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Species limits and biogeography of Rhynchospiza sparrows

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Abstract

The genus Rhynchospiza comprises two species, the monotypic Tumbes Sparrow (R. stolzmanni) and the Stripe-crowned Sparrow (R. strigiceps) with subspecies strigiceps and dabbenei. In the study reported here we evaluated the taxonomic status of these taxa and discussed key features involved in speciation. All three taxa exhibited multiple differences in plumage, morphology, and vocalizations, supporting the recognition of three species in Rhynchospiza. The very large-billed R. stolzmanni has a song composed of a succession of faster complex trilled phrases, shows a small black loral line and dark-chestnut head stripes with large dark central-stripe to individual feathers, and is resident in the Tumbes region. The large and heavy dabbenei has a song consisting of a series of simple chirping notes, shows a large black loral crescent and chestnut head stripes with a reduced to absent dark center to feathers, and inhabits the Austral Yungas as a year-round resident. The small and pale strigiceps has a song consisting of a succession of complex trilled phrases, shows a small black loral line and rufous-brown head stripes with large dark central-stripe to feathers, and inhabits Dry and Sierran Chaco where it is a partial migrant. Locality data and ecological niche modeling show that dabbenei and strigiceps are allo-parapatric and use different altitudinally segregated habitats at their zone of parapatry. Molecular phylogenetic analyses (NADH dehydrogenase 2 [ND2] gene) revealed R. stolzmanni to be sister (11.5% divergent) to a recently diverged dabbenei and strigiceps clade (1.6% divergent). We conclude that the genus Rhynchospiza comprises three species-level entities, each restricted to a major biogeographic region, and that vocalizations and facial patterns provide key evidence on species limits in these otherwise similarly plumaged taxa. The evolutionary–cultural differences in songs, with complex phrases in those of R. strigiceps and R. stolzmanni, and single notes in the songs of R. dabbenei, suggest changes in the innate vocal learning template during speciation in the latter.

Zusammenfassung

Artabgrenzung und Biogeographie der Neuweltammer-Gattung Rhynchospiza

Die Gattung Rhynchospiza umfasst zwei Arten, die monotypische Tumbesammer (R. stolzmanni) und die Streifenscheitelammer (R. strigiceps) mit den Unterarten strigiceps und dabbenei. Wir beurteilen hier den taxonomischen Status und diskutieren die Schlüsselmerkmale der Artbildung. Alle drei Taxa zeigten zahlreiche Unterschiede im Gefieder, in der Morphologie und der Lautäußerung, was die Unterscheidung der drei Arten in der Gattung Rhynchospiza unterstützt. Die Art R. stolzmanni besitzt einen kräftigen Schnabel, hat einen Gesang zusammengesetzt aus einer Abfolge von schnellen, komplexen Triller-Phrasen, weist einen schmalen schwarzen Zügelstreifen und einen kastanienbraun gefärbten Scheitelseitenstreifen mit einzelnen Federn auf, die breite dunkle Federzentren besitzen, und sie ist in der Tumbes-Region (Peru) heimisch. Die große und schwere Unterart dabbenei besitzt einen Gesang aus einer Serie von einfachen Tschilp-Elemente, einen großen schwarzen, halbmondförmigen Zügelstreifen, rotbraun gefärbte Scheitelseitenstreifen, deren Federn nur schwache bis fehlende dunkle Federzentren aufweisen, und sie bewohnt den südlichen Yungas (Region in Bolivien) als Jahresvogel. Die kleine und blass gefärbte Unterart strigiceps besitzt einen Gesang zusammengesetzt aus einer Abfolge an komplexen Triller-Phrasen, hat einen kleinen schwarzen Zügelstreifen, rötlichbraune Scheitelseitenstreifen mit Federn mit großen dunklen Federzentren und lebt in „Dry Chaco“und „Sierra Chaco“als Teilzieher. Verbreitungsdaten und ökologische Nischenmodellierungen zeigen, dass die Unterarten dabbenei und strigiceps allo-parapatrisch sind und aufgrund unterschiedlicher Höhenlagen getrennte Habitate ihres parapatrischen Verbreitungsgebiets nutzen. Molekularphylogenetische Analysen (ND2 Gene) haben gezeigt, dass R. stolzmanni eine Schwesterart (11.5% Divergenz) der jüngst aufgespaltenen Klade dabbenei und strigiceps (1.6% Divergenz) ist. Wir folgern daraus, dass die Gattung Rhynchospiza drei Einheiten auf Artniveau umfasst, jede davon beschränkt auf eine große biogeographische Region. Die Lautäußerungen und Kopfzeichnungen bieten Schlüsselmerkmale zur Artenabgrenzung in diesem, ansonsten ähnlich gefiederten Taxa. Die evolutionskulturellen Unterschiede im Gesang, die komplexen Phrasen in R. strigiceps und R. stolzmanni sowie die Einzelsilben in R. dabbenei weisen darauf hin, dass bei Letzterer Änderungen in den angeborenen Gesangslernmustern während der Artbildung entstanden sind.

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Acknowledgements

We thank all recordists, birdwatchers, and collectors who through time have helped build an impressive database. We thank Patricia Capllonch for clarification on some Tucumán localities and for making CENAA data available; Markus Unsöld (ZSM), Ben Marks and Mary Hennen (FMNH), Sara Bertelli and Sebastián Aveldaño (FML), J.V. Remsen Jr (LSUMNS), Yolanda Davies (MACN), Diego Montalti (MLP), Kristof Zyskowski (YPM), Stephen P. Rogers (CM), Nate Rice (ANSP), Hein Van Grow (BMNH), Paul Sweet (AMNH), and Carla Cicero (MVZ) for information on, access to, or pictures of museum specimens under their care; Carlos and Silvia Ferrari for advice on fieldwork with R. strigiceps; and G. Núñez-Montellano, E. Gulson, and T. Pegan for field companionship. Matt Medler and Matt Young promptly provided sound recordings from the MLNS. G. Núñez allowed use of his photograph of R. dabbenei and R. Ahlman of his photograph of R. stolzmanni. Carlos Bianchi provided crucial help by making the maps. Juan Freile, Fernando Angulo Pratolongo, and Tom Schulenberg helped clarify the distribution of R. stolzmanni. Fabricio C. Gorleri helped with sampling event data from eBird and illustrated the birds shown in the phylogenetic tree. John Klicka granted access to his lab and samples for phylogenetic analyses. This contribution was possible thanks to funding by a CONICET grant to JIA for the project “Taxonomía de las aves de los Andes del noroeste de Argentina” (Grant no. 3216/12).

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Authors and Affiliations

  1. Instituto de Bio y Geociencias del Noroeste Argentino (IBIGEO-CONICET), Laboratorio de Ecología, Comportamiento y Sonidos Naturales (ECOSON), Rosario de Lerma, Salta, Argentina

    Juan I. Areta, Emiliano A. Depino & Ingrid Holzmann

  2. Villa María, Córdoba, Argentina

    Sergio A. Salvador

  3. Museum of Natural Science, Louisiana State University, Baton Rouge, LA, USA

    Steven W. Cardiff

  4. Burke Museum of Natural History and Culture and Department of Biology, University of Washington, Seattle, WA, USA

    Kevin Epperly

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  1. Juan I. Areta
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Electronic supplementary material

Below is the link to the electronic supplementary material.

10336_2019_1695_MOESM1_ESM.xlsx

Supplementary material 1 Online Resource 1. Main database of all threeRhynchospizaspecies. List of measured and/or studied specimens, distributional records and sound recordings, type specimens and morphometric data of Yungas Sparrow (Rhynchospiza dabbenei), Chaco Sparrow (Rhynchospiza strigiceps) and Tumbes Sparrow (Rhynchospiza stolzmanni) obtained in this study. (XLSX 7063 kb)

10336_2019_1695_MOESM2_ESM.pdf

Supplementary material 2 Online Resource 2. Morphological characterization of Chaco Sparrow (R. strigiceps), Yungas Sparrow (Rhynchospiza dabbenei), and Tumbes Sparrow (R. stolzmanni). Measurements reported as mean ± SD, with range between square brackets and sample size between parentheses. All measurements in mm, except for weight in grams. Letters indicate significant sexual dimorphism within each taxon at alfa = 0.05 for Mann–Whitney U two-tailed tests. See Fig. 3 for interspecific comparisons. (PDF 58 kb)

10336_2019_1695_MOESM3_ESM.pdf

Supplementary material 3 Online Resource 3. Potential, geographic, seasonal and altitudinal distributions of all threeRhynchospizaspecies. A) Geographic and potential distribution of Yungas Sparrow (Rhynchospiza dabbenei) based on ecological-niche models using the full dataset. B) Geographic and potential distribution of Chaco Sparrow (Rhynchospiza strigiceps) based on ecological-niche models using the full dataset. C) Geographic and potential distribution of Yungas Sparrow (Rhynchospiza dabbenei) and Chaco Sparrow (Rhynchospiza strigiceps) and based on ecological-niche models using the full dataset of dabbenei and breeding records only in strigiceps. D) Geographic and potential distribution of Tumbes Sparrow (Rhynchospiza stolzmanni) based on ecological-niche models using the full dataset. E) Geographic, seasonal and altitudinal distribution of Yungas Sparrow (Rhynchospiza dabbenei) and Chaco Sparrow (Rhynchospiza strigiceps). F) Geographic, seasonal and altitudinal distribution of Tumbes Sparrow (Rhynchospiza stolzmanni). (PDF 19191 kb)

10336_2019_1695_MOESM4_ESM.pdf

Supplementary material 4 Online Resource 4. Bestiaries of songs of all threeRhynchospizaspecies. A) Yungas Sparrow (Rhynchospiza dabbenei). B) Chaco Sparrow (Rhynchospiza strigiceps). C) Tumbes Sparrow (Rhynchospiza stolzmanni). See Online Resource 1 for recording data. (PDF 7908 kb)

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Supplementary material 5 Online Resource 5. Phylogenetic tree of allRhynchospizataxa (ND2 gene) and expanded selection of species from closely related genera. MCC tree from BEAST with posterior probability values above the nodes and corresponding maximum likelihood bootstrap value from RAxML below node; “–” indicates that the specific node did not occur in the RAxML tree. (TIFF 765 kb)

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Supplementary material 6 Online Resource 6. Estimates of evolutionary divergence between ND2 gene sequences of allRhynchospizataxa and selected species species from closely related genera. The number of base substitutions per site from between sequences are shown. Rhynchospiza taxa are highlighted in bold font. See Methods for details. (PDF 86 kb)

Appendix 1: Museum source and localities of specimens used in phylogenetic reconstructions

Appendix 1: Museum source and localities of specimens used in phylogenetic reconstructions

Taxon

Sample sourcea

Collecting locality

GenBank accession number

Specimen ID

Rhynchospiza stolzmanni

LSUMNS (B‐5227)

PERU: Las Pampas, Km 885 Pan American Hwy., 11 road km N Olmos, Lambayeque

FJ547317

LSUMZ-100779

Rhynchospiza strigiceps

UWBM (DHB2425)

ARGENTINA: 40 km southeast of Joaquín V. González, Salta

MN145865

UWBM-92146

Rhynchospiza dabbenei

UWBM (DHB2376)

ARGENTINA: 24 km north of Salta city, Salta

MN145864

UWBM-92147

Chlorospingus ophthalmicus

MBM (JK99‐074)

HONDURAS: Copan

FJ547290

 

Chlorospingus flavigularis

FMNH (430078)

PERU: Cuzco

FJ547291

 

Peucaea carpalis

MZFC (ORRS102)

MEXICO: Sonora

FJ547309

 

Peucaea sumichrasti

CNAV (Po13226)

MEXICO: Oaxaca

FJ547308

 

Peucaea botterii

LSUMNS (B‐9880)

USA: Arizona

FJ547312

 

Peucaea aestivalis

LSUMNS (B‐2461)

USA: Louisiana

FJ547311

 

Peucaea cassini

MVZ (FC20222)

USA: Oklahoma

FJ547310

 

Peucaea humeralis

CNAV (Po11084)

MEXICO: Morelos

FJ547306

 

Peucaea mysticalis

MZFC (OVMP773)

MEXICO: Puebla

FJ547307

 

Aimophila ruficauda ruficauda

MBM (DAB1680)

NICARAGA: Rivas

FJ547304

 

Aimophila ruficauda acuminata

CNAV (Po13223)

MEXICO: Oaxaca

FJ547305

 

Ammodramus savannarum

BMNH (JK94‐056)

USA: Montana

AF290125

 

Ammodramus humeralis

MBM (GAV1018)

ARGENTINA: Salta

FJ547324

 

Ammodramus aurifrons

J. Avise laboratory (DS74)

Not available

FJ547323

 

Arremonops tocuyensis

Pending

Pending

Pending

 

Arremonops conirostris

MBM (DAB1049)

NICARAGUA: Atlantico Norte

FJ547296

 

Arremonops chloronotus

KU (KU2031)

MEXICO: Campeche

FJ547295

 

Arremonops rufivirgatus

BMNH (X6828)

USA: Texas

FJ547294

 
  1. aMuseum sources for specimens used in this study. LSUMNS Louisiana State University Museum of Natural Science, UWBM University of Washington, Burke Museum of Natural History, MBM Marjorie Barrick Museum of Natural History, FMNH Field Museum of Natural History, MZFC Universidad Nacional Autónoma de Mexico, Museo de Zoología, CNAV Colección Nacional de Aves, MVZ University of California, Berkeley, Museum of Vertebrate Zoology, BMNH James Ford Bell Museum of Natural History, KU University of Kansas Natural History Museum. Those numbers in parentheses represent tissue or collector/preparator numbers instead of study-skin voucher numbers. Most samples were used by DaCosta et al. (2009), except for those of Arremon tocuyensis, Rhynchospiza strigiceps, and Rhynchospiza dabbenei
  2. We provide more details on the key samples of Rhynchospiza taxa (see also ESM 1)

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Areta, J.I., Depino, E.A., Salvador, S.A. et al. Species limits and biogeography of Rhynchospiza sparrows. J Ornithol 160, 973–991 (2019). https://doi.org/10.1007/s10336-019-01695-2

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