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Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766)

Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Revista Brasileira de Ornitologia, 23(3), 341-350 ARTICLE September 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana a (Linnaeus, 1766) 1,2 1 Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga Laboratório de Ornitologia, Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, CEP 21941-971, Rio de Janeiro, RJ, Brazil. Corresponding author: fmallet@bol.com.br Received on 23 May 2014. Accepted on 4 May 2015. ABSTRACT: Th e Turquoise Tanager Tangara mexicana a is largely distributed in northern South America, and has been considered a polytypic species comprising four or fi ve subspecies. Our study on plumage coloration of 175 specimens, from localities covering the entire species’ range, revealed the existence of two variable characters: color of underparts and color of lesser upper-wing coverts. Seven morphotypes were found that combine the diff erent states presented by these two characters. Two morphotypes were very distinct, representing two of the most easily diagnosable subspecies (T T T. m. mexicana, having yellowish white underparts and a contrasting turquoise green humeral patch; and T T T. m. boliviana, having bright yellow underparts and the blue of lesser upper- wing coverts similar to that of the sides of head, throat, breast and rump). The other morphotypes (includin g those representing subspecies T T T. m. media, T T T. m. vieilloti i and T T T. m. lateralis s) are shared by birds with character states that are intermediate between those found in T. m. mexicana a and T. m. boliviana, thus representing a polymorphic population ranging widely across central Amazonia, from northern Venezuela and Trinidad to the south of the lower Amazon. This large area may be considered as a hybrid zone of considerable phenotypic instability, more evident especially in the region between the lower Rio Madeira and east of the Tocantins in the Belém area. Based on the General Lineage Species Concept two species could be recognized based on plumage: T. mexicana, restricted to the Guyana center of endemism, and T. boliviana, which is widely distributed in western Amazonia and the eastern foothills of the Andes, an area corresponding to the centers of endemism Napo and Inambari. Th e taxonomic validity of T. lateralis is once more challenged. KE E EY Y Y-WORDS: Amazonia, biodiversity, centers of endemism, hybrid zones, subspecies, taxonomy. INTRODUCTION subspecies of T. mexicana a (Zimmer 1943, Pinto 1944), but now it has been accepted as a valid and independent Comprising about fif ty species, Tangara a is one of the species again (Piacentini et al. 2015). Tangara brasiliensis shows a high level of genetic divergence (Burns & Naoki richest genera of birds and one of the most representative of Neotropical birds (Peters 1970, Sibley 1996, Clements 2004), allopatric distribution (with no apparent gene 2007, SACC 2015, Hilty 2011, Barker et al. 2013). fl ow) and consistent phenotypic differences (Isler & Isler Sedano & Burns (2010) produced a large phylogeny of 1987, Ridgely & Tudor 1989, Sick 1997), making it fully tanagers based on mitochondrial genes, which lumps many diagnosable from T. mexicana. However, T. brasiliensis s is still considered a subspecies of T. mexicana a by some authors morphologically distinctive groups into a few genera. Among the surprising results of this study is that Th raupis (Clements 2007, Hilty 2011, SACC 2015). According to was found to be embedded in Tangara. Th e Turquoise Hellmayr (1936), T. m. mexicana a is known from the north Tanager is found in forest borders, varzea, second growth, of the lower Amazon (Guyanas and Brazil); T. m. boliviana plantations and gardens from southeastern Colombia and (Bonaparte, 1851) is widely distributed in southeastern Colombia and Ecuador, Peru, northern Bolivia and Brazil Ecuador to Guyanas, northern Brazil, Peru and northern Bolivia (Isler & Isler 1987, Ridgely & Tudor 1989). Five from the Solimões to the lower Madeira; T. m. vieilloti subspecies of the Turquoise Tanager Tangara mexicana (Sclater, 1857) is endemic to Trinidad, and T. m. media (Linnaeus, 1766) have been proposed (Hellmayr 1936, (Berlepsch & Hartert, 1902) is found in Venezuela and Isler & Isler 1987, Hilty 2011). After the larger and paler extreme northern Brazil. Tangara m. lateralis s Todd, 1922, from southern Amazon (Todd 1922), was considered White-bellied Tanager Tangara brasiliensis s (Linnaeus, 1766) from southeastern Brazil had been treated as a indistinct from T. m. boliviana a by Hellmayr (1936) and separate species by Hellmayr (1936), it was considered a treated as a hybrid between T. m. mexicana a and T. m. Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga boliviana a by Isler & Isler (1987). However, Griscom & lateralis (CMNH 78031). To obtain comparable color Greenway (1941), Pinto (1944) and Gyldenstolpe (1945) measurements, the photos were taken in a standardized recognized the validity of T. m. lateralis. fashion with the specimens photographed with the use of According to several authors (Hellmayr 1936, flashes in similar conditions. The color descriptions in the Zimmer 1943, Gyldenstolpe 1945) subspecies of T. photos were taken by looking them in the same computer mexicana a are distinguished by the tone of blue on the screen. Only adult birds were included in this study. sides of head, throat, breast and rump, and by the color of Both sexes were included in the analysis because sexual underparts (belly, thighs and under-tail coverts) and lesser dimorphism in plumage is not recognized in Tangara upper-wing coverts. While the underparts are yellowish mexicana a (Isler & Isler 1987, Hilty 2011). white in the nominate form (T. m. mexicana) and bright We based our analyses on the following plumage yellow in T. m. boliviana, the other three nominal taxa T. color characters traditionally employed to diagnose taxa m. vieilloti, T. m. media a and T. m. lateralis s are transitional in T. mexicana: 1) the tone of blue on the sides of head, forms showing intermediate shades of yellow on the throat, breast and rump; 2) the color of underparts; and underparts between those found in T. m. mexicana a and 3) the color of lesser upper-wing coverts. We used Smithe T. m. boliviana. Birds from Trinidad (T. m. vieilloti) are (1975, 1981) to determine the colors corresponding usually distinguished from those in Venezuela (T. m. to diff erent character states. Th ese were referred to as media) by the darker blue plumage and brighter yellow italicized names (with corresponding numbers in the underparts, although some birds from Venezuela were fi rst citation). Th e color description of each specimen very similar to T. m. vieilloti i specimens (Hellmayr 1936). was made with no regard to its possible subspecies Tangara m. boliviana a is diagnosed primarily by the allocation or collection locality. Geographic coordinates bright yellow underparts and the blue of lesser upper- of collecting localities of the specimens analyzed were wing coverts similar to that of the sides of head, throat, obtained from Paynter (1982), Paynter Jr. & Traylor Jr. breast and rump. While this phenotype predominates in (1991) and Vanzolini (1992). western Amazonia, several specimens (especially towards Plumage color character states obtained for each the lower Amazon) have paler blue lesser upper-wing specimen were mapped separately to assess the degree and coverts (Hellmayr 1936, Zimmer 1943). kind of geografi c variation associated with each character. Understanding the geographic diff erentiation of Subsequently, all character states variations were mapped plumage in T. mexicana a has been considered a challenge together to assess overall trends of geographic variation. by some authors (Hellmayr 1936, Zimmer 1943, Hilty We gave special attention to the identification of localities 2011). Th erefore, we present here a review of the complex that had one or more specimens with intermediate pattern of geographical differentiation in pluma ge plumage characters because they could indicate the coloration of the Turquoise Tanager throughout its entire existence of hybrid zones. Localities with evidence of distribution and discuss taxonomic implications and intermediate character states were classified as representin g interpretations that emerged from the obtained data. hybrid zones. METHODS R R RESULTS We examined 101 specimens of T. mexicana a housed at Variation of character states the Museu Nacional do Rio de Janeiro (MNRJ), Museu Paraense Emílio Goeldi (MPEG), and Museu de Zoologia We found no significant individual variation in the color da Universidade de São Paulo (MZUSP) (Appendix I). of head, throat, breast and rump, which was Ultramarine Additionally, we examined photographs of 74 specimens Blue e (Color 170A) in all specimens analyzed (including pertaining to the ornithological collections of the American those examined through photographs). Museum of Natural History (AMNH), Academy of Natural Four states were recognized for the color of Sciences of Philadelphia (ANSP), Carnegie Museum of underparts, namely Pale Horn (Color 92), Cream (Color Natural History (CMNH), Collección Ornitológica Phelps 54), Straw Yellow w (Color 56) and Spectrum Yellow w (Color (COP), Field Museum of Natural History (FMNH), 55) (Figure 1), while the color of wing coverts presented Muséum National d’Histoire Naturelle (MNHN), and three states, namely Ultramarine Blue e (Color 170A), Yale Peabody Museum (YPM) (Appendix II). Photographs Sky Blue e (Color 168C) and Turquoise Green (Color 64) examined include those of the type specimens of Tangara (Figure 2). Ultramarine Blue e wing coverts always occurred mexicana boliviana a [formerly Callospiza boliviana] together with Spectrum Yellow w or Straw Yellow w underparts, (MNHN 7897), Tangara mexicana media a [formerly y Calliste while Turquoise Green wing coverts were accompanied by mexicana media] (AMNH 513316) and Tangara boliviana Pale Horn, Cream and Straw Yellow w underparts. Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga FIGURE 1. Color character states of underparts in Tangara mexicana. Colors from left to right: Pale Horn (MPEG 22995), Cream (MPEG 21553), Straw Yellow w (MPEG 43353), and Spectrum Yellow w (MPEG 23003). FIGURE 2. Color character states of lesser upper-wing coverts in Tangara mexicana. From left to right: Ultramarine Blue e (AMNH 513329), Sky Blue (AMNH 278331) and Turquoise-Green (AMNH 513315). Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga Geographic distribution of character states were widely distributed across western Amazonian Brazil, southern Colombia, eastern Peru and northern Bolivia Specimens with Pale Horn underparts were recorded (Figure 3). exclusively from the north of the lower Amazon (Guyanas Ultramarine Blue e wing coverts were predominant in and adjacent parts of Brazil). Specimens with Cream the upper Amazon, with some specimens occurring on underparts were recorded from the upper Rio Branco to the southern bank of middle and lower Amazon. Birds the Rio Orinoco in Venezuela. Several birds with Straw with Turquoise Green humeral patches were restricted Yellow w underparts were from the southern bank of middle to the north of the lower Amazon, Guyanas, upper Rio and lower Amazon (lower Rio Madeira, Rio Tapajós, Branco, Venezuela and Trinidad. Specimens with Sky Blue Rio Xingu and Rio Tocantins) but also from the upper humeral patches were found mainly in the southern bank Rio Negro, northern Guyana and all specimens from of the lower and middle Amazon, but also in the upper Trinidad. Specimens with Spectrum Yellow w underparts Rio Negro (Figure 4). FIGURE 3. Geographic distribution of underparts color character states in Tangara mexicana a (black circles – Spectrum Yellow, gray circles – Straw Yellow, light gray circles – Cream, black squares – Pale Horn). FIGURE 4. Geographic distribution of lesser upper-wing coverts color character states in Tangara mexicana a (black circles – Ultramarine Blue, gray circles – Sky Blue, white circles – Turquoise-Green). Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga Morphotypes and their geographic distribution humeral patch (Figure 5). Th e distribution of morphotype 3 coincides with that of morphotype 2, ranging from the We found seven morphotypes that combine the diff erent left bank of the Rio Madeira to the lower Rio Tocantins character states (Figure 5). Five of these morphotypes (Figure 6). correspond to described taxa that have been considered Morphotype 4 is characterized by the combination subspecies of T. mexicana. of a Sky Blue e humeral patch and Straw Yellow w underparts Morphotype 1 is characterized by having the head, (Figure 5). It occurs from Belém to Manaus, and in upper throat, breast, rump and lesser upper-wing coverts Rio Negro (Figure 6). Ultramarine Blue e and Spectrum Yellow w underparts Morphotype 5 is characterized by having Straw (Figure 5). Specimens of this morphotype were found Yellow w underparts and Turquoise Green humeral patches from the eastern foothills of the Andes (Colombia, Peru (Figure 5). It was found in lower Rio Orinoco (Venezuela), and Bolivia), to lower Rio Negro and southern bank of northern Guyana and Trinidad (Figure 6). The holotype the lower Amazon (from the middle Rio Tocantins to of Calliste vieilloti, from Trinidad, was not examined, but the Marajó island). This morphotype was very poorl y supposedly would belong to this morphotype. represented in the lower Amazon (Figure 6). It includes Morphotype 6 has Cream underparts and Turquoise the holotype of Callospiza boliviana. Green humeral patches (Figure 5). It is widely distributed Morphotype 2 differs from morphotype 1 only in central Venezuela and upper Rio Branco in Brazil by the underparts, which are Straw Yellow (Figure 5). (Figure 6). It includes the holotype of Calliste mexicana It was found on the southern bank of the middle and media. lower Amazon, between the right bank of the lower Rio Morphotype 7 diff ers from all other morphotypes by Madeira and the region of Belém (Figure 6). It includes having Pale Horn underparts and Turquoise Green humeral the holotype of Tangara boliviana lateralis. patches (Figure 5). Specimens of this morphotype were Morphotype 3 is similar to morphotype 1 with from the Guyanas and north of the lower Amazon (Figure respect to the color of underparts, but it has Sky Blue 6). It corresponds to the nominate T. m. mexicana. FIGURE 5. Morphotypes of Tangara mexicana a based on the combined coloration of underparts and lesser upper-wing coverts (drawing: Raphael Dutra). See text for details. Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga FIGURE 6. Geographic distribution of morphotypes of Tangara mexicana a recognized in this study, showing a possible hybrid zone highlighted in gray. DISCUSSION is difficult, and could be more easily accom plished by a phylogeographic study. Th erefore, our data can be viewed Our analyses revealed the existence of at least two main as evidence supporting alternative scenarios of Turquoise Tanager diversifi cation to be tested by future genetic areas of plumage color character state stability in the Turquoise Tanager (corresponding to morphotypes 1 studies. and 7), separated by a smaller geographic area where Based on the General Lineage Species Concept (de intermediate phenotypes are present, sometimes even at Queiroz 1998), in which the only necessary property of a the same locality (corresponding to morphotypes 2-6) species is existence as a separately evolving metapopulation lineage (de Queiroz 2005), we propose that morphotypes (Figures 5 and 6). Two alternative interpretations of this overall pattern are: 1) morphotypes 1 and 7 represent 1 and 2 of T. mexicana found in this study would deserve evolutionary independent lineages / taxa that intergrade the status of separate species. These two mor photypes along a wide northwestern-southeastern trend hybrid have been traditionally recognized as the most distinct zone across Central Amazonia; or 2) morphotypes 1 subspecies of the Turquoise Tanager (Zimmer 1943). One of these (T. m. mexicana) occurs on the Guiana and 7 are extremes of a cline, with a corresponding wide intergradation zone in Central Amazonia. Below, we shield, being diagnosed by having Pale Horn underparts discuss these two alternatives with respect to the plumage and a contrasting Turquoise-Green humeral patch, while color data but stress that distinguishing between them the other (T. m. boliviana) is found from the base of the Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga Andes (below 500 m, following Hilty & Brown 1986) one in central Venezuela and upper Rio Branco in Brazil, to the southern bank of the middle and lower Amazon, including birds corresponding to morphotype 6 or T. being diagnosed by having Spectrum Yellow w underparts m. media, with Cream underparts and a Turquoise-Green and the wing coverts indistinguishable from the blue of humeral patch, and the other in Trinidad and northern the rest of the plumage. Venezuela, including birds corresponding to morphotype According to Hellmayr (1936) and Zimmer (1943), 5 or T. m. vieilloti, with Straw Yellow w underparts and a however, the challenge for understanding the complex Turquoise-Green humeral patch. However, the diagnose of pattern of geographical differentiation in T. mexicana these two morphotypes may be subtle in practice, so that is in the regions of the middle Amazon and southern both could alternatively be regarded as part of a larger bank of the lower Amazon. In this area we have found a polymorphic population ranging widely across central significant individual variation in the color of underparts, Amazonia, from northern Venezuela and Trinidad to with birds at times showing them Spectrum Yellow w and the south of the lower Amazon (lower Rio Madeira to Straw Yellow w in the same locality. In the northern Amazon Belém). This includes forms described as T. m. vieilloti, (upper Negro, Branco and Orinoco rivers) and Trinidad, T. m. media a and T. m. lateralis, consisting of birds with although individual variation in the tone of yellow is less character states that are intermediate between those found evident, some specimens are clearly distinct from others in T. m. mexicana a and T. m. boliviana. As pointed out by with respect to this character, as stated by Hellmayr Price (2008), subspecies rank has been often mistakenly (1936). Th e apparent phenotypic stability of the birds assigned considering populations with different levels from Trinidad could result from the founder effect due of character intergradation between distinct species. to ca. 11,000 years of isolation from the continent (Snow However, more studies on birds of Venezuela and Trinidad 1985). However, some birds from the coast of Venezuela are needed to improve understanding of the taxonomic are barely distinct from those of Trinidad. status of T.m. media a and T.m. vieilloti. Th e color of lesser upper-wing coverts is another The existence of a rather lar ge area of polymorphism important variable character among populations of T. linking areas of phenotypic stability seems to preclude mexicana. While specimens from the Guyanas and north interpretation of morphotypes 1 and 7 as extremes of of the lower Amazon, upper Rio Branco, Venezuela a clinal pattern of variation in the Turquoise Tanager. and Trinidad have the wing coverts forming a bright Th is whole range occupied by intermediate birds could Turquoise-Green humeral patch, birds from the southern be better considered as a hybrid zone because of the bank of the middle and lower Amazon and upper Rio considerable phenotypic instability detected (distinct Negro have a Sky Blue e or Ultramarine Blue e humeral phenotypes coexisting in the same regions), which patch. All specimens from western Amazonia have dark is more evident especially in the region between the blue (Ultramarine Blue e) wing coverts. There is a trend to lower Madeira River east across the Tocantins River in the occurrence of a lighter blue humeral patch in birds the Belém area. A relatively narrow hybrid zone along of the lower Amazon, as stated by Hellmayr (1936) and the Amazon valley has also been found between two Zimmer (1943). However, birds with dark blue wing purported phylogenetic species (Icterus chrysocephalus and coverts also occur in the southern bank of the lower Icterus cayanensis s)(D’Horta et al. 2008). As advocated Amazon, and are indistinguishable from specimens from by Hellmayr (1936), who nevertheless recognized the the upper Amazon, which reveals the instability of this taxonomic validity of T. m. media a and T. m. vieilloti, this character in the lower Amazon. phenotypic instability does not allow a diagnosis of T. m. Our analysis of geographical variation in plumage lateralis, described by Todd (1922) from the region of characters, thus, revealed the existence of at least two the Rio Tapajos and recognized by Gyldenstolpe (1945). major and up to four nuclear areas (with phenotypic Zimmer (1943), in turn, also preferred to consider stability) in T. mexicana. One of these coincides with the populations from the lower Amazon as an unstable and Guyana Center of Endemism (Cracraft 1985), including intermediate T. m. mexicana/T. m. boliviana a population, birds corresponding to morphotype 7 or T. m. mexicana. in which the recognition of a taxon is rather questionable. Another nuclear area is located in western Amazonia, encompassing the Napo and Inambari centers of endemism (Cracraft 1985), and including birds corresponding to A A ACKNOWLEDGMENTS morphotype 1 or T. m. boliviana. According to Zimmer (1943), these two forms have evolved separately when We are grateful to Jorge Bruno Nacinovic, Marcos Raposo “an arm of the sea occupied the Amazon valley”, T. m. (MNRJ), Alexandre Aleixo, Fátima Lima (MPEG), and mexicana a in the Guiana shield and T. m. boliviana a in Luís Fábio Silveira (MZUSP) for permission to examine western Amazonia. Two additional smaller areas of specimens under their care. Th omas J. Trombone apparent phenotypic stability occur between those two, (AMNH), Leo Joseph (ANSP), Stephen Rogers Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga Isler, M. L. & Isler, P. R. 1987. Th e Tanagers. Washington: (CMNH), Robin Restall (COP), Shannon Kenney, Paul Smithsonian Institution Press. Sweet, Mary Hennen (FMNH), and Kristof Zyskowski Paynter Jr., R. 1982. Ornithological Gazetteer of Venezuela. 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Lawrence: American Ornithologists’ Union. Brazil. Kongliga Svenska Vetenskaps Akademiens Handlingar, 22(3): Todd, W. E. C. 1922. New forms of fi nches and tanagers from tropical 1-338. America. Proceedings of the Biological Society of Washington, 35: 89- Hellmayr, C. E. 1936. Catalogue of birds of the Americas, Part IX, Tersinidae-Th raupidae. Field Museum of Natural History, Vanzolini, P. E. 1992. A Supplement to the Ornithological Gazetteer Zoological Series, 13 (9), Publ. 365. of Brazilll. São Paulo: Museu de Zoologia da Universidade de São Hilty, S. L. 2011. Family Th raupidae (Tanagers), p. 46-329. In: del Paulo. Hoyo, J.; Elliott, A. & Christie, D. A. (eds.). Handbook of the Birds Zimmer, J. T. 1943. Studies of Peruvian Birds. XLVII. The genus of the World d d, v. 16. Tanagers to New World Blackbirds. Barcelona: Tangara. Part 2. American Museum Novitates, 1246: 1-14. Lynx Edicions. Hilty, S. L. & Brown, W. L. 1986. Birds of Colombia. Princeton: Princeton University Press. Associate Editor: Gustavo Sebastián Cabanne Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga APPENDIX X I. Material examined d (Specimens from each locality in parenthesis). TRINIDAD. Trinidad (MZUSP 3706); VENEZUELA. Monagas: Maturin (MZUSP 2476); COLÔMBIA. Bogotá (MNRJ 6808); BRAZIL. Roraima: Alto Mucajaí (MPEG 21553; MZUSP 56239); Caracaraí (MPEG 56485); Amapá: Serra do Navio (MNRJ 29248); Fazenda Prosperidade, Rio Maracá, Mazagão (MPEG 22990; MPEG 22995); Rio Vila Nova, Macapá (MPEG 22991); Estrada do Curiaú km 01, Ilha Curuçá, Macapá (MPEG 28873); Igarapé Ariramba, afluente direito do Rio Tartarugal, Acampamento 4, Amapá (MPEG 28874); Rio Maruanum, Macapá (MPEG 28388); Fazenda Nova Califórnia, Rio Araguari (MPEG 22994); Fazenda Itauqueira, Tartarugalzinho (MPEG 53651; MPEG 53652); Oiapoque (MPEG 22996); Acre: Cruzeiro do Sul, Rio Juruá (MPEG 22997; MPEG 22998); Vila Taumaturgo, Seringal Oriente, Rio Juruá (MPEG 23000; MPEG 23001); Amazonas: São Gabriel da Cachoeira (MZUSP 16979); Acajutuba, Rio Negro (MPEG 12106); Maraã, margem esquerda do Rio Japurá, Maguari (MPEG 42934; MPEG 43352; MPEG 43353); Caitaú, margem direita do Rio Solimões, Uará (MPEG 50197; MPEG 50198); Santa Cruz, Rio Eirú, Juruá (MZUSP 18498; MZUSP 18504); Santo Antônio do Içá (MZUSP 69910); Bom Lugar, Rio Purus (MPEG 3499); Rio Jutaí (MZUSP 69909); Manacapuru (MNRJ 6816; MZUSP 16977; MZUSP 16978); Reserva Ducke, Manaus (MPEG 30079; MPEG 30370; MPEG 30371); Itacoatiara (MNRJ 32790; MNRJ 32791; MZUSP 17798; MZUSP 18499; MZUSP 18500; MZUSP 18501; MZUSP 18502; MZUSP 18505; MZUSP 18506); Igarapé Anibá (MZUSP 18496; MZUSP 18508); Rio Maraú (MZUSP 62116); Lago Baptista (MPEG 18493; MZUSP 17797; MZUSP 18494; MZUSP 18495; MZUSP 18497); Pará: Rio Paru (MNRJ 27369; MNRJ 27370; MNRJ 27371); Ilha de Marajó, cerca de 4km ao sul de Chaves (MPEG 58095); Santa Bárbara, Benevides (MPEG 22190); Portel, Rio Anapu (MPEG 23012; MPEG 23014); Val-de-Cans (MPEG 23672); Utinga, Belém (MZUSP 36041; MZUSP 36098; MZUSP 36100; MZUSP 36101); Providência, Belém (MPEG 5543; MPEG 7741); Vila do Outeiro, Ilha de Caratateua, Belém (MPEG 29883; MPEG 29884); Murutucu (MZUSP 36099); Igarapé Pucuruzinho, BR-422, km 67, Tucuruí/Novo Repartimento (MPEG 35346; MPEG 47957); Santarém (MZUSP 3359; MZUSP 3360); Fordlândia, Rio Tapajós (MZUSP 47352; MZUSP 47353); Aramanaí, Rio Tapajós (MZUSP 32773); Sumaúma, Rio Tapajós (MZUSP 47354); Villa Braga, Rio Tapajós (MNRJ 6815; MPEG 13126); Boim, Rio Tapajós (MPEG 8581); Alcobaça, Rio Tocantins (MPEG 5373); Tocantins: Araguatins (MPEG 20682; MZUSP 53054; MZUSP 65820; MZUSP 66095; MZUSP 66096); Rondônia: Guajará-Mirim, Rio Mamoré (MPEG 23002; MPEG 23003; MPEG 23005; MPEG 23006; MPEG 23008; MPEG 23010); Cachoeira Nazaré, margem oeste do Rio Jiparaná (MPEG 40290); Mato Grosso: Salto de Sepotuba (MNRJ 6809); Salto do Rio Jauru (MNRJ 6810); Fazenda São José, Rio Peixoto de Azevedo (MPEG 33846); PERU. Ucayali i i: Pucallpa (MZUSP 68248). Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga APPENDIX X II. Specimens examined through color photographs (Specimens from each locality in parenthesis). TRINIDAD. Santa Cruz (YPM 26422); Brasso, Caroni (YPM 26427); Caroni Swamp, Caroni (YPM 26428); VENEZUELA. Delta Amacuro (COP 48307); Sucre e (COP 56715; COP 56715; COP 56715; COP 56715; COP 56715; COP 56715; COP 56715) Amazonas (COP 21207; COP 21208; COP 21209; COP 21391; COP 22153; COP 22154; COP 22155; COP 38788; COP 69709; COP 69710; COP 69711; COP 69712); Bolívar (COP 16591; COP 16592; COP 17977; COP 17978; COP 17979; COP 26062; COP 26063; COP 26064; COP 26065; COP 45212); GUYANA. Georgetown (FMNH 32389; FMNH 32390); North West District t t: Koriabo (FMNH 190651; YPM 26429); Demerara- Berbice: Rio Essequibo, Rockstone (FMNH 108649); Potaro-Siparuni: Rio Essequibo, Iwokrama Reserve (ANSP 189019); Rio Abary (ANSP 189015; ANSP 189016; ANSP 189018); Mahaica-Berbice: Onverwagt (ANSP 189020); FRENCH GUYANA. Mana: Mana (YPM 31203; YPM 31204; YPM 31205); COLOMBIA. Vichada: Maipures (AMNH 513316) [type specimen of T. m. media]; Meta: Serrania de Macarena, Rio Guapaya (FMNH 249262; FMNH 249263); Caquetá: Morelia (ANSP 152949); Putumayo: Guascayaco (FMNH 282349); Mocoa (FMNH 282350); Santo Antonio Guamez (FMNH 287583); Umbria (ANSP 160131); Rio San Miguel (ANSP 165547); Rio Rumyiaco (ANSP 165546);; BRAZIL. Amazonas: Padauari (COP 35056; COP 35057; COP 35059; COP 35060; COP 35061); Manacapuru, Solimões (ANSP 67172; ANSP 67173); Pará: Castanhal (ANSP 80760; ANSP 80761); Apacy, Rio Tapajós (CMNH 78031)[type specimen of T. m. lateralis s]; Pinhy, Rio Tapajós (ANSP 108373); PERU. Napo: Apayucu (ANSP 83750); San Martin: San Martin (ANSP 116134); Yurinaqui (ANSP 176557); BOLÍVIA. Huanay: Rio Mapiri (ANSP 119228; ANSP 119229; ANSP 119230); Santa Cruz: Guarayos (MNHN 7897)[type specimen of T. m. boliviana]. Revista Brasileira de Ornitologia, 23(3), 2015 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766)

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Revista Brasileira de Ornitologia, 23(3), 341-350 ARTICLE September 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana a (Linnaeus, 1766) 1,2 1 Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga Laboratório de Ornitologia, Departamento de Zoologia, Instituto de Biologia, Universidade Federal do Rio de Janeiro, CEP 21941-971, Rio de Janeiro, RJ, Brazil. Corresponding author: fmallet@bol.com.br Received on 23 May 2014. Accepted on 4 May 2015. ABSTRACT: Th e Turquoise Tanager Tangara mexicana a is largely distributed in northern South America, and has been considered a polytypic species comprising four or fi ve subspecies. Our study on plumage coloration of 175 specimens, from localities covering the entire species’ range, revealed the existence of two variable characters: color of underparts and color of lesser upper-wing coverts. Seven morphotypes were found that combine the diff erent states presented by these two characters. Two morphotypes were very distinct, representing two of the most easily diagnosable subspecies (T T T. m. mexicana, having yellowish white underparts and a contrasting turquoise green humeral patch; and T T T. m. boliviana, having bright yellow underparts and the blue of lesser upper- wing coverts similar to that of the sides of head, throat, breast and rump). The other morphotypes (includin g those representing subspecies T T T. m. media, T T T. m. vieilloti i and T T T. m. lateralis s) are shared by birds with character states that are intermediate between those found in T. m. mexicana a and T. m. boliviana, thus representing a polymorphic population ranging widely across central Amazonia, from northern Venezuela and Trinidad to the south of the lower Amazon. This large area may be considered as a hybrid zone of considerable phenotypic instability, more evident especially in the region between the lower Rio Madeira and east of the Tocantins in the Belém area. Based on the General Lineage Species Concept two species could be recognized based on plumage: T. mexicana, restricted to the Guyana center of endemism, and T. boliviana, which is widely distributed in western Amazonia and the eastern foothills of the Andes, an area corresponding to the centers of endemism Napo and Inambari. Th e taxonomic validity of T. lateralis is once more challenged. KE E EY Y Y-WORDS: Amazonia, biodiversity, centers of endemism, hybrid zones, subspecies, taxonomy. INTRODUCTION subspecies of T. mexicana a (Zimmer 1943, Pinto 1944), but now it has been accepted as a valid and independent Comprising about fif ty species, Tangara a is one of the species again (Piacentini et al. 2015). Tangara brasiliensis shows a high level of genetic divergence (Burns & Naoki richest genera of birds and one of the most representative of Neotropical birds (Peters 1970, Sibley 1996, Clements 2004), allopatric distribution (with no apparent gene 2007, SACC 2015, Hilty 2011, Barker et al. 2013). fl ow) and consistent phenotypic differences (Isler & Isler Sedano & Burns (2010) produced a large phylogeny of 1987, Ridgely & Tudor 1989, Sick 1997), making it fully tanagers based on mitochondrial genes, which lumps many diagnosable from T. mexicana. However, T. brasiliensis s is still considered a subspecies of T. mexicana a by some authors morphologically distinctive groups into a few genera. Among the surprising results of this study is that Th raupis (Clements 2007, Hilty 2011, SACC 2015). According to was found to be embedded in Tangara. Th e Turquoise Hellmayr (1936), T. m. mexicana a is known from the north Tanager is found in forest borders, varzea, second growth, of the lower Amazon (Guyanas and Brazil); T. m. boliviana plantations and gardens from southeastern Colombia and (Bonaparte, 1851) is widely distributed in southeastern Colombia and Ecuador, Peru, northern Bolivia and Brazil Ecuador to Guyanas, northern Brazil, Peru and northern Bolivia (Isler & Isler 1987, Ridgely & Tudor 1989). Five from the Solimões to the lower Madeira; T. m. vieilloti subspecies of the Turquoise Tanager Tangara mexicana (Sclater, 1857) is endemic to Trinidad, and T. m. media (Linnaeus, 1766) have been proposed (Hellmayr 1936, (Berlepsch & Hartert, 1902) is found in Venezuela and Isler & Isler 1987, Hilty 2011). After the larger and paler extreme northern Brazil. Tangara m. lateralis s Todd, 1922, from southern Amazon (Todd 1922), was considered White-bellied Tanager Tangara brasiliensis s (Linnaeus, 1766) from southeastern Brazil had been treated as a indistinct from T. m. boliviana a by Hellmayr (1936) and separate species by Hellmayr (1936), it was considered a treated as a hybrid between T. m. mexicana a and T. m. Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga boliviana a by Isler & Isler (1987). However, Griscom & lateralis (CMNH 78031). To obtain comparable color Greenway (1941), Pinto (1944) and Gyldenstolpe (1945) measurements, the photos were taken in a standardized recognized the validity of T. m. lateralis. fashion with the specimens photographed with the use of According to several authors (Hellmayr 1936, flashes in similar conditions. The color descriptions in the Zimmer 1943, Gyldenstolpe 1945) subspecies of T. photos were taken by looking them in the same computer mexicana a are distinguished by the tone of blue on the screen. Only adult birds were included in this study. sides of head, throat, breast and rump, and by the color of Both sexes were included in the analysis because sexual underparts (belly, thighs and under-tail coverts) and lesser dimorphism in plumage is not recognized in Tangara upper-wing coverts. While the underparts are yellowish mexicana a (Isler & Isler 1987, Hilty 2011). white in the nominate form (T. m. mexicana) and bright We based our analyses on the following plumage yellow in T. m. boliviana, the other three nominal taxa T. color characters traditionally employed to diagnose taxa m. vieilloti, T. m. media a and T. m. lateralis s are transitional in T. mexicana: 1) the tone of blue on the sides of head, forms showing intermediate shades of yellow on the throat, breast and rump; 2) the color of underparts; and underparts between those found in T. m. mexicana a and 3) the color of lesser upper-wing coverts. We used Smithe T. m. boliviana. Birds from Trinidad (T. m. vieilloti) are (1975, 1981) to determine the colors corresponding usually distinguished from those in Venezuela (T. m. to diff erent character states. Th ese were referred to as media) by the darker blue plumage and brighter yellow italicized names (with corresponding numbers in the underparts, although some birds from Venezuela were fi rst citation). Th e color description of each specimen very similar to T. m. vieilloti i specimens (Hellmayr 1936). was made with no regard to its possible subspecies Tangara m. boliviana a is diagnosed primarily by the allocation or collection locality. Geographic coordinates bright yellow underparts and the blue of lesser upper- of collecting localities of the specimens analyzed were wing coverts similar to that of the sides of head, throat, obtained from Paynter (1982), Paynter Jr. & Traylor Jr. breast and rump. While this phenotype predominates in (1991) and Vanzolini (1992). western Amazonia, several specimens (especially towards Plumage color character states obtained for each the lower Amazon) have paler blue lesser upper-wing specimen were mapped separately to assess the degree and coverts (Hellmayr 1936, Zimmer 1943). kind of geografi c variation associated with each character. Understanding the geographic diff erentiation of Subsequently, all character states variations were mapped plumage in T. mexicana a has been considered a challenge together to assess overall trends of geographic variation. by some authors (Hellmayr 1936, Zimmer 1943, Hilty We gave special attention to the identification of localities 2011). Th erefore, we present here a review of the complex that had one or more specimens with intermediate pattern of geographical differentiation in pluma ge plumage characters because they could indicate the coloration of the Turquoise Tanager throughout its entire existence of hybrid zones. Localities with evidence of distribution and discuss taxonomic implications and intermediate character states were classified as representin g interpretations that emerged from the obtained data. hybrid zones. METHODS R R RESULTS We examined 101 specimens of T. mexicana a housed at Variation of character states the Museu Nacional do Rio de Janeiro (MNRJ), Museu Paraense Emílio Goeldi (MPEG), and Museu de Zoologia We found no significant individual variation in the color da Universidade de São Paulo (MZUSP) (Appendix I). of head, throat, breast and rump, which was Ultramarine Additionally, we examined photographs of 74 specimens Blue e (Color 170A) in all specimens analyzed (including pertaining to the ornithological collections of the American those examined through photographs). Museum of Natural History (AMNH), Academy of Natural Four states were recognized for the color of Sciences of Philadelphia (ANSP), Carnegie Museum of underparts, namely Pale Horn (Color 92), Cream (Color Natural History (CMNH), Collección Ornitológica Phelps 54), Straw Yellow w (Color 56) and Spectrum Yellow w (Color (COP), Field Museum of Natural History (FMNH), 55) (Figure 1), while the color of wing coverts presented Muséum National d’Histoire Naturelle (MNHN), and three states, namely Ultramarine Blue e (Color 170A), Yale Peabody Museum (YPM) (Appendix II). Photographs Sky Blue e (Color 168C) and Turquoise Green (Color 64) examined include those of the type specimens of Tangara (Figure 2). Ultramarine Blue e wing coverts always occurred mexicana boliviana a [formerly Callospiza boliviana] together with Spectrum Yellow w or Straw Yellow w underparts, (MNHN 7897), Tangara mexicana media a [formerly y Calliste while Turquoise Green wing coverts were accompanied by mexicana media] (AMNH 513316) and Tangara boliviana Pale Horn, Cream and Straw Yellow w underparts. Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga FIGURE 1. Color character states of underparts in Tangara mexicana. Colors from left to right: Pale Horn (MPEG 22995), Cream (MPEG 21553), Straw Yellow w (MPEG 43353), and Spectrum Yellow w (MPEG 23003). FIGURE 2. Color character states of lesser upper-wing coverts in Tangara mexicana. From left to right: Ultramarine Blue e (AMNH 513329), Sky Blue (AMNH 278331) and Turquoise-Green (AMNH 513315). Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga Geographic distribution of character states were widely distributed across western Amazonian Brazil, southern Colombia, eastern Peru and northern Bolivia Specimens with Pale Horn underparts were recorded (Figure 3). exclusively from the north of the lower Amazon (Guyanas Ultramarine Blue e wing coverts were predominant in and adjacent parts of Brazil). Specimens with Cream the upper Amazon, with some specimens occurring on underparts were recorded from the upper Rio Branco to the southern bank of middle and lower Amazon. Birds the Rio Orinoco in Venezuela. Several birds with Straw with Turquoise Green humeral patches were restricted Yellow w underparts were from the southern bank of middle to the north of the lower Amazon, Guyanas, upper Rio and lower Amazon (lower Rio Madeira, Rio Tapajós, Branco, Venezuela and Trinidad. Specimens with Sky Blue Rio Xingu and Rio Tocantins) but also from the upper humeral patches were found mainly in the southern bank Rio Negro, northern Guyana and all specimens from of the lower and middle Amazon, but also in the upper Trinidad. Specimens with Spectrum Yellow w underparts Rio Negro (Figure 4). FIGURE 3. Geographic distribution of underparts color character states in Tangara mexicana a (black circles – Spectrum Yellow, gray circles – Straw Yellow, light gray circles – Cream, black squares – Pale Horn). FIGURE 4. Geographic distribution of lesser upper-wing coverts color character states in Tangara mexicana a (black circles – Ultramarine Blue, gray circles – Sky Blue, white circles – Turquoise-Green). Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga Morphotypes and their geographic distribution humeral patch (Figure 5). Th e distribution of morphotype 3 coincides with that of morphotype 2, ranging from the We found seven morphotypes that combine the diff erent left bank of the Rio Madeira to the lower Rio Tocantins character states (Figure 5). Five of these morphotypes (Figure 6). correspond to described taxa that have been considered Morphotype 4 is characterized by the combination subspecies of T. mexicana. of a Sky Blue e humeral patch and Straw Yellow w underparts Morphotype 1 is characterized by having the head, (Figure 5). It occurs from Belém to Manaus, and in upper throat, breast, rump and lesser upper-wing coverts Rio Negro (Figure 6). Ultramarine Blue e and Spectrum Yellow w underparts Morphotype 5 is characterized by having Straw (Figure 5). Specimens of this morphotype were found Yellow w underparts and Turquoise Green humeral patches from the eastern foothills of the Andes (Colombia, Peru (Figure 5). It was found in lower Rio Orinoco (Venezuela), and Bolivia), to lower Rio Negro and southern bank of northern Guyana and Trinidad (Figure 6). The holotype the lower Amazon (from the middle Rio Tocantins to of Calliste vieilloti, from Trinidad, was not examined, but the Marajó island). This morphotype was very poorl y supposedly would belong to this morphotype. represented in the lower Amazon (Figure 6). It includes Morphotype 6 has Cream underparts and Turquoise the holotype of Callospiza boliviana. Green humeral patches (Figure 5). It is widely distributed Morphotype 2 differs from morphotype 1 only in central Venezuela and upper Rio Branco in Brazil by the underparts, which are Straw Yellow (Figure 5). (Figure 6). It includes the holotype of Calliste mexicana It was found on the southern bank of the middle and media. lower Amazon, between the right bank of the lower Rio Morphotype 7 diff ers from all other morphotypes by Madeira and the region of Belém (Figure 6). It includes having Pale Horn underparts and Turquoise Green humeral the holotype of Tangara boliviana lateralis. patches (Figure 5). Specimens of this morphotype were Morphotype 3 is similar to morphotype 1 with from the Guyanas and north of the lower Amazon (Figure respect to the color of underparts, but it has Sky Blue 6). It corresponds to the nominate T. m. mexicana. FIGURE 5. Morphotypes of Tangara mexicana a based on the combined coloration of underparts and lesser upper-wing coverts (drawing: Raphael Dutra). See text for details. Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga FIGURE 6. Geographic distribution of morphotypes of Tangara mexicana a recognized in this study, showing a possible hybrid zone highlighted in gray. DISCUSSION is difficult, and could be more easily accom plished by a phylogeographic study. Th erefore, our data can be viewed Our analyses revealed the existence of at least two main as evidence supporting alternative scenarios of Turquoise Tanager diversifi cation to be tested by future genetic areas of plumage color character state stability in the Turquoise Tanager (corresponding to morphotypes 1 studies. and 7), separated by a smaller geographic area where Based on the General Lineage Species Concept (de intermediate phenotypes are present, sometimes even at Queiroz 1998), in which the only necessary property of a the same locality (corresponding to morphotypes 2-6) species is existence as a separately evolving metapopulation lineage (de Queiroz 2005), we propose that morphotypes (Figures 5 and 6). Two alternative interpretations of this overall pattern are: 1) morphotypes 1 and 7 represent 1 and 2 of T. mexicana found in this study would deserve evolutionary independent lineages / taxa that intergrade the status of separate species. These two mor photypes along a wide northwestern-southeastern trend hybrid have been traditionally recognized as the most distinct zone across Central Amazonia; or 2) morphotypes 1 subspecies of the Turquoise Tanager (Zimmer 1943). One of these (T. m. mexicana) occurs on the Guiana and 7 are extremes of a cline, with a corresponding wide intergradation zone in Central Amazonia. Below, we shield, being diagnosed by having Pale Horn underparts discuss these two alternatives with respect to the plumage and a contrasting Turquoise-Green humeral patch, while color data but stress that distinguishing between them the other (T. m. boliviana) is found from the base of the Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga Andes (below 500 m, following Hilty & Brown 1986) one in central Venezuela and upper Rio Branco in Brazil, to the southern bank of the middle and lower Amazon, including birds corresponding to morphotype 6 or T. being diagnosed by having Spectrum Yellow w underparts m. media, with Cream underparts and a Turquoise-Green and the wing coverts indistinguishable from the blue of humeral patch, and the other in Trinidad and northern the rest of the plumage. Venezuela, including birds corresponding to morphotype According to Hellmayr (1936) and Zimmer (1943), 5 or T. m. vieilloti, with Straw Yellow w underparts and a however, the challenge for understanding the complex Turquoise-Green humeral patch. However, the diagnose of pattern of geographical differentiation in T. mexicana these two morphotypes may be subtle in practice, so that is in the regions of the middle Amazon and southern both could alternatively be regarded as part of a larger bank of the lower Amazon. In this area we have found a polymorphic population ranging widely across central significant individual variation in the color of underparts, Amazonia, from northern Venezuela and Trinidad to with birds at times showing them Spectrum Yellow w and the south of the lower Amazon (lower Rio Madeira to Straw Yellow w in the same locality. In the northern Amazon Belém). This includes forms described as T. m. vieilloti, (upper Negro, Branco and Orinoco rivers) and Trinidad, T. m. media a and T. m. lateralis, consisting of birds with although individual variation in the tone of yellow is less character states that are intermediate between those found evident, some specimens are clearly distinct from others in T. m. mexicana a and T. m. boliviana. As pointed out by with respect to this character, as stated by Hellmayr Price (2008), subspecies rank has been often mistakenly (1936). Th e apparent phenotypic stability of the birds assigned considering populations with different levels from Trinidad could result from the founder effect due of character intergradation between distinct species. to ca. 11,000 years of isolation from the continent (Snow However, more studies on birds of Venezuela and Trinidad 1985). However, some birds from the coast of Venezuela are needed to improve understanding of the taxonomic are barely distinct from those of Trinidad. status of T.m. media a and T.m. vieilloti. Th e color of lesser upper-wing coverts is another The existence of a rather lar ge area of polymorphism important variable character among populations of T. linking areas of phenotypic stability seems to preclude mexicana. While specimens from the Guyanas and north interpretation of morphotypes 1 and 7 as extremes of of the lower Amazon, upper Rio Branco, Venezuela a clinal pattern of variation in the Turquoise Tanager. and Trinidad have the wing coverts forming a bright Th is whole range occupied by intermediate birds could Turquoise-Green humeral patch, birds from the southern be better considered as a hybrid zone because of the bank of the middle and lower Amazon and upper Rio considerable phenotypic instability detected (distinct Negro have a Sky Blue e or Ultramarine Blue e humeral phenotypes coexisting in the same regions), which patch. All specimens from western Amazonia have dark is more evident especially in the region between the blue (Ultramarine Blue e) wing coverts. There is a trend to lower Madeira River east across the Tocantins River in the occurrence of a lighter blue humeral patch in birds the Belém area. A relatively narrow hybrid zone along of the lower Amazon, as stated by Hellmayr (1936) and the Amazon valley has also been found between two Zimmer (1943). However, birds with dark blue wing purported phylogenetic species (Icterus chrysocephalus and coverts also occur in the southern bank of the lower Icterus cayanensis s)(D’Horta et al. 2008). As advocated Amazon, and are indistinguishable from specimens from by Hellmayr (1936), who nevertheless recognized the the upper Amazon, which reveals the instability of this taxonomic validity of T. m. media a and T. m. vieilloti, this character in the lower Amazon. phenotypic instability does not allow a diagnosis of T. m. Our analysis of geographical variation in plumage lateralis, described by Todd (1922) from the region of characters, thus, revealed the existence of at least two the Rio Tapajos and recognized by Gyldenstolpe (1945). major and up to four nuclear areas (with phenotypic Zimmer (1943), in turn, also preferred to consider stability) in T. mexicana. One of these coincides with the populations from the lower Amazon as an unstable and Guyana Center of Endemism (Cracraft 1985), including intermediate T. m. mexicana/T. m. boliviana a population, birds corresponding to morphotype 7 or T. m. mexicana. in which the recognition of a taxon is rather questionable. Another nuclear area is located in western Amazonia, encompassing the Napo and Inambari centers of endemism (Cracraft 1985), and including birds corresponding to A A ACKNOWLEDGMENTS morphotype 1 or T. m. boliviana. According to Zimmer (1943), these two forms have evolved separately when We are grateful to Jorge Bruno Nacinovic, Marcos Raposo “an arm of the sea occupied the Amazon valley”, T. m. (MNRJ), Alexandre Aleixo, Fátima Lima (MPEG), and mexicana a in the Guiana shield and T. m. boliviana a in Luís Fábio Silveira (MZUSP) for permission to examine western Amazonia. Two additional smaller areas of specimens under their care. Th omas J. Trombone apparent phenotypic stability occur between those two, (AMNH), Leo Joseph (ANSP), Stephen Rogers Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga Isler, M. L. & Isler, P. R. 1987. Th e Tanagers. Washington: (CMNH), Robin Restall (COP), Shannon Kenney, Paul Smithsonian Institution Press. Sweet, Mary Hennen (FMNH), and Kristof Zyskowski Paynter Jr., R. 1982. Ornithological Gazetteer of Venezuela. Cambridge: (YPM) kindly provided photographs of specimens. Museum of Comparative Zoology, Harvard University. Raphael Dutra kindly drew the bird illustrations. Paynter Jr., R. & Traylor Jr., M. 1991. Ornithological Gazetteer of Brazil. Cambridge: Museum of Comparative Zoology, Harvard University. Peters, J. L. 1970. Check-List of Birds of the World d d, v. 13. Cambridge: R R REFERENCES Harvard University Press. Piacentini, V. de Q.; Aleixo, A.; Agnes, C. E.; Maurício, G. N.; Barker, F. K.; Burns, K. J.; Klicka, J.; Lanyon, S. M. & Lovette, I. J. Pacheco, J. F.; Bravo, G. A.; Brito, G. R. R.; Naka, L. N.; Olmos, 2013. Going to extremes: contrasting rates of diversification in a F.; Posso, S.; Silveira, L. F.; Betini, G. S.; Carrano, E.; Franz, I.; recent radiation of New World passerine birds. Systematic Biology, Lees, A. C.; Lima, L. M.; Pioli, D.; Schunck, F.; Amaral, F. R. 62(2): 298-320. do; Bencke, G. A.; Cohn-Haft, M.; Figueiredo, L. F. A.; Straube, Berlepsch, H. 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Associate Editor: Gustavo Sebastián Cabanne Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga APPENDIX X I. Material examined d (Specimens from each locality in parenthesis). TRINIDAD. Trinidad (MZUSP 3706); VENEZUELA. Monagas: Maturin (MZUSP 2476); COLÔMBIA. Bogotá (MNRJ 6808); BRAZIL. Roraima: Alto Mucajaí (MPEG 21553; MZUSP 56239); Caracaraí (MPEG 56485); Amapá: Serra do Navio (MNRJ 29248); Fazenda Prosperidade, Rio Maracá, Mazagão (MPEG 22990; MPEG 22995); Rio Vila Nova, Macapá (MPEG 22991); Estrada do Curiaú km 01, Ilha Curuçá, Macapá (MPEG 28873); Igarapé Ariramba, afluente direito do Rio Tartarugal, Acampamento 4, Amapá (MPEG 28874); Rio Maruanum, Macapá (MPEG 28388); Fazenda Nova Califórnia, Rio Araguari (MPEG 22994); Fazenda Itauqueira, Tartarugalzinho (MPEG 53651; MPEG 53652); Oiapoque (MPEG 22996); Acre: Cruzeiro do Sul, Rio Juruá (MPEG 22997; MPEG 22998); Vila Taumaturgo, Seringal Oriente, Rio Juruá (MPEG 23000; MPEG 23001); Amazonas: São Gabriel da Cachoeira (MZUSP 16979); Acajutuba, Rio Negro (MPEG 12106); Maraã, margem esquerda do Rio Japurá, Maguari (MPEG 42934; MPEG 43352; MPEG 43353); Caitaú, margem direita do Rio Solimões, Uará (MPEG 50197; MPEG 50198); Santa Cruz, Rio Eirú, Juruá (MZUSP 18498; MZUSP 18504); Santo Antônio do Içá (MZUSP 69910); Bom Lugar, Rio Purus (MPEG 3499); Rio Jutaí (MZUSP 69909); Manacapuru (MNRJ 6816; MZUSP 16977; MZUSP 16978); Reserva Ducke, Manaus (MPEG 30079; MPEG 30370; MPEG 30371); Itacoatiara (MNRJ 32790; MNRJ 32791; MZUSP 17798; MZUSP 18499; MZUSP 18500; MZUSP 18501; MZUSP 18502; MZUSP 18505; MZUSP 18506); Igarapé Anibá (MZUSP 18496; MZUSP 18508); Rio Maraú (MZUSP 62116); Lago Baptista (MPEG 18493; MZUSP 17797; MZUSP 18494; MZUSP 18495; MZUSP 18497); Pará: Rio Paru (MNRJ 27369; MNRJ 27370; MNRJ 27371); Ilha de Marajó, cerca de 4km ao sul de Chaves (MPEG 58095); Santa Bárbara, Benevides (MPEG 22190); Portel, Rio Anapu (MPEG 23012; MPEG 23014); Val-de-Cans (MPEG 23672); Utinga, Belém (MZUSP 36041; MZUSP 36098; MZUSP 36100; MZUSP 36101); Providência, Belém (MPEG 5543; MPEG 7741); Vila do Outeiro, Ilha de Caratateua, Belém (MPEG 29883; MPEG 29884); Murutucu (MZUSP 36099); Igarapé Pucuruzinho, BR-422, km 67, Tucuruí/Novo Repartimento (MPEG 35346; MPEG 47957); Santarém (MZUSP 3359; MZUSP 3360); Fordlândia, Rio Tapajós (MZUSP 47352; MZUSP 47353); Aramanaí, Rio Tapajós (MZUSP 32773); Sumaúma, Rio Tapajós (MZUSP 47354); Villa Braga, Rio Tapajós (MNRJ 6815; MPEG 13126); Boim, Rio Tapajós (MPEG 8581); Alcobaça, Rio Tocantins (MPEG 5373); Tocantins: Araguatins (MPEG 20682; MZUSP 53054; MZUSP 65820; MZUSP 66095; MZUSP 66096); Rondônia: Guajará-Mirim, Rio Mamoré (MPEG 23002; MPEG 23003; MPEG 23005; MPEG 23006; MPEG 23008; MPEG 23010); Cachoeira Nazaré, margem oeste do Rio Jiparaná (MPEG 40290); Mato Grosso: Salto de Sepotuba (MNRJ 6809); Salto do Rio Jauru (MNRJ 6810); Fazenda São José, Rio Peixoto de Azevedo (MPEG 33846); PERU. Ucayali i i: Pucallpa (MZUSP 68248). Revista Brasileira de Ornitologia, 23(3), 2015 Geographic variation in plumage coloration of Turquoise Tanager Tangara mexicana (Linnaeus, 1766) Francisco Mallet-Rodrigues and Luiz Pedreira Gonzaga APPENDIX X II. Specimens examined through color photographs (Specimens from each locality in parenthesis). TRINIDAD. Santa Cruz (YPM 26422); Brasso, Caroni (YPM 26427); Caroni Swamp, Caroni (YPM 26428); VENEZUELA. Delta Amacuro (COP 48307); Sucre e (COP 56715; COP 56715; COP 56715; COP 56715; COP 56715; COP 56715; COP 56715) Amazonas (COP 21207; COP 21208; COP 21209; COP 21391; COP 22153; COP 22154; COP 22155; COP 38788; COP 69709; COP 69710; COP 69711; COP 69712); Bolívar (COP 16591; COP 16592; COP 17977; COP 17978; COP 17979; COP 26062; COP 26063; COP 26064; COP 26065; COP 45212); GUYANA. Georgetown (FMNH 32389; FMNH 32390); North West District t t: Koriabo (FMNH 190651; YPM 26429); Demerara- Berbice: Rio Essequibo, Rockstone (FMNH 108649); Potaro-Siparuni: Rio Essequibo, Iwokrama Reserve (ANSP 189019); Rio Abary (ANSP 189015; ANSP 189016; ANSP 189018); Mahaica-Berbice: Onverwagt (ANSP 189020); FRENCH GUYANA. Mana: Mana (YPM 31203; YPM 31204; YPM 31205); COLOMBIA. Vichada: Maipures (AMNH 513316) [type specimen of T. m. media]; Meta: Serrania de Macarena, Rio Guapaya (FMNH 249262; FMNH 249263); Caquetá: Morelia (ANSP 152949); Putumayo: Guascayaco (FMNH 282349); Mocoa (FMNH 282350); Santo Antonio Guamez (FMNH 287583); Umbria (ANSP 160131); Rio San Miguel (ANSP 165547); Rio Rumyiaco (ANSP 165546);; BRAZIL. Amazonas: Padauari (COP 35056; COP 35057; COP 35059; COP 35060; COP 35061); Manacapuru, Solimões (ANSP 67172; ANSP 67173); Pará: Castanhal (ANSP 80760; ANSP 80761); Apacy, Rio Tapajós (CMNH 78031)[type specimen of T. m. lateralis s]; Pinhy, Rio Tapajós (ANSP 108373); PERU. Napo: Apayucu (ANSP 83750); San Martin: San Martin (ANSP 116134); Yurinaqui (ANSP 176557); BOLÍVIA. Huanay: Rio Mapiri (ANSP 119228; ANSP 119229; ANSP 119230); Santa Cruz: Guarayos (MNHN 7897)[type specimen of T. m. boliviana]. Revista Brasileira de Ornitologia, 23(3), 2015

Journal

Ornithology Research – Springer Journals

Published: Sep 1, 2015

Keywords: Amazonia; biodiversity; centers of endemism; hybrid zones; subspecies; taxonomy

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