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Moult in Birds of Prey: A Review of Current Knowledgeand Future Challenges for Research

Authors: Zuberogoitia , Iñigo, Zabala, Jabi, and Martínez, José Enrique

Source: Ardeola, 65(2) : 183-207

Published By: Spanish Society of Ornithology

URL: https://doi.org/10.13157/arla.65.2.2018.rp1

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Review

MOULT IN BIRDS OF PREY: A REVIEW OF CURRENTKNOWLEDGE AND FUTURE CHALLENGES FOR RESEARCH

LA MUDA EN AVES RAPACES: REVISIÓN DEL CONOCIMIENTO ACTUAL Y RETOS FUTUROS PARA INVESTIGAR

Iñigo ZUBEROGOITIA1 *, Jabi ZABALA2 and José Enrique MARTíNEZ3

SUMMARY.—Moult is one of three major events in the annual cycle of birds. However, in contrast tobreeding and migration, relatively few studies have been carried out on this topic. This is particularlythe case with the large group of birds of prey and is partly a consequence of a general lack of appreciationof the relevance of moult within the life cycle of species. This factor is exacerbated by the difficulty inobtaining large enough sample sizes in this group, since some species are scarce and birds of prey arealmost always difficult to trap. Nevertheless, moult is an energy-demanding process that takes longer thanthe breeding cycle and, contrary to the latter, it occurs every year. We stress the importance of the annualmoult process for providing a “fixed image” of an individual’s biology and underline its utility infurthering knowledge of the life history of each species. In this review we first outline the basicdefinitions necessary for understanding the moult process, and discuss current information on the moultsequence of European birds of prey, as part of a comprehensive review of the mechanisms of themoult in each group. Secondly, we summarise the main methods used to study, analyse and understandthe moult, and indicate how to use these to obtain relevant information. Thirdly, we explain theimportance of the moult in the life cycle of birds of prey, and how we can use this information to advanceour understanding of the ecology of each species. Finally, we include a view of possible strategiesthat may be used to improve future research, thanks to advances in knowledge of the moult process.—Zuberogoitia, I., Zabala, J. & Martínez, J.E. (2018). Moult in birds of prey: a review of currentknowledge and future challenges for research. Ardeola, 65: 183-207.Key words: arrested moult, definitive plumage, growth rate, moult cycle, moult score, moult sequence,

prebasic moult, serial moult.

RESUMEN.—La muda es uno de los tres principales hitos en el ciclo anual de las aves. Sin embargo, alcontrario que la reproducción y la migración, el número de estudios relativo a la muda es relativamenteescaso. Esto es particularmente evidente en el caso de las aves rapaces, fruto de la falta general de apre-

Ardeola 65(2), 2018, 183-207 DOI: 10.13157/arla.65.2.2018.rp1

1 Estudios Medioambientales Icarus S.L. C/ San Vicente 8. 6 ª Planta. Dpto 8. Edificio Albia I.48001 Bilbao, Biscay, Spain.

2 C/ Sebero Otxoa 45 5 B, 48480 Arrigorriaga, Biscay, Spain.3 Bonelli’s Eagle Study and Conservation Group, Apdo. 4009, 30080 Murcia, Spain.

* Corresponding author: [email protected]


INTRODUCTION

Moult, breeding and migration are the threemajor events in the annual cycle of birds. How-ever, moult has been proportionally much lessstudied (see Newton, 2009). This is partly aconsequence of a general lack of apprecia-tion of its importance to the annual cycle andpopulation processes, and of how knowledgeof moult strategies can contribute to conser-vation-driven research (Newton, 2009). Moultis an energy-demanding process that lasts forseveral months each year, in a regular fashion,throughout the life of each species of birdsof prey. This process takes longer than thebreeding cycle and, unlike the latter, it occursevery year in all species (Rohwer et al., 2011).However, whereas studies exploring theecological correlates and consequences ofbreeding and migration are abundant, only afew are focused on moult and its role in birdecology. Obtaining comprehensive informa-tion on the moult state of a bird requires itscapture; preferably more than once duringeach moulting event, and this can be verydifficult with many species, particularly inbirds of prey (see Bird & Bildstein, 2007).

Thus, lack of knowledge of moult is often alogistical problem. Nevertheless, there is re-cent increasing interest among ornithologist inrevealing the evolution of moult in birds (seee.g. De la Hera et al., 2012; Barshep et al.,2013; Rohwer & Rohwer, 2013).

Sequential moult is the most widespreadpattern across avian taxa. However, the timeconstraint on moulting in large birds cannot beovercome by growing more feathers simulta-neously because of the size-related scaling ofthe power required for sustained flight and themaximum power available from the flightmuscles (Schmidt-Nielsen, 1984; Rohwer etal., 2009). For large birds, the difference be-tween the power required for sustained flightand the maximum power available is relative-ly small, making flight with proportionatelysimilar moult gaps than smaller birds im-possible (Tucker, 1991). Therefore birds ofprey, that fly while moulting, cannot com-pensate for the relatively slow growth of theirremiges by replacing more primaries andsecondaries simultaneously (Rohwer et al.,2011; Zuberogoitia et al., 2013; 2016a).

Intraspecific variation in moult sequence,duration and extent depends, among other

Ardeola 65(2), 2017, 183-207

ZUBEROGOITIA, I., ZABALA, J. and MARTíNEZ, J.E.184

ciación de su relevancia en el ciclo vital de las especies. Este problema se ve incrementado por la difi-cultad de obtener tamaños muestrales suficientes, dado que algunas especies son muy escasas y la mayoríade las rapaces son difíciles de capturar. La muda es un proceso que demanda gran cantidad de energía yque suele durar más que el ciclo reproductor y que, al contrario que este, tiene lugar todos los años. Así,en este trabajo mostramos la importancia de los procesos de muda anual para obtener una “imagen fija”de la biología del individuo y subrayar su utilidad en el conocimiento futuro de la historia vital de las es-pecies. En esta revisión primero describimos las definiciones básicas necesarias para entender el proce-so de la muda y tratamos la información disponible sobre la secuencia de muda de las aves rapaces eu-ropeas, como parte integral de los mecanismos de muda de cada grupo. En segundo lugar, resumimos losprincipales métodos empleados para el estudio, análisis y comprensión de la muda y cómo utilizarlos paraobtener una información relevante. En tercer lugar, explicamos la importancia de la muda en el ciclo vi-tal de las aves rapaces y cómo podemos emplear dicha información para avanzar en el conocimiento dela ecología de las especies. Por último, incluimos una visión de posibles estrategias que podrían ser em-pleadas para mejorar estudios futuros gracias a la incorporación de los avances en el conocimiento de losprocesos de muda. —Zuberogoitia, I., Zabala, J. & Martínez, J.E. (2018). La muda en aves rapaces: re-visión del conocimiento actual y retos futuros para investigar. Ardeola, 65: 183-207.Palabras clave: ciclo de muda, muda prebásica, muda retenida, muda en serie, plumaje definitivo,

puntuación de la muda, secuencia de muda.


factors, on the breeding cycle; the age and sexof the bird; territory quality; the status (dis-persive, floater, sedentary or migrant) of eachindividual; latitude; local weather and climaticvariation (Ydenberg et al., 2007; Newton &Dawson, 2011; Dietz et al., 2013; Zubero-goitia et al., 2016a). Moreover, it must be con-sidered that, once grown, each feather willnormally be retained for at least a year, duringwhich it will deteriorate progressively, due toenvironmental conditions and individual be-haviour (Zuberogoitia et al., 2013). Featherstherefore act as a datalogger, in which the con-ditions experienced by the bird during feathergrowth have been recorded. Hence, a correctunderstanding of the moult sequence unveilsvaluable information about the life processesof a given individual or population.

Some of the above-mentioned factors(e.g. migratory behaviour) have also beensuggested for modelling differences in moultduration between species (De la Hera et al.,2012). However, unlike passerine birds, inwhich there are only a few deviations from thetypical moult strategy (Kiat, 2017), birds ofprey show several different moult patternswhich may be analysed from an evolutionarypoint of view.

In this paper we provide an overview ofmoult sequences and patterns of birds of prey,focused mainly on European raptors and owls,and of how researchers are using this infor-mation to improve knowledge of the life his-tories of these species. We also identifyprospects for this research field, including aset of methods to refine its study. We havetried to include most of the relevant scientif-ic literature about moult in birds of prey. Un-like other biological traits of avian species,there is still a huge lack of basic knowledgeon this topic and therefore we stress the moultas a future tool that can be used to completethe information necessary for understandingthe life of birds of prey.

The review has four sections: (1) Moult inbirds of prey, in which we introduce the basic

definitions required to understand the moultprocess and describe the different moult se-quences of European birds of prey; (2)checking moult, where we describe methodsused to study and analyse moult; (3) the moultand ecological implications, where we showthe different factors affecting moult patternsand indicate how we can use them to developinteresting research; and (4) looking forward.

MOULT IN BIRDS OF PREY: AN OVERVIEW

Feathers

Feathers are special, lightweight structuresconsisting of keratin, a tough, inert protein.Unlike other keratinous structures, such asclaws, feathers do not undergo continualgrowth. Once fully formed, feathers are deadstructures in which damaged parts cannot berepaired. They deteriorate mainly through theactions of physical wear, sunlight, and feath-er parasites and must therefore be periodical-ly renewed (Newton, 2009). Feathers can onlybe replaced by pushing out the old quill. Thisoccurs long before the new feather is fullygrown and functional (Jenni & Winkler,1994). This is a major disadvantage since asignificant reduction in plumage function re-sults if there is a need to replace many feath-ers simultaneously (Jenni & Winkler, 1994).Birds require plumage to be in an optimalstate, in order to efficiently develop key ac-tivities including flight, thermal insulation,courtship, etc. In the case of birds of prey,plumage condition also affects hunting abili-ty, and plumage in a bad state can be fatal.Consequently, during the moult, feathers aregenerally replaced sequentially, in a fixed or-der, so that body insulation and (in most birds)flight are not severely hampered (Newton,2009).

This review of moult sequences and patternsis focused on flight feathers, including wing(remiges: primaries and secondaries) and tail

Ardeola 65(2), 2017, 183-207

MOULT IN BIRDS OF PREY 185


(rectrices) feathers, with particular empha-sis on the first group. Primaries (PP) arenumbered descendantly, from the carpaljoint, P1, outwards to P10. The secondaries(SS) are those feathers attached to the ulna,and are numbered ascendantly from thecarpal joint (S1) to the body (see Fig. 1 foran example). The number of SS varies be-tween species, and depends greatly on theconfiguration of the wing, the size of thebird and, particularly, on the length of theforearm (Ginn & Melville, 2000). Small andmedium-sized birds of prey usually have 13

SS. However, the longer the wing the moreSS appear at the inner end. Old and NewWorld vultures exhibit the largest numbersof SS, with as many as 25 in Griffon Vul-tures Gyps fulvus (Ginn & Melville, 2000;Zuberogoitia et al., 2013). Bearded VulturesGypaetus barbatus have a variable numberof SS (19 or 20), possibly due to the absenceof one of the innermost SS in some birds(Zuberogoitia et al., 2016a). The rectrices(RR) are numbered in pairs, from the cen-tral feathers (RR1) outwards. Most birds ofprey have six pairs of RR, although some ex-

Ardeola 65(2), 2017, 183-207


FIG. 1.—Moult sequence of (a) Falconids and (b) Accipitrids involved in one moult cycle. Black arrowsshow the moult foci and lateral arrows show the moult progression. Grey coloured feathers show thelast-moulted feathers, which are normally those that are arrested in unfinished moult. GC Great Covert,PC Primary Covert, S Secondary and P Primary.[Secuencia de muda de (a) Falcónidas y (b) Accipitridas sujetas a un ciclo de muda. Las flechas negrasmuestran los focos de muda y las flechas laterales muestran la progresión de la muda. Las plumascoloreadas de gris son las últimas plumas mudadas, que suelen ser las que son retenidas en las mudasincompletas. GC cobertora mayor, PC cobertora primaria, S secundaria, P primaria.]

a

b


ceptions exist (e.g. seven pairs in EgyptianVultures Neophron percnopterus).

Differential quality and shape of juvenileversus adult feathers

Nestlings have a first cover of down whichis termed the neoptile. Some species, mainlyowls, show a second generation of downyplumage known as the mesoptile. During thefirst weeks of life nestlings are fed regularly bytheir parents and they exhibit a high increase inbody mass (muscles and bones). The growthrate of the body changes significantly when theflight feathers start to appear because energy in-take is redirected to feather growth, at the ex-pense of corporal growth. Most of the energy in-take is transformed into plumage and a smallerproportion is used to finish corporal develop-ment. Juvenile plumage is that formed when thedowny cover grows out (Cieslak & Dul, 2006).This event is called the first prebasic moult(Wolfe et al., 2014; Howell & Pyle, 2015).

The entire set of juvenile flight feathers isacquired during the nestling or parental de-pendence phase and the constituent feathersgrow simultaneously. The complete growth ofa juvenile flight feather takes about threeweeks in the smaller species (e.g. Scops OwlOtus scops and Lesser Kestrel Falco nau-manni), and three to four months in the largestones (e.g., large eagles and vultures). In turn,adult feathers are moulted gradually and inrestricted sets per moult cycle. As a result, ju-venile feathers are weaker and looser in tex-ture than adult feathers. Juvenile flight feathersare narrower, longer and more pointed at thetip than those of adults.

Moult terminology

Moult in birds is defined as the periodicshedding and replacement of feathers (Camp-bell & Lack, 1985). Replacement of all flight

feathers normally takes place annually (onemoult cycle) in most small species and insome medium-sized birds of prey. However,other species, mainly large raptors, need morethan one year to complete the replacement ofall flight feathers. The whole process maytake up to five years in some owls. The highvariability of moult processes, depending onthe particular species or group of birds, meansthat scientific moult terminology is quite con-fusing (e.g., Wolfe et al., 2014; Howell &Pyle, 2015). We therefore describe here someof the terms used, in accordance with theabove references.

– Prebasic moult: The replacement offeathers that occurs approximately annu-ally in most birds. Prebasic moults arecomplete in most small birds, but are in-complete in large birds, and therefore theydelineate moult cycles (Shugart & Rohw-er, 1996).

– The first prebasic or prejuvenile moultresults in the juvenile plumage. The pre-juvenile moult usually occurs soon afterhatching and often replaces natal down.The prejuvenile moult is ubiquitous (oc-curring in all birds) and complete in extent(developing a complete, new set of feath-ers). This is not a flight feather moult, thuswe will not refer to it in this review, al-though it is necessary to explain theprocess in order to understand the fol-lowing terminology.

– The second prebasic moult starts duringthe second calendar year (hereafter cy) ofthe bird (one year old), when it starts to re-place the juvenile feathers, and it finishesin the same moult cycle, when the birdstops the annual moult. Most species startthe prebasic moult during the breeding sea-son and finish it before winter, within thesame calendar year. Prebasic moults are re-peated every year during the rest of thelife of each individual and are numberedaccording to the age (cy).

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– Moult cycle: The period between the startand finish of the prebasic moult.

– Seasonal moult cycles: This term is em-ployed in the current article for the firsttime. Some migratory raptor species moultin two periods: the post-breeding periodand the wintering period. Together, thesetwo seasonal stages constitute the sameprebasic moult and the same moult cycle,and they usually take place in different calen-dar years (e.g. July-September/January-February).

– Complete moult: When all flight feathersof the same generation have been replaced.

Juvenile plumage is moulted in either a sin-gle or several moult cycles (years) dependingon the species, until the “definitive” (mature)plumage aspect is acquired. Mature plumageis fully developed after the completion ofsecond or third prebasic moult in mostpasserine birds, the fourth or fifth prebasicmoult in most gulls, and later in some largerbird species (Pyle, 2008; Howell, 2010).Some species go through an intermediate step,showing a “subadult” plumage (e.g. BeardedVulture; Bonelli’s Eagle Aquila fasciata). Inthese cases, juvenile birds need one or moremoult cycles to reach the subadult plumage.Subadult feathers are different in colour, sizeand pattern from both juvenile and adultfeathers. Later, the subadult plumage is re-placed in one or more moult cycles until thedefinitive adult plumage is acquired. Once themoult has started, each individual exhibitsvariable plumage coloration between cycles,depending on the differential wear of thefeathers over time.

In raptors, as in all birds, moult proceedsin different directions through different partsof the wing (Edelstam, 1984). The sites fromwhich the moult originates are known as“moult foci”. The use of more moult foci, ormoult centres, may permit a more rapid moultwhile reducing the size of gaps betweenfeathers. Moult in large birds, which need

more than one year to replace all their flightfeathers, often involves more than one moultcentre and occurs in "waves" termed "serialmoult" (e.g. Edelstam, 1984) or "Staffel-mauser". “Staffelmauser” is a German wordmeaning “staggered moult”, introduced bythe German ornithologists Stresemann andStresemann (1966). Serial moult in medium-sized and large raptors typically begins withan incomplete second prebasic moult, duringwhich primary replacement proceeds distallyfrom P1, as in smaller birds, but then arrestsbefore all feathers are replaced. The bird thusretains its juvenile outer primaries for anothermoult cycle, the third prebasic moult, whichequates to an additional year. The third pre-basic moult begins where the previous moultleft off the year before, while another se-quence commences again from P1, resultingin two “waves” of simultaneous primary re-placement (Pyle, 2006). As with the pri-maries, subsequent moults of secondaries be-gin where the preceding moult arrested. At thesame time new waves begin, although not al-ways commencing at all foci every year and,as we will see, there is high variability be-tween species.

Growth rate

Few works have focused on the growth rateof flight feathers in birds of prey. Feathergrowth rates are strongly influenced byfeather size and feather type, and there is alsoan association with body size (Rohwer et al.,2009; De la Hera et al., 2011, 2012; Rohwer& Rohwer, 2013). It takes about 50-65 daysfor a single flight feather to grow in CommonBuzzards Buteo buteo and Black Kites Milvusmigrans (Ontiveros, 1995); 50-60 days inSpotted Owls Strix occidentalis (Forsman,1981) and 100-125 days in California Con-dors Gymnogyps californianus (Snyder et al.,1987) and White-backed Vultures Gypsafricanus (Houston, 1975). The mean growth

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velocity of primaries is 4.6 ± 0.8 mm/day inBlack Kites and 4.6 ± 0.5 mm/day in Com-mon Buzzards, whereas the rates in secon-daries and rectrices are slightly slower. Theaverage rate for regenerating primaries is4.2 mm/day in Spotted Owls. Five OspreysPandion haliaetus, retrapped within short pe-riods, showed average feather growth ratesof 5.7 mm/day for primaries, 3.1 mm per/dayfor secondaries and 3.2 mm per/day for rectri-ces (Prevost, 1983). The average growth ve-locity of California Condor primaries,despite their larger size, is quite similar, at4.3-6 mm/day, and 4.4 mm/day has been re-ported for captive White-backed Vultureremiges (Houston, 1975). The longest feathersshowed the highest growth rates.

Arrested moult/retained feathers/incomplete moult

Some individuals keep interspersed feathersfrom a previous generation (showing a higherdegree of wear) in the position where newones should be. In fact, it is common to findretained, non-moulted feathers in birds ofprey (Pyle, 2005a). Zuberogoitia et al. (2009)described that, during the breeding season ofEuropean Sparrowhawks Accipiter nisus,when the chicks are fledging (in July),18.75% of the breeding females and 55.5% ofthe breeding males suspended the moult. Theperiod during which some individuals werefound to have stopped moulting coincidedwith that of peak food demand by nestlings.Pyle (2005a) defines the contrasts caused bythese interruptions as “suspension limits”, andsuch instances can be identified in theplumage even after a long period of time.Following these recesses the moult is resumedand usually follows the normal sequence.However, in some cases the feather at whichthe moult stopped is retained, and the se-quence jumps to the next quill. We suspectthat this phenomenon may not be restricted to

the breeding season, and that when an indi-vidual is not able to obtain sufficient re-sources to keep up with energy demands itsuspends the moult, resuming the processwhen conditions improve. In fact, duringwinter, when the moult is finished, it is rela-tively common to find retained quills inmost species. These are evidenced by clearsigns of wear in the primaries, secondariesor rectrices moulted in the previous moultseason. There is also obvious wear separa-tion between generations, that is those ar-rested and those moulted in the current year.The presence of retained, non-moultedquills allows us to be more specific when de-termining the age of a bird, adding an addi-tional year in appropriate cases. The numberof retained feathers can also help to evaluatethe life history of an individual during theprevious year. Moreover, if the retainedfeather is of the juvenile type, it provides auseful “zero reference” with regard to theyear in which the individual was born.

The ability to replace damaged feathers outside the moult schedule

Rohwer et al. (2011) suggested that inLaysan Albatrosses Phoebastria immutabilisand Black-footed Albatrosses P. nigripes,those primaries that drag along the sand of theatolls where the birds breed, thus becomingseverely abraded, are replaced more often. Inthe same context, Brommer et al. (2003)showed that Ural Owls Strix uralensis replacethe outer primaries more frequently, suggestingthat the allocation of position-specific ener-getic costs may benefit large birds. Zubero-goitia et al. (2013; 2016a) found that adultvultures replace some feathers more oftenthan others, indicating that certain feathersmay be more important for soaring and gliding.The same authors also noted that vultures areable to provoke the replacement of damagedfeathers facultatively, prior to scheduled moult

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dates. Zuberogoitia et al. (2013) described thatadult griffons select the damaged quills re-quiring removal by considering the degree ofwear and the feathers’ position on the wing.The vultures then force these feathers to fall out,by pecking them repeatedly. Ellis et al. (2016)also documented this behaviour, in Golden Ea-gles Aquila chrysaetos, and suggested theexistence of a neurophysiological mecha-nism for preferentially replacing damagedfeathers. Even juvenile vultures are able toforce the replacement of certain primaries,thus bypassing the habitual moult sequence(Zuberogoitia et al., 2013). This capacitywould explain the relatively good plumagecondition observed in Griffon Vultures,above all in adults, despite the fact that thesebirds need at least two years for a completemoult and that they are involved in continuousdisputes whilst feeding, with consequent de-terioration of their plumage.

Importance and consequences of symmetryin the moult

Fluctuating asymmetry (i.e. random devia-tions from perfect symmetry in bilateralcharacters) has received increasing attentionfrom ecologists in recent decades (Brommeret al., 2003). Asymmetry in feathers is thoughtto reduce flight performance and symmetricalwings are therefore crucial for hunting success(Thomas, 1993). However, Thomas (1993)focused his attention on fluctuating asymme-try in the size of the wings and tail, whichdiffers from the asymmetry found in the moultsequence. Basically, the moult tends to besymmetrical between both wings and tail inthose species that develop a simple moultpattern consisting of one moult cycle. However,asymmetry increases in proportion to thecomplexity of the moult pattern and the ageof the individual (Zuberogoitia et al., 2005;2013, 2016a). The ability to carry out selec-tive replacement of damaged feathers and/or

arrest the moult process increases asymmetry.This is more evident in long-lived birds. Thehigh degree of symmetry that individuals areable to maintain, and the cost that a loss ofsymmetry has in terms of a reduction in indi-vidual survival probability, strongly suggestthat developmental homeostasis in partialmoult is maintained by (stabilising) survivalselection (Brommer et al., 2003). However,Brommer et al. (2003) did not obtain signifi-cant conclusions about the consequences ofasymmetry on the biology of an individual.Nonetheless, they stressed its potential valuefor ecological and evolutionary research.

Moult Sequence/moult pattern

The sequence of flight feather replacementis fairly constant in each species of bird andis often similar throughout larger taxonomicunits (Miller, 1941). Falconids replace theprimaries centrifugally, from P4 to the inner-most (P1) and the outermost (P10), and thesecondaries from two foci (S5 and S13)(Zuberogoitia et al., 2002; Pyle, 2005b; Fig.1a). Accipitrids, and some owl species, re-place the primaries from the innermost (P1)to the outermost (P10), and the secondariesfrom three foci (S1, S5 and S10) (Miller,1941; Stresemann & Stresemann, 1966;Martínez et al., 2002; Zuberogoitia et al.,2013, 2016a; Fig. 1b). Strigiforms, however,show high inter-genus variability and mostgenera follow unique sequences.

In small and some medium-sized accipitrids,some owls, and all falconids the moult of allflight feathers is usually completed in one year(one moult cycle). However, medium-sizedand, more particularly, large accipitrids and cer-tain owl species need more than one year (morethan one prebasic moult) to complete the re-placement of all flight feathers. In the case ofaccipitrids, the basic pattern is followed in anorderly way during the second prebasic moult.During subsequent prebasic moults the process

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becomes complicated, due to the overlapping ofdifferent moult waves (serial moult), and the ca-pacity of some species to voluntarily replacedamaged feathers. In fact, adult specimens ofmedium-sized and large accipitrids show achaotic moult pattern, which some authorsdescribe as an irregular and variable sequence(Stresemann & Stresemann, 1960; Cramp &Simmons, 1980; Schumtz, 1992; Herremans,2000). Similarly, certain owl species completethe moult in two or more years, with sometaking over five years (Martínez et al., 2002;Korpimäki & Hakkarainen, 2012). In addition,some species are long-distance migrants, whichstart moulting in the breeding grounds and con-tinue in the winter quarters, thus showing sea-sonal moult cycles.

Almost all birds of prey, except the genusBubo, prioritise moulting the primaries duringthe second prebasic moult. The moult ofsecondaries usually starts when the primarymoult is already advanced. Moreover, secondcy individuals of those species that require morethan two moult cycles to replace the juvenileplumage usually moult very few secondaries, ifany, during the second prebasic moult.

Falconids– Complete moult in one moultcycle, starting at P4

Most falconids start moulting P4 and S5during the breeding season and finish moultingP10 and S1 in the autumn (mainly October;Fig. 1a; Zuberogoitia et al., 2002; Leonardi,2015).

Falconids– Complete moult in one moult cy-cle, two seasonal moult cycles, starting at P4.

Most of the species in this group are late-breeding migrants that moult a few PP andsome SS whilst at the breeding grounds, ar-rest the moult for migration, and finishmoulting in their winter quarters. Forsman(2016) states that Eurasian Hobbies Falcosubbuteo and Eleonora`s Falcons Falcoeleonorae moult flight feathers in their win-ter quarters. However, breeding females from

southern populations moult P4 (also even P3,P5 and P6) and sometimes S5 (S4 and S6)during the last few days of nestling care, asseen in both Eurasian Hobbies (northernSpain, own, unpublished data; Gabriel deJesús pers. comm., 2017) and Eleonora’s Fal-cons (Canary Islands, Sagardía, pers. comm.,2012). The interval between the last feathermoulted in summer-autumn and the firstfeather moulted in winter is longer than onemonth, and determination of the focus of thesuspended moult is feasible, due to differen-tial wear between adjacent feathers.

Some widespread species show varying be-haviour between different populations, de-pending on the latitude. Most Peregrine FalconFalco peregrinus populations from low lati-tudes are sedentary, those from medium lati-tudes are partial migrants, and those breedingin arctic grounds are long-distance migrants(White et al., 2013). Sedentary or partial mi-grant populations show a continuous moultpattern in a single seasonal moult cycle, whilenordic peregrines (e.g. F. p. calidus) moult intwo seasonal moult cycles; they start on thebreeding grounds, arrest the moult to migrate,and finish in the winter quarters (Wegner &Kersting, 2016; Olle & Estrada, 2017).

Accipitrids– Complete moult in one moultcycle, starting at P1

Most sedentary and short-distance mi-grants in the category of small and medium-sized accipitrids follow the pattern in Figure1b. They start moulting at P1 during thebreeding season. When PP moult is advanced(P4-P6) they start moulting SS at S1, followedby two foci in SS (S5 and S11-13). P10, S4and S8 are the last flight feathers to bemoulted and are also the most frequently re-tained feathers from the previous year.

Medium-distance migrant populations ofsome species (e.g. Red Kites Milvus milvus)complete the moult in their winter quarters ifthey have not finished before migration.However, in such cases, the number of feathers

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involved is small. The affected birds do nothalt the moult process, finishing in October-November in only one seasonal moult cycle,in a similar fashion to local populations.

Owls– Complete moult in one moult cycle,starting at P1

Some small and medium-sized owl species(e.g. Little Owl Athene noctua; Short-earedOwl Asio flammeus; Long-eared Owl Asiootus; Martínez et al., 2002) follow exactlythe same pattern as the above-mentionedaccipitrids (Fig. 1b).

Accipitrids – Complete moult in one moultcycle, two seasonal cycles, starting at P1

Certain medium-sized migratory speciesstart moulting during the breeding season,with some PP and a few SS being affected(they also follow the pattern of Fig. 1b). Somespecies stop the moult before migrating (e.g.Honey Buzzard Pernis apivorus), althoughothers continue moulting during migration(e.g. Montagu’s Harriers Circus pygargus,Arroyo & King, 1996). All of them completethe moult in their winter quarters.

Owls– Complete moult in one moult cycle,two seasonal cycles, starting at P1

Scops Owls moult the innermost PP, and ina few cases some of the SS, after the breedingseason. They then arrest the moult for migra-tion, and finish it after arriving at the win-tering grounds (Martínez et al., 2002).

Accipitrids– Complete moult in multiplemoult cycles, starting at P1

Common Buzzards, for example, need twomoult cycles to complete the replacement ofall flight feathers, following the same se-quence as for other medium-sized raptors(Zuberogoitia et. al., 2005; Fig. 2a). Thisspecies, and others that need more than oneyear to complete the replacement of all flightfeathers (e.g. vultures, which need two orthree moult cycles; Fig. 2b), demonstrate se-

rial moult (Clark, 2004), although not all in-dividuals follow this pattern in the third pre-basic moult. Most individuals resume themoult sequence where they finished in thesecond prebasic moult, and only a small pro-portion start a new wave, moulting P1 and/orP2 (Zuberogoitia et al., 2005; 2013, 2016a).In fact, the moult sequence during the second,third, and fourth prebasic moults is orderly(moulted feathers form a homogeneous block)and there is high symmetry between bothwings. Serial moult is more evident in lateryears and, together with other individual fac-tors, contributes to the asymmetry and chaoticappearance of the moult in adults.

Accipitrids– Complete moult in multiplemoult cycles, multiple plumages, startingat P1

Some species change the juvenile plumageto an intermediate, subadult plumage in two orthree moult cycles (e.g. Bonelli’s Eagle, Vin-cent-Martin & Ponchon, 2013; Golden Eagle,Liguori, 2004 and Watson, 2010; White-tailedEagle Haliaeetus albicilla, Forsman, 2016;Bearded Vulture, Zuberogoitia et al., 2016a).Subadult quills usually have a different colourand pattern to juvenile and adult feathers.Subadult quills are also shorter than juvenilefeathers but are still slightly longer than adultfeathers. This can be observed mainly in thesecondaries. Adult, definitive plumage appearswhen subadult feathers are moulted in subse-quent cycles. However, some adult feathers(mainly innermost PP) appear early on, in thethird or fourth prebasic moult, due to the se-rial moult effect. Such feathers contrast strong-ly with adjacent, subadult quills.

Accipitrids– Complete moult in multiplemoult cycles, two seasonal cycles, staringat P1

This pattern applies to medium-sized mi-gratory raptors. These are trans-Saharan mi-grant species that breed late in Europe,moulting some primaries and secondaries

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FIG. 2.—Moult sequence of (a) medium-sized accipitrids and (b) large accipitrids, which need two ormore moult cycles to complete the replacement of all feathers of the same generation. Figures show thetypical moult sequence of individuals that have finished the third prebasic moult (3rd cy in winter or 4th

cy in spring). Arrows show the foci and the progression of the moult. Grey coloured feathers and arrowsshow the feathers and progression of moult during the second prebasic moult (2nd cy); black feathers andarrows belong to the third prebasic moult (3rd cy); and white feathers are juvenile, retained ones fromthe first prebasic, prejuvenile moult (1st cy). Calendar year (cy). GC Great Covert, PC Primary Covert,S Secondary and P Primary.[Secuencia de muda de (a) Accipitridas medianas y (b) Accipitridas de gran tamaño, que requieren doso más ciclos de muda para completar el reemplazo de todas las plumas de la misma generación. Lasfiguras muestran la típica secuencia de muda una vez finalizada la tercera muda prebásica (3er ac eninvierno o 4º ac en primavera). Las flechas muestran los focos de inicio de muda y la progresión de lamisma. Las plumas y flechas coloreadas de gris indican las plumas mudadas y la progresión de la mudadurante la segunda muda prebásica (2º ac); las plumas y flechas negras muestran la tercera mudaprebásica (3er ac); y las plumas y flechas blancas son aquellas juveniles, retenidas de la primera mudaprebásica, prejuvenil (1er ac). Año calendario (ac). GC cobertora mayor, PC cobertora primaria, Ssecundaria, P primaria.]

a

b

Third prebasic moult 3rd. Cy.Moulted feathersMoulted feathers during the second prebasic moultJuvenile feathers


before departure. Some of them, for exampleOspreys and Steppe Buzzards Buteo buteovulpinus, arrest the moult before migratingand continue the sequence in the winter quar-ters (Edelstam, 1984; Herremans, 2000).However, other species are able to moultwhile migrating (e.g. Booted Eagle Hieraae-tus pennatus, Short-toed Eagle Circaetusgallicus; Forsman, 2016; unpublished pers.data). Some individuals of these species win-ter in southern Europe, or behave as sedentaryspecies, expending less energy and time thanbirds that migrate to central or southern Africa(García-Dios, 2016; Sayago, 2011). We hy-pothesise that this behaviour may permit themto save energy and advance more quickly inthe moult sequence than would be expected.This theory remains to be tested, althoughsome of our data suggest it may be true. In thesame context, juveniles of some of thesespecies spend their first two years in theirwintering grounds. For example, Prevost(1983) showed that juvenile Ospreys start thesecond prebasic moult during the first autumnof life (some months after hatching), whilst intheir winter quarters. Moult then continuesuninterrupted until the age of 22-29 months,before their departure to breeding grounds.These juvenile Ospreys complete the moult inone year, and even show serial moult, whichcauses some of the innermost primaries to bemoulted twice.

Owls– Complete moult in multiple moultcycles

Contrary to raptors, Strigiforms show highvariability in moult patterns, depending onboth the start point of the moult and the di-rection. As we have mentioned above, certainowl species fall within some of the describedP1 groups (Fig. 1b). These owls display a sim-ple moult pattern. “Simple” because theyfollow an orderly schedule, and there is onlyone moult cycle, although some migratoryspecies (e.g. Scops Owls) need two seasonal

cycles. However, most owl species need mul-tiple moult cycles to complete the replace-ment of all flight feathers, and some of themrequire more years than any other raptorspecies. Another differential characteristic isthe fact that most owls do not demonstrate se-rial moult patterns. Owl moult follows an or-derly sequence, resuming where the previousmoult left off the year before.

Strix owls: starting at P5

The moult sequence starts at P5 (P4 inUral owl Strix uralensis; see Pietiäinen et al.,1984) and continues outwards to P10 (Fig.3a). Some birds do not manage to moultthese six primaries in one prebasic moult, butothers are able to moult even more quills. Inthe latter cases, the sequence continues at P4and moves inwards to P1. Secondaries showtwo foci (S10, S5 and sometimes S1/S2),which develop centrifugally (e.g. Ural Owl,Pietiäinen et al., 1984; Tawny Owl, Strixaluco, Martínez et al., 2002; and Great GreyOwl, Strix nebulosa, Solheim, 2011). Duringthe third prebasic moult, Strix owls continuewhere the previous moult finished, and thisschedule follows systematically. However,the differential wear of some feathers causessome of them to be replaced more often thanothers (Brommer et al., 2003), mainly inadult birds.

Barn owls: starting at P6

Barn owls start the second prebasic moultwith P6 and continue centrifugally with P7and P5, although a few individuals are able toshed three primaries during the first cycle(Lenton, 1984; Taylor, 1993; Martínez et al.,2002; Fig. 3b). Secondaries show two/threefoci (S12, S2 and S6), from which moult con-tinues centrifugally. During the third prebasic

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moult the sequence follows on from where theprevious moult finished, P8, P4 and P3. Thesequence is completed in the fourth prebasicmoult (4th cy), with the moult of P9, P10 andP1. There is high inter-individual variabilityin the number of remiges shed during eachmoult cycle.

Boreal Owl: starting at P10

Boreal Owls Aegolius funereus can take upto five moult cycles to complete the replace-ment of all the juvenile feathers (Hörnfeld etal., 1985; Korpimäki & Hakkarainen, 2012).During the second prebasic moult, Boreal Owls

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FIG. 3.—Moult sequence of (a) Strix owls, (b) Tyto owls, (c) Boreal Owl, and (d) Bubo owls. Figuresshow the typical moult sequence of individuals that have finished the third prebasic moult (3rd cy inwinter or 4th cy in spring). Arrows show the foci and the progression of the moult. Grey coloured feathersand arrows show the feathers and progression of moult during the second prebasic moult (2nd cy); blackfeathers and arrows belong to the third prebasic moult (3rd cy); and white feathers are juvenile, retainedones from the first prebasic, prejuvenile moult (1st cy). Calendar year (cy). GC Great Covert, PC PrimaryCovert, S Secondary and P Primary.[Secuencia de muda de (a) género Strix, (b) género Tyto, (c) mochuelo boreal y (d) género Bubo. Lasfiguras muestran la típica secuencia de muda una vez finalizada la tercera muda prebásica (3er ac eninvierno o 4º ac en primavera). Las flechas muestran los focos de inicio de muda y la progresión de lamisma. Las plumas y flechas coloreadas de gris indican las plumas mudadas y la progresión de la mudadurante la segunda muda prebásica (2º ac); las plumas y flechas negras muestran la tercera mudaprebásica (3er ac); y las plumas y flechas blancas son aquellas juveniles, retenidas de la primera mudaprebásica, prejuvenil (1er ac). Año calendario (ac). GC cobertora mayor, PC cobertora primaria, Ssecundaria, P primaria.]

a b

c d

Third prebasic moult 3rd. Cy. Moulted feathers during the second prebasic moult

Moulted feathers

Juvenile feathers


start moulting at P10 and the sequence con-tinues inwards (Fig. 3c). The number of pri-maries moulted each year depends on age, sex,latitude, breeding status, weather and rodentcycles (Korpimäki & Hakkarainen, 2012).Some individuals show serial moult, starting anew wave at P10 while still moulting the in-nermost primaries (Martínez et al., 2002).

Large owls: exceptional cases

In all the cases described above, the moultof flight feathers starts in the primaries.However, Eagle Owls Bubo bubo and SnowyOwls Nyctea scandiaca are totally different(Martínez et al., 2002; Solheim, 2012). In thesecond prebasic moult the process normallystarts with the central pair of rectrices and theshedding of the innermost secondaries (SS13-15). In favourable conditions, second cy owlsare able to continue moulting further secon-daries, following an ascendant order (out-wards). Additionally, some individuals areable to moult P6/P7 (Fig. 3d). During thethird prebasic moult, owls continue wherethey finished the year before, shedding P6 andcontinuing with P7 and P8 and advancing inan orderly manner with SS from a new focusat S1. They continue the moult of PP cen-trifugally during the following prebasicmoults, although a new focus starts from P1outwards, and P3 and P4 are the last moultedprimaries. Some birds may take up to fiveyears to complete the replacement of all flightfeathers of the same generation.

METHODS FOR ASSESSING MOULT

Once in hand, a bird of prey is firstly givenan overall check, to review the general appearance of the plumage. Juveniles haveuniform plumages, with all flight feathersshowing the same wear level, colour andpattern. By contrast, from the onset of the

second prebasic moult onwards, individualsshow heterogeneous plumage due to differen-tial feather wear. The main rule whenrecording moult is to keep in mind the pre-dictable moult sequence of the species.Knowing when and how the moult of eachfeather is going to occur will help the correctidentification of feathers. For example, thefirst flight feather(s) moulted in a PeregrineFalcon is always P4 and the last should be S1,P1 and P10. Between these extremes thereshould be a gradual difference in colour andwastage from the newest feather to the oldest.If checking a peregrine in winter we shouldfirst examine P4, which should be the oldestfeather at this time. If any other quill shows amore worn pattern, then it is a retainedfeather that has not yet been moulted or is notgoing to be moulted. This is especially usefulto identify several feather generations in largespecies.

In some species it is very difficult to detectsubtle changes in the worn feathers. This isparticularly true for owls, especially olderbirds, which are able to conserve all theirflight feathers in an excellent state. However,researchers can now use black ultraviolet(UV) light fluorescence to check moult inowls (for more details see Weidensaul et al.,2011). In owls, new feathers are covered byporphyrins, which are natural pigments thatfluoresce brightly when exposed to UV light.Porphyrins are easily destroyed by exposureto sunlight, and are hence most abundant innew feathers. Under UV light, positioned15 cm away, the ventral surfaces of newly-moulted flight feathers fluoresce an intensemagenta colour. This effect is brightest in theproximal third of the feathers, and fainter orabsent from the distal third (Supplementarymaterial appendix 1, Figure A1). The older thefeather the less magenta is present, hence it ispossible to detect the moult sequence by com-paring the magenta composition of thefeathers. Feathers replaced during the pre-vious moult cycle lack porphyrins and do not

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show the magenta colour. This method is verygood for checking the moult of some species(e.g. Tawny Owl, Supplementary materialappendix 1, Figure A1) but lacks enoughresolution for others (e.g. Barn Owl).

Field photography

The study of moult entails trapping and han-dling (and associated disturbance) of birds ofprey. Thus, the use of field photography couldbe considered as a non-invasive study tech-nique. Despite this, the use of high quality pho-tographs of wild birds of prey to create moultcards has scarcely been used since the first ar-ticles were published (Snyder et al., 1987). Thecurrent level of sophistication and widespreaduse of digital photography among ornithologistshas created a huge databank of high-quality pic-tures from which moult state can be safely in-ferred (Supplementary material appendix 1,Figure B1). Zuberogoitia et al. (2016a) used thismethod to increase the number of moultcards for a species that is difficult to handle(Bearded Vulture). This technique has alsobeen used to increase sample sizes for scarce,endangered species or those that are difficult totrap (see Ryan, 2013; Vieira et al., 2017).

Moult in captive birds

The moult sequence is the same for birds incaptivity as for wild individuals, at least forsmall and medium-sized species that completethe moult in one cycle. However, the onset,duration and end date of the moult may bedifferent (see e.g. Hörnfeldt et al., 1985;Chandler et al., 2010). Captive birds are feddaily and their energy demands: for flying,hunting, mating or defending the nest and theterritory, differ from those of wild birds (Cies-lak & Kwiecinski, 2009). Moreover, climaticconditions in captivity vary less than those ex-perienced in the wild, hence less energy is re-

quired to maintain basal metabolism. Forexample, most falconers know how to inducea peregrine or goshawk to finish the moult bythe first weeks of September, by increasingboth the quantity and quality of food andkeeping the bird in stable light and tempera-ture conditions, whereas a wild individualdoes not finish until at least a month later.

Recording and analysing moult

Moult Score

Ginn and Melville (2000) and Newton(2009) suggested a standard recording systemaccording to the growth stage of primariesand secondaries: old feathers are scored as 0,fully grown new ones as 5, and growingfeathers as 1-4 for intermediate stages of de-velopment. These individual moult scoreswere then summed to give an overall moultscore of between 0 and 50 (for 10 PP) and 0and 65 (for 13 SS). Rohwer (2008) alsoshowed how to assign scores indicating direc-tion of replacement and points where waves ofmoult started or will stop, which is really in-teresting. Combining these scores across indi-viduals yields a moult summary table, thestarting point for determining the rules offeather replacement. In this procedure,growing primaries and secondaries are scoredas decimal fractions of their full length,varying from 0.1 to 0.9 (Rohwer & Wang,2010; Rohwer & Broms, 2013), and they havealso changed the moult score system used inEurope. However, the problem of summarisingmoult in summary tables where two or threefeather generations must be considered wasnot normally addressed. Following Zubero-goitia et al. (2013), feathers scored as 0 arealso recorded as A (juvenile), K (moulted inthe previous moult season), M (moulted twoyears previously) and O (moulted three yearspreviously). In future, it would be valuable thatmoult cards of birds of prey include: 1) thenumbers of growing feathers examined at

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each locus, 2) the direction of replacement be-tween adjacent feather pairs, 3) nodal and ter-minal feathers marking points of initiation orre-initiation of moult following arrests, and 4)the age of the feathers.

Timing of Moult. Underhill-Zucchini models

The timing of primary and secondary moultcan be analysed using models developed byUnderhill and Zucchini (1988) and Underhillet al. (1990), implemented in the “moult”package (Erni et al., 2013) for R. Moult index(the ratio between the sum of moult scores atany one time and the total moult scores of allfeathers, with values between 0 and 1) is usedas the response variable. Date, converted intoJulian days, is the vector on which moult in-dexes are observed. With this data (moult in-dex and date) it is possible to build basicmodels that make use of non-moulting as wellas moulting birds, fitting the model using themaximum likelihood method (Newton, 2009).These models give estimates of moult dura-tion, average start date (from which averageend date can be calculated), and the standarddeviation of the start date. It is possible to se-lect five basic levels or types for analysis ofthe moult data: Type 1 – Where the entirepopulation is considered: those individualsthat are not yet moulting, those in moult, andbirds which have completed moult. In thiscase the value used does not matter. Type 2 –The entire population is considered but moultscores are required. Type 3 – Only birds inmoult are considered. Type 4 – Birds in moultand those that have completed moult are con-sidered. Type 5 – Birds that have not startedmoult and that are in moult are considered.However, these models cannot be applied tothose many birds of prey with incomplete orstepwise moults. Thus, these likelihoodmodels cannot be applied to tropical speciesthat moult year-round, and they sometimesfail to work for species with distinct moultseasons. Nevertheless, Zuberogoitia et al.(2016a) modelled the moult of Bearded Vul-

tures using the data type 1, requiring only in-formation on whether an individual has notyet started moult, is in moult, or has com-pleted moult, coded as 0, 0.5, and 1, respec-tively, using only the current year’s moultingfeathers for analyses.

Explanatory variables

The moult package (Erni et al., 2013)goes further, by enabling exploration of theeffects of explanatory variables (e.g. sex,age, different geographical populations,years, rainfall; Barshep et al., 2013 andZuberogoitia et al., 2016a,b) on: 1) moult du-ration, 2) start date and 3) the standard de-viation of the start date (Erni et al., 2013). Asthe authors suggest, these covariates can over-lap, and quadratic terms, interactions, etc. canbe added to either part, using the standard Rnotation for model formulae. Dietz et al.(2015) investigated the effect of body massand geographical latitude on primary moultduration with linear and quadratic models,using a non-phylogenetic conventional ordi-nary least squares regression (OLS) and aphylogenetic generalised least square re-gression (PGLS) in R. Dietz et al. (2013)also used the moult package for some analy-ses. Since the package does not allow a com-parison of nested groups they also used generallinear models (GLM) for testing differencesbetween age categories within sex, and be-tween males and females within an age cate-gory, employing a series of models that esti-mated a combination of the variables(duration, start date and SD of start date)separately for both age category and sex andcalculating AIC values.

Using moult for ageing

In species achieving a complete moult inone moult cycle, a high proportion of indi-viduals can be aged as either in their second

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cy (in second-basic plumage) or older (at leastthird-basic plumage; Pyle, 2005a). However,it is possible to go further, through analysis offeather retention patterns. An individual withadult plumage but with some retained juvenilefeathers is aged as second cy in autumn orthird cy in spring. If the retained feathers areadult (i.e., two generations of adult feathers),the individual will be aged as at least third orfourth cy (3rd cy+ in autumn/4th cy+ in spring).

For those species taking more than onemoult cycle to complete the replacement of allfeathers of the same generation, the mini-mum age of individuals can be determined upto their 5th cy (fifth-basic plumage). This isachieved by examining the number of genera-tions present among the primaries and secon-daries, and looking for retained feathers (seee.g. Martínez et al., 2002; Pyle, 2005a;Zuberogoitia et al., 2013). In some speciesshowing multiple different plumages (i.e., ju-venile, subadult and adult) birds can be agedbeyond their 5th cy (see e.g. Zuberogoitia etal., 2016a). Moreover, if the moult pattern andthe trend in the asymmetry of both wings areknown it is possible to go further in ageingcertain species (e.g. Common Buzzardhttp://depredadoresdebizkaia.blogspot.com.es/2013/01/busardo-ratonero-tercera-muda-en.html).

THE MOULT OF BIRDS OF PREY AND ITSECOLOGICAL IPLICATIONS

Trade-offs between moult, breeding, migration and wintering

The processes of breeding, flight feathermoult, and migration all require extra foodabove the needs of daily maintenance. Nor-mally, each stage requires high amounts ofenergy that determine mutually exclusive ac-tivities (Hedenström, 2006). Moult is usuallytimed to minimise peaks in energy demandsduring either reproduction or migration, and

the duration and extent of moult is constrainedby the energy invested in either of the lattertwo factors (Pietiäinen et al., 1984). In addi-tion, many birds demonstrate a quiescent pe-riod in winter, during which they are neitherbreeding, moulting or migrating (Newton,2009).

Moulting and breeding are both energeti-cally demanding activities. Hence moult inpasserines is usually delayed until breedinghas finished (Hemborg & Lundberg, 1998;Hinsley et al., 2003). However, birds ofprey require long periods for moulting, andtherefore moult normally starts during in-cubation (several weeks earlier in femalesthan males) or during the first weeks ofchick rearing (Schumtz, 1992; Newton,2009; Zuberogoitia et al., 2016a). In birds ofprey, the division of breeding duties be-tween the sexes is more marked than in mostother birds (Korpimäki & Hakkarainen,2012). In most species, except vultures, fe-males perform most or all of the incubation,brooding and feeding of the nestlings, whilemales provide most or all of the food for thefamily (Newton 1979, 1986; Cramp & Sim-mons, 1980; Krüger, 2005; Zuberogoitia etal., 2018). A period of hunger, due to in-creased demand for food on the part of off-spring, is mostly associated with a decelera-tion in the process of feather loss and alsocauses some birds, mainly males, to arrestthe moult process in order to meet their off-spring’s requirements (see Newton & Mar-quiss, 1982; Espie et al., 1996; Cieslak &Dul, 2006; Zuberogoitia et al., 2009).Hence, the more time spent rearing young,the less time there is for moult. Reciprocally,a longer moult, to clear worn feathers fromthe wing, may make breeding in the nextseason impossible (Rohwer et al., 2011).The number of moulted remiges has alsobeen found to decrease with increasingbrood size (Pietiäinen et al., 1984; Karell etal., 2013). Equally, birds losing their broodsearly, or not commencing breeding at all in

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the given season, tend to have a more ad-vanced moult (Cieslak & Dul, 2006).

Photoperiodic responses in birds differwith latitude and more northerly breeders tendto moult faster (Orell & Ojanen, 1980; Mor-ton & Morton, 1990, Bojarinova et al., 1999).Late-moulting birds will also have shorterdays in which to accumulate energy stores forovernight feather growth (Murphy & King,1990), and may face dwindling food suppliesand falling temperatures. Later breeding hasbeen associated with reductions in adult re-productive success and survival (e.g. Siikamä-ki et al., 1994; Nilsson & Svensson, 1996),and conflicts between the requirements ofbreeding and moulting have been suggestedas explanatory factors (Hinsley et al., 2003).Birds of prey, however, have corrected thisproblem and show differential moultingprocesses depending on the latitude of thebreeding grounds. Smaller raptor and owlspecies normally finish their moult before thepost-breeding migration or before winter (forsedentary species). However, late-breedingspecies (e.g. Eurasian Hobby, Scops Owl) orpopulations (e.g. arctic peregrines; Wegner &Kersting, 2016) replace their feathers in twoseasonal moult cycles: starting on theirbreeding territories and finishing at the win-tering grounds.

In long-distance migrants flight feathermoult rarely overlaps with breeding or mi-gration. However, most species start moultingduring the last part of the breeding seasonand stop before migration, resuming themoult in winter quarters (Herremans, 2000;Chandler et al., 2010). The replacement ofsome primaries before migration may enablethe birds to exploit a food resource during aperiod of the year when other pressures arenot high. It may also enable the replacementof the remaining primaries, on the winteringgrounds, to take place at a more leisurely ratethan otherwise (Mead & Watmough, 1976).However, as we have already commented,some species are able to continue moulting

during migration (e.g. Booted Eagle, Short-toed Eagle, Montagu’s Harrier). The migra-tory flight of harriers seems to be slow andgenerally takes place at relatively low alti-tudes. They combine flapping and glidingwith hunting along the way (Brown, 1976).This mode of migration may allow harriersto continue moulting slowly while migrating,as they are not obligate soaring birds, forwhich gaps in the wings would representhigher energetic costs (Arroyo & King,1996).

By contrast, large, sedentary species mayextend the time devoted to moult, but suspendmoult in winter to save energy, in order to sur-vive during adverse weather periods and buildenough reserves to start reproduction early(Zuberogoitia et al., 2013).

Individual experience and status

Age-related differences in moult may beexpected between individuals that have notyet entered the breeding population, andshould be especially prominent in long-livedspecies with delayed sexual maturation.During the first years of life, juveniles of allspecies pass through critical stages that affectthe moult process (e.g. dispersion, foragingexperience, first migration, floating). Juve-niles require more energy to obtain the samefood intake as territorial adults. Experienceand knowledge of the territory mark thedifference, and this is reflected in the moult.Although most birds of prey do not breedduring the second cy, and hence are not thenlimited by the energy demands required to de-velop the breeding cycle, juveniles normallystart moulting later than adults and they moultfewer flight feathers than adults during themoult cycle. This is especially evident in largespecies. Immature vultures, for example, needthree moult cycles to complete the moult,while adults are able to finish a completemoult in two moult cycles (Zuberogoitia et

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al., 2013; 2016a). However, subadult birds(3rd, 4th and 5th cy) start moulting earlier thanadults, although they are still not able to moultmore feathers than adults (Zuberogoitia et al.,2016a). As birds gain experience they can mo-bilise more energy, which enables them tomoult earlier and change more quills than ju-veniles.

Age-related plumage care

New quills usually contrast strongly withold feathers in both juvenile and subadultbirds. This is made more obvious by the factthat, as we have mentioned above, feathers aredifferent during the first stages of the life of abird of prey, particularly in large raptors.However, the older an individual, the moredifficult it is to detect differences between twogenerations of flight feathers. We suspect thatindividuals are able to improve feather care,and that this ability may be related to survivalprobability.

Territory quality

Individuals inhabiting a rich territory mayhave a greater food intake and feed more fre-quently than those located at a lower quali-ty site. This parameter (territory quality) isusually difficult to measure. Occupancy,breeding success, and productivity are thecommonest factors used to model it. Wesuggest that moult may be used as anotherrelevant tool for assessing territory quality.In this regard, Espie et al. (1996) showedthat male Merlins Falco columbarius, in-habiting higher quality territories had high-er moult scores, suggesting that they wereable to moult at a faster rate, or start earlier,than their counterparts in lower quality terri-tories. This example suggests that moultmay be used as a novel tool to study popu-lation ecology.

Applications of moult in ecological studies

Unfortunately, few studies of moult in birdsof prey go further than the classical objectiveof ageing an individual. As Newton (2009)suggested, the lack of knowledge of basicmoult in raptors prevents major investment inother research projects. Nevertheless, itshould be possible to develop a trend in whichmoult can be used to test the biological andecological parameters of birds of prey. By wayof an example, Karell et al. (2013) suggest thatthe colour polymorphism of Tawny Owls islikely to covary with physiological and be-havioural traits, due to genetic pleiotropy be-tween genes regulating pigment productionand those regulating physiological and be-havioural functions. The authors show thatboth male and female brown Tawny Owlsmoult significantly more primary feathersthan grey individuals, irrespective of age orreproduction decisions in the year of moult.The benefits of moulting additional feathersmay override putative costs and instead im-prove performance. In the studied popula-tion, brown adult Tawny Owls have a lowersurvival probability than grey birds, especiallyunder adverse winter conditions (Karell etal., 2011).

This type of analysis using birds of prey asmodels is scarce in the literature but nowa-days there is increasing interest in exploringthe relationship between moult and ecologi-cal processes in other groups of birds. Forinstance, moult can serve as an indicator ofother life-history stages that cannot be quan-tified directly. Zuberogoitia et al. (2016b)showed a relationship between delayed moultonset of European Storm Petrels Hydrobatespelagicus and particular episodic weatherevents. Barshep et al. (2013) quantified theeffects of environmental factors on the startand duration of moult in the Curlew Sand-piper Calidris ferruginea, demonstrating thatdisturbance at a certain stage within the annualcycle of migratory birds can alter the next

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biological event, through carry-over effects.They demonstrated that when moult startedlater the duration was often shorter, but thatlate completion of moult might have fitnessconsequences, probably jeopardising sur-vival. Rohwer et al. (2011) suggested that, iffeather quality is the currency linking trade-offsin reproductive performance between sea-sons, birds with worn feathers should have re-duced breeding success. In fact, by studyingtwo species of albatrosses, they related thefailure to replace all primaries every two yearsto a lower success rate in the breeding sea-son following the failure. The likelihood ofattempting to breed during that season wasalso reduced.

Determination of individual condition

If we know the moult pattern, age and gen-der determinations, and breeding cycle ofeach species we can assess the health status ofan individual prior to its being handled. Thisis very useful for wildlife rehabilitation cen-tres (WRC), where birds of prey are usuallyadmitted all year round in multiple circum-stances. If we know the moult pattern and theaverage extent of the moult on a certain date,we can distinguish between an acute orchronic cause of admission, where this is notreadily apparent.

LOOKING FORWARD

In recent decades there has been increasinginterest in determining the moult sequenceand related traits of raptors and owls. Conse-quently, the number of published papers onthis topic has increased considerably in recentyears, although there is still a dearth ofknowledge that prevents researchers fromgoing further. Unfortunately, there is a lack ofsufficient expertise for carrying out properstudies of moult in most birds of prey species.

One of the main reasons why moult data is notconsidered more widely is that checkingraptor moult is a skill than many researcherslack.

In this review we have summarised currentknowledge of the moult of birds of prey, andwe propose the need for further studies tocomplete basic information on the moult ofsome species. We also consider it important toincrease the use of high-resolution photogra-phy, in order to accelerate the collection ofmoult data for scarce or difficult-to-trapspecies. As a subsequent step, moult cardscould be useful tools in a new generation ofecology and evolution research. It is very in-teresting, for example, that most raptorspecies follow two basic moult patterns (Fal-conids and Accipitrids), but owls show atleast five totally different moult patterns,which are unique to each genus. We must alsoconsider that, currently, we only partiallyknow the moult sequence of a limited numberof species, mainly European and North-American birds of prey. There is still a hugegap in knowledge of tropical species andthose of other less-studied regions. This lackof information obscures potentially interestingdata and limits model variations (see e.g.Kang & Hur, 2016).

An example of how moult data could beapplied in future studies arises from the workof Margalida et al. (2013). They examined themovement patterns of pre-adult, non-breedingBearded Vultures born in the wild Pyreneanpopulation and in the reintroduced popula-tions of the Alps and Andalusia. Theyshowed that birds from the wild and rein-troduced populations differed in their move-ment patterns, with shorter dispersal in theformer. However, the authors failed to pos-tulate which of these behaviours would beadvantageous for the target populationssince they lacked data on response variables(e.g. breeding success), which is needed toevaluate individual condition. We considerthat, by using field photographs of the birds,

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it might be possible to obtain individualmoult cards. The response variable (moultscores) could then be modelled with fixedfactors, such as the origin of the population,sex, or age; and with covariates, such as dis-persal area, movement patterns and disper-sal distance

This method is also valid for testing thelife strategies of different populations or forcomparing different habitats (see e.g. Hins-ley et al., 2003). For example, some species,mainly large raptors and owls, do not breedevery year, and knowledge of moult scoresmight permit other hidden responses to beevaluated (see e.g. Rohwer et al., 2011).Moreover, moult scores and related factors(onset, standard deviation of the start date andmoult duration) may be useful for comparingthe inter-annual effects of climatic condi-tions on target populations (see e.g. Zubero-goitia et al., 2016b).

ACKNOWLEDGEMENTS.—We thank Javier Elorria-ga for his valuable comments in a first draft andthanks to Alexandra Farrell for the linguistic revi-sion. Sievert Rohwer and one anonymous review-er provided helpful comments on the manuscript.

AUTHOR’S CONTRIBUTIONS.—Study conceptionIZ, Investigation IZ, Resources IZ, JZ, JEM, Datacuration IZ, Writing initial draft IZ, Writing criti-cal review and commentary of revision JZ, JEM,Supervision IZ, Project Administration IZ.

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SUPPLEMENTARY ELECTRONIC MATERIALAdditional supporting information may be

found in the on-line version of this paper. See vol-ume 65(2) on www.ardeola.orgAppendix 1, Figure A1. Left wings of Tawny

Owls, lit by normal flash (left) and UV torch(right).

Appendix 1, Figure B1. Moult sequence of a 4th cyBonelli’s Eagle in flight, photo taken in January

Submitted: September 14, 2017Major revision: October 23, 2017

2nd revision arrives: October 26, 2017Minor revision: December 19, 2017

3rd revision arrives: December 28, 2017Accepted: January 11, 2018

Editor: Pascual López-López

Ardeola 65(2), 2017, 183-207


© Juan Varela


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