Proposal (1009) to South American Classification Committee

 

 

Treat Amazona autumnalis (Red-lored Parrot) as consisting of three species

 

 

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

 

Background:  Our current Note reads as follows:

 

34c. The Ecuadorian subspecies lilacina and the Brazilian subspecies diadema were formerly (e.g., Cory 1918, Pinto 1937) considered separate species from Amazona autumnalis, but Peters (1937) treated them as conspecific. Ridgely & Greenfield (2001) treated diadema as a separate species but did not provide justification.  Del Hoyo & Collar (2014) treated both lilacina (“Lilacine Amazon”) and diadema (“Diademed Amazon”) as separate species based on differences in plumage and bare parts coloration, and this was further supported by qualitative inspection of specimens by Donegan et al. (2016).  Smith et al. (2023) found a deep genetic divergence between autumnalis s.s. and diadema.  SACC proposal needed.

 

The status quo, maintained in most classifications (e.g. Dickinson & Remsen 2013), is that this species consists of 4 subspecies:

 

1. A. a. autumnalis from Mexico to N. Nicaragua

2. A. a. salvini from Nicaragua to the Chocó of sw. Colombia and also to n. Venezuela.

3. A. l. lilacina: endemic to the Chocó of w. Ecuador

4. A. a. diadema: disjunctly in central Amazonian Brazil along the Amazon and lower Rio Negro.

 

Here is the composite distribution map from Forshaw (2006:”Parrots of the World”):

 

 

Here is the plate by Frank Night from Forshaw (2006:”Parrots of the World”):

 

 

 

A. l. salvini apparently has a zone of intergradation with A. a. autumnalis.

 

Here’s the plate in del Hoyo & Collar (2014) by Ångels Julglar:

 

 

Here are three photos from Macaulay, L to R, nominate autumnalis pair (by John Doty), lilacina (by Edison Buenaño), diadema (by Héctor Bottai):

 

 

New information:  Del Hoyo & Collar (2014) treated lilacina and diadema as species separate from autumnalis.  Here is the HBW rationale (provided by Pam Rasmussen):

 

For diadema:

 

“Usually considered conspecific with A. autumnalis and A. lilacina, but differs from lilacina in certain characters outlined under that species, and from both in its nares being covered in red feathers, with rest of red patch on face sharply delineated to form a distinct rectangle, quite different from shape of red patches on other taxa in complex, and allowing blue on crown to extend forward to border the frons (3); powdery dorsum, resembling more that of A. farinosa (1); bill black but with pale patch below nares (2); head much flatter and longer in lateral profile (mensural score 1). Monotypic.”

 

For lilacina:

 

“Usually considered conspecific with A. autumnalis and A. diadema, but differs in its all-black upper mandible (2); red of forecrown continuing over eye (2); lilac of crown not extending onto nape (2); paler, clearer green cheek (ns[1]); possibly no red on chin (ns[1]); narrow, sharp yellow edges of wing-coverts and flight-feathers (ns[1]); retiring, non-aggressive behaviour (quite different at least from autumnalis (1) ) (ns[1]); smaller bill (tiny museum sample size supplemented by photographs; 1). Specific status considered appropriate also in unpublished recent taxonomic study (2). Monotypic.”

 

Donegan et al. (2016) evaluated the del Hoyo & Collar taxonomy with respect to how this affected the Colombian bird list.  They also provided photos of 5 specimens from AMNH.  Here is what they wrote:

 

“We concur that A. lilacina is a quite different bird from both diadema and autumnalis (Fig. 15). It has virtually no blue on the crown but extensive yellowish-green plumage on the face and throat, carpal edgings and vent and a dark bill.

 

“The split of diadema from autumnalis is less clear-cut. The more extensive blue scaling on the mantle of diadema is a noteworthy feature (Fig. 15), but the head patterning and overall coloration is more similar to autumnalis. The difference in nare feathering can be seen in online photographs of live birds but was not obvious in specimens we inspected. Differences in the shape of the red patch on the lores are less impressive when one considers variation in this feature both within autumnalis and between the nominate subspecies and salvini. It is not necessary for us to express any view on the rank of diadema, as it is extralimital as regards Colombia.”

 

Smith et al. (2023) did not sample lilacina, but they had diadema in their tree.  It comes out as sister to autumnalis in their analyses, but the divergence is deeper than that among many taxa ranked as species in Amazona.  In S27, my eyeball extrapolation down to the X-axis suggests the node that joins autumnalis and diadema is ca. 3 MYA.

 

 

 

 

 

 

Voting:  Let’s do it this way:

 

YES = Treat lilacina and diadema as separate species from A. autumnalis.

NO = maintain status quo OR treat either lilacina or diadema as a separate species but not both.

 

Discussion and recommendation: I’m not going to vote until I see what others say, but I’m leaning towards a YES for the following reasons.  First, that deep genetic split is impressive.  I don’t support using genetic distance of neutral loci as a metric for assigning species rank, but this looks like an extreme case, with diadema more divergent from autumnalis than are many sister taxa treated as species in Amazona.  As for lilacina, available evidence suggest an abrupt change from A. a. salvini in Colombia to lilacina in Ecuador, or perhaps this should be phrased to indicate that there is currently no evidence for gene flow in these parapatric taxa.  If that is really the case, then species rank is required.  Finally, Peters provided no rationale for the lump, nor has anyone subsequently.

         However, here’s what makes me wonder.  The large distance between diadema and the closest autumnalis populations suggests a long period of isolation, unlike many sister parrot species, so perhaps that genetic distance is just the long accumulation of “irrelevant” neutral mutations.  The absence of genetic samples of lilacina is unfortunate – that’s a case in which genetic data really would illuminate species limits because of the apparent parapatry: other than some governmental border posts, there is no substantial barrier to gene flow between the two.  As noted by Donegan et al. (2016) an argument can be made that diadema looks more like autumnalis than lilacina does.  Also, what is really known about the potential contact zone between autumnalis and lilacina?  There do not seem to be many specimens of lilacina in collections, but it looks to me as if careful photographic sampling of individuals might hold promise for at least a preliminary assessment of the contact zone using bill color and head pattern.

         As for plumage …. I’m still trying to reconcile why the specimens shown in Donegan et al. show what I would consider “important” differences, as reflected in del Hoyo & Collar’s description, in contrast to my impressions from the photos of living birds, the signal from which I perceive is dominated by similarities, as in the two plates.  Also note the differences between the two individual autumnalis in the photos – this is almost certainly a mated pair.  How much individual variation is there?  So, I don’t know what to make of the differences in head plumage.  All this makes me want to demand an actual formal analysis of plumage characters, with specimen N and locality data reported, before taking the plumage into account.  Evaluating N=1 samples of specimen photos, live bird photos, and artists plates is not the way science should be conducted.  Finally, as for Peters, those of us who use the Cory-Hellmayr series know that Cory’s early, single-authored volumes (1918, 1919) made few changes in taxon rank from the original ODs unless Ridgway or someone else had already done it; not until Hellmayr joined the project was more critical thinking applied to lumps and splits.

         And then there is the absence of vocal data.  This is tough to analyze in parrots for obvious reasons, but at the least flight calls seem to be fairly stereotyped and a good marker for species differences in sympatric congeners.

 

English names:  If the proposal passes, then I see no need for a separate proposal on English names given that Lilacine and Diademed have been used extensively (Diademed even goes back to Cory 1918).  If anyone objects, please speak out.

 

References:

 

DONEGAN, T., J. C. VERHELST, T. ELLERY, O. CORTES-HERRERA, AND P. SALAMAN.  2016.  Revision of the status of bird species occurring or reported in Colombia 2016 and assessment of BirdLife International's new parrot taxonomy.  Conservación Colombiana 24: 12–36.

SMITH, B. T., J. MERWIN, K. L. PROVOST, G. THOM, R. T. BRUMFIELD, M. FERREIRA, W. M. MAUCK III, R. G. MOYLE, T. F. WRIGHT, AND L. JOSEPH.  2023.  Phylogenomic analysis of the parrots of the world distinguishes artifactual from biological sources of gene tree discordance.  Systematic Biology 72: 228-241.

 

 

Van Remsen, June 2024

 

 

 

Comments from Robbins: “NO. Because of the lack of genetic data for lilacina coupled with what Van points out as potential variation in head pattern (plumage, soft part coloration), for now I vote NO until some of these issues are addressed.”

 

Comments from Jaramillo: “YES – I tis a patchwork of information here, that I am using. First large divergence time with diadema based on molecular data. Then lilacina is quite different in appearance and appears to be essentially parapatric with autumnalis. That is interesting. I tis piecemeal, and patchwork but I think the three species theory will be what will prevail over time, as more data is gathered.”

 

Comments from Areta: “I vote NO to the split of lilacina. I am unimpressed by the differences between the different populations in terms of genetic and plumage, which seem on par with those between several populations of other Amazona taxa. For example, I myself have studied and published on the sierran populations of Amazona aestiva, which lack any red or yellow in the "shoulder", no yellow on the face, and a different green colour despite the close proximity to typical xanthopteryx populations (Areta 2007).

 

“Terry Chesser suggested that the deep branch between lilacina and autumnalis in Smith et al. might be due to missing data (as these taxa are in the upper 10% of missing data taxa).

 

“In a PhD thesis (Pilgrim 2010, courtesy Paul F. Donald) the genetic data (883bp of ND2) tells a different story:

 

"Table 4.2. The average p-distances between the subspecies

 

 

1

2

3

4

5

6

1

A. a. lilacina.

 

 

 

 

 

 

2

A. a. salvini

0.012

 

 

 

 

 

3

A.a.autumnalis

0.023

0.026

 

 

 

 

4

A.a. diadema

0.011

0.000

0.025

 

 

 

5

A. viridigenalis

0.053

0.026

0.057

0.057

 

 

6

A.leucocephala

0.177

0.171

0.152

0.169

0.197

 

7

Pionus maximiliani

0.369

0.381

0.341

0.376

0.336

0.353

 

Table 4.2. Estimates of Average Evolutionary Divergence over Sequence Pairs between Groups.
The number of base substitutions per site from averaging overall sequence pairs between groups is shown. All results are based on the pairwise analysis of 22 sequences. Analyses were conducted using the Kimura 2-parameter method in MEGA 4. The rate variation among sites was modelled with a gamma distribution (shape parameter = 0.0994). Codon positions included were 1st + 2nd + 3rd + Non coding. All positions containing gaps and missing data were eliminated from the dataset (Complete deletion option). There were a total of 883 positions in the final dataset.

 

“The divergence of A. a. lilacina from A. a. salvini is 1.2% and divergence of A. a. lilacina from A. a. autumnalis is 2.3%.  A. a. diadema shows no divergence from A. a. salvini. The A. a. autumnalis group shows a divergence from A. viridigenalis of between 2.6 to 5.7% and a divergence from A. leucocephala from Cuba of between 15.2 to 19.7%."

 

“And using the same molecular ND2 dataset, Pilgrim obtained the following MP consensus tree:

 

 

“Pilgrim also reports on the smaller bill of lilacina, and mentions lack of sexual dimorphism in lilacina (as a difference between the size-dimorphism in other autumnalis taxa, and Amazona in general).

 

“A paragraph on geographic variation in plumage is worth quoting in full:

 

"The A. autumnalis specimens from the Natural History Museum at Tring are arranged taxonomically and by country of origin. While examining these to examine putative differences in area of plumage color between the subspecies, it was noted that the amount of yellow on the cheeks of A. a. autumnalis, the feature which gives this parrot its common name of Yellow–cheeked Amazon, gradually decreases in size from the northern Mexican specimens with a very large bright yellow cheek patch, to specimens which have a very small patch of yellow feathers on the cheeks in the south of its range. A. a. salvini has no yellow in the cheeks. It was not possible to assign some specimens that had merely a single fleck of yellow on the cheeks to either A. a. salvini or A. a. autumnalis. These intermediate specimens originate from Honduras and Nicaragua, an area between the ranges of A. a. autumnalis and A. a. salvini (Fig. 1.00), and may be subspecific hybrids as reported by Howell (1957). No such intermediate forms between A. a. lilacina and A. a. salvini have been observed either in the museum specimens or amongst the dozens of wild captured living specimens observed during my role as European studbook keeper for A. a. lilacina. This suggests an absence of a hybrid zone between A. a. lilacina and A. a. salvini. However, a survey of the area where the ranges of these subspecies meet on the border of Ecuador and Colombia would be required to ascertain this with any certainty. As mentioned in the introduction Olivares (1957) suggests the possibility of hybridisation but presents no evidence for it. There are no other or more recent reports of a hybrid zone between A. a. lilacina and A. a. salvini in the literature. A. a. diadema has an allopatric range."

 

“Areta, J.I. 2007. A green-shouldered variant of the Turquoise-fronted Amazon Amazona aestiva from the Sierra de Santa Bárbara, north-west Argentina. Cotinga 27: 71-73

Pilgrim, M.A., 2010, An investigation into the taxonomic status of Amazona autumnalis lilacina using a multidisciplinary approach. PhD thesis, Liverpool John Moores University, Liverpool, UK.”

 

Comments from Stiles: “NO. The data are just too patchy and inconsistent, and it would seem that more intrapopulation variation in plumage might exist as well; clearly more thorough, quantitative data on plumage and genetics are needed.”

 

Comments from Lane: “NO. This is a project or two that might benefit greatly from directed investigation into the relationships of these three groups of taxa. I suspect both lilacina and diadema will prove to be species-level with respect to the autumnalis group, but for now we have missing information.”

 

Comments from Claramunt: “YES. Going on a limb in this case and I agree that it would be better to have more detailed analyses but at least lilacina looks like a well-delineated taxon. I don’t see any signs of intergradation in photos from W Ecuador. The case of diadema is harder because the bird is remotely allopatric and the diagnostic traits may be just too subtle, but I think it is correct that the exact shape of the loral/frontal patch is diagnostic, ending in an abrupt transition to a pure green supercilium in diadema rather than a diffusing over the eye like in autumnalis. That, plus the considerable genetic divergence convinced me that we need to revert the unexplained lumping made by Peters et al.”

 

Comments from Zimmer: “YES.  I will admit up front to not having any experience with lilacina, so the lack of any genetic data for the latter taxon is vexing, because it doesn’t leave me a lot to go on.  I will say, as others have suggested, that the variation in the amount of yellow in the face doesn’t impress me either – other Amazona species (amazonica and, especially, aestiva come quickly to mind) exhibit tremendous individual variation in the amount and distribution of yellow on the head and face, even within the same population, and I suspect at least some of this variation is attributable to age.  However, I am struck by the fact that, as Van states, lilacina and salvini have seemingly parapatric distributions with respect to one another, with no obvious geographic barrier separating them, and yet, there’s no obvious intergradation, and the respective phenotypes seem to be maintained.  That, combined with the fact that this is yet another case of a pair of taxa that were described as distinct species, and then lumped without rationale provided by Peters, are enough to tilt me in favor of treating them as distinct species.  As for diadema, I feel on firmer ground in voting for a split on this one.  We do have indication of a deep genetic split on this one, and even though Van’s caveat regarding the possibility of long isolation just reflecting the accumulation of irrelevant neutral mutations is well taken, I’ve always felt that diadema was a different beast.  I had a lot of experience with autumnalis in Mexico, Panama, and Costa Rica before I first encountered diadema on my first visit to Manaus, and I remember being struck by how different it looked (particularly the farinosa-like abundant powder-down on the dorsum and different distribution of red and blue on the head, not to mention the absence of yellow in the face) and sounded.  To me, the flight calls of diadema and autumnalis are pretty different.  I haven’t heard the songs of either taxon much in recent years, so I’m a little rusty on those, but the flight calls are what you hear mostly, and my impression of those has always been that they are distinct.  So to me, if you’ve got two taxa that differ in some aspects of plumage, differ in at least some vocal characters, and have a deep genetic split relative to other recognized species-pairs in the same genus, and are clearly on independent evolutionary trajectories given their extremely allopatric distributions, it doesn’t really matter whether the depth of the genetic split is largely due to accumulation of irrelevant neutral mutations or not – they already look and sound consistently different, and they aren’t going to be sharing genetic material anytime in the foreseeable future (= ever), so why not revert to the pre-Peters treatment as distinct species?”

 

Comments from Del-Rio: “NO: Given the limited genetic data available on lilacina, I believe that future research could potentially reveal that these are all distinct taxa. However, for the time being, I will adopt a conservative approach. Again, an interesting system to track different patterns of accumulation of psittacofulvin in Psittacidae populations living in different environments.”

 

Additional comments from Stiles: “Given Kevin´s comments and reconsidering the information in the BMNH paragraph as well as other data mentioned by Pilgrim in particular, I am willing to change my vote to a YES for recognizing lilacina and diadema as separate species from autumnalis. The case for diadema seems especially clear for species status given the deep genetic difference, the morphological and apparent vocal differences and its widely divergent distribution. The case for species status of lilacina is somewhat less clear, but given the differences in plumage and bill colors. overall size and lack of sexual size dimorphism and the lack of any intermediate specimens (of many examined) I think that this tips the balance toward at least tentatively considering species status (especially because Peters did not give any real evidence for lumping them, The lack of specimens (or observations) in the potential contact zone could be interpreted simply as missing evidence, but on the other hand, it could indicate that there IS no contact, with lilacina thus considered as a peripheral isolate from autumnalis which as such  evolved a suite of phenotypic differences (often the case in such situations).”

 

Comments from Remsen: “YES.  After letting this incubate for months.  First, Kevin’s comments are persuasive, even though the data on flight calls are not published.  As for the genetic data, I don’t think we can rely on the unpublished Pilgrim data, which claim that autumnalis and diadema are identical at those loci.  Given the vast geographic distance between the two and the plumage differences, I think something must be amiss with those data, or at least they should be repeated.  The data of Smith et al. ARE published,  and although the branch length might be exaggerated by missing data, they are not identical.  As for lilacina, yes the contact zone if there is one is not sampled but I think the absence of any signal of gene flow with the data at hand puts burden-of-proof on treating them as conspecific.  This is a tough call and a data-deficient case, for sure, but with considerable trepidation, I think what we have available suggests separate species.”

 

Comments from Mario Cohn-Haft (voting for Bonaccorso): “YES. Full disclosure: I know only diadema in the field. that makes my personal experience with the complex pretty well useless. However, when has that kept me from offering an opinion? All my instincts say that diadema must be a distinct species from the rest: it's very distantly isolated geographically in the central Amazon from all the others, which are trans-Andean and more or less continuous in distribution; it has no yellow on the face but often does have yellow on the crown, both of which seem intuitively like important differences; also has what strikes me as a wider, more conspicuous bare eyering than the others, more and different blue on the crown; and finally it has an unusual and mysterious life-history, apparently involving an intra-Amazonian migration, such that I'm not sure we even know where it breeds!  See below for a few pictures of diadema from Manaus.  So, if there were no genetic data, I'd vote for recognizing diadema as a full species and would more or less instinctively visualize the other 3 as geographic variants of a single species, considering their seemingly continuous distribution.  However, the fact that experienced folks (and the pictures) suggest that lilacina too is different might convince me to vote "yes" overall. 

 

“However, there ARE genetic data.  The study showing diadema to be strongly different from autumnalis jibes with the plumage and biogeographic arguments laid out above and is intuitively satisfying. The Pilgrim study that includes lilacina and finds all 4 taxa to be between 1-2.5% different from one another, except diadema which is genetically identical to salvini, makes no sense at all, and I'm inclined to follow Van's lead and just assume it's wrong.  Not a very satisfying conclusion, i recognize, but seemingly advisable given the rest of the evidence.

 

“I was about to wimp out and vote "no" because of the incomplete and conflicting genetic data and in recognition that i don't feel like i can say anything first-hand about lilacina.  But then i reread the intro to the proposal and remembered that the only reason we're even talking about this is because of Peters' lumping without explanation (as usual).  So, really, the whole thing is quite simple:  ignore Peters and vote YES in recognition of what was right from the start and never should have been changed.”