Journal of Ornithology (2019) 160:973–991 https://doi.org/10.1007/s10336-019-01695-2

ORIGINAL ARTICLE

Species limits and biogeography of Rhynchospiza sparrows

Juan I. Areta1 · Emiliano A. Depino1 · Sergio A. Salvador2 · Steven W. Cardif3 · Kevin Epperly4 · Ingrid Holzmann1

Received: 17 April 2019 / Revised: 7 July 2019 / Accepted: 18 July 2019 / Published online: 6 August 2019 © Deutsche Ornithologen-Gesellschaft e.V. 2019

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 diferences in plum- age, 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 diferent 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 diferences 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.

Keywords Neotropical birds · Plumage conservatism · Speciation · Specifc mate recognition systems · Vocal template

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 Gefeder, in der Morphologie und der

Communicated by J. T. Lifeld.

Deceased: Sergio A. Salvador.

Electronic supplementary material The online version of this article (https​://doi.org/10.1007/s1033​6-019-01695​-2) contains supplementary material, which is available to authorized users.

* Juan I. Areta 2 Villa María, Córdoba, Argentina [email protected] 3 Museum of Natural Science, Louisiana State University, Baton Rouge, LA, USA 1 Instituto de Bio y Geociencias del Noroeste Argentino (IBIGEO‑CONICET), Laboratorio de Ecología, 4 Burke Museum of Natural History and Culture Comportamiento y Sonidos Naturales (ECOSON), and Department of Biology, University of Washington, Rosario de Lerma, Salta, Argentina Seattle, WA, USA

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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 gefederten 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.

Introduction it is embedded, coupled to the many possible levels of change, lead to the existence of a large number of types Understanding how long-term ecological and geographic of mating groups. The diversity of mating recognition barriers have acted to create biogeographic patterns requires systems includes mating groups that difer in many traits knowledge on the spatial distribution of phenotypes, the key to mate recognition (Zimmer and Whittaker 2000; level of diference between them, and what these difer- Jordan et al. 2018), cryptic species that cannot be safely ences entail from the perspective of facilitating or restrict- distinguished based on external features but instead dif- ing free interbreeding. Characterizing the multidimensional fer in vocalizations (Stein 1958; Ábalos and Areta 2009), phenotypes of populations and assessing the extent of their populations that difer in vocalizations but that seem to be abilities to interbreed remain key endeavors of the study of otherwise identical in plumage and morphology (Schwartz biodiversity. Studies on species limits that provide natural 1975; Areta and Repenning 2011; Areta 2012), the exist- history, morphological, and distributional data and informa- ence of morphs that difer markedly in plumage but appear tion on characters thought to be important in mate choice to interbreed freely (Areta 2008; Areta et al. 2011; Chavar- are paramount to the goal of understanding the origin, dif- ría-Pizarro et al. 2010) or not so freely (Pryke and Grifths ferentiation, and maintenance of lineages. 2009; Falls and Kopachena 2010), taxa with gene fow In birds, an immense array of signaling systems is used in wide or narrow contact zones (Fernando et al. 2016; for mating. Changes in these systems result in the appear- Areta et al. 2017), and the disputed “ring species” or Ras- ance and maintenance of diferent mating groups. Within senkreis (Irwin et al. 2001; Liebers et al. 2004; Alcaide each of these mating groups, genetic recombination is et al. 2014), among other possibilities. This very diversity mediated by a mate recognition system that leads to the and the relational value of mating character changes imply long-term maintenance of the respective groups (Paterson that any search for a generalized quantitative species-level 1980, 1985; Coyne and Orr 2004; Price 2008). Mate rec- threshold is doomed to fail (Tobias et al. 2010; Remsen ognition systems refect the variable emphasis of diferent 2015, 2016; Collar et al. 2016) because no single con- suites of characters, with some systems depending heavily cept or a single taxonomic category can accommodate all on visual cues, others relying more on vocal cues, and still this variation while keeping its explanatory power. Thus, other systems requiring multimodal signaling for proper a more fruitful research program would be to focus on functioning (Bradbury and Vehrencamp 1998; Price 2008). understanding how diferent levels of change in diferent Thus, changes of a certain magnitude in a signaling feature idiosyncratic suites of characters evolve to form coherent cannot be assumed to have a universal efect in all systems. signaling systems that result in complete or partial assorta- Instead, changes of the same magnitude may have drastic tive mating in diferent taxonomic groups. efects in one system but virtually no efect in another. The conservative plumages of “striped-sparrows” in This relative or context-dependent efect of the change the speciose genus Aimophila have resulted in difculties of a feature operating within the mating system in which clarifying their phylogenetic relationships and in sorting

1 3 Journal of Ornithology (2019) 160:973–991 975 them out into species (Storer 1955; Wolf 1977). Molecular phylogenetic data has shown that species formerly included in Aimophila are better allocated among four more or less distantly related genera (Aimophila, Peucaea, Amphispiza and Rhynchospiza) (DaCosta et al. 2009). The pervasive convergence and homeoplastic nature of plumage traits in striped-sparrows provides another case indicating that plum- age is only partially phylogenetically informative to solve relationships among some groups (Omland and Lanyon 2000; DaCosta et al. 2009; Burns et al. 2014). Species lim- its among populations that exhibit few plumage distinctions have been frequently clarifed by improved knowledge of their vocalizations. Thus, vocalizations may hold the key to elucidate the existence of distinct yet unrecognized species among the striped-sparrows. The genus Rhynchospiza currently comprises two species, the monotypic Tumbes Sparrow (R. stolzmanni) from Peru and Ecuador and the geographically variable Stripe-crowned Sparrow (R. strigiceps) with subspecies strigiceps and dab- benei from Argentina, Bolivia, and Paraguay (Hellmayr 1938; Navas 1965; Remsen et al. 2019). The eastern strigi- ceps is smaller and paler than the western dabbenei (Figs. 1, 2), but their diferences have been generally poorly described and confused or neglected in the literature. In a widely cited paper, Short (1975) swapped the characteristics of both taxa, thereby creating confusion, but later clarifed their distin- guishing features (Short 1976). Their distributions have been considered to be allopatric, with strigiceps in the lowlands and Sierras of central Argentina and dabbenei occupying mostly the Andean ranges in northwest Argentina (Navas 1965; Jaramillo 2011). However, at least two presumed records of dabbenei in the arid lowland plain known as the Gran Chaco (Navas 1965) and the mapping of this taxon in the lowlands of Bolivia (Jaramillo 2011) bring into ques- tion the allopatry of their ranges, possibly suggesting lim- ited sympatry. Perhaps due to the superfcial morphological similarity between nominate strigiceps and dabbenei and a reliance on traditional plumage-based taxonomy, the natu- ral history, vocalizations and taxonomic status of the less Fig. 1 Rhynchospiza dabbenei Photographs of adults of the Chaco Sparrow ( widespread have remained obscure. Furthermore, strigiceps), Yungas Sparrow (R. dabbenei), and Tumbes Sparrow while molecular phylogenetic information indicates that R. (R. stolzmanni). a Chaco Sparrow, 27 October 2016, Capilla del stolzmanni is sister to R. s. strigiceps (DaCosta et al. 2009), Monte, Córdoba (Argentina), photograph by Juan I. Areta, b Yungas the position of R. strigiceps dabbenei remains unknown. Sparrow, 18 July 2012, Vaqueros, Salta (Argentina), photograph by Gabriel Núñez, c Tumbes Sparrow, 12 November 2015, Zapotillo, In the study reported here, our aim was to provide a strong Loja (Ecuador), photograph by Roger Ahlman (http://www.pbase​ test of current species limits in Rhynchospiza and to under- .com/ahlma​n) stand their biogeography. Our goals were to (1) characterize plumage features, morphology, vocalizations, habitat, and geographic and seasonal distributions, and provide ecologi- Methods cal-niche models of all Rhynchospiza taxa; (2) evaluate their taxonomic status using our comprehensive dataset coupled Morphology and plumage to a new genus-wide molecular phylogenetic hypothesis; and (3) discuss the importance of plumage, vocal, and behavioral We measured length of the exposed culmen and culmen features in the speciation process. from the nares, bill depth and width at the anterior edge of

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◂Fig. 2 Distribution of the Chaco Sparrow (Rhynchospiza strigiceps), of these specimens allowed us to test their identifcation and Yungas Sparrow (R. dabbenei) and Tumbes Sparrow (R. stolzmanni). to assess plumage variation across time and space. a Potential distribution based on ecological-niche models using the full dataset of the parapatric Chaco and Yungas Sparrows, b potential distribution based on ecological-niche models using the full dataset Distribution and potential distribution models of the allopatric Tumbes Sparrow. See ESM 1 for raw data, ESM 3 for other maps, and the “Methods” section for modeling details We compiled presence localities for all three Rhynchospiza taxa using literature sources, museum specimens, sound nostril, tarsus length (to the nearest 0.01 mm using digi- archives (see “Vocalizations”), eBird data, documented tal and standard calipers), and unfattened wing chord and records from other online sources, and our own personal tail length (to the nearest 0.5 mm using a metallic ruler in data (ESM 1). We used these data to assess geographic dis- strigiceps and dabbenei, and to the nearest 0.01 mm using tributions and migratory patterns and to obtain potential a standard caliper in stolzmanni) in museum specimens of distribution models. Based on song, nesting, and fedgling Rhynchospiza strigiceps strigiceps (n = 27), R. strigiceps information (see ESM 1) we assigned records of dabbenei dabbenei (n = 27), and R. stolzmanni (n = 37) that were and strigiceps from 16 November to 15 April to the breeding held at the Instituto Miguel Lillo (IML; Tucumán, Argen- season, and those from 16 April to 15 November to the non- tina), Louisiana State University Museum of Natural Sci- breeding season. Given the paucity of breeding data and the ence (LSUMNS), Museo Argentino de Ciencias Naturales lack of any purported migration in the tropical stolzmanni, (MACN; Buenos Aires, Argentina), and Museo de Ciencias we did not attempt a similar analysis on this taxon; however, Naturales de La Plata (MLP; La Plata, Argentina) (Elec- year-round data from the same localities suggest a lack of tronic Supplementary Material [ESM] 1). We collated infor- migratory movements. mation on weight using data from the Centro Nacional de We modeled the distributions of all three Rhynchospiza Anillado de Argentina (CENAA), specimen labels, litera- taxa with the open-source maximum entropy modeling soft- ture providing individual weights, and our own unpublished ware MaxEnt 3.3.3k using the following default settings: data. To assess sexual dimorphism within each taxon, we 500 iterations, 0.00001 convergence threshold, 10,000 maxi- used two-tailed Mann–Whitney U tests (α level = 0.05). mum background points, one regularization multiplier, and To evaluate diferences between all adult specimens of all auto-feature classes (Phillips et al. 2006). The program the three taxa we used one-way analysis of variance for all randomly withholds 25% of the presence locations to test variables, with the exception of bill height and bill width. the model performance (Phillips et al. 2006). To avoid These latter two characters were not normally distributed skewing the model’s results, we rasterized locations to a in some taxa (Shapiro–Wilk’s test p > 0.05) and were con- 1-km2 area, so that even if numerous presence locations were sequently compared using Kruskal–Wallis tests. We did not reported within this area, presence data were reduced to a assess measurement error (i.e., consistency of measures by single record per 1 km2 grid cell (Kramer-Schadt et al. 2013; repeatedly measuring the same variables in the same indi- Holzmann et al. 2015). After rasterization, models were run viduals; see Perktaş and Gosler 2010). However, the fact using 127 presence localities for R. dabbenei, 172 for R. that diferences among taxa were found using conservative stolzmanni, and 273 for R. strigiceps (115 for the breed- non-parametric statistics and that our sample sizes were not ing season and 158 for the non-breeding season). Because large (ranging from 17 to 36 individuals depending on the strigiceps is partially migratory and we were interested in variables; ESM 2) indicate that we did not commit a Type predicting possible distributional overlap with dabbenei at II statistical error and that our morphological measurements the time of breeding in order to assess species limits, we adequately captured diferences in size and shape among performed two separate models (see following paragraph). Rhynchospiza taxa. We decided to use default MaxEnt settings, after compar- We additionally examined photographs of specimens held ing the performance of models built using diferent param- at the American Museum of Natural History (AMNH; New eters, using the breeding data of R. strigiceps as a test case York, USA), Carnegie Museum of Natural History (CMNH; (Ülker et al. 2018). We ran 12 models combining diferent Pittsburgh, USA), The Academy of Natural Sciences regularization multipliers (0.1; 1; 5; 10) and feature classes (ANSP; Philadelphia, USA), The Natural History Museum (Linear, Quadratic and Hinge), one of which was the default (NHM; London, UK), and Yale Peabody Museum (YPM; settings model. The model using default settings (LQH1) Connecticut, USA) and of the type specimens of Zonotrichia outperformed the one with the lowest small-sample cor- strigiceps (Gould 1839), Zonotrichia whitii (Sharpe 1888), rected Akaike Information Criterion score (LQ1), since the and Aimophila strigiceps dabbenei (Hellmayr 1912) (see latter greatly over-predicted. Artifcially clustered presence ESM 1 for pictures of type specimens). The type specimens localities can induce bias in distribution models (Kramer- of Haemophila stolzmanni (Taczanowski 1877) have unfor- Schadt et al. 2013), while naturally occurring clusters may tunately been destroyed (Mlíkovský 2009). Visual inspection indicate the true ecological niche of a species. To test these

1 3 978 Journal of Ornithology (2019) 160:973–991 alternatives, we fltered all breeding localities of R. strigi- the model accurately discriminates between areas of pres- ceps using a 40-km bufer, thereby reducing our database ence and non-presence, an AUC = 0.5 indicates the model from 115 to 35 presence localities and eliminating all likely predicts as well as a random model, and an AUC < 0.5 indi- clusters. The resulting model performed poorly in compari- cates that the model’s predictive capability is worse than son to the model using the original 115 localities. Thus, random (Elith et al. 2006). We used the logistic output that we retained the model derived from the original database, represents the potential habitat suitability of the species on concluding that the geographic presence of soft clusters a scale of 0–1, with higher values representing more favora- is the natural result of spatial variation in the occurrence ble conditions for the presence of the species (Phillips et al. of R. strigiceps. The use of a bias fle is another option to 2006). We applied the minimum training presence (MTP) solve potential problems associated with clusters in presence as a threshold or “cutof” value for each model because it localities (Kramer-Schadt et al. 2013). However, we decided is the most conservative threshold, as it identifes the mini- not to use a bias fle because it assumes that individuals are mum predicted area possible while still maintaining a zero uniformly distributed and, in our case, attempting to fulfll a omission rate for both training and test data (Liu et al. 2005; theoretical expectation of homogeneous distribution (Merow Bellamy et al. 2013). Ecologically, the MTP can be inter- et al. 2013) by eliminating the naturally occurring soft clus- preted to contain those cells that are predicted to be at least ters of R. strigiceps would have resulted in an undesirable as suitable as those where the species was identifed as pre- methodological error instead of a methodological correction. sent. For the year-round residents R. dabbenei and R. stolz- For all taxa, we frst ran a model in MaxEnt using all manni, we ran a single model using our complete data set, 19 bioclimatic variables of the set of global climate layers but for the partial migrant R. strigiceps we ran two separate WorldClim with data collected between 1950 and 2000 models—one using our complete dataset and another one at a resolution of 30 arc-seconds (approx. 1 km2; http:// using only presence localities from the breeding season. We www.world​clim.org/; Hijmans et al. 2005). We evaluated divided habitat suitability values in our fnal models into the predictive efcacy of these 19 variables using the jack- four discrete classes: unsuitable (0–MTP threshold) and low, knife test of variable importance (training and test data) moderate, and high suitability. To give classes representing and variable response curves (DeMatteo et al. 2017). We low, moderate, and high suitability even visual representa- eliminated variables that showed low (close to zero) or tion, we separated them into equal intervals by resting the negative gain values for the training data. Low gains indi- lowest (MTP) value to the highest limit of the prediction cate that the variables did not provide useful information set by the model and dividing this value by 3. This resulted on their own for estimating distribution, while negative in the following categories for each species: R. dabbenei gains indicate that the variables make the model less trans- (unsuitable: 0–0.03, low suitability: 0.03–0.25, moderate ferable to other areas or conditions. With these variables suitability: 0.25–0.48, high suitability: 0.48–0.71), R. strigi- removed, we ran a fnal model for each species using only ceps complete dataset (unsuitable: 0–0.012, low suitability: informative variables (DeMatteo et al. 2017). For the fnal 0.012–0.27, moderate suitability: 0.27–0.54, high suitability: models, we removed eight bioclimatic variables for the 0.54–0.81), R. strigiceps breeding data (unsuitable: 0–0.073, model of R. dabbenei (2, 9, 11, 12, 13, 14, 16, and 18), 15 low suitability: 0.073–0.31, moderate suitability: 0.31–0.56, for the model of R. stolzmanni (1, 2, 3, 5, 6, 8, 9, 10, 11, high suitability: 0.56–0.81), and R. stolzmanni (unsuitable: 13, 14, 15, 17, 18, 19), three for the model of R. strigiceps 0–0.007, low suitability: 0.007–0.30, moderate suitability: using only breeding localities, and three (5, 8, 10) for the 0.30–0.59, high suitability: 0.59–0.89). To assess whether model of R. strigiceps using our complete dataset (see modeled distributions of R. dabbenei and R. strigiceps over- Hijmans et al. 2005 for defnition of variables). Because lapped, we mapped the areas that predicted moderate and Rhynchospiza taxa (1) are distributed along a large por- high presence probabilities. tion of South America, (2) occur in relatively dry semi- open and forested habitats in western South America that Vocalizations are similar to other such areas in distinct portions of the continent (e.g., the Caatinga and the northern dry forests We compiled recordings of the song and calls of all Rhyn- of Colombia and Venezuela), and (3) pertain to a clade chospiza taxa from the sound archives of the Macaulay of Pan-American distribution and because (4) we were Library of Natural Sounds (MLNS, New York, NY, USA), interested in assessing the possible overlap of taxa, we Xeno-Canto (http://www.xeno-canto​.org), and the Florida considered South America to constitute an adequate back- Museum of Natural History (FMNH; Gainesville, FL, ground area and a reasonable possible M area (see Barve USA). We also included our own recordings for study; et al. 2011). these have been deposited at the MLNS. Our fnal database We evaluated the fnal model performance using the area contained recordings of at least 21 individuals of R. dab- under the curve (AUC). Whereas an AUC = 1 indicates that benei, 17 of R. strigiceps, and 28 of R. stolzmanni (ESM

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1). We examined recordings aurally and visually with the We applied a 10% burn-in after checking for convergence help of audio spectrograms built in the Raven Pro 1.5 soft- using TRACER v1.4 (Rambaut and Drummond 2007). The ware application (http://www.birds​.corne​ll.edu/raven​) to resulting trees were used to create a maximum clade cred- illustrate and describe the overall acoustic features and ibility tree (MCC tree) with TreeAnnotator v1.8.4 (Drum- temporal pattern of vocalizations. Song spectrograms were mond et al. 2012). constructed with the following parameters: Window—type: The above phylogenetic analyses were then run again Hann, size: 1024 samples (= 23.2 ms), 3 dB flter bandwith: using a representative subset that included each of the 61.9 Hz; Time grid—overlap: 50%, hop size: 512 samples Rhynchospiza and one representative from each major genus (= 11.6 ms); Frequency grid—DFT size: 1024 samples, grid (excluding Chlorospingus) level groupings seen in the above spacing: 43.1 Hz; Call spectrograms with Window—type: analyses, for a total of eight individuals. From this subset, Hann, size: 512 samples (= 11.6 ms), 3 dB flter bandwith: a fnal MCC tree was generated to which the corresponding 124 Hz; Time grid—overlap: 50%, hop size: 256 samples likelihood scores from the ML analysis were added. (= 5.8 ms); Frequency grid—DFT size: 512 samples, grid We performed genetic distance analyses in MEGA7 spacing: 86.1 Hz. Structural diferences in spectrogram trac- (Kumar et al. 2016) using the Maximum Composite Like- ings of vocalizations among compared taxa were marked, lihood model (Tamura et al. 2004) with the eight-sample constant, and diagnostic, indicating that quantitative analy- representative set. All codon positions were included, and ses were neither necessary nor desirable to characterize the positions containing gaps and missing data were eliminated. main vocal types of Rhynchospiza. Moreover, the multi- noted song phrases of strigiceps and stolzmanni are highly Natural history notes divergent and structurally so diferent from the succession of single notes in dabbenei that it is virtually impossible We compiled natural history information and took ad libitum to obtain comparable quantitative features due to the lack notes on habitat use, general behavior, and seasonality dur- of common measuring points. Phrase types of strigiceps ing our feldwork, with the aim to facilitate the evaluation and stolzmanni and notes of dabbenei were identifed as of species limits in Rhynchospiza. such based on clear visual diferences in spectrograms and on their repeated presence in song bouts (see ESM 4 for a bestiary). Results

Molecular phylogenetic analyses Morphology and plumage

We collected 21 individuals representing each of the three Quantitative measurements and plumage features allowed a Rhynchospiza taxa and closely related taxa (Barker et al. clear separation of all specimens and photographs of dab- 2015). The number of specimens per genus were Rhynchos- benei and strigiceps, indicating clear-cut limits with no evi- piza = 3, Peucaea = 9, Ammodramus = 3, Arremonops = 4, dence of intergradation between these forms. and Chlorospingus = 2, with the latter used as the outgroup Morphological separation of dabbenei and strigiceps is (see “ Appendix 1”, DaCosta et al. 2009, and Barker et al. obvious and clear (Fig. 3). Subspecies dabbenei was signif- 2015 for the origin of all samples, and ESM 1 for details on cantly larger than strigiceps in seven of eight measurements Rhynchospiza samples). We extracted total genomic DNA (Fig. 3; ESM 2). These diferences held when comparing all using a DNeasy tissue extraction kit (Qiagen, Valencia, CA) specimens between taxa and within sexes between taxa. Sig- following the manufacturer’s protocol. We sequenced the nifcant sexual dimorphism was only found in bill-width and mitochondrial DNA gene NADH dehydrogenase subunit 2 wing-length in strigiceps, with males having higher average (ND2; 1041 bp) using previously described methods (Klicka values than females (ESM 2). Notably, the comparison of all and Spellman 2007). individuals revealed that dabbenei had 18% longer wings, a Before proceeding with the phylogenetic analyses, we 13% longer tail, 12% longer tarsi, and was 43% heavier than determined the best-ft model of evolution using jModelTest strigiceps, without an overlapping mean ± standard deviation v. 2.1.7 (Posada 2008). We then used maximum likelihood (SD) (Fig. 3; ESM 2). The similar bill-height (statistically (RAxML v 8.2.10; Stamatakis 2006) and Bayesian (BEAST identical) in both taxa coupled to the longer bill and greater v 1.8.4; Drummond et al. 2012) methods to estimate phylo- weight of dabbenei results in the birds of these two taxa hav- genetic trees. For the maximum likelihood (ML) analysis, ing a diferent aspect in nature, with strigiceps exhibiting a we used the GTRGAMMA model and performed 1000 non- proportionately heavier bill in relation to body size (Figs. 1, parametric rapid bootstrap replicates to assess nodal support. 3). The relatively large-billed and short-tailed R. stolzmanni For the Bayesian analysis, we performed runs for 10,000,000 difered in all measurements from strigiceps and dabbenei generations, sampling every 1000 for total of 10,000 trees. (Figs. 1, 3). Males of R. stolzmanni were larger than females

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Fig. 3 Morphological com- parisons between the Chaco Sparrow (Rhynchospiza strigiceps), Yungas Sparrow (R. dabbenei), and Tumbes Sparrow (R. stolzmanni). Figure shows mean ± standard deviation (SD) values (see ESM 1 and 2 for data and tests). Diferent lower- case letters indicate statistically signifcant diferences between measurements

in terms of exposed culmen, bill height, and wing-length a wide dark central band bordered by rufous-brown sides (ESM 2). (Fig. 1). Overall, R. stolzmanni is more similar to strigiceps Plumage distinctions between dabbenei and strigiceps than to dabbenei in terms of plumage coloration and pattern are minor but constant and diagnostic (Fig. 1; Table 1). (Fig. 1; Table 1). Subspecies dabbenei has a diagnostic large black loral area that extends above and below the anterior portion of the Distribution and potential distribution models eyes and exhibits well-developed chestnut shoulders and chestnut head-stripes, with each feather displaying a very Our dataset shows that dabbenei is a year-round resident in reduced to absent dark central band bordered by chestnut Yungas scrub and grassland in the mountains of north-west (Fig. 1). In comparison, strigiceps has a reduced black loral Argentina, with a single sight-record in southern Bolivia line in front of the eyes, reduced rufous-brown shoulders, (Fig. 2; ESM 1), while strigiceps is a partial migrant breed- and rufous-brown head stripes, with each feather showing ing in Chaco scrub and grassland in the lowlands of central

Table 1 Summary of features distinguishing Chaco Sparrow (Rhynchospiza strigiceps), Yungas Sparrow (R. dabbenei), and Tumbes Sparrow (R. stolzmanni) Distinguishing features Chaco Sparrow (R. strigiceps) Yungas Sparrow (R. dabbenei) Tumbes Sparrow (R. stolzmanni)

Loral region (Fig. 1) Small black loral line Large black loral crescent Small black loral line Head-stripes (Fig. 1) Rufous-brown with large dark Chestnut with reduced to absent dark Dark chestnut with large dark central- central-stripe to feathers center to feathers stripe to feathers Shoulders Reduced and rufous-brown Large and chestnut Large and rufous-chestnut Distribution (Fig. 2) Dry and Sierran Chaco Austral Yungas Tumbes Seasonality (Fig. 2) Partial migrant Resident Resident Measurements (Fig. 3) Smaller and lighter Larger and heavier Very large bill and short tail Eggs White with chestnut and brown Plain bluish-white Plain bluish-white blotches Song (Fig. 4) Succession of slower complex trilled Series of simple chirping notes Succession of faster complex trilled phrases phrases Call (Fig. 5) Higher-pitched, ascending, two Lower-pitched, ascending-descend- Highest-pitched, descending infections ing, one infection High-pitched call (Fig. 5) ∪ shaped ∩ shaped ⎝ shaped

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Argentina and in the Sierras de Córdoba (Argentina). There town of Río del Valle. The specimen may have come from is wide overlap between the breeding and non-breeding areas the specifed locality or from somewhere near the head of of strigiceps. Some individuals apparently migrate north- the Río del Valle river. To conclude, despite occurring in wards, reaching Paraguay and eastern Bolivia during the relatively close proximity, there are no defnitive records of Austral winter, while other individuals migrate northeast- sympatry or syntopy of dabbenei and strigiceps. erly, reaching eastern Entre Ríos and Corrientes provinces in Ecological-niche models accurately discriminated eastern Argentina during the Austral winter (Fig. 2; ESM 1). between areas with presence and non-presence of all However, the breeding distribution and timing of breeding Rhynchospiza taxa, as indicated by the high AUC values of strigiceps are imperfectly known. Based on few nesting (AUC ≥ 0.98 for all models; ESM 3). The bioclimatic vari- records, it appears to be a late breeder, starting to nest by ables with the highest gain for the training and test data mid-November (see “Natural history notes” in “Results”). when used in isolation were “precipitation seasonality” in Two records from Boquerón (western Paraguay) in late Janu- dabbenei and “temperature annual range” for both strigiceps ary and late March, respectively, that included a molting (models with all data and breeding data) and stolzmanni. female with somewhat enlarged ovaries (Short 1975), and Ecological-niche modeling predicted a narrow zone of para- two records from Entre Ríos (eastern Argentina) in mid- patry in southern Tucumán and eastern Catamarca between December and mid-January, respectively, appear to sug- dabbenei and strigiceps, in the region where the species are gest breeding but may also pertain to late or early migrants known to occur in close proximity (Fig. 2; ESM 1). This (Fig. 2; ESM 1). Available data suggest that strigiceps is an zone of parapatry is predicted when modeling with all occur- endemic breeder in Argentina and that dabbenei is a near- rences (Fig. 2) and also when using only records from the endemic breeder in Argentina. breeding season in the migratory strigiceps (ESM 3). The Geographic ranges of dabbenei and strigiceps are para- model for stolzmanni accurately predicted its allopatric patric, with the former occupying the Andes and extra- range as expected (ESM 3). Andean ranges at higher altitude and the latter occupying the lowlands to the east where their ranges approach (Fig. 2). Vocalizations Outside of the breeding season both taxa occur as close as approximately 50 km in Tucuman province, with records of We identifed fve vocalizations in all Rhynchospiza taxa: dabbenei from La Cocha at 450 m a.s.l. in the lowest foot- song, contact calls, contact calls in quick succession, high- hills of the eastern slope of the Aconquija Massif (the lowest pitched calls, and interaction calls (Figs. 4, 5; ESM 4). elevational record of this species) and records of strigiceps from Taco Ralo at 340 m a.s.l. (Fig. 2; ESM 1). During Song Songs are seemingly given only by males, who sing the breeding season they occur as close as approximately when concealed among the top-most branches of trees and 65 km, with records of dabbenei from Balcozna (Catamarca) bushes. The songs of strigiceps and stolzmanni are com- at 1200 m a.s.l. in the western slope of the Sierra de Ancasti posed of distinct musical phrases that tend to be repeated and records of strigiceps from Barranca (Tucumán) at 290 m at fairly even intervals a variable number of times before a.s.l. (Fig. 2; ESM 1). A specimen of dabbenei thought to switching to another phrase. On rare occasions, differ- come from Corralito (eastern Salta, 38 km east of General ent phrases might succeed each other without repetition. Ballivián, San Martín department) at 250 m a.s.l. in the Dry Each phrase can be a simple trill or contain an introduc- Chaco by Navas (1965) would be the only indication of pos- tory note followed by the repetition of a single note or of sible geographic overlap between dabbenei and strigiceps. a multi-noted pattern (Fig. 4). The main structural difer- However, we presume that the specimen comes from a dif- ence between the songs of strigiceps and stolzmanni is the ferent Corralito locality (western Salta, Rosario de Lerma speed of repetition of notes within each phrase, which is department) at 1500 m a.s.l. in the Yungas (ESM 1). A third faster in the latter (Fig. 4; ESM 4). The largest repertoire of “Corralito” locality occurs in the very dry region of the Cal- phrases recorded in a single individual was 14 in strigiceps chaqui Valley (south-central Salta, San Carlos department) and 11 in stolzmanni. The song of dabbenei is composed of a at 1600 m a.s.l., but this locality does not harbor suitable series of chirping notes that are repeated haphazardly in long habitat for this species. Finally, a specimen of dabbenei from bouts, mostly at dawn, creating a seemingly endless string Río del Valle (central-east Salta, Anta department) at 600 m of mostly unmusical quality (Fig. 4). The largest repertoire a.s.l. in the eastern foothills of the Sierra de Santa Bárbara recorded in a single individual of dabbenei consisted of nine would represent the easternmost record of the species and notes. Unlike the cases of stolzmanni and strigiceps in which is only approximately 55 km from Joaquín V. Gonzalez calls are very diferent from song bouts, it is at times difcult (central-east Salta, Anta department) at 380 m a.s.l. where to realize whether dabbenei is giving more spaced renditions strigiceps has been recorded Fig. 2; ESM 1). However, we of the song or simply calling at a low pace. failed to locate any Rhynchospiza during a visit to the nearby

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Fig. 4 Spectrograms comparing songs of all Rhynchospiza taxa. a Chaco Sparrow (Rhynchos- piza strigiceps), b Yungas Spar- row (R. dabbenei), c Tumbes Sparrow (R. stolzmanni). Roman numerals indicate difer- ent phrases (in a, c) or notes (in b). Dashed vertical line sepa- rates individuals. See ESM 1 for recording data and ESM 4 for a bestiary of songs in these taxa

Contact calls These short calls were used while foraging in of birds (Fig. 5). Each member of the pair gave distinctive pairs or when foraging and moving in groups. The calls of notes, but we were never able to discriminate which notes stolzmanni were the highest pitched and descended through- were given by each sex. During the emission of interaction out, those of dabbenei were lower pitched, single-infected, calls, the birds generally perched nearby (< 30–50 cm) in the and ascending–descending, and those of strigiceps were same perch facing each other or nearly so, slightly lowered the lowest pitched, double-infected, and overall ascending both wings separating them from the body and fanned and (Fig. 5). quivered the tail shallowly and rhythmically in consonance with the calls. These duets showed little pattern and were Contact calls in quick succession A series of variably pitched highly variable, sometimes fnishing in a series of very high contact calls was given when the individual was excited pitched notes in dabbenei and strigiceps, and always includ- naturally or in response to playback. Sometimes the quick ing a succession of extremely fast and high-pitched diagnos- series of calls constituted the frst notes of the interaction tic warbles in stolzmanni. Occasionally, an individual would calls (Fig. 5, see subsection Interaction calls). give its part of the call in solo.

High‑pitched calls The very high-pitched shrill and metallic Molecular phylogenetic analyses notes are ∩ shaped in dabbenei, ∪ shaped in strigiceps, and mostly ⎝ shaped in stolzmanni (Fig. 5). In both dabbenei The phylogenetic analyses including all 21 samples showed and strigiceps, these notes were used among individuals to that all other samples formed a well-supported, monophy- gather together. Intra-taxon playback trials caused groups to letic group sister to the outgroup, Chlorospingus (ESM 5). approach the sound source. Within this group there is high support for genus- and spe- cies-level structure, but little to no support for how the gen- Interaction calls Long and complex trilled and chattering era are related to each other. This structure is also refected calls were given as a duet by members of a pair (1) when in the reduced sample set (Fig. 6). However, Rhynchospiza meeting after foraging separately, (2) immediately following forms a well-supported clade (posterior probability = 0.99, landing after shared long fights naturally and in response to maximum likelihood = 95), with R. stolzmanni sister to a playback, and (3) when mobbing or attacking other species fully supported R. dabbenei and R. strigiceps clade (Fig. 6).

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The genetic distance analysis (ESM 6) was run with a Chacoan species such as Cinereous Black-tyrant (Knipole- total of 1006 positions after missing data were removed, gus striaticeps) and Many-colored Chaco Finch (Saltatricula resulting in an average diference of 11.5% (0.115 substitu- multicolor), exemplify both the extreme conditions tolerated tions per site) between R. stolzmanni and the R. dabbenei/R. by this species and the role of mountains as a biogeographic strigiceps clade. An average diference of 1.6% (0.016 sub- barrier separating dabbenei from strigiceps in some parts of stitutions per site) was found between R. dabbenei and R. their allo-parapatric ranges. The eastern strigiceps inhab- strigiceps samples. its a diverse array of dry grassy scrubland types and forest borders, including Espinal dominated by Prosopis nigra, P. Natural history notes alba, Geofroea decorticans, Celtis ehrenbergiana, and Aca- cia caven (Villa María, Córdoba province); Sierran Chaco Both dabbenei and strigiceps seem to be late breeders, with Acacia caven, Celtis ehrenbergiana, Schinus longifo- beginning to nest by November (mid-spring), with nests lius, Ziziphus mistol, Zanthoxylum coco, Lithraea molle- with eggs still found in late January (mid-summer) (ESM oides, Trithrinax campestris, and Caesalpinia gilliesi (La 1). Dependent juveniles have been recorded up to early April Punilla department, Córdoba); and Dry Chaco dominated (dabbenei) and late March (strigiceps) (ESM 1). Based on a by Acacia spp., Aspidosperma quebracho-blanco, Cercid- few nests, clutch size is two to three eggs in both dabbenei ium praecox, Prosopis spp. and Ziziphus mistol (Frías, San- and strigiceps (Hoy 1971; de la Peña 2016). The allopatric tiago del Estero province, Argentina). R. stolzmanni occurs and more tropical stolzmanni lays one to four eggs, with in lowland and foothill arid scrub and open dry woodlands records of breeding in late May and early June (Williams from sea level to 1000 m a.s.l. (with the range extending, on 1981), although breeding has been reported between Janu- exception, to 1300–1900 m a.s.l. in Ecuador; ESM 1), where ary and May during the rainy season (Jaramillo 2011). At it favors a mosaic of brushy thickets and grass/weeds. The Olmos, Lambayeque department (Peru) in 1981, breeding habitat recorded on the labels of specimens from northwest- occurred March to June after modest El Niño rains in mid- ern Peru includes “arid scrub,” “arid coastal scrub foothills,” March (SW Cardif, personal observation). The observation and “open mesquite grassland” (LSUMNS specimens). At of juvenal-plumaged specimens with relatively unossifed a study site near Olmos, Lambayeque department (Peru) in skulls from this locality in September 1983 suggests that 1981 and 1983, the species was common, primarily in shrub breeding may have extended into July–August during a thickets along washes on level to hilly terrain dominated by stronger 1983 El Niño event, but the breeding season may Prosopis limensis, Cordia rotundifolia, and Capparis angu- vary yearly depending on rainfall. lata, but it was also occasionally observed in farmland and Eggs of dabbenei and stolzmanni are bluish-white, in disturbed “fallow” areas regenerating in Prosopis (SW immaculate, and without gloss (Hoy 1971; Williams 1981), Cardif, personal observation). whereas those of strigiceps, while also lacking gloss, are Outside of the breeding season groups of dabbenei and white to grayish-white with deep chestnut, dark-brown, strigiceps join mixed species focks. Only dabbenei has been and pale-brown markings concentrated on the obtuse pole. recorded focking with two Andean species, Leptasthenura A nest from a location near Rosario de la Frontera (where fuliginiceps and nominate Elaenia obscura, whereas only dabbenei is relatively common; ESM 1), attributed a pos- strigiceps has been found in focks containing three Chaco/ teriori to dabbenei, is noteworthy in that the coloration of Monte breeders, Serpophaga griseicapilla, Poospiza ornata, the eggs is like that described for strigiceps (see de la Peña and Lophospingus pusillus. Both dabbenei and strigiceps have 2016). If this nest has been correctly identifed, this record focked with a host of other open or dry woodland species, indicates polymorphism in egg coloration. Alternatively, the including Columbina picui, Asthenes baeri, Phacellodomus nest might belong to nominate strigiceps, thereby indicating sibilatrix, Cranioleuca pyrrhophia, Leptasthenura platensis, that both species breed in close proximity. Thamnophilus caerulescens, Hemitriccus margaritaceiventer, The western dabbenei occurs most often in grassy scrub- Suiriri suiriri, Stigmatura budytoides, Serpophaga subcristata, land dominated by Acacia aroma with interspersed Sapium Knipolegus aterrimus, Phytotoma rutila, Troglodytes aedon, haematospermum, Celtis ehrenbergiana, and Allophyllus Polioptila dumicola, Setophaga pitiayumi, Myioborus brun- edulis trees, in agricultural curtains, and in forest borders niceps, Polioptila dumicola, Turdus amaurochalinus, Cor- in areas with Chacoan infuence within the Austral Yungas yphospingus cucullatus, Zonotrichia capensis, Poospiza mel- (San Lorenzo, Vaqueros, and Camino del Gallinato, Salta), anoleuca, Poospiza torquata, Poospiza whitii, Sicalis faveola, but it also occurs rarely above the Yungas treeline in mon- Cyanocompsa brissonii, Saltator aurantiirostris, Saltatricula tane grasslands with Baccharis scrubs (Balcozna in Catama- multicolor, Icterus pyrrhopterus, and Agelaioides badius. In rca and El Infernillo in Tucumán). Our records of dabbenei Bolivia, strigiceps has been reported focking with several fur- in the western slope of the Sierra de Santa Bárbara (Virgilio nariids and emberizids during the Austral winter (Kratter et al. Tedín) and in open areas in Sierran Chaco, together with 1993). R. stolzmanni is a sedentary, ground-foraging species,

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◂Fig. 5 Spectrograms comparing calls, calls in quick succession, high- obsoletum, Campylorhynchus fasciatus, Cantorchilus supercil- pitched calls, and interaction calls of all Rhynchospiza taxa. a Chaco iaris, Mimus longicaudatus, Polioptila plumbea, Conirostrum Sparrow (Rhynchospiza strigiceps), Yungas Sparrow (R. dabbenei), b cinereum, Sicalis faveola, S. taczanowskii, Sporophila peruvi- c Tumbes Sparrow (R. stolzmanni). Dashed vertical lines separate call versions or renderings of the same vocalization by diferent individu- ana, Piezorina cinerea, Coereba faveola, and Sturnella belli- als. Solid vertical lines separate structurally diferent vocalizations. cosa. Most of these species became locally more abundant and See ESM 1 for recording data widespread after El Niño rains, and a few additional species arrived at the site to breed after the rains and resulting sprout- occurring as individuals, pairs, or family groups and appearing ing of vegetation and increased abundance of arthropods, such to maintain territories year round; the species generally does as Euscarthmus meloryphus, Tumbezia salvini, Conothraupis not join mixed-species focks. For many bird species inhab- speculigera, Rhodospingus cruentus, and Poospiza hispanio- iting arid scrub habitats in the Tumbesian region, seasonal lensis (SW Cardif, personal observation). distribution and abundance is dictated by wet “El Niño” years. Near Olmos, during dry conditions, other common residents recorded co-occurring with R. stolzmanni include Columbina Discussion cruziana, Forpus coelestis, Veniliornis callonotus, Lepidoco- laptes souleyetti, Furnarius leucopus, Synallaxis stictothorax, In this article we have shown that the locally parapatric dab- Sakesphorus bernardi, Muscigralla brevicauda, Pyrocephalus benei and strigiceps are recently diverged sister taxa that rubinus, Myiarchus semirufus, Myiodynastes bairdii, Tyran- can be unambiguously distinguished by consistent difer- nus niveigularis, Pseudelaenia leucospodia, Camptostoma ences in plumage, morphology, egg coloration, song, calls,

Fig. 6 Phylogenetic tree of all Rhynchospiza taxa (NADH dehydro- responding maximum likelihood bootstrap value from RAxML is genase 2 [ND2] gene) and selected species from closely related gen- shown below the node. Dash (–) indicates that the specifc node did era. The maximum clade credibility (MCC) tree from BEAST with not occur in the RAxML tree. See “Molecular phylogenetic analyses” posterior probability values is shown above the nodes and the cor- for details on analysis and software used for constructing tree

1 3 986 Journal of Ornithology (2019) 160:973–991 habitat, ecological-niche models, and seasonality (Table 1). like San Marcos Sierra and Reserva Provincial Chancaní, These diferences can be considered more or less equivalent both in Córdoba province (ESM 1, personal observation). to those between the allopatric strigiceps and R. stolzmanni Although Paynter (1967) suggested that Peucaea sumi- (Table 1) and support full species status for Rhynchospiza chrasti, R. stolzmanni, and R. strigiceps are relicts of a once dabbenei under any species concept (Mayr 1963; Cracraft widely distributed ancestor, phylogenetic data contradicts 1983; Paterson 1985). The remarkable similarity between this notion (DaCosta et al. 2009; ESM 5). Our data show a several species in Peucaea, Rhynchospiza, and Aimophila closer relationship between the locally parapatric R. strigi- is a case of conservatism of a general plumage bauplan ceps (Chaco) and R. dabbenei (Yungas), and a more distant and illustrates how subtle plumage cues can be indicative relationship to R. stolzmanni (Tumbes). of species-level diferentiation (Wolf 1977; DaCosta et al. Rhynchospiza dabbenei and R. stolzmanni have been 2009; this work). Diferences in the extent and intensity of unanimously considered to be sedentary, and our data sup- black in the lores and saturation of rusty plumage are gener- port this view (Dinelli 1918; ESM 1). Our extensive compi- ally accompanied by diferences in habitat use, behavior, lation of records indicates that some individuals of R. strigi- and vocalizations, which together result in species-specifc ceps migrate northwards and eastwards during the Austral recognition systems and consequent reproductive isolation winter, while other individuals remain at their breeding sites. among species (Wolf 1977). Such seasonality seems to be more complex than a simple complete seasonal migration and falls into the broad cat- Geographic distribution and biogeography egory of partial migration, perhaps with some individuals or groups of individuals wandering outside of the breeding The geographic ranges of R. dabbenei and R. strigiceps have season. At diferent localities in the Dry Chaco, R. strigiceps been frequently misrepresented in the literature: dabbenei has been variously considered to be nomadic, scarce during and strigiceps have been considered to be “isolated geo- the summer and frequent during the winter (Capurro and graphically” (Short 1975), clearly allopatric populations Bucher 1988), resident (Codesido and Bilenca 2004), or a have been repeatedly mapped (Ridgely and Tudor 1989; winter visitor (Short 1976). All but a few records in eastern Jaramillo 2011), and lowland records of R. strigiceps in Argentina (Fig. 2; ESM 1; Capllonch et al. 2005; Marateo southeastern Bolivia have been recently incorrectly attrib- et al. 2009) indicate that R. strigiceps is a non-breeding visi- uted to R. dabbenei (Kratter et al. 1993; Jaramillo 2011). tor to the region, and whereas some of the more southerly We consider that R. dabbenei and R. strigiceps can more records in Buenos Aires province may constitute escaped aptly be considered to be parapatric than allopatric: their cage-birds, other sightings might belong to non-breeding ranges closely approach during the breeding season, and migrants (ESM 1). intervening orographical barriers that may prevent them The range of R. dabbenei is entirely within the Bolivian from entering into contact do occur in part of the distribu- and Argentine Yungas Endemic Bird Area (Stattersfeld et al. tions, but not at other places. Thus, the role of mountains 1998). This area was defned based on only a few species, as barriers to their contact difers in diferent parts of their but should be expanded to include R. dabbenei and other distributions in northwest Argentina. In the central-east por- Austral Yungas endemic species such as the Red-faced Guan tion of the distribution of R. dabbenei, the extra-Andean (Penelope dabbenei), Rothschild’s Swift (Cypseloides roth- Sierra de Santa Bárbara/Cresta del Gallo and the Sierra de schildi), Tucuman Amazon (Amazona tucumana), Slender- la Calendaria/Castillejos may be efective barriers because tailed Woodstar (Microstilbon burmeisteri), Blue-capped there are no confrmed records on the east slopes of these Pufeg (Eriocnemis glaucopoides), Slaty Elaenia (Elaenia mountain ranges (Fig. 2; ESM 3). However, in the southern strepera), White-throated Antpitta (Grallaria albigula), portion of the distribution of R. dabbenei, the east slope White-browed Tapaculo (Scytalopus superciliaris), Rufous- foothills of the Aconquija massif/Sierra de Ancasti are in throated Dipper (Cinclus schulzi), Yellow-striped Brush- direct contact with the dry Chaco where R. strigiceps appar- fnch (Atlapetes citrinellus), Fulvous-headed Brush-fnch ently breeds (Fig. 2; ESM 3). Here, habitat use at diferent (Atlapetes fulviceps), and Rufous-browed Warbling-fnch altitudes seems to be the main factor keeping the species (Microspingus erythrophrys). spatially segregated at their distributional boundaries: while R. dabbenei is restricted to higher elevation montane scrub, Vocalizations, plumage, ecomorphology, R. strigiceps prefers lowland Chaco scrub in their zone of and mating systems parapatry. The mention of R. dabbenei in the “monte” scrub zone (Short 1976) is clearly inaccurate because this species The song of R. dabbenei, which is composed of an endless is not found in the Monte Desert (Areta et al. 2012; this and capricious series of chirping notes, is dramatically dif- work). In contrast, R. strigiceps can be found in ecotonal ferent from those of R. strigiceps and R. stolzmanni, which pockets between Sierran Chaco and Monte Desert in areas exhibit repetitive musical phrases. Previous descriptions of

1 3 Journal of Ornithology (2019) 160:973–991 987 the vocalizations of R. dabbenei are superfcial but, interest- in close proximity often facing each other, and they occur ingly, they lack reference to any complex or musical song generally either during territorial or aggressive encounters (Dinelli 1918; Hoy 1971). The local name “Chisca” seems with other birds or when meeting after some period of time to be onomatopoeic and captures the quality of its most com- apart. Wing lowering and tail fanning and quivering dis- mon call, while another local name “Charlatán” (that who plays that accompany the interaction calls in Rhynchospiza talks too much with a tendency to lie or exaggerate while have not been described in Peucaea or Pyrgisoma (Marshall doing so) aptly describes the overall pattern of the song as 1964; Wolf 1977) and might constitute a synapomorphy for an untidy, little-patterned, chat. Rhynchospiza. Facial patterns have been considered to be Songbirds that learn their songs by imitating those of a important characters involved in species-level recognition tutor have an innate vocal template that allows individuals and pair-bond maintenance during the emission of chatter to learn some vocal signals while precluding the learn- duets in Peucaea (Wolf 1977). If correct, these functional ing of others (Marler 1970). This allows the copying of interpretations of facial patterns as important mating char- species-specifc functional signals while diminishing the acters lend further support to the treatment of the spot-lored chances of learning songs that will not result in an efec- and chestnut-crowned R. dabbenei and the line-lored and tive means of signaling (Kroodsma and Pickert 1984). rufous-crowned R. strigiceps as separate species. Vocal templates are not absolutely refractory to signals The larger and darker R. dabbenei occurs in cooler and that are not a perfect ft for this template, and in unusual wetter places than does the smaller and paler R. strigiceps, cases some individuals can learn interspecifc vocaliza- which inhabits considerably hotter and drier environments; tions (Baptista and Morton 1981). However, birds with this diference provides support for both Gloger’s color and sufciently diferent templates or vocal capabilities never Bergmann’s size ecogeographic rules (Friedman and Remeš learn or produce each others’ vocalizations (Baptista 1996; 2017; Salewski and Watt 2017). Accordingly, our accurate Baptista and Kroodsma 2001). Irreversible changes in this distributional niche-models found that variables related to vocal template could thus be an important element dur- precipitation seasonality in R. dabbenei and temperature ing speciation in vocal-learning birds. More generally, annual range in R. strigiceps were important to predict their genetically based changes in the vocal template may lead distributions. to non-overlapping potential acoustic spaces, which will The existence of ecomorphological variation and difer- automatically lead to non-overlapping realized acoustic ences in habitat use in the three Rhynchospiza is consistent spaces (Slabbekoorn and Smith 2003). The dramatic dif- with the importance of habitat/niche changes as triggers ferences in the songs of R. strigiceps and R. stolzmanni of diferentiation during the speciation process (Paterson in comparison to that of R. dabbenei suggest a change 1980, 1985). The Recognition Concept of species proposes in the genetic architecture that underlays the innate vocal that populations in new habitats would experience adap- learning template in the latter. This also suggests that indi- tive changes that would lead to changes in the coadapted viduals of R. dabbenei would not be capable of incorporat- “specifc mate recognition system” (SMRS), resulting in the ing (and hence producing) the multi-note trilled phrases establishment of a new system leading to speciation (Pater- typical of songs of R. strigiceps and R. stolzmanni. Com- son 1985). The suite of features that distinguishes all Rhyn- plex multi-noted phrases are widespread and appear to be chospiza, especially those characters directly related to mat- ancestral in the Peucaea/Rhynchospiza/Ammodramus/Ar ing discussed above, such as diferences in song, interaction remonops clade. The evolutionary–cultural change from calls, and facial pattern, indicates that each has a diferent complex phrases in the most recent common ancestor of SMRS and that their recognition as separate species is fully R. strigiceps + R. dabbenei to single notes in R. dabbenei supported by our data. provides an interesting case study of vocal changes related to the speciation process. Further understanding of this Phylogenetic and taxonomic remarks process is dependent on clarifcation of vocal learning mechanisms in Rhynchospiza. Molecular phylogenetic data show that R. stolzmanni is sis- Calls of all Rhynchospiza taxa are easily distinguished ter (genetic distance 11.5%,) to the more recently split R. with the aid of spectrograms. The interaction calls of Rhyn- strigiceps and R. dabbenei (genetic distance 1.6%; Fig. 6) chospiza appear to be homologous to the chatter duets given (see also DaCosta et al. 2009; Bryson et al. 2016). The dis- by most if not all Peucaea sparrows (Wolf 1977; DaCosta tribution of shared features in Rhynchospiza is a mosaic of et al. 2009). These chatter duets have also been consid- derived and phylogenetically retained features. First, the ered to be homologous to the pair reunion ceremony of the similarly patterned interaction calls, and the structurally Brown Towhee group (genus Pyrgisoma/Melozone) (Mar- similar, albeit inverted in shape, high-pitched calls of R. shall 1964; Wolf 1977; DaCosta et al. 2009). In these three strigiceps and R. dabbenei are consistent with the closer genera, duet calls are given by the male and female of a pair relationship between them. Second, the thin loral line, pale

1 3 988 Journal of Ornithology (2019) 160:973–991 plumage colors, relatively thick bill, and complex song made stolzmanni. Fabricio C. Gorleri helped with sampling event data from up of series of phrases of R. strigiceps and R. stolzmanni eBird and illustrated the birds shown in the phylogenetic tree. John Klicka granted access to his lab and samples for phylogenetic analyses. would be the result of phylogenetic conservatism, while This contribution was possible thanks to funding by a CONICET grant those traits would have changed into the dark loral, dark to JIA for the project “Taxonomía de las aves de los Andes del noroeste plumage colors, relatively slender bill, and simple song of de Argentina” (Grant no. 3216/12). R. dabbenei. Finally, the pale-bluish and unmarked eggs of R. dabbenei and R. stolzmanni might represent the ancestral condition, while the the brown and marked eggs of R. strigi- ceps would be derived. Appendix 1: Museum source and localities We have not detected any nomenclatural problem with of specimens used in phylogenetic names in current usage. Our examination of the type speci- reconstructions mens of all Rhynchospiza taxa and the examination of the illustration in the description of R. stolzmanni (type lost; Taxon Sample Collecting GenBank Specimen ­sourcea locality accession ID Mlíkovský 2009) is in agreement with previous views number (Sharpe 1888; Hellmayr 1938). Now that the strictly South American Rhynchospiza can be recognized as three diferent Rhynchos- LSUMNS PERU: Las FJ547317 LSUMZ- piza stolz- ‐ species-level entities, we would like to propose new common (B 5227) Pam- 100779 manni pas, Km English names for the two southern representatives. The cur- 885 Pan rent common name for the entity composed by R. strigiceps American and R. dabbenei is Stripe-capped Sparrow, which is confus- Hwy., 11 ingly similar to Stripe-headed Sparrow (Peucaea rufcauda), road km N Olmos, a name that has also been applied to R. strigiceps (Hellmayr Lam- 1938). The uninformative Dabbene’s Stripe-headed Spar- bayeque row has been proposed for R. dabbenei (Hellmayr 1938). Rhynchos- UWBM ARGEN- MN145865 UWBM- The type species of Rhynchospiza is stolzmanni, the Tumbes piza strigi- (DHB2425) TINA: 92146 ceps Sparrow, although Taczanowski’s Stripe-headed Sparrow 40 km southeast of has been used (Hellmayr 1938). The minor plumage dis- Joaquín V. tinctions between Rhynchospiza species contrast markedly González, with their clear separation in diferent biogeographic realms. Salta We suggest that new comparative common names empha- Rhynchos- UWBM ARGEN- MN145864 UWBM- piza dab- sizing the biogeographic regions to which each of the three (DHB2376) TINA: 92147 benei 24 km north Rhynchospiza is restricted shall facilitate communication. of Salta We thus propose the following taxonomy, common English city, Salta names, and linear sequence: Chlorospin- MBM HONDU- FJ547290 Tumbes Sparrow Rhynchospiza stolzmanni (Taczanowski gus oph- (JK99‐074) RAS: thalmicus 1877) Copan Chlorospin- Yungas Sparrow Rhynchospiza dabbenei (Hellmayr 1912) FMNH PERU: Cuzco FJ547291 gus fav- (430078) Chaco Sparrow Rhynchospiza strigiceps (Gould 1839). igularis Peucaea MZFC MEXICO: FJ547309 Acknowledgements We thank all recordists, birdwatchers, and collec- carpalis (ORRS102) Sonora tors who through time have helped build an impressive database. We Peucaea CNAV MEXICO: FJ547308 thank Patricia Capllonch for clarifcation on some Tucumán locali- sumi- (Po13226) Oaxaca ties and for making CENAA data available; Markus Unsöld (ZSM), chrasti Ben Marks and Mary Hennen (FMNH), Sara Bertelli and Sebastián Aveldaño (FML), J.V. Remsen Jr (LSUMNS), Yolanda Davies Peucaea LSUMNS USA: Ari- FJ547312 (MACN), Diego Montalti (MLP), Kristof Zyskowski (YPM), Stephen botterii (B‐9880) zona P. Rogers (CM), Nate Rice (ANSP), Hein Van Grow (BMNH), Paul Peucaea LSUMNS USA: Loui- FJ547311 Sweet (AMNH), and Carla Cicero (MVZ) for information on, access aestivalis (B‐2461) siana to, or pictures of museum specimens under their care; Carlos and Sil- Peucaea MVZ USA: Okla- FJ547310 via Ferrari for advice on feldwork with R. strigiceps; and G. Núñez- cassini (FC20222) homa Montellano, E. Gulson, and T. Pegan for feld companionship. Matt Peucaea CNAV MEXICO: FJ547306 Medler and Matt Young promptly provided sound recordings from the humeralis (Po11084) Morelos MLNS. G. Núñez allowed use of his photograph of R. dabbenei and R. Ahlman of his photograph of R. stolzmanni. Carlos Bianchi pro- Peucaea MZFC MEXICO: FJ547307 vided crucial help by making the maps. Juan Freile, Fernando Angulo mysticalis (OVMP773) Puebla Pratolongo, and Tom Schulenberg helped clarify the distribution of R.

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Areta JI, Repenning M (2011) Systematics of the Tawny-bellied Taxon Sample Collecting GenBank Specimen Seedeater (Sporophila hypoxantha). I. Geographic variation, ecol- ­sourcea locality accession ID ogy and evolution of vocalizations. Condor 113:664–677 number Areta JI, Noriega JI, Pagano L, Roesler I (2011) Unraveling the ecolog- Aimophila MBM NICAR​AGA​: FJ547304 ical radiation of the capuchinos: systematics of the Dark-throated Sporophila rufcollis rufcauda (DAB1680) Rivas Seedeater , and description of a new black- rufcauda collared form. Bull Br Ornithol Club 131:4–23 Areta JI, Pearman M, Ábalos R (2012) Taxonomy and biogeography Aimophila CNAV MEXICO: FJ547305 of the Monte Yellow-Finch (Sicalis mendozae): understand- rufcauda (Po13223) Oaxaca acuminata ing the endemic avifauna of Argentina’s Monte Desert. Condor 114:654–671 Ammodra- BMNH USA: Mon- AF290125 Areta JI, Kirwan G, Dornas T, Araujo-Silva LE, Aleixo A (2017) Mix- mus (JK94‐056) tana ing the waters: a linear hybrid zone between two riverine Neo- savan- tropical cardinals (Paroaria baeri and P. gularis). Emu 117:40–50 narum Baptista LF (1996) Nature and its nurturing in avian vocal develop- Ammodra- MBM ARGEN- FJ547324 ment. In: Kroodsma DE, Miller EH (eds) Ecology and evolution mus (GAV1018) TINA: Salta of acoustic communication in birds. Cornell University Press, humeralis Ithaca, pp 39–60 Ammodra- J. Avise labora- Not available FJ547323 Baptista LF, Kroodsma DE (2001) Foreword: Avian bioacoustics: a mus tory (DS74) tribute to Luis Felipe Baptista. In: del Hoyo J, Elliott A, Sargatal aurifrons J (eds) Handbook of the birds of the world, vol 6. Lynx Edicions, Barcelona, pp 11–52 Arremonops Pending Pending Pending tocuyensis Baptista LF, Morton ML (1981) Interspecifc song acquisition by a white-crowned sparrow. Auk 98:383–385 Arremonops MBM NICAR​AGU​ FJ547296 Barker FK, Burns KJ, Klicka J, Lanyon SM, Lovette IJ (2015) New conirostris (DAB1049) A: Atlantico insights into new world biogeography: an integrated view from the Norte phylogeny of blackbirds, cardinals, sparrows, tanagers, warblers, Arremonops KU (KU2031) MEXICO: FJ547295 and allies. Auk 132:333–348 chlorono- Campeche Barve N, Barve V, Jiménez-Valverde A, Lira-Noriega A, Maher SP, tus Peterson AT, Soberón J, Villalobos F (2011) The crucial role of Arremonops BMNH USA: Texas FJ547294 the accessible area in ecological niche modeling and species dis- rufvirga- (X6828) tribution modeling. Ecol Model 222:1810–1819 tus Bellamy CC, Scott CD, Altringham JD (2013) Multiscale, presence- only habitat suitability models: fne resolution models for eight bat species. J Appl Ecol 50:892–901 a Museum sources for specimens used in this study. LSUMNS Louisi- Bradbury JW, Vehrencamp SL (1998) Principles of animal communica- ana State University Museum of Natural Science, UWBM University tion. Sinauer, Sunderland of Washington, Burke Museum of Natural History, MBM Marjorie Bryson RW, Faircloth BC, Tsai WLE, McCormack JE, Klicka J (2016) Barrick Museum of Natural History, FMNH Field Museum of Natural Target enrichment of thousands of ultraconserved elements sheds History, MZFC Universidad Nacional Autónoma de Mexico, Museo new light on early relationships within New World sparrows de Zoología, CNAV Colección Nacional de Aves, MVZ University of (Aves: Passerellidae). Auk 133:451–458 California, Berkeley, Museum of Vertebrate Zoology, BMNH James Burns KJ, Shultz AJ, Title PO, Mason NA, Barker FK, Klicka J, Lan- Ford Bell Museum of Natural History, KU University of Kansas yon SM, Lovette IJ (2014) Phylogenetics and diversifcation of Natural History Museum. Those numbers in parentheses represent tanagers (Passeriformes: Thraupidae), the largest radiation of tissue or collector/preparator numbers instead of study-skin voucher Neotropical songbirds. Mol Phylogenet Evol 75:41–77 numbers. Most samples were used by DaCosta et al. (2009), except Capllonch P, Lobo Allende R, Ortiz D, Ovejero R (2005) La avifauna for those of Arremon tocuyensis, Rhynchospiza strigiceps, and Rhyn- chospiza dabbenei de la selva de galería en el noreste de Corrientes, Argentina: Bio- diversidad, Patrones de Distribución y Migración. Temas de la We provide more details on the key samples of Rhynchospiza taxa Biodiversidad del Litoral fuvial argentino II INSUGEO, Misce- (see also ESM 1) lánea 14:483–498 Capurro HA, Bucher EH (1988) Lista comentada de las aves del bosque chaqueño de Joaquín V. Gonzalez, Salta, Argentina. Hornero 13:39–46 References Chavarría-Pizarro T, Gutiérrez-Espeleta G, Fuchs EJ, Barrantes G (2010) Genetic and morphological variation of the sooty-capped Ábalos R, Areta JI (2009) Historia natural y vocalizaciones del Dora- Bush Tanager (Chlorospingus pileatus), a highland endemic dito Limón (Pseudocolopteryx cf. citreola) en Argentina. Ornitol species from Costa Rica and Western Panama. Wilson Bull Neotrop 20:215–230 122:279–287 Alcaide M, Scordato ESC, Price TD, Irwin DE (2014) Genomic diver- Codesido M, Bilenca D (2004) Variación estacional de un ensamble gence in a ring species complex. Nature 511:83–85 de aves en un bosque subtropical semiárido del Chaco Argentino. Areta JI (2008) Entre Ríos Seedeater (Sporophila zelichi): a species Biotropica 36:544–554 that never was. J Field Ornithol 79:352–363 Collar NJ, Fishpool LDC, del Hoyo J, Pilgrim JD, Seddon N, Spottis- Areta JI (2012) Winter songs reveal geographic origin of three migra- woode CN, Tobias JA (2016) Toward a scoring system for species tory Seedeaters (Sporophila spp.) in southern Neotropical grass- delimitation: a response to Remsen. J Field Ornithol 87:104–110 lands. Wilson Bull 124:688–697 Coyne JA, Orr HA (2004) Speciation. Sinauer, Sunderland

1 3 990 Journal of Ornithology (2019) 160:973–991

Cracraft J (1983) Species concepts and speciation analysis. Curr Orni- Kramer-Schadt S, Niedballa J, Pilgrim JD, Schröder B, Lindenborn thol 1:159–187 J, Reinfelder V, Stillfried M, Heckmann I, Scharf AK, Augeri DaCosta JM, Spellman GM, Escalante P, Klicka J (2009) A molecu- DM, Cheyne SM, Hearn AJ, Ross J, Macdonald DW, Mathai J, lar systematic revision of two historically problematic songbird Eaton J, Marshall AJ, Semiadi G, Rustam R, Bernard H, Alfred clades: Aimophila and Pipilo. J Avian Biol 40:206–216 R, Samejima H, Duckworth JW, Breitenmoser-Wuersten C, Belant de la Peña MR (2016) Aves Argentinas: descripción, comportamiento, JL, Hofer H, Wilting A (2013) The importance of correcting for reproducción y distribución. Mimidae a Passeridae. Comunica- sampling bias in MaxEnt species distribution models. Divers Dis- ciones del Museo Provincial de Ciencias Naturales “Florentino trib 19:1366–1379 Ameghino” (Nueva Serie) 21:1–564 Kratter AW, Sillett TS, Chesser RT, O’Neill JP, Parker TA III, Castillo DeMatteo KE, Rinas MA, Zurano JP, Selleski N, Schneider RG, A (1993) Avifauna of a Chaco locality in Bolivia. Wilson Bull Arguelles CF (2017) Using niche-modelling and species-specifc 105:114–141 cost analyses to determine a multispecies corridor in a fragmented Kroodsma DE, Pickert R (1984) Repertoire size, auditory tem- landscape. PLoS One 12(8):e0183648. https​://doi.org/10.1371/ plates, and selective vocal learning in songbirds. Anim Behav journ​al.pone.01836​48 32:395–399 Dinelli L (1918) Notas biológicas sobre las aves del noroeste de la Rep, Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolution- Argentina. Hornero 1:57–68 ary genetics analysis version 7.0 for bigger datasets. Mol Biol Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian Evol 33:1870–1874 Phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol Liebers D, de Knijf P, Helbig AJ (2004) The herring gull complex is 29:1969–1973 not a ring species. Proc R Soc Lond B 271:893–901 Elith J, Graham CH, Anderson RP, Dudík M, Ferrier S, Guisan A, Liu C, Berry PM, Dawson TP, Pearson RG (2005) Selecting thresholds Hijmans RJ, Huettmann F, Leathwick J, Lehmann A, Li J, Lohm- of occurrence in the prediction of species distributions. Ecography ann LG, Loiselle B, Manion G, Moritz C, Nakamura M, Naka- 28:385–393 zawa Y, McC.Overton J, Peterson AT, Phillips S, Richardson K, Marateo G, Povedano H, Alonso J (2009) Inventario de las aves del Scachetti-Pereira R, Schapire R, Soberon J, Williams S, Wisz M, Parque Nacional El Palmar, Argentina. Cotinga 31:47–60 Zimmerman N (2006) Novel methods improve prediction of spe- Marler P (1970) A comparative approach to vocal learning: song cies’ distributions from occurrence data. Ecography 29:129–151 development in white-crowned sparrows. J Comp Physiol Psy- Falls JB, Kopachena JG (2010) White-throated Sparrow (Zonotrichia chol Monogr 71:1–25 albicollis). In: Rodewald PG (ed) The birds of North America. Marshall JT (1964) Voice in communication and relationships among Cornell Lab of Ornithology, Ithaca. https​://birds​na.org/Speci​es- brown towhees. Condor 66:345–356 Accou​nt/bna/speci​es/whtsp​a Mayr E (1963) Animal species and evolution. Harvard University Fernando SP, Irwin DE, Seneviratne SS (2016) Phenotypic and genetic Press, Cambridge analysis support distinct species status of the Red-backed Wood- Merow C, Smith MJ, Silander JA Jr (2013) A practical guide to MaxEnt pecker (Lesser Sri Lanka Flameback: Dinopium psarodes) of Sri for modeling species distributions: what it does, and why inputs Lanka. Auk 133:497–511 and settings matter. Ecography 36:1058–1069 Friedman NR, Remeš V (2017) Ecogeographical gradients in plum- Mlíkovský J (2009) Types of birds in the collections of the Museum age coloration among Australasian songbird clades. Glob Ecol and Institute of Zoology, Polish Academy of Sciences, Warszawa, Biogeogr 26:261–274 Poland. Part 3: South American birds. J Natl Mus (Prague) Nat Gould J (1839) Part 3, Birds. In: Darwin C (ed) The zoology of the Hist Ser 178:17–180 voyage of H. M. S. Beagle. Smith, Elder and Co, London Navas JR (1965) Notas sobre Aimophila strigiceps y su distribución Hellmayr C (1912) Bemerkungen über eine wenig bekannte neotropis- geográfca. Hornero 10:215–224 che Ammer (Zonotrichia strigiceps Gould). Verh Orn Ges Bay Omland KE, Lanyon SM (2000) Reconstructing plumage evolution in 11:187–190 orioles (Icterus): repeated convergence and reversal in patterns. Hellmayr C (1938) Catalogue of birds of the Americas and the adja- Evolution 54:2119–2133 cent islands. Field Mus Nat Hist Zool Ser 13 (pt. 11). https​://doi. Paterson HEH (1980) A comment on “mate recognition systems”. Evo- org/10.5962/bhl.title​.5570 lution 34:330–331 Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very Paterson HEH (1985) The recognition concept of species. In: Vrba high resolution interpolated climate surfaces for global land areas. ES (ed) Species and speciation, vol 4. Transvaal Museum Mono- Int J Climatol 25:1965–1978 graphs, Transvaal Museum, Johannesburg, pp 21–29 Holzmann I, Agostini I, DeMatteo K, Areta JI, Merino ML, Di Bitetti Paynter RA (1967) Notes on the Emberizine sparrow Rhynchospiza MS (2015) Using species distribution modeling to assess factors stolzmanni. Breviora 278:1–6 that determine the distribution of two parapatric howlers (Alouatta Perktaş U, Gosler AG (2010) Measurement error revisited: its impor- spp.) in South America. Int J Primatol 36:18–32 tance for the analysis of size and shape of birds. Acta Ornithol Hoy G (1971) Über Brutbiologie und Eier einiger Vögel aus Nordwest- 45:161–172 Argentinien II. J Ornithol 112:158–163 Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy Irwin DE, Irwin JH, Price TD (2001) Ring species as bridges between modeling of species geographic distributions. Ecol Model microevolution and speciation. Genetica 112–113:223–243 190:231–259 Jaramillo A (2011) Genus Rhynchospiza (species accounts). In: del Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Hoyo J, Elliott A, Sargatal J, Christie DA, de Juana E (eds) Hand- Evol 25:1253–1256 book of the birds of the world, vol 16. Lynx Edicions, Barcelona, Price T (2008) Speciation in birds. Roberts & Co, Denver pp 565–566 Pryke SR, Grifth SC (2009) Postzygotic genetic incompatibility Jordan EA, Areta JI, Holzmann I (2018) Mate recognition sys- between sympatric color morphs. Evolution 63:793–798 tems and species limits in a warbling-fnch complex (Poospiza Rambaut A, Drummond A (2007) Tracerv1.4. http://tree.bio.ed.ac.uk/ nigrorufa/whitii). Emu 117:344–358 softw​are/trace​r/ Klicka J, Spellman GM (2007) A molecular evaluation of the North Remsen JV Jr (2015) [Review of] HBW and BirdLife international American “Grassland” Sparrow clade. Auk 124:537–551 illustrated checklist of the birds of the world. Non-passerines (N.

1 3 Journal of Ornithology (2019) 160:973–991 991

J. Collar and J. del Hoyo, eds.), vol. 1, 903 pp. J Field Ornithol Stein RC (1958) The behavioral, ecological and morphological char- 86:182–187 acteristics of two populations of the Alder Flycatcher, Empidonax Remsen JV Jr (2016) A “rapid assessment program” for assigning spe- traillii (Audubon). N Y State Mus Sci Serv Bull 371:1–63 cies rank? J Field Ornithol 87:110–115 Storer RW (1955) A preliminary survey of the sparrows of the genus Remsen JV Jr, Areta JI, Cadena CD, Claramunt S, Jaramillo A, Pacheco Aimophila. Condor 57:193–201 JF, Pérez-Emán J, Robbins MB, Stiles FG, Stotz DF, Zimmer Taczanowski L (1877) Liste des Oiseaux recueillis en 1876 au nord KJ (2019) A classifcation of the bird species of South Amer- du Pérou occidental par MM. Jelski et Stolzmann. Proc Zool Soc ica. American Ornithologists’ Union. http://www.museu​m.lsu. Lond 1877:319–333 edu/~Remse​n/SACCB​aseli​ne.htm. Accessed 31 Jul 2019 Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large Ridgely RS, Tudor G (1989) The birds of South America, vol 1. Uni- phylogenies by using the neighbor-joining method. Proc Natl versity of Texas Press, Austin Acad Sci USA 101:11030–11035 Salewski V, Watt C (2017) Bergmann’s rule: a biophysiological rule Tobias JA, Seddon N, Spottiswoode CN, Pilgrim JD, Fishpool LDC, examined in birds. Oikos 126:161–172 Collar NJ (2010) Quantitative criteria for species delimitation. Schwartz P (1975) Solved and unsolved problems in the Sporophila Ibis 152:724–746 bouvronides/lineola complex (Aves: Emberizidae). Ann Carnegie Ülker ED, Tavşanoğlu C, Perktaş U (2018) Ecological niche model- Mus 45:277–285 ling of pedunculate oak (Quercus robur) supports the ‘expan- Sharpe RB (1888) Catalogue of birds in the British museum, vol XII. sion–contraction’ model of Pleistocene biogeography. Biol J Lin Passeriformes–Fringilliformes: Part III. Taylor & Francis, London Soc 123:338–347 Short LL (1975) A zoogeographic analysis of the South American Williams MD (1981) First description of the nest, eggs, and young Chaco avifauna. Bull Am Mus Nat Hist 154:165–352 of the Tumbes Sparrow (Aimophila [Rhynchospiza] stolzmanni). Short LL (1976) Aimophila strigiceps new to Paraguay. Auk Condor 83:83–84 93:189–190 Wolf LJ (1977) Species relationships in the avian genus Aimophila. Slabbekoorn H, Smith TB (2003) Bird song, ecology and speciation. Ornithol Monogr 23:1–220 Philos Trans R Soc Lond B 357:493–503 Zimmer KJ, Whittaker A (2000) The Rufous Cachalote (Furnariidae: Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based Pseudoseisura) is two species. Condor 102:409–422 phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690 Publisher’s Note Springer Nature remains neutral with regard to Stattersfeld AJ, Crosby MJ, Long MJ, Wege DC (1998) Endemic bird jurisdictional claims in published maps and institutional afliations. areas of the world: priorities for biodiversity conservation, vol 7. Conservation series. BirdLife International, Cambridge

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