Australian Field Ornithology 2012, 29, 210–214

Plumage aberrations in Australian birds: A comment on Guay et al. (2012) and Frith & Murphy (2012)

Hein van Grouw

Bird Group, Department of Zoology, The Natural History Museum, Akeman Street, Tring, Herts HP23 6AP, United Kingdom Email: [email protected]

Summary. Colour aberrations in birds are still poorly known among ornithologists, and the terms used to describe such variations are often used inconsistently. Here, I provide further information on aberrations described in Guay et al. (2012: Australian Field Ornithology 29, 23–30) and Frith & Murphy (2012: Australian Field Ornithology 29, 40–44), including a discussion of the ‘brown’ .

I read with interest the articles by Guay et al. (2012) and Frith & Murphy (2012) about colour aberrations published in issue 1, volume 29, of Australian Field Ornithology. Knowledge about this phenomenon is still relatively poor among ornithologists so I am pleased that the authors put the effort into publishing about this subject. Heritable colour aberrations in birds are my main research (see van Grouw 2006, 2010; van Grouw & de Jong 2009), and through the years I have learnt that the identifying and naming of colour aberrations still present a problem in the ornithological world. A variety of names is seemingly randomly used, now and in the past, to identify the . Most commonly and most often wrongly applied are the names ‘albino’ or ‘partial albino’. These names are widely used for all sorts of different colour aberrations, but in only a few cases is ‘albino’ used correctly. Because of the genetic mutation, an ‘albino’ is unable to produce pigments at all. The Laughing Kookaburra Dacelo novaeguineae pictured in Plate 4 in Guay et al. (2012) is therefore not an ‘albino’. Its bill and feet clearly still contain some melanin as there is still a light horn colour visible. Also, melanin is still clearly present in the eyes. In my opinion this Kookaburra is an ‘ino’, defined as a strong qualitative reduction of both (i.e. black eumelanin and brownish phaeomelanin) [van Grouw 2006, 2010; van Grouw et al. 2011; see also Figure 1a (normal House Sparrow Passer domesticus) compared with Figure 1b (ino House Sparrow)]. A mostly white bird which nevertheless shows some form of melanin pigmentation is never an ‘albino’, by definition. Therefore ‘partial albino’ does not exist and is a contradiction in terms. This latter name is often used for what is in fact ‘leucism’. Leucism, from the Greek leukos (= white), can be defined as the lack of melanin pigments from all or parts of the plumage (and skin) (van Grouw 2011). The lack of pigment is due to the congenital and heritable absence of pigment cells from some or all of the skin areas where they are normally present and where they normally provide the growing feathers with pigment. Depending on the sort of leucism, the number of white feathers can vary from only a few Plumage aberrations: Comment on Guay et al. (2012) and Frith & Murphy (2012) 211

a d

b

e

c f

Figure 1. Adult female House Sparrows in fresh plumage. Photos: P. van den Hooven. (a) normal. (b) ‘ino’. The synthesis of both melanins is incomplete, resulting in very pale phaeomelanin and very light brown eumelanin, so plumage pattern remains vaguely visible. However, the remaining colour is very light sensitive and the plumage will bleach quickly to white. (c) ‘brown’. Because of the incomplete eumelanin synthesis, plumage that should be black will be dark brown and dark-brown plumage will be light brown; phaeomelanin (reddish brown) is not affected. Incompletely oxidised eumelanin is very sensitive to light and the plumage will soon be bleached. (d) ‘diluted’. In this form of dilution the quantity of only the eumelanin is reduced but the phaeomelanin is unaffected. Parts of the plumage that should be black and dark brown will be grey. (e) ‘diluted’. This is genetically the same mutation as in (d), but in this individual the reduction of eumelanin is almost complete and therefore it can been seen as schizochroism. Note that eumelanin is still present in the eyes, beak and feet. (f) ‘diluted’. This is a form of dilution in which both eumelanin and phaeomelanin are reduced in quantity. Plumage that should be black or dark brown appears grey, and plumage that should be reddish brown appears cream. 212 Australian Field Ornithology H. van Grouw

(= partial leucistic) to totally white individuals. The totally white individuals always have colourless skin as well. Partial leucistic birds can have normal-coloured bill and feet, depending on where the colourless patches occur on the body. However, leucistic birds always have coloured eyes. The white pattern in leucistic birds is already present in the juvenile plumage, and the pattern is often symmetrical due to the way the pigment cells migrate from their embryonic origin into the rest of the body. Certain areas of the body are therefore not provided with pigment cells, which results in pigmentless feathers in these areas, hence to the appearance. In leucism, the pattern and the number of white feathers do not change with age. However there are other, and far more common, causes for pigmentless feathers. Whereas leucism is congenital, ‘progressive greying’ (including ), for example, is a progressive condition that arises after the bird reaches a certain age. ‘Progressive greying’ is defined as ‘the progressive loss of pigment cells with age’. From the onset of the condition, the bird will gain an increasing number of white feathers after every moult. In the early stages, these are usually randomly spread all over the bird, but finally the entire plumage will become white. ‘Progressive greying’ may or may not be heritable; some forms may be related to age, whereas in others the progressive loss of pigment cells may be due to disorders such as vitiligo. Lastly, external, non-heritable factors can also be the reason for loss of pigment. Poison or food deficiency are the main causes, and mostly the pigmentation will become normal as soon as these external causes are removed. True ‘leucism’ (the congenital and heritable absence of pigment cells) is quite rare in wild birds. ‘Progressive greying’, on the other hand, is in general more common, and even very common in particular species. Guay et al. (2012) believe that ‘progressive greying’ (vitiligo) and leucism are the same, which results in their statement that ‘leucism’ is the commonest plumage aberration in wild birds. However, not properly distinguishing the nature of the different aberrations, and therefore applying incorrect names to them, may give wrong indications about the real occurrence of certain aberrations. Probably the most common mutation in birds is ‘brown’. However, in the literature this mutation is given many different names: ‘albino’, ‘partial albino’, ‘cinnamon’, ‘leucistic’, ‘isabella’, ‘fawn’, ‘pale morph’, ‘non-eumelanic form’, ‘flavistic’, ‘erythristic’ and ‘schizochroistic’ are but a few. However, these terms are also regularly used for ‘dilution’. In short, there is confusion on all sides. This means that, without a clear photograph, records of aberrant coloration in certain species are often unreliable because of the incorrect identification and/or naming of the mutation involved. The brilliant photographs in the article by Frith & Murphy (2012) show clearly that the aberrant coloration of the Satin Bowerbird Ptilonorhynchus violaceus was due to the mutation ‘brown’. The mutation ‘brown’ is defined as ‘a qualitative reduction of eumelanin’ (van Grouw 2006, 2010; van Grouw et al. 2011). In this mutation, the number of eumelanin pigment granules remains unchanged but the appearance of the pigment is changed: the eumelanin Plumage aberrations: Comment on Guay et al. (2012) and Frith & Murphy (2012) 213 synthesis process is incomplete as the eumelanin is not fully oxidised. As a result, the pigment will not become black but will remain dark brown, although the quantity of pigment remains the same. The phaeomelanin, where it is present in the relevant species, is unaffected (e.g. see Figure 1c). It is a pity that Guay et al. (2012) have not included the mutation ‘brown’ in their review, as ‘brown’ is the most common heritable colour aberration in birds. It is caused by a single genetic mutation, which is the same in every bird species. ‘Brown’ is always sex-linked recessive in inheritance, which means that a ‘brown’ individual with normal-coloured parents is always a female. In the past, ‘brown’ was often erroneously called ‘schizochroism’ as it was thought to be caused by the absence of black pigment (eumelanin) while the brown pigment (phaeomelanin) remained unchanged. Were this indeed the case, however, then the plumage of a crow affected by the ‘brown’ mutation would be white, as phaeomelanin is not present in corvids. A ‘brown’ crow, however, is dark brown due to the incompletely oxidised eumelanin, so feathers that should have been black will be dark brown. In many species, eumelanin that is not fully oxidised is part of the original plumage colour as, for example, in the dark-brown remiges and rectrices in the female Satin Bowerbird of Frith & Murphy (2012). So in these cases, as a result of the mutation ‘brown’, the feathers that would normally be dark brown will be light brown, because the eumelanin will be less oxidised than in the normal coloration. Aberrations due to incompletely oxidised eumelanin are very sensitive to sunlight and will bleach quickly and strongly. That is why the outer edges of the primaries and secondaries of Frith & Murphy’s (2012) Satin Bowerbird were lighter in colour, as these parts are always exposed to light, even in a closed wing. In Plate 10 of Frith & Murphy (2012), the Bowerbird shows parts of the wing plumage that are normally less exposed to sunlight, and therefore these parts still show the proper effect of the mutation ‘brown’ without any external bleaching effects. The Welcome Swallow Hirundo neoxena pictured in Plate 7 of Guay et al. (2012) is also a typical example of ‘brown’ that is bleached further by the light. As the plumage coloration due to the mutation ‘brown’ is very sensitive to sunlight (and therefore old plumage is often almost white), it is sometimes hard to distinguish this aberration in the field. For a correct identification, look for parts of the plumage that should be less influenced by sunlight, such as the inner webs of flight-feathers when the bird is opening its wings (as the Satin Bowerbird is in Plate 10 of Frith & Murphy 2012). Lastly, I would like to mention that Guay et al. (2012) have quoted my 2006 paper (van Grouw 2006) incorrectly in their review. Under the heading ‘Schizochroism’, it is suggested that I stated that non-eumelanic schizochroistic birds have red eyes and pink skin. However, I neither said that nor is it true either. Indeed, eumelanin is the only melanin present in eyes and skin (although carotenoids are often also present), but the embryonic origin of eye melanin pigments is different from that of the rest of the body: eye pigments originate mainly from cells in the outer layer of the optic cup whereas the pigment cells for the rest of the body originate from the neural crests. As most colour mutations affect only the melanins originating from the neural crests, schizochroism has no influence on eye colour. The term 214 Australian Field Ornithology H. van Grouw schizochroism strictly means the total lack of only one of the two types of melanin. However, mutations causing this are very rare; in most cases the affected melanin is not completely eliminated in the plumage and the skin may be even less affected, resulting in the bill and feet still being coloured (see Figures 1d–e, for example). Therefore nowadays, I prefer to include mutations formerly called schizochroism among the many different dilution mutations, as the total lack of one melanin is nothing more than the most extreme end of the degree of dilution. Dilution is defined as a quantitative reduction of one or both melanins (van Grouw 2006, 2010; van Grouw et al. 2011; see also Figure 1f). The purpose of this comment is to share information and opinions to reach a better understanding of colour aberrations in birds in general. Read in conjunction with Guay et al. (2012) and Frith & Murphy (2012), it is hoped that this comment provides further information for ornithologists describing plumage aberrations in Australian birds.

References Frith, C.B. & Murphy, T. (2012). A pale ‘cream’ Satin Bowerbird Ptilonorhynchus violaceus (Family Ptilonorhynchidae): First documented evidence of aberrant plumage in any bowerbird. Australian Field Ornithology 29, 40–44. Guay, P.-J., Potvin, D.A. & Robinson, R.W. (2012). Aberrations in plumage coloration in birds. Australian Field Ornithology 29, 23–30. van Grouw, H. (2006). Not every white bird is an albino: Sense and nonsense about colour aberrations in birds. Dutch Birding 28, 79–89. van Grouw, H. (2011). Lappet-faced Vultures with white feathers. Vulture News 60, 13–14. van Grouw, H.J. (2010). How to recognize colour aberrations in birds (in museum collections). Journal of Afrotropical Zoology Special Issue, 53–59. van Grouw, H.J. & de Jong, J. (2009). Genetics in the Pigeon, Modern Mendelism and More for the Pigeon Fancier. Nederlandse Bond voor Sierduivenliefhebbers, Surhuisterveen, The Netherlands (in Dutch). van Grouw, H.J., Russell, S. & Merne, O.J. (2011). Notes on colour aberrations in Common Guillemot Uria aalge and Northern Gannet Morus bassanus. Seabird 24, 33–41.

Received 25 May 2012