First Documented Records of White Plumage Aberration in the White-necked Thrush (Turdus albicollis)

First Documented Records of White Plumage Aberration in the White-necked Thrush (Turdus albicollis) Author(s): Jimi Martins-Silva, Maurício B. Vecchi, and Maria Alice S. Alves Source: The Wilson Journal of Ornithology, 128(4):931-935. Published By: The Wilson Ornithological Society DOI: http://dx.doi.org/10.1676/15-133.1 URL: http://www.bioone.org/doi/full/10.1676/15-133.1 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

SHORT COMMUNICATIONS 931 The Wilson Journal of Ornithology 128(4):931 935, 2016 First Documented Records of White Plumage Aberration in the White-necked Thrush (Turdus albicollis) Jimi Martins-Silva, 1,2 Maurício B. Vecchi, 2 and Maria Alice S. Alves 2,3 ABSTRACT. Aberrations of plumage coloration are caused by hereditary and environmental factors and are not rare in wild birds, but few studies have estimated their frequency in natural populations. Here, we provide the first report of a white plumage aberration in an insular population of the White-necked Thrush (Turdus albicollis) on Ilha Grande, in southern Rio de Janeiro state, Brazil. Four (two males and two females) of the 123 individuals examined in 2013 2015 presented unusual white feathers on some part of the body (especially the hindneck), which may represent progressive graying or the result of injury. The frequency of the white plumage aberration recorded in our study (3.25%) is approximately three times higher than that expected in natural bird populations, and three of the four aberrant individuals were captured in the most disturbed forest site sampled. Further studies will be necessary to identify the true causes of the high frequency of white plumage aberrations detected in the study population, which may include diet, longevity, behavior, parasitism or other environmental factors. Received 5 August 2015. Accepted 14 February 2016. Key words: Atlantic forest, body injury, island, progressive graying, Turdidae, white feathers, wild populations. In birds, plumage coloration results from the combination of different pigments, of which the most common is melanin (van Grouw 2006). Most bird species present two types of melanin at different concentrations: eumelanin, responsible for the blackish appearance of feathers, skin and eyes, and pheomelanin, associated with the reddishbrown coloration of the feathers (van Grouw 2006). Plumage color aberrations are not rare in wild birds (Michener and Michener 1936, Sage 1963, Hosner 1 Programa de Pós-Graduação em Ecologia e Evolução, Universidade do Estado do Rio de Janeiro, Pavilhão Haroldo Lisboa da Cunha, Sala 224, Rua São Francisco Xavier, 524, Maracanã, 20550-011, Rio de Janeiro-RJ, Brazil. 2 Departamento de Ecologia, Universidade do Estado do Rio de Janeiro, Pavilhão Haroldo Lisboa da Cunha, Sala 220, Rua São Francisco Xavier, 524, Maracanã, 20550-011, Rio de Janeiro-RJ, Brazil. 3 Corresponding author; e-mail: masaalves19@gmail.com and Lebbin 2006) and can be caused by several factors (Summers and Kostecke 2004), such as diet, parasites, disease, injury, mutation, and age (Guay et al. 2012). A deficiency or excess of specific components of the diet can cause plumage aberrations (Guay et al. 2012), such as a deficiency of lysine, for example, which can cause whitish plumage (Fritz et al. 1946). Under both natural and experimental conditions, endo- and ectoparasites have been observed to affect the deposition of pigments in growing feathers (Thompson et al. 1997, Brawner et al. 2000). Injuries may also induce the appearance of aberrant plumage in the area surrounding the affected body region, although the mechanism of this response has not yet been identified (Phillips 1954). Aberrations that cause white feathers can be classified as albinism, schizochroism, leucism, and progressive graying (van Grouw 2006, 2012b, 2013; Cieslak et al. 2011), although chromatic aberrations have been misidentified frequently in the literature. For example, Ferrer-Sánchez and Rodríguez-Estrella (2014) misidentified a Turkey Vulture (Cathartes aura) as a partial albino, which is not a valid category of chromatic aberration (van Grouw 2006). In this individual, 70% of the remiges of the left wing were white, and probably represented progressive graying or the consequences of a local injury. Albinism is the total loss of both types of melanin in the whole body. The plumage of albino birds is completely white, the eyes are pink, and the skin is pale, but carotenoid is retained in the feathers (van Grouw 2006). This aberration generates visual problems and low activity rates (Lee and Keeler 1951), which may account for the rarity of wild adult birds with this plumage abnormality (van Grouw 2012b, 2013). Schizochroism is the total loss of one type of melanin (van Grouw 2006). In this case, the melanin of bird eyes has a distinct embryonic origin (cells in the outer layer of the optic cup) from that of the rest of the body (neural crests in the body). As most color mutations affect only the melanin originated from the neural crests,

932 THE WILSON JOURNAL OF ORNITHOLOGY Vol. 128, No. 4, December 2016 the color of bird eyes is not affected by schizochroism (van Grouw 2012a). Leucism is the complete absence of both types of melanin in part or all of the plumage and skin (van Grouw 2012b). Leucistic birds may have variable proportions of white feathers, but usually have pigmented eyes. In extreme (100%) cases of leucism, the individual also lacks melanin in its skin, beak, and bare horny parts (van Grouw 2006, 2012b, 2013). Progressive graying is an age-dependent process involving the gradual loss of pigment cells over time, which leads to the progressive loss of the coloration of the feathers (van Grouw 2013). This aberration has been frequently misidentified as leucism (van Grouw 2012a). White color aberrations (originally termed leucism ) are generally found in,1% of the individuals in bird populations in natural areas (Sage 1962, Bensch et al. 2000), and 1 2% in urban areas (Il enko 1960 apud Møller and Mousseau (2001). Here, we provide the first documented records of white plumage aberrations in the White-necked Thrush Turdus albicollis (Vieillot, 1818), a Neotropical forest species distributed throughout Central and South America between Mexico and Uruguay. The species is common in most of the Amazonian and Atlantic forests of Brazil (Collar 2005). METHODS Our samples were collected in 11 field trips conducted between June 2013 and May 2015, during a long term mist-netting/banding study of wild birds (permits: CEMAVE/ICMBio no. 1237, INEA no. 051/2011, SISBIO 14210-7) in the Ilha Grande State Park (approximate coordinates 238 10 0 S, 428 11 0 W; datum WGS 84). This park covers ~60% of Ilha Grande, a 19,300-ha oceanic island in the municipality of Angra dos Reis, between 2.3 km (min) and 22 km (max) off the mainland in southern Rio de Janeiro state, Brazil. Birds were collected in mist-nets set at 11 sites in the Atlantic rainforest, mostly old secondary growth. The mist-netted White-necked Thrushes were all banded and examined visually for changes in the color pattern of the plumage, tarsi, beak and eyes, and subsequently released at the capture site after ~30 mins. As this species is not sexually dimorphic in plumage, samples of 20 50 ll of blood were collected from individuals with aberration plumage via the tarsal or brachial veins using non-heparinized microcapillary tubes (50 ll) for molecular sexing. The blood samples were stored in plastic 1.5ml Eppendorf tubes with absolute ethanol. Sex molecular identification was conducted using the CHD gene technique, using the P2 and P8 primers developed by Griffiths et al. (1998), following Ritter et al. (2003). RESULTS We captured and examined 123 White-necked Thrushes (all adults), of which, four presented abnormal white feathers on some part of the body, especially the hindneck. Three aberrant individuals were captured at the edge of a disturbed forest near a village (Vila Dois Rios). This site was sampled during 3 days of fieldwork, when 34 thrushes were captured. The first thrush was captured on 22 July 2014, and was a female with white spots on the secondary remiges of the left wing and the hindneck (Fig. 1a). At the same site, we captured two aberrant individuals on the 4th (male) and 5th (female) of March 2015 (Figs. 1b c). A male with a white feather in the hindneck (Fig. 1d) was captured within a primary forest 4 km north of Vila Dois Rios on 19 August 2014. DISCUSSION The four aberrant White-necked Thrushes sampled on Ilha Grande all had abnormal white feathers but normally-colored eyes, beak, tarsus, and skin to indicate the effects of progressive graying or injury. In the New World, white color aberrations have been reported previously in at least four Turdus species from North America (Johnston 1947; Dexter 1949, 1957; Gross 1965) and South America (Henry 2005, Rodríguez- Pinnilla and Gómez-Martínez 2011), including the Rufous-bellied Thrush (Turdus rufiventris) in Brazil (Gonçalves et al. 2008). In some of these reports, the term albinism was used erroneously, given that the birds presented beak, tarsus, and eyes of normal color. To date, the only known report of a color aberration in the White-necked Thrush is Helmut Sick s (Sick 2001:700) reference to a female with a cinnamon mutation, which appears to be consistent with the brown

SHORT COMMUNICATIONS 933 FIG. 1. The four Adult White-necked Thrushes with white plumage aberrations captured between June 2014 and March 2015 on Ilha Grande, Rio de Janeiro, Brazil. Photos by J. Martins-Silva. aberration defined by van Grouw (2006), a sexlinked recessive mutation, which is among the most widespread mutations in birds (van Grouw 2013). Our records from Ilha Grande thus represent the first documented case of a white plumage aberration in a population of White-necked Thrushes, in which a frequency of 3.25% was recorded, a rate more than three times the highest value recorded typically (1%) in natural bird populations (Sage 1962, Bensch et al. 2000). Three of the four aberrant individuals were captured in the most disturbed forest sampled, adjacent to a small 10-ha village (Vila Dois Rios). White-necked Thrushes are rarely observed in open areas (Collar 2005), and Turdus albicollis is the most forest-dwelling of the five Turdus species found on Ilha Grande (Alves and Vecchi 2009). In this case, the forest surrounding Vila Dois Rios may be subject to anthropogenic effects similar to those of urban areas, which might result in a higher frequency of white color aberrations in the local birds (Il Enko 1960 apud Møller and Mousseau (2001). If we consider only the White-necked Thrushes captured in the vicinity of Vila Dois Rios (n ¼ 34, three field trips), the frequency of the aberration would reach 8.82% of the sample population, a relatively extreme value. Color plumage aberrations are usually associated with a number of different genetic mutations (van Grouw 2006). As albinism and leucism are not caused by sex-linked genes, no sexual difference would be expected. However, progressive graying may be sex-biased in some species. In the House Sparrow (Passer domesticus), for example, this

934 THE WILSON JOURNAL OF ORNITHOLOGY Vol. 128, No. 4, December 2016 condition appears to be more common in females than in males (van Grouw 2012b). In a previous mist-netting study of Whitenecked Thrushes on Ilha Grande, Ritter et al. (2003) recorded a male-biased sex ratio (2.4:1; n ¼ 74). The proportion of females with the white plumage aberration recorded in the present study (1:1) was thus much higher than expected for the population at Ilha Grande, based on mist-netting data. Somatic mutations associated with increasing age may also lead to plumage color aberrations (Hanson 1949, Warner 1963), although in this case, the unpigmented feathers are typically distributed randomly on the head, back, and flanks (van Grouw 2013). Although the individuals captured in our study were all clearly adult, we could not estimate their exact age and, it was thus impossible to associate the occurrence of aberrant plumage with age. As we detected white feathers on the heads of all the aberrant individuals captured, and one of them had white feathers asymmetrically distributed on one of the wings, it is possible that the observed condition was progressive graying, a fairly common aberration in birds (van Grouw 2012b), even though it has not yet been reported in Whitenecked Thrushes. It is possible that our findings on color aberrations in White-necked Thrushes reflect injuries to the birds, given that the white feathers were invariably concentrated at the back of the head and neck; however, there are no clues to the possible causes of any such injuries. More detailed studies of the diet, longevity, behavior, and parasitism of the population of Turdus albicollis from Ilha Grande will be required before the underlying causes of the high frequency of individuals with white plumage aberrations can be identified more conclusively. ACKNOWLEDGMENTS We thank the Brazilian National Science Council (Conselho Nacional de Desenvolvimento Científico e Tecnológico - CNPq) for a scholarship (proc. 305798/ 2014-6) and the Carlos Chagas Filho Rio de Janeiro State Research Foundation (Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro - FAPERJ) for a grant (proc. E-26/102.837868/2012) to MASA. Denise M. Nogueira, Flávia G. Chaves, and Keila F. Henud helped with the molecular sex identification. The Rio de Janeiro State Environment Institute (INEA) and the UERJ Center for Environmental Studies and Sustainable Development (Centro de Estudos Ambientais e Desenvolvimento Sustentável CEADS/UERJ) provided logistic support. 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