View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Natural History Museum Repository Title How common is albinism really? Colour aberrations in Indian birds reviewed Authors Van Grouw, H; Mahabal, A; Sharma, RM; Thakur, S Description The file attached is the Published/publisher’s pdf version of the article. How common is albinism really? Colour aberrations in Indian birds reviewed Anil Mahabal, Hein van Grouw, Radheshyam Murlidhar Sharma & Sanjay Thakur eople have always been intrigued by aberrant­ cluding galliforms Galliformes, nightjars Capri­ Ply coloured birds, and therefore sightings of mulgidae, bustards Otididae, owls Strigidae and these individuals are often reported in the litera­ turacos Musophagidae. ture. Contrary to popular belief, birds with a col­ Melanins can be divided into two forms; eu­ our aberration do not necessarily fall victim to melanin and phaeomelanin. Depending on con­ natural predators and often survive for a long time centration and distribution within the feather, (van Grouw 2012). This also increases their chance eumelanin is responsible for black, grey and/or of being seen and recorded by birders. dark brown colours. Phaeomelanin is responsible In general, plumage colour is the result of bio­ for warm, reddish­brown to pale buff colours, de­ logical pigments (biochromes), structural colour pending on concentration and distribution. Both (selective light reflection due to the structure of melanins together can give a wide range of grey­ the feather), or a combination of the two. The two ish­brown colours. In skin and eyes, only eu­ most common pigments that determine plumage melanin is present (Lubnow 1963, van Grouw colour in birds are melanins and carotenoids (Fox 2006, 2013). The development of melanin is the & Vevers 1960, van Grouw 2013). Another pig­ result of a biochemical process in the melanin ment, only found in parrots Psittacidae, is psit­ producing cells, called melanin synthesis. Genetic tacin. Finally, there are the porphyrins which are mutations affecting the presence and distribution relatively rare in birds. of the pigment cells, melanin synthesis or melanin Carotenoids are responsible for colours ranging distribution, and resulting in an aberrant colour, from pale yellow to scarlet red. They cannot be are not uncommon in birds. Besides this, pigment synthesized by the birds themselves but have to disturbance can also be caused by non­heritable, be acquired from their food and transformed into external and often temporary factors like injury, colour pigments by enzymes. Psittacin is also re­ disease, food deficiency (Law 1921, Sage 1962) or sponsible for yellow, orange and red but is not other environmental factors (van Grouw 2013). diet dependent. Porphyrins, which normally pro­ While mutations affecting carotenoid or psittacin duce reddish brown colours, are formed by the are rare, there are many genetic mutations which breakdown of hemoglobin by the liver. They are cause changes in the melanins. In domesticated sporadically found in a variety of bird groups in­ pigeons for example, more than 50 different in­ [Dutch Birding 38: 301-309, 2016] 301 How common is albinism really? Colour aberrations in Indian birds reviewed heritable melanin mutations are known, which In all these publications, a variety of names is cause c 10 distinguishable colour aberrations (van used to identify and classify the pigment abnor­ Grouw & de Jong 2009). The most commonly in­ malities. Albinism, for example, is defined as total heritable aberrations found in wild birds are albi­ or pure, partial, incomplete and imperfect (see no, leucism, brown, dilution, ino and melanism appendix). Terms used for other aberrations are (table 1; for a more detailed description of these mela nistic (blackish), rutilistic (reddish), flavistic see van Grouw 2013). (yellowish), fawn, pale and dark morph, leucistic, isabelline etc. This terminology however, is often Early records and terminology conflicting or incorrect and is therefore confusing. Since the 19th century, many scientific papers Most commonly, the term albino is widely used have dealt with the subjects of plumage colora­ for all sorts of different colour aberrations but in tion, aberration and/or their genetics (eg, M’Callum only a tiny proportion of cases it is used correctly. 1885, Rollin 1962, 1964, Sage 1962, Harrison Partial albino as a term is wrong, as albinos can­ 1963). There has also been a wealth of published not produce melanin pigment at all and therefore observations on individual sightings of colour being partial albino is simply impossible. The true aberrant birds (see appendix, published online at albino aberration is far less often encountered www.dutchbirding.nl/indian_birds_albinism) and than many would suppose. In fact, aberrant white com bined records of aberrant coloration in spe­ feathers are hardly ever caused by albinism; cies of particular countries or regions (eg, Deane usually, it is either a form of leucism or a non­ 1876, 1879, 1880, Sage 1963, Gross 1965ab, Li heritable cause such as progressive greying. et al 2011). However, until now there was no such The most obvious difference between albinism comprehensive compilation of colour aberrations and leucism is in the colour of the eyes: in an recorded from India, a gap filled by this paper. albino these are red, while in leucism the eye 471 Red­whiskered Bulbul / Roodoorbuulbuul Pycno- 472 Red­whiskered Bulbul / Roodoorbuulbuul Pycno- notus jocosus, Nawabganj Bird Sanctuary, Uttar Pradesh, notus jocosus, Palakkad, Kerala, India, 23 March 2014 India, 30 October 2012 (Nandy Soumyajit). Number (Unni Revi). Number 91, leucistic, in appendix. Muta­ 89, partial leucism, in appendix. Progressive greying in tion brown in moderately sun­bleached plumage. This early stage. bird was nesting with normally coloured individual. 302 How common is albinism really? Colour aberrations in Indian birds reviewed TABLE 1 Identification key for naming colour aberrations in birds Aberration Effect on melanins Effect on plumage Remarks colour albino total lack of both melanins in all­white plumage, red eyes albinos are rarely seen in wild feathers, eyes and skin due to and pink feet and bill as their survival chances are heritable absence of enzyme limited due to poor eyesight; tyrosinase in pigment cells most die soon after fledging leucism total lack of both melanins in all­white plumage or all­white white pattern in partial all or parts of plumage and skin feathers next to normal­coloured leucism is often patchy and due to heritable absence of ones (partial leucism); pink bill bilaterally symmetrical; pigment cells in all or parts and feet in the all­white birds pattern is already present of skin and possibly normal­coloured in juvenile plumage and bill and feet in partial leucism does not change with age depending on where pigment cells are missing; always normal­coloured eyes progressive total lack of both melanins in all­white plumage or all­white white feathers not present greying all or parts of plumage (and skin) feathers mixed with normal­ in juvenile plumage; from due to progressive loss of coloured ones; bill and feet onset of this condition, the pigment cells in all or parts of may be affected depending on bird will get increasing skin with age form of progressive greying; number of white feathers always normal­coloured eyes after every moult brown qualitative reduction of normally black parts are brown; plumage with incompletely eumelanin due to incomplete originally reddish/yellowish oxidized eumelanin is very synthesis of eumelanin; brown unaffected sensitive to sunlight and phaeomelanin unaffected therefore bleaches further rapidly to almost (dirty) white dilution quantitative reduction of both normally black parts are plumage looks like pale melanins or eumelanin only silvery grey; originally reddish/ version of their normal yellowish brown is buff/cream counterparts or unaffected ino strong qualitative reduction of normally black parts are very eyesight in ino birds is much both melanins due to incomplete pale brown/cream; originally better than in albino birds synthesis of both melanins reddish/yellowish brown hardly and, therefore, any adult bird visible; eyes pinkish, feet and in the wild with ‘white’ bill pink plumage and reddish eyes is thus ino and not albino melanism abnormal deposit of melanin increase of black and/or reddish in this mutation, there is no (not necessarily an increase brown or altered pattern loss of pigment (quantitative of pigment) reduction) or change in shape and size of melanin granules (qualitative reduction); hence, plumage of melanistic birds is, there­ fore, not obviously aberrant: plumage looks ‘natural’ but different from that of known species Melanin aberrations do not affect carotenoid pigments (yellow, orange and red) which, if present in the relevant species, remain present. 303 How common is albinism really? Colour aberrations in Indian birds reviewed colour is unaffected (note that in many species means always possible. The views of the bird may ‘red’ is the normal eye colour but this is the colour be less than ideal: the bird in the field may be too of the iris only as the pupil is ‘black’; in albinos, far away or is moving too quickly to distinguish the original eye pigmentation is absent and the the aberration in sufficient detail, or the plumage red colour of their eyes, including the pupil, is may already be strongly bleached and no longer caused by blood that is visible through the colour­ shows the original coloration. When trying to less tissue). This seemingly minor difference be­ identify a mutation correctly, it is important to tween albino and leucism is related to the under­ know exactly how the original plumage colour of lying causes of the two aberrations, which are the relevant species should look! Next, try to see actually completely different. An albino has pig­ parts of the feathering that are not strongly ex­ ment cells but is lacking the necessary enzyme to posed to sunlight in order to determine whether start melanin synthesis, whereas a leucistic bird the plumage appears to have been bleached dif­ lacks pigment cells altogether and is therefore un­ ferentially by light.