SERGIO DAVID BOLÍVAR LEGUIZAMÓN
MORPHOLOGICAL VARIATION AND TAXONOMY OF LEPIDOCOLAPTES ANGUSTIROSTRIS (Vieillot, 1818) (PASSERIFORMES: FURNARIIDAE)
VARIAÇÃO MORFOLÓGICA E TAXONOMIA DE LEPIDOCOLAPTES ANGUSTIROSTRIS (Vieillot, 1818) (PASSERIFORMES: FURNARIIDAE)
SÃO PAULO 2014
SERGIO DAVID BOLÍVAR LEGUIZAMÓN
MORPHOLOGICAL VARIATION AND TAXONOMY OF LEPIDOCOLAPTES ANGUSTIROSTRIS (Vieillot, 1818) (PASSERIFORMES: FURNARIIDAE)
VARIAÇÃO MORFOLÓGICA E TAXONOMIA DE LEPIDOCOLAPTES ANGUSTIROSTRIS (Vieillot, 1818) (PASSERIFORMES: FURNARIIDAE)
Dissertação apresentada ao programa de Pós-Graduação do Museu de Zoologia da Universidade de São Paulo para a obtenção do título de Mestre em Sistemática, Taxonomia Animal e Biodiversidade
Orientador: Luís Fábio Silveira
SÃO PAULO 2014
Autorização
Autorizo a reprodução e divulgação total ou parcial deste trabalho, por qualquer meio convencional ou eletrônico, para fins de estudo e pesquisa, desde que citada a fonte.
I authorize the reproduction and dissemination of this work in part or entirely by any means electronic or conventional, for study and research, provide the source is cited.
I
Ficha Catalográfica
Bolívar-Leguizamón, Sergio David
Variação morfológica e taxonomia de Lepidocolaptes
angustirostris (Vieillot, 1818) (Passeriformes: Furnariidae)
Morphological variation and taxonomy of Lepidocolaptes
angustirostris (Vieillot, 1818) (Passeriformes: Furnariidae)
Dissertação (Mestrado) – Programa de Pós-Graduação em
Sistemática, Taxonomia Animal e Biodiversidade, Museu de
Zoologia da Universidade de São Paulo.
1.Variação Morfológica . 2. Taxonomia – Lepidocolaptes
angustirostris. 3. Passeriformes. 4. Silveira, Luís Fábio.
Comissão Julgadora:
Prof(a). Dr(a). Prof(a). Dr(a).
Prof. Dr. Luís Fábio Silveira Orientador
II
A mi família, y aquellos que a pesar de mi Tripolaridad, se preocupan por mi...
III
“...de modo que volvió al dormitorio, abrió la ventana del mar por si acaso descubría una luz nueva para entender el embrollo que le habían contado, y vio el acorazado de siempre que los infantes de marina habían abandonado en el muelle, y mas allá del acorazado, fondeadas en el mar tenebroso, vio las tres carabelas.”
El Otoño del Patriarca, Gabriel García Márquez.
IV Acknowledgements
This work could not have been accomplished without the help and cooperation of various institutions and individuals: First, I want to thank the USP and the MZUSP for allowing me to realize my Masters career here in Brazil, and learn and work within a great collection in the MZUSP. I also thank to the staff MZUSP for helped me resolve questions and problems here at the Museum (especially Marta, Sonia, and Omair). Thanks to CAPES for funding my Masters. I want to thank my adviser, PhD. Luis F. Silveira, for the opportunity to work in the research group of Ornithology of the MZUSP, and for his continuous support during my Masters program. Thank to PhD. Alexandre Aleixo and Fátima Lima of the Museu Paraense Emilio Goeldi (MEPG, Belém, Pará, Brazil), PhD. Gustavo Cabanne and Yolanda Davies of the Museo Argentino de Ciencias Naturales Bernardino Rivadavia (Buenos Aires, Argentina). Thanks to the ornithologists\biologists that recording the vocalizations of L. angustirostris and shared these records in WikiAves.com.br and Xeno-Canto.org. Thanks to the MZUSP taxidermists; Marina Lima and Marcelo Felix, for the preparation of the last specimens collected of L. agustirostris. Thanks to Paola Maria for his great support in the beginning of my stay here in São Paulo. Thanks to my friend of Facebook, Glaucia del-Rio for his advice in the statistical methods. Thanks to Gustavo Bravo for his advice during the course of the analysis; Vagner Cavarzere for the early review of my manuscript; Anna Ferrarroni for letting me stay a few days at its home; Rafael Marcondes for his advice in the initial part of my master's thesis. Thanks to my colleagues in the laboratory (alphabetical order): Aline, Anna F., Ana L., Ariane, Chico, Cristiane, Deborah, Diego, Erika M., Erica P., Fabio, Fernanda A., Fernanda B., Glaucia, Gabriela, Gustavo, Jeremy, Karlla, Luciano, Marcelo, Marco, Marina L., Marina S., Natalia A., Natalia L., Omar, Patricia, Rafael, Thiago, Tico, Vagner, and Vitor. Thanks to my friends from afar (Yes, a have some friends...): The biologists (Erika, Federico, and Laura), and my friends of the “outgroup”: Iván, Marlón, Yesid, Gutty, Dianis, Claudia, Cristian, Edwin, Cesar R. and Yei.
Gracias a MI FAMILIA por su apoyo y cariño!
V Abstract
Lepidocolaptes angustirostris (Narrow-billed Woodcreeper) is a South American woodcreeper that inhabits predominantly open lowlands such as the Cerrado, Chaco and Caatinga. This species exhibits highly variable morphology and vocalization throughout its range. The taxonomic position of L. angustirostris is doubtful; it can be located in at the root or within the Lepidocolaptes genus radiation, depending on the author. Two main groups are recognized within the species, a northern clade distributed in the lowlands of northern Bolivia and central and northern Brazil, and a southern group, which inhabits northern and central Argentina, Uruguay and the state of Rio Grande do Sul, in Brazil. Eight subspecies are currently recognized based on plumage and geographical distribution patterns. Based on the above information, the objective of this project was to conduct a taxonomic revision of L. angustirostris using morphometrical, plumage, and vocal characters. Second, with the aim to test the existence of phenotypic gradients associated to geographical and climatic variations in the taxon, a clinal and GLM analyses were performed. The phenotypic analyses allowed us to identify six main plumage types; however, we also found a high level of intergradation among all of these populations. The PCA analyses show certain levels of morphological differentiation among the populations, with a first component correlated with bill characters (bill length, exposed and total culmen), and a second one that reflects the bill width and the tarsus-metatarsus length. These two components could explain 70.88% of the morphological variation described. Evidence of a latitudinal morphological variation was found, summarized in a series of clines partially overlapped on a region localized from the southern Cerrado and Pantanal ecoregions through the Humid and Dry Chaco and the Paraná Flooded Savanna, to the Espinal and Humid Pampas ecoregions. Some climatic variables explain the geographical variation in the taxon, mainly, temperature seasonality, annual precipitation, and minimum temperature of the coldest month. The ecogeographic rules of Bergmann and Gloger are consistent with this variation, as well as the Allen’s rule, but more narrowly. Thus, the populations of the Narrow-billed Woodcreeper tend to be larger to the south of the distribution. Due the intergradation of all populations found, with no clear diagnosable population, we propose here that Lepidocolaptes angustirostris be treated as a unique species with no subordinate taxa. Any evidence collected here did not support the taxonomic validity of the proposed subspecies in the Narrow-billed Woodcreeper. Despite colour-polymorphism identified in the plumage patterns, the high level of intergradation, the poor resolution of
VI geographical boundaries, and the existence of clinal variation with a plausible introgression among populations not support the splitting of this species in several taxonomic subunits.
VII Resumo
Lepidocolaptes angustirostris (arapaçu-do-cerrado) habita principalmente regiões abertas como a Caatinga, Cerrado e Chaco. Esta espécie apresenta morfologia e vocalização muito variáveis em toda a sua distribuição geográfica. A posição taxonômica de Lepidocolaptes angustirostris não é clara, sendo localizado na raiz ou dentro da radiação do gênero Lepidocolaptes. Dois grupos principais são reconhecidos: um ‘grupo do norte’ que habita as terras baixas do norte da Bolivia e da região central do Brasil para o norte, e um ‘grupo do sul’ das regiões do norte ao centro-norte da Argentina, Uruguai, e no Estado do Rio Grande do Sul, sul do Brazil. Oito subespécies são atualmente reconhecidas baseadas em padrões da plumagem e distribuição geográfica. Com base nas informações acima, o objetivo deste projeto foi desenvolver uma revisão taxonômica de Lepidocolaptes angustirostris usando caracteres morfológicos e vocais. Além disso, para testar a existência da variação geográfica no táxon, uma análise clinal foi realizada. Finalmente, análises de (GLM) foram feitas para identificar variáveis ambientais que possam explicar esta variação. Os resultados indicam que as diferentes populações do complexo Lepidocolaptes angustirostris que habitam as areas abertas da Caatinga, Cerrado e Chaco (mais as populações amazônicas) não têm um nível significativo de diferenciação morfológica nem da plumagem para serem consideradas como espécies válidas. As análise do PCA apresentaram baixos níveis de diferenciação morfológica entre os grupos propostos, com um primeiro componente formado por caracteres do bico (comprimento, cúlmen exposto e cúlmen total), e um segundo componente formado por largura do bico e comprimento do tarso, explicando 70,88% da variação identificada. Igualmente, há evidência de uma variação morfológica latitudinal nos dados analisados, apresentado em uma série de clinas parcialmente sobrepostas sobre uma região localizada desde o sul do Cerrado e Pantanal através das ecoregiões do Chaco Úmido e Seco e a savana inundada do Paraná, até as ecoregiões do Espinal e dos Pampas Úmidos. Nas análises do GLM, algumas variáveis climáticas explicaram a variação geográfica no táxon; principalmente a sazonalidade térmica, a precipitação anual, e a temperatura minima do mês mais frio. As leis ecogeográficas de Bergmann e Gloger podem ser aplicadas nesta variação, assim como a lei de Allen, mas de forma restrita. Assim, as populações do Arapaçu-do- cerrado tendem a ser maiores ao sul da distribuição. A proposta apresentada aqui é de manter o status taxonômico de Lepidocolaptes angustirostris como uma espécie única, e propor evitar a utilização das denominações subespecíficas para este taxon. A validade taxonômica
VIII das subespécies no Arapaçu-do-cerrado não foi suportada por quaisquer das evidências coletada aqui. A pesar do polimorfismo de cores identificado nos padrões da plumagem, o elevado nível de intergradação, a baixa resolução dos limites geográficos entre as populações, e a presença de uma variação clinal com um nível considerável de introgressão entre populações não suportam a divisão de uma única espécie em várias sub-unidades taxonômicas.
IX Table of Contents
1. Introduction ...... 1 1.1. Order Passeriformes ...... 1 1.2. SubFamily Dendrocolaptinae (Furnariidae) ...... 1 1.3. Lepidocolaptes ...... 2 1.4. Lepidocolaptes angustirostris ...... 3 1.5. Taxonomic history of L. angustirostris ...... 8 2. Objectives ...... 11 3. Material and Methods ...... 12 3.1. Data collected ...... 12 3.2. Data Analyses ...... 13 3.2.1. Plumage ...... 13 3.2.2. External morphology ...... 13 3.2.3. Vocalizations ...... 13 3.2.4. OTU's definition and diagnosable traits ...... 14 3.2.5. Statistical Analysis ...... 14 3.3. Clinal analysis ...... 15 3.4. GLM Analyzes ...... 17 3.5. Distributional patterns ...... 18 4. Results ...... 19 4.1. Plumage description in Lepidocolaptes angustirostris ...... 19 4.1.1. Dorsal pattern ...... 19 4.1.2. Ventral Patterns ...... 26 4.2. Morphometry ...... 36 4.3. Vocalizations in the Narrow-billed Woodcreeper ...... 39 4.4. Clines ...... 44 4.5. GLM analysis and environmental variables ...... 50 4.6. How many taxa in Lepidocolaptes angustirostris? ...... 56 4.7. Taxonomy of the Narrow-bille Woodcreeper ...... 59 5. Discussion ...... 63 5.1. Delimitation of the species ...... 63 5.2. Plumage patterns and polymorphism in L. angustirostris ...... 65
X 5.3. Clinal variation ...... 67 5.4. Environmental correlations and biogeographical considerations ...... 71 5.5. The ‘Amazonian’ populations of the Narrow-billed Woodcreeper ...... 75 6. Conclusions ...... 77 7. Bibliography ...... 78 Appendix A ...... 94 Appendix B ...... 127
XI List of Figures
Figure 1. Individuals/localities sampled of L. angustirostris (Individuals without coordinates not included in this map)………………………………..…………………………………… 12 Figure 2. Individual with a Strong brown pattern (MZUSP 63445, Fazenda Campos bons 38 km N. floresta, Pernambuco, Brazil)…………………………..…………………………….. 20 Figure 3. Distribution of Strong brown pattern………………………...……………………. 20 Figure 4. Individual with an Intermediate pattern (MACN 217A, Gualeguaychu, Entre Rios, Argentina)………………………………………………………………………………..….. 22 Figure 5. Distribution of Intermediate pattern………………………………………………. 22 Figure 6. Individual with an Olive-brown pattern (MACN 66339, Campus UNLP, Santa Rosa, La Pampa, Argentina). …………………………………………………………………….... 24 Figure 7. Distribution of Olive-brown pattern…………………………………….………… 24 Figure 8. Overlapped distribution of the dorsal patterns……………………………………. 25 Figure 9. Individual with cinnamon-ochraceous pattern (MZUSP 63445, Fazenda Campos bons 38 km N. floresta, Pernambuco, Brazil)...... 26 Figure 10. Individual with pale yellow pattern (MZUSP 77726, Parque Nacional da Serra das Confusões, Piauí, Brazil)...... 27 Figure 11. Distribution of cinnamon-ochraceous and pale yellow patterns……………….... 28 Figure 12. Individual with Greyish-white pattern pattern (MZUSP 29879, Rio Arica, Mato Grosso, Brazil)………………………………………………………………………...…….. 29 Figure 13. Distribution of Greyish-white pattern……………………………………………. 29 Figure 14. Individual with Intermediate ventral pattern (MZUSP 64173, Retiro da Telha, margem direita Rio Sucuríu, Mato Grosso, Brazil)...... 30 Figure 15. Distribution of Intermediate ventral pattern pattern...... 31 Figure 16a. Individual with dark brown streaked pattern (MZUSP 31795, Las cañitas, Tucumán, Argentina)……………………………………………………...………………… 32 Figure 16b. Individual with rufous streaked pattern (MACN 30516-30517, Alto Rio Santa Maria, Orán, Salta, Argentina) ……………………………………………………………… 32 Figure 17. Distribution of streaked patterns……………………………………………….… 33 Figure 18. Distribution of ventral patterns in L. angustirostris……………………………... 34 Figure 19. Overlapped distribution of cinnamon-ochraceous and pale yellow patterns………………………..……………………………………………………………... 34
XII Figure 20. Overlapped distribution of pale yellow and dirty greyish-white patterns. ……………………………………………………………………………………………….. 35 Figure 21. Overlapped distribution of dirty greyish-white and the ‘intermediate’ patterns………………………………………………………………………………………. 35 Figure 22. Contact zone of the intermediate/streaked patterns. …………………………….. 36 Figure 23. Principal components in L. angustirostris. (a) Characters in the PC1 variate. (b) Characters in the PC2 variate………………………………………………………………... 37 Figure 24. Principal components - sclatter plot. (a) Individuals plotted on the principal components. (b) OTUs identified on the PCA components. ………………………………... 38 Figure 25. Division between No-streaked and Streaked populations (PCA analysis), confidence level: 0.95……………….………………………………………………………. 38 Figure 26. Sonogram of song Type I in L. angustirostris (Curaça, Bahia, Brazil). ……………………………………………………………………………………………….. 39 Figure 27a. Sonogram of song Type II in L. angustirostris (Sento Sé, Bahia, Brazil). ……………………………………………………………………………………………….. 40 Figure 27b. Sonogram of song Type II in L. angustirostris (Faz. SantaTeresa, Mato Grosso, Brazil). ………………………………………………………………………………………. 40 Figure 27c. Sonogram of song Type II in L. angustirostris (El Cutal, Beni, Bolivia). ……………………………………………………………………………………………….. 40 Figure 27d. Sonogram of song Type II in L. angustirostris (Reserva Natural del Bosque Mbaracayu, Canindey, Paraguay)..………………………………………………………….. 41 Figure 27e. Sonogram of song Type II in L. angustirostris (2.0 km E of Ocloyas, Jujuy, Argentina).………………………….……………………………………………………….. 41 Figure 28a. Sonogram of song Type III in L. angustirostris (Corumbá, Mato Grosso do Sul, Brazil)……………………………….……………………………………………………….. 41 Figure 28b. Sonogram of song Type III in L. angustirostris (W of Santa Rosa de la Roca, Santacruz, Bolivia)……………………………….………………………………………….. 42 Figure 28c. Sonogram of song Type III in L. angustirostris (El Cutal, Beni, Bolivia). ……………………………………………………………………………………………….. 42 Figure 29a. Sonogram of song Type IV in L. angustirostris (2.0 km E of Ocloyas, Jujuy, Argentina). ………………………………………………………………………………….. 42 Figure 29b. Sonogram of song Type IV in L. angustirostris (Acambuco-Tartagal, Salta, Argentina). ………………………………………………………………………………….. 43
XIII Figure 29c. Sonogram of song Type IV in L. angustirostris (El Relincho, Ecilda Paulier, San Jose, Uruguay). ……………………………………………………………………………... 43 Figure 30a. Clinal models fitting the bill length, exposed and total culmen. Trait value: Mean of the character by point, Distance: Distances from the first point (first sampled locality) to the last point sampled………………………………………………………………………... 44 Figure 30b. Clinal region for bill length, exposed and total culmen. ………………………. 45 Figure 31a. Clinal model fitting the wing length and bill width. Trait value: Mean of the character by point, Distance: Distances from the first point (first sampled locality) to the last point sampled…..……………………………………………………………………………. 46 Figure 31b. Clinal region for wing length and bill width. ……..…………………………… 46 Figure 32a. Clinal model fitting the tail length. Trait value: Mean of the character by point, Distance: Distances from the first point (first sampled locality) to the last point sampled.…………………………………………………………...………………………… 47 Figure 32b. Clinal region for tail length. ………………………………………………….... 47 Figure 33a. Clinal model fitting the bill height. Trait value: Mean of the character by point, Distance: Distances from the first point (first sampled locality) to the last point sampled……………………………………………………………………………………… 48 Figure 33b. Clinal region for bill height.………………………….………………………… 48 Figure 34a. Clinal model fitting the tarsus-metatarsus length. Trait value: Mean of the character by point, Distance: Distances from the first point (first sampled locality) to the last point sampled.……………………………………………………………………………….. 49 Figure 34b. Clinal region for tarsus-metatarsus length……………………………………… 49 Figure 35. Correlation PC1 - Temperature seasonality……………………………..……….. 50 Figure 36. Correlation PC2 - Temperature seasonality.…………………………………...… 51 Figure 37. Correlation Size - Precipitation of Warmest Quarter…………………..………... 51 Figure 38. Correlation Ventral plumage - Temperature seasonality..……………………..… 52 Figure 39. Main models explaining the PC1 variation. Red line: relative importance of model terms 80% (support of each variable across all models)…………………………………….. 53 Figure 40. Main climatic variables explaining the PC2 variation. Red line: relative importance of model terms 80% (support of each variable across all models)………………………….. 54 Figure 41. Main climatic variables explaining the size variation. Red line: relative importance of model terms 80% (support of each variable across all models)………………………….. 55 Figure 42. Correlation of size variation and Latitude……………………………...………... 55
XIV Figure 43. Main climatic variables explaining ventral patterns (no-streaked/streaked). Red line: relative importance of model terms 80% (support of each variable across all models)…………………………………………………………..…………………………... 56 Figure 44a. Individuals of L. angustirostris analized from Caatinga to central Cerrado (from the left to right), showing the no-streaked ventral plumage, and the gradual variation between the cinnamon-ochraceous and the pale yellow patterns.…………………………………….. 57 Figure 44b. Individuals of L. angustirostris analized from central Cerrado to central-southern Great Chaco (including Humid Pampas and adjacent regions), showing the intermediate and streaked ventral plumages (from the left to right), and the gradual variation between the no- streaked, the intermediate (slightly streaks), and the dark brown streaked pattern…………. 58 Figure 44c. A graphical summary of variation of L. angustirostris, from the northern Brazil to Northern-central Argentina (from left to right)……………………………………………… 62 Map I. Localities used as “sampling units” for the clinal analysis………………………… 136
XV List of Tables
Table 1. Parameter value used in the clinal anaylses. (*) Clinal area analyzed. (**) Range of the clinal center. (a) Not normal characters. (***) Runs with free parameters...... 16 Table with the 555 skins analyzed of the Narrow-billed Woodcreeper (21 individuals without geographical coordinates)………………..………………………………………………….. 94 Table 2. Descriptive statistics of Bill length…………..…………………………...………. 127 Table 3. Descriptive statistics of Exposed culmen……….……………………………...… 127 Table 4. Descriptive statistics of Total culmen……………..……………………………… 128 Table 5. Descriptive statistics of Bill height………………….……………………………. 128 Table 6. Descriptive statistics of Bill width……………………..…………………………. 129 Table 7. Descriptive statistics of Wing length…………………….……………………….. 129 Table 8. Descriptive statistics of Tail length………………………….……………….…… 130 Table 9. Descriptive statistics of Tarsus-metatarsus length………………………………... 130 Table 10. Kruskall-Wallis test of the OTUs proposed. ns: no significance/*: 0.05 > p > 0.01/**: 0.01 > p > 0.001/ ***: p < 0.001…………………………………..…………...… 131 Table 11. Mann-Whitney test for Bill length. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01> p > 0.001/ ***: p < 0.001………………………………………………………………...... 131 Table 12. Mann-Whitney test for Exposed culmen. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001…………………………………………...... 132 Table 13. Mann-Whitney test for Total culmen. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001………………………………………………………...... 132 Table 14. Mann-Whitney test for Bill height. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001…………………………………………………………………... 133 Table 15. Mann-Whitney test for Bill width. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001…………………………………….…………….………………. 133 Table 16. Mann-Whitney test for Wing length. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001………………………………………………………………… 134 Table 17. Mann-Whitney test for Tail length. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001………………………………………………………………… 134 Table 18. Mann-Whitney test for Tarsus-metatarsus length. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001………………………………………………… 135
XVI Table 19. Summary of Mann-Whitney tests. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001…………………………………………….…….………………. 135 Table 20. Clinal models fitted to Bill length……………………………..………………… 136 Table 21. Clinal models fitted to Exposed culmen. (NA) Clinal model not available…….. 137 Table 22. Clinal models fitted to Total culmen. (NA) Clinal model not available…...... 137 Table 23. Clinal models fitted to Wing length. (NA) Clinal model not available…….....… 137 Table 24. Clinal models fitted to Bill width. (NA) Clinal model not available……………. 138 Table 25. Clinal models fitted to Tail length. (NA) Clinal model not available…………... 138 Table 26. Clinal models fitted to Bill height. (NA) Clinal model not available…….……... 138 Table 27. Clinal models fitted to Tarsus-metatarsus length. (NA) Clinal model not available……………………………………………………………………………...... 139 Table 28. BIOCLIM variables (and their codes) used in preliminary GLM analysis……... 140 Table 29. BIOCLIM variables least correlated used in the GLM with interactions……….. 141 Table 30. Correlation matrix of BIOCLIM variables…………………………………...... 142 Table 31. Models identified in the analysis of PC1 and the BIOCLIM variables…...…….. 143 Table 32. Models identified in the analysis of PC2 and the BIOCLIM variables…………. 144 Table 33. Models identified in the analysis of the size and the BIOCLIM variables……… 145 Table 34. Models identified in the analysis of ventral patterns and the BIOCLIM variables……………………………………………………………………………………. 146 Table 35. Vocalizations collected of L. angustirostris…………………………………...... 147
XVII 1. Introduction
1.1. Order Passeriformes
The order Passeriformes is the largest avian order, comprising over 5.700 species (Sibley & Monroe, 1990; Monroe & Sibley, 1993), being a dominant evolutionary component of the global avifauna. The group is considered monophyletic by several morphological and molecular studies (Raikow 1982; Sibley & Ahlquist 1990; Barker et al. 2004; Livezey & Zusi 2007; Treplin et al. 2008; Pacheco et al. 2011, among others). The following morphological characters support monophyly in Passeriformes; the palate aegithognathous (a specific type of palatal arrangement of the bones), the presence of Spermatozoa bundled with coiled head and large acrosome, presence of arrangement type VII in deep plantar tendons (where there is not connection between the flexor digitorum longus -- FDL -- and flexor hallucis longus -- FHL -- tendons), and loss of intrinsic foot muscles of digits II, III, and IV (see Raikow, 1982). Others traits are considered specific of this taxon, like a metabolic rate that tends to be higher than other avian taxa of comparable size, and superior learning abilities (see Spicer & Dunipace, 2004). The origin of Passeriformes is estimated prior to Cretaceous/Tertiary (K/T) boundary (aproximately 76-78 My, see Pacheco et al. 2011). Traditionally, the order is divided in two suborders; Tyranni (suboscines) and Passeri (oscines) (Sibley & Ahlquist 1990, among others), but other approaches have been proposed, partitioning Passeri in Passerida and Corvida (Livezey & Zusi, 2007; Pacheco et al., 2011). Passeriformes is represented by approximately 45 families, and show a broad range of ecological tolerances and trophic adaptations and their taxa habit in most terrestrial biomes.
1.2. Subfamily Dendrocolaptinae (Furnariidae)
The Dendrocolaptidae Gray, 1840 constitute a highly specialized lineage within the New World suboscine radiation that usually was regarded as the sister-group to ovenbirds (Furnariidae) (see Sibley & Ahlquist, 1990). Recent molecular studies placed this group as Dendrocolaptinae, a subgroup nested in the Furnariidae clade, excluding the genus Sclerurus
1 (sensu Irestedt et al. 2002; Derryberry et al. 2011; but see Moyle et al. 2009). The woodcreepers have 52 species which nest in existing tree cavities and are scansorial with specialized tail-tips providing support as they climb on tree-trunks (see Fjeldså et al., 2005; Bodrati & Cockle, 2011). The members of the clade primarily forage along trunks and branches. Due to their common lifestyle woodcreepers form a morphologically homogeneous assemblage, and several features in woodcreepers are certainly adaptations to their climbing behaviour, e.g. the inwards curved, stiffened tail-tips and the partly fused forwards-directed phalanges (Claramunt et al., 2012). However, the group also exhibits great variations in size and in bill morphology (Raikow, 1994; Marantz et al., 2003). They are mainly brown and rufous birds, with ferrugineous wings and tail. Though relatively easy to observe, taxonomic identification to species is often difficult. Woodcreepers are arboreal, with the majority of the species occurring in forests of varying types; they reach maximum diversity in Amazonia. Nests are usually placed in tree holes or behind pieces of bark (Ridgely & Tudor, 2009). Dendrocolaptinae appears be monophyletic in recent studies using several data resources. For example, Raikow (1994) showed that morphologically there are synapomorphies to Dendrocolaptinae group (hindlimb morphology, horns of the syrinx, among others) and Irestedt et al. (2002, 2004) and Derryberry et al. (2011) support this statement in their molecular analysis.
1.3. Lepidocolaptes
Lepidocolaptes Reichenbach, 1853 is a uniform group of slim, fairly small woodcreepers (170 - 210 mm) with distinctive pale, slender, decurved bills; they are almost always well streaked below, though many are unstreaked above. The genus contains ten species, eight of which are present in South America: Lepidocolaptes souleyetii (Des Murs, 1849), L. angustirostris (Vieillot, 1818), L. squamatus (Lichtenstein, 1822), L. falcinellus (Cabanis & Heine, 1859), L. wagleri (Spix, 1824), L. albolineatus (Lafresnaye, 1846). L. lacrymiger (Des Murs, 1849), and the recently discovered L. fatimalimae (Rodrigues et al., 2013). The other two, L. leucogaster (Swainson, 1827) and L. affinis (Lafresnaye, 1839) inhabits Central America. Lepidocolaptes range widely in forested or more lightly wooded habitats, depending on the species. They are found in a variety of habitats ranging from tall montane forest high in
2 the Andes, to the subcanopy of humid lowland forest, to fairly open scrub and Cerrado (Ridgely & Tudor, 1994, 2009). In this genus, three species inhabit montane forest and five lowlands regions, and two species are found mainly in non-forested habitats (Ridgely & Tudor, 1994; Marantz et al., 2003). The majority of biomes and ecoregions in the Neotropics are inhabited by at least one species of Lepidocolaptes. The monophyly of genus has beem discussed extensively. By the morphological and molecular data some authors (Raikow, 1994; Irestedt et al., 2004) find this genus not monophyletic. However, recent studies have confirmed the monophyly of this taxon (Derryberry et al., 2011; Arbelaéz-Cortés et al., 2012).
1.4. Lepidocolaptes angustirostris
Lepidocolaptes angustirostris (Dendrocopus angustirostris, Vieillot 1818, Paraguay), is a widespread species that inhabits semiopen areas of east and south-center South America. It is a small species, with the total length ranging from 195 to 210 mm in adult birds. Lepidocolaptes angustirostris is uncommon to locally common in gallery woodland, Chaco and Caatinga woodland, Cerrado, and agricultural areas with scattered trees. A characteristic species of deciduous forests, forests islands, gallery forest, second growth, forest edge, espinilho (Prosopis-Acacia) savanna, and open situations near humans; sometimes frequents Mauritia palm swamps and, on Marajó (Brazil), várzea forest. L. angustirostris is a conspicuous woodcreeper, usually found singly or in pairs, hitching up trunks and larger branches of trees and shrubs, also often investigating wooden fence posts, probing into crannies and flaking off pieces of loose bark. Although sometimes with loose mixed flocks, at least as often it forages independently. Inhabits primarily tropical lowlands to 1200 m in most of range; also in subtropical zone in Andean foothills to almost 3000 m in Bolivia (Ridgely & Tudor, 1994; Marantz et al., 2003) Lepidocolaptes angustirostris feeds on insects and others invertebrates. Most prey for which size could be estimated had 5-15 mm long. This taxon is often encountered sometimes in small groups, and regularly in mixed/species flocks; present in 45% of flocks at one site in Brazilian Cerrado. Observed very rarely in association with birds attending swarms of army ants (Labidus). The species forages primarily while hitching up trunks and branches, often with spiraling motion, for near base of trees to subcanopy, sometimes higher; also used
3 wooden fence posts. Most prey either gleaned from surface or taken from bark crevices, epiphytes, moss or other substrates by probing with slim bill, or by flaking or prying off bark to expose hidden prey (see Marantz et al., 2003). Generally, Lepidocolaptes angustirostris nests during the first and last months of year (Oct. to Nov.-Jan.), but in certain regions can nest in February to March (Santa Cruz, Bolivia), July (Amapá, Brazil) or August (Santa Cruz), also, the breeding season depends on each region for a widespread taxon like as the Narrow-billed Woodcreeper. The nests are found in various types of cavity, from natural holes in tree and old holes of woodpecker species (Picidae) to cavity in cement column, bridge support or other man-made structure, entrance generally quite low, from near ground level to 4 m above, and often narrow (e.g. 8 x 4 cm) but may be enlarged and rounded, cavity depth 20-160 cm; eggs placed on bed of leaves, grasses bark or wood chips, sometimes of Eucalyptus, that may lie atop thick bed of similar but coarser flakes. L. angustirostris clutchs 3-4 dull-white eggs per nest, average 25.5 x 19 mm; chick hatches naked and, like those of congeners, is quite vocal. There is no sexual dimorphism in this species (Marantz et al., 2003). Although the population size has not been quantified, the Narrow-billed Woodcreeper has an extremely large range and this population trend appears to be increasing. Thus, is does not seem to be in a vulnerable state. To IUCN, L. angustirostris is evaluated as Least Concern (IUCN list). The populations of L. angustirostris inhabit throughout the open/dry areas of South America. These regions can be represented in three ‘main’ regions: The Cerrados, The Caatinga, and The Chaco (The Gran Chaco). These three regions form part of the so-called diagonal of open formations by Vanzolini (1963) or corridor of ‘xeric vegetation’ (Bucher, 1982). The Cerrado(s) occupies Brazil plus small areas of Bolivia and northwestern Paraguay; the much drier Caatinga the northeastern Brazil; and the Chaco occupies Paraguay (western and central regions), Bolivia (south), and Argentina (northern and central regions) (Morrone, 2001; Oliveira-Filho & Ratter, 2002; Morrone, 2014). Other authors have classified these ecoregions in different way, Pennington et al. (2006) divides the ‘Cerrado Biome’ into three main regions; the savanna (Cerrado and related regions), the Chaco, and the seasonally dry tropical forest (Caatinga and related regions) regions. The typical vegetation landscape of the Cerrado consists of savanna of very variable structure, on the well-drained interfluves, with gallery forests or other moist vegetation
4 following the watercourses; in this gallery forests, a considerable number of species are shared with the two great adjacent South American forest provinces: the Amazon and the Atlantic coast forests of Brazil (Oliveira-Filho & Ratter, 1995). The strict sense of Caatinga may be characterized as a low forest composed mostly of small trees and shrubs, frequently having twisted trunks and thorns, with small leaves that are deciduous in the dry season. Succulent plants of the family Cactaceae are common, and there is an ephemeral herbaceous layer present only during the short rainy season (Pennington et al., 2006; de Queiroz, 2006). The Chaco vegetation is bounded by several different vegetation types, some of which are transitional in floristic composition, particularly along the eastern Chaco boundary. The dominant form of Chaco vegetation is characterized by a forest of trees and shrubs that are often spiny and mostly deciduous in the dry season. The understory is often shrubby, with a variety of herbs and grasses growing in association with bromeliads and cacti, some of which are arborescent (Daly & Mitchell, 2000). The taxonomic position of Lepidocolaptes angustirostris is not definitive and clear; some authors suggest that this species is sister to all other taxa within the genus (Arbelaéz- Cortés et al. 2012). On the other hand, evidence supports that L. angustirostris seems to be sister to L. leucogaster (Raikow, 1994; García-oreno & Da Silva, 1997; Derryberry et al., 2011). Phylogeographycally, low genetic differences between samples of L. angustirostris were found from Brazil, Bolivia and Argentina populations (using COI and cyt b haplotypes), suggesting a recent range expansion of species (Arbelaéz-Cortés et al., 2012). Generally, two groups are distinguished, and they apparently intergrade across a broad zone of contact extending from east Bolivia south to south-east Brazil: members of the “angustirostris group” which also includes certhiolus, hellmayri, and praedatus; are browner above and more heavily streaked below. The populations of the “bivittatus group” (bivittatus, bahiae, coronatus, and griseiceps subspecies) are more rufescent above and largely unstreaked below (see Marantz et al., 2003). Additional races have been proposed but are currently considered invalid: dabbenei (south-west Paraguay and north Argentina) and chacoensis (north-east Argentina), which were synonymized with the subspecies praedatus, for intergrading widely with the nominotipic form. Another described race, immaculatus (northern Bolivia) was synonymized with bivittatus. Description of L. angustirostris griseiceps was possibly based on individual variance with extremely pale plumage; known
5 only from type locality (Sipaliwini savanna, Suriname). The geographical variation in plumage is difficult by age-related (immature individuals have streaked, see Luz et al., 2007) and seasonal differences (it inhabits highly variable environments). Also, to the presence of adventitious plumage (mainly in the Cerrado, some individuals acquire a dark coloration in their underparts due to that they perch in the newly burned trees). However, currently eight subspecies are recognized based in colour patterns and geography (Marantz et al., 2003): L. a. angustirostris (Vieillot, 1818), south-west Brazil (west Mato Grosso do Sul) and east Paraguay in drainages of Paraguay and Paraná rivers; intergrades with praedatus in north and north-east Argentina (west Salta, Formosa, west Chaco, north Corrientes, north Santa Fe). L. a. bivittatus (Lichtenstein, 1822), center and south-east Brazil (Mato Grosso E to Goiás and Minas Gerais, and south to Rio de Janeiro and São Paulo; also in Pará along south bank of lower Amazon river from east rio Tapajós to Marajó Island) and north and east Bolivia (La Paz, Beni, Santa Cruz). L. a. coronatus (Lesson, 1830), in north-east Brazil from south and east Maranhão east to north Piauí, and south to Tocantins and north-west Bahia. L. a. bahiae (Hellmayr, 1903), north-east Brazil in interior Bahia (east of river São Francisco); populations north of São Francisco river from Ceará east to Paráıba, south to east Piauí and Alagoas probably represent this race. L. a. certhiolus (Todd, 1913), lowlands at east base of Andes in center and south Bolivia (south-west Santa Cruz south to Tarija), west Paraguay (Alto Chaco) and north-west Argentina (south-east Jujuy, north Salta). L. a. praedatus (Cherrie, 1916), north and center Argentina (southern Salta, Santiago del Estero, southern Santa Fe, southern Corrientes and south-western Misiones, south to Mendoza, northern La Pampa and north-eastern and south-western Buenos Aires), west and centre Uruguay and extreme southern Brazil (western and south-western Rio Grande do Sul; Marantz et al. 2003). L. a. hellmayri (Naumburg, 1925), in Andean foothills of central Bolivia (Cochabamba, Santa Cruz, Tarija). L. a. griseiceps (Mees, 1974) is known only from the type locality in southern Suriname (Sipaliwini Savanna), but populations on north side of lower Amazon river in north Brazil (east Pará and Amapá) appear to represent this subspecies. The nominotipic group (east Bolivia, Paraguay, and north Argentina) has a long,
6 narrow, somewhat decurved, mostly pinkish bill (with base of maxilla dusky). Crown and nape dusky streaked with buffy whitish, broad superciliary buffy whitish, and auriculars plain blackish; above otherwise rufous brown. Throat whitish; remaining underparts buffy whitish with diffuse dusky streaking (Marantz et al., 2003). The northern group (lowlands of north Bolivia and south-center Brazil northward), which includes L. a. bivittatus and related forms, is similar to nominate group but is brighter rufous above and essentially unstreaked buffy whitish below. The southern group (north to north-center Argentina, Uruguay and Rio Grande do Sul at Brazil) includes L. angustirostris praedatus and L. a. dabbenei subspecies; they are similar but somewhat duller and browner above and more prominently streaked with blackish below (Ridgely & Tudor, 1994). Races vary mainly in tone of colour above and below and degree of streaking below: within “angustirostris group”, L. a. praedatus is larger and longer-billed than nominotipic, upperparts being more olive-brown overall, the rufous is duller and restricted to centers of back feathers, streaking below being heavier and blacker; hybrids between nominotipic and L. a. praedatus occur over a broad zone in north and north-east Argentina, and, as expected, show a mixture of characters (degree of streaking below, coloration above, bill length; Marantz et al. 2003). Linking streaked southern races with unstreaked northern forms, L. a. certhiolus is lighter above than nominotipic (cinnamon-rufous to ferruginous); L. a. hellmayri is much brighter rufous above than southern birds, but deeper rufous above and more conspicuously streaked below than L. a. bivittatus; it is also larger and longer-billed than nominotipic, L. a. certhiolus, and L. a. bivittatus. Members of “bivittatus group” are more rufescent above and at most weakly streaked below; within this group, L. a. bivittatus is comparatively pale (creamy to dirty greyish-white) below, with breast and undertail-coverts indistinctly streaked; L. a. coronatus is similar to L. a. bivittatus, but underparts deeper buff, approaching ochraceous on undertail-coverts, which shows at most a few fine streaks; L. a. bahiae is even more richly coloured below, extensively deep cinnamon to ochraceous, brightest on sides and undertail-coverts; L. a. griseiceps is the palest of all, crown being brownish-grey with broad but indistinct streaking, underparts unstreaked and entirely creamy white (lacking contrast between belly and undertail coverts; Marantz et al. 2003).
7 1.5. Taxonomic history of L. angustirostris
The first naturalist describing the Narrow-billed Woodcreeper was Azara (1802). He called them as “Trepadores del Comun”, written in a classic book on avifauna of Paraguay, and with no type specimen. Based on Azara’s work, Vieillot (1818) formally described and named L. angustirostris, using the name Dendrocopus angustirostris. According to the description of author (translation from French): “A Picucule with bill slightly curved along its length… a Spanish Tobacco coloration spread the superior parts of neck and body… throat with white feathers, frontal part of neck and inferior part of body dirty and slightly streaked” (Vieillot, 1818). Dendrocolaptes bivittatus Lichtenstein, 1822 was the second taxon described on this complex. This is a species with “sub-arched comprised palid bill, white throat and abdomen cinerascent-whitish”, based on birds from São Paulo. Spix (1824) attributed birds from Piauí, Brazil, to D. bivittatus Lichtenstein. However, Lesson (1830), described Spix’s birds as Picolaptes coronatus. Hellmayr (1903) described Picolaptes bivittatus bahiae (type locality: Bahia), a subspecies “similar to P. bivittatus, but the inferior parts (with exception of white throat) rusty yellow, the body sides and the lower part of tail are more vivid”. Todd (1913) described P. b. certhiolus based on specimens from Curiche, Rio Grande, Bolivia. These birds were considered by him “Similar to Picolaptes bivittatus bivittatus (Lichtenstein), but less suffused with buffy below; back and under wing-coverts less rufescent; and the superciliaries and streaks on the pileum paler, less buffy”. Picolaptes angustirostris praedatus Cherrie, 1916 was another subspecies described as “Similar to P. a. angustirostris but larger and bill longer…the streaking on the crown and nape extends further back than in P. a. angustirostris” (Cherrie, 1916). Naumburg (1925) described Lepidocolaptes angustirostris hellmayri for populations found in the subtropical zone of the Bolivian Andes (Cochabamba, Santa Cruz, and Tarija). This subspecies was considered “similar to L. a. bivittatus, but larger, with a longer, more powerful bill; back, wings, and tails generally of a deeper rufous; under parts conspicuously streaked with dusky or blackish brown, specially on the sides”. Another subspecies recognized in the L. angustirostris complex is L. a. griseiceps Mees, 1974; this taxon is “the palest of all subspecies. Throat white, remainder of the underparts, including the under tail coverts, cream. Crown brownish grey, with broad and not very well-defined white streaks”. Mees (1974) compared his two specimens from Sipaliwini savanna (Suriname) with the
8 representatives of the taxa bahiae, bivittatus, and coronatus, and concluded that his specimens belonged to an undescribed subspecies. As shown above, Lepidocolaptes angustirostris is a highly polymorphic woodcreeper, with a wider geographical distribution. The phenotypic traits of this taxon varies vary along its distribution, from northern Brazil to Argentina, on the open lands of Caatinga, Cerrado, and Chaco ecoregions. However, despite this marked variation, no comprehensive taxonomic study was carried out to clarify the status of the named populations. In the literature, Ridgely & Tudor (1994) proclaim the need to develop a review of the races of this taxon. Marantz et al. (2003) stated that the study of the geographical variation in plumage of the L. angustirostris populations is difficult by age-related and seasonal differences. For example, it is possible to find immature streaked individuals in regions mainly inhabited by no-streaked populations, and it could be a cause of errors in the taxonomic identification (as immature individuals in L. angustirostris are streaked). Other problem in the taxonomy of the Narrow- billed Woodcreeper is the presence of intermediate phenotypes throughout their distribution, and descriptions of the current subspecies based in very few specimens from geographically separated material. For the above reasons, a taxonomic review of L. angustirostris is desirable to clarify the taxonomic components of the species.
9 2. Objectives
The objective in this project is (1) to conduct a taxonomic revision of the Lepidocolaptes angustirostris complex. Additionally, (2) to determine the factors that shape the plumage variation (to identify the presence or not of clinal variation), and (3) to map the distributional range of the species.
10 3. Material and Methods
3.1. Data collected
A total of 555 skins of Lepidocolaptes angustirostris complex were examined at three main Museums (Appendix A); Museu de Zoologia da Universidade de São Paulo (MZUSP, 213 specimens), Museu Paraense Emilio Goeldi (MPEG, 104 specimens), and Museo Argentino de Ciencias Naturales (MACN, 217 specimens). Despite specimens from museums outside South America has not been examined, the sampling size and quality was considered sufficient in terms of individuals, phenotypic variation, and geographic coverage. The Figure 1 shows the distribution of the individuals examined (also, additional individuals without geographical coordinates were examined).
Figure 1: Individuals/localities sampled of L. angustirostris (Individuals without coordinates not included in this map).
The available literature about L. angustirostris and Dendrocolaptinae was consulted, including the original descriptions of taxa analyzed. All individuals were measured and analyzed, including types housed at the collections cited above. Complete measurements were
11 taken from 370 individuals, 226 have incomplete data due to loss or damage of structures (mainly bill measurements). Similarly, in some skins the plumage patterns and coloration were not adequate to study due to age or condition of the preparations (the age of skins can influence the coloration of plumage).
3.2. Data Analyses
3.2.1. Plumage
A visual analysis of plumage was conducted with the aim of identify variations in the patterns and coloration of individuals of L. angustirostris complex. All plumage characters were discretized, including the intensity of ventral streaking. These analyzed patterns and colorations were classified following Munsell's coloration chart (Munsell, 1994). So, two main regions were used to identify plumage patterns; namely ventral and dorsal regions. In the literature reviewed, other regions were proposed to be analyzed (crown, superciliary stripe, auriculars, undertail-coverts), but a visual analysis of these characters not shown diagnosable differences.
3.2.2. External morphology
The characters used were the bill length (distance between a proximal part of nostril related to bill tip), exposed culmen (distance between the bill tip to the point where the tips ofthe forehead feathers begin to hide the culmen), total culmen (distance between bill tip to the cranium), height and width of bill to at the nostril, wing length, tail length and tarsus- metatarsus length. The measurements were obtained using a digital caliper of 0,1 mm of precision (accuracy) in agreement with Baldwin et al. (1931).
3.2.3. Vocalizations
The vocal records were gathered mainly from ornithological websites (http://www.xeno- canto.org/, http://wikiaves.com.br/, http://www.macaulaylibrary.org/) and others multimedia
12 resources. Vocal records from the compilation of Lopéz-Lanús (2008), records from WikiAves website, the Macaulay Library of the Cornell Lab of Ornithology, and from Xeno- Canto website were analyzed and the best quality records were included in the test (see Appendix B, table 35) were analyzed. The software Raven Pro 1.4 (The Cornell Lab of Ornithology, 2003; Charif et al., 2010) was used to analyze the sounds. We followed Vielliard (1990) for the analyses.
3.2.4. OTU's definition and diagnosable traits
The criterion adopted to identify and delimit taxa in the Lepidocolaptes angustirostris complex was the diagnosability of populations. A diagnostic character is a trait whose states occur at different frequencies between two supposed species. These characters indicate genetic differentiation accumulated over a period of reduced or absent genic flow, permitting the separation of evolutionary lineages (Helbig et al., 2002). In this way, the individuals examined were grouped using morphological similarity and the identification was applied after the analyses. This discrete character(s) were used to identify and delimit ‘the smallest cluster of individuals organisms’ (populations) that are diagnosably distinct from other such clusters (sensu Cracraft 1983, 1989) in Lepidocolaptes angustirostris (see an example within Lepidocolaptes in Silva & Straube, 1996). Previous classifications were not considered. Also, some characters proposed as diagnostic in others studies were not taken in consideration. The main reason not to use some criteria of classification and diagnosis is its ambiguity to identify the diagnosable groups in L. angustirostris complex. Namely, after the analysis in this work, these characters were considered as not informative. In the examination and analysis of specimens of visited museums, the identification and information taxonomic of labels were not considered.
3.2.5. Statistical Analysis
Prior to statistical analysis, the immature individuals and those without geographical coordinates were discarded. The analyses were elaborated using the R statistical package version 3.0.2 (R Core Team, 2013). First, an Anderson Darling and Levene tests were developed to determine if the data were normally distributed and had equality of variances,
13 respectively. As the data showed no evidence of normality or equality of variances (see Results), non-parametric tests were performed to estimate if there are significant differences among groups eventually found. So, Kruskall Wallis and Mann-Whitney tests were used to estimate between all groups and within them, respectively. Mann-Whitney test was performed using the “Wilcoxon rank sum test” from R software (R Core Team, 2013). Posteriorly, a Principal Component Analysis (PCA) was performed to summarize the total variation of characters (eight) to the two main ‘groups’ which showed the variation among plumage types identified (FactoMineR package from the R software). In this way, these two principal components can be plotted showing the variation most readily (Husson et al., 2014). In all mentioned statistical analyses, a significance level use was of 5% (Zar, 2010). Prior to PCA analysis, a transformation of the initial data was performed in order to eliminate the effect of shape and size in the eight measurements gathered; the ‘size’ vector was included in the database (Mosimann, 1970).
3.3. Clinal analysis
In a preliminar visual analysis of plumage patterns of L. angustirostris complex was possible to identify the presence of some individuals with intermediate stages in the dorsal and ventral patterns, and similarly, a geographical variation in some bill characteristics (see PCA results). So, an alternative hypothesis of clinal variation of phenotypic traits in L. angustirostris complex was proposed. In this alternative hypothesis, the presence of a morphological cline(s) could explain the geographical variation in the populations of the Narrow-billed Woodcreeper. In order of test that hypothesis, a clinal analysis was performed using a methodological approach proposed and developed by Szymura & Barton (1991), among others (Barton & Gale, 1993; Brumfield et al., 2001; Gay et al., 2008), and summarized and implemented in the R package ‘hzar’ (Derryberry, 2013). The R script used was modified from the published by Derryberry et al. (2013) in its ‘Supporting Information’ (Data S2-script for morphological characters). The ‘hzar’ package allows identifying and analyzing hybrid zones and their characteristics fitting clines of molecular and phenotypic data simultaneously. Among its features, can estimate the geographical extension of hybrid/clinal zones, to test concordance and coincidence in clines of molecular markers and phenotypic traits, and to
14 compare the observed cline widths with expectations of a neutral diffusion model. A useful implementation is the posibility to modify the parameter values of the cline to analyze, such as the values of center or width of the fitted clines. One requirement of ‘hzar’ package to analyze morphological data is that they could be “reasonably approximated by normal distributions” (Derryberry et al., 2013). The log-normalize data were included in the clinal analyses. For each character, three/four (depending of character analyzed) runs with different parameter values were realized (Table 1), modifying the range of clinal center and the total study area (hzar.model.addBoxReq and hzar.model.addCenterRange commands). In hzar, five different types of models can be described for quantitative traits, and they can vary by fitting exponential tails (none fitted; left only; right only; mirror tails; both tails estimated separately). Here, three main models were used; a model with none tail fitted and the values of the initial point A fixed (mean and variance, model I), a second one with none tail fitted and free parameters (Model II), and a third model estimating both tails and with free parameters (Model III).
Exposed Total Wing Tarsus Bill length Bill height Bill width Tail lengtha Pc1 Pc2 culmen culmen lengtha length 3800 Km** 3800 Km** 3800 Km** 3800 Km** 3800 Km** 3800 Km** 3800 Km** 3800 Km** 3800 Km** 3800 Km**
3500 - 3000 - 3000 - 3000 - 2000 - 3000 - 3500 - 3500 - 3000 - 3900* 3000 - 3900* 3900* 3900* 3900* 3900* 3500* 3900* 3900* 3900* 3000 - 3000 - 3000 - 3500 - 2000 - 2500 - 3000 - 3000 - 3500 - 3900* 2500 - 3900* 3800* 3500* 3500* 3900* 3900* 3900* 3800* 3800* 3000 - 3000 - 3000 - 3000 - Free Free Free Free Free 2000 - 3500* 3500* 3500* 3500* 3500* NA NA NA NA NA NA NA 2000 - 3000* NA NA
Table 1. Parameter value used in the clinal anaylses. (*) Clinal area analyzed. (**) Range of the clinal center. (a) Not normal characters. (***) Runs with free parameters.
The clines with the lowest Akaike Information criterion (AIC) score estimated were chosen. This AIC for each clinal model is estimated with the observed data versus its null model (frequency independent of location). Other information recovered from the chosen models was the values of cline width and cline center. A graphic showing the shape of modeled clines for the data of L. angustirostris was elaborated. Similarly, the coincidence and concordance between the cline widths for each character were analyzed.
15
3.4. GLM Analyzes
Lepidocolaptes angustirostris is a widespread species, and each of their populations is subject to different biotic and abiotic selective forces. In this way, these factors may affect the phenotypic characters in the taxon. With the aim of identify possible environmental factors that explain the geographical variation in the Narrow-billed Woodcreeper populations, a series of Generalized Linear Models analyzes (GLM) were elaborated using the phenotypic data collected. Mainly, four ‘phenotypic traits’ were analyzed; the principal components 1 and 2 (PC1 and PC2) from PCA analysis, the size estimate (the log-normalize data using the approach proposed by Mosimann 1970), and the ventral pattern codified into two states: Non- streaked and Streaked (the intermediate pattern was codified as Streaked). The environmental variables were collected from the online database BIOCLIM with 2.5 arc-minutes resolution (Hijmans et al., 2005). Initially, all variables from BIOCLIM (the 19 climatic measurements) were included in the analyses (Appendix B, Table 28). A GLM analyses were developed a methodological approach proposed by Calcagno & de Mazancourt (2010) and implemented in the R ‘glmulti’ package Calcagno (2014). In ‘glmulti’ package; “from a list of explanatory variables, builds all possible unique models involving these variables and, optionally, their pairwise interactions”. Here, the explanatory variables were the BIOCLIM data, and the response variables the morphological data gathered. In this way, these analyses were conducted in two phases; first, a preliminary runs with the whole dataset from BIOCLIM database (19 variables) were realized to identify the most related variables to the four phenotypic traits. These runs were developed without interations among covariates (quantitative variables) and plotted. One of the problems associated with the use of correlated variables is the presence of multicollinearity and superparametrization. To prevent these statistical phenomena, a Pearson’s correlation test was developed to examine the correlation among climatic variables. The least correlated variables were: Isothermality, Temperature Seasonality, minimum Temperature of Coldest Month, Temperature Annual Range, Annual Precipitation, and Precipitation of Coldest Quarter (Appendix B, Tables 29 and 30). Posteriorly, these variables
16 were used to conduct a second analysis with and without interactions.
3.5. Distributional patterns
Geo-referenced records of the individuals analyzed (with available geographical information) were despicted on scaled maps with the aim to define the congruence among the plumage patterns and geographical distribution of the OTUs and to identify possible hybrids zones throughout the region inhabited by L. angustirostris.
17 4. Results
4.1. Plumage description in Lepidocolaptes angustirostris
The analysis of the plumage of the Narrow-billed Woodcreeper shows two main plumage traits, a dorsal and ventral pattern. With the aim of to define the diagnostic value for these traits, a complete description and a geographical comparison among distributions of each pattern was elaborated.
4.1.1. Dorsal pattern
The dorsal plumage pattern coloration was classified into three main states: Strong brown (with some specimens showing a variation among brown and strong brown rufous), an Intermediate state (strong brown-light olive brown), and a Light olive brown.
Strong brown pattern: The strong brown coloration (HUE 7.5YR, among 4/6 and 5/8) was identified in populations inhabiting from northern Brazil (including Amapá and Pará) to central Humid and Dry Chaco (northern Argentina at Corrientes, Chaco, Formosa, and Salta provinces), also in the eastern zones of Pantanal and Chiquitano forest (Fig. 2 and Fig. 3).
18
Figure 2. Individual with a Strong brown pattern (MZUSP 63445, Fazenda Campos bons 38 km N. floresta, Pernambuco, Brazil).
Figure 3. Distribution of Strong brown pattern
19
A brown coloration (HUE 7.5YR 4/4) was found in five skins from Piauí (MPEG 71427), Bahia (MZUSP 86264, possibly an immature individual), Mato Grosso (MPEG 38906 and 38907), and Mato Grosso do Sul (MZUSP 73637). Similarly, a brown-strong brown coloration (HUE 7.5YR 4/4 - 4/6) was present in some individuals collected in Goiás (MPEG 14937, 16318, 19278, 19514, 19564, 19698, 19699, 19700, 21972, 44532). Other uncommon dorsal coloration was identified in individuals from Pará (MPEG 25843, an immature specimen), Alto Paraguay (Paraguay; MACN 2055a) and Salta (Argentina; MACN 30516, 30517, 30702) with a very rufous strong-brown coloration (a tonality more intense than HUE 7.5YR 5/8).
Intermediate pattern: The intermediate state, a strong brown - light olive brown pattern (HUE 7.5YR 4/6 and HUE 2.5Y 5/4) was identified in specimens from south-eastern Paraguay (Itapú a and Ñeembucu), northern Argentina (provinces of Misiones, Formosa, Entre Ríos, Salta, Jujuy, Corrientes, north-eastern of Buenos Aires, Santa Fe, and Santiago de Estero), Uruguay (Río Negro), and in adjacent zones along the Paraná River at São Paulo and Paraná states at Brazil (this distribution extends to zones of central to southern Humid and Dry Chaco, as well in the Southern Cone Mesopotamian savanna, Espinal, and Humid Pampas ecoregions) (Fig. 4 and Fig. 5).
20
Figure 4. Individual with a Intermediate pattern (MACN 217A, Gualeguaychu, Entre Rios, Argentina)
Figure 5. Distribution of Intermediate pattern.
21 This dorsal pattern consists in a mosaic of brown and olive colour patches, in an approximate ratio 1:1. This ratio shows variation among the individuals analyzed, it is possible to find skins with a coloration more ‘olivaceous’ that brown, or the opposite. A further analysis of the intra-variation in this pattern showed that as advances towards the south; the extension of ‘olive’ patches increases, and if it moves northward of the distribution, the brown patches are more extensive.
Light Olive-brown pattern: The most southern dorsal pattern is characterized by a olive coloration (‘light brownish olive’, HUE 2.5Y 5/4). This pattern was found in the individuals inhabiting the northern region of Argentina (Corrientes, Córdoba, Santiago de Estero, Tucumán, Catamarca, La Rioja, San Luis, Mendoza, and La Pampa provinces), and Uruguay (Río Negro province). This pattern spreads from central Humid and Dry Chaco to north of Low Monte-Espinal ecoregions, and the Uruguayan savanna (Fig. 6 and Fig. 7).
22
Figure 6. Individual with an Olive-brown pattern (MACN 66339, Campus UNLP, Santa Rosa, La Pampa, Argentina)
Figure 7. Distribution of Olive-brown pattern.
23 Within this pattern, a little variation was found; in the southern extreme of its distribution, a ‘brownish olive’ color (HUE 2.5Y 5/6) was showed by individuals from La Pampa (MACN 65819, 66340, 66318, 66339, 65822), and San Luis (MACN 64690). In the same way, a mixed state (HUE 2.5Y 5/4 - 5/6) was identified in three skins from Buenos Aires region (MZUSP 9, 18, 3878).
Distribution of the dorsal patterns: The distributions of the three main patterns of dorsal plumage allow identifying an intergradation region. This region was placed between the south-eastern extreme of Paraguay to northern Argentina, and west of Uruguay (central zone of Dry and Humid Chacoan ecoregions). Here, populations with the three dorsal patterns were sampled. Moving further to south, it is possible to find the intermediate and olive patterns cohabiting the south of the Gran Chaco and the adjacent regions of Paraná river basin (the Espinal and the Humid Pampas ecoregions).
Figure 8. Overlapped distribution of the dorsal patterns
Summarizing, the ‘strong brown’ pattern (predominant in the Caatinga-Cerrado ecoregions) was found from the northern Brazil to the northern border of Argentina (in Formosa-Chaco provinces), cohabiting with populations with the intermediate and the ‘olive’ patterns that inhabits to the south (Fig. 8). Further south, the ‘olive’ pattern becomes predominant in the populations.
24
4.1.2. Ventral Patterns
In the Lepidocolaptes angustirostris complex the ventral plumage pattern is highly variable. Six plumage patterns were identified: cinnamon-ochraceous, pale yellow, white to greyish- white, greyish-white weakly streaked, rufous streaked, and dark brown streaked. Also, intermediate states among all six patterns were found, and it was not possible to identify geographic boundaries defined among them.
Cinnamon-ochraceous and pale yellow patterns: In the north of Brazil, two plumage patterns were identified. One coloration cinnamon-ochraceous very intense in individuals from the most north-eastern zone, from Ceará, extending to Alagoas, Paraiba, and Pernambuco (Fig. 9).
Figure 9. Individual with cinnamon-ochraceous pattern (MZUSP 63445, Fazenda Campos bons 38 km N. floresta, Pernambuco, Brazil).
25 The second one, a pale yellow coloration (HUE 2.5Y between 8/3 - 8/4, or some cases 7/4) characteristic of individuals inhabiting the Amazonian regions of eastern Amapá (Macapá to north) and Pará (MPEG 25843, Rio Fresco, Rio Xingu; MPEG 54319, Missão Tiriós; and Rio Tapajós), and the Brazilian north-eastern region, in Maranhão, Piauí, western Paraíba, and Bahia (Fig. 10). This pale yellow coloration extends to the south to Cerrado regions, from western Bahia to central Goiás and to south-east of Mato Grosso (in zones with Cerrado vegetation).
Figure 10. Individual with pale yellow pattern (MZUSP 77726, Parque Nacional da Serra das Confusões, Piauí, Brazil).
26
Figure 11. Distribution of cinnamon-ochraceous and pale yellow patterns
Greyish-white pattern: A third ventral pattern was found in individuals in the Cerrado ecoregion. A white to greyish-white coloration, frequently called “dirty white” coloration in the literature. This ventral plumage is very restricted to zones with Cerrado vegetation (HUE 2.5Y, 8/1 - 7/1). The pattern extends from Maranhão to Tocantins, western Bahia, Goiás (including Brasilia D.F.), east to south-west of Mato Grosso southward to Mato Grosso do Sul. Also, some individuals with this pattern were found from western to central Minas Gerais and São Paulo (Fig. 12 and Fig. 13). Four individuals with this pattern were identified out of proposed range; three records from Tapajós river localities (MPEG 19701; MZUSP 14674 and 14675) present a dirty white coloration. In this zone, the dirty white and the pale yellow patterns was found. Also, other individual was identified in the south-east of Bahia (not in Cerrado vegetation) and shows that pattern (MZUSP 86264), but was identified as an immature specimen.
27
Figure 12. Individual with Greyish-white pattern pattern (MZUSP 29879, Rio Arica, Mato Grosso, Brazil)
Figure 13. Distribution of Greyish-white pattern.
28 Intermediate ventral pattern: In the southern zone of Cerrado ecoregion, a fourth ventral pattern was identified. An intermediate ventral plumage between the unstreaked (northern groups) and the streaked (southern groups) patterns. This pattern has a greyish-white coloration weakly streaked, which can be differentiated from the southern populations by the intensity of the color of the streaks, producing a less contrasting ventral pattern than the southern populations (Fig. 14). Likewise, this pattern is different to the unstreaked groups to the north (Central Cerrado-Caatinga).
Figure 14. Individual with Intermediate ventral pattern (MZUSP 64173, Retiro da Telha, margem direita Rio Sucuríu, Mato Grosso, Brazil).
The greyish-white weakly streaked pattern extends from south Cerrado (Central Goiás-south Mato Grosso) through Mato Grosso do Sul and southward the Paraguayan region throughout the Río Paraguay to northern Argentina (Corrientes, Chaco, Formosa, and Entre Ríos provinces; along the Paraná river). Likewise, individuals with this pattern were identified
29 in the samples from Yabaré (MACN 72555, 72572, 72590) and Comarapa, Santa Cruz, Bolivia (MACN 37563, see Fig. 15).
Figure 15. Distribution of Intermediate ventral pattern pattern.
Some individuals more to north were found with a similar pattern (MZUSP 80903, Ponto Nacional, Tocantins; MZUSP 72378, Trindade, Goiás). However, were identified as inmature individuals. The weakly ventral streaked is a trait that has immature individuals analyzed in this work (see Luz et al. 2007).
Streaked patterns: In the extreme south of distribution of Lepidocolaptes angustirostris complex one streaked ventral pattern was identified. This pattern is composed by dirty white feathers and dark brown streaks (HUE 7.5 3/2 or 3/3, but is possible to find individuals 4/3), more defined than the greyish-white weakly streaked pattern (Fig. 16a). Similarly, a distinctive nested ventral pattern was identified; a rufescent coloration more intense than the dark brown pattern, recognized by a bright rufous tonality in the white feathers (Fig. 16b).
30
Figure 16a. Individual with dark brown streaked pattern (MZUSP 31795, Las cañitas, Tucumán, Argentina)
Figure 16b. Individual with rufous streaked pattern (MACN 30516-30517, Alto Rio Santa Maria, Orán, Salta, Argentina)
31
The defined streaked pattern(s) were found in individuals from south-east of Paraguay, between the Paraguay and Paraná rivers to northern Argentina (south to La Pampa and Mendoza provinces) and west of Uruguay (Rio Negro), from the Gran Chaco ecoregions to the south. The rufous pattern was restricted to SE Paraguay to extreme north of Argentina (Corrientes, Chaco, Formosa, and Salta). The dark brown spreads from SE Paraguay to regions of La Pampa and Mendoza provinces (Fig. 17).
Figure 17. Distribution of streaked patterns.
Distribution of the ventral patterns: Despite a geographical distribution highly mixed and overlapped of the patterns of ventral plumage in Lepidocolaptes angustirostris complex, it is possible to identify some geographical structure in this taxon (Fig. 18).
32
Figure 18. Distribution of ventral patterns in L. angustirostris.
First, the unstreaked populations intergrade from the northeastern Brazil (Caatinga) to the southern Cerrado ecoregions; from cinnamon-ochraceous to dirty greyish-white colorations (Fig. 19 and Fig. 20).
Figure 19. Overlapped distribution of cinnamon-ochraceous and pale yellow patterns.
33
Figure 20. Overlapped distribution of pale yellow and dirty greyish-white patterns.
In the south of the Cerrado, the southernmost unstreaked populations coexist with the ‘intermediate’ group (Fig. 21).
Figure 21. Overlapped distribution of dirty greyish-white and the ‘intermediate’ patterns.
34 The ‘intermediate’ pattern is the dominant plumage from the southern Cerrado to SE Paraguay (plus the east region of Bolivia, in Santa Cruz). The zone between SE Paraguay and the north of Argentina seems a great intergradation area, where the ‘intermediate’ and the streaked pattern are cohabiting. Individuals presenting these two patterns were collected from this area. Now, southward the ‘intermediate’ pattern is replaced by the streaked ones, first by the rufous pattern, and finally, in the southernmost zone of the distribution, only the dark brown pattern was found (Fig. 22).
Figure 22. Contact zone of the intermediate/streaked patterns.
4.2. Morphometry
Despite the high level of intergradation in the plumage of L. angustirostris, the results of statistical analyses were able to find some differences among the populations analyzed. These analyses identified these groups as non-normally distributed and with the equality of variances not reached for four of eight measurements (bill length, exposed culmen, total culmen, and tail length). Therefore, a non-parametric statistics was run. The general Kruskall-Wallis test showed differences among all groups (p < 0.001, see Table 11 in Appendix B) for eight characters analyzed. In the Mann-Whitney tests, the comparisons within pairs of named populations showed that the most differentiated characters
35 were the length, height, and width of the bill, and tarsus-metatarsus length. The least variable measure was the wing length (see Appendix A). The comparisons (pairs of groups) with the lowest level of differentiation (based on the number of characters analyzed) were the groups one and two (cinnamon-ochraceous and pale yellow patterns) and five and six (rufous streaked and dark brown streaked) with two characters showing low differentiation (see Table 20). The pairs of groups that shown the higher differentiation were the plumage types two and six (pale yellow-dark brown pattern) with eight characters present significant differences. In general, the northern (1-3) v.s. the southern groups (4 and 6) showed higher significance levels of differentiation than groups occurring nearest one another. Despite this, the estimated differences (p values of 0.01 and 0.001 in some comparisons) not confirm a real morphometrical ‘divergence’ that could support the hypothesis of two or more valid taxa within the material examinated. The principal components analysis (PCA) identified two variates that explain the 70.88% of the variation in eight quantitative traits. The first component was interpreted as representing three variables (bill length, exposed and total culmen) in equal proportions (Fig. 23a), while the second variate represents primarily the bill width and the tarsus-metatarsus length (Fig. 23b).
(a) Characters in the PC1 variate (b) Characters in the PC2 variate
Figure 23. Principal components in L. angustirostris.
36 The Fig. 24a and Fig. 24b shows a plot of the six “plumage types” proposed over the two principal components. Despite the groups present a significant morphological variation, the distribution of their individuals overlapping along the two principal components.
(a) Individuals plotted on the principal (b) OTUs identified on the PCA components components
Figure 24. Principal components - sclatter plot.
From these results, it is possible to propose the existence of morphological divergence between the No-Streaked and the Streaked groups, as well as a close relationship between the Pale yelow and the ‘White to greyish-white’ patterns from Caatinga-Cerrado ecoregions (Fig. 25).
Figure 25. Division between No-streaked and Streaked populations (PCA analysis), confidence level: 0.95.
37
PCA results appear inconsistent with the geographical and plumage evidence; morphological variation among “plumage types” exists, but it is not high enough to conclude the presence of several taxonomic units in the L. angustirostris complex.
4.3. Vocalizations in the Narrow-billed Woodcreeper
In a preliminary analysis, four main types of songs were identified in the L. angustirostris complex, with some level of intergradation. In the same way, intra-variation within these songs was found, and a definited pattern could not be established. First, songs in the northernmost populations (Alagoas and Bahia, in the Caatinga ecoregion) were identified as an only type of song. Three records from the ‘Caatinga da Serra Alta’ and Pão de Açúcar (Alagoas), and Curaçá (Bahia) shown a song with more than 20 notes that descend and accelerate gradually. Also, one record from Brasilia (WA222451a), with 46 notes was congruent with these type of song (see Fig. 26). The number of notes is this type of vocalization varies.
Figure 26. Sonogram of song Type I in L. angustirostris (Curaça, Bahia, Brazil).
A second type of loudsong was identified from central Brazil to northern Argentina (including a record from the Department of Beni, Bolivia). The song varies from eight to 15 descending notes (approximately 3 second long), with the first note being slightly isolated note from the others, marking the beginning of the song. Mostly, the notes have a stable frequency, without variations. Within this group, it was not possible to find some geographical pattern, the duration of the loudsongs can vary indistinctly in the north or south of geographival range of this vocalization, e.g., it is possible find songs with different number
38 of notes in a same locality, and, in the same way, similar songs were identified in different localities (see Figures 27a to 27e). In the same way, this vocalization could be intergrade with the type I (in the regions of Bahia, Brazil) and the third type (El Cutal, B eni, Bolivia).
Figure 27a. Sonogram of song Type II in L. angustirostris (Sento Sé, Bahia, Brazil).
Figure 27b. Sonogram of song Type II in L. angustirostris (Faz. SantaTeresa, Mato Grosso, Brazil).
Figure 27c. Sonogram of song Type II in L. angustirostris (El Cutal, Beni, Bolivia).
39
Figure 27d. Sonogram of song Type II in L. angustirostris (Reserva Natural del Bosque Mbaracayu, Canindey, Paraguay).
Figure 27e. Sonogram of song Type II in L. angustirostris (2.0 km E of Ocloyas, Jujuy, Argentina).
A third type of song was identified in populations from south-western Brazil and eastern Bolivia. The loudsong was composed by nine to 19 descending notes approximately, which increase their speed as the sound continues. The structure of song was similar to the second type (II), but each of their notes has a considerable variation in its frequency (see Figures 28a to 28c). In a similar way to second type, variations among the songs can be identified.
Figure 28a. Sonogram of song Type III in L. angustirostris (Corumbá, Mato Grosso do Sul, Brazil).
40
Figure 28b. Sonogram of song Type III in L. angustirostris (W of Santa Rosa de la Roca, Santacruz, Bolivia).
Figure 28c. Sonogram of song Type III in L. angustirostris (El Cutal, Beni, Bolivia).
In the southern region of the distribution of L. angustirostris, a fourth type of song was found (see map). The basic structure is similar to type III, one or two high first notes slightly isolated from the rest, and more that 10 descending notes increasingly fast (see Figures 29a to 29c). However, the variations in the frequency of notes were higher than the type III. In the same way, the speed of song is greater. The variation within this vocal pattern was considerable. The fourth type covers the samples from Uruguay (San Javier) and northern Argentina (Salta, Jujuy).
Figure 29a. Sonogram of song Type IV in L. angustirostris (2.0 km E of Ocloyas, Jujuy, Argentina).
41
Figure 29b. Sonogram of song Type IV in L. angustirostris (Acambuco-Tartagal, Salta, Argentina).
Figure 29c. Sonogram of song Type IV in L. angustirostris (El Relincho, Ecilda Paulier, San Jose, Uruguay).
The vocalizations in L. agustirostris have no defined pattern. Although its structure is similar (with one ot two first high notes slightly isolated and the rest descending and faster notes), the number of notes highly variable, the presence of possible “hybrid” songs (Figure 28a), and the poor geographical delimitation does not allow the identification of any diagnosable character that helps to clarify the taxonomic status of their populations. As additional information, in a field test using playback, individuals collected from the Fazenda Fartura (Pará, Brazil) responded to a recorded song of northern Argentina (Jujuy record), while not responded to songs previously recorded in the same area (cross playback, individuals: MZUSP 97173, 97207, and 97208). Also, it could be inferred that the differences in the vocalizations of the Narrow-billed Woodcreeper would not be a selective force for choosing a mate (this affirmation based in the Biological Species Concept, see Mayr, 1963).
42 4.4. Clines
In the analyzes with hzar package the eight morphological characters were associated to different clinal models, i.e., not all theses characters built a common cline or with the same properties. Three characters of the bill (components in the PC1, from the PCA analyzes) shown a common clinal model, with the following properties: The bill length showed a cline with a center placed between 3.357 to 3.531 km from the initial point A, and a width that varies from 37,3 to 486,3 km (see Table 20 and Fig. 30a). In the exposed culmen cline, the center was ranged between 3.363,6 to 3.533,4 km from point A, and the width of clinal zones varies between 4,54 to 172,2 km (Table 21). Finally, the cline fitted using the total culmen measurements has a clinal center ranged between 3.386 to 3.414 km, and a width from 122 to 232,5 km (Table 22). According to these clinal models, a morphological clinal zone is present in the southern region of distribution of L. angustirostris; among the Paraná Flooded Savanna, Humid Chaco, the Espinal, and Humid Pampas ecoregions (see Fig. 30b).
Figure 30a. Clinal models fitting the bill length, exposed and total culmen. Trait value: Mean of the character by point, Distance: Distances from the first point (first sampled locality) to the last point sampled.
43
Figure 30b. Clinal region for bill length, exposed and total culmen.
Other clines were recovered using the remaining characters; for the wing length, three possible clinal zones were recovered, one with a center to 1.816,8 km from point A, and a width 180 km. The second one, with a center of 2.014,5 km from point A and a width of 14,2 km was also recorded. The third was localized to 2.120,5 km from point A and has a width of 9,9 km (searching clines with a range of center between 2.000 and 3.500 km) (see Table 23 and Fig. 31a). These three clines spread at the boundaries of Cerrado with the northernmost patches of the Alto Paraná Atlantic Forests ecoregion (approximately at the 49º to 50º S), and are congruent with the limits distribution between no-streaked and the intermediate/streaked forms (see Fig. 31b). A cline fitted with bill width data was congruent with the wing length models (center: 1.816,8 km), spreading on the southern Cerrado (Table 24).
44
Figure 31a. Clinal model fitting the wing length and bill width. Trait value: Mean of the character by point, Distance: Distances from the first point (first sampled locality) to the last point sampled.
Figure 31b. Clinal region for wing length and bill width.
Using the tail length, two congruent clinal zones were recovered; with centers to 2.832 and 2,828 km, and with width of 9,8 and 12,2 km, respectively (see Table 25 and Fig. 32a).
45 This clinal zones spread the Cerrado, Pantanal, Humid and Dry Chaco, and the Alto Paraná Atlantic Forests ecoregions along of their geographical boundaries (Fig. 32b). These clines could to support a possible division among the no-streaked/Intermediate and streaked populations in the Narrow-billed Woodcreeper.
Figure 32a. Clinal model fitting the tail length. Trait value: Mean of the character by point, Distance: Distances from the first point (first sampled locality) to the last point sampled.
Figure 32b. Clinal region for tail length.
46 The bill height data shows a cline with a center to 1.180 Km from point A, and a extension of 933 km. This zone is placed among Caatinga, Atlantic Dry Forest, and Cerrado boundaries (see Table 26 and Fig. 33a). This cline covers the contact zone between the Pale Yellow and white to greyish-white ventral patterns (Fig. 33b).
Figure 33a. Clinal model fitting the bill height. Trait value: Mean of the character by point, Distance: Distances from the first point (first sampled locality) to the last point sampled.
Figure 33b. Clinal region for bill height.
47 Another cline was identified using a tarsus-metatarsus data, with a center of 2.946,9 km from point A, and a width of 17 km. This zone of variation covers the southern Cerrado, Pantanal, Humid and Dry Chaco, and the Alto Paraná Atlantic Forests (Table 27 and Fig. 34a and 34b).
Figure 34a. Clinal model fitting the tarsus-metatarsus length. Trait value: Mean of the character by point, Distance: Distances from the first point (first sampled locality) to the last point sampled.
Figure 34b. Clinal region for tarsus-metatarsus length.
48 4.5. GLM analysis and environmental variables
The GLM analyses identified significant correlation between some climatic variables and the phenotypic traits in L. angustirostris. In the individual preliminary analyses, one temperature variable was the most explanatory; the Temperature Seasonality (BIOCLIM 4) was recovered in three traits analyzed; PC1, PC2, and ventral plumage: Presence/absence of streaks (see Fig. 35 to 38, and Tables in Appendix B). With the size estimative, the most correlated variable was the Precipitation of Warmest Quarter (BIOCLIM 18, AIC=-1175.1 and weight=1.0). To identify the model with the most explanatory climatic variable, the information of all models were computed (AICtab command, bbmle R package, Bolker 2014).
Figure 35. Correlation PC1 - Temperature seasonality.
49
Figure 36. Correlation PC2 - Temperature seasonality.
Figure 37. Correlation Size - Precipitation of Warmest Quarter.
50
Figure 38. Correlation Ventral plumage - Temperature seasonality.
For PC1 data and the least correlated climatic variables, two models were found (Fig. 39); (a) One with an interaction between the annual precipitation and the minimum temperature of coldest month (BIOCLIM 12:BIOCLIM 6). The components from PC1 exhibited a positive relationship with these two variables, at higher latitude and lower annual precipitation (plus lower minimum temperature in the coldest month), beak size appear to increase (relative weight > 0.8). A second model (b) shows an interaction between BIOCLIM 12 and the temperature seasonality (BIOCLIM 12:BIOCLIM 4), here, the decrease of annual precipitation in addition to increased temperature seasonality as latitude increases, appears to have a effect the size of the bill.
51
Figure 39. Main models explaining the PC1 variation. Red line: relative importance of model terms 80% (support of each variable across all models).
For PC2, in addition to the previous models (BIOCLIM 12:BIOCLIM 6 and BIOCLIM 12:BIOCLIM 4), other four models were found (relative weight > 0.8). One model (c) gathering the BIOCLIM 19 and BIOCLIM 4, where at a higher precipitation of coldest quarter plus lower temperature seasonality, the size of the tarsus increases and the bill width decreases. (d) A fourth model, the PC2 was correlated to BIOCLIM 12 and BIOCLIM 7. The increase of the temperature annual range and the decrease of annual precipitation while increase the latitude, appear to affect the tarsus-metatarsus length. Other two models including the BIOCLIM 3 (Isothermality) were identified (see Fig. 40).
52
Figure 40. Main climatic variables explaining the PC2 variation. Red line: relative importance of model terms 80% (support of each variable across all models).
For the size, the models BIOCLIM 12:BIOCLIM 6 and BIOCLIM 12:BIOCLIM 4 from PC1 and PC2 were found. In addition, one model with BIOCLIM 4 and BIOCLIM 6 (temperature seasonality and minimum temperature of coldest month) was identified (see Fig. 41). In this analysis, the correlation among climatic variables and size was not well defined. Here, the variation of the size in the Narrow-billed Woodcreeper along its distribution appears to have a pattern with two opposing tendencies. First, from the northeast Brazil to the southern Cerrado (from 5º S to 20º S, approximately) the size decreases. However, from southern Cerrado, the size increases to the southernmost region of the distribution (see Fig. 42). In this case, no climatic variable in the models identified could fully explain the variation in size in L. angustirostris. However, in the preliminary test, the size shows a high correlation with the Precipitation of Warmest Quarter (BIOCLIM 18).
53
Figure 41. Main climatic variables explaining the size variation. Red line: relative importance of model terms 80% (support of each variable across all models).
Figure 42. Correlation of size variation and Latitude.
54
For the ventral plumage variation, no models with interactions were identified. The six variables used were correlated individually (see Fig. 43). The most explanatory was the temperature seasonality (BIOCLIM 4), in agreement with the preliminary test for this trait.
Figure 43. Main climatic variables explaining ventral patterns (no-streaked/streaked). Red line: relative importance of model terms 80% (support of each variable across all models).
4.6. How many taxa are there within Lepidocolaptes angustirostris?
Previously to this taxonomic review of L. angustirostris complex six taxa were accepted.; the main trait used to delimit these taxa was the ventral plumage pattern (see plumage subsection) while others characters were not definitive, and the morphological data (measurements of eight characters analized) were inconclusive. Our results, however, found a no significant divergence among the taxa (see PCA results). In the same way, the remaining plumage characters (dorsal and undertail-coverts coloration, patterns of the crown and superciliaries, and others traits used in the literature) were not useful to unambiguolsy detect any diagnosable units. Despite the first suggestion and naming of more than one taxa in the complex, this
55 hypothesis cannot be corroborated. The populations found along geographical distribution of L. angustirostris were assigned to different valid taxa due to the high plumage variation and the presence of a relative morphological variation among the individuals/populations analyzed. However, our results demonstrated a vey high level of intergradation and the absence of defined geographic boundaries do not permit the recognition of more taxa than the nominate, suggesting a continuous, morphologically diverse population, with no evolutionary distinctiveness (i. e., not expressed in the phenotype). The figures 44a and 44b show the variation of plumage patterns and coloration observed in the regions inhabited by L. angustirostris (see also the Fig. 44c summarizing the latitudinal variation). The Figure 44a shows individuals from north-eastern Brazil (Caatinga) to central Brazil (Cerrado). It is clear the presence of a gradual variation in the coloration of patterns observed, from a cinnamon-ochraceous to a pale yellow pattern. In the same way, individuals with a intermediate stages were found.
Figure 44a. Individuals of L. angustirostris analized from Caatinga to central Cerrado (from the left to right), showing the no-streaked ventral plumage, and the gradual variation between the cinnamon- ochraceous and the pale yellow patterns.
The Figure 44b presents the variation identified in the populations from the central Cerrado to
56 central-southern Great Chaco ecoregions. Intermediate stages were found, and a considerable level of intergradation was identified, with no-streaked, intermediate, and streaked individuals cohabiting in some regions (northern Chacoan ecoregions, extreme southern Cerrado).
Figure 44b. Individuals of L. angustirostris analized from central Cerrado to central-southern Great Chaco (including Humid Pampas and adjacent regions), showing the intermediate and streaked ventral plumages (from the left to right), and the gradual variation between the no-streaked, the intermediate (slightly streaks), and the dark brown streaked pattern.
57 4.7. Taxonomy of the Narrow-bille Woodcreeper
Lepidocolaptes Reichenbach 1853
Lepidocolaptes angustirostris (Vieillot, 1818)
Trepador Del Comun, Azara, 1802, Apuntamientos para la Historia Natural de los Páxaros del Paragüay y del Rio de la Plata, Tomo II, p. 279. Type no existent.
Dendrocopus angustirostris Vieillot, 1818, Nouveau Dictionnaire D’historie Naturelle, Appliquée Aux Arts. XXVI, p. 116, locality: “Paraguay”. Based in Azara 1802.
Dendrocolaptes bivittatus, Lichtenstein, 1822, Abhandlungen der physikalischen (-mathematischen) Klasse der Koeniglich-Preussischen Akademie der Wissenschaften, (1820-1821), p. 258-266, pl. 2, fig. 2, locality: “in province São Paulo”. Spix, 1824, Avium species novae, quas Brasíliam, I, p. 87, locality: Piauí, Brazil. Lafresnaye & D’Orbigny, 1838, Magasin Zoologie, p. 8, locality: Corrientes.
Picolaptes coronatus, Lesson, 1830, Traite d’Ornithologie, Livr. 4, p. 314, locality: Piauí, Brazil.
Dendrocolaptes rufus, Wied, 1830, Beiträge zur Naturgeschichte von Brasilien, 3, p. 1130, locality: Between provinces Minas and Bahia, Brazil.
Picolates bivittatus, Lafresnaye, 1850, Revue et Magasin de Zoologie pure et Appliquée, 2, p. 152, locality: São Paulo. Allen, 1876, Bulletin of the Essex Institute, 8, p. 80, locality: Santarém, Brazil.
Picolaptes angustirostris, Lafresnaye, 1850, Revue et Magasin de Zoologie pure et Appliquée, 2, p. 151, locality: “Paraguay”. Sclater, 1890, Catalogue of Birds in the British Museum, 15, p. 155, locality: “Bolivia”. Salvadori, 1897, Bollettino dei Musei di Zoologia ed Anatomia Comparata della Reale Universitá di Torino, 12, N. 292, p. 21, locality: San Francisco, Caiza, province Tarija, Bolivia.
Lepidocolaptes atripes, Hudson, 1870, Proceedings of the Zoological Society of London, p. 113, locality: Concepción del Uruguay.
Picolaptes bivittatus bahiae, Hellmayr, 1903, Verhandlungen der kaiserlichkönigiglichen zoologisch- botanischen Gesellschaft in Wien, 53, p. 219, locality: Joazeiro, Bahia, Brazil.
58
Picolaptes angustirostris bivittatus, Hellmayr, 1908, Novitates Zoologicae, 15, p. 65, locality: “Goyaz”, Rio Araguaya, Rio Thesouras, Faz. Esperança (“Goyaz” = Goiás, Brazil).
Picolaptes angustirostris angustirostris, Dabbene, 1910, Anales del Museo Nacional de Buenos Aires, 18, p. 307, locality: Catamarca, Entre Ríos, Córdoba, Jujuy, Mendoza, Tucumán, Salta, Chaco; idem, l.c. 23, p. 318, 1912 – San Rafael, Uruguay.
Lepidocolaptes angustirostris certhiolus, Todd, 1913, Proceedings of the Biological Society of Washington, 26, p. 173, locality: Curiche, Rio Grande, Bolivia.
Lepidocolaptes angustirostris praedatus, Cherrie, 1916, Bulletin of the American Museum of Natural History, 35, p. 187, locality: Entre Ríos, Concepción del Uruguay (Probably Argentina/Uruguay limits).
Lepidocolaptes angustirostris, Serié & Smyth, 1923, El Hornero, 3, p. 49, locality: Santa Elena, Entre Ríos. Wetmore, 1926, US National Museum Bulletin, 133, p. 235.
Lepidocolaptes angustirostris hellmayri, Naumburg, 1925, Auk, 42, p. 421, locality: Chilón, Santa Cruz, Bolivia.
Lepidocolaptes angustirostris bahiae, Cory & Hellmayr, 1925, Catalogue of Birds of the Americas and The Adjacent Islands in Field Museum of Natural History, vol. IV. p. 339.
Lepidocolaptes angustirostris bivittatus, Wetmore, 1926, US National Museum Bolletin, 133, p. 235.
Lepidocolaptes angustirostris coronatus, Wetmore, 1926, US National Museum Bolletin, 133, p. 235.
Lepidocolaptes angustirostris griseiceps Mees, 1974, Zool. Mededelingen Rijksmus. Nat. Hist. Leiden, 48, p. 57, locality: Sipaliwini, Suriname.
Distribution: From extreme northeastern Brazil to southern-central regions at Argentina, including isolated populations at the Sipaliwini savanna and the Amazonian regions of east Amapá and Pará. Inhabits mainly in the open/dry lands of Caatinga, Cerrado, and El Gran Chaco ecoregions, and adjacent regions (Pantanal, Chiquitano Dry Forest, Espinal, Paraná
59 Flooded Savanna, Southern Cone Mesopotamian Savanna, Alto Paraná Atlantic Forests ecoregions). Diagnosis: Unlike other Lepidocolaptes from South America, the white superciliaries are broad, the bill is more pinkish than the other Lepidocolaptes, and the streaked ventral pattern less intense (but see the southern populations), head and neck blackish with numerous pale fulvous shaft-spots, darker than others species. Size is similar to other species of the genus. Description: A woodcreeper of medium size (19-22 cm). A long, slim and moderately decurved pale grey to pinkish horn bill; base of upper mandible wit dusky sides. Brown to Brown-olivaceous above; superciliaries broad and white; head and neck blackish with numerous pale fulvous shaft-spots; tail ferruginous; from unstreaked cinnamon-ochraceous to dark-brown streaked below, from the north to south of the distribution; legs and feets grey to dark grey. No sexual dimorphism in the plumage. Despite of high intergradation level and geographical variation, two main morphs can be found: an unstreaked group found from the northeastern to southern Brazil (southern boundary not defined), including isolated populations in the north Amazonas and in the savannas of Sipaliwini. This group does not show streaks in the ventral side and have a strong brown coloration in the dorsal surface. From north to south the ventral plumage varies from cinnamon-ochraceous to greyish-white. A second morph streaked can be found from the southern Brazil to north-central Argentina, including populations from the eastern Bolivia. It is characterized by a strong brown-light Olive brown to light Olive-brown dorsal patterns cohabiting in a very mixed region. Different variations of these dorsal plumages can be found. Regarding the ventral plumage, a slight streaked pattern, considered as an intermediate stage between unstreaked and streaked groups is present from the southern Brazil to northern Argentina. Intraspecific variation: The populations of L. angustirostris complex are highly polymorphic. The phenotypic variation has allowed the classification of this taxon into several subspecies by many authors. However, the undefined geographical boundaries and the intermediate stages of morphological and plumage characters do not support this subspecific division. The plumage patterns are the most variable traits in the species. The dorsal and ventral plumages in the northernmost and southernmost populations are extremely different, and the intermediate groups present gradual variations between these two extremes. Additionally, individuals with distinct patterns can be found in the same region along its geographic distribution.
60 The size of the individuals varies, but this morphological variation was not unidirectional. The largest populations can be found in the northern and southern regions (Caatinga and southern Chacoan ecoregions), while smaller individuals were identified between the southern Cerrado-Pantanal to the northern Chacoan ecoregions (see Fig. 14). The size decreases gradually from the northeastern to southern Brazil, where we found the smaller individuals.
Figure 44c. A graphical summary of variation of L. angustirostris, from the northern Brazil to Northern- central Argentina (from left to right).
61 5. Discussion
5.1. Delimitation of the species
The main objective of this work was to review the taxonomic status of Narrow-billed Woodcreeper, and establish if the variation in the plumage patterns and other traits are sufficient to recognize the colour-polymorphic populations as valid taxonomic units to a specific level. However, the analyses show no significant differences among any of the named populations. In terms of plumage, the geographic boundaries among ventral patterns were not defined, as well as in the analyses based in morphometric and geographic evidence. Intergradation and a possible latitudinal geographic variation were found. Statistical analyzes were also inconclusive; PCA tests found significant differences among groups studied, but is not congruent with the level of intergradation observed. Additionally, the vocalizations do not appear to be useful in clarifying the taxonomic status of this species. So, how to explain the high colour-polymorphism found in the populations of Lepidocolaptes angustirostris through South American open/dry lands? Is there any convenience in splitting contiguous colour-polymorphic populations from a unique recognized species to several valid taxonomic units? The delimitation of species and subspecies is a topic highly debated, and theoretical and methodological approaches have been proposed (Amadon, 1949; Zink, 2006; Alström et al., 2008; Cicero, 2010; Marantz & Patten, 2010; Tobias et al., 2010; Zapata & Jiménez, 2012; Camargo & Sites, 2013). However, there is still no consensus about concepts and methods applied to different taxa (Agapow et al., 2004; de Queiroz, 2007; Gill, 2014; Sangster, 2014). In this study, using mainly the diagnosability criteria (based in the species concept from Cracraft 1983, 1989); the taxonomic validity of subspecies of L. angustirostris proposed in the literature is rejected due to poor definition of geographical, morphological and plumage boundaries among them. The Narrow-billed Woodcreeper is composed by polymorphic populations intergrading from the northeast of Brazil to south of Chacoan ecoregions (Dry and Humid Chaco), through the open/dry lands of Caatinga, Cerrado, and the Gran Chaco. So, division of this taxon could not be applied. Cardoso et al. (2003) state that
62 species like as L. angustirostris inhabiting climatic gradients show morphological variation in a clinal trend. This variation could be difficult in taxonomy, as no clear morphological entities can be delineated. It is common for taxonomists to split the clines into distinct subspecies, but in this case this is purely arbitrary and artificial. Several authors have critiziced the concept and application of subspecies rank in taxonomic works (Zink 2004; Alström et al. 2008, among others). For Fitzpatrick (2010), subspecies, unlike species are human constructs. While Zink (2004) concluded that the use of subspecific rank in taxonomy is not useful and adds uncertainty to biological classifications. The absence of defined criteria in the delimitation of these biological groups is one of obstacles when are implemented. At the other hand, some works have shown the convenience of subspecific status in study of certain taxa (Patten & Unitt, 2002; Cicero, 2010; Patten, 2010). For example, Haig & Winker (2010) states that the study of subspecies address the geographic component of variation and differentiation, if the criteria used to define the subespecific groups each case were made explicit. A pausible hypothesis to explain the high phenotypic diversity in L. angustirostris is an existence of an incipient speciation in this taxon. In an incipient speciation, two or more populations from one species are dividing into two new ones, but are still capable of interbreeding. These ‘early stages’ of divergence among populations of the same species has been analyzed in some groups of birds (Dendroica coronata, Brelsford & Irwin 2009) and other taxa (the Arctic charr Salvelinus alpinus, Adams & Huntingford 2004). Indicators of incipient speciation can be the presence of low genetic divergence among populations and morphological polymorphism (Price, 2008). For instance, in an analyses testing adaptive radiation of the capuchino seedeaters (11 species from genus Sporophila), Campagna et al. (2011) found high phenotypic variation in vocalizations and coloration but extremely low levels of neutral genetic differentiation, proposing a ‘recent’ speciation (middle Pleistocene) occurring in the group. Some molecular evidence could support this hypothesis in the Narrow-billed Woodcreeper; in a phylogenetic analysis of genus Lepidocolaptes, Arbelaéz-Cortés et al. (2012) found low genetic differences between both COI and cyt b haplotypes for L. angustirostris samples from Brazil, Bolivia and Argentina. Here, 10 individuals from six localities were analyzed (COI haplotype). According to these authors, four subspecies (L. a. bahiae, L. a. hellmayri or L. a. certhiolus, and L. a. praedatus) could be sampled, and their
63 observed genetic variation was low, suggesting “a recent range expansion”. The partial results found by Arbelaéz-Cortés et al. (2012); the low genetic differentiation among populations analyzed and the high color polymorphism in the individuals sampled in this study could support the hypothesis of an early speciation occurring in the populations of the Narrow- billed Woodcreeper. One of the most debated points in taxonomy is the dichotomy “splitting vs lumping” of taxa with intraspecific variation and uncertain taxonomic position; the need to describe all the diversity present in biological groups faces the absence of strong and verifiable evidence about the limits of these divisions. In cases like as L. angustirostris, the situation is similar; the phenotypic variation exists, but evidence was not found that allow the delimitation of the populations identified as diagnosable units. Additionally, geographic barriers (frequently used in Ornithology to delimit subspecific lineages) in the distribution of Narrow-billed Woodcreeper are absent or seem not to affect the gene flow among the populations. For these reasons, contrary to the cited literature, the subspecific rank was dismissed and only one valid taxonomic unit is proposed here. Literature about L. angustirostris used the subspecific rank to describe the differences in the ventral/dorsal plumage (see Marantz et al., 2003; Ridgely & Tudor, 2009). Undertail coverts coloration, plumage pattern of crown, and tone of color in dorsal and ventral sides has been used to sort this taxon in at least eight subspecies recognized. Despite finding these variations, their distribution along the sampled individuals cannot identify clear patterns of differentiation among populations. A possible cause is the scarce comparative analysis of additional samples from intermediate regions of the geographical distribution of the taxon. Initial descriptions were elaborated based on very restricted samples, putting aside other samples from the same location or adjacent areas. In this study, more than one ventral plumage pattern was identified in the same localities (e.g. localities from the central Brazil (Goiás), and in the boundaries of southern Brazil and Paraguay), rejecting a possible delimitation among populations. In a recent study about morphological variation in Schistochlamys ruficapillus (Esteves-Lopes & Gonzaga, 2014), a similar conclusion was proposed; the recognition of the three subspecies in the Cinnamon Tanager were based individuals from distant populations (scarse sampling), and intermediate stages were not included in these descriptions.
64 5.2. Plumage patterns and polymorphism in L. angustirostris
The plumage patterns in L. angustirostris complex are highly diverse, showing three dorsal and six ventral patterns along of its distribution, covering the eight subspecies identified in previous works. Analyzing these plumage patterns were identified two subgroups proposed by Marantz et al. (2003): the “bivittatus” and “angustirostris” groups in the north and the south of the distribution, respectively. Likewise, intergradation and intermediate colorations were found among the populations sampled. Despite of high divergence between the populations from the northeast Brazil and the northern Argentina, defined boundaries among plumage patterns were not possible to identify. Given the existence of a high color polymorphism in the taxon, a review of the possible causes that influenced the rise of this plumage variation were elaborated. The color polymorphism is defined as the presence of two or more distinct, genetically determined color morphs within a single interbreeding population. This different color exemplifies extreme morphological diversity within populations (Huxley, 1955; Gray & McKinnon, 2007). Has been theorized that, in color-polymorphic species with large geographic ranges (similar to L. angustirostris), there is probability to occur parapatric speciation at the ends of a ratio cline in morph frequencies (Endler, 1977). The color polymorphism has been associated with differences in groups of correlated traits (behavior, life history, morphology, physiology etc.) due to correlational or epistatic selection or shared developmental pathways (Forsman et al., 2008). Other situations that could predispose color polymorphism occurs when populations come into secondary contact after diverging in coloration allopatrically or when color forms are under disruptive selection associated with different microhabitats (Endler, 1977; Roulin, 2004). Also, in some circumstances, the color polymorphism may represent incomplete speciation (Gray & McKinnon, 2007; Hugall & Stuart-Fox, 2012). Galeotti et al. (2003) developed a study about color-polymorphism in birds in order to analyze some biological mechanisms proposed to explain the maintenance of polymorphism. Here, the authors tested three forms of selection: apostatic, disruptive, and sexual selection, plus a no selection model. In addition to establishing that the polymorphism is a relatively rare phenomenon (only 3.5% of bird species show polymorphism), one of the conclusions proposed was that the color polymorphism in birds is not a nonadaptive consequence of
65 selection on other adaptive traits, but an trait evolved probably by disruptive selection. In this disruptive selection hypothesis, the patterns of variation in light conditions may be the most important selective mechanism maintaining color polymorphism in birds. Hugall & Stuart- Fox (2012) developed a study about speciation in color-polymorphic birds using genetic data from five families of non-passerine taxa. The authors concluded that the color polymorphism tends to be associated with diverse ecological conditions or relatively recent speciation, being this statement applied to the passerines taxa. For Roulin (2004), the presence of color morphs in a species have an adaptative value, namely, the different attributes of morphs could be correlated to environmental variations. This hypothesis predicts covariation with life-history, behavioral, morphological and physiological traits. Using only morphological data, some statements could be proposed about polymorphism in the Narrow-billed Woodcreeper. First, the color polymorphism in the taxonomic complex is not a suitable trait for split the taxon into several valid taxonomic units due to the high level of intergradation and lack of defined boundaries among populations. Second, environmental factors were correlated to the ventral plumage in the species. Based in the GLM analyses, temperature seasonality (BIOCLIM 4) seem to explain the ventral plumage variation using the two main states identified in the groups; No-streaked/Streaked (tests with and without interactions, see Results). Additionally, the Gloger’s rule (darker plumages are more expected in more humid environments, and plumage lighter plumages at dry regions) fit with the variation observed. Third, if the statements of Arbelaéz-Cortés et al. (2012) are considered and added to the findings of this work, the color polymorphism could be a result of a recent speciation of populations in the open/dry lands of Caatinga, Cerrado and Chaco ecoregions.
5.3. Clinal variation
In its simplest definition, a hybrid zones are areas where divergent lineages come into contact, mate and produce offspring of mixed ancestry. Natural hybrid zones represent a continuum of different levels of differentiation, as expected if speciation is a gradual process (Barton & Hewitt, 1985, 1989). These contact zones have different geographical ranges and forms, and diverse involved process. In the hybridization phenomena, cline theory provides a powerful conceptual framework to understand the maintenance of hybrid zones and estimate the
66 strength of dispersal and selection from combined measures of cline width and linkage disequilibrium (Barton & Hewitt, 1985; Gay et al., 2008). Clines are useful to estimate the extension of contact zone between groups and to identify which characteristics are involved in the reproductive isolation (Gay et al., 2008). A ratio-cline or ‘cline’ is a graded alternation in the frequency of the morphs of a polymorphic system (Galeotti et al., 2003). However, others definitions have been proposed: “A gradual, smooth, unidirectional change in the character with space...” used by Thorpe (1987), and “a gradient or set of gradients in morphology or gene frequency, at one or more loci” (Barton & Hewitt, 1985). Also, its common to find in most of the literature that ‘hybrid zone’ is synonymized as ‘cline’. Several empirical studies and theoretical reviews have been elaborated with the purpose of understanding the biological processes that lead to a gradual differentiation between biological populations (Huxley, 1938; Wunderle Jr., 1983; Barton & Hewitt, 1985; Saetre et al., 1999; Jiggins & Mallet, 2000; Brumfield et al., 2001; Gay et al., 2008; Fitness et al., 2011; Lee & Jabloński, 2012; Abbott et al., 2013; Derryberry et al., 2013; Hut et al., 2013; Taylor et al., 2014). One of the main conclusions on the subject is that clinal variation is the result of environmental and evolutionary processes that allow the emergence and maintenance of a gradual differentiation between populations of a species. For example, in a study about polymorphism in birds, Galeotti et al. (2003) found that 78% of polymorphic species present geographic clines, and concluded that different environmental features and selective forces appeared to be associated with clines in color polymorphism. In the same way, the authors stated that this variation was related to geographic, climatic and habitat factors. Clinal variation is also considered a frequent phenomenon in polymorphic species and a wide geographical distribution (like as the Narrow-billed Woodcreeper). Also, in a pioneer review, Behle (1950) stated that the influence of environmental factors may affect the traits in populations of species. In the same way, empirical works in different taxonomic groups have been developed to identified and describe clinal variation; Bidau & Martí (2007) tested the existence of the Bergmann’s rule in one species of grasshopper, Dichroplus pratensis (Orthoptera: Acrididae), and found an inverse clinal variation among populations analyzed, namely, the individuals tend to be smaller in higher latitudes (cooler environments) than in low latitudes. In birds, a some studies can be cited; Isler et al. (2005) identified clinal variation of a
67 vocal character in contiguous populations of Thamnophilus caerulescens (Passeriformes: Thamnophilidae), result in agreement with the clines identified by Brumfield (2005) using mitochondrial cytochrome-b gene, showing the usefulness that different sources of biological information can bring to identify intraspecific variation. Analyzing the geographic variation in the European populations of Tyto alba (Strigiformes: Tytonidae), Antoniazza et al. (2010) concluded that the barn owl’s clinal pheomelanic coloration is the result of local adaptation to different niches. Here, despite a high rate of gene flow, probably indirect and direct selection forces maintain the polymorphism in the groups. Likewise, in a work with Diglossa carbonaria (Thraupidae: Passeriformes), Graves (1991) concluded that the clinal patterns of variation in birds correlated with climatic variables are not restricted to temperate latitudes and may occur in relatively non-seasonal tropical environments. For last, in the Suiriri suiriri (Passeriformes: Tyrannidae), an species inhabiting the open lands of South America, an hybrid/clinal variation was identified using morphometric and plumage data, and some hypothesis about speciation and differentiation of species were proposed (Hayes, 2001). The sampled populations of Lepidocolaptes angustirostris were different in their plumage patterns, and the preliminary results shown morphometrical divergence for some characters among the six taxa. However, the results of PCA analyses, the high intergradation found among populations, and absence of defined geographical boundaries among the taxa do not allow clarifying the taxonomic situation of the Narrow-billed Woodcreeper. In this point, the hybrid/clinal analyzes were a useful approach to identify and explain this variation. The morphological data from L. angustirostris allows finding a group of partially overlapped models of clinal variation. In these models, two regions of the distribution were areas exhibiting a gradual morphological variation, not summarized by a same clinal model. First, a core subgroup of partially overlapping clines was discovered. Here, the tail length clines (southern Cerrado, eastern Pantanal, and northern Dry Chaco contact zone) overlapping with one cline from the width of bill data, localized among the Humid Chaco, western Alto Párana Atlantic Forests, northern Párana Flooded Savanna, and southern Cerrado contact zones. In this same region, a cline fitted by the tarsus-metatarsus data was identified (see Fig. 34b). Finally, these last two clines overlap with the clines recovered by the bill length, total culmen, and exposed culmen characters (the PCA1 components), that cover the Humid Chaco, Párana Flooded Savanna, Southern Cone Mesopotamian Savanna, and Espinal ecoregions (see Fig. 30b). Other clinal zones were identified; the data from the wing length
68 recovered three clines placed in the boundaries of Cerrado with the northernmost patches of the Alto Paraná Atlantic Forest ecoregion. This cline is geographically congruent with cline of the width of bill. The clinal zones described above have partial congruence with the phenotypic distribution of L. angustirostris, and allow to identified three major regions without geographic boundaries defined; a region from the northeastern to central Brazil (mainly inhabited by the no-streaked populations), a second region between the first clinal zone in central Brazil to the extreme southern Brazil/northern Paraguay (‘intermediate’ populations), and a third region to southern Brazil to the southernmost region of the distribution (streaked forms). The northern zone of this last region presents the highest number of clines recovered. In the same way, this division of the populations in the angustirostris complex can be compared with the results of the analysis of plumage; with two main groups identified; a no- streaked populations from the northeast Brazil to southern Cerrado (including the isolated populations from the Guianan Savanna, and the Uatuma-Trombetas Moist Forests/Tapajós- Xingú Moist Forests ecoregions), and a Streaked group from The Gran Chaco to the southeast to the Humid Pampas-Espinal ecoregions, and finally, the ‘intermediate’ group inhabiting the areas between the clinal zones. The group(s) proposed as a ‘hybrid’ population between two different taxa, is actually a a population that present intermediate stages in the dorsal/ventral plumage patterns in a latitudinal gradient, in a colour-polymorphic species. Mainly, the clines identified and with the lower AIC belong to models type II (models with none tail fitted and free parameters). i.e., the intermediates restrictive models were chosen as the best fits the data. This result could be correlated to the level of contact among populations. Gay et al. (2008) summarized a list of possible situations of phenotypic distribution across hybrid zones. In this summary, the diverse types of hybridation/cline are subject to the level of introgression present between populations. In this way, and assuming that the extreme populations are allopatric (based in the supplementary information of Gay et al. 2008), the phenotypic distribution in L. angustirostris could be trimodal with introgression, i.e., three main phenotypes (no-streaked, intermediate, and streaked populations) having considerable levels of introgression (equilibrium between dispersal/selection forces). This morphological variation could difficult the definition of taxonomic boundaries along clines, and constitute also a problem for conservation, due to the need for delineating distinct entities for management (Cardoso et al., 2003). Summarizing the
69 information collected in these clines analysis and adding to the results of plumage and morphometric tests, we would propose the presence of clinal variation in the distribution of the Narrow-billed Woodcreeper.
5.4. Environmental correlations and biogeographical considerations
The Narrow-billed Woodcreeper is a species widely distributed that inhabits through open/dry lands of South America, and its populations are subject to diverse environmental factors. Additionally, statistical and clinal tests support the presence of a geographical variation from the northern of Brazil to the Central Argentina in this taxonomic complex. Considering this information, it can be expected that environmental factors have had an effect on the evolution of genetic/phenotypic traits in the species. Geographic variation is the occurrence of morphologic, genetic, or other differences among spatially segregated populations of a species (Gay & Best, 1996). The study of geographic variation of organismal traits has long been of interest in the fields of ecology and evolution. In this way, a large amount of literature has been written in order to propose and discuss the theoretical and empirical works elaborated by ecologists and evolutionary biologists, among others (Scholander, 1955; Mayr, 1956; Power, 1969; James, 1970; Rhymer, 1992; Fitzpatrick & Dunk, 1999; Ashton et al., 2000; Meiri & Dayan, 2003). In species with geographical variation, the morphological character with more variation is the size, which varies in widespread species (Mayr, 1963; Galeotti et al., 2003). Also, taxa can have a sectorized variation, i.e., some traits or group of traits in some specific area of the individuals vary along their geographical distribution. The study of these variations in the populations of widespread taxa has allow to propose ‘ecogeographic’ theories describing the correlation between morphological variation and environmental variation. Among them, the rules of Bergmann’s (Bergmann, 1847), Allen’s (Allen, 1877), Gloger’s (Gloger, 1833), and the ‘Neo-Bergmannian’ rules (a re-interpretation by James, 1970) explain the variation in the phenotypes of the populations. The ecogeographic rule most tested in analyses of geographical variation is the Bergmann’s rule, that states in its original version that warm blooded vertebrate species from cooler climates tend to be larger than congeners from warmer climates (see Meiri & Dayan, 2003). Subsequently, the modification of James (1970) proposed that the intraspecific variation in
70 size is related to a combination of climatic variables that includes temperature and humidity, i.e., the small size is associated with hot and humid conditions, larger size with cooler or drier conditions. The other two ecogeographic rules are less used, but are of equal importance when testing variation. In the Allen’s rule, the individuals in hot climates should have longer appendages relative to body core size in order to dissipate heat more efficiently. While that in the Gloger’s rule, defined as the expectation that plumages of birds are darker in more humid environments. It is important note that other selection forces (dense vegetation, interspecific competition, diet, among others factors) might also operate for slight variations in size at the population or species level (see Hamilton, 1961). In works on geographical variation in Aves, several remarks have been proposed and tested with empirical methodologies. In an early review of the adaptive significances of the intra-specific variation in continental birds, (Hamilton, 1961) concluded that the variation in wing length and body size in birds exist, and is correlated to gradient factors of the environment. Also, and maybe important for the analysis of L. angustirostris, the clinal variation of each of these morphological traits could not be concordant. In the same way, James (1983) stated that phenotypic variation in the Red-winged Blackbird contains an important environmental component. In populations of birds, regional trends of size variation change gradually in a way that may reflect topographic features (James, 1970). In a review by Meiri & Dayan (2003), the authors found that the presence of the Bergmann’s rule is more common in sedentary than in migratory species, and concluded that this ecogeographic rule is “a valid ecological generalization for birds and mammals at the class, order, and family levels”. In the same work, the non passerines show a higher percentage of species following to Bergmann’s rule than do passerines, but the difference is not significant. In a study about Red-winged Blackbirds, Power (1969) concluded that size increases in arid regions may facilitate conservation of metabolic water and size decreases in humid regions may facilitate heat dissipation. In populations of Turdus migratorius, the morphological variation and plumage is concordant with the predicted by the Bergmann’s and Gloger’s rules, but the relationships among the explanatory variables were not well elucidated (Aldrich & James, 1991). For mammals, some empirical works has been found correlations between environmental variables and phenotypic characters. For example, Cardini et al. (2007) concluded that some climatic variables (seasonality and rainfall) appears as important factors
71 to explain the variation in shape and size of skull in vervet monkeys. Fooden & Albrecht (1993) analyzed the latitudinal and peninsular variation in Macaca fascicularis (Cercopithecidae: Primates) populations, and concluded that this variation in the skull length follow the Bermann’s rule of increasing size with increasing latitude. In this work, the GLM analyses were conducted to establish a correlation between the geographical variation existing in the Narrow-billed Woodcreeper and the climatic information gathered from each geographic record sampled. In these analyses, the climatic factors most explanatory of the geographical variation were temperature seasonality (BIOCLIM 4), annual precipitation (BIOCLIM 12), and minimum temperature of coldest month (BIOCLIM 6). In all models identified, these three variables appear to be the most correlated to the traits analyzed (PC1, PC2, size, and ventral plumage pattern). For PC1 (bill length, exposed culmen, and total culmen), a positive correlation was found with the latitude and the temperature seasonality. Namely, the size of components from PC1 increases as the temperature seasonality and latitude increases to south (from the Equator line to south). In contrary, a negative correlation was identified with the annual precipitation and the minimum temperature of coldest month; with the decrease of these two variables, the size of bill length, exposed culmen, and total culmen increases. The model interaction annual precipitation-temperature seasonality, have a positive and negative correlation with the PC1 variation, respectively. For PC2, the bill width is positively correlated to the increase to south of latitude. The same type of correlation (+) is recovered in models with temperature seasonality and the temperature annual range as explanatory variables. With the increase of these climatic variables, the bill width increases too. In the other hand, the character is negatively correlated with annual precipitation, minimum temperature of coldest month, and precipitation of coldest quarter. The correlation between the size and the climatic variables is not clear. Despite of show correlations with same models identified in PC1 and PC2 analyses, the variation of size have two variation tendencies, a decreasing cline from the northeast to the central Brazil, and a increasing cline from this last zone to the southernmost region in central Argentina. The only climatic variable fitting in the size variation was the precipitation of warmest quarter. It is possible that the low levels of precipitation in the Caatinga and Chaco ecoregions (extreme regions of the distribution), additional to the high temperature in certain time of year can
72 influence the size of individuals. The temperature seasonality was the most correlated variable to the ventral plumage variation. In L. angustirostris the darker and streaked plumages were found in the southern Cerrado and Humid Chaco ecoregions, while the no-streaked patterns (cinnamon-ochraceous, pale yellow, Greyish-white pattern) inhabits northern Cerrado and Caatinga. Here, the Gloger’ rule could be applied, where the darker plumage are found in more humid environments (Humid Chaco, southern Cerrado), and the lighter inhabits dry regions (Caatinga). Overall, the variation in the Narrow-billed Woodcreeper appears to follow the ecogeographic rules of Bergmann and the Gloger. First, individuals with larger bills are present at higher latitudes to south (El Gran Chaco ecoregions), while groups with smaller bills can be found near to Equator, and populations with darker plumages can be found the the south of the distribution with an high levels of humidity, and the ligther/no-streaked populations at the central and north of Brazil (dry regions). Also, the Allen’s rule (individuals in hot climates should have longer appendages relative to body core size than individuals in cold environments) could be applied to the populations of L. angustirostris; the tarsus- metatarsus length increases with the increase of latitude to south. However, this correlation seems not significative (see Fig. 36). The study of geographical variation in the Narrow-billed Woodcreeper can also be addressed from a biogeographical perspective. Geological changes have influenced the diversity of plants and animals in the open/dry lands of South America. For example, several authors have proposed that geological events are contributed to modify the evolutionary history of species. Campagna et al. (2011) proposed that the fluctuation in predominance of rainforest over open habitats and vice versa and the interdigitation of these two biomes could have contributed to isolating small populations in islands of suitable habitat, or a grassland refugia. In the works of Werneck (2011) and Werneck et al. (2011), the biogeographical patterns of the open/dry lands in South America are the result of a correlation of geological processes that occurred during the Tertiary and Quaternary ages. From them, perhaps the most studied are the climatic fluctuations in the Pleistocene. Periodical glaciations and interglaciations affected the geographical extension of forest and savanna biomes. In the most accepted hypothesis, glaciation periods were characterized by cool and dry climates, with a reduction of Amazonian and Atlantic forests and the increase of open biomes (savannas).
73 During the interglacial periods (wet and hot climates), the savanna area was reduced and isolated refugia emerged. In this scenario, the geographical range of the savanna species was reduced to these isolated refugia (a similar situation to the Amazonian refugia proposed by Haffer 1969), starting a genetic and morphological differentiation among their populations. Using the grassland refugia hypothesis, the partial molecular data from Arbelaéz-Cortés et al. (low genetic divergence among the sampled individuals of the Narrow-billed woodcreeper), and the results in this taxonomic review, it is plausible to propose that the high variation in plumage and low genetic divergence among the populations of L. angustirostris could be influenced indirectly by the climatic variations during the Pleistocene. However, additional biogeographical analyses should be performed to confirm this hypothesis.
5.5. The ‘Amazonian’ populations of the Narrow-billed Woodcreeper
Isolated populations were found in the Guianan Savanna, and the Uatuma-Trombetas Moist Forests/Tapajós-Xingpú Moist Forests ecoregions. In the literature reviewed, these populations belong the griseiceps subspecies (Mees, 1974; Marantz et al., 2003). Mainly, the individuals from these groups show a dorsal plumage Strong brown. Also, a white to greyish- white and pale yellow colorations were found in the ventral plumage. These plumage patterns are characteristic of the “bivittatus” group. Morphometric data show no divergence with the other populations from Caatinga-central Cerrado. Due the limitations of the hzar algorithm, the data from these populations were not included in the clinal analysis. The taxonomic validity of the griseiceps subspecies is doubtful. Geographically, is isolated, but their phenotypic characters show no signs of divergence from other populations. Mees (1974) proposed as a diagnostic character of griseiceps a crown brownish grey, more lighter that the adjacent groups (Caatinga-Cerrado populations). However, in the skins analized in this work, this difference was not found. Some biogeographical remarks can be elaborated with the aim to explain the presence of L. angustirostris in these Amazonian ecoregions. Following the classification of Olson et al. (2001), the distribution of L. angustirostris covers regions within the Tropical and subtropical Grasslands, savannas, and shrublands biome. This biome is present in South America (Neotropic), Africa (Afropic) and the northern of Australasia. In South America, is represented by the Cerrado, The Great Chaco (the Dry and Humid Chaco ecoregions
74 together), the Benni savanna, ‘Los LLanos’, and the Guianan savanna ecoregions. From these ecoregions, three are habited by the Narrow-billed Woodcreeper. In this way, the ‘grassland refugia’ (see Campagna et al. 2011 and Haffer 1969) hypothesis could help to solve this question. With the climatic variations of Pleistocene and Holocene, the forest regions of South America reduced its extension (glacial periods), and the grasslands regions were predominant (open areas), including the northern savannas of Los Llanos and Guianan savanna (see Werneck et al. 2011). In these glacial periods, populations of the Narrow-billed were able to expand through all these open areas, and, posteriorly, in the interglacial periods, forests were recovering their extension in these warmer and humid periods, and the northernmost populations were isolated from the rest (groups of Caatinga-Cerrado-Chaco ecoregions). Another isolated population, with a few specimens collected, inhabiting the localities around the outlet of Tapajós river in the Amazon (e.g. Boca Río Tapajós, MZUSP 14675), and most to east (Monte Alegre locality, MPEG 4732 and 54361) could be affected by the same geological events.
75 6. Conclusions
The taxonomic status of L. angustirostris complex is an interesting subject of study. Based in morphological information, the tests of diagnosability, and the clinal analyses, we conclude that the populations of Narrow-billed Woodcreeper are highly color polymorphic, but this is no compelling evidence to suggest the existence of several individual evolutionary lineages. Namely, the divergence exhibited by their populations is considerable, but this ‘phenotypic variation’ could not be decisive as to sort each morph in a different species. Perhaps the most notorious evidence supporting one unique species and the elimination of subespecific ranks in the taxon is the level of introgression found among the populations sampled. The PCA and clinal analyses show that the different groups proposed (groups identified from the plumage analysis) are connected by broad contact zones, with individuals with intermediate phenotypic traits (mainly plumage). Other factor in favor of the results is the absence of geographical barriers that reduce the genetic interchange among populations. The main habits of L. angustirostris are the Cerrado(s), Caatinga, and the Great Chaco ecoregions, that represent the savannas and the seasonally dry forests in South America. These ecoregions form an ecological barrier between the Amazonian and Atlantic forests. On the other hand, among these three ecoregions no barriers are found, a region succeeds another without ‘drastic’ changes in its ecological or geographical characteristics. That is, the transformation of the landscape is continuous, not abrupt. Additionally, patches of one ecoregion can be placed within other. Thus it is not possible to separate subspecies for habitat, as occurs commonly in studies of Ornithology. The used of recent methodologies implementing old/new theoretical approaches is very useful to understand the biological process that modeled the morphological/genetic characteristics of the populations. New statistical packages to analyze these data (e.g. the R package hzar) are optimal tools to develop automatized and better studies in Biology. The use of free software and a basic knowledge about computer programming is now a pressing need in the biological sciences. Also, the development of the R software environment for statistical computing is a promising area of scientific research.
76 7. Bibliography
Abbott, R., Albach, D., Ansell, S., Arntzen, J. W., Baird, S. J. E., Bierne, N., Boughman, J., Brelsford, A., Buerkle, C. A., Buggs, R., Butlin, R. K., Dieckmann, U., Eroukhmanoff, F., Grill, A., Cahan, S. H., Hermansen, J. S., Hewitt, G., Hudson, A. G., Jiggins, C., Jones, J., Keller, B., Marczewski, T., Mallet, J., Martinez-Rodriguez, P., Möst, M., Mullen, S., Nichols, R., Nolte, A. W., Parisod, C., Pfennig, K., Rice, A. M., Ritchie, M. G., Seifert, B., Smadja, C. M., Stelkens, R., Szymura, J. M., Väinölä, R., Wolf, J. B. W., & Zinner, D. 2013. Hybridization and speciation. Journal of Evolutionary Biology, 26, 229-246.
Adams, C. E. & Huntingford, F. A. 2004. Incipient speciation driven by phenotypic plasticity? Evidence from sympatric populations of Arctic charr. Biological Journal of the Linnean Society, 81, 611-618.
Agapow, P. M., Bininda-Emonds, O. R. P., Crandall, K. A., Gittleman, J. L., Mace, G. M., Marshall, J. C., & Purvis, A. 2004. The impact of species concept on biodiversity studies. The Quarterly Review of Biology, 79, 161-179.
Aldrich, J. W. & James, F. C. 1991. Ecogeographic variation in the American robin (Turdus migratorius). The Auk, 108, 230-249.
Allen. 1876. Picolaptes bivittatus. Bulletin of the Essex Institute, 8, 80.
Allen, J. A. 1877. The influence of physical conditions in the genesis of species. The Radical Review, 1, pp. 140.
Alström, P., Rasmussen, P. C., Olsson, U., & Sundberg, P. 2008. Species delimitation based on multiple criteria: the Spotted Bush-Warbler Bradypterus thoracicus complex (Aves: Megaluridae). Zoological Journal of the Linnean Society, 154, 291-307.
Amadon, D. 1949. The seventy-five per cent rule for subspecies. The Condor, 51, 250-258.
77 Antoniazza, S., Burri, R., Fumagalli, L., Goudet, J., & Roulin, A. 2010. Local adaptation maintains clinal variation in melanin-based coloration of european barn owls (Tyto alba). Evolution, 64, 1944-1954.
Arbelaéz-Cortés, E., Navarro-Sigüenza, A. G., & García-Moreno, J. 2012. Phylogeny of woodcreepers of the genus Lepidocolaptes (Aves, Furnariidae), a widespread Neotropical taxon. Zoologica Scripta, 2012, 41, 363-373.
Ashton, K. G., Tracy, M. C., & de Queiroz, A. 2000. Is Bergmann’s rule valid for mammals? The American Naturalist, 156, 390-415.
Azara, D. F. 1802. Apuntamientos para la historia natural de los páxaros del Paragüay y Rio de la Plata. Tomo II. Imprenta de la Viuda de Ibarra. Madrid.
Baldwin, S., Oberholser, H., & Worley, L. 1931. Measurements of birds. volume 2. Cleveland, Cleveland Museum of Natural History, IV , 165.
Barker, F. K., Cibois, A., Schikler, P., Feinstein, J., & Cracraft, J. 2004. Phylogeny and diversification of the largest avian radiation. Proceedings of National Academy of Sciences of the United States of America, 101, 11040-11045.
Barton, N. H. & Gale, K. S. 1993. Genetic analysis of hybrid zones. In: Hybrid Zones and the Evolutionary Process, Oxford University Press, chap. 2. 13-42.
Barton, N. H. & Hewitt, G. M. 1985. Analysis of hybrid zones. Ann. Rev. Ecol. Syst., 16, 113-148.
Barton, N. H. & Hewitt, G. M. 1989. Adaptation, speciation and hybrid zones. Nature, 341, 497-503.
Behle, W. H. (1950). Clines in the yellow-throats of western north america. The Condor, 52, 193-219.
78
Bergmann, C. 1847. Über die Verhältnisse der Wärmeökonomie der Thiere zu Ihrer Grösse. Göttinger Studien, 3, 595-708.
Bidau, C. J. & Martí, D. A. 2007. Clinal variation of body size in Dichroplus pratensis (Orthoptera: Acrididae): Inversion of bergmanns and renschs rules. Annals of the Entomological Society of America, 100, 850-860.
Bioacoustics Research Program. 2011. Raven Pro: Interactive Sound Analysis Sfotware (Version 1.4). The Cornell Lab of Ornithology, Ithaca, New York.
Bodrati, A. & Cockle, K. L. 2011. Nesting of the scalloped woodcreeper (Lepidocolaptes falcinellus). Ornitologia Neotropical, 22, 195-206.
Bolker, B. 2014. Tools for general maximum likelihood estimation. R package version 1.0.17 - For new features, see the ’Changelog’ file (in the package source).
Brelsford, A. & Irwin, D. E. 2009. Incipient speciation despite little assortative mating: The Yellow-rumped Warbler hybrid zone. Evolution, 63, 3050-3060.
Brumfield, R. T. (2005). Mitochondrial variation in Bolivian populations of the variable antshrike (Thamnophilus caerulescens). The Auk, 122, 414-432.
Brumfield, R. T., Jernigan, R. W., Mcdonald, D. B., & Braun, M. J. 2001. Evolutionary implications of divergent clines in an avian (Manacus: Aves) hybrid zone. Evolution, 55, 2070-2087.
Bucher, E. H. 1982. Chaco and Caatinga-South American Arid Savannas, Woodland sand Thickets. In Ecology of Tropical Savannas, Berlin: Springer-Verlag, chap. 3. 48-79.
Cabanis, J. & Heine, F. 1860. Lepidocolaptes falcinellus. Museum Heineanum: Verzeichniss der Ornithologischen Sammlung. II. Theil: die Schreivögel enthaltend.
79 Halberstadt: R. Franz. 2, p. 38.
Calcagno, V. 2014. Model selection and multimodel inference made easy. R package version 1.0.7 - For new features, see the ’Changelog’ file (in the package source).
Calcagno, V. & de Mazancourt, C. 2010. glmulti: An r package for easy automated model selection with (generalized) linear models. Journal of Statistical Software, 34, 1-29. URL http://www.jstatsoft.org/v34/i12.
Camargo, A. & Sites, J. J. 2013. Species Delimitation: A Decade After the Renaissance. In The Species Problem - Ongoing Issues, Pavlinov YI, editor, chap. 9. 225-247.
Campagna, L., Benites, P., Lougheed, S. C., Lijtmaer, D. A., Giacomo, A. S. D., Eaton, M. D., & Tubaro, P. L. 2011. Rapid phenotypic evolution during incipient speciation in a continental avian radiation. Proceedings of the Royal Society: Biological Sciences, 279, 1847-1856.
Cardini, A., Jansson, A., & Elton, S. 2007. A geometric morphometric approach to the study of ecogeographical and clinal variation in Vervet monkeys. Journal of Biogeography, 34, 1663-1678.
Cardoso, A., Vogler, A. P., & Serrano, A. 2003. Morphological and genetic variation in Cicindela lusitanica Mandl, 1935 (Coleoptera, Carabidae, Cicindelinae): Implications for conservation. Graellsia, 59, 415-426.
Charif, R., Waack, A., & Strickman, L. 2010. Raven Pro 1.4 user’s manual. Cornell Lab of Ornithology, Ithaca, NY.
Cherrie, G. K. 1916. Some apparently undescribed birds from the collection of the Roosevelt South American Expedition. Bulletin of the American Museum of Natural History, 35, 183-190.
80 Cicero, C. 2010. The significance of subspecies: A case study of Sage Sparrows (Emberizidae, Amphispiza belli). Ornithological Monographs, 67, 103-113.
Claramunt, S., Derryberry, E. P., Brumfield, R. T., & Remsen, J. V. 2012. Ecological Opportunity and Diversification in a Continental Radiation of Birds: limbing Adaptations and Cladogenesis in the Furnariidae. The American Naturalist, 179, 649-666.
Cracraft, J. 1983. Species concepts and speciation analysis. Current Ornithology, 1, 159- 187.
Cracraft, J. 1989. Speciation and its ontology: The empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. In D. Otte & J. Endler (Eds.), Speciation and its Consequences, Sinauer Associates, chap. 2. 28-59.
Dabenne, 1910. Picolaptes angustirostris angustirostris. Anales del Museo Nacional de Buenos Aires, 18, 307.
Daly, D. C. & Mitchell, J. D. 2000. Lowland Vegetation of Tropical South America: An Overview. In Imperfect Balance: Landscape Transformations in the pre-Columbian Americas, Columbia University Press, New York., chap. 14. 391-454.
Queiroz, K., 2007. Species concepts and species delimitations. Systematic Biology, 56, 879- 886.
Queiroz, L. P. 2006. The Brazilian Caatinga: Phytogeographical Patterns Inferred from Distribution Data of the Leguminosae. In Neotropical Savannas and Seasonally Dry Forests: Plant Diversity, Biogeography and Conservation, CRC Press, chap. 6. 121-157.
Derryberry, E. P., Claramunt, S., Derryberry, G., Chesser, R. T., Cracraft, J., Aleixo, A., Pérez- Emán, J., Remsen, J. V., & Brumfield, R. T. 2011. Lineage diversification and morphological evolution in a large-scale continental radiation: The Neotropical ovenbirds and woodcreepers (Aves: Furnariidae). Evolution, 65, 2973-2986.
81
Derryberry, E. P., Derryberry, G. E., Maley, J. M., & Brumfield, R. T. 2013. Hzar: hybrid zone analysis using an r software package. Molecular Ecology Resources, 14, 1-12.
Derryberry, G. 2013. hzar: Hybrid Zone Analysis using R. R package version 0.2.5 - For new features, see the ’Changelog’ file (in the package source).
Des Murs, M. 1849. Iconographie ornithologique. Livr. 12[”1848], pl. 71, text.
Des Murs, M. 1849. Iconographie ornithologique. Livr. 12[”1848], pl. 70, text.
D’Orbigny 1838. Synopsis Avium. Magasin de Zoologie, 8, 1-34.
Endler, J. A. 1977. Geographic Variation, Speciation and Clines. Princeton University Press.
Esteves-Lopes, L., & Gonzaga, L. 2014. Morphological variation in the Cinnamon Tanager Schistochlamys ruficapillus (Aves: Thraupidae). Zootaxa, 3853, 477-494.
Fitness, J., Hitchmough, R. A., & Morgan-Richards, M. 2011. Little and large: body size and genetic clines in a New Zealand gecko (Woodworthia maculata) along a coastal transect. Ecology and Evolution, 2, 273-285.
Fitzpatrick, B. M. & Dunk, J. R. 1999. Ecogeographic variation in morphology of Red-tailed Hawks in western North America. Journal of Raptor Research, 33, 305-312.
Fitzpatrick, J. W. 2010. Subspecies are for convenience. Ornithological Monographs, 67, 54-61.
Fjeldså, J., Irestedt, M., & Ericson, P. G. P. 2005. Molecular data reveal some major adaptational shifts in the early evolution of the most diverse avian family, the Furnariidae. Journal of Ornithology, 146, 1-13.
82
Fooden, J. & Albrecht, G. H. 1993. Latitudinal and insular variation of skull size in Crab- eating Macaques (Primates, Cercopithecidae: Macaca fascicularis). American Journal of Physical Anthropology, 92, 521-538.
Forsman, A., Ahnesjo, J., Caesar, S., & Karlsson, M. 2008. A model of ecological and evolutionary consequences of color polymorphism. Ecology, 89, 34-40.
Galeotti, P., Rubolini, D., Dunn, P. O., & Fasola, M. 2003. Colour polymorphism in birds: causes and functions. Journal of Evolutionary Biology, 16, 635-646.
García-moreno, J. & Silva, J. M. C. 1997. An interplay between forest and non-forest South American avifaunas suggested by a phylogeny of Lepidocolaptes woodcreepers (Dendrocolaptinae). Studies on Neotropical Fauna and Environment, 32, 164-173.
Gay, L., Crochet, P., Bell, D. A., & Lenormand, T. 2008. Comparing clines on molecular and phenotypic traits in hybrid zones: A window on tension zone models. Evolution, 62, 2789- 2806.
Gay, S. W. & Best, T. L. 1996. Relationships between abiotic variables and geographic variation in skulls of pumas (Puma concolor: Mammalia, felidae) in North and South America. Zoological Journal of the Linnean Society, 117, 259-282.
Gill, F. B. 2014. Species taxonomy of birds: Which null hypothesis? The Auk, 131, 150-161.
Gloger, C. L. 1833. Das Abandern der Vögel durch Einfluss des Klimas Breslau: A. Schulz.
Graves, G. R. 1991. Bergmann’s rule near the equator: Latitudinal dines in body size of an Andean passerine bird. Proceedings of National Academy of Sciences of the United States of America, 88, 2322-2335.
83 Gray, G. 1840. A list of the genera of birds, with an indication of the typical species of each genus. Londres: Richard e J. E. Taylor.
Gray, S. M. & McKinnon, J. S. 2007. Linking color polymorphism maintenance and speciation. Trends in Ecology and Evolution, 22, 71-79.
Haffer, J. 1969. Speciation in amazonian forest birds. Science, New Series, 165, 131-137.
Haig, S. M. & Winker, K. 2010. Avian subspecies: Summary and prospectus. Ornithological Monographs, 67, 172-175.
Hamilton, T. H. 1961. The adaptive significances of intraspecific trends of variation in wing length and body size among bird species. Evolution, 15, 180-195.
Hayes, F. E. 2001. Geographic variation, hybridization, and the leapfrog pattern of evolution in the Suiriri flycatcher (Suiriri suiriri) complex. The Auk, 118, 457-471.
Helbig, A. J., Knox, A. G., Parkin, D. T., Sangster, G., & Collinson, M. 2002. Guidelines for assigning species rank. Ibis, 144, 518-525.
Hellmayr, H. E. 1903. Über neue und wenig bekannte südamerikanische Vögel. Verhandllungen der kaiserlich - königlichen zoologisch-botanischen Gesellschaft in Wien, 53, 199-223.
Hellmayr, C. E. 1908. An account of the birds collected by Mons. G. A. Baer in the State of Goyaz, Brazil. Novitates Zoologicae, 15, 13-102.
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965-1978.
Hugall, A. F. & Stuart-Fox, D. 2012. Accelerated speciation in colour-polymorphic birds.
84 Nature, 485, 631-634.
Husson, F., Josse, J., Le, S., & Mazet, J. 2014. Multivariate Exploratory Data Analysis and Data Mining with R. URL http://factominer.free.fr. R package version 1.27 - For new features, see the ’Changelog’ file (in the package source).
Hut, R. A., Paolucci, S., Dor, R., Kyriacou, C. P., & Daan, S. 2013. Latitudinal clines: an evolutionary view on biological rhythms. Proceedings of the Royal Society: Biological Sciences, 280, 1-9.
Huxley, J. 1938. Clines: an auxiliary taxonomic principle. Nature, 142, 219-220.
Huxley, J. 1955. Morphism in birds. Acta Int. Congr. Ornithol., 11, 309-328.
Irestedt, M., Fjeldså, J., & Ericson, P. G. P. 2004. Phylogenetic relationships of woodcreepers (Aves: Dendrocolaptinae) - incongruence between molecular and morphological data. Journal of Avian Biology, 35, 280-288.
Irestedt, M., Fjeldså, J., Johansson, U. S., & Ericson, P. G. 2002. Systematic relationships and biogeography of the tracheophone suboscines (Aves: Passeriformes). Molecular Phylogenetics and Evolution, 23, 499-512.
Isler, M. L., Isler, P. R., & Brumfield, R. T. 2005. Clinal variation in vocalizations of an antbird (Thamnophilidae) and implications for defining species limits. The Auk, 122, 433- 444.
James, F. C. 1970. Geographic size variation in birds and its relationship to climate. Ecology, 51, 365-390.
James, F. C. 1983. Environmental component of morphological differentiation in birds. Science, 221, 184-186.
85 Jiggins, C. D. & Mallet, J. 2000. Bimodal hybrid zones and speciation. TREE, 15, 250-255.
Lafresnaye, F. 1846. Sur quelques nouvelles espèces d’oiseaux de Colombie. Revue Zoologique. 9, 206-209.
Lafresnaye, F. 1850. Essai d’une monographie du genre Picucule (Buffon), Dendrocolaptes (Hermann, Illiger), devenu aujourd’hui la sous-famille Dendrocolaptinae (Gray, Genera of Birds), de la famille Certhidae de Swains. Revue et Magasin de Zoologie pure et appliquée, 13, 145-154.
Lee, J. & Jabloński, P. G. 2012. Egg color polymorphism and morph-ratio variation in korean populations of the Vinous-throated parrotbill. Chinese Birds, 3, 312-319.
Lesson, R. P. (1830). Traite d’Ornithologie. 2, Paris: F. G. Levraud.
Lichtenstein, H. K. 1822. Abhandlungen der physikalischen (-mathematischen) Klasse der Koeniglich-Preussischen Akademie der Wissenschaften. Berlin. (1820-1821), p. 258, 266.
Livezey, B. C. & Zusi, R. L. 2007. Higher-order phylogeny of modern birds (Theropoda, Aves: Neornithes) based on comparative anatomy. ii. Analysis and discussion. Zoological Journal of the Linnean Society, 149, 1-95.
Lopéz-Lanús, B (Ed.). 2008. Bird Sounds from Southern South America. Audiornis Producciones. Buenos Aires, Argentina.
Luz, H. R., Ferreira, I., & Ventura, P. E. C. 2007. Reprodução do arapaçu-do-cerrado (Lepidocolaptes angustirostris vieillot, 1918) (Aves: Dendrocolaptidae) no estado do Rio de Janeiro, Brasil. Lundiana, 8, 75-78.
Marantz, C. A., Aleixo, A., Bevier, L. R., & Patten, M. A. 2003. Family Dendrocolaptidae (Woodcreepers). In J. Del Hoyo, A. Elliott, & D. A. Christie (Eds.), Handbook of the birds
86 of the world Vol 8 Broadbills to Tapaculos, Lynx Edicions, vol. 8. 358-447.
Marantz, C. A. & Patten, M. A. 2010. Quantifying subspecies analysis: A case study of morphometric variation and subspecies in the woodcreeper genus Dendrocolaptes. Ornithological Monographs, 67, 123-140.
Mayr, E. 1956. Geographical character gradients and climatic adaptation. Evolution, 10, 105- 108.
Mayr, E. 1963. Animal Species and Evolution. Cambrigde, Massachusetts: Belknap Press of Harvard University Press.
Mees, G. F. 1974. Additions to the Avifauna of Suriname. Zoologische Mededelingen, 48, 55-67.
Meiri, S. & Dayan, T. 2003. On the validity of Bergmann’s rule. Journal of Biogeography, 30, 331-351.
Monroe, B. L. & Sibley, C. G. 1993. A World Checklist of Birds. New Haven and London: Yale University Press.
Morrone, J. J. 2001. Biogeografía de América Latina y el Caribe. Mexico, GORFI, S.A.
Morrone, J. J. 2014. Biogeographical regionalization of the Neotropical region. Zootaxa, 3782, 1-110.
Mosimann, J. E. 1970. Size allometry: Size and shape variables with characterizations of the lognormal and generalized gamma distributions. Journal of the American Statistical Association, 65, 930-945.
Moyle, R. G., Chesser, R. T., Brumfield, R. T., Tello, J. G., Marchese, D. J., & Cracraft, J. 2009. Phylogeny and phylogenetic classification of the antbirds, ovenbirds, woodcreepers,
87 and allies (Aves: Passeriformes: infraorder Furnariides). Cladistics, 25, 1-20.
Munsell, A. 1994. Soil, color charts, revised edition. Nova York. MacBeth Division of Kollmorgan Instruments Corporation.
Naumburg, E. M. B. 1925. A new Lepidocolaptes. The Auk, 42, 421-422.
Oliveira-Filho, A. T. & Ratter, J. A. 1995. A study of the origin of central brazilian forests by the analysis of plant species distribution patterns. Edinburgh Journal of Botany, 52, 141- 194.
Oliveira-Filho, A. T. & Ratter, J. A. 2002. Vegetation physiognomies and woody Flora of the Cerrado Biome. In The Cerrados of Brazil: Ecology and natural history of a Neotropical savanna, Columbia University Press, chap. 6. 91-120.
Olson, D. M., Dinerstein, E., Wikramanayake, E. D., Burgess, N. D., Powell, G. V. N., Underwood, E. C., D’Amico, J. A., Itoua, I., Strand, H. E., Morrison, J. C., Loucks, C. J., Allnutt, T. F., Ricketts, T. H., Kura, Y., Lamoreux, J. F., Wettengel, W. W., Hedao, P., & Kassem, K. R. 2001. Terrestrial ecoregions of the world: A new map of life on earth. BioScience, 52, 933-938.
Pacheco, M. A., Battistuzzi, F. U., Lentino, M., Aguilar, R. F., Kumar, S., & Escalante, A. A. 2011. Evolution of modern birds revealed by mitogenomics: Timing the radiation and origin of major orders. Molecular Biology and Evolution, 28, 1927-1942.
Patten, M. A. 2010. Null expectations in subspecies diagnosis. Ornithological Monographs, 67, 35-41.
Patten, M. A. & Unitt, P. 2002. Diagnosability versus mean differences of Sage sparrow subspecies. The Auk, 119, 26-35.
Pennington, R. . T., Lewis, G. P. ., & Ratter, J. A. 2006. An overview of the plant diversity,
88 Biogeography and Conservation of Neotropical Savannas and Seasonally Dry Forests. In Neotropical Savannas and Seasonally Dry Forests: Plant Diversity, Biogeography and Conservation, CRC Press, chap. 1. 1-29.
Power, D. M. 1969. Evolutionary implications of wing and size variation in the red winged blackbird inrelation to geographic and climatic factors: A multiple regression analysis. Systematic Zoology, 18, 363-373.
Price, T. 2008. Speciation in Birds. Greenwood Villege, Colorado. Roberts and Company Publishers.
R Core Team. 2013. R: A Language and Environment for Statistical Computing. R Founda- tion for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/. ISBN 3- 900051-07-0.
Raikow, R. J. 1982. Monophyly of the Passeriformes: Test of a phylogenetic hypothesis. The Auk, 99, 431-445.
Raikow, R. J. 1994. A phylogeny of the woodcreepers (Dendrocolaptinae). The Auk, 111, 104-114.
Reichenbach, H. 1853. Icones ad Synopsin Avium, Leipzig: Verlag Hofmeister.
Rhymer, J. M. 1992. An experimental study of geographic variation in avian growth and development. Journal of Evolutionary Biology, 5, 289-306.
Ridgely, R. S. & Tudor, G. 1994. The birds of South America. Volume 2: The suboscine passerines. Austin. University of Texas Press.
Ridgely, R. S. & Tudor, G. 2009. Field guide to the songbirds of South America. The passerines. Austin. University of Texas Press.
89 Rodrigues, E. B., Aleixo, A., Whittaker, A., & Naka, L. N. 2013. Molecular systematics and taxonomic revision of the Lineated Woodcreeper complex (Lepidocolaptes albolineatus: Dendrocolaptidae), with description of a new species from southwestern Amazonia. In Handbook of the Birds of the World. Special Volume: New Species and Global Index, Barcelona, Lynx Edicions, 248-252.
Roulin, A. 2004. The evolution, maintenance and adaptive function of genetic colour polymorphism in birds. Biological Reviews, 79, 815-848.
Sætre, G., Král, M., Buresï, S., & Ims, R. A. 1999. Dynamics of a clinal hybrid zone and a comparison with island hybrid zones of flycatchers (Ficedula hypoleuca and F. albicollis). Journal of Zoology (London), 247, 53-64.
Sangster, G. 2014. The application of species criteria in avian taxonomy and its implications for the debate over species concepts. Biological Reviews, 89, 199-214.
Scholander, P. F. 1955. Evolution of climatic adaptation in homeotherms. Evolution, 9, 15- 26.
Sclater, P. L. 1890. Catalogue of Birds in the British Museum. Volume XV: Catalogue of the Passeriformes or perching birds in the collection of the British Museum: Tracheophonae or the families Dendrocolaptidae, Formicariidae, Conopophagidae, and Pteroptochidae. Londres: British Museum (Natural History).
Sibley, C. G. & Ahlquist, J. E. 1990. Phylogeny and classification of the birds of the world. Yale University Press, New Haven & London.
Sibley, C. G. & Monroe, B. L. 1990. Distribution and Taxonomy of the Birds of the World. Yale Univ. Press, New Haven, CT.
Silva, J. M. C. & Straube, F. C. 1996. Systematics and biogeography of Scaled Woodcreepers (Aves: Dendrocolaptidae). Studies on Neotropical Fauna and Environment, 31, 3-10.
90
Spicer, G. S. & Dunipace, L. 2004. Molecular phylogeny of songbirds (Passeriformes) inferred from mitochondrial 16s ribosomal rna gene sequences. Molecular Phylogenetics and Evolution, 30, 325-335.
Spix, J. 1824. Avium species novae, quas in itinere anni DCCCXVII – MDCCCXX per Brasiliam. Volume, 1, Mônaco: Impensis Editoris.
Szymura, J. & Barton, N. H. 1991. The genetic structure of the hybrid zone between the fire- bellied toads Bombina bombina and B. variegata: comparisons between transects and between loci. Evolution, 45, 237-261.
Taylor, S. A., White, T. A., Hochachka, W. M., Ferretti, V., Curry, R. L., & Lovette, I. 2014. Climate-mediated movement of an avian hybrid zone. Current Biology, 24, 671-676.
Thorpe, R. S. 1987. Geographic variation: A synthesis of cause, data, pattern and congruence in relation to subspecies, multivariate analysis and phylogenesis. Bolletino di Zoologia, 54, 3-11.
Tobias, J. A., Seddon, N., Spottiswoode, C. N., Pilgrim, J. D., Fishpool, L. D. C., & Collar, N. J. 2010. Quantitative criteria for species delimitation. Ibis, 152, 724-746.
Todd, W. E. C. 1913. Preliminary diagnoses of apparently new species from Tropical America. Proceedings of the Biological Society of Washington, 26, 169-174.
Treplin, S., Siegert, R., Bleidorn, C., Thompson, H. S., Fotso, R., & Tiedemann, R. 2008. Molecular phylogeny of songbirds (aves: Passeriformes) and the relative utility of common nuclear marker loci. Cladistics, 24, 328-349.
Vanzolini, P.E. 1963. Problemas faunísticos do Cerrado, p.305-321. In: M.G. FerrI (Ed.). Simpósio sobre o Cerrado. São Paulo, Univ. de São Paulo, X+424p.
91 Vieillot, L. J. P. 1818. Nouveau Dictionnaire d’Histoire Naturelle. Volume 26. Paris: Chez Deterville.
Vielliard, J. 1990. Estudo bioacústico das Aves do Brasil. Ararajuba, 1, 5-18.
Wied. 1830. Beiträge zur Naturgeschichte von Brasilien. Volume 3. Weimar: Verlage des G. S. priv. Landes-Industries-Comptoirs.
Werneck, F. P. 2011. The diversification of eastern South American open vegetation biomes: Historical biogeography and perspectives. Quaternary Science Reviews, 30, 1630-1648.
Werneck, F. P., Costa, G. C., Colli, G. R., Prado, D. E., & Jr., J. W. S. 2011. Revisiting the historical distribution of seasonally dry tropical forests: new insights based on palaeodistribution modelling and palynological evidence. Global Ecology and Biogeography, 20, 272-288.
Wetmore, B. 1926. Observations on the birds of Argentina, Paraguay, Uruguay, and Chile. United States National Museum Bulletin, 133, 235-240.
Wunderle Jr., J. M. 1983. A shift in the morph ratio cline in the Bananaquit on grenada, West Indies. Condor, 85, 365-367.
Zapata, F. & Jiménez, I. 2012. Species delimitation: Inferring gaps in morphology across geography. Systematic Biology, 61, 179-194.
Zar, J. H. 2010. Biostatistical Analysis. Englewood Cliffs, New Jersey. Prentice Hall, fifth edition.
Zink, R. M. 2004. The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proceedings of the Royal Society B: Biological Sciences, 271, 561-564.
92 Zink, R. M. 2006. Rigor and species concepts. The Auk, 123, 887-891.
93 Appendix A
Table with the 555 skins analyzed of the Narrow-billed Woodcreeper (21 individuals without geographical coordinates).
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 1970a Lepidocolaptes angustirostris -30,050 -66,883 “Santa Rosa”, Patquia, La Rioja La Rioja Argentina
MACN 65045 Lepidocolaptes angustirostris -24,550 -60,830 3 Km Ne De J. Bazan, Patiño, Formosa Formosa Argentina
MACN 65058 Lepidocolaptes angustirostris -24,250 -61,233 4 Km Ne De Laguna Yema, Bermejo, Formosa Formosa Argentina
MACN 62391 Lepidocolaptes angustirostris -25,950 -60,620 47 Km Ne Castelli (C-57), Guemes, Chaco Chaco Argentina
MACN 53413 Lepidocolaptes angustirostris NA NA 5 Km De Yaciri, Rio Yacuicito, Salta, Depto San Martin Salta Argentina
MACN 2480a Lepidocolaptes angustirostris -22,267 -63,733 Aguaray, Salta Salta Argentina
MACN 30516 Lepidocolaptes angustirostris -23,283 -64,233 Alto Rio Santa Maria, Depto Oran, Salta Salta Argentina
MACN 30517 Lepidocolaptes angustirostris -23,283 -64,233 Alto Rio Santa Maria, Depto Oran, Salta Salta Argentina
MACN 30702 Lepidocolaptes angustirostris -23,283 -64,233 Alto Rio Santa Maria, Depto Oran, Salta Salta Argentina
MACN 7202 (160q) Lepidocolaptes angustirostris -32,617 -62,700 Belleville, Cordoba Córdoba Argentina
MACN 64666 Lepidocolaptes angustirostris -25,450 -57,580 Bouvier, Pilcomayo, Formosa Formosa Argentina
MZUSP 3878 Lepidocolaptes angustirostris -36,000 -60,000 Buenos Aires Buenos Aires Argentina
MACN 61663 Lepidocolaptes angustirostris -27,367 -59,087 Camino A Maria Sara, 3 Km W Rn. 11, San Fernando, Chaco Argentina Chaco
94
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 62369 Lepidocolaptes angustirostris -27,283 -58,617 Camino Col. Benitez, Isla Cerrito, San Fernando, Chaco Chaco Argentina
MACN 59647 Lepidocolaptes angustirostris -29,983 -59,317 Campo Romero, Capital, Corrientes Corrientes Argentina
MACN 59778 Lepidocolaptes angustirostris -29,983 -59,317 Campo Romero, Capital, Corrientes Corrientes Argentina
MACN 66318 Lepidocolaptes angustirostris -36,617 -64,283 Campus Unlp, Santa Rosa, La Pampa La Pampa Argentina
MACN 66339 Lepidocolaptes angustirostris -36,617 -64,283 Campus Unlp, Santa Rosa, La Pampa La Pampa Argentina
MACN 66340 Lepidocolaptes angustirostris -36,617 -64,283 Campus Unlp, Santa Rosa, La Pampa La Pampa Argentina
MACN 62251 Lepidocolaptes angustirostris -27,500 -58,567 Cañada Ipacu, San Cosme, Corrientes Corrientes Argentina
MACN 56554 Lepidocolaptes angustirostris -27,567 -58,683 Caprim, San Cayetano, Capital, Corrientes Corrientes Argentina
MACN 56821 Lepidocolaptes angustirostris -27,567 -58,683 Caprim, San Cayetano, Capital, Corrientes Corrientes Argentina
MACN 56993 Lepidocolaptes angustirostris -27,567 -58,683 Caprim, San Cayetano, Capital, Corrientes Corrientes Argentina
MACN 56995 Lepidocolaptes angustirostris -27,567 -58,683 Caprim, San Cayetano, Capital, Corrientes Corrientes Argentina
MACN 58799 Lepidocolaptes angustirostris -27,567 -58,683 Caprim, San Cayetano, Capital, Corrientes Corrientes Argentina
MACN 33962 Lepidocolaptes angustirostris -28,467 -65,783 Catamarca, Alrededores De La Ciudad Catamarca Argentina
MACN 7719 Lepidocolaptes angustirostris NA NA Chaco, Salfene Chaco Argentina
MACN 6245a Lepidocolaptes angustirostris NA NA Col. Nascias Santa Fe Santa Fe Argentina
MACN 56145 Lepidocolaptes angustirostris -27,388 -58,931 Colonia Rio Tragadero, Dto. San Fernando, Chaco Chaco Argentina
MACN 9647 (160 n) Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 8914 (160 L) Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
95
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 160 K Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 160 J Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 160g Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23231 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23232 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23233 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23234 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23235 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23236 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23236 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23237 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23238 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23239 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23240 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23241 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23242 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23243 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23244 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
96
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 23245 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23246 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23247 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23248 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23249 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23250 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23251 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23252 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23253 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23254 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23255 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23256 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 23257 Lepidocolaptes angustirostris -27,333 -63,583 Concepción, Tucumán Tucumán Argentina
MACN 3965a Lepidocolaptes angustirostris -36,017 -64,600 Conhello, La Pampa La Pampa Argentina
MACN 64667 Lepidocolaptes angustirostris NA NA Cordoba Córdoba Argentina
MACN 56252 Lepidocolaptes angustirostris -30,717 -64,733 Cruz Del Eje, Cordoba Córdoba Argentina
MACN 46623 Lepidocolaptes angustirostris -28,667 -56,283 Cuay Grande, Corrientes Corrientes Argentina
MACN 46627 Lepidocolaptes angustirostris -28,667 -56,283 Cuay Grande, Corrientes Corrientes Argentina
97
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 46630 Lepidocolaptes angustirostris -28,667 -56,283 Cuay Grande, Corrientes Corrientes Argentina
MACN 46631 Lepidocolaptes angustirostris -28,667 -56,283 Cuay Grande, Corrientes Corrientes Argentina
MACN 30628 Lepidocolaptes angustirostris -23,550 -64,417 El Bananal, Urundel?, Salta Salta Argentina
MACN 61007 Lepidocolaptes angustirostris -27,533 -59,017 El Palmar, San Fernando, Chaco Chaco Argentina
MZUSP 31797 Lepidocolaptes angustirostris -26,800 -65,250 El Saladillo, Tucuman Tucumán Argentina
MACN 1342a Lepidocolaptes angustirostris -33,400 -58,617 Entre Rios, Gualeguay Entre Rios Argentina
MACN 39856 Lepidocolaptes angustirostris -33,400 -58,617 Entre Rios, Gualeguay, Es. La Calera Entre Rios Argentina
MACN 39857 Lepidocolaptes angustirostris -33,400 -58,617 Entre Rios, Gualeguay, Es. La Calera Entre Rios Argentina
MACN 39858 Lepidocolaptes angustirostris -33,400 -58,617 Entre Rios, Gualeguay, Es. La Calera Entre Rios Argentina
MACN 43656 Lepidocolaptes angustirostris -33,400 -58,617 Entre Rios, Gualeguay, Es. La Calera Entre Rios Argentina
MACN 43658 Lepidocolaptes angustirostris -33,400 -58,617 Entre Rios, Gualeguay, Es. La Calera Entre Rios Argentina
MACN 43477 Lepidocolaptes angustirostris -31,133 -59,767 Entre Rios, Santa Helena, Es. Viscacheras Entre Rios Argentina
MACN 43478 Lepidocolaptes angustirostris -31,133 -59,767 Entre Rios, Santa Helena, Es. Viscacheras Entre Rios Argentina
MACN 43657 Lepidocolaptes angustirostris -31,133 -59,767 Entre Rios, Santa Helena, Es. Viscacheras Entre Rios Argentina
MACN 43659 Lepidocolaptes angustirostris -31,133 -59,767 Entre Rios, Santa Helena, Es. Viscacheras Entre Rios Argentina
MACN 160 Y Lepidocolaptes angustirostris -35,000 -65,250 Es. El Bosque, San Luis, Nueva Galia San Luis Argentina
MACN 160u Lepidocolaptes angustirostris -35,000 -65,250 Es. El Bosque, San Luis, Nueva Galia San Luis Argentina
MACN 46624 Lepidocolaptes angustirostris -28,650 -57,417 Es. El Socorro, Compañia Pellegrini, Corrientes Corrientes Argentina
98
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 46625 Lepidocolaptes angustirostris -28,650 -57,417 Es. El Socorro, Compañia Pellegrini, Corrientes Corrientes Argentina
MACN 46629 Lepidocolaptes angustirostris -28,650 -57,417 Es. El Socorro, Compañia Pellegrini, Corrientes Corrientes Argentina
MACN 44252 Lepidocolaptes angustirostris -27,333 -58,000 Es. Tucyuli (Tuyutí?), Corrientes Corrientes Argentina
MACN 44253 Lepidocolaptes angustirostris -27,333 -58,000 Es. Tucyuli (Tuyutí?), Corrientes Corrientes Argentina
MACN 44257 Lepidocolaptes angustirostris -27,333 -58,000 Es. Tucyuli (Tuyutí?), Corrientes Corrientes Argentina
MACN 44261 Lepidocolaptes angustirostris -27,333 -58,000 Es. Tucyuli (Tuyutí?), Corrientes Corrientes Argentina
MACN 44263 Lepidocolaptes angustirostris -27,333 -58,000 Es. Tucyuli (Tuyutí?), Corrientes Corrientes Argentina
MACN 44264 Lepidocolaptes angustirostris -27,333 -58,000 Es. Tucyuli (Tuyutí?), Corrientes Corrientes Argentina
MACN 44265 Lepidocolaptes angustirostris -27,333 -58,000 Es. Tucyuli (Tuyutí?), Corrientes Corrientes Argentina
MACN 44267 Lepidocolaptes angustirostris -27,333 -58,000 Es. Tucyuli (Tuyutí?), Corrientes Corrientes Argentina
MACN 44260 Lepidocolaptes angustirostris -27,333 -58,000 Es. Tucyuli, Corrientes Corrientes Argentina
MACN 65819 Lepidocolaptes angustirostris -36,667 -64,350 Estancia La Florida, Se Suan Toro, Toay, La Pampa La Pampa Argentina
MACN 65822 Lepidocolaptes angustirostris -36,667 -64,350 Estancia La Florida, Se Suan Toro, Toay, La Pampa La Pampa Argentina
MACN 56948 Lepidocolaptes angustirostris -29,983 -59,317 Estancia Romero, Capital, Corrientes Corrientes Argentina
MACN 65862 Lepidocolaptes angustirostris -27,567 -58,683 Estero Valenzuela, 7 Km Al Este De San Cayetano, Corrientes Argentina Capital, Corrientes
MACN 68016 Lepidocolaptes angustirostris -27,567 -58,683 Estero Valenzuela, 7 Km Al Este De San Cayetano, Corrientes Argentina Capital, Corrientes
MACN 59467 Lepidocolaptes angustirostris -27,567 -58,683 Estero Valenzuela, Capital, Corrientes Corrientes Argentina
99
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 29824 Lepidocolaptes angustirostris -28,033 -61,500 Gato Colorado, El Tostado, Santa Fe Santa Fe Argentina
MACN 64665 Lepidocolaptes angustirostris NA NA Geral. Belgrano, San Luis San Luis Argentina
MACN 217A Lepidocolaptes angustirostris -33,017 -59,333 Gualeguaychu, Entre Rios Entre Rios Argentina
MACN 1342a ?? Lepidocolaptes angustirostris -33,017 -59,333 Gualeguaychu, Entre Rios Entre Rios Argentina
MACN 794A Lepidocolaptes angustirostris -24,217 -57,850 Guerrero, Jujuy Jujuy Argentina
MACN 794A Lepidocolaptes angustirostris -24,217 -57,850 Guerrero, Jujuy Jujuy Argentina
MACN 46628 Lepidocolaptes angustirostris -27,600 -56,683 Ituzaingo, Corrientes Corrientes Argentina
MACN 7719 (160 h) Lepidocolaptes angustirostris NA NA Jujuy Oriental Jujuy Argentina
MACN 4231a Lepidocolaptes angustirostris NA NA La Pampa, Juan Goro La Pampa Argentina
MACN 27984 Lepidocolaptes angustirostris -36,183 -65,250 La Pampa, Loventuel La Pampa Argentina
MZUSP 18 Lepidocolaptes angustirostris -34,917 -57,950 La Plata Buenos Aires Argentina
MACN 4202 (160A) Lepidocolaptes angustirostris -34,917 -57,950 La Plata, Buenos Aires Buenos Aires Argentina
MACN 4202 (160B) Lepidocolaptes angustirostris -34,917 -57,950 La Plata, Buenos Aires Buenos Aires Argentina
MACN 1989a Lepidocolaptes angustirostris -29,300 -67,600 La Rioja, Sañogasta La Rioja Argentina
MACN 57689 Lepidocolaptes angustirostris -28,480 -58,980 Lag. Paira, B. Lomas, Capital, Corrientes Corrientes Argentina
MACN 55642 Lepidocolaptes angustirostris -28,480 -58,980 Laguna Paisa, Barrio Lomas, Capital, Corrientes Corrientes Argentina
MACN 56175 Lepidocolaptes angustirostris -28,480 -58,980 Laguna Paisa, Barrio Lomas, Capital, Corrientes Corrientes Argentina
MACN 56368 Lepidocolaptes angustirostris -28,480 -58,980 Laguna Paisa, Barrio Lomas, Capital, Corrientes Corrientes Argentina
100
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 31794 Lepidocolaptes angustirostris -26,800 -65,250 Las Cañitas, Tucuman Tucumán Argentina
MZUSP 31795 Lepidocolaptes angustirostris -26,800 -65,250 Las Cañitas, Tucuman Tucumán Argentina
MZUSP 31796 Lepidocolaptes angustirostris -26,800 -65,250 Las Cañitas, Tucuman Tucumán Argentina
MACN 55639 Lepidocolaptes angustirostris -28,480 -58,980 Las Lomas, Capital, Corrientes Corrientes Argentina
MACN 2248a Lepidocolaptes angustirostris -24,700 -60,600 Las Lomitas, Formosa Formosa Argentina
MACN 8578 (160 V) Lepidocolaptes angustirostris -34,867 -57,883 Los C(T?)Alas, La Plata, Buenos Aires Buenos Aires Argentina
MACN 429A Lepidocolaptes angustirostris -34,867 -57,883 Los C(T?)Alas, La Plata, Buenos Aires Buenos Aires Argentina
MACN 29823 Lepidocolaptes angustirostris -29,233 -61,767 Los Guasunchos, El Tostado, Santa Fe Santa Fe Argentina
MACN 62546 Lepidocolaptes angustirostris -26,200 -60,250 Lote 23, Campo Milan, 40 Km Norte De Saenz Peña, Chaco Argentina Maipu, Chaco
MACN 62325 Lepidocolaptes angustirostris -25,016 -61,508 Lote 42, Campo Pibernus, El Asustado, C-56, Guemes, Chaco Argentina Chaco
MACN 54336 Lepidocolaptes angustirostris -34,567 -59,117 Lujan, Buenos Aires Buenos Aires Argentina
MACN 2054a Lepidocolaptes angustirostris NA NA MACNhado, Tucumán Tucumán Argentina
MACN 44254 Lepidocolaptes angustirostris -29,200 -58,100 Mercedes, Corrientes Corrientes Argentina
MACN 44255 Lepidocolaptes angustirostris -29,200 -58,100 Mercedes, Corrientes Corrientes Argentina
MACN 44256 Lepidocolaptes angustirostris -29,200 -58,100 Mercedes, Corrientes Corrientes Argentina
MACN 44258 Lepidocolaptes angustirostris -29,200 -58,100 Mercedes, Corrientes Corrientes Argentina
MACN 44259 Lepidocolaptes angustirostris -29,200 -58,100 Mercedes, Corrientes Corrientes Argentina
101
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 44266 Lepidocolaptes angustirostris -29,200 -58,100 Mercedes, Corrientes Corrientes Argentina
MACN 44268 Lepidocolaptes angustirostris -29,200 -58,100 Mercedes, Corrientes Corrientes Argentina
MACN 57303 Lepidocolaptes angustirostris -24,917 -61,483 Mision Nueva Pompeya, Guemes, Chaco Chaco Argentina
MACN 60093 Lepidocolaptes angustirostris -24,917 -61,483 Mision Nueva Pompeya, Guemes, Chaco Chaco Argentina
MACN 60296 Lepidocolaptes angustirostris -24,917 -61,483 Mision Nueva Pompeya, Guemes, Chaco Chaco Argentina
MACN 60382 Lepidocolaptes angustirostris -24,917 -61,483 Mision Nueva Pompeya, Guemes, Chaco Chaco Argentina
MACN 8633 (160c) Lepidocolaptes angustirostris NA NA Monte Toro, Tucumán Tucumán Argentina
MACN 54522 Lepidocolaptes angustirostris -34,050 -67,967 Nãcuman, Santa Rosa, Mendoza Mendoza Argentina
MACN 160 E Lepidocolaptes angustirostris -28,467 -59,367 Ocampo, Chaco Austral Chaco Argentina
MACN 160 K Lepidocolaptes angustirostris -28,467 -59,367 Ocampo, Chaco Austral Chaco Argentina
MACN 160 i Lepidocolaptes angustirostris -28,467 -59,367 Ocampo, Chaco Austral, Santa Fe Santa Fe? Argentina
MACN 63606 Lepidocolaptes angustirostris -26,233 -58,617 Paraje Ñandhy Vera, Laishi, Formosa Formosa Argentina
MACN 63618 Lepidocolaptes angustirostris -26,233 -58,617 Paraje Ñandhy Vera, Laishi, Formosa Formosa Argentina
MACN 63620 Lepidocolaptes angustirostris -26,233 -58,617 Paraje Ñandhy Vera, Laishi, Formosa Formosa Argentina
MACN 63662 Lepidocolaptes angustirostris -26,233 -58,617 Paraje Ñandhy Vera, Laishi, Formosa Formosa Argentina
MACN 64406 Lepidocolaptes angustirostris -26,233 -58,617 Paraje Ñandhy Vera, Laishi, Formosa Formosa Argentina
MACN 64413 Lepidocolaptes angustirostris -26,233 -58,617 Paraje Ñandhy Vera, Laishi, Formosa Formosa Argentina
MACN 64414 Lepidocolaptes angustirostris -26,233 -58,617 Paraje Ñandhy Vera, Laishi, Formosa Formosa Argentina
102
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 337A Lepidocolaptes angustirostris -31,733 -60,533 Paraná, Entre Rios Entre Rios Argentina
MACN 52423 Lepidocolaptes angustirostris -24,700 -64,633 Parque Nacional El Rey, Salta Salta Argentina
MACN 58191 Lepidocolaptes angustirostris -30,000 -59,517 Paso La Llama, Libertades, Esquina, Corrientes Corrientes Argentina
MACN 160f Lepidocolaptes angustirostris -23,317 -64,217 Pichamal, Oran, Salta Salta Argentina
MACN 9631 (160 S) Lepidocolaptes angustirostris -34,783 -58,183 Platanos, Buenos Aires Buenos Aires Argentina
MACN 9631 Lepidocolaptes angustirostris -34,783 -58,183 Platanos, Buenos Aires Buenos Aires Argentina
MACN 9631 Lepidocolaptes angustirostris -34,783 -58,183 Platanos, Buenos Aires Buenos Aires Argentina
MACN 57554 Lepidocolaptes angustirostris -25,033 -64,233 Pozo De Los Suris, Guemes, Chaco Chaco Argentina
MACN 64508 Lepidocolaptes angustirostris -24,550 -60,830 Pozo De Navagan, Patiño, Formosa Formosa Argentina
MACN 64509 Lepidocolaptes angustirostris -24,550 -60,830 Pozo De Navagan, Patiño, Formosa Formosa Argentina
MACN 64690 Lepidocolaptes angustirostris -32,650 -66,467 Pozo Negro, Villa General Roca, Geral. Belgrano, San San Luis Argentina Luis
MACN 710A Lepidocolaptes angustirostris -31,383 -60,100 Pueblo Brugo, Entre Rios Entre Rios Argentina
MACN 56362 Lepidocolaptes angustirostris -27,250 -58,967 Puente San Pedro, 1ro De Mayo, Chaco Chaco Argentina
MZUSP 9 Lepidocolaptes angustirostris -34,817 -57,983 Punta Lara, Buenos Aires Buenos Aires Argentina
MACN 9563(160z?) Lepidocolaptes angustirostris -34,733 -58,267 Quilmes, Buenos Aires Buenos Aires Argentina
MACN 9291 (160 v) Lepidocolaptes angustirostris -34,733 -58,267 Quilmes, Buenos Aires Buenos Aires Argentina
MACN 160(p? S?) Lepidocolaptes angustirostris -34,733 -58,267 Quilmes, Buenos Aires Buenos Aires Argentina
103
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 160 W Lepidocolaptes angustirostris -34,733 -58,267 Quilmes, Buenos Aires Buenos Aires Argentina
MACN 8914 (160 J) Lepidocolaptes angustirostris -27,450 -58,983 Resistencia, Chaco Chaco Argentina
MACN 63869 Lepidocolaptes angustirostris -27,433 -56,250 Rincon Del Ombu, Ituzaingo, Corrientes Corrientes Argentina
MACN 333A Lepidocolaptes angustirostris -27,417 -58,833 Rio Antequera, Chaco (frente A Corrientes) Chaco Argentina
MACN 1516a Lepidocolaptes angustirostris -34,200 -58,300 Rio Uruguay, Entre Rios Entre Rios Argentina
MACN 9631 Lepidocolaptes angustirostris NA NA Salta - Parana Salta - Parana Argentina
MACN 41065 Lepidocolaptes angustirostris NA NA Salta, Depto Metan, Col. Colorado Salta Argentina
MACN 44262 Lepidocolaptes angustirostris -27,750 -55,900 San Carlos, Corrientes Corrientes Argentina
MACN 40444 Lepidocolaptes angustirostris -28,133 -58,767 San Lorenzo, Corrientes Corrientes Argentina
MACN 46626 Lepidocolaptes angustirostris -29,017 -56,483 Santa Ana, Alvear, Corrientes Corrientes Argentina
MACN 43112 Lepidocolaptes angustirostris -27,450 -58,667 Santa Ana, Depto. San Cosme, Corrientes Corrientes Argentina
MACN 235A Lepidocolaptes angustirostris -27,367 -55,567 Santa Ana, Misiones Misiones Argentina
MACN 4320 (160 m) Lepidocolaptes angustirostris -27,467 -65,683 Santa Ana, Tucumán Tucumán Argentina
MACN 6244a Lepidocolaptes angustirostris NA NA Santa Fe Santa Fe Argentina
MACN 52719 Lepidocolaptes angustirostris -29,233 -61,767 Santa Fe, Tostado, Es. El Orden Santa Fe Argentina
MACN 39859 Lepidocolaptes angustirostris -30,083 -58,767 Sauce, Corrientes Corrientes Argentina
MACN 461A Lepidocolaptes angustirostris -32,600 -66,133 Sierra San Francisco, San Luis San Luis Argentina
MACN 160 A Lepidocolaptes angustirostris NA NA Simoral, Tucuman Tucumán Argentina
104
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 8148 (160f) Lepidocolaptes angustirostris -27,933 -63,450 Suncho? Corral, Estero Santiago del Estero Argentina
MACN 8148 (160 e) Lepidocolaptes angustirostris -27,933 -63,450 Suncho? Corral, Estero Santiago del Estero Argentina
MACN 9451 (160 O) Lepidocolaptes angustirostris -26,600 -65,300 Tapia, Tucumán Tucumán Argentina
MACN 160 B Lepidocolaptes angustirostris -26,600 -65,300 Tapia, Tucumán Tucumán Argentina
MACN 3827a Lepidocolaptes angustirostris -34,417 -58,567 Tigre, Buenos Aires Buenos Aires Argentina
MACN 8428 (160i) Lepidocolaptes angustirostris NA NA Tucuman Tucumán Argentina
MACN 160 H Lepidocolaptes angustirostris NA NA Tucuman Tucumán Argentina
MACN 21304 (2155a) Lepidocolaptes angustirostris NA NA Tucumán Tucumán Argentina
MACN 6318a Lepidocolaptes angustirostris -31,233 -64,317 Unquillo, Cordoba Córdoba Argentina
MACN 2414a Lepidocolaptes angustirostris -27,567 -60,533 Urien, Chaco Chaco Argentina
MACN 43113 Lepidocolaptes angustirostris -29,467 -60,217 Vera, Santa Fe Santa Fe Argentina
MACN 52551 Lepidocolaptes angustirostris -33,233 -60,333 Villa Constitucion, Santa Fe, Islar Rio Parana Santa Fe Argentina
MACN 52552 Lepidocolaptes angustirostris -33,233 -60,333 Villa Constitucion, Santa Fe, Islar Rio Parana Santa Fe Argentina
MACN 55711 Lepidocolaptes angustirostris -24,478 -60,552 Villa Gral. Urquiza, Patiño, Formosa Formosa Argentina
MACN 8428 (160d) Lepidocolaptes angustirostris -26,483 -65,367 Vipos, Tucumán Tucumán Argentina
MACN 57304 Lepidocolaptes angustirostris -24,683 -61,417 Wichi, Guemes, Chaco Chaco Argentina
MACN 57305 Lepidocolaptes angustirostris -24,683 -61,417 Wichi, Guemes, Chaco Chaco Argentina
MACN 35254 Lepidocolaptes angustirostris -34,350 -58,867 Zelaya, Buenos Aires Buenos Aires Argentina
105
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 37563 Lepidocolaptes angustirostris -17,900 -64,483 Comarapa, Santa Cruz Santa Cruz Bolivia
MACN 72555 Lepidocolaptes angustirostris -17,433 -61,167 Yabaré, Prov. Chiquitos, Santa Cruz Santa Cruz Bolivia
MACN 72572 Lepidocolaptes angustirostris -17,433 -61,167 Yabaré, Prov. Chiquitos, Santa Cruz Santa Cruz Bolivia
MACN 72590 Lepidocolaptes angustirostris -17,433 -61,167 Yabaré, Prov. Chiquitos, Santa Cruz Santa Cruz Bolivia
MZUSP 38152 Lepidocolaptes angustirostris -6,117 -45,150 Aldeia Do Ponto, Maranhao Maranhão Brasil
MZUSP 38153 Lepidocolaptes angustirostris -6,117 -45,150 Aldeia Do Ponto, Maranhao Maranhão Brasil
MZUSP 38155 Lepidocolaptes angustirostris -6,117 -45,150 Aldeia Do Ponto, Maranhao Maranhão Brasil
MZUSP 38156 Lepidocolaptes angustirostris -6,117 -45,150 Aldeia Do Ponto, Maranhao Maranhão Brasil
MZUSP 60186 Lepidocolaptes angustirostris -21,433 -45,950 Alfenas, Minas Gerais Minas Gerais Brasil
MZUSP 60187 Lepidocolaptes angustirostris -21,433 -45,950 Alfenas, Minas Gerais Minas Gerais Brasil
MZUSP 60188 Lepidocolaptes angustirostris -21,433 -45,950 Alfenas, Minas Gerais Minas Gerais Brasil
MZUSP 60640 Lepidocolaptes angustirostris -21,433 -45,950 Alfenas, Minas Gerais Minas Gerais Brasil
MPEG 43455 Lepidocolaptes angustirostris -2,750 -44,333 Alto Rio Parnaíba, Estiva Maranhão Brasil
MPEG 43456 Lepidocolaptes angustirostris -2,750 -44,333 Alto Rio Parnaíba, Estiva Maranhão Brasil
MPEG 43457 Lepidocolaptes angustirostris -2,750 -44,333 Alto Rio Parnaíba, Estiva Maranhão Brasil
MPEG 43458 Lepidocolaptes angustirostris -2,750 -44,333 Alto Rio Parnaíba, Estiva Maranhão Brasil
MPEG 43459 Lepidocolaptes angustirostris -2,750 -44,333 Alto Rio Parnaíba, Estiva Maranhão Brasil
MPEG 43460 Lepidocolaptes angustirostris -2,750 -44,333 Alto Rio Parnaíba, Estiva Maranhão Brasil
106
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MPEG 40848 Lepidocolaptes angustirostris -5,100 -47,250 Amarante, Fazenda Centro Maranhão Brasil
MZUSP 54497 Lepidocolaptes angustirostris -22,800 -48,117 Anhembí, São paulo São Paulo Brasil
MZUSP 54498 Lepidocolaptes angustirostris -22,800 -48,117 Anhembí, São paulo São Paulo Brasil
MZUSP 54499 Lepidocolaptes angustirostris -22,800 -48,117 Anhembí, São paulo São Paulo Brasil
MZUSP 54500 Lepidocolaptes angustirostris -22,800 -48,117 Anhembí, São paulo São Paulo Brasil
MZUSP 12594 Lepidocolaptes angustirostris -20,467 -55,800 Aquídauana, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 51864 Lepidocolaptes angustirostris -15,917 -52,250 Aragarças, Goias Goiás Brasil
MZUSP 74792 Lepidocolaptes angustirostris -14,450 -56,217 Arinos, Mato Grosso Mato Grosso Brasil
MZUSP 38154 Lepidocolaptes angustirostris -5,500 -45,250 Atolador, Chapada Do Ponto, Maranhao Maranhão Brasil
MZUSP 34648 Lepidocolaptes angustirostris -21,950 -44,883 Baependi, Minas Gerais Minas Gerais Brasil
MPEG 46373 Lepidocolaptes angustirostris -12,983 -38,517 Bahia Bahia Brasil
MZUSP 73873 Lepidocolaptes angustirostris -17,617 -49,583 Bela-Vista, Goiás Goiás Brasil
MPEG 68196 Lepidocolaptes angustirostris -5,433 -42,317 Beneditinos, Fazenda Santa Teresa Piauí Brasil
MZUSP 14674 Lepidocolaptes angustirostris -2,433 -54,700 Boca Rio Tapajós, santarém, Pará Pará Brasil
MZUSP 14675 Lepidocolaptes angustirostris -2,433 -54,700 Boca Rio Tapajós, santarém, Pará Pará Brasil
MPEG 72161 Lepidocolaptes angustirostris -6,950 -41,283 Bocaina, Comunidade Salseiro Piauí Brasil
MPEG 72162 Lepidocolaptes angustirostris -6,950 -41,283 Bocaina, Comunidade Salseiro Piauí Brasil
MPEG 51820 Lepidocolaptes angustirostris -21,267 -56,667 Bonito, Fazenda Formoso Mato Grosso do Sul Brasil
107
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MPEG 51821 Lepidocolaptes angustirostris -21,267 -56,667 Bonito, Fazenda Formoso Mato Grosso do Sul Brasil
MPEG 51822 Lepidocolaptes angustirostris -21,267 -56,667 Bonito, Fazenda Formoso Mato Grosso do Sul Brasil
MPEG 51823 Lepidocolaptes angustirostris -21,267 -56,667 Bonito, Fazenda Formoso Mato Grosso do Sul Brasil
MPEG 51824 Lepidocolaptes angustirostris -21,267 -56,667 Bonito, Fazenda Formoso Mato Grosso do Sul Brasil
MPEG 51818 Lepidocolaptes angustirostris -20,867 -56,917 Bonito, Fazenda Pitangueiras Mato Grosso do Sul Brasil
MPEG 51819 Lepidocolaptes angustirostris -20,867 -56,917 Bonito, Fazenda Pitangueiras Mato Grosso do Sul Brasil
MZUSP 51865 Lepidocolaptes angustirostris -15,783 -47,917 Brasilia, Df DF Brasil
MZUSP 40922 Lepidocolaptes angustirostris -10,717 -43,650 Buritirama, Bahia Bahia Brasil
MZUSP 33263 Lepidocolaptes angustirostris -17,750 -48,633 Caldas Novas, Goias Goiás Brasil
MZUSP 68990 Lepidocolaptes angustirostris -17,750 -48,633 Caldas Novas, Goias Goiás Brasil
MZUSP 94628 Lepidocolaptes angustirostris -13,915 -48,504 Campinaçu Goiás Brasil
MZUSP 12282 Lepidocolaptes angustirostris -20,450 -54,617 Campo Grande, Mato Grosso Mato Grosso Brasil
MZUSP 15862 Lepidocolaptes angustirostris -13,850 -46,950 Cana Brava, Goias Goiás Brasil
MZUSP 15863 Lepidocolaptes angustirostris -13,850 -46,950 Cana Brava, Goias Goiás Brasil
MPEG 76053 Lepidocolaptes angustirostris -8,110 -42,944 Canto De Buriti, Pn Serra Das Confusões Piauí Brasil
MPEG 75510 Lepidocolaptes angustirostris -9,279 -43,330 Caracol, Pn Serra Das Confusões, Projeto Cajugaia Piauí Brasil
MPEG 68192 Lepidocolaptes angustirostris -5,217 -41,683 Castelo Do Piauí, Fazenda Bonito Piauí Brasil
MPEG 68205 Lepidocolaptes angustirostris -5,217 -41,683 Castelo Do Piauí, Fazenda Bonito Piauí Brasil
108
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MPEG 68206 Lepidocolaptes angustirostris -5,217 -41,683 Castelo Do Piauí, Fazenda Bonito Piauí Brasil
MPEG 68207 Lepidocolaptes angustirostris -5,217 -41,683 Castelo Do Piauí, Fazenda Bonito Piauí Brasil
MPEG 68208 Lepidocolaptes angustirostris -5,217 -41,683 Castelo Do Piauí, Fazenda Bonito Piauí Brasil
MPEG 68209 Lepidocolaptes angustirostris -5,217 -41,683 Castelo Do Piauí, Fazenda Bonito Piauí Brasil
MPEG 68210 Lepidocolaptes angustirostris -5,217 -41,683 Castelo Do Piauí, Fazenda Bonito Piauí Brasil
MPEG 38906 Lepidocolaptes angustirostris -15,433 -55,750 Chapada Dos Guimarães, Escola Buriti Mato Grosso Brasil
MPEG 38907 Lepidocolaptes angustirostris -15,433 -55,750 Chapada Dos Guimarães, Escola Buriti Mato Grosso Brasil
MZUSP 32403 Lepidocolaptes angustirostris -11,750 -50,733 Chavantina, Rio Das Mortes, Mato Grosso Mato Grosso Brasil
MZUSP 32404 Lepidocolaptes angustirostris -11,750 -50,733 Chavantina, Rio Das Mortes, Mato Grosso Mato Grosso Brasil
MZUSP 8524 Lepidocolaptes angustirostris -11,083 -43,167 Cidade Da Barra, Bahia Bahia Brasil
MZUSP 39712 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 39713 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 39714 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 39715 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 39716 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 39717 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 39718 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 39719 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
109
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 39720 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 39721 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 39722 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 39723 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 39724 Lepidocolaptes angustirostris -7,017 -37,967 Coremas, Paraiba Paraiba Brasil
MZUSP 10035 Lepidocolaptes angustirostris -19,017 -57,650 Corumbá, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 10036 Lepidocolaptes angustirostris -19,017 -57,650 Corumbá, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 10037 Lepidocolaptes angustirostris -19,017 -57,650 Corumbá, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 29884 Lepidocolaptes angustirostris -19,017 -57,650 Corumbá, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 29885 Lepidocolaptes angustirostris -19,017 -57,650 Corumbá, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 29887 Lepidocolaptes angustirostris -19,017 -57,650 Corumbá, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 29888 Lepidocolaptes angustirostris -19,017 -57,650 Corumbá, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 29889 Lepidocolaptes angustirostris -19,017 -57,650 Corumbá, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 29890 Lepidocolaptes angustirostris -19,017 -57,650 Corumbá, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 29891 Lepidocolaptes angustirostris -19,017 -57,650 Corumbá, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 29893 Lepidocolaptes angustirostris -19,017 -57,650 Corumbá, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 29876 Lepidocolaptes angustirostris -15,583 -56,083 Cuiabá (Margem Direita Rio); Mato Grosso Mato Grosso Brasil
MZUSP 29892 Lepidocolaptes angustirostris -15,583 -56,083 Cuiabá (Margem Direito Rio); Mato Grosso Mato Grosso Brasil
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Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 29883 Lepidocolaptes angustirostris -15,583 -56,083 Cuiabá (Margem Esquerda Rio); Mato Grosso Mato Grosso Brasil
MZUSP 35149 Lepidocolaptes angustirostris -14,500 -51,000 Dumbá, Mato Grosso Mato Grosso Brasil
MZUSP 75301 Lepidocolaptes angustirostris -8,867 -44,967 EE Urucui-UNA, Piaui Piauí Brasil
MZUSP 75302 Lepidocolaptes angustirostris -8,867 -44,967 EE Urucui-UNA, Piaui Piauí Brasil
MZUSP 75303 Lepidocolaptes angustirostris -8,867 -44,967 EE Urucui-UNA, Piaui Piauí Brasil
MZUSP 75304 Lepidocolaptes angustirostris -8,867 -44,967 EE Urucui-UNA, Piaui Piauí Brasil
MPEG 68193 Lepidocolaptes angustirostris -5,967 -42,400 Elesbão Veloso, Fazenda Columba Piauí Brasil
MPEG 68194 Lepidocolaptes angustirostris -5,967 -42,400 Elesbão Veloso, Fazenda Columba Piauí Brasil
MZUSP 79639 Lepidocolaptes angustirostris -10,664 -46,808 ESEC Serra geral do Tocantins, Tocantins Tocantins Brasil
MZUSP 79640 Lepidocolaptes angustirostris -10,664 -46,808 ESEC Serra geral do Tocantins, Tocantins Tocantins Brasil
MZUSP 79641 Lepidocolaptes angustirostris -10,664 -46,808 ESEC Serra geral do Tocantins, Tocantins Tocantins Brasil
MZUSP 73772 Lepidocolaptes angustirostris -21,303 -52,830 Fazenda Barma??, Santa Rita Do Pardo, Mato Grosso Do Mato Grosso do Sul Brasil Sul
MZUSP 73773 Lepidocolaptes angustirostris -21,303 -52,830 Fazenda Barma??, Santa Rita Do Pardo, Mato Grosso Do Mato Grosso do Sul Brasil Sul
MZUSP 37775 Lepidocolaptes angustirostris -22,750 -48,150 Fazenda Barreiro Rico, Anhembi, São Paulo São Paulo Brasil
MZUSP 43213 Lepidocolaptes angustirostris -22,750 -48,150 Fazenda Barreiro Rico, Anhembi, São Paulo São Paulo Brasil
MZUSP 74553 Lepidocolaptes angustirostris -21,130 -56,470 Fazenda Beija-Flor, Margem Isquerdo Do Rio Sucurui, Mato Grosso do Sul Brasil Tres Lagoas, Mato Grosso Do Sul
111
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 38613 Lepidocolaptes angustirostris -21,267 -47,167 Fazenda Campininha, São Paulo São Paulo Brasil
MZUSP 63444 Lepidocolaptes angustirostris -8,290 -38,580 Fazenda Campos bons 38 km N. floresta, Pernambuco Pernambuco Brasil
MZUSP 63445 Lepidocolaptes angustirostris -8,290 -38,580 Fazenda Campos bons 38 km N. floresta, Pernambuco Pernambuco Brasil
MZUSP 78905 Lepidocolaptes angustirostris NA NA Fazenda Cantagalo, Jaiba, Mato Grosso Mato Grosso Brasil
MZUSP 78906 Lepidocolaptes angustirostris NA NA Fazenda Cantagalo, Jaiba, Mato Grosso Mato Grosso Brasil
MZUSP 80883 Lepidocolaptes angustirostris -10,710 -48,310 Fazenda da Da Serra, Porto Nacional, Tocantins Tocantins Brasil
MZUSP 81167 Lepidocolaptes angustirostris -10,710 -48,310 Fazenda Da Serra, Porto Nacional, Tocantins Tocantins Brasil
MZUSP 86264 Lepidocolaptes angustirostris -14,923 -40,727 Fazenda Do Marcelo, Vicinal, Bahia Bahia Brasil
MZUSP 97152 Lepidocolaptes angustirostris -9,783 -50,200 Fazenda Fartura, Barra das Princesas Pará Brasil
MZUSP 97173 Lepidocolaptes angustirostris -9,833 -50,367 Fazenda Fartura, Retiro 8 Pará Brasil
MZUSP 97207 Lepidocolaptes angustirostris -9,833 -50,367 Fazenda Fartura, Retiro 8 Pará Brasil
MZUSP 97208 Lepidocolaptes angustirostris -9,845 -50,291 Fazenda Fartura, Retiro 8 Pará Brasil
MZUSP 97209 Lepidocolaptes angustirostris -9,845 -50,291 Fazenda Fartura, Retiro 8 Pará Brasil
MZUSP 97210 Lepidocolaptes angustirostris -9,839 -50,284 Fazenda Fartura, Retiro 8 Pará Brasil
MZUSP 97228 Lepidocolaptes angustirostris -9,854 -50,339 Fazenda Fartura, Retiro 8 Pará Brasil
MZUSP 76073 Lepidocolaptes angustirostris -11,850 -48,617 Fazenda Funil, margem esquerdo Rio Tocantins, Peixe, Tocantins Brasil Tocantins
MZUSP 74549 Lepidocolaptes angustirostris -20,751 -51,678 Fazenda José Mendes, Margem Isquerdo Do Rio Mato Grosso do Sul Brasil Sucurui, Tres Lagoas, Mato Grosso Do Sul
112
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 74551 Lepidocolaptes angustirostris -20,751 -51,678 Fazenda José Mendes, Margem Isquerdo Do Rio Mato Grosso do Sul Brasil Sucurui, Tres Lagoas, Mato Grosso Do Sul
MZUSP 74552 Lepidocolaptes angustirostris -20,751 -51,678 Fazenda José Mendes, margem isquerdo do Rio Sucurui, Mato Grosso do Sul Brasil Tres Lagoas, Mato Grosso do Sul
MZUSP 73635 Lepidocolaptes angustirostris -22,500 -53,017 Fazenda Primavera, Bataiporã, Mato Grosso Do Sul Mato Grosso do Sul Brasil
MZUSP 73636 Lepidocolaptes angustirostris -22,500 -53,017 Fazenda Primavera, Bataiporã, Mato Grosso Do Sul Mato Grosso do Sul Brasil
MZUSP 73637 Lepidocolaptes angustirostris -22,500 -53,017 Fazenda Primavera, Bataiporã, Mato Grosso Do Sul Mato Grosso do Sul Brasil
MZUSP 73638 Lepidocolaptes angustirostris -22,500 -53,017 Fazenda Primavera, Bataiporã, Mato Grosso Do Sul Mato Grosso do Sul Brasil
MZUSP 73639 Lepidocolaptes angustirostris -22,500 -53,017 Fazenda Primavera, Bataiporã, Mato Grosso Do Sul Mato Grosso do Sul Brasil
MACN 64783 Lepidocolaptes angustirostris -17,750 -48,633 Fazenda Primavera, Caldas Novas, Goias, Brasil Goiás Brasil
MZUSP 76096 Lepidocolaptes angustirostris -11,267 -48,450 Fazenda Roma, margem direita Rio Tocantins, Santa Tocantins Brasil Rosa de Tocantins, Tocantins
MZUSP 53334 Lepidocolaptes angustirostris -23,083 -48,917 Fazenda Santa Tereza, avaré, São Paulo São Paulo Brasil
MZUSP 80425 Lepidocolaptes angustirostris -11,950 -48,850 Fazenda São Luís, Sucupira, Tocantins Tocantins Brasil
MZUSP 29101 Lepidocolaptes angustirostris -21,283 -47,300 Fazenda São Miguel, Cajurú, São Paulo São Paulo Brasil
MZUSP 80785 Lepidocolaptes angustirostris -12,191 -43,347 Fazenda Sto. Antônio, Muquém Do São Francisco, Bahia Bahia Brasil
MZUSP 81543 Lepidocolaptes angustirostris -12,191 -43,347 Fazenda Sto. Antônio, Muquém Do São Francisco, Bahia Bahia Brasil
MZUSP 26694 Lepidocolaptes angustirostris -17,217 -51,550 Fazenda Transvaal, Goias Goiás Brasil
MPEG 19278 Lepidocolaptes angustirostris -13,617 -48,900 Formosa Goiás Brasil
113
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 2697 Lepidocolaptes angustirostris -20,533 -47,400 Franca, São Paulo São Paulo Brasil
MZUSP 8026 Lepidocolaptes angustirostris -20,533 -47,400 Franca, São Paulo São Paulo Brasil
MZUSP 8067 Lepidocolaptes angustirostris -20,533 -47,400 Franca, São Paulo São Paulo Brasil
MZUSP 8069 Lepidocolaptes angustirostris -20,533 -47,400 Franca, São Paulo São Paulo Brasil
MZUSP 8070 Lepidocolaptes angustirostris -20,533 -47,400 Franca, São Paulo São Paulo Brasil
MZUSP 8071 Lepidocolaptes angustirostris -20,533 -47,400 Franca, São Paulo São Paulo Brasil
MZUSP 15052 Lepidocolaptes angustirostris -18,533 -49,600 Goiabeira, Goias Goiás Brasil
MZUSP 15053 Lepidocolaptes angustirostris -18,533 -49,600 Goiabeira, Goias Goiás Brasil
MPEG 14937 Lepidocolaptes angustirostris -16,383 -49,317 Goiânia Goiás Brasil
MPEG 19514 Lepidocolaptes angustirostris -16,383 -49,317 Goiânia Goiás Brasil
MPEG 19564 Lepidocolaptes angustirostris -16,383 -49,317 Goiânia Goiás Brasil
MPEG 21972 Lepidocolaptes angustirostris -16,383 -49,317 Goiânia Goiás Brasil
MPEG 22475 Lepidocolaptes angustirostris -16,383 -49,317 Goiânia Goiás Brasil
MACN 52081 Lepidocolaptes angustirostris -16,670 -49,270 Goiania, Goias Goiás Brasil
MZUSP 34059 Lepidocolaptes angustirostris -16,667 -49,267 Goiania, Goiás Goiás Brasil
MZUSP 51863 Lepidocolaptes angustirostris -16,667 -49,267 Goiania, Goiás Goiás Brasil
MZUSP 52656 Lepidocolaptes angustirostris -16,667 -49,267 Goiania, Goiás Goiás Brasil
MZUSP 68992 Lepidocolaptes angustirostris -16,667 -49,267 Goiania, Goiás Goiás Brasil
114
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 68993 Lepidocolaptes angustirostris -16,667 -49,267 Goiania, Goiás Goiás Brasil
MZUSP 68994 Lepidocolaptes angustirostris -16,667 -49,267 Goiania, Goiás Goiás Brasil
MZUSP 68995 Lepidocolaptes angustirostris -16,667 -49,267 Goiania, Goiás Goiás Brasil
MZUSP 68996 Lepidocolaptes angustirostris -16,667 -49,267 Goiania, Goiás Goiás Brasil
MZUSP 68997 Lepidocolaptes angustirostris -16,667 -49,267 Goiania, Goiás Goiás Brasil
MZUSP 68998 Lepidocolaptes angustirostris -16,667 -49,267 Goiania, Goiás Goiás Brasil
MZUSP 72379 Lepidocolaptes angustirostris -16,667 -49,267 Goiania, Goiás Goiás Brasil
MZUSP 72377 Lepidocolaptes angustirostris -16,496 -49,426 Goianira, Goiás Goiás Brasil
MZUSP 73870 Lepidocolaptes angustirostris -16,496 -49,426 Goianira, Goiás Goiás Brasil
MPEG 37684 Lepidocolaptes angustirostris -6,217 -46,117 Grajaú, Transmaranhão Km 36, Fazenda Canto Da Onça Maranhão Brasil
MPEG 37685 Lepidocolaptes angustirostris -6,217 -46,117 Grajaú, Transmaranhão Km 36, Fazenda Canto Da Onça Maranhão Brasil
MPEG 71427 Lepidocolaptes angustirostris -6,917 -43,617 Guadalupe, Fazenda São Pedro Piauí Brasil
MPEG 71428 Lepidocolaptes angustirostris -6,917 -43,617 Guadalupe, Fazenda São Pedro Piauí Brasil
MZUSP 68991 Lepidocolaptes angustirostris -16,966 -49,229 Hidrolândia, Goiás Goiás Brasil
MZUSP 73867 Lepidocolaptes angustirostris -16,966 -49,229 Hidrolândia, Goiás Goiás Brasil
MZUSP 73868 Lepidocolaptes angustirostris -16,966 -49,229 Hidrolândia, Goiás Goiás Brasil
MZUSP 73869 Lepidocolaptes angustirostris -16,966 -49,229 Hidrolândia, Goiás Goiás Brasil
MZUSP 73872 Lepidocolaptes angustirostris -16,966 -49,229 Hidrolândia, Goiás Goiás Brasil
115
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 73876 Lepidocolaptes angustirostris -16,966 -49,229 Hidrolândia, Goiás Goiás Brasil
MPEG 44853 Lepidocolaptes angustirostris -14,150 -46,617 Iaciara, Fazenda São Bernardo Goiás Brasil
MPEG 44854 Lepidocolaptes angustirostris -14,150 -46,617 Iaciara, Fazenda São Bernardo Goiás Brasil
MPEG 44855 Lepidocolaptes angustirostris -14,150 -46,617 Iaciara, Fazenda São Bernardo Goiás Brasil
MPEG 44856 Lepidocolaptes angustirostris -14,150 -46,617 Iaciara, Fazenda São Bernardo Goiás Brasil
MPEG 44857 Lepidocolaptes angustirostris -14,150 -46,617 Iaciara, Fazenda São Bernardo Goiás Brasil
MPEG 44858 Lepidocolaptes angustirostris -14,150 -46,617 Iaciara, Fazenda São Bernardo Goiás Brasil
MPEG 44859 Lepidocolaptes angustirostris -14,150 -46,617 Iaciara, Fazenda São Bernardo Goiás Brasil
MPEG 44860 Lepidocolaptes angustirostris -14,150 -46,617 Iaciara, Fazenda São Bernardo Goiás Brasil
MPEG 44861 Lepidocolaptes angustirostris -14,150 -46,617 Iaciara, Fazenda São Bernardo Goiás Brasil
MPEG 51139 Lepidocolaptes angustirostris -12,583 -40,833 Ibiquera, Fazenda Bananeira Bahia Brasil
MZUSP 41663 Lepidocolaptes angustirostris -3,050 -39,633 Icarai, Mosquito, Ceará Ceará Brasil
MPEG 15765 Lepidocolaptes angustirostris -5,450 -47,500 Imperatriz Maranhão Brasil
MPEG 19699 Lepidocolaptes angustirostris -16,367 -49,500 Inhumas Goiás Brasil
MPEG 19700 Lepidocolaptes angustirostris -16,367 -49,500 Inhumas Goiás Brasil
MZUSP 72376 Lepidocolaptes angustirostris -16,367 -49,500 Inhumas, Goiás Goiás Brasil
MPEG 7180 Lepidocolaptes angustirostris -4,333 -40,700 Ipú, Serra Do Ibiapaba Ceará Brasil
MZUSP 41662 Lepidocolaptes angustirostris -3,500 -39,583 Itapipoca, Ceará Ceará Brasil
116
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 4250 Lepidocolaptes angustirostris -24,117 -49,333 Itararé, São Paulo São Paulo Brasil
MZUSP 4251 Lepidocolaptes angustirostris -24,117 -49,333 Itararé, São Paulo São Paulo Brasil
MZUSP 11759 Lepidocolaptes angustirostris -24,117 -49,333 Itararé, São Paulo São Paulo Brasil
MZUSP 11771 Lepidocolaptes angustirostris -24,117 -49,333 Itararé, São Paulo São Paulo Brasil
MZUSP 88888 Lepidocolaptes angustirostris -15,230 -56,480 Jangada, Mato Grosso Mato Grosso Brasil
MZUSP 15055 Lepidocolaptes angustirostris -14,583 -49,033 Jaraguá, Rio Das Almas, Goias Goiás Brasil
MPEG 68195 Lepidocolaptes angustirostris -6,167 -42,650 Jardim Do Mulato, Chapada Dos Macedos, Povoado Zé Piauí Brasil Ferreira
MZUSP 7280 Lepidocolaptes angustirostris -9,417 -40,500 Juazeiro, Bahia Bahia Brasil
MZUSP 7281 Lepidocolaptes angustirostris -9,417 -40,500 Juazeiro, Bahia Bahia Brasil
MZUSP 7282 Lepidocolaptes angustirostris -9,417 -40,500 Juazeiro, Bahia Bahia Brasil
MZUSP 7283 Lepidocolaptes angustirostris -9,417 -40,500 Juazeiro, Bahia Bahia Brasil
MZUSP 7284 Lepidocolaptes angustirostris -9,417 -40,500 Juazeiro, Bahia Bahia Brasil
MZUSP 74791 Lepidocolaptes angustirostris -15,800 -46,980 Lagoa Formosa, Cabeceiras, Goiás Goiás Brasil
MPEG 46451 Lepidocolaptes angustirostris 0,450 -50,933 Macapá, Campus Experimental Da Embrapa, Br156 Amapá Brasil Km48
MPEG 46452 Lepidocolaptes angustirostris 0,450 -50,933 Macapá, Campus Experimental Da Embrapa, Br156 Amapá Brasil Km48
MPEG 46453 Lepidocolaptes angustirostris 0,450 -50,933 Macapá, Campus Experimental Da Embrapa, Br156 Amapá Brasil Km48
117
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MPEG 46454 Lepidocolaptes angustirostris 0,450 -50,933 Macapá, Campus Experimental Da Embrapa, Br156 Amapá Brasil Km48
MPEG 46455 Lepidocolaptes angustirostris 0,450 -50,933 Macapá, Campus Experimental Da Embrapa, Br156 Amapá Brasil Km48
MPEG 46456 Lepidocolaptes angustirostris 0,450 -50,933 Macapá, Campus Experimental Da Embrapa, Br156 Amapá Brasil Km48
MPEG 46457 Lepidocolaptes angustirostris 0,450 -50,933 Macapá, Campus Experimental Da Embrapa, Br156 Amapá Brasil Km48
MPEG 46458 Lepidocolaptes angustirostris 0,450 -50,933 Macapá, Campus Experimental Da Embrapa, Br156 Amapá Brasil Km48
MZUSP 54773 Lepidocolaptes angustirostris -20,800 -51,717 Margem Direita Rio Sucurui, Tres Lagoas, Mato Grosso Mato Grosso do Sul Brasil Do Sul
MZUSP 64175 Lepidocolaptes angustirostris -20,800 -51,717 Margem Direito Do Rio Sucurui, Tres Lagoas, Mato Mato Grosso do Sul Brasil Grosso Do Sul
MZUSP 74240 Lepidocolaptes angustirostris -14,750 -48,750 Margem Esquerda Do Rio Peixe, Niquelândia, Goiás Goiás Brasil
MZUSP 74241 Lepidocolaptes angustirostris -14,750 -48,750 Margem Esquerda Do Rio Peixe, Niquelândia, Goiás Goiás Brasil
MZUSP 74422 Lepidocolaptes angustirostris -20,751 -51,678 Margem Esquerda Rio Sucurui, Tres Lagoas, Mato Mato Grosso do Sul Brasil Grosso
MZUSP 64174 Lepidocolaptes angustirostris -20,751 -51,678 Margem Isquerdo Do Rio Sucurui, Tres Lagoas, Mato Mato Grosso do Sul Brasil Grosso Do Sul+G87
MZUSP 79642 Lepidocolaptes angustirostris -10,527 -46,106 Mata do Rio Galhão, Tocantins Tocantins Brasil
MZUSP 79643 Lepidocolaptes angustirostris -10,527 -46,106 Mata do Rio Galhão, Tocantins Tocantins Brasil
118
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 4677 Lepidocolaptes angustirostris NA NA Minas, Rio Grande do Sul Rio Grande do Sul Brasil
MZUSP 12220 Lepidocolaptes angustirostris -20,233 -56,367 Miranda Mato Grosso do Sul Brasil
MPEG 4732 Lepidocolaptes angustirostris -2,000 -54,067 Monte Alegre, Margem Esquerda Rio Amazonas Pará Brasil
MPEG 54361 Lepidocolaptes angustirostris -2,017 -54,167 Monte Alegre, Serra Do Ererê Pará Brasil
MPEG 44532 Lepidocolaptes angustirostris -16,417 -49,233 Nerópolis, Fazenda Dois Irmãos Goiás Brasil
MZUSP 77726 Lepidocolaptes angustirostris -9,226 -43,463 P.N. da Serra das confusões, Piaui Piauí Brasil
MZUSP 77727 Lepidocolaptes angustirostris -9,226 -43,463 P.N. da Serra das confusões, Piaui Piauí Brasil
MPEG 47039 Lepidocolaptes angustirostris -14,283 -43,333 Palmas De Monte Alto, Fazenda Boa Vista Bahia Brasil
MPEG 47040 Lepidocolaptes angustirostris -14,283 -43,333 Palmas De Monte Alto, Fazenda Boa Vista Bahia Brasil
MPEG 47041 Lepidocolaptes angustirostris -14,283 -43,333 Palmas De Monte Alto, Fazenda Boa Vista Bahia Brasil
MPEG 47042 Lepidocolaptes angustirostris -14,283 -43,333 Palmas De Monte Alto, Fazenda Boa Vista Bahia Brasil
MPEG 47043 Lepidocolaptes angustirostris -14,283 -43,333 Palmas De Monte Alto, Fazenda Boa Vista Bahia Brasil
MPEG 47044 Lepidocolaptes angustirostris -14,283 -43,333 Palmas De Monte Alto, Fazenda Boa Vista Bahia Brasil
MPEG 47045 Lepidocolaptes angustirostris -14,283 -43,333 Palmas De Monte Alto, Fazenda Boa Vista Bahia Brasil
MPEG 47046 Lepidocolaptes angustirostris -14,283 -43,333 Palmas De Monte Alto, Fazenda Boa Vista Bahia Brasil
MPEG 47038 Lepidocolaptes angustirostris -14,283 -43,333 Palmas De Monte Alto, Fazenda Boa Vista Bahia Brasil (14o17'S;43o20'W)
MZUSP 37331 Lepidocolaptes angustirostris -8,900 -36,483 Palmeira De Indios, Alagoas Alagoas Brasil
119
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 29881 Lepidocolaptes angustirostris -19,033 -57,217 Palmeiras, Mato Grosso Mato Grosso Brasil
MZUSP 29886 Lepidocolaptes angustirostris -19,033 -57,217 Palmeiras, Mato Grosso Mato Grosso Brasil
MPEG 72170 Lepidocolaptes angustirostris -6,450 -40,650 Parambú, Fazenda Arsênio Ceará Brasil
MPEG 68211 Lepidocolaptes angustirostris -4,750 -41,717 Piracuruca, Parque Nacional 7 Cidades, Estrada Da Piauí Brasil Piedade
MZUSP 8384 Lepidocolaptes angustirostris -17,350 -44,933 Pirapora, Minas Gerais Minas Gerais Brasil
MZUSP 78535 Lepidocolaptes angustirostris -20,751 -51,678 Ponte Do Rio Sucurui, Tres Lagoas, Mato Grosso Do Sul Mato Grosso do Sul Brasil
MZUSP 78084 Lepidocolaptes angustirostris -15,086 -59,856 Ponte E Lacerda, Mato Grosso Mato Grosso Brasil
MZUSP 5121 Lepidocolaptes angustirostris NA NA Pôrto Faia, Fazenda Faia, Mato Grosso Mato Grosso Brasil
MZUSP 26835 Lepidocolaptes angustirostris -21,850 -47,467 Pôrto Ferreira, São Paulo São Paulo Brasil
MZUSP 80866 Lepidocolaptes angustirostris -10,710 -48,310 Porto Nacional, Tocantins Tocantins Brasil
MZUSP 80903 Lepidocolaptes angustirostris -10,710 -48,310 Porto Nacional, Tocantins Tocantins Brasil
MZUSP 12766 Lepidocolaptes angustirostris -21,817 -52,167 Pôrto Tibirica, São Paulo São Paulo Brasil
MPEG 54319 Lepidocolaptes angustirostris 2,233 -55,950 Reserva Indígena Missão Tiriós Pará Brasil
MZUSP 64173 Lepidocolaptes angustirostris -20,800 -51,717 Retiro da Telha, margem direito do Rio Sucurui, Tres Mato Grosso do Sul Brasil Lagoas, Mato Grosso do Sul
MZUSP 74550 Lepidocolaptes angustirostris -20,800 -51,717 Retiro da Telha, margem direito do Rio Sucurui, Tres Mato Grosso do Sul Brasil Lagoas, Mato Grosso do Sul
MZUSP 69298 Lepidocolaptes angustirostris -12,540 -51,520 Rgs Base Camp, Serra Do Roncador, Mato Grosso Mato Grosso Brasil
120
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MPEG 42139 Lepidocolaptes angustirostris -7,367 -46,617 Riachão, Fazenda Malhadinha Maranhão Brasil
MZUSP 93106 Lepidocolaptes angustirostris -7,530 -45,243 Ribeiro Gonçalves, Piaui Piauí Brasil
MZUSP 1695 Lepidocolaptes angustirostris -21,583 -48,083 Rincao, São Paulo São Paulo Brasil
MPEG 14936 Lepidocolaptes angustirostris -15,917 -52,250 Rio Araguaia, Margem Direita, Aragarças Goiás Brasil
MPEG 16318 Lepidocolaptes angustirostris -15,917 -52,250 Rio Araguaia, Margem Direita, Aragarças Goiás Brasil
MPEG 19697 Lepidocolaptes angustirostris -15,917 -52,250 Rio Araguaia, Margem Direita, Aragarças Goiás Brasil
MPEG 19698 Lepidocolaptes angustirostris -15,917 -52,250 Rio Araguaia, Margem Direita, Aragarças Goiás Brasil
MZUSP 29875 Lepidocolaptes angustirostris -17,083 -56,600 Rio Arica, Fazenda Arica, Mato Grosso Mato Grosso Brasil
MZUSP 29877 Lepidocolaptes angustirostris -17,083 -56,600 Rio Arica, Fazenda Arica, Mato Grosso Mato Grosso Brasil
MZUSP 29878 Lepidocolaptes angustirostris -17,083 -56,600 Rio Arica, Fazenda Arica, Mato Grosso Mato Grosso Brasil
MZUSP 29879 Lepidocolaptes angustirostris -17,083 -56,600 Rio Arica, Fazenda Arica, Mato Grosso Mato Grosso Brasil
MZUSP 29880 Lepidocolaptes angustirostris -17,083 -56,600 Rio Arica, Fazenda Arica, Mato Grosso Mato Grosso Brasil
MZUSP 29882 Lepidocolaptes angustirostris -17,083 -56,600 Rio Arica, Fazenda Arica, Mato Grosso Mato Grosso Brasil
MZUSP 74048 Lepidocolaptes angustirostris -14,442 -48,114 Rio Bagagem, Margem Isquerdo, Serra Negra, Goiás Brasil Niquelândia, Goiás
MZUSP 17588 Lepidocolaptes angustirostris -12,633 -50,667 Rio Cristalino, Mato Grosso Mato Grosso Brasil
MZUSP 15051 Lepidocolaptes angustirostris -14,583 -49,033 Rio Das Almas, Goias Goiás Brasil
MZUSP 15054 Lepidocolaptes angustirostris -14,583 -49,033 Rio Das Almas, Goias Goiás Brasil
121
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MZUSP 54772 Lepidocolaptes angustirostris -20,751 -51,678 Rio Sucurui, Tres Lagoas, Mato Grosso Do Sul Mato Grosso do Sul Brasil
MPEG 19701 Lepidocolaptes angustirostris -2,433 -54,700 Rio Tapajós, Margem Direita, Santarém Pará Brasil
MZUSP 31997 Lepidocolaptes angustirostris -2,433 -54,700 Rio Tapajós, santarém, Pará Pará Brasil
MPEG 28649 Lepidocolaptes angustirostris 2,050 -50,800 Rio Tartarugal, Amapá, Igarapé Ariramba, Reserva Amapá Brasil Dneru No. 4
MPEG 25843 Lepidocolaptes angustirostris -6,650 -51,983 Riosinho, Margem Esquerda Rio Fresco, Posto Nilo- Pará Brasil Peçanha
MZUSP 18341 Lepidocolaptes angustirostris -20,167 -56,517 Salobra, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 18342 Lepidocolaptes angustirostris -20,167 -56,517 Salobra, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 18343 Lepidocolaptes angustirostris -20,167 -56,517 Salobra, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 26814 Lepidocolaptes angustirostris -20,167 -56,517 Salobra, Mato Grosso do Sul Mato Grosso do Sul Brasil
MZUSP 26822 Lepidocolaptes angustirostris -20,167 -56,517 Salobra, Mato Grosso Do Sul Mato Grosso do Sul Brasil
MZUSP 53331 Lepidocolaptes angustirostris -22,667 -53,150 Santa Madalena, São Paulo São Paulo Brasil
MZUSP 53332 Lepidocolaptes angustirostris -22,667 -53,150 Santa Madalena, São Paulo São Paulo Brasil
MZUSP 53333 Lepidocolaptes angustirostris -22,667 -53,150 Santa Madalena, São Paulo São Paulo Brasil
MZUSP 40923 Lepidocolaptes angustirostris -11,350 -43,867 Santa Rita De Cassia, Bahia Bahia Brasil
MZUSP 40924 Lepidocolaptes angustirostris -11,350 -43,867 Santa Rita De Cassia, Bahia Bahia Brasil
MZUSP 40925 Lepidocolaptes angustirostris -11,350 -43,867 Santa Rita De Cassia, Bahia Bahia Brasil
MZUSP 40926 Lepidocolaptes angustirostris -11,350 -43,867 Santa Rita De Cassia, Bahia Bahia Brasil
122
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MPEG 48696 Lepidocolaptes angustirostris -9,667 -50,183 Santana Do Araguaia, Fazenda Barra Das Princesas Pará Brasil
MPEG 51140 Lepidocolaptes angustirostris -13,400 -46,317 São Domingos, Fazenda Cipasa Goiás Brasil
MPEG 51141 Lepidocolaptes angustirostris -13,400 -46,317 São Domingos, Fazenda Cipasa Goiás Brasil
MPEG 68212 Lepidocolaptes angustirostris -6,600 -43,600 São João Dos Patos, Povoado Jatobá Dos Noletos, Serra Maranhão Brasil Da Raposa
MPEG 75497 Lepidocolaptes angustirostris -9,015 -42,699 São Raimundo Nonato, Pn Serra Da Capivara, Baixão Piauí Brasil Do Perna
MZUSP 74142 Lepidocolaptes angustirostris -14,017 -48,200 Serra Da Mesa, Colinas Do Sul, Goiás Goiás Brasil
MZUSP 75912 Lepidocolaptes angustirostris -12,000 -53,400 Sitio Jacare, Mato Grosso Mato Grosso Brasil
MACN 9218 Lepidocolaptes angustirostris -14,850 -57,750 Tapirapoan, Mato Grosso (MS?) Mato Grosso do Sul Brasil
MPEG 53353 Lepidocolaptes angustirostris 1,383 -50,750 Tartarugalzinho, Fazenda Casemiro Amapá Brasil
MPEG 53354 Lepidocolaptes angustirostris 1,383 -50,750 Tartarugalzinho, Fazenda Casemiro Amapá Brasil
MPEG 53355 Lepidocolaptes angustirostris 1,383 -50,750 Tartarugalzinho, Fazenda Casemiro Amapá Brasil
MZUSP 74423 Lepidocolaptes angustirostris -20,751 -51,678 Tres Lagoas, Mato Grosso Do Sul Mato Grosso do Sul Brasil
MZUSP 72378 Lepidocolaptes angustirostris -16,667 -49,500 Trindade, Goiás Goiás Brasil
MZUSP 73875 Lepidocolaptes angustirostris -16,667 -49,500 Trindade, Goiás Goiás Brasil
MPEG 68213 Lepidocolaptes angustirostris -3,200 -43,383 Urbano Santos, Fazenda Monte Carlo Maranhão Brasil
MPEG 68214 Lepidocolaptes angustirostris -3,200 -43,383 Urbano Santos, Fazenda Monte Carlo Maranhão Brasil
MPEG 68190 Lepidocolaptes angustirostris -7,300 -44,467 Uruçuí, Fazenda Morro Redondo Piauí Brasil
123
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MPEG 68191 Lepidocolaptes angustirostris -7,300 -44,467 Uruçuí, Fazenda Morro Redondo Piauí Brasil
MPEG 68215 Lepidocolaptes angustirostris -7,229 -44,556 Uruçuí, Fazenda União Piauí Brasil
MPEG 68216 Lepidocolaptes angustirostris -7,229 -44,556 Uruçuí, Fazenda União Piauí Brasil
MPEG 68217 Lepidocolaptes angustirostris -7,229 -44,556 Uruçuí, Fazenda União Piauí Brasil
MPEG 68218 Lepidocolaptes angustirostris -7,229 -44,556 Uruçuí, Vale Do Rio Pratinha Piauí Brasil
MPEG 68219 Lepidocolaptes angustirostris -7,229 -44,556 Uruçuí, Vale Do Rio Pratinha Piauí Brasil
MPEG 68220 Lepidocolaptes angustirostris -7,229 -44,556 Uruçuí, Vale Do Rio Pratinha Piauí Brasil
MZUSP 73871 Lepidocolaptes angustirostris -17,083 -50,033 Varjao, Goiás Goiás Brasil
MZUSP 73874 Lepidocolaptes angustirostris -17,083 -50,033 Varjao, Goiás Goiás Brasil
MZUSP 98537 Lepidocolaptes angustirostris -15,056 -59,782 Vila Bela da Santissima Trindade Mato Grosso Brasil
MZUSP 98544 Lepidocolaptes angustirostris -15,056 -59,782 Vila Bela da Santissima Trindade Mato Grosso Brasil
MZUSP 98561 Lepidocolaptes angustirostris -15,056 -59,782 Vila Bela da Santissima Trindade Mato Grosso Brasil
MZUSP 98562 Lepidocolaptes angustirostris -15,056 -59,782 Vila Bela da Santissima Trindade Mato Grosso Brasil
MZUSP 7279 Lepidocolaptes angustirostris -10,450 -40,183 Villa Nova, Bahia Bahia Brasil
MACN 42993 Lepidocolaptes angustirostris -22,333 -57,917 265 Km West, Pto Casado Alto Paraguay Paraguai
MACN 64084 Lepidocolaptes angustirostris -27,000 -57,828 Ayo. Dos Hermanas Y Rn. Iv, Ñeembucu, Paraguay Ñeembucu Paraguai
MACN 67962 Lepidocolaptes angustirostris -27,000 -57,828 Ayo. Montuoso Y Rn. Iv, Ñeembucu, Paraguay Ñeembucu Paraguai
MACN 67991 Lepidocolaptes angustirostris -27,000 -57,828 Ayo. Montuoso Y Rn. Iv, Ñeembucu, Paraguay Ñeembucu Paraguai
124
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 63824 Lepidocolaptes angustirostris -27,000 -57,828 Ea. Paso Pucu, Curupayty, Neembucu, Paraguay Ñeembucu Paraguai
MACN 63837 Lepidocolaptes angustirostris -27,000 -57,828 Ea. Paso Pucu, Curupayty, Neembucu, Paraguay Ñeembucu Paraguai
MACN 63922 Lepidocolaptes angustirostris -27,000 -57,828 Ea. Paso Pucu, Curupayty, Neembucu, Paraguay Ñeembucu Paraguai
MACN 29599 Lepidocolaptes angustirostris -22,333 -57,917 Es. Casilda, Pto Casado Alto Paraguay Paraguai
MACN 29600 Lepidocolaptes angustirostris -22,333 -57,917 Es. Guayho, Puerto Casado, Paraguay Alto Paraguay Paraguai
MACN 8560 Lepidocolaptes angustirostris -25,650 -57,017 Escobar Paraguarí Paraguai
MACN 64168 Lepidocolaptes angustirostris -27,000 -57,828 Estancia San Antonio, Tacuara, Ñeembucu, Paraguay Ñeembucu Paraguai
MACN 68044 Lepidocolaptes angustirostris -27,000 -57,828 Estero Camba, E De Tacuara, Ñeembucu, Paraguay Ñeembucu Paraguai
MACN 68062 Lepidocolaptes angustirostris -27,000 -57,828 Estero Camba, E De Tacuara, Ñeembucu, Paraguay Ñeembucu Paraguai
MACN 68123 Lepidocolaptes angustirostris -27,000 -57,828 Estero Camba, E De Tacuara, Ñeembucu, Paraguay Ñeembucu Paraguai
MACN 65431 Lepidocolaptes angustirostris -27,000 -57,828 Mburica, Rn Iv, Neembucu, Paraguay Ñeembucu Paraguai
MACN 64184 Lepidocolaptes angustirostris -27,000 -57,828 Medina, 15 Km E Pilar, Ñeembucu, Paraguay Ñeembucu Paraguai
MACN 29598 Lepidocolaptes angustirostris -22,333 -57,917 Pto. Casado Alto Paraguay Paraguai
MACN 2055a Lepidocolaptes angustirostris -21,300 -57,917 Puerto Guaraní, Paraguay Alto Paraguay Paraguai
MACN 64377 Lepidocolaptes angustirostris -27,000 -57,828 Puerto Tayru, Rio Paraguay, Ñeembucu, Paraguay Ñeembucu Paraguai
MACN 9218 Lepidocolaptes angustirostris -23,400 -57,333 Rio Negro NA Paraguai
MACN 160 E Lepidocolaptes angustirostris -26,667 -54,883 San Rafael, Paraguay Itapúa Paraguai
MACN 68050 Lepidocolaptes angustirostris -27,000 -57,828 San Roque, Medina, Ñeembucu, Paraguay Ñeembucu Paraguai
125
Museum Museum Number Species Latitude Longitude Locality Estate (Depto) Country
MACN 67964 Lepidocolaptes angustirostris -27,000 -57,828 Tacuara, Ñeembucu, Paraguay Ñeembucu Paraguai
MACN 35253 Lepidocolaptes angustirostris -32,750 -57,333 Rio Negro Rio Negro Uruguai
MACN 26564 Lepidocolaptes angustirostris -32,750 -57,333 Rio Negro, R.O., Del Uruguay Rio Negro Uruguai
MACN 41265 Lepidocolaptes angustirostris -30,550 -57,867 San Gregorio, Artigas Artigas Uruguai
MACN 1531a Lepidocolaptes angustirostris NA NA Santa Rita NA Uruguai
126
Appendix B
Table 2. Descriptive statistics of Bill length.
Data OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
Mean 27,4706 28,1022 26,5008 26,1885 28,8478 29,5521
Median 27,6300 28,0900 26,5700 25,7600 29,2200 29,6150
Variance 6,7028 7,8804 3,2800 6,1499 8,8345 13,6212
Standard Deviation 2,5890 2,8072 1,8111 2,4799 2,9723 3,6907
Standard error 0,2100 0,2277 0,1469 0,2011 0,2411 0,2994
Anderson-Darling test 0,0351 0,1075 0,0794 0,0549 0,7353 0,3751
Anderson-Darling test NO normal normal normal normal normal
Table 3. Descriptive statistics of Exposed culmen.
Data OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
Mean 31,1018 31,6432 30,8579 30,2283 32,4661 33,4570
Median 31,5900 31,7000 30,9650 30,0950 32,6200 33,6400
Variance 7,5186 6,9062 3,6020 8,0855 10,9782 16,4142
Standard Deviation 2,7420 2,6280 1,8979 2,8435 3,3133 4,0514
Standard error 0,2224 0,2132 0,1539 0,2306 0,2687 0,3286
Anderson-Darling test 0,1168 0,9423 0,4003 0,3318 0,9511 0,5916
Anderson-Darling test normal normal normal normal normal normal
127 Table 4. Descriptive statistics of Total culmen.
Data OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
Mean 36,0953 36,4987 35,1497 34,4912 36,2906 37,7340
Median 36,4200 36,5600 35,0800 34,3100 36,7200 37,7900
Variance 6,0068 8,5133 3,9294 6,8506 8,4689 12,9035
Standard Deviation 2,4509 2,9178 1,9823 2,6174 2,9101 3,5921
Standard error 0,1988 0,2367 0,1608 0,2123 0,2360 0,2914
Anderson-Darling test 0,2393 0,6637 0,5271 0,0512 0,7478 0,6546
Anderson-Darling test normal normal normal normal normal normal
Table 5. Descriptive statistics of Bill height.
Data OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
Mean 5,6545 5,3721 5,1842 5,0406 5,0032 5,1549
Median 5,6000 5,3850 5,1600 5,0550 5,0500 5,1200
Variance 0,1211 0,0873 0,0774 0,0689 0,0459 0,0821
Standard Deviation 0,3481 0,2954 0,2782 0,2624 0,2141 0,2865
Standard error 0,0282 0,0240 0,0226 0,0213 0,0174 0,0232
Anderson-Darling test 0,8772 0,7110 0,6534 0,9655 0,4811 0,0176
Anderson-Darling test normal normal normal normal normal NO
128 Table 6. Descriptive statistics of Bill width.
Data OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
Mean 4,5569 4,5400 4,5699 4,2800 4,1424 4,3515
Median 4,5700 4,5200 4,5700 4,2400 4,1900 4,2800
Variance 0,1148 0,0985 0,1197 0,1142 0,0685 0,1449
Standard Deviation 0,3388 0,3139 0,3460 0,3379 0,2617 0,3806
Standard error 0,0275 0,0255 0,0281 0,0274 0,0212 0,0309
Anderson-Darling test 0,3091 0,0463 0,7537 0,0108 0,5603 0,0280
Anderson-Darling test normal NO normal NO normal NO
Table 7. Descriptive statistics of Wing length.
Data OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
Mean 97,7059 97,8348 97,1763 95,5026 96,8654 95,7288
Median 99,0000 98,0000 97,5000 95,0000 96,5000 95,2500
Variance 12,1268 14,9768 11,8200 16,7135 25,5712 18,1395
Standard Deviation 3,4824 3,8700 3,4380 4,0882 5,0568 4,2590
Standard error 0,2825 0,3139 0,2789 0,3316 0,4102 0,3455
Anderson-Darling test 0,0462 0,6367 0,0924 0,2208 0,5220 0,0557
Anderson-Darling test NO normal normal normal normal normal
129 Table 8. Descriptive statistics of Tail length.
Data OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
Mean 83,9688 81,9171 81,1259 79,5089 79,7115 76,7759
Median 84,0000 82,0000 81,0000 80,0000 79,0000 77,7500
Variance 18,0490 35,8785 27,7734 30,5681 41,5835 45,8493
Standard Deviation 4,2484 5,9899 5,2701 5,5288 6,4485 6,7712
Standard error 0,3446 0,4858 0,4275 0,4484 0,5230 0,5492
Anderson-Darling test 0,0692 0,6395 0,0154 0,0253 0,5863 0,0647
Anderson-Darling test normal normal NO NO normal normal
Table 9. Descriptive statistics of Tarsus-metatarsus length.
Data OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
Mean 19,4471 20,5587 20,1643 20,6097 20,9346 21,1344
Median 19,1600 20,4800 20,1600 20,4750 20,8050 21,0400
Variance 1,1816 1,8009 0,4777 0,6305 0,5446 1,8969
Standard Deviation 1,0870 1,3420 0,6912 0,7941 0,7380 1,3773
Standard error 0,0882 0,1088 0,0561 0,0644 0,0599 0,1117
Anderson-Darling test 0,0943 NA 0,9172 0,3275 0,2222 0,0000
Anderson-Darling test normal normal normal normal normal NO
130 Results of Kruskall-Wallis analyses to identify differences among OTUs proposed:
Table 10. Kruskall-Wallis test of the OTUs proposed. ns: no significance/*: 0.05 > p > 0.01/**: 0.01 > p > 0.001/ ***: p < 0.001.
Kruskal-Wallis Significance Value
Bill length *** 0,0000
Exposed culmen *** 0,0000
Total culmen *** 0,0000
Bill Height *** 0,0000
Bill Width *** 0,0000
Wing length *** 0,0001
Tail length *** 0,0000
Tarsus−metatarsus length *** 0,0000
Table 11. Mann-Whitney test for Bill length. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01> p > 0.001/ ***: p < 0.001.
Bill length OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
OTU 1 NA 0,5858 0,0118 0,0168 0,1157 0,0183
OTU 2 ns NA 0,0000 0,0000 0,1473 0,0005
OTU 3 * *** NA 0,0993 0,0001 0,0000
OTU 4 * *** ns NA 0,0003 0,0000
OTU 5 ns ns *** *** NA 0,4888
OTU 6 * *** *** *** ns NA
131 Table 12. Mann-Whitney test for Exposed culmen. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001.
Exposed Culmen OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
OTU 1 NA 0,7113 0,3379 0,1062 0,2108 0,0169
OTU 2 ns NA 0,0086 0,0012 0,2614 0,0002
OTU 3 ns ** NA 0,0342 0,0131 0,0000
OTU 4 ns ** * NA 0,0051 0,0000
OTU 5 ns ns * ** NA 0,2900
OTU 6 * *** *** *** ns NA
Table 13. Mann-Whitney test for Total culmen. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001.
Total Culmen OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
OTU 1 NA 0,7854 0,0347 0,0112 0,8228 0,0754
OTU 2 ns NA 0,0001 0,0000 0,8142 0,0114
OTU 3 * *** NA 0,0133 0,0717 0,0000
OTU 4 * *** * NA 0,0244 0,0000
OTU 5 ns Ns ns * NA 0,1525
OTU 6 ns * *** *** ns NA
132 Table 14. Mann-Whitney test for Bill height. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001.
Bill Height OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
OTU 1 NA 0,0148 0,0001 0,0000 0,0000 0,0001
OTU 2 * NA 0,0000 0,0000 0,0000 0,0000
OTU 3 *** *** NA 0,0032 0,0039 0,2617
OTU 4 *** *** ** NA 0,5951 0,0509
OTU 5 *** *** ** ns NA 0,0341
OTU 6 *** *** ns ns * NA
Table 15. Mann-Whitney test for Bill width. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001.
Bill Width OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
OTU 1 NA 0,7615 0,9191 0,0052 0,0005 0,0269
OTU 2 ns NA 0,5223 0,0000 0,0000 0,0001
OTU 3 ns ns NA 0,0000 0,0000 0,0000
OTU 4 ** *** *** NA 0,2084 0,2068
OTU 5 *** *** *** ns NA 0,0290
OTU 6 * *** *** ns * NA
133 Table 16. Mann-Whitney test for Wing length. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001.
Wing length OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
OTU 1 NA 0,8729 0,4277 0,0307 0,3771 0,0478
OTU 2 ns NA 0,2528 0,0005 0,2491 0,0001
OTU 3 ns ns NA 0,0033 0,4936 0,0011
OTU 4 * *** ** NA 0,3473 0,9824
OTU 5 ns ns ns ns NA 0,3387
OTU 6 * *** ** ns ns NA
Table 17. Mann-Whitney test for Tail length. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001.
Tail length OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
OTU 1 NA 0,2277 0,0338 0,0008 0,0099 0,0000
OTU 2 ns NA 0,2334 0,0049 0,0813 0,0000
OTU 3 * ns NA 0,0247 0,1366 0,0000
OTU 4 *** ** * NA 0,9562 0,0138
OTU 5 ** ns ns ns NA 0,0797
OTU 6 *** *** *** * ns NA
134 Table 18. Mann-Whitney test for Tarsus-metatarsus length. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001.
Tarsus-metatarsus length OTU 1 OTU 2 OTU 3 OTU 4 OTU 5 OTU 6
OTU 1 NA 0,0000 0,0006 0,0000 0,0000 0,0000
OTU 2 *** NA 0,0015 0,3628 0,0128 0,0000
OTU 3 *** ** NA 0,0008 0,0000 0,0000
OTU 4 *** ns *** NA 0,0632 0,0015
OTU 5 *** * *** ns NA 0,5916
OTU 6 *** *** *** ** ns NA
Table 19. Summary of Mann-Whitney tests. ns: no significance/*: 0.05 > p > 0.01/ **: 0.01 > p > 0.001/ ***: p < 0.001.
Pairs of OTUs Bill Length Exposed Culmen Total Culmen Bill Height Bill Width Wing Length Tail Length Tarsus-metatarsus length
OTU 1-OTU 2 ns ns ns * ns ns ns ***
OTU 1-OTU 3 * ns * *** ns ns * ***
OTU 1-OTU 4 * ns * *** ** * *** ***
OTU 1-OTU 5 ns ns ns *** *** ns ** ***
OTU 1-OTU 6 * * ns *** * * *** ***
OTU 2-OTU 3 *** ** *** *** ns ns ns **
OTU 2-OTU 4 *** ** *** *** *** *** ** ns
OTU 2-OTU 5 ns ns ns *** *** ns ns *
OTU 2-OTU 6 *** *** * *** *** *** *** ***
OTU 3-OTU 4 ns * * ** *** ** * ***
OTU 3-OTU 5 *** * ns ** *** ns ns ***
OTU 3-OTU 6 *** *** *** ns *** ** *** ***
OTU 4-OTU 5 *** ** * ns ns ns ns ns
OTU 4-OTU 6 *** *** *** ns ns ns * **
OTU 5-OTU 6 ns ns ns * * ns ns ns
135 Values of the fitted clinal models by hzar for L. angustirostris.
Map I. Localities used as “sampling units” for the clinal analysis.
Table 20. Clinal models fitted to Bill length.
Parameter Center Width AIC Clinal Model
3400 Km* 3356,994 37,31897 -696,5102 Model II
3500 - 3900** 3531,094 486,2727 -694,4684 Model II
3000 - 3800** 3424,662 225,6402 -696,6473 Model II
3000 - 3500** 3531,094 486,2727 -694,4684 Model II
136 Table 21. Clinal models fitted to Exposed culmen. (NA) Clinal model not available.
Parameter Center Width AIC Clinal Model
3400 Km* 3363,586 4,5432 -771,9524 Model II
3000 – 3900** 3363,586 4,5432 -771,9524 Model II
3500 – 3900** 3533,41 172,203 -771,1847 Model II
NA Free*** 10679,75 1330,33 -758,93 Model III
Table 22. Clinal models fitted to Total culmen. (NA) Clinal model not available.
Parameter Center Width AIC Clinal Model
3400 Km* 3413,932 232,4986 -818,4388 Model II
3000 – 3900** 3386,058 121,9124 -819,2245 Model II
NA Free*** 7171,15 2481,449 -806,8152 Model III
Table 23. Clinal models fitted to Wing length. (NA) Clinal model not available.
Parameter Center Width AIC Clinal Model
3800* 1816,729 180,1207 -1297,52 Model II
2000 – 3500** 2120,503 9,899084 -1295,789 Model II
2000 – 3900** 2014,458 14,28445 -1295,795 Model II
NA Free*** 1158304 184720,9 -1264,609 Model II
137 Table 24. Clinal models fitted to Bill width. (NA) Clinal model not available.
Parameter Center Width AIC Clinal Model
3800* 1816,387 129,9104 -845,899 Model II
3000 – 3900** 3031,589 409,9952 -814,4114 Model II
NA 3500 – 3900** 3500,046 2558,76 -8,08E+002 Model I
Table 25. Clinal models fitted to Tail length. (NA) Clinal model not available.
Parameter Center Width AIC Clinal Model
3800* 2832,099 9,75892 -907,7641 Model II
NA 3000 – 3900** 3143,532 10744,11 -8,96E+002 Model II
Free*** 2828,024 12,16257 -899,3376 Model III
2500 – 3900** 2814,322 20,7831 -907,761 Model II
Table 26. Clinal models fitted to Bill height. (NA) Clinal model not available.
Parameter Center Width AIC Clinal Model
3800* 1180,772 933,1617 -1036,359 Model I
NA 3000 – 3900** 3510,929 27470,43 -9,66E+002 Model I
NA Free*** -64941853 10967060 -976,6058 Model II
138 Table 27. Clinal models fitted to Tarsus-metatarsus length. (NA) Clinal model not available.
Parameter Center Width AIC Clinal Model
NA 3800* 3286,346 1534,102 -1293,344 Model II
NA 3000 – 3900** 3308,83 1534,513 -1293,215 Model II
NA 2500 – 3900** 3337,916 1627,408 -1293,34 Model II
2000 – 3500** 2946,866 16,99181 -1282,964 Model II
NA 2000 – 3000** 2997,048 1423,215 -1291,913 Model II
139 Table 28. BIOCLIM variables (and their codes) used in preliminary GLM analysis.
Code of variable Name
BIO1 Annual Mean Temperature
BIO2 Mean Diurnal Range (Mean of monthly (max temp - min temp))
BIO3 Isothermality (BIO2/BIO7) (* 100)
BIO4 Temperature Seasonality (standard deviation *100)
BIO5 Max Temperature of Warmest Month
BIO6 Min Temperature of Coldest Month
BIO7 Temperature Annual Range (BIO5-BIO6)
BIO8 Mean Temperature of Wettest Quarter
BIO9 Mean Temperature of Driest Quarter
BIO10 Mean Temperature of Warmest Quarter
BIO11 Mean Temperature of Coldest Quarter
BIO12 Annual Precipitation
BIO13 Precipitation of Wettest Month
BIO14 Precipitation of Driest Month
BIO15 Precipitation Seasonality (Coefficient of Variation)
BIO16 Precipitation of Wettest Quarter
BIO17 Precipitation of Driest Quarter
BIO18 Precipitation of Warmest Quarter
BIO19 Precipitation of Coldest Quarter
140 Table 29. BIOCLIM variables least correlated used in the GLM with interactions.
Code of variable Name
BIO3 Isothermality (BIO2/BIO7) (* 100)
BIO4 Temperature Seasonality (standard deviation *100)
BIO6 Min Temperature of Coldest Month
BIO7 Temperature Annual Range (BIO5-BIO6)
BIO12 Annual Precipitation
BIO19 Precipitation of Coldest Quarter
141 Table 30. Correlation matrix of BIOCLIM variables.
Matrix Bio 1 Bio 2 Bio 3 Bio 4 Bio 5 Bio 6 Bio 7 Bio 8 Bio 9 Bio 10 Bio 11 Bio 12 Bio 13 Bio 14 Bio 15 Bio 16 Bio 17 Bio 18 Bio 19
Bio 1 1 -0,155 0,8 -0,78 0,482 0,921 -0,682 0,709 0,953 0,697 0,962 0,29 0,532 -0,515 0,528 0,529 -0,469 -0,305 0,066
Bio 2 -0,155 1 -0,202 0,334 0,439 -0,471 0,668 0,121 -0,273 0,107 -0,251 -0,443 -0,376 -0,238 0,158 -0,36 -0,227 0,167 -0,473
Bio 3 0,8 -0,202 1 -0,957 -0,005 0,863 -0,851 0,285 0,914 0,178 0,91 0,332 0,672 -0,617 0,663 0,667 -0,576 -0,297 0,089
Bio 4 -0,78 0,334 -0,957 1 0,083 -0,883 0,908 -0,2 -0,922 -0,106 -0,918 -0,477 -0,749 0,558 -0,59 -0,756 0,52 0,3 -0,052
Bio 5 0,482 0,439 -0,005 0,083 1 0,202 0,268 0,733 0,248 0,893 0,278 -0,237 -0,186 -0,209 0,149 -0,183 -0,191 -0,303 -0,099
Bio 6 0,921 -0,471 0,863 -0,883 0,202 1 -0,89 0,486 0,964 0,476 0,963 0,411 0,627 -0,409 0,455 0,618 -0,373 -0,386 0,22
Bio 7 -0,682 0,668 -0,851 0,908 0,268 -0,89 1 -0,136 -0,833 -0,052 -0,818 -0,515 -0,704 0,305 -0,378 -0,694 0,277 0,238 -0,262
Bio 8 0,709 0,121 0,285 -0,2 0,733 0,486 -0,136 1 0,505 0,869 0,524 -0,114 0,038 -0,338 0,265 0,031 -0,311 -0,084 -0,037
Bio 9 0,953 -0,273 0,914 -0,922 0,248 0,964 -0,833 0,505 1 0,469 0,995 0,392 0,66 -0,549 0,577 0,659 -0,502 -0,361 0,104
Bio 10 0,697 0,107 0,178 -0,106 0,893 0,476 -0,052 0,869 0,469 1 0,49 -0,077 -0,009 -0,174 0,16 -0,02 -0,147 -0,245 0,083
Bio 11 0,962 -0,251 0,91 -0,918 0,278 0,963 -0,818 0,524 0,995 0,49 1 0,39 0,655 -0,555 0,578 0,656 -0,511 -0,348 0,079
Bio 12 0,29 -0,443 0,332 -0,477 -0,237 0,411 -0,515 -0,114 0,392 -0,077 0,39 1 0,788 0,156 -0,141 0,818 0,197 0,178 0,385
Bio 13 0,532 -0,376 0,672 -0,749 -0,186 0,627 -0,704 0,038 0,66 -0,009 0,655 0,788 1 -0,367 0,449 0,99 -0,334 -0,062 0,211
Bio 14 -0,515 -0,238 -0,617 0,558 -0,209 -0,409 0,305 -0,338 -0,549 -0,174 -0,555 0,156 -0,367 1 -0,926 -0,376 0,989 0,391 0,39
Bio 15 0,528 0,158 0,663 -0,59 0,149 0,455 -0,378 0,265 0,577 0,16 0,578 -0,141 0,449 -0,926 1 0,432 -0,927 -0,39 -0,316
Bio 16 0,529 -0,36 0,667 -0,756 -0,183 0,618 -0,694 0,031 0,659 -0,02 0,656 0,818 0,99 -0,376 0,432 1 -0,343 -0,058 0,204
Bio 17 -0,469 -0,227 -0,576 0,52 -0,191 -0,373 0,277 -0,311 -0,502 -0,147 -0,511 0,197 -0,334 0,989 -0,927 -0,343 1 0,403 0,411
Bio 18 -0,305 0,167 -0,297 0,3 -0,303 -0,386 0,238 -0,084 -0,361 -0,245 -0,348 0,178 -0,062 0,391 -0,39 -0,058 0,403 1 -0,136
Bio 19 0,066 -0,473 0,089 -0,052 -0,099 0,22 -0,262 -0,037 0,104 0,083 0,079 0,385 0,211 0,39 -0,316 0,204 0,411 -0,136 1
142 Table 31. Models identified in the analysis of PC1 and the BIOCLIM variables.
Model AIC dAIC df weight
Pc1-Bio4 -553,7 0 3 0,885
Pc1-Bio7 -549,2 4,5 3 0,091
Pc1-Bio9 -545,1 8,6 3 0,012
Pc1-Bio3 -543,8 9,9 3 0,006
Pc1-Bio11 -542,8 10,9 3 0,004
Pc1-Bio16 -540,3 13,4 3 0,001
Pc1-Bio13 -540,3 13,5 3 0,001
Pc1-Bio6 -534,3 19,4 3 <0,001
Pc1-Bio1 -531,7 22,1 3 <0,001
Pc1-Bio12 -526,4 27,3 3 <0,001
Pc1-Bio15 -500 53,8 3 <0,001
Pc1-Bio14 -498,5 55,2 3 <0,001
Pc1-Bio18 -497,9 55,8 3 <0,001
Pc1-Bio2 -497 56,8 3 <0,001
Pc1-Bio5 -496,2 57,5 3 <0,001
Pc1-Bio17 -495,3 58,5 3 <0,001
Pc1-Bio8 -494,6 59,1 3 <0,001
Pc1-nulo -493,1 60,6 2 <0,001
Pc1-Bio19 -492 61,7 3 <0,001
Pc1-Bio10 -491,4 62,3 3 <0,001
143
Table 32. Models identified in the analysis of PC2 and the BIOCLIM variables.
Model AIC dAIC df weight
pc2_bio4 -898,7 0 3 0,843
pc2_bio7 -894,1 4,6 3 0,083
pc2_bio3 -893,9 4,9 3 0,074
pc2_bio9 -880,5 18,3 3 <0,001
pc2_bio6 -880,3 18,5 3 <0,001
pc2_bio11 -880,2 18,5 3 <0,001
pc2_bio16 -874 24,8 3 <0,001
pc2_bio13 -873,7 25 3 <0,001
pc2_bio1 -868,8 29,9 3 <0,001
pc2_bio5 -868,8 30 3 <0,001
pc2_bio12 -867 31,7 3 <0,001
pc2_bio15 -866,7 32 3 <0,001
pc2_bio2 -866,3 32,4 3 <0,001
pc2_bio14 -866,2 32,5 3 <0,001
pc2_bio17 -865,5 33,2 3 <0,001
pc2_bio10 -865 33,7 3 <0,001
pc2_nulo -862,4 36,4 2 <0,001
pc2_bio8 -861,8 36,9 3 <0,001
pc2_bio18 -861,7 37,1 3 <0,001
pc2_bio19 -860,8 38 3 <0,001
144
Table 33. Models identified in the analysis of the size and the BIOCLIM variables.
Model AIC dAIC df weight
size_bio18 -1175,1 0 3 1
size_bio8 -1151,3 23,8 3 <0,001
size_bio19 -1151,1 24 3 <0,001
size_bio1 -1144,4 30,7 3 <0,001
size_bio2 -1144,1 31 3 <0,001
size_bio10 -1142,5 32,6 3 <0,001
size_bio16 -1142,2 32,8 3 <0,001
size_bio13 -1142,1 33 3 <0,001
size_bio12 -1142 33 3 <0,001
size_bio9 -1141,6 33,5 3 <0,001
size_nulo -1141,3 33,8 2 <0,001
size_bio14 -1141,2 33,9 3 <0,001
size_bio11 -1141,1 34 3 <0,001
size_bio17 -1140,2 34,9 3 <0,001
size_bio15 -1140 35,1 3 <0,001
size_bio4 -1139,7 35,4 3 <0,001
size_bio3 -1139,7 35,4 3 <0,001
size_bio6 -1139,4 35,7 3 <0,001
size_bio5 -1139,4 35,7 3 <0,001
size_bio7 -1139,4 35,7 3 <0,001
145
Table 34. Models identified in the analysis of ventral patterns and the BIOCLIM variables.
Model AIC dAIC df weight
bin_bio4 127,7 0 2 1
bin_bio3 151,5 23,7 2 <0,001
bin_bio7 176,4 48,7 2 <0,001
bin_bio9 218,1 90,4 2 <0,001
bin_bio11 219,4 91,7 2 <0,001
bin_bio6 250 122,3 2 <0,001
bin_bio16 284,9 157,2 2 <0,001
bin_bio13 289,3 161,6 2 <0,001
bin_bio1 312,3 184,6 2 <0,001
bin_bio15 337,4 209,7 2 <0,001
bin_bio14 346,1 218,4 2 <0,001
bin_bio17 358,4 230,7 2 <0,001
bin_bio12 407,1 279,4 2 <0,001
bin_bio2 424,8 297 2 <0,001
bin_bio18 430,2 302,5 2 <0,001
bin_bio5 436,4 308,7 2 <0,001
bin_nulo 445,2 317,4 1 <0,001
bin_bio8 445,3 317,6 2 <0,001
bin_bio10 446,4 318,7 2 <0,001
bin_bio19 447,1 319,3 2 <0,001
146
Table 35. Vocalizations collected of L. angustirostris.
Species Code Locality State Country Latitude Longitude Source Lepidocolaptes WA103303 Turmalina Sao Paulo Brasil -20,100 -50,480 WikiAves BR angustirostris Lepidocolaptes WA103325 Santa Vitoria Minas Gerais Brasil -18,839 -50,121 WikiAves BR angustirostris Lepidocolaptes WA136083 Conceição das Alagoas Minas Gerais Brasil -19,920 -48,380 WikiAves BR angustirostris Lepidocolaptes WA136084 Conceição das Alagoas Minas Gerais Brasil -19,920 -48,380 WikiAves BR angustirostris Lepidocolaptes WA141084 Curaça Bahia Brasil -8,980 -39,900 WikiAves BR angustirostris Lepidocolaptes WA155261 Jau Sao Paulo Brasil -22,300 -48,550 WikiAves BR angustirostris Lepidocolaptes WA222451 Brasilia Distrito Federal Brasil -15,827 -47,955 WikiAves BR angustirostris Lepidocolaptes WA380578 Pará de Minas Minas Gerais Brasil -19,850 -44,620 WikiAves BR angustirostris Lepidocolaptes WA401898 Sento Sé Bahia Brasil -9,670 -41,300 WikiAves BR angustirostris Lepidocolaptes WA429219 Jacarei Sao Paulo Brasil -23,320 -45,970 WikiAves BR angustirostris Lepidocolaptes WA440193 São João del Rei Minas Gerais Brasil -21,150 -44,270 WikiAves BR angustirostris Lepidocolaptes WA457226 Carmo do Cajuru Minas Gerais Brasil -20,180 -44,770 WikiAves BR angustirostris Lepidocolaptes WA491586 Petrópolis Rio de Janeiro Brasil -22,510 -43,180 WikiAves BR angustirostris Lepidocolaptes WA543242 uruguaiana Rio Grande do Sul Brasil -29,750 -57,080 WikiAves BR angustirostris Lepidocolaptes WA563982 Lorena Sao Paulo Brasil -22,730 -45,130 WikiAves BR angustirostris Lepidocolaptes WA590241 Jau Sao Paulo Brasil -22,300 -48,550 WikiAves BR angustirostris Lepidocolaptes WA693993 Juiz de Fora Minas Gerais Brasil -21,750 -43,350 WikiAves BR angustirostris Lepidocolaptes WA699455 Jacarei Sao Paulo Brasil -23,320 -45,970 WikiAves BR angustirostris 147
Species Code Locality State Country Latitude Longitude Source Lepidocolaptes WA720399 Pão de Açucar Alagoas Brasil -9,750 -37,430 WikiAves BR angustirostris Lepidocolaptes WA729264 Viçosa Minas Gerais Brasil -20,750 -42,880 WikiAves BR angustirostris Lepidocolaptes WA74113 Corumba Mato Grosso do Brasil -19,020 -57,650 WikiAves BR angustirostris Sul Lepidocolaptes WA75122 São Felix do Tocantins Tocantins Brasil -10,180 -46,540 WikiAves BR angustirostris Lepidocolaptes WA766603 Araras Sao Paulo Brasil -22,370 -47,380 WikiAves BR angustirostris Lepidocolaptes WA767132 Mogi Guaçu Sao Paulo Brasil -22,370 -46,950 WikiAves BR angustirostris Lepidocolaptes WA769809 São Borja Rio Grande do Sul Brasil -28,650 -56,000 WikiAves BR angustirostris Lepidocolaptes WA784739 Piraju Sao Paulo Brasil -23,200 -49,380 WikiAves BR angustirostris Lepidocolaptes WA80402 Brasilia Distrito Federal Brasil -15,827 -47,955 WikiAves BR angustirostris Lepidocolaptes WA97187 Juazeiro Bahia Brasil -12,530 -38,970 WikiAves BR angustirostris Lepidocolaptes 17726 5.0 km NE of Robore Santa Cruz Bolivia -18,350 -59,750 Macaulay angustirostris Library Lepidocolaptes 19073 Itaqui; Fazenda Silencio Rio Grande do Sul Brazil NA NA Macaulay angustirostris Library Lepidocolaptes 38362 8.0 km S of Trinidad El Beni Bolivia -14,780 -64,950 Macaulay angustirostris Library Lepidocolaptes 52033 W of Santa Rosa de la Roca Santa Cruz Bolivia NA NA Macaulay angustirostris Library Lepidocolaptes 55857 - - - NA NA Macaulay angustirostris Library Lepidocolaptes 57888 Estancia Iparoma, Filadelfia Chaco Paraguay NA NA Macaulay angustirostris Library Lepidocolaptes 82651 Curuyuqui Santa Cruz Bolivia -18,776 -62,244 Macaulay angustirostris Library Lepidocolaptes 101381 Reserva Natural del Bosque Mbaracayu Canindey Paraguay NA NA Macaulay angustirostris Library Lepidocolaptes 101407 Reserva Natural del Bosque Mbaracayu Canindey Paraguay NA NA Macaulay angustirostris Library Lepidocolaptes 116081 W of J.V. Gonzales Salta Argentina -25,217 -64,933 Macaulay angustirostris Library Lepidocolaptes 129076 E side of Sierra Santa Barbara Jujuy Argentina -24,091 -64,399 Macaulay 148
Species Code Locality State Country Latitude Longitude Source angustirostris Library Lepidocolaptes 129082 E side of Sierra Santa Barbara; near El Fuerte Jujuy Argentina -24,091 -64,399 Macaulay angustirostris Library Lepidocolaptes 129395 E slope Sierra Santa Barbara, near El Fuerte Jujuy Argentina -24,091 -64,399 Macaulay angustirostris Library Lepidocolaptes 132442 30.0 km SW of Estancia Rincon El Socorro Corrientes Argentina -28,690 -57,434 Macaulay angustirostris Library Lepidocolaptes 144197 Madrejon Alto Paraguay Paraguay -20,667 -59,833 Macaulay angustirostris Library Lepidocolaptes 144201 Madrejon Alto Paraguay Paraguay -20,667 -59,833 Macaulay angustirostris Library Lepidocolaptes 146429 Villa Monte, E side of Sierra Santa Barbara Jujuy Argentina -24,083 -64,383 Macaulay angustirostris Library Lepidocolaptes 146519 2.0 km E of Ocloyas Jujuy Argentina -23,938 -65,218 Macaulay angustirostris Library Lepidocolaptes 168082 Estancia Los Gingos Chuquisaca Bolivia -20,557 -62,943 Macaulay angustirostris Library Lepidocolaptes XC10292 São Jose da Barra Minas Gerais Brasil -20,708 -46,133 Xeno-Canto angustirostris Lepidocolaptes XC106024 Caatinga da Serra, Mata Grande Alagoas Brazil -9,135 -37,772 Xeno-Canto angustirostris Lepidocolaptes XC106025 Caatinga da Serra, Mata Grande Alagoas Brazil -9,135 -37,772 Xeno-Canto angustirostris Lepidocolaptes XC108158 Estancia Rincon del Socorro, Pellegrini Corrientes Argentina -28,579 -57,223 Xeno-Canto angustirostris Lepidocolaptes XC108159 Laguna Esquel Chubut Argentina -42,900 -71,077 Xeno-Canto angustirostris Lepidocolaptes XC113391 El Cutal Beni Bolivia -14,114 -64,933 Xeno-Canto angustirostris Lepidocolaptes XC13957 Parque Rivera Montevideo Uruguay -34,880 -56,093 Xeno-Canto angustirostris Lepidocolaptes XC2196 Guus Knijnenburg's Farm Santa Cruz Bolivia -17,167 -62,417 Xeno-Canto angustirostris Lepidocolaptes XC29149 Parque Nacional Calilegua, Aguas Negras Jujuy Argentina -23,750 -64,850 Xeno-Canto angustirostris Lepidocolaptes XC29150 Parque Nacional Calilegua, Aguas Negras Jujuy Argentina -23,750 -64,850 Xeno-Canto angustirostris Lepidocolaptes XC29151 Parque Nacional Calilegua, Aguas Negras Jujuy Argentina -23,683 -64,750 Xeno-Canto angustirostris Lepidocolaptes XC2921 Lomas de Arena Santa Cruz Bolivia -17,833 -63,167 Xeno-Canto angustirostris 149
Species Code Locality State Country Latitude Longitude Source Lepidocolaptes XC45043 Santa Vitoria Minas Gerais Brazil -18,849 -50,120 Xeno-Canto angustirostris Lepidocolaptes XC45170 Turmalina São Paulo Brazil -20,049 -50,453 Xeno-Canto angustirostris Lepidocolaptes XC4554 Parapetiguasu, Serrania Imboche Santa Cruz Bolivia -20,246 -63,231 Xeno-Canto angustirostris Lepidocolaptes XC48502 Las Maderas Jujuy Argentina -24,465 -65,263 Xeno-Canto angustirostris Lepidocolaptes XC48580 Fazenda Siri Floresta Pernambuco -8,340 -38,156 Xeno-Canto angustirostris Lepidocolaptes XC48581 Fazenda Siri Floresta Pernambuco -8,340 -38,156 Xeno-Canto angustirostris Lepidocolaptes XC48896 Estancia El Potrero (La Zanja), Gualeguaychu Entre Rios Argentina -32,983 -58,250 Xeno-Canto angustirostris Lepidocolaptes XC48897 Estancia El Potrero (La Zanja), Gualeguaychu Entre Rios Argentina -32,983 -58,250 Xeno-Canto angustirostris Lepidocolaptes XC50114 Laguna Ibera Corrientes Argentina -28,500 -57,150 Xeno-Canto angustirostris Lepidocolaptes XC50115 Laguna Ibera Corrientes Argentina -28,500 -57,150 Xeno-Canto angustirostris Lepidocolaptes XC50116 Laguna Ibera Corrientes Argentina -28,500 -57,150 Xeno-Canto angustirostris Lepidocolaptes XC52563 La Potola Santafé Argentina -30,383 -59,950 Xeno-Canto angustirostris Lepidocolaptes XC52564 Acambuco Salta Argentina -22,193 -63,944 Xeno-Canto angustirostris Lepidocolaptes XC52565 Acambuco, Tartagal Salta Argentina -22,193 -63,944 Xeno-Canto angustirostris Lepidocolaptes XC52566 Acambuco, Tartagal Salta Argentina -22,193 -63,944 Xeno-Canto angustirostris Lepidocolaptes XC52567 Acambuco, Tartagal Salta Argentina -22,193 -63,944 Xeno-Canto angustirostris Lepidocolaptes XC52568 Acambuco, Tartagal Salta Argentina -22,193 -63,944 Xeno-Canto angustirostris Lepidocolaptes XC52569 Acambuco, Tartagal Salta Argentina -22,193 -63,944 Xeno-Canto angustirostris Lepidocolaptes XC53592 Parque Nacional Lihue Calel La Pampa Argentina -37,950 -65,550 Xeno-Canto angustirostris Lepidocolaptes XC54208 El Relincho, Ecilda Paulier San Jose Uruguay -34,317 -57,033 Xeno-Canto angustirostris Lepidocolaptes XC55966 Laguna Blanca San Pedro Paraguay -23,813 -56,295 Xeno-Canto 150
Species Code Locality State Country Latitude Longitude Source angustirostris Lepidocolaptes XC5888 Jau São Paulo Brazil -22,314 -48,503 Xeno-Canto angustirostris Lepidocolaptes XC61068 Parque Nacional Mburucuya Corrientes Argentina -28,017 -58,017 Xeno-Canto angustirostris Lepidocolaptes XC61069 Mercedes Corrientes Argentina -29,185 -58,074 Xeno-Canto angustirostris Lepidocolaptes XC61205 Campo Avalos, Estancia Cambai-puente rio Mirinay, Monte Corrientes Argentina -30,250 -57,683 Xeno-Canto angustirostris Caseros Lepidocolaptes XC6321 Lagoa Grande Pernambuco Brazil -8,832 -40,177 Xeno-Canto angustirostris Lepidocolaptes XC7153 Porteiras, Altinho Pernambuco Brazil -8,300 -37,750 Xeno-Canto angustirostris Lepidocolaptes XC75704 10 km S Pocone on Transpantaneira Mato Grosso Brazil -16,362 -56,648 Xeno-Canto angustirostris Lepidocolaptes XC80444 Aquidauana Mato Grosso do Brazil -20,483 -55,817 Xeno-Canto angustirostris Sul Lepidocolaptes XC80445 Aquidauana Mato Grosso do Brazil -20,483 -55,817 Xeno-Canto angustirostris Sul Lepidocolaptes XC80446 Chapada Mato Grosso Brazil -15,100 -55,617 Xeno-Canto angustirostris Lepidocolaptes XC80447 Jeremoabo Bahia Brazil -10,064 -38,339 Xeno-Canto angustirostris Lepidocolaptes XC80451 Aquidauana Mato Grosso do Brazil -20,483 -55,817 Xeno-Canto angustirostris Sul Lepidocolaptes XC80953 Fazenda Santa Tereza, Rio Pixaim Mato Grosso Brazil -16,750 -56,850 Xeno-Canto angustirostris Lepidocolaptes XC80954 Fazenda Santa Tereza, Rio Pixaim Mato Grosso Brazil -16,750 -56,850 Xeno-Canto angustirostris
151
152