The Open Ornithology Journal




(Discontinued)

ISSN: 1874-4532 ― Volume 13, 2020
RESEARCH ARTICLE

Description of New American Carduelis/Spinus Bird Species in La Paz (Bolivia): C./S. lapazensis.



Antonio Arnaiz-Villena1, *, Valentín Ruiz-del-Valle1, Fabio Suarez-Trujillo1, Adrian Lopez-Nares1, Alvaro Callado1, Eduardo Gomez-Casado2, Estefania Crespo-Yuste1, Cristina Campos1
1 Department of Immunology, School of Medicine, University Complutense,, Madrid, Spain
2 Department of Biotechnology, INIA, Madrid, Spain

Abstract

Introduction:

South American siskins (Genus Carduelis/Spinus) are the outcome of regional evolutionary radiation from an extant (or other extinct) species: C. notata, a North America siskin, which thrives in Mexico subtropical areas and is parental of one of the three described North American siskin radiations.

Methods:

Speciation and/or subspeciation of this South American siskin radiation have probably occurred during Pleistocene Epoch. In the present paper, a new species/subspecies akin to C./S. atrata is described by genetic and phenotypic parameters: this new species/subspecies was previously considered a subspecies of C./S. xanthogastra, which thrives further North and is separated about 1,762 km, 1,094 miles, from this described subspecies, Carduelis/ Spinus xanthogastra stejnegeri.

Results:

Our genetic study using mt cyt b, phenotypic and behavior observations show that this putative C./S. xanthogastra subspecies is either a different species or a C./S.atrata subspecies; we have proposed a provisional name for this finch, C./S. lapazensis, instead of C./S. x. stejnegeri.

Conclusion:

Species definition is movable and controversial, and it is uncertain in South American siskins, which all show a close genetic and phenotypical relationship, which may be still immersed in speciation processes since Pleistocene Epoch.

Keywords: Songbirds, Finches, Serinus, Carduelis, Spinus, Carduelinae, Siskins, Bolivia, Lapazensis, La Paz, Atrata, Xanthogastra, Stejnegeri, Fringillinae, Fringilidae, Notata, Andes, Ecuador, Peru, Bird.


Article Information


Identifiers and Pagination:

Year: 2020
Volume: 13
First Page: 24
Last Page: 33
Publisher Id: TOOENIJ-13-24
DOI: 10.2174/1874453202013010024

Article History:

Received Date: 23/01/2020
Revision Received Date: 05/04/2020
Acceptance Date: 02/05/2020
Electronic publication date: 19/08/2020
Collection year: 2020

© 2020 Arnaiz-Villena et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Department of Immunology, School of Medicine, University Complutense, Madrid, Spain; Tel: +34 913941632; +34 606993161; E-mails: aarnaiz@med.ucm.es, arnaizville@hotmail.com and chopo.pntic.mec.es/biolmol





1. INTRODUCTION

Genus Carduelis (family Fringillidae, subfamily Fringillinae, tribe Carduelini) includes goldfinches, siskins, redpolls, greenfinches, and crossbills, among others [1Sibley CG, Monroe BL. Distribution and Taxonomy of Birds of the World 1990., 2Arnaiz-Villena A, Guillén J, Ruiz-del-Valle V, et al. Phylogeography of crossbills, bullfinches, grosbeaks, and rosefinches. Cell Mol Life Sci 2001; 58(8): 1159-66.
[http://dx.doi.org/10.1007/PL00000930] [PMID: 11529508]
]. It comprises over 30 species, and it is widespread all over the World except for Subsaharan Africa and Australia. It belongs to the Fringillidae family of birds, which also includes many sparrows, bramblings, and chaffinches [3Arnaiz-Villena A, Areces C, Rey D, et al. Three different North American siskin/goldfinch evolutionary radiations (genus Carduelis): Pine Siskin Green Morphs and European Siskins in America. Open Ornithol J 2012; 5(1): 73-81.
[http://dx.doi.org/10.2174/1874453201205010073]
]. Many of the species comprised within this genus and other genera have recently been classified by using Molecular Systematics and the mitochondrial cytochrome b (cyt b) gene [4Arnaiz-Villena A, Ruiz-del-Valle V, Gomez-Prieto P, et al. Carduelini New Sistematics: Crimson-winged Finch (Rhodopechys sanguineus) is Included in “Arid-Zone” Carduelini Finches by Mitochondrial DNA Phylogeny. Open Ornithol J 2014; 7: 55-62.
[http://dx.doi.org/10.2174/1874453201407010055]
, 5Arnaiz-Villena A, Ruiz del Valle V, Reguera R, Gomez-Prieto P, Serrano-Vela JI. What might have been the ancestor of New World siskins? Open Ornithol J 2008; 1: 46-7.
[http://dx.doi.org/10.2174/1874453200801010046]
].

The estimated divergence time for most of the genus Carduelis species suggests that they appeared in a range of time between the Miocene and Pliocene; there is no evidence for a divergence time consistent with late Pleistocene origin for most radiation groups [6Arnaiz-Villena A, Moscoso J, Ruiz-del-Valle V, et al. Mitochondrial DNA phylogenetic definition of a group of ‘arid-zone’ Carduelini finches. Open Ornithol J 2008; 1(1): 1-7.
[http://dx.doi.org/10.2174/1874453200801010001]
-10Arnaiz-Villena A, Ruiz-del-Valle V, Gomez-Prieto P. Phylogeography of finches and sparrows 2009. Available from https://www.acade mia.edu /38868100/In_Animal_Genetics_PHYLOGEOGRAPHY_OF _FINCHES_AND_SPARROWS]. This radiation was intermingled in time with Serinus species radiation. However, it is possible that certain Carduelis birds, classically considered as subspecies, originated during Pleistocene glaciations i. e.: the divergence time calculated for C. carduelis subspecies (grey-headed Asian and black-headed European goldfinch) is less than 800,000 years [6Arnaiz-Villena A, Moscoso J, Ruiz-del-Valle V, et al. Mitochondrial DNA phylogenetic definition of a group of ‘arid-zone’ Carduelini finches. Open Ornithol J 2008; 1(1): 1-7.
[http://dx.doi.org/10.2174/1874453200801010001]
-10Arnaiz-Villena A, Ruiz-del-Valle V, Gomez-Prieto P. Phylogeography of finches and sparrows 2009. Available from https://www.acade mia.edu /38868100/In_Animal_Genetics_PHYLOGEOGRAPHY_OF _FINCHES_AND_SPARROWS].

Three different and apparently parallel North and South American siskin evolutionary radiations have occurred in the last five million years, all three are genetically related, but a common ancestor, if any, is undetermined [3Arnaiz-Villena A, Areces C, Rey D, et al. Three different North American siskin/goldfinch evolutionary radiations (genus Carduelis): Pine Siskin Green Morphs and European Siskins in America. Open Ornithol J 2012; 5(1): 73-81.
[http://dx.doi.org/10.2174/1874453201205010073]
, 5Arnaiz-Villena A, Ruiz del Valle V, Reguera R, Gomez-Prieto P, Serrano-Vela JI. What might have been the ancestor of New World siskins? Open Ornithol J 2008; 1: 46-7.
[http://dx.doi.org/10.2174/1874453200801010046]
]. Regarding South American radiation, it has to be noted that Black-headed siskin (Carduelis notata) at present thriving at the Mexican mountains gave rise to these group of siskins [3Arnaiz-Villena A, Areces C, Rey D, et al. Three different North American siskin/goldfinch evolutionary radiations (genus Carduelis): Pine Siskin Green Morphs and European Siskins in America. Open Ornithol J 2012; 5(1): 73-81.
[http://dx.doi.org/10.2174/1874453201205010073]
, 7Arnaiz-Villena A, Alvarez-Tejado M, Ruíz-del-Valle V, et al. Phylogeny and rapid northern and southern hemisphere speciation of goldfinches during the Miocene and Pliocene epochs. Cell Mol Life Sci 1998; 54(9): 1031-41.
[http://dx.doi.org/10.1007/s000180050230] [PMID: 9791543]
]. This happened after 3 MYA when Panama Isthmus closed and mesothermal plants, appropriate for siskin feeding, passed to the Andean Spine [3Arnaiz-Villena A, Areces C, Rey D, et al. Three different North American siskin/goldfinch evolutionary radiations (genus Carduelis): Pine Siskin Green Morphs and European Siskins in America. Open Ornithol J 2012; 5(1): 73-81.
[http://dx.doi.org/10.2174/1874453201205010073]
, 10Arnaiz-Villena A, Ruiz-del-Valle V, Gomez-Prieto P. Phylogeography of finches and sparrows 2009. Available from https://www.acade mia.edu /38868100/In_Animal_Genetics_PHYLOGEOGRAPHY_OF _FINCHES_AND_SPARROWS].

In the present paper, the aim is to study the phylogenetic relationship of certain South American radiation birds: Carduelis xanthogastra (distributed in Costa Rica, Central America to Mt. Andes including most of Ecuador Country), Carduelis xanthogastra stejnegeri (Northern Bolivia) and Carduelis atrata (Mt. Andes of Peru, Bolivia, North Argentina and North Chile) (Figs. 1, 2). C. x. stejnegeri has been considered a subspecies of C. xanthogastra. C. x. stejnegeri description [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12., 12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.] pointed out the differences between C. xanthogastra and C. x. stejnegeri. However, it has been observed that C. x. stejnegeri habitat was geographically different and separated from C. xanthogastra Fig. (2). In contrast, the geographical habitat was adjacent and sometimes overlapping to that of C. atrata, but generally in warmer valleys. We observed during several years C. x. stejnegeri behavior and habitat and carried out a genetic study in order to establish a relationship among these three species Fig. (1).

Fig. (1)
Males of Carduelis species targeted for analysis. a) C. x. stejnegeri (Photographed by Fabian Beltrán at Botanic Gardens, La Paz, Bolivia) [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12.]. Adult male, female and juvenile characters and their distribution in [12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.] b) C. xanthogastra [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12., 13Du Bus G. Bulletins de l'Académie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique. Bruxelles 1855; XXII(Part 1): 152-53.]. Adult male, female and juvenile description, status, habitat, behaviour and their distribution in the study [12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.] (Photographed by A. Arnaiz-Villena. Bird from Valencia, Venezuela) c) C. atrata [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12., 14Lafresnaye AD and d’Orbigny D. Synopsis avium. Magasin de Zoologie (París) 1837; 7: 83.]. Description adult male, female and juvenile characters and their distribution in the study [12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.] (Photographed by A. Arnaiz-Villena. Bird from La Paz, Bolivia).


Fig. (2)
Distribution map of studied species and species photographs [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12., 12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.]. A.C. x. stejnegeri (Distribution is shown in red colour), B.C. xanthogastra (Distribution is shown in green colour) and C.C. atrata (Distribution is shown in blue colour). A photography is taken by ornithologist Fernando Dolset. B photography is also shown in Fig. 1 (A. A-V). C Photograph is taken by A. Arnaiz-Villena in El Alto, La Paz, Bolivia. Inset R: Americas map. Inset L: Arrows mark distance of thriving margins of C. xanthogastra (North: southern Ecuador) and C.xanthogastra stejnegeri (South: northern Bolivia).A gap of 1,094 miles,1,765 km, separates both birds thriving ranges. It is not discarded that C. x. stejnegeri may thrive in southernmost Peru [15Restall R, Rodner C, Lentino R. Birds of Northern South America 2006., 16Schulenberg TS, Stotz DF, Lane DF, O’Neill JP, Parker TA III. Birds of Peru: Revised and updated edition 2010.].


Table 1
Origin and Cytochrome b GenBank accession numbers of the species used in this study.



2. MATERIALS AND METHODS

For the original description of the following species, (Appendix 1): C. xanthogastra (yellow-bellied siskin), C. x. stejnegeri (yellow-bellied siskin), C. atrata (black siskin).

2.1. Bird Samples, DNA Extraction and PCR Amplifications

Original species bird descriptions are detailed in Appendix 1 after the Acknowledgements section.

Fifteen species of Carduelis (order Passeriformes) have been included in this study (Table 1). They belong to the tribe Carduelini. One male and two females of C. x. stejnegeri [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12., 12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.] were collected, sexed (Labs Edyma, Valdepeñas, Spain), DNA sequenced and photographed. Blood from living birds was drawn as described in our previous papers [6Arnaiz-Villena A, Moscoso J, Ruiz-del-Valle V, et al. Mitochondrial DNA phylogenetic definition of a group of ‘arid-zone’ Carduelini finches. Open Ornithol J 2008; 1(1): 1-7.
[http://dx.doi.org/10.2174/1874453200801010001]
, 7Arnaiz-Villena A, Alvarez-Tejado M, Ruíz-del-Valle V, et al. Phylogeny and rapid northern and southern hemisphere speciation of goldfinches during the Miocene and Pliocene epochs. Cell Mol Life Sci 1998; 54(9): 1031-41.
[http://dx.doi.org/10.1007/s000180050230] [PMID: 9791543]
] and preserved in EDTA at 4ºC until use; otherwise, DNA was taken from feathers. DNA extraction was performed using a commercial DNA purification kit (QuickGene DNA Whole Blood Kit S, FUJIFILM, Tokyo, Japan). Amplification and sequencing of mt cyt b gene 924 base pairs (bp) were performed as previously described [8Arnaiz-Villena A, Alvarez-Tejado M, Ruiz-del-Valle V, et al. Rapid radiation of canaries (genus Serinus). Mol Biol Evol 1999; 16(1): 2-11.
[http://dx.doi.org/10.1093/oxfordjournals.molbev.a026034]
, 17Zamora J, Lowy E, Ruiz-del-Valle V, et al. Rhodopechys obsoleta (desert finch): A pale ancestor of greenfinches (Carduelis spp.) according to molecular phylogeny. J Ornithol 2006; 147(3): 448-56.
[http://dx.doi.org/10.1007/s10336-005-0036-2]
]. Internal primers used for sequencing were: H15149 3’-TGCAGCCCCTCA GAATGA TATTTGTCCTCA-5’ and L15299 5’-GGATT CTTCGCCCT GCACTTCCTCC-3’. C. x. stejnegeri flocks were observed during 3 different years around La Paz City small valleys, ravines and La Paz Cactus Gardens.

One of our C. x. stejnegeri sample was a female whose photographs are shown in the discussion section. It cannot be confused with C. atrata females, which may thrive in the same area, but usually at higher altitudes (see below). C. atrata females show a full black back; the back is less bright than it is in males. Sometimes both sexes are difficult to distinguish [12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.]. In order to avoid confusion when authors refer to this work and before nomenclature committees decide a name for the species or subspecies described in this paper, we propose a provisional name: Carduelis/Spinus lapazensis.

2.2. Phylogenetic Analyses

DNA sequences were aligned by using the MEGA 5 computer program [18Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28(10): 2731-9.
[http://dx.doi.org/10.1093/molbev/msr121] [PMID: 21546353]
] for further phylogenetic calculations and calculating the cytochrome b DNA distances and cytochrome b protein distances. MEGA 5 has also been used to compare differences in the codons between C. x. stejnegeri, C. atrata and C. xanthogastra. The final length of the sequences used was 924 nucleotides. Chaffinch, Fringilla coelebs (family Fringillidae, subfamily Fringillinae), was chosen as an outgroup to root the phylogenetic dendrograms. Phylogenetic dendrograms were obtained using the Maximum Likelihood (ML) methodology [19Felsenstein J. Evolutionary trees from DNA sequences: A maximum likelihood approach. J Mol Evol 1981; 17(6): 368-76.
[http://dx.doi.org/10.1007/BF01734359] [PMID: 7288891]
] with PAUP* v. 4.0b10 program [20Swofford D. Phylogenetic analysis using parsimony and other methods. Sunderland. MA: Sinauer Associates 2002; b10.] and Bayesian Inference (BI) methodology using Mr. Bayes program [21Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001; 17(8): 754-5.
[http://dx.doi.org/10.1093/bioinformatics/17.8.754] [PMID: 11524383]
, 22Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003; 19(12): 1572-4.
[http://dx.doi.org/10.1093/bioinformatics/btg180] [PMID: 12912839]
]. Model test v.3.7 [23Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics 1998; 14(9): 817-8.
[http://dx.doi.org/10.1093/bioinformatics/14.9.817] [PMID: 9918953]
] was used to find out a DNA substitution model that fits the data best. The best model was used prior to both ML and BI analyses. Linearized ML dendrograms were obtained with PAUP* v.4.0b10 [18Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28(10): 2731-9.
[http://dx.doi.org/10.1093/molbev/msr121] [PMID: 21546353]
] with the estimated branch length [24Thorne JL, Kishino H, Painter IS. Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol 1998; 15(12): 1647-57.
[http://dx.doi.org/10.1093/oxfordjournals.molbev.a025892] [PMID: 9866200]
], which assumes that the rates among the evolutionary lineages may not be constant.

3. RESULTS

3.1. Phylogeny of C. x. stejnegeri

Fig. (3) shows a linearized Bayesian dendrogram (Fig. 3A). Sample DNA sequence of C. x. stejnegeri (Fig. 3A) is not related phylogenetically with C. xanthogastra, as it had been thought. However, C. x. stejnegeri is related to C. atrata with 92% of the bootstrap value. In addition, these results are supported by (Fig. 3B), a Linearized Maximum Likelihood dendrogram (Fig. 3B): the close relationship between C. atrata and C. x. stejnegeri has also been observed. In addition, C. xanthogastra appeared on Earth earlier than C. atrata and C. x. stejnegeri, as shown in Fig. (3B) and more amplified in Fig. (3C).

Fig. (3A)
A Linearized Bayesian dendrogram based on mitochondrial cytochrome b (mt cyt b) DNA sequences.


Fig. (3B)
Linearized Maximum Likelihood dendrogram based on mt cyt b DNA sequences. Fringilla coelebs was chosen as an outgroup for both trees [3Arnaiz-Villena A, Areces C, Rey D, et al. Three different North American siskin/goldfinch evolutionary radiations (genus Carduelis): Pine Siskin Green Morphs and European Siskins in America. Open Ornithol J 2012; 5(1): 73-81.
[http://dx.doi.org/10.2174/1874453201205010073]
, 7Arnaiz-Villena A, Alvarez-Tejado M, Ruíz-del-Valle V, et al. Phylogeny and rapid northern and southern hemisphere speciation of goldfinches during the Miocene and Pliocene epochs. Cell Mol Life Sci 1998; 54(9): 1031-41.
[http://dx.doi.org/10.1007/s000180050230] [PMID: 9791543]
, 8Arnaiz-Villena A, Alvarez-Tejado M, Ruiz-del-Valle V, et al. Rapid radiation of canaries (genus Serinus). Mol Biol Evol 1999; 16(1): 2-11.
[http://dx.doi.org/10.1093/oxfordjournals.molbev.a026034]
]. Only significant bootstrap values are depicted, which are concordant with previous studies [3Arnaiz-Villena A, Areces C, Rey D, et al. Three different North American siskin/goldfinch evolutionary radiations (genus Carduelis): Pine Siskin Green Morphs and European Siskins in America. Open Ornithol J 2012; 5(1): 73-81.
[http://dx.doi.org/10.2174/1874453201205010073]
, 8Arnaiz-Villena A, Alvarez-Tejado M, Ruiz-del-Valle V, et al. Rapid radiation of canaries (genus Serinus). Mol Biol Evol 1999; 16(1): 2-11.
[http://dx.doi.org/10.1093/oxfordjournals.molbev.a026034]
].


Fig. (3C)
Amplified part of 4B dendrogram showing also that speciation occurred for C. atrata/ C. x. stejnegeri about 0.5 MYA (million years ago) and for C. xanthogastra about 1.4 MYA.


Similar to the results obtained in dendrograms from Fig. (3) with mt cytochrome b DNA genetic distances, (Table 2) shows a close relationship between C. x. stejnegeri and C. atrata (0.004) than that between C. x. stejnegeri and C. xanthogastra (0.012). Although at the DNA level, there were differences between these three taxa, not at the protein level, because these DNA differences were synonymous mutations.

Table 2
Cytochrome b DNA genetic distances between the species used in the analysis. DNA genetic distances between C. x. stejnegeri, C. xanthogastra and C. atrata are marked by grey shadow.


Table 3
Cytochrome b DNA differences between C. x. stejnegeri and C. atrata.


Table 4
Cytochrome b DNA differences between C. x. stejnegeri and C. xanthogastra.


In order to further study this close relationship between C. x. stejnegeri and C. atrata, cytochrome b DNA sequences of the concerned three taxa were compared codon by codon according to their position number and the mutation order inside codon. Two comparisons were made: C. x. stejnegeri vs C. atrata (Table 3) and C. x. stejnegeri vs C. xanthogastra (Table 4).

C. x. stejnegeri and C. atrata comparison show four mutations, one with a mutation in the first base of codon number 4, and the other three located at the third position of codon 71, 80 and 260 (Table 3). All of these mutations were synonymous, they do not imply change at the protein level, and they were transitions. More abundant mutations have been found between C. x. stejnegeri and C. xanthogastra DNA sequences (Table 4). One of them was found in the first base of the codon (168 codon), and the rest were found in the third position of codons 30, 71, 99, 123, 186, 199, 238, 271, 278 and 306. All of these mutations were synonymous: they do not imply change at protein level; however, one of them was a transversion as compared to (Table 3) (C. x. stejnegeri vs C. atrata) where of them all were transitions.

4. DISCUSSION

South American siskins present close molecular genetics and phenotype relationships, as observed in Fig. (3). In fact, Fig. (3B) shows a very rapid regional radiation of most South American siskins except for Carduelis barbata, which seems the closest extant relative to parental Carduelis barbata. This is striking since present-day habitats of both birds are the most distant ones, (Mexico for C. notata and southern Chile for C. barbata) [12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.]. It was established that South American siskin radiation occurred between 5-3 MYA [3Arnaiz-Villena A, Areces C, Rey D, et al. Three different North American siskin/goldfinch evolutionary radiations (genus Carduelis): Pine Siskin Green Morphs and European Siskins in America. Open Ornithol J 2012; 5(1): 73-81.
[http://dx.doi.org/10.2174/1874453201205010073]
, 7Arnaiz-Villena A, Alvarez-Tejado M, Ruíz-del-Valle V, et al. Phylogeny and rapid northern and southern hemisphere speciation of goldfinches during the Miocene and Pliocene epochs. Cell Mol Life Sci 1998; 54(9): 1031-41.
[http://dx.doi.org/10.1007/s000180050230] [PMID: 9791543]
, 10Arnaiz-Villena A, Ruiz-del-Valle V, Gomez-Prieto P. Phylogeography of finches and sparrows 2009. Available from https://www.acade mia.edu /38868100/In_Animal_Genetics_PHYLOGEOGRAPHY_OF _FINCHES_AND_SPARROWS] and speciation of most South American siskins occurred rapidly and in more recent time (Pleistocene glaciations), (Figs. 3B, 3C) and [3Arnaiz-Villena A, Areces C, Rey D, et al. Three different North American siskin/goldfinch evolutionary radiations (genus Carduelis): Pine Siskin Green Morphs and European Siskins in America. Open Ornithol J 2012; 5(1): 73-81.
[http://dx.doi.org/10.2174/1874453201205010073]
, 7Arnaiz-Villena A, Alvarez-Tejado M, Ruíz-del-Valle V, et al. Phylogeny and rapid northern and southern hemisphere speciation of goldfinches during the Miocene and Pliocene epochs. Cell Mol Life Sci 1998; 54(9): 1031-41.
[http://dx.doi.org/10.1007/s000180050230] [PMID: 9791543]
, 10Arnaiz-Villena A, Ruiz-del-Valle V, Gomez-Prieto P. Phylogeography of finches and sparrows 2009. Available from https://www.acade mia.edu /38868100/In_Animal_Genetics_PHYLOGEOGRAPHY_OF _FINCHES_AND_SPARROWS].

4.1. Singular Peru Coast Geography and Climate

Most Peru coast except its northernmost part is dry and desert; some parts where any river cut it and ravines appear, more humid weather may occur. In addition, most coastal Peru is high and is a part of Mt. Andes. The cold Humboldt ocean stream makes the coastal climate unexpectedly cold according to its latitude. It should be tropical-like according to its equatorial proximity, and similar to that of Ecuador Country. Peru extreme coast climate and also Mt Andes may have stopped C. xanthogastra to thrive in Peru while it does in southernmost Ecuador. In addition, it has been shown that South American siskin/golfinch speciation has particularly been favoured in Mt. Andes [25Beckman EJ, Witt CC. Phylogeny and biogeography of the New World siskins and goldfinches: Rapid, recent diversification in the Central Andes. Mol Phylogenet Evol 2015; 87: 28-45.
[http://dx.doi.org/10.1016/j.ympev.2015.03.005] [PMID: 25796324]
]. Most of C.xanthogastra thriving range has a tropical and or less extreme weather and altitude (Fig. 2) [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12., 12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993., 14Lafresnaye AD and d’Orbigny D. Synopsis avium. Magasin de Zoologie (París) 1837; 7: 83., 26de Gisignies DB. Descriptions of some new species of Birds. Ann Mag Nat Hist 1855; 16(94): 298-300.
[http://dx.doi.org/10.1080/037454809495537]
]: its range includes, the Cordillera Central to Cordillera Talamanca, Costa Rica, to western Chiriquí, western Panama, Andes of Colombia (except Nariño), Perija Mountains, Colombia/Venezuela, also coastal mountains (west to Yaracuy) and Andes, south of Merida, Venezuela; also irregularly recorded in El Oro and Pichincha, western Ecuador; extreme southeast Peru (Puno) to central Bolivia (La Paz and Santa Cruz); scarce in Ecuador. All thriving range with tropical and/or mild weather except for southern Peru and adjacent Bolivia highlands,where C/S x.stegnegeri inhabits. All these factors may have stop C. xanthogastra to thrive throughout Peru (Fig. 2).

4.2. Carduelis xanthogastra vs Carduelis x. stejnegeri

Carduelis xanthogastra and its still considered subspecies of C. x. stejnegeri, as described in the study [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12.-13Du Bus G. Bulletins de l'Académie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique. Bruxelles 1855; XXII(Part 1): 152-53.]. The resemblance between these two “subspecies” was quite strong, phenotypes were similar in males. However, nominal C. xanthogastra female is different from the male [1Sibley CG, Monroe BL. Distribution and Taxonomy of Birds of the World 1990., 11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12.-13Du Bus G. Bulletins de l'Académie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique. Bruxelles 1855; XXII(Part 1): 152-53.]. No uniform black is seen and the general colour is dull olive-green above [12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.]. Nominal C. xanthogastra habitat was described from Costa Rica to Ecuador, including areas of Colombia and Venezuela (Fig. 2). In contrast, C. x. stejnegeri male was described as being similar to nominal, but the female colour was also similar to the male. According to Mr. Buckley, no dull olive-green like in nominal was observed, but black and yellow similar to males were obvious. In Dr. Sclater's collection, a Bolivian specimen collected by Mr. D. Forbes had dark olive-green above with some yellow spots in the crown: [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12.]. In either case, the plumage of hen is very different from nominal C. xanthogastra hen, (Figs. 5, 6) [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12., 12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.].

Fig. (4)
AC. x. stejnegeri (male) photographed by Fernando Dolset. BC. atrata (male) photographed by A. Arnaiz-Villena (Specimen from El Alto, La Paz, Bolivia)


Fig. (5)
A Scheme of male C. x. stejnegeri from [15Restall R, Rodner C, Lentino R. Birds of Northern South America 2006.]. B Scheme of female C. x. stejnegeri taken from [16Schulenberg TS, Stotz DF, Lane DF, O’Neill JP, Parker TA III. Birds of Peru: Revised and updated edition 2010.].



Fig. (6)
Carduelis xanthogastra stejnegeri. Sexed female. It cannot be confused with C. atrata females which may thrive in the same area (breeding season), usually at a higher altitude, see also Fig. (2, 5). C. atrata females show a full black back; the back is less bright than in the male. Sometimes, both sexes are difficult to distinguish [12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.]. C. xanthogastra stejnegeri, female (La Paz, Bolivia) photographed by A. Arnaiz-Villena.


Our female specimen is shown in Figs. (5 and 6). Carduelis x. stejnegeri habitat was described to be in Bolivia (Sorata and Mapiri towns) [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12.]. Our genetic data show that C. x. stejnegeri is close to C. atrata, which is full black in both sexes except a yellow wing stripe and yellow lower abdomen and thighs [16Schulenberg TS, Stotz DF, Lane DF, O’Neill JP, Parker TA III. Birds of Peru: Revised and updated edition 2010.] (Figs. 4-6). C. atrata habitat was described in South Peru, Bolivia and North Argentina, down to Mendoza City [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12., 12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993., 14Lafresnaye AD and d’Orbigny D. Synopsis avium. Magasin de Zoologie (París) 1837; 7: 83.]. In Fig. (3B), a linearized ML tree, nominal C. xanthogastra species appeared on Earth about 1.4 MYA in South America (Fig. 3C), however ,both sister species C. x. stejnegeri and C. atrata appeared on Earth later, around 500,000 years ago, being one of them ancestral or ancestor has disappeared now. This is not distinguished by our present genetic study.

4.3. Carduelis atrata vs Carduelis x. stejnegeri

Carduelis atrata was described by Lafresnaye and D’Orbigny, 1837 [14Lafresnaye AD and d’Orbigny D. Synopsis avium. Magasin de Zoologie (París) 1837; 7: 83.]. This has been maintained as a monotypic species without subspecies, and it does not present sexual dimorphism. (Material and Methods Section). Both sexes are black and adult male shows brighter black colours, as shown in Figs. (1, 2, 4) [12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993., 14Lafresnaye AD and d’Orbigny D. Synopsis avium. Magasin de Zoologie (París) 1837; 7: 83.].

Carduelis. x. stejnegeri male is still regarded as a Carduelis xanthogastra subspecies in modern books but slightly larger [12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.]. It was originally described as “rather larger” [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12.] and was considered a separate species because of C. x. stejnegeri shows less male/female dimorphism than expected like it occurs in Carduelis atrata where both sexes are black, with a yellow wings strip and yellow on belly and tail spots [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12.]. C. x. stejnegeri female was not “dull olive-green above” but similar to male or, according to others, a bit duller [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12., 12Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.]. Observations during 3 different years confirmed no sex marked differences (Figs. 5, 6). Habitat was described in Bolivia (Sorata, Nairapi) [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12.]; this is coincidental with our own observations. This species was observed in breeding raining season (December-February) around La Paz. It was not observed in Santa Cruz lower lands or Peru highlands, but only in warmer valleys about 2,500 – 3,500 meters (8,202 – 11,482 feet) altitude. This somewhat contradicts information detailed in the study [11Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12.], at least in the breeding season. Seasonal movements are not discarded in the non-breeding season.

Thus, C. atrata and C. xanthogastra stejnegeri are birds bigger than C. xanthogastra; sexes show little colour differences in contrast to C. xanthogastra, as shown in Figs. (1,5 and 6), and they have overlapping habitats, while C. xanthogastra habitats are further North-separated by Peru and 1,761.7 Km, 1,094.6 miles distance (Fig. 2).


CONCLUSION

  1. C. xanthogastra stegnejeri is a subspecies or a close species of C. atrata. (Figs. 4A, 4B, 5A, 5B, 6). Genetics analyses also confirm it, as shown in Figs. (3, 4) and (Tables 2, 3, 4).
  2. Linearized ML mt cytochrome phylogenetics show that both C. x. stejnegeri and C. atrata appeared on Earth much later than C. xanthogastra.
  3. Habitat of C. atrata and C. x. stejnegeri overlaps, although more restricted for the latter, which thrives at lower and warmer Bolivia highlands valleys in the breeding season.
  4. C. x. stejnegeri sexes are more monotypic, similar to those of Carduelis notata, which is the extant parental species of the South American radiation.
  5. We propose for naming this species or C. atrata subspecies the provisional name of C. lapazensis since it has been first observed and characterized in phenotype and genetics in samples at La Paz (Bolivia) surroundings. Moreover, ongoing phenotypic studies are being performed.
  6. It is not genetically possible to establish a clear distinction between C. atrata / C. x. stejgeneri, as it occurs with other South American Siskin species, probably, because of close relatedness and recent speciation or phenotypic change [2Arnaiz-Villena A, Guillén J, Ruiz-del-Valle V, et al. Phylogeography of crossbills, bullfinches, grosbeaks, and rosefinches. Cell Mol Life Sci 2001; 58(8): 1159-66.
    [http://dx.doi.org/10.1007/PL00000930] [PMID: 11529508]
    , 3Arnaiz-Villena A, Areces C, Rey D, et al. Three different North American siskin/goldfinch evolutionary radiations (genus Carduelis): Pine Siskin Green Morphs and European Siskins in America. Open Ornithol J 2012; 5(1): 73-81.
    [http://dx.doi.org/10.2174/1874453201205010073]
    ].

APPENDIX 1

ORIGINAL SPECIES BIRDS DESCRIPTIONS

C. xanthogastra description, may be consulted in Sharpe 1888 [11], Du Bus 1855 [13] and Clement et al. 1993 [12].

Description was like this: “Adult male: general colour above uniform black including the whole of the wing-coverts, bastard-wing, and primary-coverts: quills black, yellow at the base, with black shafts, on the secondaries, the innermost of which are entirely black; upper tail-coverts and center tail-feathers black, the remainder yellow for the basal half; head all round, sides of neck, and entire throat black; remainder of under surface yellow, greener on the sides of body and flanks; thighs black; under tail-coverts yellow; under wing-coverts and axillaries yellow, the former with blackish, yellow towards the base of the inner web. Total length 4.5 inches, Culmen 0.4, wing 2.6, tail 1.5, tarsus 0.6.

Adult female: different from the male. General colour above dull olive-green; lesser wing-coverts like the back; median and greater coverts dusky blackish, tipped with pale olive-green, whitish at the ends; bastard-wing, primary-coverts, and quills dusky blackish, fringed with pale olive-green, whitish at the ends of the secondaries; upper tail-coverts like the back; tail-feathers dusky blackish, edged with olive-green; crown of head like the back; sides of face olive-greenish, a little yellower on the fore part of the cheeks; throat and under tail-coverts; thighs ashy; under wing-coverts and axillaries ashy, fringed with olive-yellow; quills below dusky; ashy along the inner web. Total length 4 inches, culmen 0.4, wing 2.35, tail 1.45, tarsus 0.45.”

C. x. stejnegeri was described (first in 1855 by Du Bus), may be consulted in Sharpe 1888 [11] and Clement et al. 1993 [12].

Description was like this: “Adult male: similar to C. xanthogastra, but rather larger, and distinguished by its yellow things, larger yellow wing-patch (the greater coverts being tipped with yellow), and whitish edgings to 4 inches, culmen 0.45, wing 2.7, tail 1.55, tarsus 0.55.

Adult female: According to Mr. Bukley is like the male, but with colours not so bright. Total length 4 inches, culmen 0.4, wing 2.5, tail 1.55, tarsus 0.5.

If the similarity in the colour of the sexes is really correctly determined, it is another proof of the difference between C. x. stejnegeri and C.xanthogastra, with which it has always been united.

In Dr. Sclater's collection is a Bolivian specimen collected by Mr. D. Forbes and marked a female (apparently by Dr. Sclater himself), which is dark olive-green above with some yellow spots on the crown; the head and sides of face are dingy greenish, blacker on the lores and region of the eye; wing-coverts greenish or edged with the latter colour; otherwise the wing marked as in the male but more dingy black, the greater coverts being tipped with yellow; under surface of body yellow, the throat being dull greenish. This seems to me more likely to be the plumage of the adult female, and I think Mr. Bukley's identification must be wrong. In either case the plumage of the hen bird is very different from that of the female of C. xanthogastra.”

C. atrata was described in Lafresnaye and d’Orbigny 1837 [14], Sharpe 1888 [11] and Clement et al. 1993 [12].

Description was like this: “Adult male: general colour above sooty black. Wing-coverts black. The greater coverts tipped with yellow. Bastard-wing and primary-covers black. Quills yellow at base, black at the ends, the inner secondary entirely black. Upper tail-coverts and center tail-feathers black, the rest yellow at base, black at the ends. Head black all rounds as well as the entire under surface, excepting the abdomen and under tail-coverts, which are yellow. Things pale yellow. Under wing-coverts and axillaries yellow, the lower primary-coverts black: quills below blackish, yellow at base. Total length 4.8 inches, culmen 0.4, wing 3.15, tail 1.9, tarsus 0.6.

Adult female: differs from the male only in being more brownish black. The median as well as the greater coverts tipped with pale yellow, and the quills edged with yellowish white near the end of the outer web. The yellow on the under surface is rather paler and extends up to the fore neck, but is mottled with brown on the breast. Total length 4.8 inches, culmen 0.4, wing 3.2, tail 2, tarsus 0.6.”

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This study was approved by the Ethics Committée of University Complutense, Spain on March 13th 2008. Ethical approval number is 2008-AAV-UC.003.

HUMAN AND ANIMAL RIGHTS

No humans were used in this study. All animal procedures were performed in accordance with the International and Madrid Regional Laws. Permission for publication is issued for Researches attached to University Complutense, Madrid, Spain.

CONSENT FOR PUBLICATION

Not applicable.

AVAILABILITY OF DATA AND MATERIALS

Material is deposited in Immunology Dept, University Complutense, Madrid, Spain [https://www.ucm.es/micro biologia-1/antonio-arnaiz-villena]. International data is also deposited in GeneBank [https://www.ncbi.nlm.nih.gov/nucleo tide/].

FUNDING

This work was supported by grants from the Spanish Ministry of Science and Universities (PI14/01067, PI18/00720 and PI18/00626) and European FEDER funds.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

We thank Fabian Beltran and Fernando Dolset for their photographs depicted in Figs.(2 and 4).

REFERENCES

[1] Sibley CG, Monroe BL. Distribution and Taxonomy of Birds of the World 1990.
[2] Arnaiz-Villena A, Guillén J, Ruiz-del-Valle V, et al. Phylogeography of crossbills, bullfinches, grosbeaks, and rosefinches. Cell Mol Life Sci 2001; 58(8): 1159-66.
[http://dx.doi.org/10.1007/PL00000930] [PMID: 11529508]
[3] Arnaiz-Villena A, Areces C, Rey D, et al. Three different North American siskin/goldfinch evolutionary radiations (genus Carduelis): Pine Siskin Green Morphs and European Siskins in America. Open Ornithol J 2012; 5(1): 73-81.
[http://dx.doi.org/10.2174/1874453201205010073]
[4] Arnaiz-Villena A, Ruiz-del-Valle V, Gomez-Prieto P, et al. Carduelini New Sistematics: Crimson-winged Finch (Rhodopechys sanguineus) is Included in “Arid-Zone” Carduelini Finches by Mitochondrial DNA Phylogeny. Open Ornithol J 2014; 7: 55-62.
[http://dx.doi.org/10.2174/1874453201407010055]
[5] Arnaiz-Villena A, Ruiz del Valle V, Reguera R, Gomez-Prieto P, Serrano-Vela JI. What might have been the ancestor of New World siskins? Open Ornithol J 2008; 1: 46-7.
[http://dx.doi.org/10.2174/1874453200801010046]
[6] Arnaiz-Villena A, Moscoso J, Ruiz-del-Valle V, et al. Mitochondrial DNA phylogenetic definition of a group of ‘arid-zone’ Carduelini finches. Open Ornithol J 2008; 1(1): 1-7.
[http://dx.doi.org/10.2174/1874453200801010001]
[7] Arnaiz-Villena A, Alvarez-Tejado M, Ruíz-del-Valle V, et al. Phylogeny and rapid northern and southern hemisphere speciation of goldfinches during the Miocene and Pliocene epochs. Cell Mol Life Sci 1998; 54(9): 1031-41.
[http://dx.doi.org/10.1007/s000180050230] [PMID: 9791543]
[8] Arnaiz-Villena A, Alvarez-Tejado M, Ruiz-del-Valle V, et al. Rapid radiation of canaries (genus Serinus). Mol Biol Evol 1999; 16(1): 2-11.
[http://dx.doi.org/10.1093/oxfordjournals.molbev.a026034]
[9] Arnaiz-Villena A, Moscoso J, Ruiz-del-Valle V, et al. Bayesian phylogeny of Fringillinae birds: status of the singular African oriole finch Linurgus olivaceus and evolution and heterogeneity of the genus Carpodacus. Dong Wu Xue Bao 2007; 53(5): 826-34.
[10] Arnaiz-Villena A, Ruiz-del-Valle V, Gomez-Prieto P. Phylogeography of finches and sparrows 2009. Available from https://www.acade mia.edu /38868100/In_Animal_Genetics_PHYLOGEOGRAPHY_OF _FINCHES_AND_SPARROWS
[11] Sharpe RB. Catalogue of the Passeriformes or Perching Birds, in the collection of the British Museum. Fringillidae. Cat Birds Brit Mus 1888; XXII(Part III): 209-12.
[12] Clement P, Harris A, Davis J. Finches and Sparrows Helm Identification Guides 1993.
[13] Du Bus G. Bulletins de l'Académie Royale des Sciences, des Lettres et des Beaux-Arts de Belgique. Bruxelles 1855; XXII(Part 1): 152-53.
[14] Lafresnaye AD and d’Orbigny D. Synopsis avium. Magasin de Zoologie (París) 1837; 7: 83.
[15] Restall R, Rodner C, Lentino R. Birds of Northern South America 2006.
[16] Schulenberg TS, Stotz DF, Lane DF, O’Neill JP, Parker TA III. Birds of Peru: Revised and updated edition 2010.
[17] Zamora J, Lowy E, Ruiz-del-Valle V, et al. Rhodopechys obsoleta (desert finch): A pale ancestor of greenfinches (Carduelis spp.) according to molecular phylogeny. J Ornithol 2006; 147(3): 448-56.
[http://dx.doi.org/10.1007/s10336-005-0036-2]
[18] Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011; 28(10): 2731-9.
[http://dx.doi.org/10.1093/molbev/msr121] [PMID: 21546353]
[19] Felsenstein J. Evolutionary trees from DNA sequences: A maximum likelihood approach. J Mol Evol 1981; 17(6): 368-76.
[http://dx.doi.org/10.1007/BF01734359] [PMID: 7288891]
[20] Swofford D. Phylogenetic analysis using parsimony and other methods. Sunderland. MA: Sinauer Associates 2002; b10.
[21] Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 2001; 17(8): 754-5.
[http://dx.doi.org/10.1093/bioinformatics/17.8.754] [PMID: 11524383]
[22] Ronquist F, Huelsenbeck JP. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003; 19(12): 1572-4.
[http://dx.doi.org/10.1093/bioinformatics/btg180] [PMID: 12912839]
[23] Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics 1998; 14(9): 817-8.
[http://dx.doi.org/10.1093/bioinformatics/14.9.817] [PMID: 9918953]
[24] Thorne JL, Kishino H, Painter IS. Estimating the rate of evolution of the rate of molecular evolution. Mol Biol Evol 1998; 15(12): 1647-57.
[http://dx.doi.org/10.1093/oxfordjournals.molbev.a025892] [PMID: 9866200]
[25] Beckman EJ, Witt CC. Phylogeny and biogeography of the New World siskins and goldfinches: Rapid, recent diversification in the Central Andes. Mol Phylogenet Evol 2015; 87: 28-45.
[http://dx.doi.org/10.1016/j.ympev.2015.03.005] [PMID: 25796324]
[26] de Gisignies DB. Descriptions of some new species of Birds. Ann Mag Nat Hist 1855; 16(94): 298-300.
[http://dx.doi.org/10.1080/037454809495537]
Track Your Manuscript:


Endorsements



"Open access will revolutionize 21st century knowledge work and accelerate the diffusion of ideas and evidence that support just in time learning and the evolution of thinking in a number of disciplines."


Daniel Pesut
(Indiana University School of Nursing, USA)

"It is important that students and researchers from all over the world can have easy access to relevant, high-standard and timely scientific information. This is exactly what Open Access Journals provide and this is the reason why I support this endeavor."


Jacques Descotes
(Centre Antipoison-Centre de Pharmacovigilance, France)

"Publishing research articles is the key for future scientific progress. Open Access publishing is therefore of utmost importance for wider dissemination of information, and will help serving the best interest of the scientific community."


Patrice Talaga
(UCB S.A., Belgium)

"Open access journals are a novel concept in the medical literature. They offer accessible information to a wide variety of individuals, including physicians, medical students, clinical investigators, and the general public. They are an outstanding source of medical and scientific information."


Jeffrey M. Weinberg
(St. Luke's-Roosevelt Hospital Center, USA)

"Open access journals are extremely useful for graduate students, investigators and all other interested persons to read important scientific articles and subscribe scientific journals. Indeed, the research articles span a wide range of area and of high quality. This is specially a must for researchers belonging to institutions with limited library facility and funding to subscribe scientific journals."


Debomoy K. Lahiri
(Indiana University School of Medicine, USA)

"Open access journals represent a major break-through in publishing. They provide easy access to the latest research on a wide variety of issues. Relevant and timely articles are made available in a fraction of the time taken by more conventional publishers. Articles are of uniformly high quality and written by the world's leading authorities."


Robert Looney
(Naval Postgraduate School, USA)

"Open access journals have transformed the way scientific data is published and disseminated: particularly, whilst ensuring a high quality standard and transparency in the editorial process, they have increased the access to the scientific literature by those researchers that have limited library support or that are working on small budgets."


Richard Reithinger
(Westat, USA)

"Not only do open access journals greatly improve the access to high quality information for scientists in the developing world, it also provides extra exposure for our papers."


J. Ferwerda
(University of Oxford, UK)

"Open Access 'Chemistry' Journals allow the dissemination of knowledge at your finger tips without paying for the scientific content."


Sean L. Kitson
(Almac Sciences, Northern Ireland)

"In principle, all scientific journals should have open access, as should be science itself. Open access journals are very helpful for students, researchers and the general public including people from institutions which do not have library or cannot afford to subscribe scientific journals. The articles are high standard and cover a wide area."


Hubert Wolterbeek
(Delft University of Technology, The Netherlands)

"The widest possible diffusion of information is critical for the advancement of science. In this perspective, open access journals are instrumental in fostering researches and achievements."


Alessandro Laviano
(Sapienza - University of Rome, Italy)

"Open access journals are very useful for all scientists as they can have quick information in the different fields of science."


Philippe Hernigou
(Paris University, France)

"There are many scientists who can not afford the rather expensive subscriptions to scientific journals. Open access journals offer a good alternative for free access to good quality scientific information."


Fidel Toldrá
(Instituto de Agroquimica y Tecnologia de Alimentos, Spain)

"Open access journals have become a fundamental tool for students, researchers, patients and the general public. Many people from institutions which do not have library or cannot afford to subscribe scientific journals benefit of them on a daily basis. The articles are among the best and cover most scientific areas."


M. Bendandi
(University Clinic of Navarre, Spain)

"These journals provide researchers with a platform for rapid, open access scientific communication. The articles are of high quality and broad scope."


Peter Chiba
(University of Vienna, Austria)

"Open access journals are probably one of the most important contributions to promote and diffuse science worldwide."


Jaime Sampaio
(University of Trás-os-Montes e Alto Douro, Portugal)

"Open access journals make up a new and rather revolutionary way to scientific publication. This option opens several quite interesting possibilities to disseminate openly and freely new knowledge and even to facilitate interpersonal communication among scientists."


Eduardo A. Castro
(INIFTA, Argentina)

"Open access journals are freely available online throughout the world, for you to read, download, copy, distribute, and use. The articles published in the open access journals are high quality and cover a wide range of fields."


Kenji Hashimoto
(Chiba University, Japan)

"Open Access journals offer an innovative and efficient way of publication for academics and professionals in a wide range of disciplines. The papers published are of high quality after rigorous peer review and they are Indexed in: major international databases. I read Open Access journals to keep abreast of the recent development in my field of study."


Daniel Shek
(Chinese University of Hong Kong, Hong Kong)

"It is a modern trend for publishers to establish open access journals. Researchers, faculty members, and students will be greatly benefited by the new journals of Bentham Science Publishers Ltd. in this category."


Jih Ru Hwu
(National Central University, Taiwan)


Browse Contents




Webmaster Contact: info@benthamopen.net
Copyright © 2023 Bentham Open