Complex ageing of Griffon Vulture as a result of different moulting strategies in immature birds
Griffon Vulture is usually considered a resident species in Europe, but actually c.30-40% of the juvenile birds migrate towards the Sahel and spend a variable amount of time south of the Sahara. The annual counts at the Strait of Gibraltar reach 6,000 birds – and the sighting of hundreds of these magnificent beasts crossing the 14km stretch over the ocean is one of the most breathtaking (and less well known) birding experiences within the Western Palearctic.
A unique aspect of this migration is that within a single population some birds are resident and others are trans-Saharan migrants, something rarely seen in raptors (in Europe, only the Sparrowhawk and, to a lower extent, the Booted Eagle show this behaviour on a regular basis). Both resident and migratory populations follow their own moult strategy, leading to a diverse variety of moult stages that make ageing of immature Griffon quite tricky, as qualitatively explained in Fig. 1. This may not be an appealing identification topic that will help you find a nice rarity in the future, but it’s undoubtedly most interesting for raptor enthusiasts and anyone with an interest in moult and ageing.
Figure 1. Illustrative plot showing the qualitative differences in moult between the resident and migratory populations of Griffon (no real data!). The main idea is that resident birds in Iberia do not moult during the winter months, whereas migratory birds that spend their first years of life in the Sahel do moult in winter, leading to a +50% of progress in terms of replaced remiges. Hence, 3cy that return to Iberia look quite avanced compared to resident birds of the same age; in the case of birds that remain in Africa and return in their 4cy, they have benefitted from 8 extra months of active moult compared to resident birds, looking indeed like resident 5cy Griffons.
Moult in resident Griffon Vultures
The moult of resident Griffon Vultures has been described in detail by several authors (Zuberogoitia et al. 2013, Forsman 2016) following the classic pattern of large raptors. My experience is mainly based on the detailed study of Griffons in Catalonia, NE Spain, where they seem to be fairly resident based on ringing recoveries. In Spain, Griffons typically moult between March and November (thus 8 months of active moult). They moult roughly 4 primaries (range 3-5) and around 8 secondaries (range 6-7) per year and wing, and this rate seems to be pretty constant regardless of the bird’s age. Feather wear in Spain is relatively slow; for instance, juvenile primaries look relatively fresh during the 2cy, and in some 3cy birds it is truly difficult to spot the replaced remiges amongst the only slightly worn juvenile ones.
The moult pattern in immature birds progresses as follows:
Second calendar year (2cy) birds. Griffons show an immaculated juvenile plumage during most of their second year, Primary moult starts in mid May the earliest, when p1 is usually shed, but many birds have not started their primary moult in June. During the 2cy they moult 3-5 primaries, being 4 moulted primaries the most common state. Just a couple of secondaries are replaced, but birds with no secondary moult at all are quite common.
Third calendar year (3cy) birds. During the 3cy the moult progresses, and most birds have replaced p8 by the end of the year. The whole set of replaced primaries look fresh but typically with a noticeable contrast between those moulted in the present year and those moulted the previous year. A few secondaries are typically replaced, but still retaining a good number of juvenile ones that by now look quite worn. Around c.20% of birds start a new moult front, replacing p1.
Fourth calendar year (4cy) birds. During their 4cy, resident birds complete the replacement of the juveniles feathers (moulting p9&p10), and start a new locus at p1; by the end of the year/beginning of the 5cy most birds show newly moulted p10 and inner primaries p1, p2 and sometimes p3. All the juvenile secondaries are finally replaced.
In addition to the flight feathers moult, other features such as the bill color, iris, and ruff change with age. At the beginning of the 5cy, birds retain a dark eye but show pale areas on the bill’s rim and the ruff starts to lighten, although still looking quite immature-like compared to adult birds. The fully adult-like appearence (including very pale iris, bill and ruff, and marked terminal band on the secondaries) is not attained until, at least, the 9-10th year of life.
Moult progress in a resident population of Griffon Vultures (all photos taken in late February, Catalonia, N Spain by Guillermo Rodríguez), from left to right: 2cy, 3cy, 4cy, and 5cy. The 2cy bird still sports a neat plumage without much wear. The 3cy bird has moulted the three innermost primaries, but not a single secondary has been replaced. In the 4cy bird, the primary moult has reached p7, and about 50% of secondaries have been moulted. The 5cy bird has completed its first primary moult and started a new front that now reaches p3. All the juvenile secondaries have been replaced too (note that the worn secondaries are second generation feathers: rounded and lacking the characteristic pointed tip of juvenile feathers).
Figure 2. Number of replaced primaries by April in resident (N Spain) and migratory (birds seen crossing the Strait of Gibraltar) Griffon Vultures. The analysis was done in an unsupervised manner (without ageing the birds), but the different age-classes clearly emerge as separate clusters. The average number of replaced primaries in migratory 3cy Griffons roughly lies in between the mean values of resident 3cy and 4cy birds. The distribution of moulted primaries in migratory 4cy overlaps with that of resident 5cy Griffons.
Moult in migratory Griffon Vultures
I have studied the migration of Griffon in the Strait of Gibraltar during the 2021 spring migration, with 3000+ birds seen, of which several hundreds were photographed.
Migratory Griffon Vultures leave the Iberian Peninsula in late autumn of their first calendar year and migrate towards the Sahel (mainly Senegal). Many birds return to Europe already in their 2cy and thus only spend a few months in Africa; but a good proportion remains there during their first one or two years of life, returning in their 3cy or 4cy (or very rarely even older). For those birds that do not return in the 2cy spring, it is unknown whether they remain south of the Sahara during their entire stay in Africa or they wander and reach northern Africa during the 2cy summer (as it seems to be common in Short-toed Snake Eagle, for instance). It seems that very few non-juvenile birds migrate to Africa, meaning they typically make the trip only once in their lifes.
Rüppell’s and White-backed Vultures moult during the entire year, showing a high rate of plumage replacement that allows them to sport a fresh plumage despite the strong sun abrasion at tropical latitudes. Griffon Vultures that migrate to Africa (and all other migratory raptors, actually) also moult in a continuous manner during their stay, and thus they benefit from 12 months of active moult per year. Assuming a similar feather growth rate as in Europe, linear inference suggests that Griffons that stay in Africa will advance the moult progress 1.5 times per year of stay with respect to resident birds from the Iberian Peninsula. It is surprining to check that this simple argument perfectly explains the moult patterns exhibited by Griffon Vultures returning to Europe in spring in the Strait of Gibraltar.
The most common moult state of Griffon Vultures returning from Africa during the spring migration (April) is:
Second calendar year (2cy) birds usually return showing an entire juvenile plumage except for p1 an occasionally p2, which are often replaced before/during migration. This suggests that birds wintering in Africa start their primary moult in early March, around 2-3 months earlier than resident birds of the Iberian Peninsula.
Third calendar year (3cy) birds typically show replaced p1-p6, often moulting p7, and around 3-6 new secondaries. Late migrants (those arriving in June) may show even more advanced moults. The retained juvenile feathers look extremely worn.
Fourth calendar year (4cy) birds have replaced all the juvenile primaries and started a new front in the inner primaries that usually reach p2-p3. All the juvenile secondaries have been replaced too.
Thus the initial prediction about the moult progress proves to be right, and migratory 3cy birds look c.50% more advanced than resident birds of the same age, and for 4cy birds migratory birds have advanced their moult the equivalent to one cycle of moult compared to resident birds, showing the same moult stage as resident 5cy birds.
Moult progress in migratory Griffon Vultures in April (all photos taken in April at Tarifa, Andalucia, Spain by Guillermo Rodríguez), from left to right: 2cy, 3cy and 4cy. Most 2cy arrive without any trace of moult in April and early May, but late migrants in June and July usually do show 1-2 replaced primaries. 3cy birds typically show new p1-p6 and a mix of new and very worn secondaries. 4cy birds have completely replaced all the juvenile flight feathers.
Migratory 2cy Griffon Vultures, June (left) and May (right) (Guillermo Rodríguez). Note that some 2cy arrive at the Iberian Peninsula with 1 or 2 inner primaries replaced, meaning they have started their primary moult a few months before in the winter quarters.
Migratory 3cy Griffon Vultures (all photos taken in May by Guillermo Rodríguez). The number of replaced primaries typically varies between 6 and 7, with several secondaries moulted too. The remaining juvenile remiges look very worn and faded.
Resident 3cy Griffon Vultures, pictures taken in (from left to right) June, July and late August in N Spain (Guillermo Rodriguez). During the 3cy the primary moult of resident birds progresses, typically reaching p6/7 in August, around 4 months later than in migratory 3cy birds. Note the moderate wear of the juvenile feathers as compared to those of the migratory 3cy shown in the previous plate.
Migratory 4cy Griffon Vulture, April, Tarifa, Andalucia, Spain (Javier Elorriaga). This bird shows a slightly retarded moult for its age, actively moulting p10 and only showing two third-generation inner primaries. Griffons are aggresively harassed by local Yellow-legged Gulls when they hit the coast of Tarifa, some of them even falling down to the sea and dying.
Migratory 4cy Griffon Vulture, April, Tarifa, Andalucia, Spain (Guillermo Rodríguez). Another classic example of a 4cy that has replaced the complete set of juvenile primaries and secondaries, and has started a new wave in the inner primaries moulting p1-3. These birds retain a very dark iris but both the bill and the ruff are slighly paler than in juvenile birds.
Challenging ageing
The different moult patterns shown by birds of the same population makes a challenging ageing. Upon arrival to Europe, migratory 3cy Griffons look intermediate between resident 3cy and 4cy. In the case of migratory 4cy, it’s even more complex: their moult stage exactly matches that of resident 5cy, making their ageing nearly impossible if the migratory history of the bird isn’t known (which, obviously, rarely occurs).
To complicate things further, birds that only spend one winter in Africa are usually more advanced than their resident cousins during (at least) the entire 2cy, since seemingly they start the primary moult in Africa in late Feruary/early March, around 2-3 months earlier than resident birds. This fact raises the question of whether the most advanced birds that we see in the Iberian Peninsula correspond to birds that went to Africa in their first year. The same applies in subsequent plumages, with a good number of similar moult patterns expected to be found depending on the migratory history of the bird.
Interestingly, whereas migratory Griffons are considerably more advanced than resident Griffons in terms of moult progress, migratory birds seem to retain signs of immaturity (such as dark bill, ruff, iris) in a similar way as the resident birds, suggesting they aren’t more advanced in terms of hormones/sexual maturity. In addition to subtle differences in the feather condition, this often helps to address whether we are in front of a resident or migratory bird, for instance:
In spring, 4cy resident birds with replaced p1-p8 often show some contrast between those primaries replaced during the 2cy (p1-4) and those moulted during the 3cy (p5-8). In migratory 3cy birds, the wear shows a more uniform gradient, generally without contrasts. Also no migratory 3cy bird shows a second wave at inner primaries.
In spring, 5cy resident birds with replaced p10 and p1-p3 in the inner primaries typically show palish bill and rufous ruff, whereas migratory 4cy with a similar moult pattern look way more juvenile like.
Comparison between a 5cy resident (left) and a 4cy migratory (right) Griffon Vultures (left picture taken in July at Catalonia, N Spain, by Guillermo Rodríguez; right picture taken in April at Tarifa, Spain, by Javier Elorriaga). Note the very similar moult pattern in both birds despite the one-year difference in age. In resident birds, the degree of wear is more homogeneous than in migratory birds, in which recently moulted feathers strongly contrast with older feathers.
Why do vultures show latitude-dependent moult?
Several explanations have been put forward for the different moult strategies of migratory vs resident raptors, often related to differences in diet, such as percentage of cold-blooded prey (Newton in Forsman, 2016). This certainly doesn’t seem to be the case for Griffon Vultures; food availability for Iberian Griffons is quite uniform throughout the year and is arguably similar to what migratory Griffons find in Africa. Hereafter I discuss another explanation that, although I do not have any empiric proof, seems to explain well the phenomenological evidence described for moult in raptors.
The distribution of replaced feathers (Fig. 2) is quite narrow and well-defined (and, although not proven here, it is extremely constant in different years). It therefore seems improbable that the moult timing is related to highly noisy factors such as food or even temperature – there has to be a more deterministic variable driving moult activity. The strong coupling between moult and latitude strongly suggests that moult is somehow triggered or controlled by the sun and, given that moult is such an energetically demanding process, one would tend to think that the sun’s power may be playing a role (Zuberogoitia 2018). This hypothesis suggests there is no active moult below a certain threshold of solar irradiance (for instance, in winter at temperate latitudes) but non-stop, year-round moult can continue in areas with high, constant solar radiation (around the equator). I’m not discussing the molecular mechanisms affected or controlled by the sun; just suggesting that there is a strong correlation between sun irradiance levels and moult in large raptors, likely suggesting causality.
Figure 3. Global irradiance at three relevant locations: Dakar, Barcelona and Stockholm, averaged over the 2005-2015 period. The red line represents a potential ‘threshold‘ value=140kWh/m2 of solar irradiance below which a large raptor might not be able to moult. Source: PHOTOVOLTAIC GEOGRAPHICAL INFORMATION SYSTEM.
This hypothesis is of course notoriously difficult to prove, but it consistently explains most of the phenomenology described in the literature regarding moult in raptors, including the different moult strategy shown by resident and migratory raptors, as well as the different duration (and thus extension) of moult in resident birds at different latitudes. Think of Golden Eagles, for instance, that moult only 3-4 primaries in a cycle in Scandinavia, 5-6 primaries in Spain and 7-8 primaries in southern Morocco & Arabia – and a similar pattern occurs with latitude in North America.
Temperature might be considered as well as another factor driving moult but there are a number of arguments against it. For instance, in Golden Eagles in the Iberian Peninsula there seems to be little or no difference in moult progress between high-elevation and low-elevation birds, despite a considerable difference in temperature. Both solar irradiance and temperature are obviously related so we will not discuss further about this.
To give a more visual explanation of the dependence of sun irradiance with latitude and its potential impact on moult, Figure 3 shows the evolution of solar irradiance across the year at different latitudes. Let’s imagine a raptor species that has a threshold irradiance of 140kWh/m2 below which it does not moult. If the bird spends a year in Senegal, it may be able to moult during the entire year without much constraint. Another individual resident in Spain will enjoy 8 months of moult but in winter it may need to arrest its moult until spring. A third individual in Scandinavia would only moult during the summer months of the year.
There are a lot of guesses here, sure, so hopefully molecular-based studies will shed some light about the factors controlling moult in large birds in the future!
Acknowledgements
I would like to thank Javier Elorriaga and Laura Rollán for joining me on many occasions and patiently wait for Griffons to cross the Strait (sometimes to no avail!). Javi allowed me to post a couple of his magnificent pictures and he has shared with me lots of interesting information about vultures over the years. Laura and Sabrina Hepburn also made invaluable comments on this post that helped to make it more reader-friendly and rigorous from a biological point of view. Also thanks to the Calldetenes-Osona ringing group (GACO) and especially Carles Durà and Roger Jutglà for allowing me to join them and study Griffon Vultures in the hand.
