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Taxonomy and molecular systematics of the Yellow-green Grosbeak Caryothraustes canadensis (Passeriformes: Cardinalidae)

Taxonomy and molecular systematics of the Yellow-green Grosbeak Caryothraustes canadensis... Revista Brasileira de Ornitologia 25(3): 176–189. ARTICLE September 2017 Taxonomy and molecular systematics of the Yellow-green Grosbeak Caryothraustes canadensis (Passeriformes: Cardinalidae) 1,4 2 2 3 Vinicius Rodrigues Tonetti , Fernanda Bocalini , Luís Fábio Silveira & Glaucia Del-Rio São Paulo State University (UNESP), Department of Ecology, Av. 24A, 1515, 13506-900, Rio Claro, SP, Brazil. Museu de Zoologia da Universidade de São Paulo. Avenida Nazaré 481, Ipiranga, 04263-000, São Paulo, SP, Brazil. Museum of Natural Science, Louisiana State University, 119 Foster Hall, 70803, Baton Rouge, LA, USA. Corresponding author: vrtonetti@gmail.com Received on 20 November 2016. Accepted on 18 September 2017. ABSTRACT: The Yellow-green Grosbeak Caryothraustes canadensis is a South American passerine occurring in Amazon and Atlantic Forests. Currently, it comprises four subspecies: Caryothraustes canadensis canadensis, Caryothraustes canadensis brasiliensis, Caryothraustes canadensis frontalis and Caryothraustes canadensis simulans. No study has ever revisited its taxonomy, hindering a complete understanding of the available diversity in Caryothraustes canadensis complex. We examined color and morphometric variation in 259 scientific specimens and sequenced t he mitochondrial gene ND2 of 29 tissue samples. We also quantitatively and qualitatively analyzed 52 spectrograms of vocal recordings. Molecular analyzes demonstrated the existence of two divergent lineages in C. canadensis complex, one from Amazonia and the other in the Atlantic Forest, which can also be distinguished by morphometric and plumage characters. Here we propose that the C. canadensis complex is composed of two full species: C. canadensis and C. brasiliensis. Caryothraustes canadensis frontalis shows no reciprocal monophyly in the phylogenetic analyzes, despite having weak plumage diagnostic characters; therefore, we suggest it should be considered a synonym of C. brasilensis. KEY-WORDS: Amazon, Atlantic Forest, genetic analysis, Oscines, Pernambuco Endemism Center, phylogeny, vocal analysis. INTRODUCTION canadensis canadensis (Linnaeus, 1766) occurs in parts of the Brazilian Amazon Forest, Colombia, French Caryothraustes canadensis was described by Linnaeus Guiana, Guyana, Suriname and Venezuela. Other two (1766) based on a plate of a yellow-bellied, black masked sub-species are restricted to the Brazilian Atlantic Forest (Brewer 2016a): Caryothraustes canadensis brasiliensis bird individual from Cayenne, French Guiana (not Canada as erroneously interpreted and used to name the Cabanis, 1851 occurs in eastern Brazil in the states of species; Brewer 2016a). Long after, one related species Bahia, Espírito Santo, Minas Gerais and Rio de Janeiro, with a distinctive gray belly and occurring in Central and Caryothraustes canadensis frontalis (Hellmayr, 1905) America – Caryothraustes poliogaster (Du Bus de Gisignies, is endemic to the Pernambuco Endemism Center, i.e. the Atlantic Forest north of the São Francisco River (Silva 1847) – was described (Klicka et al. 2007, Brewer 2016b). Besides C. canadensis and Caryothraustes poliogaster, et al. 2004, Brewer 2016a). Cabanis (1851) separated C. the genus had already included the Yellow-shouldered c. brasiliensis from C. c. canadensis based on its brighter Grosbeak Caryothraustes humeralis (Lawrence, 1867). yellow forehead and Hellmayr (1905) described C. c. However, based on molecular analysis, C. humeralis is frontalis based on the unique black-strip on the forehead. Ultimately, Caryothraustes canadensis simulans is exclusive now in the monotypic genus Parkerthraustes (Remsen-Jr. 1997), family Thraupidae, while the genus Caryothraustes to northern South America and Central America and was is allocated in the family Cardinalidae (Burns et al. 2014, described based mostly on brighter colors, comprising Piacentini et al. 2015). more golden yellow on forehead, more yellowish olive Currently, the Yellow-green Grosbeak comprises four green on back and larger and heavier bill (Nelson 1912, Brewer 2016a, b). subspecies of small-size (~17 cm) passerines, all of which inhabit the canopy of tropical lowland forests in Central No other study has ever reanalyzed the taxonomy and South America where they forage for fruits and seeds of this group, hindering a complete understanding of the and emit a loud song (Brewer 2016a). Caryothraustes diversity in Caryothraustes canadensis complex. Taxonomic Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. studies are of paramount importance in delimiting 9.1.2 (2016), it was checked if the sequences did not species and indicating the true diversity of a given region, include stop codes or anomalous base, the alignment aiding studies of phylogeny and biogeography (Silveira & was performed using MAFFT v. 7 (Katoh et al. 2005) Olmos 2007). Moreover, they are crucial to biodiversity H-INS-i, F-INS-i and G-INS-i, in which pairwise conservation, as conservation programs frequently ignore alignment information are incorporated into objective threatened taxa at the subspecific or population levels function. These new options of MAFFT showe d higher (Zink 2004, Aleixo 2007). Accordingly, our aim was accuracy than currently available methods including to integrate molecular data with traditional plumage TCoffee version 2 and CLUSTAL W in benchmark coloration, morphometric and vocal data of the Yellow- tests consisting of alignments of >50 sequences. Like green Grosbeak to revise the taxonomy of this species. the previously available options, the new options of MAFFT can handle hundreds of sequences on a standard desktop computer. We also examined the effect of the METHODS number of homologues included in an alignment. For a multiple alignment consisting of \u223c8 sequences with Taxon sampling and laboratory procedures low similarity, the accuracy was improved (2\u201310 percentage points plug-in at Geneious. Genetic analysis was conducted using tissue samples of 29 specimens of three subspecies of the Yellow-green Phylogenetic analyses Grosbeak, C. c. brasiliensis (n = 11), C. c. frontalis (n = 7), C. c. canadenis (n = 11). Vouchers are housed in the Phylogenetic relationships among individuals were following institutions: Museu de Zoologia da Universidade inferred using the Maximum Likelihood (ML) in RAxML de São Paulo (MZUSP, Brazil), Field Museum of v. 7.2.7 (Stamatakis 2006), and Bayesian Inference (BI) Natural History (FMNH, EUA) and Museu Paraense in MrBayes v. 3.1.2 (Ronquist & Huelsenbeck 2003), Emílio Goeldi (MPEG, Brazil) (Table 1). We also added both on Cipres Science Gateway v. 3.1 (Miller et al. sequences available on Genbank for C. c. simulans 2010). The best-fitting model of evolution for BI analysis (EF529916.1), Caryotrhaustes poliogaster poliogaster was estimated using the Bayesian Information Criterion (EF529915.1), Periporphyrus erythromelas (EF529919.1), (BIC) in jModelTest v. 2.1.6 (Darriba et al. 2012) and Rhodothraupis celaeno (EF529920.1) and Cardinalis HKY+G were selected as the best fitting model. BI cardinalis (JF795780.1). The last three were used as analysis was performed using two independent runs with outgroups following Klicka et al. (2007) and Cardinalis 10,000,000 generations each, 4 chains, the parametres cardinalis was used to root the trees. and the trees were be sampled every 1000 generations Total genomic DNA was extracted using the and the burn-in was 20%, the posterior probabilities for Genomic DNA Mini Kit (Invitrogen). The mitochondrial each estimated node were obtained through a majority molecular marker NADH Dehydrogenase Subunit 2 rule consensus of the remaining MCMC samples. ML (ND2, 1041 bp) was amplified using primers L5215, analysis was done using a GTR-GAMMA model, with H6313, L5758, H5766 (Hackett 1996, Sorenson et al. 100 independent searches, nodal support was estimated 1999) mitochondrial DNA (mtDNA. Polymerase chain with 1000 bootstrap replicates. Additionally, mean reaction (PCR) amplifications were performed using an pairwise p-distances among populations were calculated initial denaturation step at 94 C for 2 min, followed in MEGA v. 7.0 (Kumar et al. 2016). by 35 cycles of 94 C for 1 min, a 30 s annealing step at 50 C, and a 72°C extension for 1 min, and the final Taxonomic assessment extension was at 72°C for 7 min. In a 25 μL total volume, PCR amplifications contained approximately 20 ng of Supported clades in the phylogenetic analyses were used genomic DNA, buffer 10 ×, 200 mM of DNTPs, 1.5 as a priori clades for the study of phenotypic diagnostic mM of MgCl , 0.4 μM of each primer (forward and characters. We examined a total of 163 skins of the reverse), 0.2 × of BSA, and 0.1 U of Platinum Taq DNA three C. canadensis subspecies (107 belonging to C. c. Polymerase (Invitroven). PCR products were visually canadensis, 19 to C. c frontalis and 37 to C. c. brasiliensis) inspected in a 1% agarose gel, after electrophoresis, and housed in the Museu de Zoologia da Universidade de São positive results were purified using PEG precipitation Paulo (MZUSP, Brazil) and the Museu Paraense Emílio protocol. Sequencing was carried out on an ABI 3130 Goeldi (MPEG, Brazil) (see Appendix I). We did not automated capillary sequencer (Applied Biosystems) with have personal access to C. c. simulans, what prevented the ABI Prism Big Dye terminator Kit. Both strands us to include this taxa in this review. By the time this and one internal primer of each sample were sequenced. research was conducted, a spectrometer was not available, Sequences were edited and aligned using Geneious v. restricting colorimetric analysis to comparisons to color Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Table 1. Voucher information of Caryothraustes canadensis tissue samples. Museum Taxon Locality MZUSP 91568 Caryothraustes canadensis brasiliensis Brazil, Bahia, Mata do Pacange, Reserva Michelin MZUSP 91569 Caryothraustes canadensis brasiliensis Brazil, Bahia, Mata do Pacange, Reserva Michelin MZUSP 98351 Caryothraustes canadensis brasiliensis Brazil, Espirito Santo, Reserva Florestal CVRD MZUSP 98352 Caryothraustes canadensis brasiliensis Brazil, Espirito Santo, Reserva Florestal CVRD MZUSP 98350 Caryothraustes canadensis brasiliensis Brazil, Espirito Santo, Reserva Florestal CVRD MZUSP 101537 Caryothraustes canadensis brasiliensis Brazil, Bahia, Camacan, Serra das Lontras MZUSP 101536 Caryothraustes canadensis brasiliensis Brazil, Bahia, Camacan, Serra das Lontras MPEG 70826 Caryothraustes canadensis brasiliensis Brazil, Bahia, Ilheus Ecoparque de UNA MPEG 70827 Caryothraustes canadensis brasiliensis Brazil, Bahia, Ilheus Ecoparque de UNA MPEG 70825 Caryothraustes canadensis brasiliensis Brazil, Bahia, Ilheus Ecoparque de UNA MPEG 79859 Caryothraustes canadensis brasiliensis Brazil, Bahia, Amargosa, Serra do Timbo Brazil, Amazonas, Sucunduri River (right margin), in front MZUSP 96547 Caryothraustes canadensis canadensis of Castanho Island MZUSP 96548 Caryothraustes canadensis canadensis Brazil, Amazonas, lower Canuma River (right margin) MZUSP 96549 Caryothraustes canadensis canadensis Brazil, Amazonas, lower Canuma River (right margin) MPEG 65547 Caryothraustes canadensis canadensis Brazil, Pará, Alenquer, ESEC Grao-Para Brazil, Pará, Itaituba, FLONA Amaná, right margin Amana MPEG 65661 Caryothraustes canadensis canadensis River Brazil, Pará, Itaituba, FLONA Amaná, right margin Amana MPEG 65660 Caryothraustes canadensis canadensis River MPEG 66890 Caryothraustes canadensis canadensis Brazil, Pará, Faro, Maracana Village, Xingu River MPEG 74145 Caryothraustes canadensis canadensis Brazil, Pará, Santarém, RESEX Tapajos/Arapiuns Capixaua MPEG 74146 Caryothraustes canadensis canadensis Brazil, Pará, Santarém, RESEX Tapajos/Arapiuns Capixaua MPEG 74147 Caryothraustes canadensis canadensis Brazil, Pará, Santarém, RESEX Tapajos/Arapiuns Capixaua MPEG 76879 Caryothraustes canadensis canadensis Brazil, Maranhão, Centro Novo, REBIO Gurupi MZUSP 98475 Caryothraustes canadensis frontalis Brazil, Alagoas, São Miguel dos Campos, Usina Porto Rico Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho FMNH 427231 Caryothraustes canadensis frontalis Coimbra Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho FMNH 427232 Caryothraustes canadensis frontalis Coimbra Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho FMNH 427233 Caryothraustes canadensis frontalis Coimbra Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho FMNH 427234 Caryothraustes canadensis frontalis Coimbra Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho MPEG 70547 Caryothraustes canadensis frontalis Coimbra Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho MPEG 70548 Caryothraustes canadensis frontalis Coimbra catalogues. To standardize color analyses, only VRT distance between nostril and bill tip, lower jaw width, compared forehead, crown, nape, back, rump, rectrices, right tarsus, right wing chord (i.e. closed wing-lenght) throat, malar, ear coverts, breast, belly and primaries and tail length with a caliper (precisions of 0.005 mm) colors with a Villalobos & Villalobos (1947) color chart and a ruler (for wing and tail measurements with a for all museums specimens analyzed and under the same precision of 0.5 mm). light conditions. An additional 97 specimens housed in Museu de We collected measurements of exposed culmen, Biologia Professor Mello Leitão (MBML, Brazil; 22 C. c. Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. brasiliensis), Museu Nacional da Universidade Federal do descending or vice versa; Catchpole & Slater 2008). Rio de Janeiro (MNRJ, Brazil; 9 C. c. brasiliensis, 5 C. We used frequency and time resolution of 46.9 Hz and c. canadensis and 2 C. c. frontalis), Colección Ornitológica 1.06 ms respectively, and the qualitative analyses were Phelps (COP, Venezuela; 39 C. c. canadensis), Museum performed using the same window size to avoid shape of Natural Science of the Louisiana State University distortions in notes used in qualitative analysis (Charif (LSUMZ, USA; 11 C. c. canadensis and 1 C. c. simulans), et al. 2010). All notes were analyzed in black and white. Muséum National d'Histoire Naturelle (MNHN, France; To perform vocalization analysis, we used RAVEN 4 C. c. canadensis) and Museum für Naturkunde (ZMB, PRO v. 1.4 (Charif et al. 2010). From the 92 original Germany; 5 C. c. canadensis; Appendix I) were examined recordings, only 52 (25 of C. c. canadensis, 17 of C. c. via high quality pictures taken by some of us and brasiliensis and 10 of C. c. frontalis) had a reasonable colleagues (see Acknowledgements). All specimens were quality needed for analysis, i.e., allowed accurate photographed under white light. Although we did not measures. Recordings were obtained from the following compare the plumage of those individuals with color sound archives: Macaulay Library of Natural Sounds chart, we used their photographs as a post hoc analysis (CORNELL, Cornell University, USA); Arquivo Sonoro following valid species delimitation, aiming to confirm Elias Coelho (ASEC, UFRJ, Brazil); Fonoteca Neotropical the usefulness of the putative diagnostic characters. Jacques Vielliard (FNJV, UNICAMP, Brazil); Xeno- Canto (XC, http://www.xeno-canto.org); and also from Vocal analysis researchers who provided their personal recordings (see Appendix II). To measure MaF, MiF, BW, pF and Following Catchpole & Slater (2008), we defined a note duration we used only WAV sound fi les due their high as a continuous line on spectrogram and a phrase as a quality and precision, and we used WAV as well as MP3 sequence of similar notes followed each other by a short files to count NN and analyze note shapes. interval of time. Because the species emits two different types of phrase (defined here as Type-I and II; Fig. 1), Vocal and morphometric statistics we analyzed them separately. Type-I phrase is composed by “whistled” notes, and Type-II is composed by shorter We assayed for morphometric and vocal differences notes followed each other by a very short time lapse, between populations using parametric tests, when data popularly known as “trill” (Fig. 1). We measured the showed normality and homoscedasticity, or their non- maximum frequency (MaF), minimum frequency (MiF), parametric equivalents when these two assumptions bandwidth (BW), peak frequency (pF) and time duration were not fulfilled (Gotelli & Ellison 2012). Analysis of for each single note in Type- I phrases and for all Type-II variance (ANOVA; parametric) or Kruskal-Wallis (non- phrases and for all Type-II phrases as if they were a single parametric) were used to compare morphometric and note (Charif et al. 2010). We also counted the number of vocal differences between groups. The Tukey test, or its notes (NN) for all phrases. non-parametric equivalent Newman-Keuls, was used Besides the quantitative measurements cited above, as post hoc tests to investigate for significant pairwise we analyzed the aspect of Type-I notes, shaped by differences. Sexual dimorphism within putative groups frequency modulation. Frequency modulation occurs was tested using the Student's t or Wilcox tests. We used when the direction of frequency changes in y-axis of 0.05 as critical value of p and we did not use any p-value the spectrogram, thus causing inflections in the note corrections (e.g. Bonferroni) as this kind of correction is (i.e. frequency modulation changes from ascending to extremely conservative and its use has been discouraged Figure 1. Spectrogram exemplifying a song (CORNELL 127847) with two Type-I and one Type-II phrases. Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. by some authors (Nakagawa 2004, Gotelli & Ellison Morphometric analysis 2012). To assess diagnosability between clades indicated by phylogenetic trees, we log-transformed measurements Morphometry indicated higher similarity between birds for all the individuals studied and conducted discriminant from Atlantic Forest sites than those and Amazonian function analyses (DFA) in R software v. 3.2.2 (R Core locations. Except for the exposed culmen length, Team 2017), clustering groups by 95% confidence measurements did not differ significantly between the intervals. Except for the Newman-Keuls test (performed two Atlantic Forest lineages (P < 0.05; Table 3). The in the “agricolae” package in the R software; Mendiburu discriminant analysis of morphometric variation (Fig. 2015), we performed statistical analyses in the package 3) showed that the clades canadensis population 2 and “stats” (R Core Team 2017). brasiliensis/frontalis are diagnosable mainly by differences in exposed culmen and wing length (factor 1). The clade canadensis population 1 overlaps in size with brasiliensis/ RESULTS frontalis, its sister group. Molecular analysis Plumage variation Maximum-likelihood and Bayesian analyses produced Individuals from the Amazon Basin showed olive forehead similar topologies with high support, indicating that both coloration ranging mainly from Y-12 -6 (MZUSP Atlantic Forest taxa belong to the same clade (Fig. 2). 46064) to Y-12 -9 (MZUSP 46059; Fig. 4). There is Caryothraustes c. frontalis and C. c. brasiliensis are closely weak plumage diagnosis between the two Amazonian related, with only 0.3% of mitochondrial divergence clades pointed by phylogenetic trees, although the olive (mean p-distance, Table 2). On the other hand, head distinguishes both from the Atlantic forms. individuals of C. canadensis from the Madeira-Tapajós Although showing no genetic distinctiveness, interfluvium show 6.3% of mitochondrial divergence the subspecies C. c. frontalis and C. c. brasiliensis show from brasiliensis/frontalis. Phylogenetic trees also indicate consistent differences in forehead color. Birds from the that canadensis is not a monophyletic group, since it Atlantic Forest south of the São Francisco River, in comprises C. c. simulans and the C. brasiliensis/frontalis Brazilian states of Bahia, Espírito Santo, Minas Gerais clade. In this sense, two distinct groups of C. canadensis and Rio de Janeiro can be distinguished by a bright- form distinct Amazonian clades, one sister to the Atlantic yellow forehead (YYO-12 -10; MZUSP 6274, or YYO- form, restricted to the southern Amazon (from left bank 12 -11; MZUSP 24675). Forehead color did not vary in of Madeira to both banks of Tapajós River, herein called individuals from the Pernambuco Endemism Center; all population 1), and one containing individuals from birds from this region exhibited a discrete black forehead northern and eastern Amazon Forest (population 2). (Fig. 4). For specimens from the Amazon and Atlantic Table 2. Genetic p-distance (%) between Caryothraustes canadensis subspecies estimated using NADH dehydrogenase 2 (ND2) sequences. Caryothraustes canadensis canadensis was divided into the two populations evidenced in the phylogenetic analyzes. C. c. brasiliensis C. c. frontalis C. p. simulans C. c. canadenis (population 1) C. c. brasiliensis C. c. frontalis 0.3 C. c. simulans 6.7 6.6 C. c. canadensis (population 1) 6.2 6.1 6.5 C. c. canadensis (population 2) 6.4 6.3 5.8 5.5 Table 3. Morphological measurements (in mm) as mean ± standard deviation and range in parenthesis for each sampled taxa. Taxon Culmen Bill length Bill width Jaw height Tarsus Wing Tail 15.36 ± 0.96 11.51 ± 0.68 11.26 ± 0.51 6.6 ± 0.59 20.52 ± 0.97 88.9 ± 3.93 62.51 ± 6.08 C. c. canadensis (12.6 – 17.8) (9.6 – 13.4) (9.9 – 12.3) (5.65 – 11.5) (17.3 – 22.8) (72 – 99) (51 – 80) 16.63 ± 0.8 12.33 ± 0.63 12.7 ± 0.69 7.41 ± 0.43 22.02 ± 1.24 96.16 ± 3.21 70.81 ± 4.39 C. c. brasiliensis (15 – 18.8) (11.2 – 13.55) (11.55 – 14.9) (6.9 – 9.02) (19.5 – 25.3) (90 – 103) (66 – 83) 17.66 ± 0.83 12.8 ± 0.55 13.2 ± 0.57 7.6 ± 0.27 21.96 ± 1.29 95.18 ± 2.74 68.18 ± 3.41 C. c. frontalis (16.25 – 18.8) (11.9 – 13.85) (12.4 – 14.05) (6.95 – 7.85) (20.1 – 24.6) (90 – 100) (63 – 77) Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Figure 2. Phylogenetic relationships of Caryothraustes canadensis. (A) Maximum likelihood topology, nodes supports are bootstrap values. (B) topology obtained by Bayesian inference, node supports are posterior probabilities. Figure 3. Discriminant function analysis. Ellipses indicate clusters of populations by 95% intervals. Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Forest south of the São Francisco River crown and nape and primaries (Fig. 5; Table 4). Through t he analysis of showed the same color as the forehead (olive and bright- the photographs, C. c. simulans show brighter underparts yellow respectively), but of a slightly darker shade. The than the other specimens from Amazon basin. However, two Atlantic Forest subspecies showed the same pattern due to the low sample size (n = 1) we are not able to of crown and nape color (bright-yellow, Table 4), with conclude if it can be considered a full species. We did not small individual variation (ranging from YYO-12 -8; find sexually dimorphic features in any studied group. MZUSP 6274 to YYO-12 -10; MPEG 70547 for crown, o o and from YYO-12 -4; MZUSP 37733 to YYO-12 -6; Vocal variation MPEG 70827 for nape). Amazonian birds showed breast coloration ranging from olive-yellow (Y-12 -9; MZUSP No signifi cant differences (Newman-Keuls or Tukey tests 46072) to bright-yellow (YYO-12 -14; MZUSP 96546), P > 0.05) were observed in vocal characters between whereas the Atlantic Forest birds consistently showed the the songs of the three subspecies analyzed here (Tables same color (YYO-12 -11). The following parts of the body 5 & 6). Of the 52 vocalizations analyzed, individuals showed small, if any, variation between all individuals and emitted the Type-I phrase in 48 of them, and Type-II cannot be used as diagnostics characters: back, rump, in 39. In most recordings (70%), both types of phrases upper surface of tail, throat, malar parch, ear parch, belly were given, while in 23.5% and 5% only Type-I and II Figure 4. Lateral part of the head (upper left corner) and forehead (right side) of specimens: Caryothraustes canadensis frontalis (MZUSP 37731), Caryothraustes canadensis brasiliensis (MZUSP 34605) and Caryothraustes canadensis canadensis (MZUSP 46047). The distribution of all specimens analyzed is given in the map. Locations of genetic samples analyzed are represented by white symbols with black dots; specimens and recordings are represented by totally black symbols. Photograph location of Caryothraustes canadensis simulans is represented by a black star. Table 4. Colors found in specimens examined. Numbers in parenthesis indicate the proportion of individuals showing the respective colors. O = olive; Y = yellow; B = black; BY = bright-yellow; OY = olive-yellow. Malar Ear Taxon Forehead Crown Nape Back Rump Tail Wing Throat Breast Belly parch parch C. c. canadensis O O O O O O OY B OY O Y BY (107 specimens) (97%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) C. c. brasiliensis BY BY BY O O O OY B OY O BY BY (37) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) C. c. frontalis B BY BY O O O OY B OY O BY BY (19) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Figure 5. Dorsal (A), ventral (B) and lateral (C) parts of the body of specimens: Caryothraustes canadensis frontalis (MZUSP 37731; left A and B and upper C), Caryothraustes canadensis brasiliensis (MZUSP 34605; middle, south of São Francisco River) and Caryothraustes canadensis canadensis (MZUSP 46047; right A and B and bottom C). Table 5. Measurements of vocal variables of Type-I phrases as mean ± standard deviation and range, in parenthesis, for each taxa. Each variable was measured for each single note. Number = number of notes within each phrase. As different recor dings could have different number of phrases and notes, these values were extracted from the mean values of each recording. Maximum Minimum Bandwidth Peak frequency Taxon Time (s) Number frequency (kHz) frequency (kHz) (kHz) (kHz) Caryothraustes 5619 ± 938 1300 ± 230 4319 ± 944 3838 ± 444 0.148 ± 0.03 2.85 ± 1.17 canadensis canadensis (3773 – 8167) (1003 – 1898) (2439 – 7022) (3155 – 5054) (0.087 – 0.247) (1 – 5.5) Caryothraustes 5571 ± 1394 1160 ± 375 4411 ± 1506 4147 ± 655 0.205 ± 0.02 2.01 ± 0.72 canadensis brasiliensis (3854 – 7534) (846 – 2331) (2560 – 6687) (3281 – 5343) (0.134 – 0.239) (1 – 3) Caryothraustes 6732 ± 1478 1215 ± 248 5571 ± 1538 4197 ± 534 0.184 ± 0.02 2.57 ± 0.81 canadensis frontalis (4360 – 8464) (816 – 1584) (3333 – 7562) (3416 – 5203) (0.147 – 0.22) (1 – 4) Table 6. Measurements of vocal variables of Type-II phrases as mean ± standard deviation and range, in parenthesis, for each taxa. Each variable was measured for each entire phrase. Number = number of notes within each phrase. As different recor dings could have different number of phrases and notes, these values were extracted from the mean values of each recording. Maximum Minimum Bandwidth Peak frequency Taxon Time (s) Number frequency (kHz) frequency (kHz) (kHz) (kHz) Caryothraustes 8704 ± 938 2060 ± 297 6644 ± 945 6130 ± 955 0.124 ± 0.03 6.17 ± 1.44 canadensis canadensis (6674 – 9897) (1633 – 2851) (4941 – 8208) (4392 – 7838) (0.08 – 0.23) (4 – 10) Caryothraustes 8063 ± 1162 1961 ± 347 6101 ± 1229 5571 ± 586 0.176 ± 0.02 7.343 ± 1.26 canadensis brasiliensis (5963 – 10001) (1565 – 2827) (4036 – 7872) (4664 – 6773) (0.131 – 0.231) (5 – 9) Caryothraustes 8478 ± 613 1827 ± 348 6650 ± 613 5996 ± 190 0.169 ± 0.04 7.6 ± 1.79 canadensis frontalis (7284 – 9159) (1323 – 2565) (5502 – 7526) (5713 – 6304) (0.11 – 0.235) (5 – 10) Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. if they should be treated as separate species (Bocalini et al. in prep.). In the Atlantic Forest, we suggest that both forms should be treated as Caryothraustes brasiliensis, since it has priority over C. c. frontalis. Beside the black forehead, Hellmayr (1905) cited the bright-yellow breast as a diagnostic character for C. c. frontalis compared to specimens from other parts of the Atlantic Forest. Although for some specimens (e.g. MPEG 70547) we found slightly brighter breast when compared to some individuals of C. brasiliensis (e.g. MZUSP 91569), this was due to intraspecific variation and cannot be used to distinguish the two Atlantic Forest populations. In this sense, both groups share almost all plumage colors except on the forehead. Our phylogenetic trees indicate that C. c. brasiliensis and C. c. frontalis form a unique clade with very shallow divergence. As our results do not indicate reciprocal monophyly between the two taxa, here we synonymize C. c. frontalis in C. brasiliensis. Further analysis using genomic markers, such as ultraconserved elements Figure 6. Spectrograms exemplifying individual variation (Bocalini et al. in prep.) could clarify if the variation on found in qualitative voice analysis. Above are two recordings forehead color corresponds with phylogenetic divergence of Caryothraustes canadensis brasiliensis from Espírito Santo of the two populations putatively isolated by the São state, Brazil (FNJ 9140 [A]; ASEC JMB07514 [B]) and below is one recording of Caryothraustes canadensis canadensis from Francisco River barrier. the Amazonas state, Brazil (CORNELL 127705 [C]). Contrary Besides that, the clade formed by C. c. simulans is to expectations, we observed more similarity between the supported by our phylogenetic trees, and photography recordings B and C (different species) t han between A and B analyses reveal slight plumage differences when compared (same species). to C. canadensis and the Atlantic forms. However, as we used only one sequence from the GenBank and few specimens were studied by us, we prefer to keep its current status until we collect enough morphometric, voice and were observed, respectively. A total of 859 Type-I notes genomic data (Bocalini et al. in prep.). (in 349 Type-I phrases) and 210 Type-II phrases were individually measured. We measured all Type-I notes and Vocal analysis all Type-II phrases available in all analyzed recordings. As the recordings did not have the same number of notes Within the order Passeriformes there is a dichotomy and phrases, we performed the tests using a simple mean between the usage of song in taxonomy of species for each recording to avoid pseudoreplication. Qualitative included in the Oscines and Suboscines suborders analysis of Type-I phrases, measured by visual analysis (Raposo & Höfling 2003). Laboratory experiments and of the shape of the notes, showed a great variation even field studies have suggested that some suboscine species within the same locality and, therefore, could not be used songs are innate (i.e. genetically defined, without changes to diagnose taxa (e.g. Fig. 6). associated to learning) and the species are unable to learn their songs (Stein 1963, Payne & Budde 1979, Kroodsma DISCUSSION 1984). Conversely, variations observed in oscine songs have been thought as consequence of a learning ability, and theoretically with no taxonomic value (Marler & Tamura Plumage variation and diagnosis 1962). These assumptions made decades ago and for a limited species have been used to support the separation Our phylogenetic trees support the existence of two Amazonian clades, that although weakly diagnosable of a variety of suboscine taxa (e.g. Willis 1992, Whitney et al. 1995, Isler et al. 1998, Zimmer 2008, Carneiro et between them in terms of size, voice and plumage, are al. 2012), while few attempts have been made to use song both different in forehead color when compared to the in the taxonomy of oscine species (Raposo & Höfling Atlantic forms. Here we propose that the Amazonian 2003, but see Cadena & Cuervo 2010). However, based clades should be treated as Carytohraustes canadensis until genomic data or more detailed morphological data reveal on recent empirical evidence, this dichotomy has been Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. revised (Payne 1986, Trainer et al. 2002, Price & Lanyon – see, for example, that some of the best sampled 2002, Cadena & Cuervo 2010, Kroodsma et al. 2013). Amazonian localities (Serra dos Carajás and Fartura Although the use of oscine vocalization in Farm) are within Tapajós-Tocantins interfluvium and taxonomy is encouraged by some authors (Raposo & has no record of the Yellow-green Grosbeak (Pacheco et Höfling 2003) and could be used to diagnose species in al. 2007, Somenzari et al. 2011, Aleixo et al. 2012) and Arremon torquatus complex (Cadena & Cuervo 2010) other well-sampled regions west from Madeira River have in addition to corroborating phylogenetic relationships also not accounted for the species (Gyldenstolpe 1945, for Dendroica Warblers (Payne 1986) and Oropendolas 1951, Guilherme 2012). A few other Amazonian species (genera Psarocolius, Gymnostinops, and Ocyalus) (Price show similar distributions patterns (i.e. present in some & Lanyon 2002), our analysis found that none of the interfluvium and a bsent in others), albeit not exactly as vocalization characters used were useful in delimiting C. canadensis, such as Chestnut-crowned Foliage-gleaner the proposed species. This was similar to other study Automolus rufipileatus, Dusky-capped Greenlet Hylophilus with Wrens Troglodytes (Rice et al. 1999); these birds hypoxanthus, and Black Bushbird Neoctantes niger, which also have a complex and highly-variable song. Despite present disjunct populations with an absence area in the the relatively small sample size (52 recordings analyzed), intermediate region (Ridgely & Tudor 2009). high levels of individual variation in qualitative analysis prevented us from identifying diagnosable groups. For Taxonomy of the Yellow-green Grosbeak example, it is possible to find greater differences in the shape of notes between single recordings of birds from Caryothraustes canadensis (Linnaeus, 1766) the state of Espírito Santo (Fig. 6A & B), than between English name: Yellow-green Grosbeak recordings from Espírito Santo and Amazonas (Fig. 6C). Portuguese name: Furriel This was contrary to the expectation that recor dings Loxia canadensis Linnaeus 1766: 304 from individuals that belong to the same species (e.g. C. Pitylus viridis Sclater 1886: 306 brasiliensis, Figs. 6A & B) would be more similar than Pitylus canadensis Snethlage 1914: 461 recordings of different species (e.g. C. brasiliensis, Figs. Caryothraustes canadensis canadensis Peters 1970: 224 6B and C. canadensis, Fig. 6C). This likely reflects song- Type-locality: Cayenne, French Guiana learning ability within Caryothraustes species. In relation Diagnosis: individuals can be distinguished from other to quantitative analysis, as well as shape of notes, it is Caryothraustes species by the presence of olive color on possible that high levels of variation prevented us from forehead, crown and nape. Although Amazonian birds diagnosing the groups of individuals by their song. have significantly smaller body size in comparison to However, because oscine song proved useful in taxonomic the other two species (Fig. 3; Table 3), due to overlap in and systematic previous studies (see above), we suggest measurements it cannot be used as a diagnostic character. it should be tested with other passerines and at different Average dimensions (mm): bill length 11.5; tail 62.5; taxonomic levels (e.g. populations) in an attempt to tarsus 20.5; wing 89. delimit differentiated taxa (Raposo & Höfling 2003). Distribution: mostly Amazon Basin in southern Colombia, eastern and southern Venezuela, in most parts of Guyana, Distribution remarks French Guiana and Suriname and on both banks of Negro, Trombetas and Jari Rivers in Brazil. In the southern Recent records on the right bank of the Parnaíba River, in Amazon it occurs in the Madeira-Tapajós interfluve and the Brazilian state of Piauí (Simas 2016) may represent on the right bank of Tocantins River. It seems that the the southeastern range limit of C. canadensis. Northwest southeastern range limit to its distribution occurs on the Piauí occurs in a very extensive ecological transition zone east bank of Parnaíba River, out of Amazon Basin and in between the Amazon, Cerrado and Caatinga domains the municipality of Altos, Piauí, Brazil (Simas 2016. and has semideciduous forests as its predominant vegetation type (IBGE 2012). Bird inventories in the western part Caryothraustes canadensis simulans Nelson 1912 of that state have recorded Amazonian taxa (e.g. the Pied English name: Cana Green Grosbeak Puff bird Notharchus tectus and the Rufous-capped Antthrush Type locality: Cana, eastern Panama Formicarius colma amazonicus; Santos et al. 2010). Additionally, there is an apparent gap in the Diagnosis: underparts yellowish olive green and smaller distribution of C. canadensis in the Tapajós-Tocantins than other members of C. canadensis (Nelson 1912, interfluvium, in southern Amazonia, as well as in the Hellmayr 1938). Average dimensions (mm): bill length Inambari Center of Endemism. These absences might 18; tail 66; wing 86 (Hellmayr 1938). not arise from sampling problems, once these regions Distribution: eastern Panama and northern Colombia have historically been as much sampled as the others (Hellmayr 1938). Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Brewer D. 2016a. Yellow-green Grosbeak (Caryothraustes canadensis). Caryothraustes brasiliensis Cabanis, 1851 In: del Hoyo J., Elliot A., Sargatal J., Christie D. & de Juana E. English name: Yellow-faced Grosbeak (eds.). Handbook of the birds of the world alive. http://www.hbw. Portuguese name: Furriel-do-sul com/node/62190 (access on 14 June 2017). Caryothraustes brasiliensis Cabanis 1851: 144 Brewer D. 2016b. Black-faced Grosbeak (Caryothraustes poliogaster). In: del Hoyo J., Elliot A., Sargatal J., Christie D. & de Juana E. Pitylus brasiliensis Sclater 1886: 306 (eds.). Handbook of the birds of the world alive. http://www.hbw. Pitylus canadensis frontalis Hellmayr 1905: 277 com/node/621890 (access on 14 June 2017). Caryothraustes canadensis brasiliensis Peters 1970: 226 Burns K.J., Shultz A.J., Title P.O., Mason N.A., Barker F.K., Caryothraustes canadensis frontalis Peters 1970: 225 Klicka J., Lanyon S.M. & Lovette I.J. 2014. Phylogenetics and diversification of tanagers (Passeriformes: Thraupidae), the largest Type-locality: Bahia, Brazil radiation of Neotropical songbirds. Molecular Phylogenetics and Diagnosis: specimens north to the São Francisco River Evolution 75: 41–77. show distinctive black stripe on the forehead in contrast to Cabanis J. 1851. Museum Heineanum: Verzeichniss der ornithologischen southern forms, which possess a bright-yellow forehead, Sammlung. Halberstadt. Cadena C.D. & Cuervo A.M. 2010. Molecules, ecology, morphology, both different from the olive forehead of Amazonian and songs in concert: how many species is Arremon torquatus species (Fig. 4). Average dimensions (mm): bill length (Aves: Emberizidae)? Biological Journal of the Linnean Society 99: 12.8; tail 70.8; tarsus 22; wing 96.7. 152–176. Distribution: Atlantic Forest from Pernambuco, eastern Carneiro L.S., Gonzaga L.P., Rêgo P.S., Sampaio I., Schneider H. & Aleixo A. 2012. Systematic revision of the Spotted Antpitta Bahia and Minas Gerais, to the lowland forests in Espírito (Grallariidae: Hylopezus macularius), with description of a cryptic Santo and Rio de Janeiro. new species from Brazilian Amazon. Auk 129: 338–351. Catchpole C.K. & Slater P.J.B 2008. Bird song: biological themes and nd variations. 2 edn. New York: Cambridge University Press. ACKNOWLEDGEMENTS Charif R.A., Waack A.M. & Strickman L.M. 2010. Raven Pro 1.4 User's Manual. Ithaca: Cornell Laboratory of Ornithology. Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest We are grateful to the São Paulo Research Foundation 2: more models, new heuristics and parallel computing. Nature (FAPESP) for the fellowship provided to V.R.T. (Proc. Methods 9: 772. No. 2010/19876-5) and F.B. (Proc. No. 2015/11397- nd Gotelli N.J. & Ellison A.M. 2012. A primer of ecological statistics, 2 4) and the Brazilian National Council for Scientific an d edn. Sunderland: Sinauer Associates. Guilherme E. 2012. Birds of the Brazilian state of Acre: diversity, Technological Development (CNPq) for the grants to zoogeography, and conservation. Revista Brasileira de Ornitologia L.F.S. To the curators and staff of the museums and 20: 393–442. sound archives: Museu Paraense Emílio Goeldi, Museum Gyldenstolpe N.C.G.F. 1945. The bir d fauna of Rio Juruá in western of Natural Science of the Louisiana State University, Brazil. Kungliga Svenska Vetenskapsakademien. Akademiens Handlingar 22: 1–337. Museu de Biologia Professor Mello Leitão, Museu Nacional Gyldenstolpe N.C.G.F. 1951. The ornithology of the Rio Purús region da Universidade Federal do Rio de Janeiro, Colección in western Brazil. Arkiv för Zoologi 2: 1–230. Ornitológica Phelps, Muséum National d'Histoire Hackett S.J. 1996. Molecular phylogenetics and biogeography of Naturelle, Museum für Naturkunde, Macaulay Library, tanagers in the genus Ramphocelus (Aves). Molecular Phylogenetics and Evolution 5: 368–382. Arquivo Sonoro Elias Coelho, Fonoteca Neotropical Jacques Hellmayr C.E. 1905. Notes on a colletion of birds, made by Mons. A. Vielliard and to MPEG and FMNH for providing us Robert in the district of Pará, Brazil. In: Rothschild H.W., Hartert the tissue samples used in the analyzes. We are also E. & Jordan K. (eds.). London: Novitates Zoologicae: A Journal grateful to the colleagues who provided us their personal of Zoology in connection with the Tring Museum. Hazell, Watson & Viney. recordings (see Apppendix II); Vagner Cavarzere Hellmayr C.E. 1938. Catalogue of birds of the Americas and the adjacent and Rafael Marcondes for the high-quality photos, islands in the Field Museum of Natural History, v. 13 part 11. Jaqueline Battilana for helping F.B. with the laboratory Zoological Series of the Field Museum of Natural History. procedures, and Adrian Barnett and Gustavo Bravo for IBGE (Instituto Brasileiro de Geografia e Estatística). 2012. Manual nd técnico da vegetação brasileira. 2 edn. Rio de Janeiro: Instituto critical review. Brasileiro de Geografia e Estatística, Manuais Técnicos em Geociências. Isler M.L., Isler P.R. & Whitney B.M. 1998. Use of vocalizations REFERENCES to establish species limits in antbirds (Passeriformes: Thamnophilidae). Auk 115: 577–590. Aleixo A. 2007. Conceitos de espécie e o eterno conflito entre Katoh K., Kuma K., Toh H. & Miyata T. 2005. MAFFT version 5: continuidade e operacionalidade: uma proposta de normatização improvement in accuracy of multiple sequence alignment. Nucleic de critérios para o reconhecimento de espécies pelo Comitê Acids Research 33: 511–518. Brasileiro de Registros Ornitológicos. Revista Brasileira de Klicka J., Burns K. & Spellman G.M. 2007. Defining a monophyletic Ornitologia 15: 297–310. Cardinalini: a molecular perspective. Molecular Phylogenetics and Aleixo A., Carneiro L.S. & Dantas S.M. 2012. Aves, p. 103–143. In: Evolution 45: 1014–1032. Martins F.D., Castilho A.F., Campos J., Hatano F.M. & Rolim Kroodsma D.E. 1984. Songs of the Alder Flycatcher (Empidonax S.G. (eds.). Fauna da Floresta Nacional dos Carajás: estudos sobre alnorum) and Willow Flycatcher (Empidonax traillii) are innate. vertebrados terrestres. São Paulo: Nitro Editorial. Auk 101: 13–24. Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Kroodsma D., Hamilton D., Sánchez J.E., Byers B.E., Fandiño- Ridgely R.S. & Tudor G. 2009. Field guide to the songbirds of South Mariño H., Stemple D.W., Trainer J.M. & Powell G.V.N. 2013. America. The Passerines. Austin: University of Texas Press. Behavioral evidence for song learning in the Suboscine Bellbirds Ronquist F. & Huelsenbeck J.P. 2003. MrBayes 3: Bayesian (Procnias spp.; Cotingidae). Wilson Journal of Ornithology 125: phylogenetic inference under mixed models. Bioinformatics 19: 1–14. 1572–1574. Kumar S., Stecher G. & Tamura K. 2016. MEGA7: Molecular Santos M.P.D., Cerqueira P.V. & Soares L.M.S. 2010. Avifauna em Evolutionary Genetics Analysis version 7.0 for bigger datasets. seis localidades no centro-sul do estado do Maranhão, Brasil. Molecular Biology and Evolution 33: 1870–1874. Ornithologia 4: 49–65. Linnaeus C. 1766. Systema naturae per regna tria naturae: secundum Sclater P.L. 1886. The catalogue of the bir ds in the British Museum. classes, ordines, genera, species, cum characteribus, differentiis, London: Taylor and Francis. synonymis, locis (v. 12). Stockholm: Laurentius Salvius. Silva J.M.C., Souza M.C. & Castelletti C.H.M. 2004. Areas of Marler P. & Tamura M. 1962. Song “dialects” in three populations of endemism for passerine birds in the Atlantic Forest, South White-crowned Sparrows. Condor 64: 368–377. America. Global Ecology and Biogeography 13: 85–92. Mendiburu F. 2015. Package ‘agricolae’: statistical procedures Silveira L.F. & Olmos F. 2007. Quantas espécies de aves existem no for agricultural research. https://CRAN.R-project.org/ Brasil? Conceitos de espécie, conservação e o que falta descobrir. package=agricolae. (access on 24 January 2016). Revista Brasileira de Ornitologia 15: 289–296. Miller M.A., Pfeiffer W. & Schwartz T. 2010. Creating the CIPRES Simas M. 2016. WA2080606,  Caryothraustes canadensis  (Linnaeus, Science Gateway for inference of large phylogenetic trees. New 1766). http://www.wikiaves.com.br. (access on 29 July 2016). Orldean: Gateway Computing Environments Workshop (GCE). Snethlage E. 1914. Catálogo das aves amazônicas contendo todas as Nakagawa S. 2004. A farewell to Bonferroni: the problems of low espécies descriptas e mencionadas até 1913. Boletim do Museu statistical power and publication bias. Behavioral Ecology 15: Paraense de História Natural e Etnographia, Belém 8: 1–530. 1044–1045. Somenzari M., Silveira L.F., Piacentini V.Q., Rego M.A., Schunck F. Nelson E.W. 1912. Descriptions of new genera, species and subspecies & Cavarzere V. 2011. Birds of an Amazonia-Cerrado ecotone in of birds from Panama, Colombia and Ecuador. Smithsonian southern Pará, Brazil, and the efficiency of associating multiple Miscellaneous Collections 60: 1–25. methods in avifaunal inventories. Revista Brasileira de Ornitologia Pacheco J.F., Kirwan G.M., Aleixo A., Whitney B.M., Whitakker A., 19: 260–275. Minns J., Zimmer K.J., Fonseca P.S.M., Lima M.F.C. & Oren Sorenson M.D., Ast J.C., Dimcheff D.E., Tamaki Y. & Mindell D.C. 2007. An avifaunal inventory of the CVRD Serra dos D.P. 1999. Primers for a PCR-based approach to mitochondrial Carajás project, Pará, Brazil. Cotinga 27: 15–30. genome sequencing in birds and other vertebrates. Molecular Payne R.B. 1986. Bird songs and avian systematics. Current Phylogenetics and Evolution 12: 105–114. Ornithology 3: 87–126. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based Payne R.B. & Budde P. 1979. Song differences and map distances in phylogenetic analyses with thousands of taxa and mixed models. a population of Acadian Flycatchers. Wilson Bulletin 91: 29–41. Bioinformatics 22: 2688–2690. Peters J.L. 1970. Check-list of birds of the world, a continuation of the Stein R.C. 1963. Isolating mechanisms between populations of Traill's work of James L. Peters, v. 13. Paynter R.A. & Storer R.W. (eds.) Flycatchers. Proceedings of the American Philosophical Society 107: Cambridge: Museum of Comparative Zoology. 21–50. Piacentini V.Q., Aleixo A., Agne C.E., Maurício G.N., Pacheco J.F., Trainer J.M., McDonald D.B. & Learn W.A. 2002. The development Bravo G.A., Brito G.R.R., Naka L.N., Olmos F., Posso S., Silveira of coordinated singing in cooperatively displaying long-tailed L.F., Betini G.S., Carrano E., Franz I., Lees A.C., Lima L.M., manakins. Behavioral Ecology 13: 65–69. Pioli D., Schunck F., Amaral F.R., Bencke G.A., Cohn-Haft M., Villalobos D.C. & Villalobos J. 1947. Atlas de colores. Buenos Aires: Figueiredo L.F.A., Straube F.C. & Cesari E. 2015. Annotated El Ateneo. checklist of the birds of Brazil by the Brazilian Ornithological Whitney B.M., Pacheco J.F., Isler P.R. & Isler M.L. 1995. Hylopezuz Records Committee. Revista Brasileira de Ornitologia 23: 91–298. nattereri (Pinto, 1937) is a valid species (Passeriformes: Price J.J. & Lanyon S.M. 2002. Reconstructing the evolution of Formicariidae). Ararajuba 3: 37–42. complex bird song in the Oropendolas. Evolution 56: 1514–1529. Willis E.O. 1992. Three Chamaeza Antthrushes in eastern Brazil R Core Team. 2017. R: a language and environment for statistical (Formicariidae). Condor 94: 110–116. computing. Vienna: R Foundation for Statistical Computing. Zimmer K.J. 2008. The White-eyed Fo liage-gleaner (Furnaridae: http://www.R-project.org/. Automolus) is two species. Wilson Journal of Ornithology 120: Raposo M.A. & Höfling E. 2003. Overestimation of vocal characters 10–25. in Suboscine taxonomy (Aves: Passeriformes: Tyranni): causes and Zink R.M. 2004. The role of subspecies in obscuring avian biological implications. Lundiana 4: 35–42. Remsen-Jr. J.V. 1997. A new genus for the Yellow-Shouldered diversity and misleading conservation policy. Proceedings of the Grosbeak. Ornithological Monographs 48: 89–90. Royal Society of London B: Biological Sciences 271: 561–564. Rice N.H., Peterson A.T. & Escalona-Segura G. 1999. Phylogenetic patterns in montane Troglodytes wrens. Condor 101: 446–451. Associate Editor: Gustavo S. Cabanne. Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. APPENDIX I Specimens examined. For collection acronyms see Methods. Caryothraustes canadensis frontalis – 21: BRAZIL: São Miguel dos Campos (11 MZUSP 98475, MNRJ 34361); São Miguel (1 2 MZUSP 37728, MZUSP 37729, MZUSP 37730); Mangabeiras, Usina Sinimbu (7 4 MZUSP 37731, MZUSP 37732, MZUSP 37733, MZUSP 37734, MZUSP 39304, MZUSP 39305, MZUSP 39306, MZUSP 39307, MZUSP 39309, MZUSP 39308, MZUSP 39310); Quebrangulo, Engenho Riachão (1 MZUSP 39311); Ibateguara, Usina Serra Grande, Engenho Coimbra (2 MPEG 70547, MPEG 70548); Murici (1 35819); Igarassú, Recife, Usina São José (1? MNRJ 24749). Caryothraustes canadensis brasiliensis – 66: Porto Seguro, Estação Veracruz (2 MZUSP 76257, MZUSP 76258); Bahia (1 MZUSP 2538); Jequié, Serra do Talhão (1 MZUSP 14323); Ilhéus (1 1 MZUSP 33874, MZUSP 33875); Pacangê, Michellin Reserve (1 1? MZUSP 91568 MZUSP 91569); Ilhéus, Ecoparque de Una (2 1? MPEG 70825, MPEG 70826, MPEG 70827); Ilhéus, Fortuna River (2? MNRJ 25199, MNRJ 25200); Ilhéus (1 MNRJ 28011); Camumu (MNRJ 38130). Doce River, lower Suassuí (3 5 MZUSP 25280, MZUSP 25285, MZUSP 25289, MZUSP 25290, MZUSP 25287, MZUSP 25286, MZUSP 25288); Doce River, lower Piracicaba, right margin (1 1 MZUSP 25281, MZUSP 25282); Doce River, right margin (1 1 MZUSP 25283, MZUSP 25284). Reserva Florestal CRVD (2 1 MZUSP 98351, MZUSP 98350, MZUSP 98352); P. Cachoeiro (2 MZUSP 6155, MZUSP 6156); Espírito Santo (1 1 MZUSP 6274, MBML 6155); Pau Gigante (2 MZUSP 24675, MNRJ 7877); São José River (1? MZUSP 28124); Itaúna River, north of state (2 1 MZUSP 34603, MZUSP 34604, MZUSP 34605); Terra Alta (1 MBML 6235); Santa Tereza (7 2 MBML 6136, MBML 6138, MBML 6139, MBML 6140, MBML 6146, MBML 6147, MBML 6148, MBML 6152, MBML 6143); Santa Tereza Biological Station (1 MNRJ 44411); Santa Lúcia Biological Station (1 MNRJ 44410); Colatina (1 MNRJ 10500); Linhares (1 2 MNRJ 39558, MBML 6149, MBML 6144); Aracruz, Santa Cruz (4 3 MBML 6137, MBML 6141, MBML 6142, MBML 6145, MBML 6150, MBML 6154, MBML 6156); São Mateus (2 MBML 6151, MBML 6153). Muriaé River, Cardoso Moreira (1 MZUSP 27323); Petrópolis (1 MPEG 23645). Caryothraustes canadensis canadensis – 157: BRAZIL: Paca, right margin of Abacaxis River (1 MZUSP 77097); Camarão, right margin of Abacaxis River (1 MZUSP 77099); Camarão, left margin of Abacaxis River (1 MZUSP 77098); right margin of Canunmã River, lower part (1 MZUSP 96549); right margin of Canunmã River (1 1 MZUSP 96548, LSUMZ Field number B-81337); right margin of Sucunduri River, Across Ilha do Castanho (4 1? MZUSP 96546, MZUSP 96547, LSUMZ Field number B-85545, LSUMZ Field number B-85543, LSUMZ Field number B-96547); right margin of Sucunduri River, Igarapé da Cabaça (1 LSUMZ Field number B-80869); Manaus, Ducke Reserve (2 1 MPEG 30055, MPEG 30056, MPEG 30057); Tootobi River, tributary of Demini River (1? MPEG 37549); Jau River, left margin, Novo Airão (1 MPEG 50688); Itacoatiara (2 MNRJ 32808, MNRJ 32809). Serra do Navio (1 MZUSP 65511, 1 MNRJ 29265); Araguari River, right margin (1 2 MPEG 21649, MPEG 21649, MPEG 21652); Amapari River, Macapá (1 1 MPEG 23643, MPEG 23644); Amapari River, Serra do Navio (1 MPEG 24103); Igarapé Novo, left margin Igarapé Amazonas, left margin Iratapuru River (1 MPEG 29386). Igarapé Açu (2 MZUSP 6759, ZMB 281736); Capanema (3 1 MZUSP 32791, MPEG 23613, MPEG 23614, MPEG 23615); Belém, Utinga (2 5 MZUSP 36061, MZUSP 36060, MZUSP 46074, MZUSP 46075, MZUSP 46076, MZUSP 46077, MNRJ 10904); Belém (3 1 MZUSP 42814, MPEG 1541, MPEG 23616, ZMB 19026, 1 ZMB 31179); Município de Capim, Estrada Belém Brasília km 93 (19 11 2? MZUSP 46044, MZUSP 46045, MZUSP 46042, MZUSP 46043, MZUSP 46070, MZUSP 46046, MZUSP 46047, MZUSP 46048, MZUSP 46049, MZUSP 46051, MZUSP 46068, MZUSP 46069, MZUSP 46053, MZUSP 46057, MZUSP 46055, MZUSP 46054, MZUSP 46060, MZUSP 46058, MZUSP 46056, MZUSP 46059, MZUSP 46061, MZUSP 46062, MZUSP 46063, MZUSP 46050, MZUSP 46071, MZUSP 46072, MZUSP 46073, MZUSP 46067, MZUSP 46064, MZUSP 46065, MZUSP 46066, MZUSP 46052); Tailândia, Agropalma Reserve (1 1 MZUSP 77583, MZUSP 77584); Jubatituba (1 MPEG 898); Peixe Boi Experimental Station (1 MPEG 5664); Quatipuru River, Flor do Prado (2 MPEG 12629, MPEG 12630); Belém Brasília Road km 96 (4 MPEG 14343, MPEG 14344, LSUMZ 67926, LSUMZ 67927); Belém Brasília Road km 86 (1 1 MPEG 17977, MPEG 17978); Benevides, Baía do Sol, Retiro do Sol (2 1 MPEG 22148, MPEG 22156, MPEG 22183); Santa Barbara do Pará (1 MPEG 22194); Castanhal/Manaparim Road, km 86 (1 MPEG 23631); Acará-Mirim River, left margin, Tomé-Açu, Massaranduba (2 1 1? MPEG 26336, MPEG 26337, MPEG 26338, MPEG 26339); Bragança, Benjamin Constant, Sítio Manoel Horácio (1 MPEG 32331); Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Castanhal, Curuça Road (1 MPEG 35217); Santa Bárbara, Morelândia Farm, Genipaúba Road km 6 (1 MPEG 55920); Aveiro, Tapajós River, left margin, Escrivão (1 MPEG 64329); Alenquer, ESEC Grão-Pará (1 MPEG 65547); Itaituba, FLONA Amaná, right margin of Amaná River (1 1 MPEG 65660, MPEG 65661); Faro, Maracanã Village, Xingu River (1 MPEG 66890); Tomé Açu (1? MPEG 70274); Benevides (2 MPEG 8436, ZMB 8435); Baião (1 ZMB 31177); Bragança (1 1 MNRJ 10907, LSUMZ 67925). Mucajaí, Apiaú Colony (2 1 MPEG 46269, MPEG 46270, MPEG 46271); Couto de Magalhães River, Garimpo União (1 MPEG 49385). FRENCH GUIANA: French Guiana (2? MNHN 790, MNHN 1064). GUYANA: British Guiana (1 MZUSP 6760); Guiana (2 MNHN 2493, MNHN 2494); Kopinang River, 7 km SW Kopinang (2 LSUMZ 175537, LSUMZ 175537). VENEZUELA: Salto Maiza, Paragua River (1 1? COP 30837, COP 30841); Paragua River, Raudal (1 COP 26702); Paragua River, Raudal (1 1 1? COP 22805, COP 26701, COP 26698); La Faisca, mina Cerro Paraui-Tepui (1 2 2? COP 33166, COP 33162, COP 33163, COP 33164, COP 33165); Campamento Cruz, Yarra (1 2 COP 34782, COP 34783, COP 34784); San Fernando de Atabapó (1 2 COP COP 22185, COP 22186, COP 22187); Puerto Yapacana (4 5 COP 39779, COP 39778, COP 39781, COP 39782, COP 39784, COP 39785, COP 39786, COP 39787, COP 39780); Carabobo, Cuyum River (1 COP 46700); El Nenamo (1 COP 68100); Salto Guaiguinima, Paragua River (1 COP 30838); Paragua River, Cerro Tabarerupá (2? COP 26699, COP 26700); Puerto Yapacana (2? 1 COP 39783, COP 39778, 39777); Icabarú River (1 COP 42268); Culebra, Cunucunuma River (1 COP 74970); M. Parima (1 COP 70866); São Carlos of Negro River (2 COP 41883, COP 41884); Camp Jaime Benitez, slopes of Mt. Marahuaca (1 LSUMZ 25269). Caryothraustes canadensis simulans – 2: PANAMÁ: Prov. Darien, c. 9 km NW Cana on slopes of Cerro Pirre (2 LSUMZ 104752, LSUMZ 104753). APPENDIX II Recordings examined. For collection acronyms see methods. Caryothraustes canadenses frontalis – 10: BRAZIL: Usina Serra Grande, Engenho Coimbra (2 CORNELL 127847, CORNELL 127855); Santa Justina Farm (2 ASEC LPGD02715, ASEC LPGD02616 a-c ); Ibateguara, Usina Grande (1 ASEC LPGD03056); Campo Alegre, Mata Matão (1 Laherte Lobo de Araújo). Usina Trapiche, Mata do Tanguá (3 ASEC LPGD03223, ASEC LPGD03227, ASEC LPGD03308); Barreiros (1 Sidinei Dantas). Caryothraustes canadenses brasiliensis – 17: BRAZL: Jaguaquara (2 Vagner Cavarzere); Itacaré (1 Leonardo Patrial); Boa Nova (1 XC 84457). Pirapetinga (1 ASEC LPG08108). Linhares reserve (3 CORNELL 115347, CORNELL 115390, CORNELL 115401); Conceição da Barra, São Joaquim Farm (2 FNJV 8940, FNJV 9604); Santa Tereza, Nova Lombardia Reserve (2 FNJV 9140, FNJV 9142); Cafundó Farm (1 JMB07514); FLONA of Preto River (1 ASEC RR04122). Casemiro de Abreu (1 ASEC LPGDA1247-48); Guapiaçu Ecological Reserve (1 Ricardo Gagliardi); Casemiro de Abreu, União Biological Reserve (1 ASEC LPGD06903). Caryothraustes canadensis canadensis – 25: BRAZIL: Manaus (4 Marcelo Villegas, FNJV 7122); Presidente Figueiredo (1 XC 76377); Projeto de Assentamento Puxurizal (1 CORNELL 127705); Cachoeira Porteira, Cachorro River (2 FNJV 9978, FNJV 7123); Santa Bárbara, Mosqueiro (1 FNJV 7121). FRENCH GUIANA: Mana, piste ONF Dardanelles (1 XC 44065). GUYANA: E bank Waruma River (1 CORNELL 134927); Upper Demerara-Berbice 10.0 km N of Linden (1 CORNELL 85816). VENEZUELA: Capuchinbird Road, Bolívar (1 XC 12161); San Carlos of Negro River (1 Cornell 63330); Cuyuni River (1 CORNELL 63329); Grande River (4 CORNELL 63325, CORNELL 63326, CORNELL 63327, CORNELL 63328); Grande River, El Palmar (3 CORNELL 63321, CORNELL 63322, CORNELL 63323); La Tigra, El Palmar (1 CORNELL 63320); E of El Palmar, along road in Grande River Forest (1 CORNELL 60563); 19.0 km S of Las Claritas (1 CORNELL 112218). Revista Brasileira de Ornitologia 25(3): 2017 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Ornithology Research Springer Journals

Taxonomy and molecular systematics of the Yellow-green Grosbeak Caryothraustes canadensis (Passeriformes: Cardinalidae)

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Springer Journals
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Copyright © Sociedade Brasileira de Ornitologia 2017
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2178-7875
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10.1007/bf03544396
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Abstract

Revista Brasileira de Ornitologia 25(3): 176–189. ARTICLE September 2017 Taxonomy and molecular systematics of the Yellow-green Grosbeak Caryothraustes canadensis (Passeriformes: Cardinalidae) 1,4 2 2 3 Vinicius Rodrigues Tonetti , Fernanda Bocalini , Luís Fábio Silveira & Glaucia Del-Rio São Paulo State University (UNESP), Department of Ecology, Av. 24A, 1515, 13506-900, Rio Claro, SP, Brazil. Museu de Zoologia da Universidade de São Paulo. Avenida Nazaré 481, Ipiranga, 04263-000, São Paulo, SP, Brazil. Museum of Natural Science, Louisiana State University, 119 Foster Hall, 70803, Baton Rouge, LA, USA. Corresponding author: vrtonetti@gmail.com Received on 20 November 2016. Accepted on 18 September 2017. ABSTRACT: The Yellow-green Grosbeak Caryothraustes canadensis is a South American passerine occurring in Amazon and Atlantic Forests. Currently, it comprises four subspecies: Caryothraustes canadensis canadensis, Caryothraustes canadensis brasiliensis, Caryothraustes canadensis frontalis and Caryothraustes canadensis simulans. No study has ever revisited its taxonomy, hindering a complete understanding of the available diversity in Caryothraustes canadensis complex. We examined color and morphometric variation in 259 scientific specimens and sequenced t he mitochondrial gene ND2 of 29 tissue samples. We also quantitatively and qualitatively analyzed 52 spectrograms of vocal recordings. Molecular analyzes demonstrated the existence of two divergent lineages in C. canadensis complex, one from Amazonia and the other in the Atlantic Forest, which can also be distinguished by morphometric and plumage characters. Here we propose that the C. canadensis complex is composed of two full species: C. canadensis and C. brasiliensis. Caryothraustes canadensis frontalis shows no reciprocal monophyly in the phylogenetic analyzes, despite having weak plumage diagnostic characters; therefore, we suggest it should be considered a synonym of C. brasilensis. KEY-WORDS: Amazon, Atlantic Forest, genetic analysis, Oscines, Pernambuco Endemism Center, phylogeny, vocal analysis. INTRODUCTION canadensis canadensis (Linnaeus, 1766) occurs in parts of the Brazilian Amazon Forest, Colombia, French Caryothraustes canadensis was described by Linnaeus Guiana, Guyana, Suriname and Venezuela. Other two (1766) based on a plate of a yellow-bellied, black masked sub-species are restricted to the Brazilian Atlantic Forest (Brewer 2016a): Caryothraustes canadensis brasiliensis bird individual from Cayenne, French Guiana (not Canada as erroneously interpreted and used to name the Cabanis, 1851 occurs in eastern Brazil in the states of species; Brewer 2016a). Long after, one related species Bahia, Espírito Santo, Minas Gerais and Rio de Janeiro, with a distinctive gray belly and occurring in Central and Caryothraustes canadensis frontalis (Hellmayr, 1905) America – Caryothraustes poliogaster (Du Bus de Gisignies, is endemic to the Pernambuco Endemism Center, i.e. the Atlantic Forest north of the São Francisco River (Silva 1847) – was described (Klicka et al. 2007, Brewer 2016b). Besides C. canadensis and Caryothraustes poliogaster, et al. 2004, Brewer 2016a). Cabanis (1851) separated C. the genus had already included the Yellow-shouldered c. brasiliensis from C. c. canadensis based on its brighter Grosbeak Caryothraustes humeralis (Lawrence, 1867). yellow forehead and Hellmayr (1905) described C. c. However, based on molecular analysis, C. humeralis is frontalis based on the unique black-strip on the forehead. Ultimately, Caryothraustes canadensis simulans is exclusive now in the monotypic genus Parkerthraustes (Remsen-Jr. 1997), family Thraupidae, while the genus Caryothraustes to northern South America and Central America and was is allocated in the family Cardinalidae (Burns et al. 2014, described based mostly on brighter colors, comprising Piacentini et al. 2015). more golden yellow on forehead, more yellowish olive Currently, the Yellow-green Grosbeak comprises four green on back and larger and heavier bill (Nelson 1912, Brewer 2016a, b). subspecies of small-size (~17 cm) passerines, all of which inhabit the canopy of tropical lowland forests in Central No other study has ever reanalyzed the taxonomy and South America where they forage for fruits and seeds of this group, hindering a complete understanding of the and emit a loud song (Brewer 2016a). Caryothraustes diversity in Caryothraustes canadensis complex. Taxonomic Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. studies are of paramount importance in delimiting 9.1.2 (2016), it was checked if the sequences did not species and indicating the true diversity of a given region, include stop codes or anomalous base, the alignment aiding studies of phylogeny and biogeography (Silveira & was performed using MAFFT v. 7 (Katoh et al. 2005) Olmos 2007). Moreover, they are crucial to biodiversity H-INS-i, F-INS-i and G-INS-i, in which pairwise conservation, as conservation programs frequently ignore alignment information are incorporated into objective threatened taxa at the subspecific or population levels function. These new options of MAFFT showe d higher (Zink 2004, Aleixo 2007). Accordingly, our aim was accuracy than currently available methods including to integrate molecular data with traditional plumage TCoffee version 2 and CLUSTAL W in benchmark coloration, morphometric and vocal data of the Yellow- tests consisting of alignments of >50 sequences. Like green Grosbeak to revise the taxonomy of this species. the previously available options, the new options of MAFFT can handle hundreds of sequences on a standard desktop computer. We also examined the effect of the METHODS number of homologues included in an alignment. For a multiple alignment consisting of \u223c8 sequences with Taxon sampling and laboratory procedures low similarity, the accuracy was improved (2\u201310 percentage points plug-in at Geneious. Genetic analysis was conducted using tissue samples of 29 specimens of three subspecies of the Yellow-green Phylogenetic analyses Grosbeak, C. c. brasiliensis (n = 11), C. c. frontalis (n = 7), C. c. canadenis (n = 11). Vouchers are housed in the Phylogenetic relationships among individuals were following institutions: Museu de Zoologia da Universidade inferred using the Maximum Likelihood (ML) in RAxML de São Paulo (MZUSP, Brazil), Field Museum of v. 7.2.7 (Stamatakis 2006), and Bayesian Inference (BI) Natural History (FMNH, EUA) and Museu Paraense in MrBayes v. 3.1.2 (Ronquist & Huelsenbeck 2003), Emílio Goeldi (MPEG, Brazil) (Table 1). We also added both on Cipres Science Gateway v. 3.1 (Miller et al. sequences available on Genbank for C. c. simulans 2010). The best-fitting model of evolution for BI analysis (EF529916.1), Caryotrhaustes poliogaster poliogaster was estimated using the Bayesian Information Criterion (EF529915.1), Periporphyrus erythromelas (EF529919.1), (BIC) in jModelTest v. 2.1.6 (Darriba et al. 2012) and Rhodothraupis celaeno (EF529920.1) and Cardinalis HKY+G were selected as the best fitting model. BI cardinalis (JF795780.1). The last three were used as analysis was performed using two independent runs with outgroups following Klicka et al. (2007) and Cardinalis 10,000,000 generations each, 4 chains, the parametres cardinalis was used to root the trees. and the trees were be sampled every 1000 generations Total genomic DNA was extracted using the and the burn-in was 20%, the posterior probabilities for Genomic DNA Mini Kit (Invitrogen). The mitochondrial each estimated node were obtained through a majority molecular marker NADH Dehydrogenase Subunit 2 rule consensus of the remaining MCMC samples. ML (ND2, 1041 bp) was amplified using primers L5215, analysis was done using a GTR-GAMMA model, with H6313, L5758, H5766 (Hackett 1996, Sorenson et al. 100 independent searches, nodal support was estimated 1999) mitochondrial DNA (mtDNA. Polymerase chain with 1000 bootstrap replicates. Additionally, mean reaction (PCR) amplifications were performed using an pairwise p-distances among populations were calculated initial denaturation step at 94 C for 2 min, followed in MEGA v. 7.0 (Kumar et al. 2016). by 35 cycles of 94 C for 1 min, a 30 s annealing step at 50 C, and a 72°C extension for 1 min, and the final Taxonomic assessment extension was at 72°C for 7 min. In a 25 μL total volume, PCR amplifications contained approximately 20 ng of Supported clades in the phylogenetic analyses were used genomic DNA, buffer 10 ×, 200 mM of DNTPs, 1.5 as a priori clades for the study of phenotypic diagnostic mM of MgCl , 0.4 μM of each primer (forward and characters. We examined a total of 163 skins of the reverse), 0.2 × of BSA, and 0.1 U of Platinum Taq DNA three C. canadensis subspecies (107 belonging to C. c. Polymerase (Invitroven). PCR products were visually canadensis, 19 to C. c frontalis and 37 to C. c. brasiliensis) inspected in a 1% agarose gel, after electrophoresis, and housed in the Museu de Zoologia da Universidade de São positive results were purified using PEG precipitation Paulo (MZUSP, Brazil) and the Museu Paraense Emílio protocol. Sequencing was carried out on an ABI 3130 Goeldi (MPEG, Brazil) (see Appendix I). We did not automated capillary sequencer (Applied Biosystems) with have personal access to C. c. simulans, what prevented the ABI Prism Big Dye terminator Kit. Both strands us to include this taxa in this review. By the time this and one internal primer of each sample were sequenced. research was conducted, a spectrometer was not available, Sequences were edited and aligned using Geneious v. restricting colorimetric analysis to comparisons to color Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Table 1. Voucher information of Caryothraustes canadensis tissue samples. Museum Taxon Locality MZUSP 91568 Caryothraustes canadensis brasiliensis Brazil, Bahia, Mata do Pacange, Reserva Michelin MZUSP 91569 Caryothraustes canadensis brasiliensis Brazil, Bahia, Mata do Pacange, Reserva Michelin MZUSP 98351 Caryothraustes canadensis brasiliensis Brazil, Espirito Santo, Reserva Florestal CVRD MZUSP 98352 Caryothraustes canadensis brasiliensis Brazil, Espirito Santo, Reserva Florestal CVRD MZUSP 98350 Caryothraustes canadensis brasiliensis Brazil, Espirito Santo, Reserva Florestal CVRD MZUSP 101537 Caryothraustes canadensis brasiliensis Brazil, Bahia, Camacan, Serra das Lontras MZUSP 101536 Caryothraustes canadensis brasiliensis Brazil, Bahia, Camacan, Serra das Lontras MPEG 70826 Caryothraustes canadensis brasiliensis Brazil, Bahia, Ilheus Ecoparque de UNA MPEG 70827 Caryothraustes canadensis brasiliensis Brazil, Bahia, Ilheus Ecoparque de UNA MPEG 70825 Caryothraustes canadensis brasiliensis Brazil, Bahia, Ilheus Ecoparque de UNA MPEG 79859 Caryothraustes canadensis brasiliensis Brazil, Bahia, Amargosa, Serra do Timbo Brazil, Amazonas, Sucunduri River (right margin), in front MZUSP 96547 Caryothraustes canadensis canadensis of Castanho Island MZUSP 96548 Caryothraustes canadensis canadensis Brazil, Amazonas, lower Canuma River (right margin) MZUSP 96549 Caryothraustes canadensis canadensis Brazil, Amazonas, lower Canuma River (right margin) MPEG 65547 Caryothraustes canadensis canadensis Brazil, Pará, Alenquer, ESEC Grao-Para Brazil, Pará, Itaituba, FLONA Amaná, right margin Amana MPEG 65661 Caryothraustes canadensis canadensis River Brazil, Pará, Itaituba, FLONA Amaná, right margin Amana MPEG 65660 Caryothraustes canadensis canadensis River MPEG 66890 Caryothraustes canadensis canadensis Brazil, Pará, Faro, Maracana Village, Xingu River MPEG 74145 Caryothraustes canadensis canadensis Brazil, Pará, Santarém, RESEX Tapajos/Arapiuns Capixaua MPEG 74146 Caryothraustes canadensis canadensis Brazil, Pará, Santarém, RESEX Tapajos/Arapiuns Capixaua MPEG 74147 Caryothraustes canadensis canadensis Brazil, Pará, Santarém, RESEX Tapajos/Arapiuns Capixaua MPEG 76879 Caryothraustes canadensis canadensis Brazil, Maranhão, Centro Novo, REBIO Gurupi MZUSP 98475 Caryothraustes canadensis frontalis Brazil, Alagoas, São Miguel dos Campos, Usina Porto Rico Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho FMNH 427231 Caryothraustes canadensis frontalis Coimbra Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho FMNH 427232 Caryothraustes canadensis frontalis Coimbra Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho FMNH 427233 Caryothraustes canadensis frontalis Coimbra Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho FMNH 427234 Caryothraustes canadensis frontalis Coimbra Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho MPEG 70547 Caryothraustes canadensis frontalis Coimbra Brazil, Alagoas, Ibateguara, Usina Serra Grande, Engenho MPEG 70548 Caryothraustes canadensis frontalis Coimbra catalogues. To standardize color analyses, only VRT distance between nostril and bill tip, lower jaw width, compared forehead, crown, nape, back, rump, rectrices, right tarsus, right wing chord (i.e. closed wing-lenght) throat, malar, ear coverts, breast, belly and primaries and tail length with a caliper (precisions of 0.005 mm) colors with a Villalobos & Villalobos (1947) color chart and a ruler (for wing and tail measurements with a for all museums specimens analyzed and under the same precision of 0.5 mm). light conditions. An additional 97 specimens housed in Museu de We collected measurements of exposed culmen, Biologia Professor Mello Leitão (MBML, Brazil; 22 C. c. Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. brasiliensis), Museu Nacional da Universidade Federal do descending or vice versa; Catchpole & Slater 2008). Rio de Janeiro (MNRJ, Brazil; 9 C. c. brasiliensis, 5 C. We used frequency and time resolution of 46.9 Hz and c. canadensis and 2 C. c. frontalis), Colección Ornitológica 1.06 ms respectively, and the qualitative analyses were Phelps (COP, Venezuela; 39 C. c. canadensis), Museum performed using the same window size to avoid shape of Natural Science of the Louisiana State University distortions in notes used in qualitative analysis (Charif (LSUMZ, USA; 11 C. c. canadensis and 1 C. c. simulans), et al. 2010). All notes were analyzed in black and white. Muséum National d'Histoire Naturelle (MNHN, France; To perform vocalization analysis, we used RAVEN 4 C. c. canadensis) and Museum für Naturkunde (ZMB, PRO v. 1.4 (Charif et al. 2010). From the 92 original Germany; 5 C. c. canadensis; Appendix I) were examined recordings, only 52 (25 of C. c. canadensis, 17 of C. c. via high quality pictures taken by some of us and brasiliensis and 10 of C. c. frontalis) had a reasonable colleagues (see Acknowledgements). All specimens were quality needed for analysis, i.e., allowed accurate photographed under white light. Although we did not measures. Recordings were obtained from the following compare the plumage of those individuals with color sound archives: Macaulay Library of Natural Sounds chart, we used their photographs as a post hoc analysis (CORNELL, Cornell University, USA); Arquivo Sonoro following valid species delimitation, aiming to confirm Elias Coelho (ASEC, UFRJ, Brazil); Fonoteca Neotropical the usefulness of the putative diagnostic characters. Jacques Vielliard (FNJV, UNICAMP, Brazil); Xeno- Canto (XC, http://www.xeno-canto.org); and also from Vocal analysis researchers who provided their personal recordings (see Appendix II). To measure MaF, MiF, BW, pF and Following Catchpole & Slater (2008), we defined a note duration we used only WAV sound fi les due their high as a continuous line on spectrogram and a phrase as a quality and precision, and we used WAV as well as MP3 sequence of similar notes followed each other by a short files to count NN and analyze note shapes. interval of time. Because the species emits two different types of phrase (defined here as Type-I and II; Fig. 1), Vocal and morphometric statistics we analyzed them separately. Type-I phrase is composed by “whistled” notes, and Type-II is composed by shorter We assayed for morphometric and vocal differences notes followed each other by a very short time lapse, between populations using parametric tests, when data popularly known as “trill” (Fig. 1). We measured the showed normality and homoscedasticity, or their non- maximum frequency (MaF), minimum frequency (MiF), parametric equivalents when these two assumptions bandwidth (BW), peak frequency (pF) and time duration were not fulfilled (Gotelli & Ellison 2012). Analysis of for each single note in Type- I phrases and for all Type-II variance (ANOVA; parametric) or Kruskal-Wallis (non- phrases and for all Type-II phrases as if they were a single parametric) were used to compare morphometric and note (Charif et al. 2010). We also counted the number of vocal differences between groups. The Tukey test, or its notes (NN) for all phrases. non-parametric equivalent Newman-Keuls, was used Besides the quantitative measurements cited above, as post hoc tests to investigate for significant pairwise we analyzed the aspect of Type-I notes, shaped by differences. Sexual dimorphism within putative groups frequency modulation. Frequency modulation occurs was tested using the Student's t or Wilcox tests. We used when the direction of frequency changes in y-axis of 0.05 as critical value of p and we did not use any p-value the spectrogram, thus causing inflections in the note corrections (e.g. Bonferroni) as this kind of correction is (i.e. frequency modulation changes from ascending to extremely conservative and its use has been discouraged Figure 1. Spectrogram exemplifying a song (CORNELL 127847) with two Type-I and one Type-II phrases. Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. by some authors (Nakagawa 2004, Gotelli & Ellison Morphometric analysis 2012). To assess diagnosability between clades indicated by phylogenetic trees, we log-transformed measurements Morphometry indicated higher similarity between birds for all the individuals studied and conducted discriminant from Atlantic Forest sites than those and Amazonian function analyses (DFA) in R software v. 3.2.2 (R Core locations. Except for the exposed culmen length, Team 2017), clustering groups by 95% confidence measurements did not differ significantly between the intervals. Except for the Newman-Keuls test (performed two Atlantic Forest lineages (P < 0.05; Table 3). The in the “agricolae” package in the R software; Mendiburu discriminant analysis of morphometric variation (Fig. 2015), we performed statistical analyses in the package 3) showed that the clades canadensis population 2 and “stats” (R Core Team 2017). brasiliensis/frontalis are diagnosable mainly by differences in exposed culmen and wing length (factor 1). The clade canadensis population 1 overlaps in size with brasiliensis/ RESULTS frontalis, its sister group. Molecular analysis Plumage variation Maximum-likelihood and Bayesian analyses produced Individuals from the Amazon Basin showed olive forehead similar topologies with high support, indicating that both coloration ranging mainly from Y-12 -6 (MZUSP Atlantic Forest taxa belong to the same clade (Fig. 2). 46064) to Y-12 -9 (MZUSP 46059; Fig. 4). There is Caryothraustes c. frontalis and C. c. brasiliensis are closely weak plumage diagnosis between the two Amazonian related, with only 0.3% of mitochondrial divergence clades pointed by phylogenetic trees, although the olive (mean p-distance, Table 2). On the other hand, head distinguishes both from the Atlantic forms. individuals of C. canadensis from the Madeira-Tapajós Although showing no genetic distinctiveness, interfluvium show 6.3% of mitochondrial divergence the subspecies C. c. frontalis and C. c. brasiliensis show from brasiliensis/frontalis. Phylogenetic trees also indicate consistent differences in forehead color. Birds from the that canadensis is not a monophyletic group, since it Atlantic Forest south of the São Francisco River, in comprises C. c. simulans and the C. brasiliensis/frontalis Brazilian states of Bahia, Espírito Santo, Minas Gerais clade. In this sense, two distinct groups of C. canadensis and Rio de Janeiro can be distinguished by a bright- form distinct Amazonian clades, one sister to the Atlantic yellow forehead (YYO-12 -10; MZUSP 6274, or YYO- form, restricted to the southern Amazon (from left bank 12 -11; MZUSP 24675). Forehead color did not vary in of Madeira to both banks of Tapajós River, herein called individuals from the Pernambuco Endemism Center; all population 1), and one containing individuals from birds from this region exhibited a discrete black forehead northern and eastern Amazon Forest (population 2). (Fig. 4). For specimens from the Amazon and Atlantic Table 2. Genetic p-distance (%) between Caryothraustes canadensis subspecies estimated using NADH dehydrogenase 2 (ND2) sequences. Caryothraustes canadensis canadensis was divided into the two populations evidenced in the phylogenetic analyzes. C. c. brasiliensis C. c. frontalis C. p. simulans C. c. canadenis (population 1) C. c. brasiliensis C. c. frontalis 0.3 C. c. simulans 6.7 6.6 C. c. canadensis (population 1) 6.2 6.1 6.5 C. c. canadensis (population 2) 6.4 6.3 5.8 5.5 Table 3. Morphological measurements (in mm) as mean ± standard deviation and range in parenthesis for each sampled taxa. Taxon Culmen Bill length Bill width Jaw height Tarsus Wing Tail 15.36 ± 0.96 11.51 ± 0.68 11.26 ± 0.51 6.6 ± 0.59 20.52 ± 0.97 88.9 ± 3.93 62.51 ± 6.08 C. c. canadensis (12.6 – 17.8) (9.6 – 13.4) (9.9 – 12.3) (5.65 – 11.5) (17.3 – 22.8) (72 – 99) (51 – 80) 16.63 ± 0.8 12.33 ± 0.63 12.7 ± 0.69 7.41 ± 0.43 22.02 ± 1.24 96.16 ± 3.21 70.81 ± 4.39 C. c. brasiliensis (15 – 18.8) (11.2 – 13.55) (11.55 – 14.9) (6.9 – 9.02) (19.5 – 25.3) (90 – 103) (66 – 83) 17.66 ± 0.83 12.8 ± 0.55 13.2 ± 0.57 7.6 ± 0.27 21.96 ± 1.29 95.18 ± 2.74 68.18 ± 3.41 C. c. frontalis (16.25 – 18.8) (11.9 – 13.85) (12.4 – 14.05) (6.95 – 7.85) (20.1 – 24.6) (90 – 100) (63 – 77) Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Figure 2. Phylogenetic relationships of Caryothraustes canadensis. (A) Maximum likelihood topology, nodes supports are bootstrap values. (B) topology obtained by Bayesian inference, node supports are posterior probabilities. Figure 3. Discriminant function analysis. Ellipses indicate clusters of populations by 95% intervals. Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Forest south of the São Francisco River crown and nape and primaries (Fig. 5; Table 4). Through t he analysis of showed the same color as the forehead (olive and bright- the photographs, C. c. simulans show brighter underparts yellow respectively), but of a slightly darker shade. The than the other specimens from Amazon basin. However, two Atlantic Forest subspecies showed the same pattern due to the low sample size (n = 1) we are not able to of crown and nape color (bright-yellow, Table 4), with conclude if it can be considered a full species. We did not small individual variation (ranging from YYO-12 -8; find sexually dimorphic features in any studied group. MZUSP 6274 to YYO-12 -10; MPEG 70547 for crown, o o and from YYO-12 -4; MZUSP 37733 to YYO-12 -6; Vocal variation MPEG 70827 for nape). Amazonian birds showed breast coloration ranging from olive-yellow (Y-12 -9; MZUSP No signifi cant differences (Newman-Keuls or Tukey tests 46072) to bright-yellow (YYO-12 -14; MZUSP 96546), P > 0.05) were observed in vocal characters between whereas the Atlantic Forest birds consistently showed the the songs of the three subspecies analyzed here (Tables same color (YYO-12 -11). The following parts of the body 5 & 6). Of the 52 vocalizations analyzed, individuals showed small, if any, variation between all individuals and emitted the Type-I phrase in 48 of them, and Type-II cannot be used as diagnostics characters: back, rump, in 39. In most recordings (70%), both types of phrases upper surface of tail, throat, malar parch, ear parch, belly were given, while in 23.5% and 5% only Type-I and II Figure 4. Lateral part of the head (upper left corner) and forehead (right side) of specimens: Caryothraustes canadensis frontalis (MZUSP 37731), Caryothraustes canadensis brasiliensis (MZUSP 34605) and Caryothraustes canadensis canadensis (MZUSP 46047). The distribution of all specimens analyzed is given in the map. Locations of genetic samples analyzed are represented by white symbols with black dots; specimens and recordings are represented by totally black symbols. Photograph location of Caryothraustes canadensis simulans is represented by a black star. Table 4. Colors found in specimens examined. Numbers in parenthesis indicate the proportion of individuals showing the respective colors. O = olive; Y = yellow; B = black; BY = bright-yellow; OY = olive-yellow. Malar Ear Taxon Forehead Crown Nape Back Rump Tail Wing Throat Breast Belly parch parch C. c. canadensis O O O O O O OY B OY O Y BY (107 specimens) (97%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) C. c. brasiliensis BY BY BY O O O OY B OY O BY BY (37) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) C. c. frontalis B BY BY O O O OY B OY O BY BY (19) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) (100%) Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Figure 5. Dorsal (A), ventral (B) and lateral (C) parts of the body of specimens: Caryothraustes canadensis frontalis (MZUSP 37731; left A and B and upper C), Caryothraustes canadensis brasiliensis (MZUSP 34605; middle, south of São Francisco River) and Caryothraustes canadensis canadensis (MZUSP 46047; right A and B and bottom C). Table 5. Measurements of vocal variables of Type-I phrases as mean ± standard deviation and range, in parenthesis, for each taxa. Each variable was measured for each single note. Number = number of notes within each phrase. As different recor dings could have different number of phrases and notes, these values were extracted from the mean values of each recording. Maximum Minimum Bandwidth Peak frequency Taxon Time (s) Number frequency (kHz) frequency (kHz) (kHz) (kHz) Caryothraustes 5619 ± 938 1300 ± 230 4319 ± 944 3838 ± 444 0.148 ± 0.03 2.85 ± 1.17 canadensis canadensis (3773 – 8167) (1003 – 1898) (2439 – 7022) (3155 – 5054) (0.087 – 0.247) (1 – 5.5) Caryothraustes 5571 ± 1394 1160 ± 375 4411 ± 1506 4147 ± 655 0.205 ± 0.02 2.01 ± 0.72 canadensis brasiliensis (3854 – 7534) (846 – 2331) (2560 – 6687) (3281 – 5343) (0.134 – 0.239) (1 – 3) Caryothraustes 6732 ± 1478 1215 ± 248 5571 ± 1538 4197 ± 534 0.184 ± 0.02 2.57 ± 0.81 canadensis frontalis (4360 – 8464) (816 – 1584) (3333 – 7562) (3416 – 5203) (0.147 – 0.22) (1 – 4) Table 6. Measurements of vocal variables of Type-II phrases as mean ± standard deviation and range, in parenthesis, for each taxa. Each variable was measured for each entire phrase. Number = number of notes within each phrase. As different recor dings could have different number of phrases and notes, these values were extracted from the mean values of each recording. Maximum Minimum Bandwidth Peak frequency Taxon Time (s) Number frequency (kHz) frequency (kHz) (kHz) (kHz) Caryothraustes 8704 ± 938 2060 ± 297 6644 ± 945 6130 ± 955 0.124 ± 0.03 6.17 ± 1.44 canadensis canadensis (6674 – 9897) (1633 – 2851) (4941 – 8208) (4392 – 7838) (0.08 – 0.23) (4 – 10) Caryothraustes 8063 ± 1162 1961 ± 347 6101 ± 1229 5571 ± 586 0.176 ± 0.02 7.343 ± 1.26 canadensis brasiliensis (5963 – 10001) (1565 – 2827) (4036 – 7872) (4664 – 6773) (0.131 – 0.231) (5 – 9) Caryothraustes 8478 ± 613 1827 ± 348 6650 ± 613 5996 ± 190 0.169 ± 0.04 7.6 ± 1.79 canadensis frontalis (7284 – 9159) (1323 – 2565) (5502 – 7526) (5713 – 6304) (0.11 – 0.235) (5 – 10) Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. if they should be treated as separate species (Bocalini et al. in prep.). In the Atlantic Forest, we suggest that both forms should be treated as Caryothraustes brasiliensis, since it has priority over C. c. frontalis. Beside the black forehead, Hellmayr (1905) cited the bright-yellow breast as a diagnostic character for C. c. frontalis compared to specimens from other parts of the Atlantic Forest. Although for some specimens (e.g. MPEG 70547) we found slightly brighter breast when compared to some individuals of C. brasiliensis (e.g. MZUSP 91569), this was due to intraspecific variation and cannot be used to distinguish the two Atlantic Forest populations. In this sense, both groups share almost all plumage colors except on the forehead. Our phylogenetic trees indicate that C. c. brasiliensis and C. c. frontalis form a unique clade with very shallow divergence. As our results do not indicate reciprocal monophyly between the two taxa, here we synonymize C. c. frontalis in C. brasiliensis. Further analysis using genomic markers, such as ultraconserved elements Figure 6. Spectrograms exemplifying individual variation (Bocalini et al. in prep.) could clarify if the variation on found in qualitative voice analysis. Above are two recordings forehead color corresponds with phylogenetic divergence of Caryothraustes canadensis brasiliensis from Espírito Santo of the two populations putatively isolated by the São state, Brazil (FNJ 9140 [A]; ASEC JMB07514 [B]) and below is one recording of Caryothraustes canadensis canadensis from Francisco River barrier. the Amazonas state, Brazil (CORNELL 127705 [C]). Contrary Besides that, the clade formed by C. c. simulans is to expectations, we observed more similarity between the supported by our phylogenetic trees, and photography recordings B and C (different species) t han between A and B analyses reveal slight plumage differences when compared (same species). to C. canadensis and the Atlantic forms. However, as we used only one sequence from the GenBank and few specimens were studied by us, we prefer to keep its current status until we collect enough morphometric, voice and were observed, respectively. A total of 859 Type-I notes genomic data (Bocalini et al. in prep.). (in 349 Type-I phrases) and 210 Type-II phrases were individually measured. We measured all Type-I notes and Vocal analysis all Type-II phrases available in all analyzed recordings. As the recordings did not have the same number of notes Within the order Passeriformes there is a dichotomy and phrases, we performed the tests using a simple mean between the usage of song in taxonomy of species for each recording to avoid pseudoreplication. Qualitative included in the Oscines and Suboscines suborders analysis of Type-I phrases, measured by visual analysis (Raposo & Höfling 2003). Laboratory experiments and of the shape of the notes, showed a great variation even field studies have suggested that some suboscine species within the same locality and, therefore, could not be used songs are innate (i.e. genetically defined, without changes to diagnose taxa (e.g. Fig. 6). associated to learning) and the species are unable to learn their songs (Stein 1963, Payne & Budde 1979, Kroodsma DISCUSSION 1984). Conversely, variations observed in oscine songs have been thought as consequence of a learning ability, and theoretically with no taxonomic value (Marler & Tamura Plumage variation and diagnosis 1962). These assumptions made decades ago and for a limited species have been used to support the separation Our phylogenetic trees support the existence of two Amazonian clades, that although weakly diagnosable of a variety of suboscine taxa (e.g. Willis 1992, Whitney et al. 1995, Isler et al. 1998, Zimmer 2008, Carneiro et between them in terms of size, voice and plumage, are al. 2012), while few attempts have been made to use song both different in forehead color when compared to the in the taxonomy of oscine species (Raposo & Höfling Atlantic forms. Here we propose that the Amazonian 2003, but see Cadena & Cuervo 2010). However, based clades should be treated as Carytohraustes canadensis until genomic data or more detailed morphological data reveal on recent empirical evidence, this dichotomy has been Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. revised (Payne 1986, Trainer et al. 2002, Price & Lanyon – see, for example, that some of the best sampled 2002, Cadena & Cuervo 2010, Kroodsma et al. 2013). Amazonian localities (Serra dos Carajás and Fartura Although the use of oscine vocalization in Farm) are within Tapajós-Tocantins interfluvium and taxonomy is encouraged by some authors (Raposo & has no record of the Yellow-green Grosbeak (Pacheco et Höfling 2003) and could be used to diagnose species in al. 2007, Somenzari et al. 2011, Aleixo et al. 2012) and Arremon torquatus complex (Cadena & Cuervo 2010) other well-sampled regions west from Madeira River have in addition to corroborating phylogenetic relationships also not accounted for the species (Gyldenstolpe 1945, for Dendroica Warblers (Payne 1986) and Oropendolas 1951, Guilherme 2012). A few other Amazonian species (genera Psarocolius, Gymnostinops, and Ocyalus) (Price show similar distributions patterns (i.e. present in some & Lanyon 2002), our analysis found that none of the interfluvium and a bsent in others), albeit not exactly as vocalization characters used were useful in delimiting C. canadensis, such as Chestnut-crowned Foliage-gleaner the proposed species. This was similar to other study Automolus rufipileatus, Dusky-capped Greenlet Hylophilus with Wrens Troglodytes (Rice et al. 1999); these birds hypoxanthus, and Black Bushbird Neoctantes niger, which also have a complex and highly-variable song. Despite present disjunct populations with an absence area in the the relatively small sample size (52 recordings analyzed), intermediate region (Ridgely & Tudor 2009). high levels of individual variation in qualitative analysis prevented us from identifying diagnosable groups. For Taxonomy of the Yellow-green Grosbeak example, it is possible to find greater differences in the shape of notes between single recordings of birds from Caryothraustes canadensis (Linnaeus, 1766) the state of Espírito Santo (Fig. 6A & B), than between English name: Yellow-green Grosbeak recordings from Espírito Santo and Amazonas (Fig. 6C). Portuguese name: Furriel This was contrary to the expectation that recor dings Loxia canadensis Linnaeus 1766: 304 from individuals that belong to the same species (e.g. C. Pitylus viridis Sclater 1886: 306 brasiliensis, Figs. 6A & B) would be more similar than Pitylus canadensis Snethlage 1914: 461 recordings of different species (e.g. C. brasiliensis, Figs. Caryothraustes canadensis canadensis Peters 1970: 224 6B and C. canadensis, Fig. 6C). This likely reflects song- Type-locality: Cayenne, French Guiana learning ability within Caryothraustes species. In relation Diagnosis: individuals can be distinguished from other to quantitative analysis, as well as shape of notes, it is Caryothraustes species by the presence of olive color on possible that high levels of variation prevented us from forehead, crown and nape. Although Amazonian birds diagnosing the groups of individuals by their song. have significantly smaller body size in comparison to However, because oscine song proved useful in taxonomic the other two species (Fig. 3; Table 3), due to overlap in and systematic previous studies (see above), we suggest measurements it cannot be used as a diagnostic character. it should be tested with other passerines and at different Average dimensions (mm): bill length 11.5; tail 62.5; taxonomic levels (e.g. populations) in an attempt to tarsus 20.5; wing 89. delimit differentiated taxa (Raposo & Höfling 2003). Distribution: mostly Amazon Basin in southern Colombia, eastern and southern Venezuela, in most parts of Guyana, Distribution remarks French Guiana and Suriname and on both banks of Negro, Trombetas and Jari Rivers in Brazil. In the southern Recent records on the right bank of the Parnaíba River, in Amazon it occurs in the Madeira-Tapajós interfluve and the Brazilian state of Piauí (Simas 2016) may represent on the right bank of Tocantins River. It seems that the the southeastern range limit of C. canadensis. Northwest southeastern range limit to its distribution occurs on the Piauí occurs in a very extensive ecological transition zone east bank of Parnaíba River, out of Amazon Basin and in between the Amazon, Cerrado and Caatinga domains the municipality of Altos, Piauí, Brazil (Simas 2016. and has semideciduous forests as its predominant vegetation type (IBGE 2012). Bird inventories in the western part Caryothraustes canadensis simulans Nelson 1912 of that state have recorded Amazonian taxa (e.g. the Pied English name: Cana Green Grosbeak Puff bird Notharchus tectus and the Rufous-capped Antthrush Type locality: Cana, eastern Panama Formicarius colma amazonicus; Santos et al. 2010). Additionally, there is an apparent gap in the Diagnosis: underparts yellowish olive green and smaller distribution of C. canadensis in the Tapajós-Tocantins than other members of C. canadensis (Nelson 1912, interfluvium, in southern Amazonia, as well as in the Hellmayr 1938). Average dimensions (mm): bill length Inambari Center of Endemism. These absences might 18; tail 66; wing 86 (Hellmayr 1938). not arise from sampling problems, once these regions Distribution: eastern Panama and northern Colombia have historically been as much sampled as the others (Hellmayr 1938). Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Brewer D. 2016a. Yellow-green Grosbeak (Caryothraustes canadensis). Caryothraustes brasiliensis Cabanis, 1851 In: del Hoyo J., Elliot A., Sargatal J., Christie D. & de Juana E. English name: Yellow-faced Grosbeak (eds.). Handbook of the birds of the world alive. http://www.hbw. Portuguese name: Furriel-do-sul com/node/62190 (access on 14 June 2017). Caryothraustes brasiliensis Cabanis 1851: 144 Brewer D. 2016b. Black-faced Grosbeak (Caryothraustes poliogaster). In: del Hoyo J., Elliot A., Sargatal J., Christie D. & de Juana E. Pitylus brasiliensis Sclater 1886: 306 (eds.). Handbook of the birds of the world alive. http://www.hbw. Pitylus canadensis frontalis Hellmayr 1905: 277 com/node/621890 (access on 14 June 2017). Caryothraustes canadensis brasiliensis Peters 1970: 226 Burns K.J., Shultz A.J., Title P.O., Mason N.A., Barker F.K., Caryothraustes canadensis frontalis Peters 1970: 225 Klicka J., Lanyon S.M. & Lovette I.J. 2014. Phylogenetics and diversification of tanagers (Passeriformes: Thraupidae), the largest Type-locality: Bahia, Brazil radiation of Neotropical songbirds. Molecular Phylogenetics and Diagnosis: specimens north to the São Francisco River Evolution 75: 41–77. show distinctive black stripe on the forehead in contrast to Cabanis J. 1851. Museum Heineanum: Verzeichniss der ornithologischen southern forms, which possess a bright-yellow forehead, Sammlung. Halberstadt. Cadena C.D. & Cuervo A.M. 2010. Molecules, ecology, morphology, both different from the olive forehead of Amazonian and songs in concert: how many species is Arremon torquatus species (Fig. 4). Average dimensions (mm): bill length (Aves: Emberizidae)? Biological Journal of the Linnean Society 99: 12.8; tail 70.8; tarsus 22; wing 96.7. 152–176. Distribution: Atlantic Forest from Pernambuco, eastern Carneiro L.S., Gonzaga L.P., Rêgo P.S., Sampaio I., Schneider H. & Aleixo A. 2012. Systematic revision of the Spotted Antpitta Bahia and Minas Gerais, to the lowland forests in Espírito (Grallariidae: Hylopezus macularius), with description of a cryptic Santo and Rio de Janeiro. new species from Brazilian Amazon. Auk 129: 338–351. Catchpole C.K. & Slater P.J.B 2008. Bird song: biological themes and nd variations. 2 edn. New York: Cambridge University Press. ACKNOWLEDGEMENTS Charif R.A., Waack A.M. & Strickman L.M. 2010. Raven Pro 1.4 User's Manual. Ithaca: Cornell Laboratory of Ornithology. Darriba D., Taboada G.L., Doallo R. & Posada D. 2012. jModelTest We are grateful to the São Paulo Research Foundation 2: more models, new heuristics and parallel computing. Nature (FAPESP) for the fellowship provided to V.R.T. (Proc. Methods 9: 772. No. 2010/19876-5) and F.B. (Proc. No. 2015/11397- nd Gotelli N.J. & Ellison A.M. 2012. A primer of ecological statistics, 2 4) and the Brazilian National Council for Scientific an d edn. Sunderland: Sinauer Associates. Guilherme E. 2012. Birds of the Brazilian state of Acre: diversity, Technological Development (CNPq) for the grants to zoogeography, and conservation. Revista Brasileira de Ornitologia L.F.S. To the curators and staff of the museums and 20: 393–442. sound archives: Museu Paraense Emílio Goeldi, Museum Gyldenstolpe N.C.G.F. 1945. The bir d fauna of Rio Juruá in western of Natural Science of the Louisiana State University, Brazil. Kungliga Svenska Vetenskapsakademien. Akademiens Handlingar 22: 1–337. Museu de Biologia Professor Mello Leitão, Museu Nacional Gyldenstolpe N.C.G.F. 1951. The ornithology of the Rio Purús region da Universidade Federal do Rio de Janeiro, Colección in western Brazil. Arkiv för Zoologi 2: 1–230. Ornitológica Phelps, Muséum National d'Histoire Hackett S.J. 1996. Molecular phylogenetics and biogeography of Naturelle, Museum für Naturkunde, Macaulay Library, tanagers in the genus Ramphocelus (Aves). Molecular Phylogenetics and Evolution 5: 368–382. Arquivo Sonoro Elias Coelho, Fonoteca Neotropical Jacques Hellmayr C.E. 1905. Notes on a colletion of birds, made by Mons. A. Vielliard and to MPEG and FMNH for providing us Robert in the district of Pará, Brazil. In: Rothschild H.W., Hartert the tissue samples used in the analyzes. We are also E. & Jordan K. (eds.). London: Novitates Zoologicae: A Journal grateful to the colleagues who provided us their personal of Zoology in connection with the Tring Museum. Hazell, Watson & Viney. recordings (see Apppendix II); Vagner Cavarzere Hellmayr C.E. 1938. Catalogue of birds of the Americas and the adjacent and Rafael Marcondes for the high-quality photos, islands in the Field Museum of Natural History, v. 13 part 11. Jaqueline Battilana for helping F.B. with the laboratory Zoological Series of the Field Museum of Natural History. procedures, and Adrian Barnett and Gustavo Bravo for IBGE (Instituto Brasileiro de Geografia e Estatística). 2012. Manual nd técnico da vegetação brasileira. 2 edn. Rio de Janeiro: Instituto critical review. Brasileiro de Geografia e Estatística, Manuais Técnicos em Geociências. Isler M.L., Isler P.R. & Whitney B.M. 1998. Use of vocalizations REFERENCES to establish species limits in antbirds (Passeriformes: Thamnophilidae). Auk 115: 577–590. Aleixo A. 2007. Conceitos de espécie e o eterno conflito entre Katoh K., Kuma K., Toh H. & Miyata T. 2005. MAFFT version 5: continuidade e operacionalidade: uma proposta de normatização improvement in accuracy of multiple sequence alignment. Nucleic de critérios para o reconhecimento de espécies pelo Comitê Acids Research 33: 511–518. Brasileiro de Registros Ornitológicos. Revista Brasileira de Klicka J., Burns K. & Spellman G.M. 2007. Defining a monophyletic Ornitologia 15: 297–310. Cardinalini: a molecular perspective. Molecular Phylogenetics and Aleixo A., Carneiro L.S. & Dantas S.M. 2012. Aves, p. 103–143. In: Evolution 45: 1014–1032. Martins F.D., Castilho A.F., Campos J., Hatano F.M. & Rolim Kroodsma D.E. 1984. Songs of the Alder Flycatcher (Empidonax S.G. (eds.). Fauna da Floresta Nacional dos Carajás: estudos sobre alnorum) and Willow Flycatcher (Empidonax traillii) are innate. vertebrados terrestres. São Paulo: Nitro Editorial. Auk 101: 13–24. Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Kroodsma D., Hamilton D., Sánchez J.E., Byers B.E., Fandiño- Ridgely R.S. & Tudor G. 2009. Field guide to the songbirds of South Mariño H., Stemple D.W., Trainer J.M. & Powell G.V.N. 2013. America. The Passerines. Austin: University of Texas Press. Behavioral evidence for song learning in the Suboscine Bellbirds Ronquist F. & Huelsenbeck J.P. 2003. MrBayes 3: Bayesian (Procnias spp.; Cotingidae). Wilson Journal of Ornithology 125: phylogenetic inference under mixed models. Bioinformatics 19: 1–14. 1572–1574. Kumar S., Stecher G. & Tamura K. 2016. MEGA7: Molecular Santos M.P.D., Cerqueira P.V. & Soares L.M.S. 2010. Avifauna em Evolutionary Genetics Analysis version 7.0 for bigger datasets. seis localidades no centro-sul do estado do Maranhão, Brasil. Molecular Biology and Evolution 33: 1870–1874. Ornithologia 4: 49–65. Linnaeus C. 1766. Systema naturae per regna tria naturae: secundum Sclater P.L. 1886. The catalogue of the bir ds in the British Museum. classes, ordines, genera, species, cum characteribus, differentiis, London: Taylor and Francis. synonymis, locis (v. 12). Stockholm: Laurentius Salvius. Silva J.M.C., Souza M.C. & Castelletti C.H.M. 2004. Areas of Marler P. & Tamura M. 1962. Song “dialects” in three populations of endemism for passerine birds in the Atlantic Forest, South White-crowned Sparrows. Condor 64: 368–377. America. Global Ecology and Biogeography 13: 85–92. Mendiburu F. 2015. Package ‘agricolae’: statistical procedures Silveira L.F. & Olmos F. 2007. Quantas espécies de aves existem no for agricultural research. https://CRAN.R-project.org/ Brasil? Conceitos de espécie, conservação e o que falta descobrir. package=agricolae. (access on 24 January 2016). Revista Brasileira de Ornitologia 15: 289–296. Miller M.A., Pfeiffer W. & Schwartz T. 2010. Creating the CIPRES Simas M. 2016. WA2080606,  Caryothraustes canadensis  (Linnaeus, Science Gateway for inference of large phylogenetic trees. New 1766). http://www.wikiaves.com.br. (access on 29 July 2016). Orldean: Gateway Computing Environments Workshop (GCE). Snethlage E. 1914. Catálogo das aves amazônicas contendo todas as Nakagawa S. 2004. A farewell to Bonferroni: the problems of low espécies descriptas e mencionadas até 1913. Boletim do Museu statistical power and publication bias. Behavioral Ecology 15: Paraense de História Natural e Etnographia, Belém 8: 1–530. 1044–1045. Somenzari M., Silveira L.F., Piacentini V.Q., Rego M.A., Schunck F. Nelson E.W. 1912. Descriptions of new genera, species and subspecies & Cavarzere V. 2011. Birds of an Amazonia-Cerrado ecotone in of birds from Panama, Colombia and Ecuador. Smithsonian southern Pará, Brazil, and the efficiency of associating multiple Miscellaneous Collections 60: 1–25. methods in avifaunal inventories. Revista Brasileira de Ornitologia Pacheco J.F., Kirwan G.M., Aleixo A., Whitney B.M., Whitakker A., 19: 260–275. Minns J., Zimmer K.J., Fonseca P.S.M., Lima M.F.C. & Oren Sorenson M.D., Ast J.C., Dimcheff D.E., Tamaki Y. & Mindell D.C. 2007. An avifaunal inventory of the CVRD Serra dos D.P. 1999. Primers for a PCR-based approach to mitochondrial Carajás project, Pará, Brazil. Cotinga 27: 15–30. genome sequencing in birds and other vertebrates. Molecular Payne R.B. 1986. Bird songs and avian systematics. Current Phylogenetics and Evolution 12: 105–114. Ornithology 3: 87–126. Stamatakis A. 2006. RAxML-VI-HPC: maximum likelihood-based Payne R.B. & Budde P. 1979. Song differences and map distances in phylogenetic analyses with thousands of taxa and mixed models. a population of Acadian Flycatchers. Wilson Bulletin 91: 29–41. Bioinformatics 22: 2688–2690. Peters J.L. 1970. Check-list of birds of the world, a continuation of the Stein R.C. 1963. Isolating mechanisms between populations of Traill's work of James L. Peters, v. 13. Paynter R.A. & Storer R.W. (eds.) Flycatchers. Proceedings of the American Philosophical Society 107: Cambridge: Museum of Comparative Zoology. 21–50. Piacentini V.Q., Aleixo A., Agne C.E., Maurício G.N., Pacheco J.F., Trainer J.M., McDonald D.B. & Learn W.A. 2002. The development Bravo G.A., Brito G.R.R., Naka L.N., Olmos F., Posso S., Silveira of coordinated singing in cooperatively displaying long-tailed L.F., Betini G.S., Carrano E., Franz I., Lees A.C., Lima L.M., manakins. Behavioral Ecology 13: 65–69. Pioli D., Schunck F., Amaral F.R., Bencke G.A., Cohn-Haft M., Villalobos D.C. & Villalobos J. 1947. Atlas de colores. Buenos Aires: Figueiredo L.F.A., Straube F.C. & Cesari E. 2015. Annotated El Ateneo. checklist of the birds of Brazil by the Brazilian Ornithological Whitney B.M., Pacheco J.F., Isler P.R. & Isler M.L. 1995. Hylopezuz Records Committee. Revista Brasileira de Ornitologia 23: 91–298. nattereri (Pinto, 1937) is a valid species (Passeriformes: Price J.J. & Lanyon S.M. 2002. Reconstructing the evolution of Formicariidae). Ararajuba 3: 37–42. complex bird song in the Oropendolas. Evolution 56: 1514–1529. Willis E.O. 1992. Three Chamaeza Antthrushes in eastern Brazil R Core Team. 2017. R: a language and environment for statistical (Formicariidae). Condor 94: 110–116. computing. Vienna: R Foundation for Statistical Computing. Zimmer K.J. 2008. The White-eyed Fo liage-gleaner (Furnaridae: http://www.R-project.org/. Automolus) is two species. Wilson Journal of Ornithology 120: Raposo M.A. & Höfling E. 2003. Overestimation of vocal characters 10–25. in Suboscine taxonomy (Aves: Passeriformes: Tyranni): causes and Zink R.M. 2004. The role of subspecies in obscuring avian biological implications. Lundiana 4: 35–42. Remsen-Jr. J.V. 1997. A new genus for the Yellow-Shouldered diversity and misleading conservation policy. Proceedings of the Grosbeak. Ornithological Monographs 48: 89–90. Royal Society of London B: Biological Sciences 271: 561–564. Rice N.H., Peterson A.T. & Escalona-Segura G. 1999. Phylogenetic patterns in montane Troglodytes wrens. Condor 101: 446–451. Associate Editor: Gustavo S. Cabanne. Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. APPENDIX I Specimens examined. For collection acronyms see Methods. Caryothraustes canadensis frontalis – 21: BRAZIL: São Miguel dos Campos (11 MZUSP 98475, MNRJ 34361); São Miguel (1 2 MZUSP 37728, MZUSP 37729, MZUSP 37730); Mangabeiras, Usina Sinimbu (7 4 MZUSP 37731, MZUSP 37732, MZUSP 37733, MZUSP 37734, MZUSP 39304, MZUSP 39305, MZUSP 39306, MZUSP 39307, MZUSP 39309, MZUSP 39308, MZUSP 39310); Quebrangulo, Engenho Riachão (1 MZUSP 39311); Ibateguara, Usina Serra Grande, Engenho Coimbra (2 MPEG 70547, MPEG 70548); Murici (1 35819); Igarassú, Recife, Usina São José (1? MNRJ 24749). Caryothraustes canadensis brasiliensis – 66: Porto Seguro, Estação Veracruz (2 MZUSP 76257, MZUSP 76258); Bahia (1 MZUSP 2538); Jequié, Serra do Talhão (1 MZUSP 14323); Ilhéus (1 1 MZUSP 33874, MZUSP 33875); Pacangê, Michellin Reserve (1 1? MZUSP 91568 MZUSP 91569); Ilhéus, Ecoparque de Una (2 1? MPEG 70825, MPEG 70826, MPEG 70827); Ilhéus, Fortuna River (2? MNRJ 25199, MNRJ 25200); Ilhéus (1 MNRJ 28011); Camumu (MNRJ 38130). Doce River, lower Suassuí (3 5 MZUSP 25280, MZUSP 25285, MZUSP 25289, MZUSP 25290, MZUSP 25287, MZUSP 25286, MZUSP 25288); Doce River, lower Piracicaba, right margin (1 1 MZUSP 25281, MZUSP 25282); Doce River, right margin (1 1 MZUSP 25283, MZUSP 25284). Reserva Florestal CRVD (2 1 MZUSP 98351, MZUSP 98350, MZUSP 98352); P. Cachoeiro (2 MZUSP 6155, MZUSP 6156); Espírito Santo (1 1 MZUSP 6274, MBML 6155); Pau Gigante (2 MZUSP 24675, MNRJ 7877); São José River (1? MZUSP 28124); Itaúna River, north of state (2 1 MZUSP 34603, MZUSP 34604, MZUSP 34605); Terra Alta (1 MBML 6235); Santa Tereza (7 2 MBML 6136, MBML 6138, MBML 6139, MBML 6140, MBML 6146, MBML 6147, MBML 6148, MBML 6152, MBML 6143); Santa Tereza Biological Station (1 MNRJ 44411); Santa Lúcia Biological Station (1 MNRJ 44410); Colatina (1 MNRJ 10500); Linhares (1 2 MNRJ 39558, MBML 6149, MBML 6144); Aracruz, Santa Cruz (4 3 MBML 6137, MBML 6141, MBML 6142, MBML 6145, MBML 6150, MBML 6154, MBML 6156); São Mateus (2 MBML 6151, MBML 6153). Muriaé River, Cardoso Moreira (1 MZUSP 27323); Petrópolis (1 MPEG 23645). Caryothraustes canadensis canadensis – 157: BRAZIL: Paca, right margin of Abacaxis River (1 MZUSP 77097); Camarão, right margin of Abacaxis River (1 MZUSP 77099); Camarão, left margin of Abacaxis River (1 MZUSP 77098); right margin of Canunmã River, lower part (1 MZUSP 96549); right margin of Canunmã River (1 1 MZUSP 96548, LSUMZ Field number B-81337); right margin of Sucunduri River, Across Ilha do Castanho (4 1? MZUSP 96546, MZUSP 96547, LSUMZ Field number B-85545, LSUMZ Field number B-85543, LSUMZ Field number B-96547); right margin of Sucunduri River, Igarapé da Cabaça (1 LSUMZ Field number B-80869); Manaus, Ducke Reserve (2 1 MPEG 30055, MPEG 30056, MPEG 30057); Tootobi River, tributary of Demini River (1? MPEG 37549); Jau River, left margin, Novo Airão (1 MPEG 50688); Itacoatiara (2 MNRJ 32808, MNRJ 32809). Serra do Navio (1 MZUSP 65511, 1 MNRJ 29265); Araguari River, right margin (1 2 MPEG 21649, MPEG 21649, MPEG 21652); Amapari River, Macapá (1 1 MPEG 23643, MPEG 23644); Amapari River, Serra do Navio (1 MPEG 24103); Igarapé Novo, left margin Igarapé Amazonas, left margin Iratapuru River (1 MPEG 29386). Igarapé Açu (2 MZUSP 6759, ZMB 281736); Capanema (3 1 MZUSP 32791, MPEG 23613, MPEG 23614, MPEG 23615); Belém, Utinga (2 5 MZUSP 36061, MZUSP 36060, MZUSP 46074, MZUSP 46075, MZUSP 46076, MZUSP 46077, MNRJ 10904); Belém (3 1 MZUSP 42814, MPEG 1541, MPEG 23616, ZMB 19026, 1 ZMB 31179); Município de Capim, Estrada Belém Brasília km 93 (19 11 2? MZUSP 46044, MZUSP 46045, MZUSP 46042, MZUSP 46043, MZUSP 46070, MZUSP 46046, MZUSP 46047, MZUSP 46048, MZUSP 46049, MZUSP 46051, MZUSP 46068, MZUSP 46069, MZUSP 46053, MZUSP 46057, MZUSP 46055, MZUSP 46054, MZUSP 46060, MZUSP 46058, MZUSP 46056, MZUSP 46059, MZUSP 46061, MZUSP 46062, MZUSP 46063, MZUSP 46050, MZUSP 46071, MZUSP 46072, MZUSP 46073, MZUSP 46067, MZUSP 46064, MZUSP 46065, MZUSP 46066, MZUSP 46052); Tailândia, Agropalma Reserve (1 1 MZUSP 77583, MZUSP 77584); Jubatituba (1 MPEG 898); Peixe Boi Experimental Station (1 MPEG 5664); Quatipuru River, Flor do Prado (2 MPEG 12629, MPEG 12630); Belém Brasília Road km 96 (4 MPEG 14343, MPEG 14344, LSUMZ 67926, LSUMZ 67927); Belém Brasília Road km 86 (1 1 MPEG 17977, MPEG 17978); Benevides, Baía do Sol, Retiro do Sol (2 1 MPEG 22148, MPEG 22156, MPEG 22183); Santa Barbara do Pará (1 MPEG 22194); Castanhal/Manaparim Road, km 86 (1 MPEG 23631); Acará-Mirim River, left margin, Tomé-Açu, Massaranduba (2 1 1? MPEG 26336, MPEG 26337, MPEG 26338, MPEG 26339); Bragança, Benjamin Constant, Sítio Manoel Horácio (1 MPEG 32331); Revista Brasileira de Ornitologia 25(3): 2017 Taxonomy and systematics of Caryothraustes canadensis Tonetti et al. Castanhal, Curuça Road (1 MPEG 35217); Santa Bárbara, Morelândia Farm, Genipaúba Road km 6 (1 MPEG 55920); Aveiro, Tapajós River, left margin, Escrivão (1 MPEG 64329); Alenquer, ESEC Grão-Pará (1 MPEG 65547); Itaituba, FLONA Amaná, right margin of Amaná River (1 1 MPEG 65660, MPEG 65661); Faro, Maracanã Village, Xingu River (1 MPEG 66890); Tomé Açu (1? MPEG 70274); Benevides (2 MPEG 8436, ZMB 8435); Baião (1 ZMB 31177); Bragança (1 1 MNRJ 10907, LSUMZ 67925). Mucajaí, Apiaú Colony (2 1 MPEG 46269, MPEG 46270, MPEG 46271); Couto de Magalhães River, Garimpo União (1 MPEG 49385). FRENCH GUIANA: French Guiana (2? MNHN 790, MNHN 1064). GUYANA: British Guiana (1 MZUSP 6760); Guiana (2 MNHN 2493, MNHN 2494); Kopinang River, 7 km SW Kopinang (2 LSUMZ 175537, LSUMZ 175537). VENEZUELA: Salto Maiza, Paragua River (1 1? COP 30837, COP 30841); Paragua River, Raudal (1 COP 26702); Paragua River, Raudal (1 1 1? COP 22805, COP 26701, COP 26698); La Faisca, mina Cerro Paraui-Tepui (1 2 2? COP 33166, COP 33162, COP 33163, COP 33164, COP 33165); Campamento Cruz, Yarra (1 2 COP 34782, COP 34783, COP 34784); San Fernando de Atabapó (1 2 COP COP 22185, COP 22186, COP 22187); Puerto Yapacana (4 5 COP 39779, COP 39778, COP 39781, COP 39782, COP 39784, COP 39785, COP 39786, COP 39787, COP 39780); Carabobo, Cuyum River (1 COP 46700); El Nenamo (1 COP 68100); Salto Guaiguinima, Paragua River (1 COP 30838); Paragua River, Cerro Tabarerupá (2? COP 26699, COP 26700); Puerto Yapacana (2? 1 COP 39783, COP 39778, 39777); Icabarú River (1 COP 42268); Culebra, Cunucunuma River (1 COP 74970); M. Parima (1 COP 70866); São Carlos of Negro River (2 COP 41883, COP 41884); Camp Jaime Benitez, slopes of Mt. Marahuaca (1 LSUMZ 25269). Caryothraustes canadensis simulans – 2: PANAMÁ: Prov. Darien, c. 9 km NW Cana on slopes of Cerro Pirre (2 LSUMZ 104752, LSUMZ 104753). APPENDIX II Recordings examined. For collection acronyms see methods. Caryothraustes canadenses frontalis – 10: BRAZIL: Usina Serra Grande, Engenho Coimbra (2 CORNELL 127847, CORNELL 127855); Santa Justina Farm (2 ASEC LPGD02715, ASEC LPGD02616 a-c ); Ibateguara, Usina Grande (1 ASEC LPGD03056); Campo Alegre, Mata Matão (1 Laherte Lobo de Araújo). Usina Trapiche, Mata do Tanguá (3 ASEC LPGD03223, ASEC LPGD03227, ASEC LPGD03308); Barreiros (1 Sidinei Dantas). Caryothraustes canadenses brasiliensis – 17: BRAZL: Jaguaquara (2 Vagner Cavarzere); Itacaré (1 Leonardo Patrial); Boa Nova (1 XC 84457). Pirapetinga (1 ASEC LPG08108). Linhares reserve (3 CORNELL 115347, CORNELL 115390, CORNELL 115401); Conceição da Barra, São Joaquim Farm (2 FNJV 8940, FNJV 9604); Santa Tereza, Nova Lombardia Reserve (2 FNJV 9140, FNJV 9142); Cafundó Farm (1 JMB07514); FLONA of Preto River (1 ASEC RR04122). Casemiro de Abreu (1 ASEC LPGDA1247-48); Guapiaçu Ecological Reserve (1 Ricardo Gagliardi); Casemiro de Abreu, União Biological Reserve (1 ASEC LPGD06903). Caryothraustes canadensis canadensis – 25: BRAZIL: Manaus (4 Marcelo Villegas, FNJV 7122); Presidente Figueiredo (1 XC 76377); Projeto de Assentamento Puxurizal (1 CORNELL 127705); Cachoeira Porteira, Cachorro River (2 FNJV 9978, FNJV 7123); Santa Bárbara, Mosqueiro (1 FNJV 7121). FRENCH GUIANA: Mana, piste ONF Dardanelles (1 XC 44065). GUYANA: E bank Waruma River (1 CORNELL 134927); Upper Demerara-Berbice 10.0 km N of Linden (1 CORNELL 85816). VENEZUELA: Capuchinbird Road, Bolívar (1 XC 12161); San Carlos of Negro River (1 Cornell 63330); Cuyuni River (1 CORNELL 63329); Grande River (4 CORNELL 63325, CORNELL 63326, CORNELL 63327, CORNELL 63328); Grande River, El Palmar (3 CORNELL 63321, CORNELL 63322, CORNELL 63323); La Tigra, El Palmar (1 CORNELL 63320); E of El Palmar, along road in Grande River Forest (1 CORNELL 60563); 19.0 km S of Las Claritas (1 CORNELL 112218). Revista Brasileira de Ornitologia 25(3): 2017

Journal

Ornithology ResearchSpringer Journals

Published: Sep 1, 2017

Keywords: Amazon; Atlantic Forest; genetic analysis; Oscines; Pernambuco Endemism Center; phylogeny; vocal analysis

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