Proposal (1057) to South American Classification Committee

Revise species limits in Automolus ochrolaemus. A. Treat extralimital Central American exsertus as a separate species; B. Treat extralimital Middle American cervinigularis as a separate species (from exsertus and ochrolaemus)

Note from Remsen: The two parts of this proposal are separate proposals relayed from NACC, which treated exsertus as a separate species in 2018 (Chesser et al. 59^th Supplement 2018; proposal 2018-A-2) and cervinigularis as a separate species in 2024 (Chesser et al. 65^th Supplement 2024; proposal 2024-c-22; passed 8-2). We have to process these because they affect what SACC considers to be A. ochrolaemus and also because these extralimital splits potentially affect our English names.

Also, the sequence of the proposals and the names can be confusing because they were separate proposals in NACC. The first one A deals with splitting Pacific slope exsertus from everything else, namely broadly defined ochrolaemus, and then B deals with splitting the rest of the Middle American populations (as cervinigularis) from the basically South American ochrolaemus.

Effect on SACC: No effect other than to change what we would assign to the range of A. ochrolaemus

Our current SACC note reads:

85c. Chesser at al. (2018) treated the Central American exsertus group as a separate species following the results of Freeman and Montgomery (2017). Dyer and Howell (2023) treated exsertus group and the Middle American cervinigularis group as separate species from A. ochrolaemus. Chesser et al. (2024) treated Middle American cervinigularis as a separate species from A. ochrolaemus based on comparative genetic distances (Smith et al. 2014). SACC proposal needed.

Part A. Treat Automolus ochrolaemus exsertus as a separate species from Buff-throated Foliage-gleaner A. ochrolaemus

Background: Automolus ochrolaemus, the Buff-throated Foliage-gleaner, is found in humid lowland forests across a large swath of Central and South America. There is substantial plumage, vocal and genetic variation within its broad distribution (see Smith et al. 2014 for phylogeographic structure, and Remsen 2017 for descriptions of plumage and vocal variation). This proposal concerns two of the populations found within Central America: exsertus, which occurs on the Pacific slope of Costa Rica (and adjacent western Panama), and hypophaeus, which is found along the Caribbean slope of Central America. These two populations are geographically isolated and ~ 6% different in mtDNA (cyt b), suggesting they last shared a common ancestor around 3 million years ago. They differ in voice and are roughly similar in plumage (Remsen 2017).

New information: Freeman and Montgomery (2017) conducted playback experiments on 15 territories of exsertus and 14 territories of hypophaeus. Each playback experiment measured whether populations discriminated against song from the other population; thus, these experiments simulated secondary contact between these two geographically isolated populations. Briefly, each experiment measured the behavioral response of a territorial bird to two treatments: 1) song from the local population (sympatric treatment) and 2) song from the allopatric population (allopatric treatment). All territorial birds responded to sympatric song by approaching the speaker (typically to within 5 m).

We defined song discrimination as instances in which the territory owner(s) ignored allopatric song, defined as a failure to approach within 15 m of the speaker in response to the allopatric treatment. We calculated song discrimination for each taxon pair as the percentage of territories that failed to approach the speaker in response to allopatric song. For example, a song discrimination score of 0.8 indicates that 80% of territorial birds (e.g. 8 out of 10) ignored allopatric song while simultaneously actively defending a territory. We assume that song discrimination is a proxy for premating reproductive isolation; that is, our experiments provide insight into whether these populations would recognize each other as conspecific and interbreed (or not) were they to come into contact with one another. It is unknown what degree of song discrimination is “enough” that song constitutes a strong enough premating barrier to reproduction that allopatric populations merit classification as distinct biological species. To provide a yardstick, we considered nine allopatric Neotropical taxon pairs that were recently split (or have pending proposals to the South American Classification Committee) in part based on differences in vocalizations. We found the average song discrimination in these nine taxon pairs to be ~ 0.6 (60% of territorial birds ignored allopatric song) and suggest that species limits deserve to be reconsidered when taxon pairs currently classified as subspecies have song discrimination scores above ~ 0.6.

We found that 13 out of 15 territorial birds from the Pacific slope of Costa Rica (exsertus) discriminated against song playback of Caribbean hypophaeus (discrimination = fail to approach within 15 m of the speaker). Results were similar in the opposite direction: 12 out of 14 territorial birds from the Caribbean slope of Costa Rica (hypophaeus) discriminated against song playback of Pacific exsertus (discrimination = fail to approach within 15 m of the speaker).

Recommendation:

Populations of Buff-throated Foliage-gleaners from the Pacific and Caribbean slopes of Costa Rica respond strongly to local song but essentially ignore song from their relatives across the mountains. This suggests that vocal differences constitute a strong premating barrier to reproduction between these taxa and is consistent with the genetic data that indicates that, despite their close geographic proximity, these populations last shared a common ancestor ~ 3 million years ago. I therefore recommend treating exsertus and hypophaeus as distinct biological species. In practice, this means that I recommend treating exsertus as a distinct biological species from the entire rest of the Buff-throated Foliage-gleaner complex. There may be additional biological species lurking within this complex. For example, we documented strong song discrimination between hypophaeus and pallidigularis (found in eastern Panama and northwestern South America; these two taxa presumably interact in a contact zone in central Panama and may prove to be distinct biological species. As for an English name for exsertus, Ridgway (1911) and Cory and Hellmayr (1927) called it "Chiriqui Automolus", which would translate to "Chiriqui Foliage-gleaner", which would seem to be a reasonable name.

Literature Cited:

Freeman, B. G., & Montgomery, G. A. 2017. Using song playback experiments to measure species recognition between geographically isolated populations: A comparison with acoustic trait analyses. The Auk 134(4), 857-870.

Remsen, J.V., Jr (2017). Buff-throated Foliage-gleaner (Automolus ochrolaemus). In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A. & de Juana, E. (eds.). Handbook of the Birds of the World Alive. Lynx Edicions, Barcelona. (retrieved from http://www.hbw.com/node/56571 on 20 October 2017).

Smith, B.T., McCormack, J.E., Cuervo, A.M., Hickerson, M.J., Aleixo, A., Cadena, C.D., Perez-Eman, J., Burney, C.W., Xie, X., Harvey, M.G. and Faircloth, B.C., 2014. The drivers of tropical speciation. Nature 515. 406-406.

Benjamin Freeman, May 2025

Part B. Treat Automolus cervinigularis as a separate species from Buff-throated Foliage-gleaner A. ochrolaemus

Description of the problem: Automolus ochrolaemus (Tschudi, 1844) is a wide-ranging polytypic species of the lowland Neotropics, found in lowland rainforest nearly throughout the Neotropics from southern Mexico through the Amazon Basin. Until 2018, this was generally considered a single polytypic species with seven subspecies. From north to south, these taxa are: cervinigularis (Sclater, 1857) of Mexico to Guatemala; hypophaeus Ridgway, 1909 of Nicaragua to northwestern Panama on the Caribbean slope; exsertus Bangs, 1901 of the Pacific slope of Costa Rica and far southwestern Panama; pallidigularis Lawrence, 1862 of eastern Panama south through the Choco to northwestern Ecuador; turdinus (Pelzeln, 1859) of the western Amazon Basin and Guiana Shield; ochrolaemus (Tschudi, 1844) of the southwestern Amazon Basin; and auricularis Zimmer, 1935 of the southeastern Amazon Basin (Birds of the World, 2023). Another subspecies, amusos, is sometimes recognized from Honduras and Nicaragua, or considered a synonym of cervinigularis or hypophaeus.

Ridgway (1911) considered the complex to comprise three species: A. cervinigularis (including hypophaeus), A. pallidigularis (including exsertus), and although not covered in his volumes, implicitly considered A. ochrolaemus for all the extralimital taxa.

NACC proposal 2018-A-2 elevated exsertus to species rank based on allopatry from hypophaeus, mitochondrial divergence, and song discrimination in playback trials between exsertus and hypophaeus, and NACC adopted the English name Chiriqui Foliage-gleaner. NACC adopted this split 8-2, with some committee member comments mentioning that the rest of the taxa found west of the Andes might eventually be split from the Amazonian taxa, pending further research. WGAC, in addressing discrepancies among global lists, also chose to adopt the split of A. exsertus, but went one step further and split the other two Middle American taxa as a species (A. cervinigularis, with hypophaeus) separate from the South American taxa. They opted, however, to retain pallidigularis of eastern Panama and the Choco with A. ochrolaemus of the Amazon Basin and Guiana Shield.

New information:

1. Genetics:

Smith et al. (2014) sampled all taxa in this group using the mitochondrial gene cytochrome b and estimated a gene tree that was fairly well resolved. Below is the supplemental figure for the genus from Smith et al. (2014) showing the sampling map, ecological niche model, and the gene tree. On the left is the time-calibrated gene tree, and on the right is the same tree with species as circumscribed by the species delimitation method bGMYC.

Broadly, Smith et al. (2014) found that exsertus and cervinigularis/hypophaeus were sister groups, which in turn were sister to the remainder of the ochrolaemus complex. The Choco taxon pallidigularis was embedded within the rest of the South American taxa from east of the Andes. To better illustrate these relationships, I have included an enlarged version of the bGMYC tree above, with the corresponding taxa labeled to the right of each cluster. Note that that outgroup has been removed here to better highlight the few samples of exsertus at the bottom of the tree. The time scale is in millions of years.

Shultz et al. (2017) sampled two mitochondrial genes (ND2 and cytochrome b) for most taxa in the group, except exsertus, and recovered a similar topology to Smith et al. (2014). However, they recovered pallidigularis as sister to the remaining South American taxa rather than embedded within them. Shultz et al. (2017) also sequenced three nuclear genes for these samples, but they showed no differentiation across the group, as is often the case. They are not shown here.

Harvey et al. (2020) sampled two individuals in the complex: one hypophaeus from Costa Rica and one turdinus from Peru. These samples were sisters, with a divergence time of about 2 Ma, which is consistent with the mitochondrial data, but doesn’t provide much information for taxonomy.

Claramunt et al. (2013) sequenced three mitochondrial and three nuclear genes and recovered a topology consistent with the other studies included here, with pallidigularis clustering with the Amazonian taxa, and hypophaeus sister to the rest (exsertus, cervinigularis, and auricularis not sampled). A portion of the tree from Claramunt et al. (2013) is shown below.

2. Voice:

Although nothing is published on vocalizations that I can find, there is considerable vocal variation in the group, and this is partly the basis for elevating exsertus to species rank. In listening to vocalizations, there are essentially two vocal groups in the complex: one with a slower series of nasal descending notes comprised of ochrolaemus, auricularis, turdinus, and pallidigularis, and another with a faster song comprised of harsher notes sometimes strung into a longer rattle. This latter group is comprised of cervinigularis, hypophaeus, and (to an extent) exsertus. In listening to recordings, it does seem like exsertus (https://birdsoftheworld.org/bow/species/butfog4/cur/multimedia?media=audio) has consistently slower songs than cervinigularis/hypophaeus (https://birdsoftheworld.org/bow/species/butfog9/cur/multimedia?media=audio) with a somewhat harsher quality to the notes (thus, very unlike the South American group). Some recordings of cervinigularis/hypophaeus also have a two-parted aspect to the song, with the note shape being distinctly different in the first half of the song, and with the second half often trailing off into a long rattle.

Songs of the three Amazonian taxa (ochrolaemus, auricularis, and turdinus) are remarkably constant across their range: https://birdsoftheworld.org/bow/species/btfgle1/cur/multimedia?media=audio. However, pallidigularis adds a bit of complexity to the matter. Recordings from the southern end of its range in Ecuador closely resemble those of the Amazonian taxa (e.g. https://macaulaylibrary.org/asset/140267791, whereas those at the northern end of its range in eastern Panama and northwestern Colombia are a bit faster (https://macaulaylibrary.org/asset/60369, https://macaulaylibrary.org/asset/286906, https://macaulaylibrary.org/asset/610186681). That variation aside, there does seem to be a rather sharp break between sweeter-sounding birds in the Canal Zone (e.g. https://macaulaylibrary.org/asset/28412) and rattling birds in the far west of Panama on the Caribbean slope (https://macaulaylibrary.org/asset/214530601). It is also possible that some of the recordings linked above are after playback so the birds may be singing a more intense song, as at least some recordings from the Canal Zone are slower and much more like Amazonian birds (https://xeno-canto.org/448169).

Plumage:

David Vander Pluym was nice enough to photograph a series of specimens of the taxa in this complex that are housed at the Louisiana State University Museum of Natural Science (LSUMNS). Photos in dorsal, lateral, and ventral views are shown below. In each photo, 2-3 individuals of each taxon are shown, with the taxon name written above, and the red vertical lines separating the proposed species. The taxa from left to right are: auricularis, ochrolaemus, turdinus, pallidigularis, exsertus, hypophaeus, and cervinigularis.

Ridgway (1911) had some insights into the plumage and morphometrics of this complex. As is noted above, he recognized three species in the group, although these are not the arrangement that is currently being considered, it is also not the broad polytypic circumscription. Regarding cervinigularis, he noted:

“Mexican specimens average decidedly deeper in color than others, especially the buff of superciliary stripe, throat, etc., and brown of pileum, the latter almost sooty in its darkness. Guatemalan examples have the back, etc., more rufescent or castaneous, those from Honduras, British Honduras, and Nicaragua more olivaceous than Mexican specimens. The series examined is, however, inadequate.”

For hypophaeus, he noted that it was “Similar to A. c. cervinigularis but coloration decidedly darker, especially under parts of the body, which are isabella color medially darkening laterally into deep buffy olive, contrasting strongly and abruptly with the buff or ochraceous-buff of chin and throat.” Ridgway (1911) considered specimens from Veraguas in western Panama to be hypophaeus but had no samples between there and the Canal Zone, which he considered pallidigularis. Thus, no specimens from the potential contact zone were available to him. Regarding these samples of pallidigularis, he noted that it was “Somewhat like cervinigularis but superciliary stripe much less distinct (the supra-auricular portion more or less obsolete), general coloration paler, feathers of chest without darker margins, and size smaller.” Regarding exsertus, which he considered a subspecies of A. pallidigularis, he said it was “Similar to A. p. pallidigularis but slightly larger, with relatively longer bill, color of back, etc., more olivaceous, chest uniform in color, and buff of throat, etc., deeper.”

All of Ridgway’s comments seem (unsurprisingly) consistent with the patterns shown in the photos above. Plumage is clearly conserved across the group, with more intra-specific (if the split is adopted) than inter-specific plumage variation. To my eye, the pale throat of pallidigularis really stands out, as do the generally warmer underparts of cervinigularis. However, other characters like bill size, degree of mottling on the chest, and intensity of the olive below, all seem to vary.

Cory and Hellmayr (1925) merged all taxa into a polytypic A. ochrolaemus, which seems to be the basis for much of the modern treatment of the group until exsertus was elevated to species rank by NACC. Although they did not elaborate on the decision to merge all these taxa into one species, the following footnote for pallidigularis is of particular interest:

“It will be remembered that Salvin and Godman (Biol. Centr.-Americ, Aves, 2, p. 158, 159) record both A. cervinigularis and A. "pallidigularis" from the Veraguas. Although no specimens are available I have little doubt that all the birds of that region will ultimately prove to belong to A. o. exsertus. One of our Bogava skins, by reason of its distinct postocular stripe and decidedly rufous under tail-coverts, closely approaches the eastern hypophaeus, and it is probable that similar examples (which obviously represent only the extreme of individual variation) have given rise to the reported occurrence of “cervinigularis" in the Veraguas.”

Bogava is in the lowlands of Chiriquí, well within the range of exsertus. If I am interpreting this passage correctly, Cory and Hellmayr (1925) are suggesting that exsertus from the far east of its range might approach hypophaeus in plumage. There are low passes over the Talamancas in this region, and it is possible that the two taxa might locally be in secondary contact.

Recommendation: I very tentatively recommend a YES vote on splitting cervinigularis from ochrolaemus, which would bring us in line with WGAC. The vocal differences between the cervinigularis group and the ochrolaemus group are certainly much greater than those that led to the split of exsertus from cervinigularis. However, those taxa are allopatric and had good data on vocal discrimination, whereas cervinigularis and ochrolaemus are certainly in contact in west-central Panama but without any data from the contact zone.

The split then rests on two primary factors: the primarily mitochondrial gene trees showing a close relationship between cervinigularis and exsertus (thus rendering ochrolaemus sensu lato paraphyletic if it includes the cervinigularis group) and the very qualitative assessment of vocal differences included here. Those two factors are admittedly quite highly differentiated, and more so than are the differences that led to the split of exsertus. WGAC used this same reasoning to strongly advocate for the split of cervinigularis.

WGAC adopted the English common names of Fawn-throated Foliage-gleaner for A. cervinigularis and Ochre-throated Foliage-gleaner for A. ochrolaemus, and if the split passes I recommend that we follow suit. Because this is a parent-daughter split (mostly, anyway), new names should be adopted for the daughter species and Buff-throated should be abandoned. I note, however, that Ridgway (1911) used Buff-throated for cervinigularis sensu stricto. ‘Cervinus’ refers to ‘stag-like’, hence the common name of Fawn-throated, which I think is a good name. Ochre-throated also parallels the scientific name for ochrolaemus and is similar to the “Ochraceous-throated” used by Cory and Hellmayr (1925). Ridgway (1911) used Pale-throated for pallidigularis sensu stricto, which is an appropriate name if that taxon is eventually elevated to species rank.

Literature Cited:

Birds of the World. 2023. Edited by S. M. Billerman, B. K. Keeney, P. G. Rodewald, and T. S. Schulenberg. Cornell Laboratory of Ornithology, Ithaca, NY, USA. https://birdsoftheworld.org/bow/home.

Claramunt, S., Derryberry, E.P., Cadena, C.D., Cuervo, A.M. Sanín, C., and Brumfield, R.T. 2013. Phylogeny and classification of Automolus foliage-gleaners and allies (Furnariidae). The Condor, 115(2), 375–385, https://doi.org/10.1525/cond.2013.110198

Cory, C. B. and Hellmayr, C. E. 1925. Catalogue of Birds of the Americas, pt. 4. Field Mus. Nat. Hist. Zool. Ser. 13: 1–390.

Harvey, M.G., et al. 2020. The evolution of a tropical biodiversity hotspot. Science 370,1343-1348. DOI:10.1126/science.aaz6970

Ridgway, R. 1911. The Birds of North and Middle America, part 5. Bull. U.S. Nat. Mus. 50: 1–859.

Schultz, E.D., Burney, C.W., Brumfield, R.T., Polo, E.M. Cracraft, J., Ribas, C.C. 2017. Systematics and biogeography of the Automolus infuscatus complex (Aves; Furnariidae): Cryptic diversity reveals western Amazonia as the origin of a transcontinental radiation. Molecular Phylogenetics and Evolution, 107: 503-515. https://doi.org/10.1016/j.ympev.2016.12.023.

Smith, B., McCormack, J., Cuervo, A. et al. 2014. The drivers of tropical speciation. Nature 515, 406–409. https://doi.org/10.1038/nature13687.

Oscar Johnson, May 2025

Note from Remsen on English names: If the proposals pass, I see no immediate reason for us to meddle with English names already chosen by NACC (Chiriqui Foliage-gleaner and Fawn-throated Foliage-gleaner), but if someone objects, speak up and be prepared to write separate proposals.

Comments from Remsen:

“A. [taken from his comments on the original NACC proposal]: YES. Discrimination in playback trials usually correlates with assortative mating and absence of free gene flow, and so I interpret these data as showing that these two taxa have differentiated to the point associated with barriers to gene flow between parapatric/sympatric species. No one who does playback trials thinks that this is directly equivalent to mate choice, but rather that it is an index of potential gene flow if the two were in contact based, empirically, on many examples that go both ways, i.e. taxa that do not mate assortatively show strong playback responses, and those that do mate assortatively show low levels of response. All of this is discussed in detail in various papers using playback trials. In the imperfect world of assigning taxon rank to allotaxa, use of playback trials is one of the stronger tools we have, for better or worse. Much of our current taxonomy is based on playback trials or degree of divergence in vocal characters. That professional and amateur ornithologists worldwide use tape playback to find particular species provides testimony to the common sense behind interpretation of playback as a determinant of taxon rank.

“Of course, in a perfect world we would wait for comparable data between other taxa in the ochrolaemus complex, but without a guarantee that such a project is underway, I favor endorsing this split now. Perhaps this will catalyze work on other members of the group.

“There seems to be confusion in terms of what the proposal actually proposes. As in the Recommendation, the allopatric population of the Chiriquí lowlands is proposed as a separate species, A. exsertus (Chiriqui Foliage-gleaner) from all other populations of A. ochrolaemus. As for Pam's question on whether they are truly allopatric, I assumed that this is the case because these birds don't get higher than 1400 m, but I have now checked with César Sánchez (who is doing his dissertation on birds of this region of endemism), who confirms that they are allopatric as far as is known. The reason hypophaeus remains associated with A. ochrolaemus s.l. is that it is parapatric with other subspecies treated within A. ochrolaemus; these form a nearly contiguous set of 3 subspecies that extend from SE Mexico through Panama across N Colombia. Then, there is a gap between those populations and the 3 subspecies east of the Andes in Amazonia, and as noted by Pam, that's where a big change occurs in song. That the song of hypophaeus may or may not be closer to nominate ochrolaemus or other subspecies is a separate issue that should be addressed in future research. As Cadena and Cuervo have shown with Arremon brush-finches in the Andes, geographic patterns in song variation can show a leapfrog pattern, so comparisons of these two Costa Rican taxa to the rest of the complex must be done comprehensively.”

“B. NO, reluctantly. I can see why Oscar’s recommendation was highly tentative, and I wonder if WGAC had not already voted on this whether the recommendation would be different. Using a mtDNA gene tree to infer phylogeny (from Smith et a. 2014) is just not scientifically valid in 2025, in my opinion. As for the voices, I can hear a difference, of course, between the few linked recordings. But we’ve debated about with Boesman’s published analyses were sufficient for taxonomic decisions, so how can we make a taxonomic decision based, in my opinion, solely (given uncertainty of mtDNA gene tree) on a couple of recordings without knowing the full variation represented across the ranges of these taxa? As a matter of principle, I think we should require better scientific evidence to change the status quo, even if the status quo is insufficiently grounded in data. This does not mean that I interpret the current data as indicating BSC conspecificity but rather than the data so far are inadequate for making a change.

“The two dissenting NACC voters made these points independently and were not willing to vote for a split based on a gene tree and unpublished qualitative assessment of a few sonograms. Both emphasized the need to study the contact zones.”

“The big problem with a NO on this is that it would leave our broadly ochrolaemus as paraphyletic with respect to exsertus if the gene trees of Smith et al. (2014) and Schultz et al. (2017) are species trees. I suspect this will be resolved soon with genomic data from the Harvey lab or elsewhere.”