the flight feather molt of griffon vultures (gyps fulvus) and associated biological consequences

THE FLIGHT FEATHER MOLT OF GRIFFON VULTURES (GYPSFULVUS) AND ASSOCIATED BIOLOGICAL CONSEQUENCES

INIGO ZUBEROGOITIA1

Estudios Medioambientales Icarus S.L., Pintor Sorrolla 6, 1uC, 26007 Logrono, Spainand

Ornithology Department, Sociedad de Ciencias Aranzadi, Alto Zorroaga, 11, 20014, Donostia/San Sebastian, Spain

JAVIER DE LA PUENTEGrupo Ornitologico SEO-Monticola, Unidad de Zoologıa, Edificio de Biologıa, Universidad Autonoma de Madrid,

28049 Madrid, Spain

JAVIER ELORRIAGAFundacion Migres, CN-340 km 96.2 Huerta Grande, Pelayo, 11390, Algeciras, Cadiz, Spain

RAUL ALONSO AND LUIS E. PALOMARESBRINZAL, Albergue Juvenil Richard Schirrmann, Casa de Campo, s/n 28011 Madrid, Spain

JOSE E. MARTINEZBonelli’s Eagle Study and Conservation Group, Apdo. 4009, E-30080, Murcia, Spain

ABSTRACT.—Molt patterns are poorly understood in most large bird species; however, they are of paramountimportance in the development of surveys in which age is a key parameter. From 2000 to 2011, we studied thebody condition and molt patterns of 214 Griffon Vultures (Gyps fulvus) in Spain. Adult Griffon Vultures (‘‘grif-fons’’) demonstrated a poor body condition in winter during the incubation period, which then improved afterhatching. Conversely, subadults were fairly uniform throughout the year, with their condition slightly inferior tothat of adults throughout the year (except during the incubation period). The molt period lasted from April toDecember, ending in winter. Juveniles started their first molt in May of their second calendar year, beginningfrom the innermost primary (pp1) and proceeding outwards. Later, in midsummer, some individuals moltedsecondaries (only 17% of secondaries were molted in the first molt season) beginning at four foci: from theinnermost (ss25) outwards, the outermost (ss1) and ss5 or ss6 inwards, and centrifugally from ss12. In the thirdcalendar year, griffons continued molting primaries outwards in an orderly fashion and two new foci appeared insecondaries, apparently at ss6 and ss15. Most juvenile feathers were completely molted by the fourth calendaryear, although some fifth-calendar-year griffons had retained juvenile secondaries. Subsequently, adults did notshow a consistent molt pattern, but had a high degree of asymmetry between the two wings. Some quills weremolted more often than others and this led us to hypothesize that adult griffons might molt quills on demand.

KEY WORDS: Griffon Vulture; Gyps fulvus; age determination; body condition; molt phenology; molt sequence.

MUDA DE LAS PLUMAS DE VUELO DE GYPS FULVUS Y CONSECUENCIAS BIOLOGICAS ASOCIADAS

RESUMEN.—El conocimiento sobre los patrones de muda de la mayorıa de las grandes aves es aun escaso, sinembargo resulta de fundamental importancia para desarrollar investigaciones en las que la determinacionde la edad es clave. Entre 2000 y 2011 estudiamos la condicion corporal y el patron de muda de 214individuos de Gyps fulvus en Espana. Los buitres adultos mostraron una condicion corporal baja en in-vierno, durante el periodo de incubacion, la cual mejoro tras el nacimiento de los pollos. Por el contrariolos sub-adultos mantuvieron una condicion corporal uniforme a lo largo del ano, un poco mas baja que losadultos a lo largo del ano, exceptuando el periodo de incubacion. El periodo de muda duro desde abrilhasta diciembre, finalizando en el invierno. Los juveniles comenzaron su primera muda en mayo de su

1 Email address: [email protected]

J. Raptor Res. 47(3):292–303

E 2013 The Raptor Research Foundation, Inc.

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segundo ano de calendario, iniciandola desde las plumas primarias mas internas (pp1) hacia fuera. Des-pues, a mediados del verano, algunos jovenes mudaron las plumas secundarias (solo el 17% de las secun-darias fueron mudadas en la primera sesion de muda), comenzando en cuatro focos, desde la mas interna(ss25) hacia fuera, desde la mas externa (ss1), desde la ss5 o ss6 hacia dentro y centrıfugamente desde lasss12. En el tercer ano calendario, los buitres continuaron la muda de las primarias de forma ordenada haciafuera y aparecieron dos focos nuevos en las secundarias, en ss6 y ss15. Para el cuarto ano calendario lamayorıa de las plumas juveniles estuvieron completamente mudadas, aunque algunos buitres del quintoano aun presentaban secundarias juveniles retenidas. Tras esto, los adultos no mostraron un patron con-sistente de muda, con un alto grado de asimetrıa entre ambas alas. Algunas remiges fueron mudadas masfrecuentemente que otras, lo que nos permite hipotetizar que los buitres adultos podrıan mudar lasremiges cuando fuera necesario.

[Traduccion de los autores editada]

Once formed, feathers become attached deadstructures in which damaged areas cannot be re-paired. They deteriorate mainly through the actionsof physical wear, solar exposure, and feather mitesand must therefore be renewed periodically. Duringmolt in large aerial species such as raptors, feathersare generally replaced sequentially, in predeter-mined order, such that body insulation and (inmost birds) flight are maintained throughout themolting process (Newton 2009). For large birds,the difference in the power required for sustainedflight and the maximum power available is relativelysmall, making flight impossible if they were to allowmolt gaps proportionately similar to those of small-er birds (Tucker 1991). Therefore, those that flywhile molting cannot compensate for the relativelyslow growth of their primaries by replacing moreprimaries simultaneously (Rohwer et al. 2009).

In large vultures, a quill takes a long time to grow:40–60 d or more (Edelstam 1984); 100–108 d in thecase of White-backed Vultures (Gyps africanus; Hous-ton 1975) or 180 d in Bearded Vultures (Gypaetusbarbatus; Adam and Llopis 2003). Thus, a singlemolt wave could not replace the ten primaries with-in one year and perhaps not even a set of seven oreight secondaries, unless several quills were missingor growing simultaneously which would result in biggaps in the aerofoil. Large birds solve this dilemmaby creating several consecutive molt waves that pro-ceed concurrently through each of the larger moltunits (Edelstam 1984, Clark 2004). The presence ofserial molt was demonstrated by Houston (1975),among others, who described it in two African vul-ture species.

In some of the biggest flying birds, such as vul-tures, condors, storks, and albatrosses, each moltcycle lasts more than a year but may be interruptedduring difficult periods, such as nestling-rearing ormigration, and at times of food shortage, such as

midwinter in high latitudes or during extendeddroughts (Mundy 1982, Edelstam 1984, Clark2004, Newton 2009). The process of molting placesadditional energy demands on a bird: (1) to pro-duce replacement plumage; (2) to regulate bodytemperature while feather insulation is reducedand (3) when gaps in the wing, caused by droppedor growing feathers, result in less efficient flight(Ginn and Melville 2000). Overlap of molt andbreeding may be more common in larger speciesbecause the time required both to rear young andto replace flight feathers increases with body size(Rohwer et al. 2009), although in these instancesthe growth of feathers is slowed (Snyder et al. 1987).

In this paper, we describe for the first time themolt pattern of the flight feathers of Griffon Vul-tures and discuss its relationship to other biologicalmechanisms of the species.

METHODS

From 2000 to 2011, 129 Griffon Vultures weretrapped, 76 of them in Biscay (northern Spain)and 53 in Madrid and Segovia (central Spain). Werecorded the molt patterns of 214 birds, including115 free-living individuals of the 129 trapped and 99from wildlife rehabilitation centers (WRC) in Biscay(81 individuals) and Madrid (18 individuals). Forbirds rehabilitating in the WRCs we only consideredthose recently (1–2 wk) admitted, dead or alive, be-cause a captive bird with a constant supply of foodmay renew its entire flight-feather set in one moltperiod.

The birds were inspected following a standard-ized protocol by four trained researchers (Martınezet al. 2002). We recorded a molt card for both wingsof each individual, identifying feather generation bywear, shape, color, age pattern, and growth of theremiges. This gave us data for 10 primaries and 25secondaries for each wing. Primaries (pp) were

SEPTEMBER 2013 THE MOLT OF GRIFFON VULTURES 293

numbered descendantly (from inside toward out-side) and secondaries (ss) were numbered ascen-dantly (from outside toward inside). Feathers wererecorded as A (juvenile), 1 (dropped), 2–4 (grow-ing), 5 or C (completely grown in the current moltseason), K (molted in the previous molt season), M(molted two years ago) and O (molted three yearsago). Based on suspensions and variable rates ofwear among individuals it can be difficult to sepa-rate generations M and O and we interpreted theseresults conservatively.

Age Determination. Juvenile feathers (primaries,secondaries, primary coverts and greater coverts) aremore pointed and narrower than those of adults.Juvenile greater coverts (GGCC) are pointed andedged by a narrow buff zone, whereas adult GGCCare more rounded and edged by a wider buff zone;thus, they are easy to differentiate (Forsman 1999).Greater coverts are molted simultaneously with theircorresponding secondaries and this also occurs withprimary coverts (PPCC) and primaries.

Reportedly, Griffon Vultures do not molt anyfeathers in their first year and begin molting juvenileflight feathers at second prebasic molt in their sec-ond calendar year (2cy) as in other raptors (see Pyle2005a for details about molt cycles and terminology).During the first and second calendar years (cy), untilthe onset of the second prebasic molt, all flight feath-ers belong to the same generation (i.e., were devel-oped simultaneously while in the nest) and show thesame wear pattern. Subsequently, Griffon Vultures,like other large raptors, molt their primaries in suc-cessive waves, starting anew at P1 at the beginning ofeach annual molt, regardless of whether or not allten primaries were molted in the previous cycle. Thispattern is important for ageing immature raptors(Clark 2004). Thus, in observing molt, we were ableto find up to four different feather generations,which allowed us to determine the age until 5cy or4cy+ (Table 1, Fig.1; see Clark 2004, Pyle 2005b).

Simultaneously, we also examined bill color, eyecolor, and the shape and color of neck ruff feathers(Duriez et al. 2011), which can assist in the deter-mination of age. Using our data on 755 resightingsmade of 247 Griffon Vultures banded with alphanu-merically coded bands in Biscay (northern Spain),combined with that of Duriez et al. (2011), we de-termined a suite of characteristics which made itpossible for us to age Griffon Vultures (Table 2).

Body Condition. To determine the body condi-tion of the vultures, we calculated the ratio betweenforearm length in mm (see Ferrer and de le Court1992) and body mass in g. Forearm length is a stableskeletal measure which does not vary once the birdis fully grown (i.e., fledged). Conversely, body masschanges according to the availability of food re-sources. We only used trapped, wild griffons to mea-sure this ratio.

Molt Score. Following Ginn and Melville (2000)and Newton (2009) we created a recording systemaccording to the stage of growth of primaries andsecondaries: old feathers were scored as 0, fullygrown new ones as 5, and growing ones as 1–4. Add-ing together the scores of the different primariesand secondaries produced a single score reflectingthe stage of molt in the individual concerned. Grif-fon Vultures with 10 fully grown primaries and 25fully grown secondaries in each wing scored a max-imum of 100 for primaries and 250 for secondaries,considering feathers on both wings. We then plot-ted the scores of different birds against trappingdate to enable us to estimate the mean start dateand mean molt rate (or duration).

This technique is valid only for monitoring thecurrent year wave molt, as the use of molt scoringfor numerically determining the extent of primarymolt is useful only for those species that replace allten primaries annually (Clark 2004). However, thisscore is useful in describing the extent of the moltannually (Fig. 3).

Symmetry. To calculate the symmetry of the moltprocess between wings, we superimposed bothwings and compared each corresponding primaryand secondary. We assigned ‘‘1’’ when both featherswere at the same molt level and ‘‘0’’ in those caseswhere the feathers were at a different stage. Wethen added the total and obtained the percentageof symmetry for primaries and secondaries (see alsoZuberogoitia et al. 2005).

Statistical Analyses. To test for differences in bodycondition between periods (‘‘incubation’’ [pre-hatching, incubation, and the first weeks of nest-

Table 1. Summary key for ageing Griffon Vultures byplumage state. Cy 5 calendar year.

AUTUMN SPRING REMIGES

1cy 2cy All juvenile feathers2cy 3cy Juvenile and one adult generation3cy 4cy Juvenile and two adult generations4cy 5cy Three adult generations and some

juvenile retained4cy+ 5cy+ Three adult generations

294 ZUBEROGOITIA ET AL. VOL. 47, NO. 3

ling-rearing] 5 January–March; ‘‘rearing’’ [fromthe nestlings’ second month until fledging] 5

April–July; ‘‘post-fledging’’ 5 August–December)and between different ages (subadults 5 between1 cy and 5 cy; adults 5 more than 10 cy), we useda two-way analysis of the variance (two-way ANOVA).

A contingency table was developed to test for dif-ferences in the percentage of molted feathers inadults. The significance of association between thevariables (based on chi-square) is given, with P-val-ues from the chi-square distribution and from apermutation test with 9999 replicates.

Analysis was carried out using SPSS version 18(SPSS Inc., Chicago, Illinois, U.S.A.) and with PASTSoftware (PAleontological STatistics) 2.1. (Hammer2011).

RESULTS

Body Condition. Adult Griffon Vultures had poorbody condition during the incubation period (De-cember–March), which improved significantly afterthe young hatched (one way ANOVA, F2,86 5 16.3, P, 0.0001, Tukey B test P , 0.05, Fig. 2). Subadultshowever, did not show significant differences in thebody condition throughout the year (one way AN-OVA, F2,50 5 2.1, P 5 0.14). Considering the entiredata set, there were no differences in body condi-tion between adults and subadults (one way AN-OVA, F1,142 5 0.015, P 5 0.90), although differenceswere statistically significant when age and periodswere both included as covariates (two way ANOVA,F2,142 5 4.7, P 5 0.01). In winter, during incubation,

Figure 1. Summary key for ageing Griffon Vultures following table 2, considering features of bill and eye color and size,and shape and color of neck ruff feathers. Cy 5 calendar year.


body condition of adults was lower than that of sub-adults. However, adults’ body condition subsequent-ly improved in the springtime, increasing to a levelgreater than that of subadults (Fig. 2). The bodycondition reached its peak level in autumn for bothadults and subadults.

Molt. Juveniles. There was no evidence of flight-feather molt in any of the 80 first-calendar-year Grif-fon Vultures analyzed between the fledging seasonand the end of the year, although one individual,trapped in November, showed growth of p9 and p10on the left wing. This was attributed to an accidentalloss of those feathers and was not considered to bepart of the normal molt process.

Second prebasic molt, second calendar year. Griffonsstarted molting in their second calendar year. Therewas no evidence of molt in 2cy griffons until May.The first active molt was detected on 11 May whenone griffon presented both pp1 just starting togrow. From then until December, 2cy griffons molt-ed on average 7.3 primaries (SD 5 1.6; range 4–11;n 5 19, considering both wings, Fig. 3). Normallythey molted the three or four innermost primariesalthough 12.5% of the pp1 were not molted withinthis first molt cycle.

When the third primary was molted, by midsum-mer, 2cy griffons started to molt secondaries, nor-mally ss25 first, followed by ss24. Three more moltfoci were detected in September, at ss1, ss5 or ss6,and ss12, showing three molt waves, from ss25 out-wards, centrifugally from ss12, and from ss1 and ss5or ss6 inwards (Fig. 4). In total, during the second

prebasic molt, griffons replaced on average 8.5 sec-ondaries (SD 5 9; range 0–20; n 5 19, consideringboth wings).

Summarizing, on average 36.5% of the primariesand 17% of the secondaries were molted within thesecond prebasic molt. The pattern of primaries wasconsistent, whereas the pattern in secondaries variedgreatly among individuals. Four second-calendar-year birds showed an extended molt in secondariesfar from the regular molt pattern (Fig. 4). Despitethe individual variation, the molting process wasclearly symmetric (Fig. 5).

Third prebasic molt, third calendar year. The thirdprebasic molt started at the end of April. Griffonscontinued molting the primaries, beginning wherethey had left off in December of the previous year(pp4 or pp5), and we detected 38.9% of birds be-ginning a new wave from the pp1. During the thirdprebasic molt they replaced on average 8 primaries(SD 5 2.7; range 5–12; n 5 8, considering bothwings). In some cases griffons completed the moltof all the juvenile primaries (31.2% of the pp10were molted) during this molt.

In the 3cy griffons, the molt of secondaries start-ed at the same time as primaries, in April, and fin-ished in December. During this period, griffonsmolted on average 24 secondaries (SD 5 8.7; range10–35; n 5 6, considering both wings). Summariz-ing, on average 40% of the primaries and 48% ofthe secondaries were molted during the third calen-dar year. The molt pattern in primaries continuedoutwards in an orderly manner, whereas in the sec-

Table 2. Summary key for ageing Griffon Vultures by features of bill and eye color and size, shape and color of neckruff feathers. Cy 5 calendar year.

AUTUMN SPRING BILL COLOR EYE COLOR SHAPE AND COLOR OF NECK RUFF FEATHERS

1cy 2cy Black Dark Large brown lanceolate ruff2cy 3cy Black. Some birds present the front

of the bill clearDark Large brown lanceolate ruff

3cy 4cy The front of the bill is clear Dark Large brown lanceolate ruff4cy 5cy The clear area starts to advance to

both sides of the front of the billBrown Three quarters of large brown lanceolate

ruff and one quarter buff-white short ruff5cy 6cy The dark area is mainly detected

at the base of the billBrown One half of large brown lanceolate ruff

and the other buff-white short ruff6cy 7cy The dark area is mainly detected

at the base of the billBrown-hazel One quarter of large brown lanceolate ruff

and three quarters buff-white short ruff7cy 8cy Almost completely clear Hazel Short white ruff with some large brown

lanceolate feathers8cy 9cy Clear Hazel-yellow Short white ruff with some large brown

lanceolate feathers9cy+ 10cy+ Clear Hazel to yellow Short white ruff


ondaries five foci were detected, those previouslyobserved within the first molt of the 2cy (ss25,ss12, ss5/ss6, and ss1) and, in addition, from s15toward both sides (Fig. 4). At this stage, griffonskept the symmetry in 90% of primaries and 85%of secondaries (Fig. 5).

Fourth prebasic molt, fourth calendar year. The fourthprebasic molt started in April and lasted until De-cember. Griffons completed the molt cycle of pri-maries and started a new cycle. We found that 25%of pp1, 58.3% of pp2, 33.39% of pp3, 41.7% of pp4,33.3% of pp5 and 8.3% of pp6 were molted in thisthird molt season. On average, 8 primaries (SD 5

1.76; range 6–9; n 5 4, considering both wings)were molted.

In the 4cy griffons, the molt of secondaries con-tinued the molt waves from the five foci, filling the

gaps (Fig. 4). During this period, griffons moltedon average 18.75 secondaries (SD 5 3.77; range15–22; n 5 4, considering both wings).

Summarizing, on average 40% of the primariesand 37.5% of the secondaries were molted duringthe fourth calendar year. At this stage, griffons keptthe symmetry in 86% of the primaries but symmetrywas greatly reduced in secondaries, being only41.3% (Fig. 5).

Retained juvenile secondaries, fifth calendar year. Atthe end of the fourth calendar year there were stillsome arrested secondaries. In fact, we trapped one5cy griffon which still had retained juvenile featherss10 and s25 on the right wing, perhaps anomalouslyin the case of ss25.

Molt in adults, sixth calendar year and older. Adultsstarted molting primaries in April and secondaries

Figure 2. Box plot (median, 25–75 percent quartiles and minimal and maximal values) showing the changes in thebody condition of subadults and adult Griffon Vultures during the three critical periods (incubation: January–March;chick-rearing: April–July; post-fledging: August–December).


Figure 3. Box plot (median, 25–75 percent quartiles and minimal and maximal values) showing the numerical moltscores of primaries (a) and secondaries (b) of subadults (from 2nd cy to 5th cy) and adult (older than 10 cy) GriffonVultures plotted relative to date.


Figure 4. Molt pattern of Griffon Vultures. The pattern shows the most frequently molted primaries and secondaries insecond, third, and fourth calendar years. Moreover, the molt pattern of an adult (more than 10th cy) trapped inNovember, just one month before finishing the molt season, is shown in order to illustrate molt differences betweenadults and the first molt seasons. The quills molted in the current season are black, those molted in the previous year aredark grey and those molted two years previously are light grey. Molt foci and molt direction are indicated by arrows.


in May and the molt process was fairly continuousuntil the end of December (Fig. 3). Molt did notfollow an evident pattern at this age due to the factthat, from the third molt onwards, the percentageof primaries and secondaries molted (and conse-quently the commencement point of each molt)varied considerably among individuals and even be-tween both wings of the same vulture. In fact thesymmetry between wings was on average 66.7% inprimaries (SD 5 19.8%, n 5 62) and 53% in sec-ondaries (SD 5 13.0%, n 5 57). Certain secondariesand primaries were molted more often than others(x2

34 5 47.7; Monte Carlo P 5 0.05, Fig. 5, 6).On average, adults molted 9.8 primaries (SD 5

2.8; range 3–16; n 5 62, considering both wings)and 28.1 secondaries (SD 5 6.1; range 14–40; n 5

56, considering both wings) in one year’s molt, fromApril to December. Summarizing, on average 48.9%of the primaries and 56.1% of the secondaries weremolted during the adult molt season.

DISCUSSION

The poor body condition of adults during thefirst three months of the year might be related toa low food intake and a high energy demand duringthe pre-laying and incubation periods. This reduc-tion in body condition from autumn to winter couldbe associated with poor weather conditions or withthe photoperiod, which would limit the time avail-able for foraging (see Snyder et al. 1987). The bodycondition of griffons during the autumn reaches

the peak levels observed, even though day lengthis quite similar to that in winter at our latitudeand rainfall is notably higher in autumn.

The low body condition of adults may well be relat-ed to mating, pre-laying and incubating behaviors. Infact, during the mating, nest building, and egg-layingperiod, vultures remain in the nesting area for extend-ed periods in order to prevent extra-pair-copulation(i.e., mate guarding) and to avoid competition for thenesting sites and predation (Xirouchakis and Mylonas2007, Margalida and Bertran 2010). This behavior re-duces the time available for foraging. Moreover, dur-ing the laying period, females reduce their food intake(Kenward 2006) and later, during the incubation pe-riod, birds increase their energy expenditure, especial-ly during episodes of low ambient temperature(Deeming 2004). The mean frequency of incubationswitches between male and female indicates that, dur-ing incubation, breeding vultures forage every otherday (Xirouchakis and Mylonas 2007).

Finally, the amount of time that the nests wereactively attended was negatively correlated with thenestlings’ age (Xirouchakis and Mylonas 2007).Consequently, during the first 3–4 mo of the year,the energy expenditure of griffons is mainly devot-ed to breeding; thus, to minimize the energetic andflight-performance costs of molting in addition toreproduction (see Rohwer et al. 2009), griffons stopmolting from December to April.

After the nest attendance is reduced and bothadults can spend more time searching for food, grif-

Figure 5. Median 6 standard deviation of the percentage of symmetry between both wings of Griffon Vultures in theirsecond, third, and fourth calendar years and adults. Squares represent primaries and black circles represent secondaries.


fons’ body condition increases. In April, adults startthe molt slowly, reaching a balance between the foodintake, the energy investment in rearing the brood,and their own feather molt. The highest rate of molt-ing is found in July and August, when fledglings leavethe nests (Zuberogoitia et al. 2009) and the weatherand photoperiod are still optimal for foraging. Peri-ods of reduced number of carcasses available in thewild, and differential energy demands among thosevultures raising young, those that have failed due tothe loss of the brood (see Zuberogoitia et al. 2009,2010) and those that did not breed, could be thecause of the variability detected in the molt amongindividuals (see also Edelstam 1984).

By contrast, subadults do not need to save energyfor breeding. In Biscay, we detected only one sub-adult (i.e., 4cy) griffon breeding of 92–102 breedingpairs monitored over 5 yr (2006–11, see Zuberogoi-tia et al. 2010). The remaining breeders were classi-fied as 10cy or older (I. Zuberogoitia unpubl. data).However, as we have detected, 2cy griffons startmolting 1 mo later than adults and the number ofmolted feathers is lower. Moreover, 2cy griffons onlymolt a few secondaries, if any, and they stop moltingin December, as do the adults. This pattern is re-peated in the following years, although the numberof primaries and secondaries molted indicates thatthe shedding is slower than that of adults. In mostcases, the first feathers start to be replaced in Apriland the last feathers finish growing in December.The time gap between January and March, even insubadults, would suggest that factors other than re-production are influencing griffon molt. Subadults

could be influenced by their inexperience in forag-ing, mainly during adverse weather conditions andshort daylight duration and also by intraspecificcompetition with adults, by interference and exploi-tation, when they feed on carrion (Bose and Sarra-zin 2007). In fact many juveniles die of starvationeach year after their first flights, in August–October(Zuberogoitia et al. 2009). In autumn, as we havedescribed above, subadults reach a body conditionalmost equivalent to that of adults. The body condi-tion decreases in winter, but not as much as inadults. We believe that subadults probably spendtheir resources and time in maintaining energy lev-els during cold periods, but they do not haveenough in excess for molting.

The difference in winter severity among differentlatitudes seems to influence the timing of the moltand the number of feathers molted. For example,Houston (1975), observed in the White-backed Vul-tures (Gyps africanus) and Ruppell’s Griffon Vul-tures (G. rueppellii) that, after a winter pause, moltis resumed about April; Forsman (1999) suggestedthat Griffon Vultures start to molt in January orFebruary and finish in October or November inSpain (probably southern Spain). Although themolt duration is the same in both Houston’s andForsman’s cases and in our study, vultures in Spainare advanced by 2 mo with respect to those in ourstudy. It is therefore reasonable to expect a diver-gent molt strategy in those subadult griffons fromthe Iberian population, which annually cross theStrait of Gibraltar to overwinter in the African Sahelregion (see Programa MIGRES 2009).

Figure 6. Percentage of molted feathers in adult Griffon Vultures.


As we have seen, griffons start the molt of flightfeathers in their second cy following the typical pat-tern described for most large raptor species, namelyfrom pp1 outwards (Houston 1975, Mundy 1982,Snyder et al. 1987, Adam and Llopis 2003, Pyle2005b). Edelstam (1984) mentioned the presenceof two or three foci in the secondaries of large birdsof prey, following an inward pattern starting from s1and s5 and progressing centrifugally from a focussituated somewhere around s22 (in Aegypius). Ac-cording to Forsman (1999) in Griffon Vultures,which have 25 secondaries, the first molt focus islocated in the innermost secondaries (ss25) and itproceeds outwards. This is similar, for instance, tothe pattern reported in large North American rap-tors (Pyle 2005b) and Eagle Owls (Bubo bubo) inSpain (Martınez et al. 2002). Most 2cy griffons donot molt any secondaries in the first molt season(see also Forsman 1999), whereas others can moltup to 20 secondaries (both wings included). Subse-quently they show two more foci, from ss1 inwardsand centrifugally from ss12, and after that, theyshow two additional new foci from ss5 or ss6 andss15 inwards. Nevertheless, we detected a high vari-ability in the molt of secondaries, both in terms ofthe total number of feathers molted and the orderthat they followed; therefore, this pattern may wellvary among individuals (see Fig. 4).

During the first and second molt seasons, themolt pattern in primaries progresses outwards inan orderly fashion, as has been described in othervultures and related species (Houston 1975, Mundy1982, Snyder et al. 1987), whereas secondaries arereplaced following a more or less multifocus pat-tern. The more quills that are replaced the higheris the asymmetry between wings, mainly in second-aries, although asymmetry is still far below the levelobserved in adults.

Subadult griffons take three years to complete themolt of all quills (i.e., replace all juvenile feathers byadult-type feathers); however, adults can replace allof them within two seasons. Although adults mustalso invest a great amount of energy in reproduc-tion, our results suggest that territorial adults canmolt at a faster pace and still maintain an adequateenergy balance, perhaps because of their greaterexperience, but juveniles are less able to devotethe same amount of energy to molting, perhapsbecause of their inexperience or because they mustforage more widely.

Once the molt cycle is finished, fourth or fifth cygriffons begin the described molt sequence of pri-

maries again, but it is difficult to ascertain whetherthe same occurs in secondaries due to the high var-iability observed. Later, the molt sequence followedduring the early years is lost and we believe thatadults molt quills on demand, although they mayalso maintain a regular sequence as found in NorthAmerican raptors (Pyle 2005b). Our results show ahigh degree of asymmetry (approximately 60%) be-tween wings and considering that adults replace halfof their quills per season, one might surmise thatmolting occurs in a random pattern. Nevertheless,we found that some quills were replaced more oftenthan others, indicating that some feathers may bemore important for griffons or more subject to wearthan others.

An individual that undergoes a succession of in-complete molts can accumulate so many worn feath-ers that its success in subsequent breeding attemptsdeclines; this can progress even to the point of skip-ping a breeding opportunity to clear overworn flightfeathers from the wing (Rohwer et al. 2009). Theenergy balance between breeding and molting can-not be maintained in situations where feathers arehighly deteriorated and this could even result indeath. As Rohwer et al. (2009) suggest–feathers sim-ply cannot be repaired! However, we believe thatadult griffons may select the quill to remove, consid-ering its degree of wear and its position on the wing,and then facultatively provoke the replacement ofthat feather. This behavior has been observed in cap-tive birds in wildlife rehabilitation centers. Somebirds with broken quills were observed pecking re-peatedly at those feathers, thus causing them to fallout. Even juvenile griffons were able to force thereplacement of certain primaries, bypassing the ha-bitual molt sequence. This capacity would explainthe relatively good plumage condition observed ingriffons, particularly in adults, despite the fact thatthey need at least 2 yr for a complete molt and thatthey are commonly involved in disputes while feed-ing, which can cause feathers to deteriorate.

The molt pattern described hereby provides a re-liable technique to accurately age wild Griffon Vul-tures from the time they fledge until they acquirefull adult plumage (i.e., when they replace the lastretained juvenile feather). This technique comple-ments the ageing criteria proposed in Duriez et al.(2011), maximizing the accuracy for ageing this spe-cies. A correct interpretation of the molt pattern ina given individual typically requires an in-hand ex-amination. However, the current sophistication andwidespread use of digital photography among orni-


thologists provides a huge data bank of high-qualityvulture photos on which the state of the molt can besafely inferred, thus broadening the application ofthe molt pattern as an ageing tool for free-rangingGriffon Vultures.

ACKNOWLEDGMENTS

We especially thank Lander Astorkia, Inaki Castillo, Im-anol Gomez, Ainara Azkona, Agurtzane Iraeta, Josean Isasi,Sonia Hidalgo, Jabi Zabala, Josune Iturralde, Ma Jose Ca-ballero, Barbara Culubret, Ana Bermejo, Emilio Escudero,Jose Francisco Pedreno, Mariano Velazquez, Julio Yanez,Nacho Otero, Rafa Martın, and other members of SEO-Monticola Ornithological Group for help in the field. Wealso are greatly indebted to Inaki Intxausti (Wildlife Reha-bilitation Center of Bizkaia), Ignacio Otero (WRC GREFA,Madrid), Patricia Orejas (WRC Brinzal, Madrid), TatianaAlvarez and Fernando Villarino (WRC Buitrago, Madrid).Antonio Galera (Dpto Agricultura, Diputacion Foral deBizkaia), environmental administrations of Comunidadde Madrid and Castilla y Leon gave us permits to workwith Griffon Vultures. SEO-Monticola OrnithologicalGroup helped fund our fieldwork in central Spain. We alsothank Alexandra Farrell for linguistic revision and PeterPyle, William S. Clark, and one anonymous referee forcomments on an earlier version of the manuscript.

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Received 9 February 2012; accepted 22 January 2013Associate Editor: Christopher J. Farmer


the flight feather molt of griffon vultures (gyps fulvus) and associated biological consequences

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