 1 1 5 (4) 142.1 208.1 141.5 138.2
M3 Age | Age | 1 1 7 (6) 139.9 168.6 143.4 137.7
M4 Age | Age | Age 1 9 (6) 136.9 171.2 144.2 132.6
M5 1 | Age | Age 1 7 (6) 134.2 169.0 144.0 132.0
M6 1 | 1 | Age 1 5 (4) 140.7 187.3 142.5 135.2
Model ranking was assessed by Akaike information criteria (AIC). The models were fitted to four data sets:
primaries (PP), secondaries (SS), secondaries without 2nd cy birds (SS*), and all remiges (PP&SS). The
best model is marked in bold. The number of parameters is different (in parentheses) for the model of SS*
SD standard deviation in start date, K number of parameters
Fig. 2 Box plots of total moult
scores for primaries and
secondaries per age category.
All sampled birds were
considered for performing this
plot
Table 2 Duration (days), start date, and standard deviation in start
date (days) estimates for each age class obtained from the M4 models
for primaries (PP) and primaries and secondaries (PP&SS)
Duration (SE) Start (SE) SD in start (SE)
M4 PP
2nd cy 166.4 (21.1) May 17th (10.1) 24.9 (16.3)
Subadults 184.7 (30.4) March 3rd (22.5) 80.6 (35.0)
Adults 143.0 (24.8) April 27th (18.8) 48.4 (23.3)
M4 PP&SS
2nd cy 184.2 (13.2) May 10th (6.3) 13.2 (10.1)
Subadults 239.0 (33.7) March 6th (22.3) 79.5 (36.8)
Adults 216.1 (39.9) April 26th (27.6) 76.5 (41.0)
SE standard error
Fig. 3 Observed moult index (0, not started; 0.5, actively moulting;
1, moult completed for season) for moult in primaries and secondaries
of Bearded Vultures versus date (Julian days). The lines represent
estimated moult trajectories of the three age classes obtained with
model M4, starting at the mean start date, ending at mean end date
J Ornithol (2016) 157:209–217 213
123
Fig. 4 Moult pattern of
Bearded Vultures. The pattern
shows the most frequently
moulted primaries and
secondaries in second, third,
fourth, and fifth calendar years.
The feathers moulted in the
current season are black, those
moulted in the previous year are
grey and those which have not
been moulted are white. Moult
foci and moult direction are
indicated by arrows
214 J Ornithol (2016) 157:209–217
123
Fourth calendar year (4cy)
On average, 3.95 PP (SD = 1.10; range 3–7; n = 20) of
each wing were moulted, completing the first moult cycle
(Fig. 4). During their fourth calendar year, Bearded Vul-
tures moulted on average 7.05 SS (SD = 2.01; range 3–10;
n = 19) and 2.5 RR of each side of the tail (SD = 0.95,
range 1–4, n = 20). The moult of SS followed the trajec-
tory from the three above-mentioned foci, although two
more foci may appear in S10 and S13. These new foci are a
continuation of the moult wave. The same occurred in the
tail feathers, filling the gaps and starting again. The
moulting process during the 4th cy was less symmetrical in
PP (89.3 %) than in the previous calendar year, but mainl y
in SS (60.6 %) and RR (60.3 %).
Fifth calendar year (5cy)
The moult followed where they had left off in winter of the
previous year. Some birds (44.4 %) completed the second
moult cycle of all P during this year, and all birds had
advanced the second moult of SS, mainly in the three first
foci (S1, S5, S15). In contrast, 29.4 % of the birds still had
juvenile SS (mainly S10, S11, and S12) in summer, at the
middle of the moulting season. On average, 4.44 PP
(SD = 0.88; range 3–6; n = 9), 7.11 SS (SD = 1.17;
range 6–9; n = 9), and 3 RR (SD = 0.71; range 2–4;
n = 9) were moulted in the fifth cy. The symmetry of
moult in PP (82.29 %) and SS (58.65 %) was similar to 4
cy birds, but less in RR (40.09 %).
Moult in adults
Adults moulted almost half of the flight feathers every
year. On average, 4.8 PP (SD = 0.79; range 4–6; n = 22),
8.2 SS (SD = 1.4; range 5–10; n = 22), and 2.7 RR
(SD = 0.48; range 2–3 ; n = 22) were moulted in adults.
Moult did not follow an evident pattern at this age because,
from the third moult onwards, the perc entage of PP, SS and
RR moulted (and consequently the start point of each
moult) varied considerably among individuals and even
between wings of the same bird. In fact, the symmetry
between wings was on average 77.7 % in PP, 50.6 % in SS,
and 52.3 % in RR.
Discussion
Bearded Vultures fledge between late June and early
August, and birds remain in their natal areas for the first
2 months after fledging, starting a post-fledging depen-
dence period close to the natal areas until the onset of
dispersal that coincides with the adult’s next breeding
season (Lo
´
pez-Lo
´
pez et al. 2014). During the following
months, they will wander over extensive areas, and they
must learn to become self-sufficient, acquire flight skills,
find food resources, and exploit them efficientl y. This
period is, therefore, critical for survival (Margalida et al.
2013; Gil et al. 2014;Lo
´
pez-Lo
´
pez et al. 2014). Possibly as
a consequence, we found that 2nd cy birds delayed start of
primary moult until late in May, and only few birds were
able to moult secondaries during the last month before the
end of the moulting season, in winter. During the second
calendar year, they only moulted on average four inner
primaries of each wing and rarely any secondaries. Possi-
bly, only birds that had enough energy or could start sooner
moulted the central pair of the tail feathers.
Feathers grown during the nestling period are of poorer
quality than those of grown-up birds (Ginn and Melville
2000), so the wear of the feathers may be more pronounced
until the individuals replace them. In the case of Bearded
Vultures, juvenile secondaries are significantly longer than
moulted ones, and these feather s show increasing degra-
dation from 2nd cy onwards, greatly contrasting with adult
feathers, which are of much better quality. During the
following years, birds should invest any surplus energy into
moult in order to improve plumage quality. Remaining
juvenile feathers are worn in the fourth calendar year.
Insofar as birds have moulted their plumage during their
first 4 cy, they will be in a better condition to overcome
winter. Subadults (3–5 cy) started moult in March, con-
siderably earlier than 2nd cy birds and adults, although
they showed high variability among individuals. As birds
gain experience they can mobilize more energy to moult
secondaries, increasing the percentage of secondaries
moulted with age, whereas the number of primaries
moulted per year remains the same or slightly increases
with age. We would expect that non-breeding birds moult
more feathers than breeders. The reduction in the number
of feathers moulted after breeding has been proposed to
reflect energy limitation due to reproductive activit y (Pi-
etia
¨
inen et al. 1984); however, we did not have data on
breeding status. In the case of subadults, foraging inexpe-
rience may be a limiting factor for the extent of moult.
The moult pattern of Bearded Vultures is char acterised
by the replacement of few flight feathers during the first
moult periods. Following the usual moult pattern in large
soaring raptors (i.e. moult waves; Edelstam 1984 ; Clar k
2004), the innermost primaries and neighbouring secon-
daries tend to be replaced more often than others (Houston
1975; Mundy 1982; Snyder et al. 1987; Pyle 2005;
Zuberogoitia et al. 2013a). In fact, our results (Fig. 4)
showed that before outer primaries or some secondaries of
the fourth and fifth foci (S10 and S13) were moulted for the
first time, bir ds had replaced inner primaries and secon-
daries for the second time. Langst on and Rohwer (1995)
J Ornithol (2016) 157:209–217 215
123
suggested that Laysan (Phoebastria immutabilis) and
Black-footed Albatrosses (Pygathrix nigripes) more often
replace those primaries that drag on the sand of the atolls
where the birds breed and become severely abraded. In the
same line, Brommer et al. (2003) showed that Ural Owls
(Strix uralensis) more often replace oute r primaries, sug-
gesting that the allocation of position-specific energetic
costs may benefit large birds. The moult pattern of subadult
Bearded Vultures reflects the importance of the good
maintenance of inner primaries and secon daries for soaring
and gliding.
Bearded Vultures reach definitive plumage in their 6th
calendar year (Sese
´
2011), approximately the same age at
which they start to establish a territory (Lo
´
pez-Lo
´
pez et al.
2014). This, in turn, reflects the importance of the rela-
tionship between the acquisition of definitive plumage, the
reach of sexual maturity and the settlement in a breeding
territory (Rohwer et al. 2011).
Adults started moult 1.5 months later than subadults,
possibly due to breeding requirements. The onset of moult
synchronizes with the presence of 1-month-old nestlings
(see Margalida et al. 2005). For example, Rohwer et al.
(2011) showed that the Black-footed Albatross’s moult is
so time-constrained by reproduction that some individuals
fail to replace all their flight feathers every 2 years. This
resulted in reduced breeding performance due to skipping
behaviour or breeding with worn feathers. Moult in birds
that overlap moult and breeding was found to be slow and
protracted (Foster 1975; Rohwer et al. 2009 ), confirming
the high cost of replaci ng flight feathers while breeding.
Most adults moulted all flight feathers in 2 year s. They
started a bit later than subadults, moulted more feathers,
but duration was almost the same. Our findings correspond
to those of Dietz et al. (2013) who showed that moult of
adult Red Knots (Calidris canutus) is seriously time-con-
strained by reproduction and that adults moult later but
faster than second calendar year birds.
Adult Bearded Vultures show a high degree of asym-
metry, mainly in secondaries and tail feathers. According
to Rohwer et al. (2011) and Zuberogoitia et al. (2013a)
some mechanism may enable them to replace feathers that
are damaged or unusually worn, regardless of the biennial
cycle. However, asymmetry appears to have negative
consequences for survival (Brommer et al. 2003). In
agreement with Brommer et al. (2003), asymmetry in pri-
maries, which are used for flight propulsion (Hickman et al.
1993), appears to be less than the asymmetry in secon-
daries, which are used for lift.
Acknowledgments This paper has been developed under the
agreement signed by the Foundation for the Conservation of the
Bearded Vulture (FCQ), Arago
´
n regional government and the Spanish
Ministry of Environment, under the actions of the Bearded Vulture
Recovery Plan in Arago
´
n and the Bearded Vulture Reintroduction
Program in Picos de Europa. We are indebted to the Departamento de
Agricultura, Ganaderı
´
a y Medio Ambiente (Arago
´
n regional gov-
ernment), European Union (LIFE 1998–2006, and INTERREG IIIA
2002–2006 programs), MIMAM (Spain), Guardia Civil (GREIM),
Arago
´
n Forest Rangers (APN), Wildlife Rehabilitation Centre at La
Alfranca (Zaragoza), LVFS, IREC-CSIC, EBD-CSIC, SEO/BirdLife,
‘‘Arago
´
n’’ Ringing Group, Trango, Zeiss and Land Rover. Thanks to J
Guiral, J Insausti and M. Alcantara. G. Gonza
´
lez, I. Otra, J. Serra, J.
Sa
´
nchez, J. Marti, S. Marcedos, J. Vecino, D. Forsman, for sharing
with us their picture collections of Bearded Vultures. L Palomares
helped us drawing the Fig. 4. Special thanks are due to all the
members of the FCQ and particularly to O Dı
´
ez, G Baguena, L
Lorente, R Antor, G Che
´
liz, JC Ascaso and JC Gonzalez. Two
anonymous reviewers provided helpful comments on the manuscript.
This paper complies with the current laws in Spain. The authors
declare that no conflict of interest exists.
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