Proposal (921) to South American Classification Committee
Treat Trogon rufus (Black-throated Trogon) as consisting of five species, including one newly described
Effect on SACC list: This proposal would treat our Trogon rufus as consisting of five species, one of which is newly described.
Background: Our current Note reads as follows:
7c. Dickens et al. (2021) found evidence that T. rufus should be treated as five separate species, including one newly described: Trogon muriciensis of the Atlantic Forest patches of northeastern Brazil; they recommended elevating the subspecies tenellus, cupreicauda, and chrysochloros to species rank. SACC proposal badly needed.
Trogon rufus (Black-throated Trogon) is a polytypic species with one of the largest distributions of any trogon, with taxa treated as (nine described) subspecies occurring in three disjunct regions: (1) from Honduras to the Chocó of northwestern South America, (2) Amazonia; and (3) the Atlantic Forest from Alagoas through Brazil to eastern Paraguay and Misiones, Argentina. They have all been treated as conspecific from Cory (1919; albeit as T. curucui due to early name confusion), Pinto (1937), and Peters (1945) through the present.
Here's the map (from Dickens et al. 2021), which will be useful in evaluating the proposal:
New information: Jeremy Kenneth Dickens and colleagues examined 906 specimens at 17 different museums, including all taxa and all available type specimens, and gathered spectrophotometric data, patterning, bare parts coloration, and standard morphometric data on subsets of these specimens. They quantified vocal characters from 273 songs from throughout the distribution and including all named taxa. They also analyzed genetic samples (ND2 and Cyt-b) from 29 specimens from throughout the distribution and all taxa. In other words, Dickens, Britton, Bravo, and Silveira conducted an amazing study in terms of sample size, geographic coverage, and critical data. Although the genetic sampling included only mtDNA, I don’t think data from additional genes would have made a difference in terms of determining species limits. The analyses are really excellent, and I encourage everyone to check out the great graphics (my favorite is Fig. 3a on male uppertail covert hue, although the color illustrations by Eduardo Brettas of the taxa and their critical features is tough to beat). If only we had papers of this quality and depth, from sophisticated analyses to classical taxonomy. The only weakness, given the vocal differences, is the absence of playback trials, although to do that properly would require fieldwork in multiple regions in the Neotropics.
A detailed synopsis of all these data would take up a lot of space here. Check out the details for yourselves, but here’s what stands out to me: the voices of all their proposed species are qualitatively and quantitatively different; in contrast, no such major differences are found among the Amazonian taxa that they recommend be treated as subspecies of T. rufus sensu stricto. For three of their proposed species-level taxa, 100% of the recordings were correctly classified to species using linear discriminant analysis for three of their proposed species-level taxa (chrysochloros, cupreicauda, tenellus).
As for the genetic data (ND2 1041 bp, cytb1011 bp), the results show prefect congruence between geographic samples and relationships, and genetic distances within geographic clusters and within taxa are small. The cis-Andean taxa are all weakly differentiated, with time calibrations suggesting divergence times among species at ca. 3-4 million years. The big break is between cis-Andean and trans-Andean taxa, with a divergence time estimated at ca. 5 million years ago. The single sample of cupreicauda is fairly divergent from the 9 samples of tenellus.
(There are lots of little nuggets within this 42 page paper that I could itemize, but I will stop at just one because it has direct relevance to species limits. Atlantic forest chrysochloros is almost exclusively insectivorous, in contrast to the other omnivorous taxa, and it has a more heavily serrated bill for grasping large arthropods; they are also known to be regular followers of monkeys, army ants, and coatis, evidently more so than other trogons, so this all fits. Actually, I can’t resist adding a second one because as the authors note, it is important to keep in mind when assessing plumage in trogons: they found evidence that there may be an environmental influence on iridescence, which changes with elevation in chrysochloros.)
A summary of their recommended species classification is as follows. See the paper for detailed diagnosis of each, including coloration, pattern, eyering color, and song features. These sections also contain detailed descriptions of each taxon, detailed synonymies, and useful notes on type specimens
• Trogon tenellus Cabanis, 1862: Central America to extreme NW Colombia (dpto. Chocó)
• Trogon cupreicauda (Chapman, 1914: N Colombia south on Pacific slope to NW Ecuador
• Trogon rufus Gmelin, 1788 (including nominate rufus of Guianan Shield, T. r. sulphureus of western Amazonia, and T. r. amazonicus of eastern Amazonia)
• Trogon muriciensis sp. nov.: Alagoas Forest region; known only from type locality at Estação Ecologica de Murici.
• Trogon chrysochloros Pelzeln, 1856: Atlantic Forest region
Here is a screen shot of the outstanding color plate by Eduardo Brettas that illustrates the taxa:
The quality of evidence for species rank varies among the 4 newly recognized or new species, so I think we should subdivide the proposal as follows below. I suggest listening to the recordings of the various taxa on xeno-canto: https://www.xeno-canto.org/explore?query=trogon+rufus&pg=1
A. Treat tenellus as a separate species from T. rufus
Because tenellus is entirely trans-Andean, it is not parapatric with any subspecies of T. rufus, and thus the decision on taxon rank must rely on comparative methods. The vocal differences from other taxa are given as follows:
“Song: Diagnosed from neighbouring T. cupreicauda by fewer notes per phrase, longer note durations and generally higher note frequencies, particularly the introductory note high frequency. Note frequencies, particularly the introductory note high frequency, are higher than for T. rufus subspecies. Fewer notes per phrase, slower pace and longer durations of notes and pause following introductory note than T. chrysochloros.”
In terms of phenotype, It has a breast band, unlike T. r. sulphureus or T. r. amazonicus, from which it differs in several other less conspicuous details (p. 26, and see the color plate (Fig. 6, p. 14, and above). The Diagnosis states that its pale (blue-gray to white) eyering that distinguishes is from everything else, including parapatric cupreicauda, but chrysochloros also is listed as having the same color eyering.
B. Treat cupreicauda as a separate species from. T. tenellus
This is the other trans-Andean taxon, and it is sister to tenellus as one would predict on biogeographic grounds. If someone does not endorse tenellus as separate from the rufus group, then also endorsing cupreicauda as a separate species from either of those would be unlikely and would require special explanations. The vocal differences from other taxa are given as follows:
“Song: Compared to T. tenellus, the song has more notes per phrase, shorter note durations and generally lower note frequencies. It also has more notes per phrase, shorter note durations but a longer pause after introductory note, and generally higher note frequencies, especially for the introductory note, than in T. rufus subspecies. Compared to T. chrysochloros, the song has a slower pace, longer pause following the introductory note, generally longer note durations and generally lower note frequencies.”
In their Factor Analysis (Fig. 4A), cupreicauda shows no overlap with the other taxa on the axis heavily weighted by pace (slow) and note length (short).
In terms of phenotype, the most striking feature to me is that the tail color is closer to distant chrysochloros than to any other taxon, and in fact, it differs the most in this feature from parapatric tenellus. The yellow eyering distinguishes it from all other taxa. See p. 28 for a listing and discussion of other color differences.
C. Recognize T. muriciensis as a species.
As rightfully emphasized by Dickens et al., little comparative material was available:
“Diagnosis: We had little material available for the diagnosis of the new species Trogon muriciensis, particularly regarding external morphology, so caution must be taken until more information is collected. For comparison of plumage coloration and barred patterning, only the holotype was available. For morphometric traits, in addition to the holotype, we had measurements from the paratype and a ringed individual. For other discrete traits, we had photos from online depositories, in addition to those of the holotype (Supporting Information, Fig. S8) and ringed individual. For the song, we had slightly more material, with recordings from five separate individuals (including the holotype).”
The vocal differences from other taxa are given as follows:
“Song: Compared to T. chrysochloros, the song of T. muriciensis has fewer notes per phrase, slower pace, longer note durations, longer pause following introductory note and generally lower note frequencies. It is similar to T. r. rufus but with generally more notes per phrase, higher introductory note frequencies and higher loudsong note low frequencies. Compared to T. r. sulphureus, it has wider bandwidth frequencies and generally more notes per phrase, whilst against T. r. amazonicus, it has faster pace, shorter note durations and a higher frequency introductory note. In relation to T. tenellus, it has a greater number of notes per phrase, shorter pause after the introductory note a generally lower introductory note high frequency, and generally lower peak and high loudsong note frequencies. It differs from T. cupreicauda by having fewer notes per phrase, longer note durations but a shorter pause after the introductory note. The bandwidth frequencies of the introductory and loudsong notes are generally wider than all other taxa, except T. chrysochloros.”
In terms of phenotype (with their caveats concerning N), there is no single diagnostic character than I can see, but rather a combination of differences not shared with any other taxon. See p. 30 for an enumeration of the ways it differs from adjacent chrysochloros and members of the nominate group. Genetically (Fig. 5), the single sample is sister to all 9 samples of chrysochloros; however, all nine are distant, i.e. from São Paulo south (no samples from closer Bahia to RJ), so that result would be expected on the basis of isolation by distance alone.
D. Treat chrysochloros as a separate species from T. rufus
The vocal differences from other taxa are given as follows:
“Song: More notes per phrase, faster pace, shorter note durations and pause following introductory note, as well as higher note frequencies and wider introductory note bandwidth than T. rufus subspecies. The greater number of notes per phrase, faster pace and shorter durations are also diagnostic against T. tenellus. Compared to T. cupreicauda, the pace is faster, the pause duration shorter and frequencies usually higher.”
In their Factor Analyses (Fig. 4A, B [beware that B is mis-labeled as Trans-Andean]), chrysochloros shows no overlap with the other taxa on the axes heavily weighted by pace, pauses between notes, and number of notes.
As for phenotype, this taxon has a relatively smaller bill that is more highly serrated than any other taxon. The density of barring on the wing panel and undertail coverts is diagnosably higher than for any other taxon. The Diagnosis says that it can be diagnosed from all other taxa (except evidently muriciensis) by its blue-gray to white eyering, but I think this is an error – see tenellus. See p. 25 and the plates for additional differences.
There is no doubt that all taxa are diagnosable at some phenotypic level. But at what rank? Dickens et al. noted introgression at the phenotypic level between T. r. rufus and T. r. amazonicus, T. r. amazonicus and T. r. sulphureus, and T. r. rufus and T. r. sulphureus; thus, they treated them as subspecies of the same species, which is the logical treatment. Contact zones are valuable test cases. Those three contact zones provide a defensible standard for seeing which phenotypic characters matter and which ones don’t in terms of barriers to gene flow. In the vocal analyses, these three taxa mostly overlap in every feature analyzed, so song, as we have known empirically for 70+ years, matters. The characters that do not seem to matter in terms of barriers to gene flow, at least in this group of trogons, are tail color (which varies dramatically among the three), presence of subterminal tail band, presence of breast band (no surprise here, because there is intraspecific variation in this in other trogons), width of undertail barring, eye-ring color (ranges from blue to yellow even within amazonicus) and any mensural characters. In other words, almost every plumage and morphological characters they measured is irrelevant as a barrier to gene flow, and so an important message of this paper is that all these characters may be irrelevant when considering species limits in trogons. (And I wish they had measured the implications of this for the highly flawed Tobias-BLI 7 point scoring scheme in terms of taxon ranking, but this would have added a tangent that would likely have increased the paper length by a page.)
The only other known contact zone is the one between tenellus and cupreicauda at the Panama-Colombia border, where there are no documented cases of introgression. Therefore, with the usual caveats, I think we can take the differences between tenellus and cupreicauda as potential isolating mechanisms, at least if they differ from those between taxa in the T. rufus group. These “if/then” comparative extrapolations come with obvious solutions, but in the absence of alternatives, at least provide defensible rationale for extrapolation to allopatric taxa in terms of assessing potential barriers to gene flow, for better or worse. However, none of the phenotypic characters other than voice show any difference from those shown by Dickens et al. to not be potential isolating mechanisms in the T. rufus group.
That leaves vocalizations as the best proxy for estimating gene flow or lack of it.
I personally am not the person to assess what the vocal differences mean in a trogon framework -- -way too rusty. Are the reported differences comparable to species level differences in other trogon groups? I will leave that up to those of you who have extensive recent comparative experience with trogon voices. To me, when I listen to the recordings, all I hear are the features in common, which to me are considerable; but then again, many for-sure trogon species sound moderately similar. Is the absence of playback trials crippling given what I perceive as subtle differences? Ridgely & Greenfield (ergo also Mark Robbins) in the taxonomy volume of Birds of Ecuador were consistently alert to vocal differences between bird taxa west and east of the Andes in that country; however, they considered the differences between voices cupreicauda and sulphureus to be only “slight”, which is slightly worrisome to me. So, I look forward to your comments.
A. Treat tenellus as a separate species from T. rufus. I hesitate to make a recommendation on this one other than noting my subjective feeling that I trust the authors of this paper on this one because of the depth to which they have gone in these analyses. Certainly, tenellus occupies a nearly unique multivariate space in the Factor Analysis of plumage characters in both sexes (Fig. 2), more distinctive than any other taxon other than chrysochloros. However, in terms of vocal characters, tenellus overlaps nearly completely with the T. rufus group despite differing in average ways from them.
B. Treat cupreicauda as a separate species from. T. tenellus. Because there is no phenotypic evidence of gene flow between presumably parapatric cupreicauda and tenellus, I regard this alone as a sufficient criterion for species rank between those two. See the Discussion on p. 32 --- the authors were keenly aware of the significance of this. With cupreicauda vocalizations not overlapping with those of the other taxa in multivariate space, we have additional indirect evidence for species rank. I’m also impressed with the phenotypic differences between cupreicauda and tenellus, which are arguably greater than between any two adjacent taxa. The genetic distance between the two appears at least as larger as that between any two adjacent taxa in the tree; however, there were no genetic samples from Colombia, much less NW Colombia, closer to the contact zone than the sample of cupreicauda from Provincia Esmeraldas, and perhaps sampling within that ca. 700 km gap might produce a different result.
C. Recognize T. muriciensis as a species. With a tiny N and no truly diagnostic characters known, this one unfortunately represents the weakest case for species rank, as the authors noted.
D. Treat chrysochloros as a separate species from T. rufus. With its distinctive plumage characters and vocalizations, the evidence for this split is strong in my opinion.
A. Treat tenellus as a separate species from T. rufus. I’m ambivalent on this one, which is awkward, because the evidence is nearly mandatory for treating its sister taxon cupreicauda as a separate species, which would make Trogon rufus a paraphyletic taxon if tenellus were included in T. rufus but not cupreicauda. On the other hand, at the population-species level I don’t think monophyly, especially when only two labile mtDNA loci were sampled, is a valid requirement for species rank (as I have argued several times previously). With every passing month, it seems that new data reveal ancient hybridization among species that would make perilous the use of any single gene tree as representing the “true” history.
B. Treat cupreicauda as a separate species from T. tenellus. YES. I think these have to be treated as separate species given the parapatry with no sign of introgression.
C. Recognize T. muriciensis as a species. Ambivalent. The endangered status of this one should not, in my opinion, influence the taxonomic decision; otherwise, this undermines the credibility of the scientific process. Certainly this should be recognized as a separate subspecies, minimally, and I look forward to others’ comments on this.
D. Treat chrysochloros as a separate species from T. rufus. YES on this one for reasons given above.
E. English names: Dickens et al. proposed the following:
• Trogon tenellus = Graceful Black-throated Trogon
• Trogon cupreicauda = Kerr’s Black-throated Trogon
• Trogon rufus = Amazonian Black-throated Trogon
• Trogon muriciensis = Alagoas Black-throated Trogon
• Trogon chrysochloros = Southern Black-throated Trogon
• Trogon chrysoc
A lot of you don’t like long compound names. In fact, Tom’s blood pressure just skyrocketed when he read this. I understand that view, but in this case I like the compound names because: (1) it keeps intact the link to Black-throated Trogon, thus making it clear within a long list of trogon names which species are members of the T. rufus superspecies; (2) maintaining Black-throated in the name retains a somewhat useful character in separating them from other trogons within their range (I think); (3) they are marginally distinguishable anyway by plumage; and (4) if one drops the “Black-throated”, then we would probably have to invent new names for two of the species because “Southern Trogon” and “Amazonian Trogon” are misleading names from the perspective of the genus as a whole. Southern Black-throated Trogon, as noted by Dickens et al., resurrects a historical name, thus providing continuity with older literature.
Also, “Graceful” is somewhat unsatisfactory for tenellus (Latin for “delicate”, fide Jobling), with or without Black-throated, although as noted by Dickens et al., it resurrects the historical name used in Middle American bird literature from at least Ridgway (1911) on, until Eisenmann (1955) changed it to Black-throated after its lump (Peters 1945) into T. rufus. And “Kerr’s” is an eponym, which will anger the anti-eponymous zealots; however, Kerr was a female collector, which was highly unusual for the era (1912!), an American living in Colombia and collecting birds, and she collected the type specimen. In my opinion, not only deserves the honor but also calls attention to her generally overlooked contributions. See the attached provided through Gustavo Bravo, admirably dug out by Andrés Cuervo. (You may have lost your chance to buy Ingram’s Milkweed Cream, unfortunately).
At this point, for English names, let’s keep it simple: A YES means acceptance of the proposed names, as per above for any species that we recognize, and a NO means something else, either no compound names or modifications of the modifiers or both.
DICKENS, J. K., P.-P. BRITTON, G. A. BRAVO, AND L. F. SILVEIRA. 2021. Species limits, patterns of secondary contact and a new species in the Trogon rufus complex (Aves: Trogonidae). Zoological Journal Linnean Society: 1–42.
Van Remsen, September 2021
Comments from Areta:
“A. YES. Plumage and genetics support this split. See comments on C regarding vocalizations.
“B. YES. Mostly based on the apparently distinctive vocalizations (despite methodological shortcomings), marked change in tail hue over a short distance near the zone of geographic proximity between them and less so based on the phylogenetic information (the single sample of cupreicauda is quite away from the southern limit of tenellus).
“C. NO to recognizing muriciensis as a separate species. The data is very limited and unsatisfactory to make this move. The shallow genetic divergence, lack of diagnostic plumage features, and similar vocalizations to chrysochloros indicate to me, at most, subspecific status. Regarding the vocalizations, I have trouble in seeing the most basic parameters of the spectrograms in Figure 4 (e.g., time and frequency values), but these seem to have been built using different scales, thereby presumably distorting the similarities and differences among vocalizations. It also seems to me that there are important vocal differences among sexes in Trogons (fleetingly disregarded by the authors) that were not taken into account when making the comparisons; this can easily be heard and seen in spectrograms when couples of birds duet or respond to each other. I have trouble in matching the presumably "typical" songs depicted in the spectrograms to results of the discriminant analyses: songs which look very different overlap widely, suggesting that measurements were not able to capture key features of the sounds or that the spectrograms are not so typical. Finally, several recordings of chrysochloros sound exactly like muriciensis.
“D. YES to splitting chrysochloros from rufus. Plumage, vocal and genetic data agree in this split.”
Comments from Donsker: “E. My formal vote is NO. I think that we can come up with better English names than those proposed.”
Comments from Bonaccorso:
“A. YES, but it makes more sense to accept 921B.
“B. YES. T. tenellus and T. cupreicauda seem to have reached enough phenotypic differentiation (especially tail color; I love the tail-hue figure!) and vocal differences. However, I am not impressed by their genetic differences because the range of the species along Colombia was not covered in the phylogenetic analysis, thus, differences could result from isolation by distance. However, the possibility of parapatry and lack of intermediate individuals supports the potential lack of gene flow.
“C. “YES, but a bit hesitantly (I agree with Nacho that the data are sparse). Phenotypically, the Alagoas population is not so different from chrysochloros. However, vocally (and I am no expert), it seems to be very different. Still, the low sample size (N = 5) may not reveal the variation spectrum of vocalizations in the Alagoas population. Genetic differentiation is weak and based on one sample, whereas genetic sampling of chrysochloros does not cover localities closest to the Alagoas population. In short, I think the decision should be based on the acoustic data if some of you (experts on the subject) think the level of differentiation merits species status.
“I disagree with the position that no special considerations need to be made when the decision is about endangered species. I think there has to be asymmetry when considering species that may or may not be endangered. If, in the end, they are no good species, some money and effort may be lost, but at least the habitat of the species may get some level of protection for a while (which, needless to say, will benefit many other species). It is much worse to err in the other way. Not recognizing an endangered species and waiting for more data may have much worse consequences, especially in cases like this, where the range seems tiny. Also, from my experience with the Blue-throated Hillstar, the fact that we recognize new, endangered species does not guarantee immediate incorporation into IUCN lists (even after repeated requests to BirdLife International). Meanwhile, deforestation continues, and funds are not available for research, research-based conservation, or protection. So, our delay in recognizing these species may have fatal consequences under the current circumstances.”
“D. YES. In this case, vocal and genetic evidence seems to support species status. I don´t think phenotypic differentiation is so strong or useful in defining species status in this case. T. sulphureus seems very different from rufus and still, they hybridize.”
Comments from Pacheco: “A, B and D. YES. Plumage, genetics, and vocal repertoire provide a good endorsement for treating these taxa at the species rank.
“C. A vacillating YES, for the exact reasons explained by Elisa. Obtaining more data (vocalizations, genetics) and conservation measures for this population becomes dramatic races against the clock.”