Proposal (1011) to South American Classification Committee

Treat Arremon axillaris as a separate species from A. taciturnus

Note: This is a high-priority issue for WGAC.

Background: Our SACC note on this is as follows:

45b. Hellmayr (1938) treated axillaris as one of four subspecies in his broadly defined Arremon taciturnus (including also “nigrirostris” [see Buainain et al. 2017] and semitorquatus; for the latter, see Note 45). The Colombian subspecies axillaris was treated as a separate species from Arremon taciturnus by del Hoyo & Collar (2016), although Boesman (2016j) did not find major differences between the two. Buainain et al. (2017) provided rationale for treatment of axillaris as a species based on plumage in a PSC framework.

This issue has been on out high priority list for years, but no one seems to want to tackle the problems in this complicated genus. What’s really needed is an overview study of all the taxa, and a synopsis of what’s known about parapatric taxa with little of no gene flow vs. intergrading subspecies taxa (if there are any) so that we at least have some comparative guidelines for assessing data-deficient. I’m not prepared to do that for a SACC proposal.

To set the stage, here are some illustrations and photos. First, here is the plate in Rising (2011) by Brian Small; here axillaris is treated as a subspecies of A. taciturnus , as was “nigrirostris” (see below); and semitorquatus was not illustrated:

And here are cutouts, assembled in a crude geographical layout, from the plate by Brian Small in del Hoyo & Collar (2016) in which axillaris, semitorquatus, and newly described franciscanus are all treated as species:

Here is a photo of axillaris from Macaulay by Linda Rudolph:

Here is a photo from Macaulay by Tini & Jacob Wijpkema from Bolivia of A. taciturnus “nigrirostris”

Here’s a photo from Macaulay of A. semitorquatus from Rio de Janeiro by Ian Davies:

My take from the photos is that I can certainly see why all these were or are considered conspecific if only looking at plumage. Also, note the differences between the photos and the plates, especially the dorsum of semitorquatus.

New information: Del Hoyo & Collar (2014) treated axillaris as a separate species based on the Tobias et al. point scheme as follows (provided by Pam Rasmussen):

“Until recently considered conspecific with A. semitorquatus and hitherto with A. taciturnus, from which it differs in its yellow vs blackish lower mandible (2); more extensive yellow on carpal area (1); no green fringes to flight-feathers, making folded wing much browner (2); slightly shorter tail (effect size vs nominate –1.44, vs nigrirostris –1.29, score 1); use of lower frequencies (typically 7–7.5 vs >8 kHz) in otherwise similar song (2)

(Boesman 2016). This split was confirmed independently by Buainain et al. (2017). Monotypic."

Boesman (2016j), unlike most of his Notes, provided only sample sonograms and did not indicate the sample size on which he based the following conclusion:

“Song of all 3 races is structurally very similar. Race axillaris seems to reach lower frequencies, with hissing end notes typically going down to 7 - 7.5kHz. Other races have end notes staying well above 8kHz. Score 2.

“This vocal difference is thus rather minor, and much less outspoken than vocal difference with Half-collared Sparrow A. semitorquatus.”

The recordings of these birds are tough to work with. To me, they sound more like insects than birds, and most recordings are masked in part by “background” bird vocalizations that are louder than the target species. (I think if I were going to work on these, I would slow recordings down to about ¼ speed – I suspect these birds can hear differences that we can’t appreciate.)

Here’s one of Boesman’s recordings of taciturnus from Suriname: https://xeno-canto.org/271892

And one by Andrew Spencer from Mato Grosso: https://xeno-canto.org/39132

Here’s an axillaris by Oscar Humberto Marin Gómez from Casanare, Colombia: https://xeno-canto.org/245235

Buianain et al. (2017) produced a detailed and rigorous analysis of plumage, morphometrics, and vocalizations in the taciturnus complex, included a wealth of basic taxonomy and nomenclature that will be valuable for any subsequent research. This is a data-rich paper that I encourage you to at least skim. Here, I focus only on the data relevant to the proposal. They proposed that axillaris be treated as a species based on its plumage (under a PSC framework) and a comparison of 8 recordings that were “were not of ideal quality” and so “a quantitative analysis was not possible.” Nevertheless, they found a song type in two of those recordings that was unique to that taxon and not found in their big sample (74) of recordings of taciturnus. Within that sample, in which they also included “nigrirostris” of southwestern Amazonia (which they showed in their plumage analysis represented clinal variation in pectoral band width), quantitative (DFA) analysis of song parameters revealed considerable subtle geographic variation, generally associated with geographic region, i.e. dialect formation, although they did not use that term. Descriptive analyses of the same variation, however, did not reveal any consistent differences among regions. Their conclusion in the Abstract is: “All these species, besides A. taciturnus and A. axillaris, also have clearly different vocalizations”. (By “all these species they were referring also to A. semitorquatus and A. franciscanus.). Thus, they recognized that their N for axillaris was insufficient for drawing strong conclusions.

Here is the figure that summarizes their classification and distribution. (Beware that the wing coverts show color distortion, especially for axillaris unfortunately, due perhaps to them being four separate images; compare to photos above)

Buainain et al. (2022) added genetic data to explore the relationships of these and all other Arremon, including the Andean taxa formerly included in Atlapetes and Lysurus. They sampled 92 individuals representing 18 of 19 species and 47 of 50 recognized subspecies to generate a UCE data-set. Here is their time-calibrated tree:

The goal of Buainain et al. (2022) was to study diversification rates and historical biogeography in lowland and highland taxa in Arremon, not phylogenetics per se, and they implied that further studies focusing on taxonomy are under way. Therefore, I think it is best to postpone any taxonomic recommendations on species rank until that follow-up study is published. Most of the tree is consistent with current taxonomy, but there are some bug surprises. For now, relevant to the current proposal, the important results is that axillaris and taciturnus are sister taxa, as they have been treated “forever”, but (1) the branch connecting them is fairly long compared to many taxa currently ranked as species, and (2) these two are not sisters to the semitorquatus-franciscanus pair, thus removing any doubt on species rank for semitorquatus vs. taciturnus. If we were to base our current decision on comparative branch lengths, then we would also have to elevate four subspecies in A. aurantiirostris to species rank as well … which could be the best decision in the long run, but not now. Clearly, this genus is a goldmine for the study of comparative rates of phenotypic characters.

Discussion and Recommendation: I don’t have a firm recommendation on this one. In my view, it all depends on interpretation of differences in song between axillaris and taciturnus, and without an analysis of a larger sample of good recordings of axillaris, I lean slightly towards a NO, pending comments from others, especially those more familiar with vocal analyses.

English names: If the proposal passes, the name “Yellow-mandibled Sparrow” has a track record of at least 7 years and has merit with respect to taciturnus (but not semitorquatus; both have yellow mandibles, but in axillaris the yellow extends to upper mandible also; to be pedantic, mandible and maxilla refer to separate bones, whereas the correct terms for their surfaces are upper mandible and lower mandible). The range of axillaris is tiny compared to taciturnus, so no need to concoct new names for both, as per our SACC guidelines. If someone objects to this, then please write a proposal. Otherwise, I suggest we just go with the existing name.

References: (see SACC Bibliography for standard references)

BOESMAN, P. 2016j. Notes on the vocalizations of Pectoral Sparrow (Arremon taciturnus). HBW Alive Ornithological Note 361. In: Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona.

BUAINAIN, N., C. P. DE ASSIS, AND M. A. RAPOSO. 2017. Geographic variation and taxonomy of the Arremon taciturnus (Hermann, 1783) species complex (Aves: Passerellidae). J. Ornithology 158: 631–650.

BUAINAIN, N., , M. FERREIRA, J. E. AVENDAÑO, C. D. CADENA, B. C. FAIRCLOTH, R. T. BRUMFIELD, J. CRACRAFT, AND C. C. RIBAS. 2022. Biogeography of a Neotropical songbird radiation reveals similar diversification dynamics between montane and lowland clades. J. Biogeography 49: 1260-1273.

Van Remsen, June 2024

Comments from Robbins: “For now, NO, primarily based on the statement Buainain et al. apparently are doing further work that will elucidate the taxonomy.”

Comments from Jaramillo: “YES – I don’t think there is a need to wait. But in the future we likely will be separating these further.”

Comments from Areta: “Here is some background info in case it is needed:

Photos of axillaris
Photos of taciturnus/nigrirostris

Sounds at ML of taciturnus/nigrirostris
Sounds at ML of axillaris
Sounds at XC

“I found this photograph (misplaced?) of a black-billed bird at a locality in which the birds look like typical axillaris.

“There are some minor plumage distinctions between axillaris and taciturnus (see Table 2 from Buainain et al 2017):

“Regarding vocalizations, the abstract of Buainain et al (2017) seems to convincingly indicate that the vocalizations are very different, but then the body of the paper portraits a very different message, in which there are two song types that are very similar between them and also very similar to the song of taciturnus (see how different the other species are by looking at spectrograms in Buainain et al 2017):

‘Arremon axillaris (n = 8) has two song types. Unfortunately because recordings were not of ideal quality, a quantitative analysis was not possible. Song type 1 is very similar, possibly identical, in sound and structure to the pattern found in A. taciturnus. Both song types seem to occupy the same frequencies and have similar quantitative parameters, with highly overlapping values. Song type 2 (Fig. 11) is very similar to type 1 (and the song of A. taciturnus), but it is at least 1 kHz lower in frequency with possibly no overlap. Song type 2 was registered in only two recordings. In the first, the song was performed by a single individual. In the second, the song was performed just a little after a second individual had finished singing song type 1. Although this might be a variation of repertoire in the second individual, the pattern resembles a duet between male and female since the songs are highly similar but occupy slightly different frequencies (Koloff and Menill 2013). Unfortunately, the lack of information with regards to the sex of the singing individuals prevents us from making any further assumptions. Nevertheless, if A. axillaris is a duetting species, this would provide valuable information regarding the evolution and taxonomy of the group as it has not been recorded in any other Arremon species. Either way, song type 2 is clearly different from song type 1 and the song of A. taciturnus, and can be used to differentiate the two taxa. In addition to the several plumage similarities between A. axillaris and A. taciturnus, the similarities in song provide further evidence of a possible close relationship between them.’

“Then, there is Buainain et al (2022), showing a level of genetic divergence that would seem in principle more consistent with two species-level taxa in the genus than with subspecies status. Although the tree may seem to have been based on single samples, the Appendix S1 shows that 2 axillaris and 8 taciturnus were sampled.

“I am not wholly convinced of treating axillaris and taciturnus as species or subspecies. The plumage distinctions seem relatively minor, the bill colour is a striking difference, vocalizations seem to differ to some degree but are much more similar than the similarly diverged A. franciscanus and A. semitorquatus, and there is a fairly deep genomic divergence. Buainain et al. (2017) already discussed the taxonomy of taciturnus (splitting axillaris), and Buainain et al. (2022) adopted that classification. Thus, I don´t think that an upcoming paper will propose a different taxonomy, especially given the new phylogenetic data. I will thus vote YES to the recognition of Arremon axillaris, while acknowledging that more song samples for a better acoustic characterization and some clarification on whether there are black-billed and half-yellow-billed birds coexisting in Meta (Colombia) would be most welcome.”

Comments from Stiles: “NO, at least for now, given that this situation is receiving further study that could tip the balance one way or the other for splitting.”

Comments from Lane: “YES, largely based on the comments Nacho provided. I will add that most of the color-billed Arremon sparrows have blackish bills as juveniles, so I suspect the photo he linked to of a black-billed bird in the range of axillaris is going to be a juv. Now, we need to split off A. spectabilis from the A. aurantiirostris group, given that they are not even sisters (and sound worlds apart)!”

Comments from Claramunt: “YES. The differences in the color of the bill and wings are notable, plus more subtle but consistent difference in the extension of the white supercilium suggest that axillaris is a separate lineage. I don’t see how these differences can be considered “minor” given how conservative the genus Arremon is; the differences are even more obvious in the photographs than in the illustrations. I see no justification for maintaining axillaris as a subspecies of taciturnus.”

Comments from Gustavo Bravo (voting for Remsen): “YES. I think there is enough published evidence to support a two-species treatment here. I agree with Santiago that, given the context of relatively conserved phenotypic variation in the genus, the observed differences between axillaris and taciturnus are substantial."

Additional comments from Stiles: “I will very tentatively maintain my NO on this one, but for different reasons. First, the ranges of these two are decidedly misleading in the figure: that of taciturnus extends well to the west and may approach that of axillaris, which in turn extends eastward more than is noted in the same figure. The two could be in contact in the Macarena region: at least, a difference of ca. 25-30 km may separate specimens of the two here. However, my examination of the data was very brief, and I need to get back to the collection to apply the scheme for separating them given in Table 1. I note that how the make of the specimens often obscures differences in carpal and wing patterns and should be taken into account, and I must check to see if any voice recordings have been made in the possible contact area.”

Comments from Luciano Naka (voting for Del-Rio): “YES. With the information provided, I am happy to consider the Colombian population as a species-level taxon. There are two allopatric populations with morphological (and potential ecological) differentiation, and subtle vocal differences, but with a unique diagnostic song type in axillaris. Unfortunately, the tree is not very useful, except for showing that axillaris and taciturnus are each other’s closest relatives within the sample provided. In my view, branch length does not help decide whether the two taxa are best considered different species. It would be nice to see a population level admixture analysis, which could show if there is extensive introgression or not, but I don’t think this information is coming any time soon. At the time being, Buainain et al. (2022) show morphological and vocal diagnostic features, and their allopatric distribution seem to indicate lack of current gene flow. So, I would go for a YES for separating the Colombian form from the more widespread Amazonian lowland population.”

Comments from Bonaccorso: “YES. Although the plumage differences are not significant and bill color seems labile (according to the Buainain et al. 2022 tree), they make Arremon axillaris diagnosable. Even if the songs of axillaris and taciturnus are not different enough, there might not be strong selection pressures for these two allopatric lineages (if they are indeed allopatric) to change their song extensively. Also, I am impressed by the long branches separating axillaris and taciturnus, despite the meager sample size. Even if they hybridize in eastern Colombia, I would expect that such differences in UCEs would be accompanied by more differences that could generate important genome conflicts, rendering hybrids less fit, which would generate a very narrow contact zone.”

Comments from Stiles: “YES after a detailed examination of plumages and distributions. The most interesting discovery regarding distributions was that, with reference to the map presented in the proposal indicating a gap of 400-500 km between these taxa, the ICN collection supplied specimens of personatus from Araracuara and the Sierra de Chiribiquete, the latter reducing this gap to ca. 100 km (to the Olivares record of axillaris just SE of the southern tip of the Serranía de la Macarena, with no suggestion of a hybrid zone (a few specimens of axillaris approach personatus in colors, but are scattered throughout its distribution and essentially the same occurs in personatus).

“Hice un examen de especímenes y registros en la colección del ICN y encontré registros de personatus del Sa. de Chiribiquete y Araracuara que extendieron su distribución en Colombia hacia el S y SW, reduciendo la brecha entre axillaris y personatus desde ca. 400 km (en la mama de la propuesta) hasta ca. 100 km. -en el proceso, encontré algunos especímenes de ambas que muestran similitudes con la otra pero regados en todas sus respectivas distribuciones sin indicios de ser concentradas en la zona de máxima aceración - es decir, sin dar inicios de una zona de hibridación. Por esto, mi voto sería YES para la separación de las dos como especies.”

Comments from Zimmer: “YES, for all of the reasons given by Nacho, Santiago, Gustavo, Elisa, Luciano and Gary. I would particularly echo the comments that phenotypic variation within the genus is relatively conserved, lending greater weight, in my opinion, to any diagnosable morphological characters. The relatively similar vocalizations between axillaris and taciturnus give me a little pause, given what I’ve always felt were significant differences between songs of taciturnus and semitorquatus, but then again, we now know, thanks to the tree in Buainain et al. 2022, that taciturnus and semitorquatus are not sisters, whereas taciturnus and axillaris are. Again, despite the similarities between the two, axillaris does appear to have a diagnosably different 2^nd song type. I’m further persuaded by the relatively long branch length connecting axillaris and taciturnus. I would note that the tree shows a similarly long branch connecting A. aurantiirostris rufidorsalis (which, I believe, is the subspecies occupying the Caribbean lowlands of Costa Rica – Gary, please correct me if I’m wrong on this.) and A. a. aurantiirostris, which is the taxon occupying the Pacific lowlands of Costa Rica. Back when I was spending a lot of time in Costa Rica, it was always my impression that those two taxa had VERY different songs, differing not just in mean frequency, but also, markedly, in syntax and pattern. I always thought of them as ripe for splitting on vocalizations alone, but never pursued it, and it has now been ca. 20 years since I was last there. I never noticed any such Caribbean versus Pacific Slope differences in the songs of Orange-billed Sparrows in C & E Panama, but then again, a lot of lowland taxa down there extend across both slopes, once you get south of the Talamanca highlands. Anyway, I realize this is a digression, but my overall impression of the genus is that it has been under-split in terms of species-limits, and that if there are demonstrable diagnostic plumage/bare parts differences coupled with vocal differences, no matter how subtle, and no evidence of hybridization/intergradation, then that suggests two species to me.”