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Revista Brasileira de Ornitologia, 22(3), 251-259 ARTICLE September 2014 Age and gender related plumage variation of psittacofulvine pigments: the case of the Yellow-faced Parrot Alipiopsitta xanthops 1, 2, 4 3 Carlos Barros de Araújo and Luiz Octavio Marcondes-Machado Programa de Pós-graduação em Ecologia, Instituto de Biologia, Unicamp. Current address: Universidade Federal da Paraíba, Centro de Ciências Exatas e da Natureza - Campus I. Departamento de Sistemática e Ecologia, CEP 58059-900, João Pessoa, PB, Brazil. Departamento de Biologia Animal, Instituto de Biologia, Unicamp, CP 6109, CEP 13083-970, Campinas, SP, Brazil. Corresponding author: firstname.lastname@example.org Received on 22 October 2013. Accepted on 24 September 2014. ABSTRACT: The Yellow-faced Parrot Alipiopsitta xanthops presents considerable phenotypic variation with a belly coloration that may vary from green to yellow-red. Though it has been hypothesized that this variation could be related to sex or age, these possibilities remain untested. We therefore tested these hypotheses by verifying geographical, sexual, and age-related trends in coloration based on museum specimens, wild populations, and captive developing juvenile birds. We found colored belly parrots (CBP) throughout the species distribution of A. xanthops. We found no diﬀerences in the proportion of CBP individuals between the two wild populations sampled (overall mean of 8.7%), but the proportion of CBP in museums was higher (32%) indicating that specimens were probably not randomly collected. We also found a skewed sex ratio in museums, as females represented only 25% of the specimens. We found that 37% of museum males had colored bellies, in contrast with only 18% of females; furthermore, colored bellied males presented a greater area of yellow-red patch on their bodies. None of the 16 observed ﬂedglings presented colored bellies. The yellow head coloration slowly grew over the 14 days of observation of 16 nestlings. Together, our results suggest that color variation in the Yellow- faced Parrot seems to be related to both age and gender. KEYWORDS: Arinii, dichromatism, feather coloration, morphology, Psittacidae, sexual dimorphism. INTRODUCTION carotenoids (the pigments responsible for similar colors in most avian species), which are obtained through the Among the myriad explanations for bird plumage variation, diet, psittacofulvins seem to be endogenously produced. sexual selection is the most studied (Savalli 1995). Plumage Parrots are very unlikely to absorb the pigments directly from diet, especially if we consider that no pigment was may convey information that could be used by females to choose a high quality partner (Fitzpatrick 1998; Perrier et found in blood samples of 44 Psittacidae species (McGraw al. 2002; Siitari & Huhta 2002; Saks et al. 2003; Masello & Nogare 2005), or that most species maintain their color et al. 2004). However, there are alternative hypotheses to in captivity despite diet restrictions (Nemesio 2001). explain the remarkable plumage variation found in birds. Sexual plumage dimorphism or dichromatism is not common in Psittacidae, but it may be observed in For instance, feather coloration may be used for individual recognition (Whitﬁeld 1986, 1987; Rohwer & Røskaft some parrot species. For instance, males of the Blue- 1989), ﬂock cohesion (Røskaft & Rohwer 1987; Selander winged Parrotlet (Forpus xanthopterygius) exhibit primary & Hunter 1960), species recognition (Sibley 1957; Pierotti and secondary violet-blue wing-coverts (Forshaw 1989); 1987), or dominance relationships (Rohwer 1977, 1985; males of the Burrowing-parrots (Cyanoliseus patagonus) are slightly larger and exhibit larger red patches on their chest Parsons & Baptista 1980; Fugle et al. 1984; Ryan et al. 1987; Holberton 1990). (Masello & Quillfeldt 2003); males of the Blue-bellied Unlike most birds that sediment carotenoid- Parrot Triclaria malachitacea exhibit a bluish-violet bely based compounds on their feathers, most Psittacidae (that may turn red as they age), and males of the Red- derive their yellow-red coloration from psittacofulvins, capped Parrot Pionopsitta pileata exhibit a conspicuous red crown (Sick 1997). But what would be the roles of a family of lipochromes pigments found exclusively within the family (McGraw & Nogare 2005). Unlike such a conspicuous plumage among parrots? Age and gender related plumage variation of psittacofulvine pigments: the case of the Yellow-faced Parrot Alipiopsitta xanthops Carlos Barros de Araújo and Luiz Octavio Marcondes-Machado It has been shown that plumage may vary according among distinct localities. This was accomplished through to body-condition in Cyanoliseus patagonus, as feathers a comprehensive analysis of specimens found in museums reﬂect body-condition during feather development worldwide, ﬁeld observations, as well as the study of (Masello et al. 2004). Furthermore, the size of the red captive juveniles. patch exhibited by males is positively correlated to body condition, and males with large red patches will produce higher quality oﬀspring. Hence, plumage coloration METHODS seems to be a reliable signal of body condition that indicates higher male ﬁtness accurately (Masello & We obtained a total of 109 ventral photographs of Quillfeldt 2003). Biogeography may also lead to plumage parrot specimens from worldwide museum collections. diﬀerences, as isolated populations could be under However, here we used only the ones that presented distinct selection pressures ultimately leading to distinct gender classiﬁcation, so that our analysis was restricted to 65 pictures / specimens. Additionally, we used pictures plumage patterns. In fact, the Cuban Amazon (Amazona leucocephala) exhibits plumage variation among diﬀerent of 16 chicks from the Mato Grosso do Sul rehabilitation island populations (Reynolds & Hayes 2009). However, center (“Centro de Reabilitação de Animais Silvestres” - plumage dichromatism has not been properly addressed CRAS/MS). All specimens measured in this study (n = among parrot species, leading to many competing 81) are listed in Table 1. We used pictures to classify adult parrots (n = 65) hypotheses related to age, gender, genetic, or ecological explanations (Sick 1997, Masello et al. 2004). according to the amount of yellow/reddish coloration The Yellow-faced Parrot (Alipiopsitta xanthops) is in their bellies. If the yellow patch covered the belly a comparatively small species (27 cm) (Sick 1997) that completely the specimens were classiﬁed as color- presents remarkable plumage variation. It has orange bellied parrots (CBP); if they were green or presented incomplete yellow/reddish patches on their bellies, the ear-coverts and a variable amount of yellow on the head (Miranda-Ribeiro 1920). The belly coloration varies specimens were classiﬁed as non color-bellied parrots from green to conspicuous yellow/orange/red (Forshaw (non-CBP). Additionally, we created a plumage index 1989; Sick 1997). The species has a wide distribution (I) that is given by the relative ratio of the longitudinal throughout the Cerrado in central Brazil, from southern length of the colored patch on the center of the ventral region divided by the total body length (Figure 1; Maranhão and Piauí States, throughout Goiás, Tocantins, Mato Grosso, Mato Grosso do Sul, western Bahia, and Index (I) = Color patch length/ body length). All northern São Paulo as well as Bolivia (Sick 1997). Despite measurements were made through the pictures with the its wide distribution and high local abundance, the help of software ImageJ. To test for index diﬀerences biology of A. xanthops began to be studied only recently between sexes, we used a unilateral Fischer exact test, as it is expected that males should exhibit higher indexes (Bianchi 2009; de Araújo & Marcondes-Machado 2011; de Araújo et al. 2011, 2014; Dias 2011). However, none as dichromatism (when present) as veriﬁed in other of these previously published studies describes the species’ parrot species such as Forpus xanthopterygius, Cyanoliseus plumage variation, in spite of the role it may have on the patagonus, Triclaria malachitacea, and Pionopsitta pileata species’ biology (e.g. Masello & Quillfeldt 2003; Masello (Forshaw 1989, Sick 1997, Masello & Quillfeldt 2003). We used the Ornithological Gazetteer (Paynter & et al. 2004; Heinsohn et al. 2005; Hill 2006). Authors disagree on the cause and form of the Traylor 1991) to geo-reference specimens and build a Yellow-faced Parrot’s color variation. Some authors map of colored belly occurrences along the Yellow-faced simply inform of the variation (Perlo 2009, Antas et al Parrot’s distribution. 2009, Sigrist 2009), while others relate it to age (Collar Weekly pictures from the CRAS/MS allowed for observations of nestling development (n = 16 individuals) 1997, Erize et al. 2006, Mata et al. 2006, Juniper & Parr 1998, Forshaw 1989, Sick 1997) or sex (Sick 1997, for a period of 21 days. Pictures were taken ventrally (in Collar 1997). Still, all these studies have in common order to observe the presence of yellow coloration on the an anecdotal approach, without a formal or systematic belly), and laterally (in order to allow for observations approach to elucidate or diﬀerentiate between competing of the size of the mask, and the presence of the orange patch over the ears). Nestlings were classiﬁed following hypotheses. As a consequence, contradictory information may be found in the literature (i.e. Alderton 1991, which the categories described above (CBP or non-CBP). states that sexes actually exhibit similar plumage and no During 2005, we studied wild populations of the dichromatism at all). Yellow-faced Parrot in Cerrado fragments of the “Cana We aim to test whether Yellow-faced Parrot’s do Reino” stream (Vicente Pires – DF, Central Brazil; 146 parrots in 9 ﬂocks). In September of the same year plumage variation is 1) age-related, that is, if juveniles present distinct plumage when compared to adults; 2) we took a 20-day ﬁeld trip to the Emas National Park gender related; or 3) geographically-related, varying (southern state of Goiás, Brazil), where we observed the Revista Brasileira de Ornitologia, 22(3), 2014 Age and gender related plumage variation of psittacofulvine pigments: the case of the Yellow-faced Parrot Alipiopsitta xanthops Carlos Barros de Araújo and Luiz Octavio Marcondes-Machado color bellies of 61 parrots from 7 distinct ﬂocks. Overall, populations. Even though some individuals could be we observed 207 parrots in 16 ﬂocks in the wild at both recounted, we expect that our ﬁnal estimation represents localities. We classiﬁed the plumage of the individuals a value very close to what may be found in these areas. observed in the ﬁeld as CBP or non-CBP, following the Additionally, we made the observations on distinct criteria above described. We were thus able to determine days and (as much as possible) in distinct areas, further the proportion of colored bellied individuals in both wild reducing the possibility of overlapping parrot counts. FIGURE 1. Top: some of the variation found in colored bellied parrots. A and B represent the measurements needed to calculate the plumage index (I) given by I = A/B. Parrot 3 is an example of a yellow neck parrot. (Picture by Dr. Ernst Bauernfeind, Naturhistorisches Museum Wien). Bottom left: an adult Alipiopsitta xanthops showing the orange ear-covert. Bottom right: an A. xanthops nestling with a small yellow mask, and no orange ear-covert. Revista Brasileira de Ornitologia, 22(3), 2014 Age and gender related plumage variation of psittacofulvine pigments: the case of the Yellow-faced Parrot Alipiopsitta xanthops Carlos Barros de Araújo and Luiz Octavio Marcondes-Machado TABLE 1. Specimens of Alipiopsitta xanthops examined in this study. Voucher Institution Sex Index number Academy of Natural Sciences, Philadelphia, USA (ANSP) 170759 F 0.23 American Museum of Natural History, New York, USA (AMNH) 174597 F - AMNH 241824 M - AMNH 241825 F - AMNH 241826 M 0.24 AMNH 475312 M 0.27 Coleção Ornitológica Marcelo Bagno, Brasília-DF (COB) 404 M - COB 285 M - COB 281 M - COB 282 M - Field Museum of Natural History, Chicago, USA (FMNH) 46971 M - FMNH 46972 M - FMNH 350841 M 0.24 Forschungsinstitut Senckenberg, Frankfurt, Germany (SMF) 26282 M 0.26 Louisiana Museum of Natural History, Baton Rouge, USA (LSUMNS) 64937 F - LSUMNS 166429 M - Museu de Zoologia da Universidade de São Paulo, São Paulo (MZUSP) 4330 M 0.27 MZUSP 5078 F - MZUSP 5079 M - MZUSP 13107 M - MZUSP 17098 M - MZUSP 17100 M 0.35 MZUSP 30161 M 0.31 MZUSP 30162 M 0.22 MZUSP 30163 M - MZUSP 30164 M - MZUSP 30165 M 0.24 MZUSP 30166 M 0.29 MZUSP 30167 F - MZUSP 35030 M - MZUSP 35031 M - MZUSP 5081 M - Naturhistorisches Museum Wien, Vienna, Austria (NHMW) 44930 M 0.54 NHMW 41146 F - NHMW 41141 M 0.31 NHMW 41142 M - NHMW 41144 M - NHMW 41145 F - NHMW 41146 M - NHMW 41147 M (Immature) - NHMW 41148 F 0.12 NHMW 41149 M 0.20 Revista Brasileira de Ornitologia, 22(3), 2014 Age and gender related plumage variation of psittacofulvine pigments: the case of the Yellow-faced Parrot Alipiopsitta xanthops Carlos Barros de Araújo and Luiz Octavio Marcondes-Machado Voucher Institution Sex Index number Museu Paraense Emílio Goeldi, Belém (MPEG) 14810 M - MPEG 15589 M 0.27 Museu Nacional da Universidade Federal do Rio de Janeiro, Rio de Janeiro 3992 M - (MN) MN 3997 M 0.26 MN 4007 F 0.17 MN 9447 M - MN 9448 M - MN 31573 F - MN 31575 M - MN 42780 F - MN 43617 F - Without MN accession M- number Museum of Comparative Zoology, Cambridge, USA (MCZ) 160970 M - MCZ 198332 F - MCZ 198333 M 0.21 Natural History Museum of Los Angeles County, Los Angeles, USA (LACM) 32371 F - LACM 32372 M - LACM 32373 M 0.10 LACM 32374 M - LACM 32375 M - The Natural History Museum, Tring, UK (NHM) 19188.8.131.52 F - Museu de Zoologia da Universidade Estadual de Campinas, Campinas 1015 M - (ZUEC) ZUEC 0408 M 0.23 Centro de Reabilitação de Animais Silvestres, Campo Grande A4_2066 ? (Immature) - (CRAS-MS) CRAS-MS A4_2067 ? (Immature) - CRAS-MS A4_2068 ? (Immature) - CRAS-MS A4_2069 ? (Immature) - CRAS-MS A4_2070 ? (Immature) - CRAS-MS A4_2071 ? (Immature) - CRAS-MS A4_2072 ? (Immature) - CRAS-MS A4_2073 ? (Immature) - CRAS-MS A4_2074 ? (Immature) - CRAS-MS A4_2075 ? (Immature) - CRAS-MS A4_2076 ? (Immature) - CRAS-MS A4_2077 ? (Immature) - CRAS-MS A4_2078 ? (Immature) - CRAS-MS A4_2079 ? (Immature) - CRAS-MS A4_2080 ? (Immature) - CRAS-MS A4_2081 ? (Immature) - For Index calculation see methods. Revista Brasileira de Ornitologia, 22(3), 2014 Age and gender related plumage variation of psittacofulvine pigments: the case of the Yellow-faced Parrot Alipiopsitta xanthops Carlos Barros de Araújo and Luiz Octavio Marcondes-Machado RESULTS length (n = 21, median = 24%). The yellow mask also presents a great deal of variation, as adults have a yellow The belly color in A. xanthops varied from a complete mask that completely covers the top of the head, while green to a yellow, orange or red coloration (Figure 1), younger parrots generally display smaller masks without and color belied parrots (CBP) were found throughout its the orange ear-coverts (Figure 1). Some individuals have much broader yellow masks, contiguous towards the breast entire distribution (Figure 2). The amount of color on the and belly (Figure 1, parrot 3). We observed 3 individuals belly was also quite variable. Museum specimens could be completely green or present belies with yellow/red/orange with this particular coloration phenotype (hereafter patches that in some cases extended to its upper chest yellow necked parrots, YNP), and they were restricted to (Figure 1, parrot 3) reaching up to 54% of the total body the southwestern distribution of the species (Figure 2). FIGURE 2. Black dots represent the occurrences of the studied colored bellied Alipiopsitta xanthops individuals, whereas the squares represent the locations of yellow neck individuals. Revista Brasileira de Ornitologia, 22(3), 2014 Age and gender related plumage variation of psittacofulvine pigments: the case of the Yellow-faced Parrot Alipiopsitta xanthops Carlos Barros de Araújo and Luiz Octavio Marcondes-Machado The proportion of CBP individuals in ﬂocks was CBP between sexes, we found no diﬀerences (Fischer similar in the two wild populations – 8.9% in Emas exact test; p = 0.12; Figure 3), despite the proportion and 8.2% in Brasília ( = 0.001; d.f.=1; p = 0.98). of CBP among males (37%) being more than twice However, museum specimens presented approximately that among females (17%). The comparison of three times more CBP individuals than the two wild the plumage indexes (I) between sexes of museum populations studied (32%; 2 =25.6; d.f.=1; p<0.01; specimens revealed that males exhibit a signiﬁcantly Figure 3). We also found a skewed sex (male:female) wider colored patch (t = 1.81, unilateral p = 0.04), ratio of 3:1 in museums, as 75% of the specimens presenting a mean index of 27%, while females were males. When we compared the proportion of presented a lower value of 16%. FIGURE 3. Left: proportions of adult color belied parrots in nature (Brasília and Emas National Park) and museums. Right: proportions of museum colored belied parrots specimens for each sex. Numbers over each bar represents the sample size. between males and females, but that males have larger colored patches on the belly. Chicks did not present colored bellies and orange ear-coverts, whereas yellow masks were smaller than in adults. Yellow coloration seems to increase in area during aging, since none of the 16 nestlings observed presented colored bellies. Also, the yellow mask, a trait observed in all adults, grew during nestling development, whereas the presence of orange ear-coverts was never observed in sub- adults. Despite these ﬁndings, our data does not allow for any further discussion on the ontogeny of the plumage patterns found. Orange ear-coverts have been reported by Miranda-Ribeiro (1920) to be absent in some individuals. FIGURE 4. Mean and standard deviation of the plumage index (I) As this character seems to be always present in adults and of color belied parrots (adults) of Alipiopsitta xanthops calculated from absent in young parrots, we believe that Miranda-Ribeiro pictures for females (n = 3) and males (n = 18). (1920) probably observed young parrots to draw his conclusions. DISCUSSION The diﬀerences in the proportion of CBP individuals between wild and museum specimens indicate that Overall, the Yellow-faced parrot presents great plumage museum sampling may be biased. This is likely to occur in variation throughout its distribution range. Plumage species that present such conspicuous plumage variation, variation observed includes diﬀerent colors, but also as naturalists may focus their sampling eﬀorts towards morphological diﬀerences on colored patches. We found rare morphs in order to obtain specimens encompassing no signiﬁcant diﬀerences in the proportion of CBP the full color variation for the species. Revista Brasileira de Ornitologia, 22(3), 2014 Age and gender related plumage variation of psittacofulvine pigments: the case of the Yellow-faced Parrot Alipiopsitta xanthops Carlos Barros de Araújo and Luiz Octavio Marcondes-Machado Male-skewed sex ratios seem to be the norm within improving this manuscript; Emas National Park for logistic Psittacidae (Taylor & Parkin 2008). Still, the skewed support; CRAS/MS, Ana Paula Felício, Vinicius Andrade sex ratio of 3.0 male:female found in this study is larger Lopes, Raphael Dias and Gláucia Seixas for the pictures of than what has been reported for other species in nature chicks sent. We would like to thank worldwide museums (maximum of 2.42 in Pyrrhura egregia; review in Taylor curators for gently sending the material, especially Luis & Parkin 2008). The presence of such highly skewed sex Fábio Silveira for his comments and encouragement. ratio elicit three distinct possibilities: 1) the sex ratio is We would also like to thank Dr. Alexandre Aleixo and an actual trend in Yellow-faced Parrot’s wild populations; two anonymous referees for the many comments that 2) males are easier to catch (for instance, females spend helped to improve the quality of this manuscript. We also more time inside the nest), or; 3) males are more colorful thank the collections mentioned in Table 1 for providing and thus attract additional attention from collectors. A us with pictures and data on the specimens under their combination of these three possibilities could also be an care. Faepex – Unicamp and Mclennan Brown Charitable explanation. 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Ornithology Research – Springer Journals
Published: Sep 1, 2014
Keywords: Arinii; dichromatism; feather coloration; morphology; Psittacidae; sexual dimorphism
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