Proposal (970) to South American Classification Committee

Note from Remsen: This proposal is being evaluated by NACC concurrently

Revise generic limits among Rhodothraupis, Periporphyrus, and Caryothraustes, and adopt a new linear sequence for these taxa

Background:

Rhodothraupis celaeno (Deppe, 1830) is a dichromatic understory cardinalid of the lowlands of northeastern Mexico, the males being largely dark red with a solid black head and dark back, whereas the females have the red replaced by yellowish olive (Brewer 2020b). This overall plumage pattern is shared by Periporphyrus erythromelas ("Gmelin, JF", 1789) of northeastern South America and the southeastern Amazon Basin, although that species is brighter red (males) or yellow (females), especially on the back, and has a larger bill (Brewer 2020a, eBird records). After being placed in various ‘catchall’ genera (e.g., Loxia, Fringilla) in the 19^th century, Rhodothraupis celaeno bounced around between the monotypic genus Rhodothraupis Ridgway 1898, Periporphyrus Reichenbach 1850, Caryothraustes Reichenbach 1850, and Pitylus Cuvier 1829 (Ridgway 1901, Hellmayr 1938), whereas Periporphyrus erythromelas moved between its current genus and Pitylus Cuvier 1829 (Hellmayr 1938). Molecular data have now shown Pitylus to be part of Saltator in the Thraupidae, but the remaining three genera are closely related and part of the Cardinalidae (Barker et al. 2015). Parkerthraustes humeralis (Lawrence 1867) was previously considered a Caryothraustes until molecular data showed it belonged in the Thraupidae (Demastes and Remsen 1994). In the current treatment of NACC/SACC, Caryothraustes contains two species: poliogaster of Mexico and Central America and canadensis of northeastern South America, southeastern Brazil, and eastern Panama (Clements et al. 2022). Both species of Caryothraustes are monochromatic, largely arboreal lowland species. Both Rhodothraupis celaeno and Periporphyrus erythromelas are mostly understory / midstory species, and at least Periporphyrus will join mixed flocks (Brewer 2020a).

All four species in this group give leisurely whistled songs in short but widely separated strophes (i.e., typical cardinalid songs), although the pattern differs between species. The two Caryothraustes also give a variety of “loud and arresting” calls when flocking, described as a “zzzrt”, “tree-dreek”, or “chew-chew-chew” (Gulson 2020). Rhodothraupis and Periporphyrus both give more subtle calls; a “high, clear, penetrating slurred ‘sseeuu’” in Rhodothraupis and a ”high-pitched, sharp ‘spink’” in Periporphyrus (Brewer 2020a, 2020b).

The last major generic revision of this group was that of Ridgway (1901), resulting in the treatment followed by most subsequent authors, with Rhodothraupis and Periporphyrus each being monotypic, and Caryothraustes with two species (e.g. Dickinson and Christidis 2014, Gill et al. 2020, Clements et al. 2022, Chesser et al. 2023). Paynter (1970) lumped Caryothraustes poliogaster with canadensis, but that treatment was not followed by subsequent authors. SACC recently considered a proposal to split Caryothraustes canadensis, which did not pass. In addition to whether the species were dichromatic or monochromatic, Ridgway (1901) used the following structural characters to delimit genera: Periporphyrus with a culmen longer than the tarsus, concave mandibular tomium, and a “broad truncated prominence” at the base of the tomium (i.e. a “toothed” tomium), Rhodothraupis with a relatively longer tail and narrower bill, and Caryothraustes with a relatively shorter tail and broader bill. We now know that bill shape is extremely labile in the Cardinalidae, with a particularly drastic example being “Guiraca” [=Passerina] caerulea.

del Hoyo et al. (2016) transferred both Rhodothraupis and Periporphyrus to Caryothraustes but provided no rationale for this action. Both Periporphyrus and Caryothraustes were described in the same volume by Reichenbach (Reichenbach 1850), but I am unable to locate a copy of this volume to review the genus descriptions. Hellmayr (1938) lists the two genera as being described on sequential plates 77 (Periporphyrus) and 78 (Caryothraustes). My interpretation is that these genera were therefore simultaneously published, and that in transferring Periporphyrus to Caryothraustes, del Hoyo et al. (2016) should be considered the First Revisers when they selected Caryothraustes as having priority.

New Information:

Barker et al. (2015) used a supertree approach to estimate a phylogeny for the 9-primaried oscines which resulted in many genus and family level rearrangements that have since been adopted by NACC, SACC, and other authorities. This tree was based primarily on the mitochondrial genes Cyt-B and ND2, augmented by four nuclear genes for representatives of most genera. Below I have reproduced a portion of the tree showing most of the Cardinalidae, including the species relevant to this proposal (Figure 1). Of note is that Rhodothraupis, Periporphyrus, and Caryothraustes form a clade sister to Cardinalis. Rhodothraupis and Periporphyrus are sister taxa, separated by about 5 Ma (right-most dashed line in Figure 1). A more recent phylogenetic analysis of Caryothraustes (Tonetti et al. 2017; with Rhodothraupis and Periporphyrus as outgroups) using the mitochondrial locus ND2 found similar branch lengths and topology as Barker et al. (2015).

Figure 1. A portion of the Cardinalidae phylogeny from Barker et al. (2015). The two vertical dashed lines correspond to 10 Ma (left-hand line) and 5 Ma (right-hand line). Rhodothraupis celaeno is indicated with a red arrow.

A more recent study on sister relationships of multiple complexes of Amazonian and Atlantic Forest taxa (Bocalini et al. 2021) included all subspecies of Caryothraustes and both Rhodothraupis and Periporphyrus as outgroups. They estimated a coalescent-based species tree from 3,826 UCE SNPs, which I have reproduced below (Figure 2). As an aside, Bocalini et al. (2021) found that Caryothraustes canadensis simulans of eastern Panama was sister to C. poliogaster, rather than to the remainder of C. canadensis, so a species-level taxonomic change should be considered for simulans, either considering it a separate species or transferring it to C. poliogaster.

Figure 2. The phylogeny of Caryothraustes and two outgroups, estimated in SNAPP. From Bocalini et al. (2021).

The topology of the phylogenies in Barker et al. (2015) and Bocalini et al. (2021) are concordant, but the branch lengths are extremely different. Most notably, the UCE tree in Bocalini et al. (2021) found extremely low divergence between Rhodothraupis and Periporphyrus (far less than the divergence within Caryothraustes), although I note that this is a coalescent-based analysis, which in my experience often recovers lower divergence estimates than maximum likelihood methods like those used in Barker et al. (2015). The Barker et al. (2015) study was based on many fewer loci, which may also explain the different branch lengths between the two studies.

A series of specimens of the relevant species in this group are shown on below, courtesy of Terry Chesser. Within each species, males are on the left and females on the right, and the species from left to right are: Rhodothraupis celaeno, Periporphyrus erythromelas, Caryothraustes poliogaster, and Caryothraustes canadensis.

Effect on AOS-CLC area:

Merging Rhodothraupis into Periporphyrus would result in a name change from Rhodothraupis celaeno to Periporphyrus celaeno. Merging all species into Caryothraustes (following del Hoyo et al. 2016) would result in name changes for Rhodothraupis celaeno and Periporphyrus erythromelas in the following linear sequence: Caryothraustes celaeno, C. erythromelas, C. poliogaster, C. canadensis.

Recommendation:

The two major clades in this group have the same number of species (2), and Rhodothraupis celaeno is the northern-most member of the group, so regardless of any genus-level transfers celaeno should go first in the linear sequence. I recommend adopting a new linear sequence (see below), which differs only slightly from the current NACC treatment.

The ~5 Ma divergence between Rhodothraupis and Periporphyrus in Barker et al. (2015) is less than that shown by most related cardinalid genera, and the very low divergence between the two species found by Bocalini et al. (2021) suggests that these two species are very closely related. The bill size / shape differences are best not considered genus-level characters in the Cardinalidae, and I find the wing and tail length differences to not be drastically different. Combined with the broadly similar red-and-black (male) and green-and-black (female) plumages of Rhodothraupis and Periporphyrus, I think Rhodothraupis celaeno is best transferred to Periporphyrus.

Based solely on relative branch lengths in Barker et al. (2015), the divergence between Caryothraustes and Rhodothraupis + Periporphyrus is roughly comparable to some other genus-level divergences in the Cardinalidae, such as those among Amaurospiza, Cyanoloxia, and Cyanocompsa. These similar genus-level clade ages, combined with the differing plumage dimorphism (monochromatic in Caryothraustes vs. dichromatic in Rhodothraupis and Periporphyrus), and a more canopy-dwelling habit and differing calls of Caryothraustes, are sufficient in my view to keep Caryothraustes and Periporphyrus as separate genera. Although I minimized the importance of the bill shape differences in advocating for the merger of Rhodothraupis and Periporphyrus, the two Caryothraustes do have a notably wide bill. Caryothraustes do also look superficially like females of Rhodothraupis and Periporphyrus, albeit with restricted black on the head. That said, I don’t think that a merger of Caryothraustes and Periporphyrus is necessary, although it would maintain a monophyletic grouping.

Please vote on the following:

A. Adopt the following linear sequence: celaeno (extralimital), erythromelas, poliogaster (extralimital), canadensis.

B. Transfer Rhodothraupis celaeno (extralimital) to Periporphyrus (advisory only)

C. Transfer Rhodothraupis celaeno and Periporphyrus erythromelas to Caryothraustes (only if B passes)

I recommend a YES on A and B, and a NO on C.

Literature Cited:

Barker, F. K., Burns, K. J., Klicka, J., Lanyon, S. M., and Lovette, I. J. 2015. New insights into New World biogeography: An integrated view from the phylogeny of blackbirds, cardinals, sparrows, tanagers, warblers, and allies. The Auk, 132(2), 333–348. https://doi.org/10.1642/AUK-14-110.1

Bocalini, F., Bolívar-Leguizamón, S. D., Silveira, L. F., and Bravo, G. A. 2021. Comparative phylogeographic and demographic analyses reveal a congruent pattern of sister relationships between bird populations of the northern and south-central Atlantic Forest. Molecular Phylogenetics and Evolution, 154, 106973. https://doi.org/10.1016/j.ympev.2020.106973

Brewer, D. 2020a. Red-and-black Grosbeak (Periporphyrus erythromelas), version 1.0. In Birds of the World (J. del Hoyo, A. Elliott, J. Sargatal, D. A. Christie, and E. de Juana, Editors). Cornell Lab of Ornithology, Ithaca, NY, USA. https://doi.org/10.2173/bow.rabgro1.01

Brewer, D. 2020b. Crimson-collared Grosbeak (Rhodothraupis celaeno), version 1.0. In Birds of the World (J. del Hoyo, A. Elliott, J. Sargatal, D. A. Christie, and E. de Juana, Editors). Cornell Lab of Ornithology, Ithaca, NY, USA. https://doi.org/10.2173/bow.crcgro.01

Chesser, R. T., S. M. Billerman, K. J. Burns, C. Cicero, J. L. Dunn, A. W. Kratter, I. J. Lovette, N. A. Mason, P. C. Rasmussen, J. V. Remsen, Jr., D. F. Stotz, and K. Winker. 2023. Check-list of North American Birds (online). American Ornithological Society.

Clements, J. F., T. S. Schulenberg, M. J. Iliff, T. A. Fredericks, J. A. Gerbracht, D. Lepage, S. M. Billerman, B. L. Sullivan, and C. L. Wood. 2022. The eBird/Clements checklist of Birds of the World: v2022. Downloaded from https://www.birds.cornell.edu/clementschecklist/download/

Demastes, J. W., and J. V. Remsen, Jr. 1994. The genus Caryothraustes (Cardinalinae) is not monophyletic. Wilson Bulletin 106(4): 738–743.

Dickinson, E. C., and L. Christidis (Editors) (2014). The Howard and Moore Complete Checklist of the Birds of the World. 4^th edition. Volume Two. Passerines. Aves Press Ltd., Eastbourne. UK.

Gill, F., D. Donsker, and P. C. Rasmussen (Editors) (2020). IOC World Bird List (v 10.2). DOI 10.14344/IOC.ML.10.2. http://www.worldbirdnames.org/

Gulson, E. R. 2020. Black-faced Grosbeak (Caryothraustes poliogaster), version 1.0. In Birds of the World (T. S. Schulenberg, Editor). Cornell Lab of Ornithology, Ithaca, NY, USA. https://doi.org/10.2173/bow.blfgro1.01

Hellmayr, C. E. 1938. Catalogue of birds of the Americas, part XI. Field Museum of Natural History Zoological Series Vol. XIII. Chicago, USA.

del Hoyo, J., Collar, N.J., Christie, D.A., Elliott, A., Fishpool, L.D.C., Boesman, P. and Kirwan, G.M. 2016. HBW and BirdLife International Illustrated Checklist of the Birds of the World. Volume 2: Passerines. Lynx Edicions and BirdLife International, Barcelona, Spain and Cambridge, UK.

Paynter, R. A., JR. 1970. Subfamily Cardinalinae. Pp. 216-245 in Check-list of birds of the world (R. A. Paynter, Jr., ed.). Museum of Comparative Zoology, Cambridge, Massachusetts

Reichenbach, H. G. L. 1850. Avium systema naturale. Das natürliche System der Vögel. Expedition der vollständigsten naturgeschichte. Dresden and Leipzig.

Ridgway, R. 1901. The birds of North and Middle America. Part I. Bulletin of the United States National Museum. No. 50.

Tonetti, V. R., F. Bocalini, L. F. Silveira, and G. Del-Rio. 2017. Taxonomy and molecular systematics of the Yellow-green Grosbeak Caryothraustes canadensis (Passeriformes: Cardinalidae). Revista Brasileira de Ornitologia 25: 176–189.

Oscar Johnson, February 2023

Vote tabulation: https://www.museum.lsu.edu/~Remsen/SACCPropChart864+.htm

Comments from Robbins: “YES. I support the new linear sequence proposed by Oscar and also vote Yes for the rationale he presents in placing Rhodothraupis celaeno in Periporphyrus. I would support either maintaining Periporphyrus or placing it within Caryothraustes.”

Comments from Stiles: “YES to all recommendations. A- the new sequence based on geography fits with the closer affinities between Periporphyrus and Rhodothraupis than with Caryothraustes; B- genetic, plumage and ecological similarities lend support to merging Rhodothraupis into Periporphyrus, and C- vocal, genetic and ecological differences support maintaining separate Periporphyrus from Caryothraustes.”

Comments from Areta:

“A-YES to the proposed linear sequence.

“B-NO. I don´t see a pressing need to move Rhodothraupis into Periporphyrus. My main arguments have to deal with side-effects that I think should be considered with a broader comparative framework in mind. This seems a borderline case to me in which any option can be defended, but merging them should (from my perspective) lead to a cascade effect also requiring decisions on what to do with other genera, given the lack of monophyly of Habia, and the deep divergences in Piranga. I think that it would be more appropriate to deal with the Rhodothraupis/Periporphyrus case after a comparative study is published dealing with generic limits in this clade. I find it difficult to decide what to do with the long branch length of Rhodothraupis/Periporphyrus, without further context on generic limits in the group. For example, H. rubica seems to have diverged from Chlorothraupis at about the same time as Rhodothraupis and Periporphyrus, and two even more deeply diverged clades have been uncovered in Piranga. I feel that we need a better comparative internal yardstick in order to decide. Otherwise, this merger might (or might not) need to be undone soon. I am not strongly opposed to merging Rhodothraupis into Periporphyrus, it is just that I do not know how other pieces in the puzzle will fit and I prefer to have the advantage of a broader comparative look before deciding to change this well-entrenched taxonomy.

“C-NO. Pretty much for the same reasons that I voted NO to B: one could choose to accommodate the generic limits in different ways depending on different criteria, but I do not think it is advisable to mess around with Rhodothraupis/Periporphyrus/Caryothraustes without a clear perspective on what to do with other close relatives. For example, one could follow the merger of Rhodothraupis and Periporphyrus into Caryothraustes and then also decide to merge Habia with Chlorothraupis and recognizing a deeply diverged Piranga. I would possibly vote against all these three if the moment arrives, but this would be another way of dealing with generic limits in this clade. An integrative perspective on genetic and phenotypic variation in this clade should give us more elements to make a balanced decision towards establishing generic limits.”

Comments from Lane: “A) YES. B) NO, I don’t see a need to do this, given the long branches involved and the distinctions between the two species. C) NO, as per B, this seems an unnecessary move given the distinctiveness of the taxa involved.”

Comments from Claramunt: “I broadly concur with Oscar’s assessment and recommendation:

“A – YES

“B – YES. erythromelas and celaeno are two sister species with similar morphologies, plumage, and ecology. Treating them in the same genus makes total sense. The genus category is most useful when it groups multiple species indicating relationships and monophyletic groups. Monotypic genera fail at that. I know that monotypic genera are sometimes unavoidable, but this is a case in which they are avoidable, and a single genus with two species in it makes a lot of sense.

“C – NO. If it were only for their plumage, I would merge all fours species into a single genus, but I think it makes more sense to maintain the big and red erythromelas and celaeno separated from the smaller, yellow, and canopy-dwelling Caryothraustes.”

Comments from Remsen:

“A. YES. Required book-keeping.

“B. YES. The genetic differences are minor, and the differences in plumage insufficient on their own to assign them to different genera.

“C. NO. The estimated divergence time is early Miocene, well within the range of lineage ages of most groups considered to be in separate genera, so I see no objective reason to upset the status quo

Comments from Zimmer:

“A) YES on adopting the proposed linear sequence of celaeno, erythromelas (NOTE that it is celaeno that is extralimital, not erythromelas as stated in the Proposal), poliogaster, canadensis.

“B) YES on transferring Rhodothraupis celaeno to Periporphyrus, as supported by multiple data sets.

“C) NO, on folding Rhodothraupis celaeno and Periporphyrus erythromelas into Caryothraustes. In addition to all of the differences between these two species-pairs cited by Oscar, I would add that both Caryothraustes troop through the forest in noisy groups of up to 20 (or more) individuals – very unlike celaeno or erythromelas, which, at least in my experience, tend to be encountered as rather retiring, inconspicuous pairs or individuals.”

Comments from Bonaccorso: “YES on A. The phylogenies are concordant. I wouldn't worry too much about the differences in branch lengths since we are basically comparing a mitochondrial-DNA-driven tree with a coalescent-based tree. Based on plumage dichromatism, and overall size and bill size, transferring Rhodothraupis celaeno to Periporphyrus seems reasonable, so YES to B. No to C.”

Comments from Gustavo Bravo (who has Del-Rio vote): “Given the evidence from various datasets, I support keeping the two larger-sized and sexually dichromatic (red/yellow) species in one genus and the smaller and sexually monochromatic in another. Species limits within Caryothraustes will have to be revisited in the future. Thus, my vote goes as follows:

A – YES.

B – YES.

C– NO.”

Comments from Stiles: “YES to A + B, NO on C. I especially dislike lumping all of these in Caryothraustes, which differs in plumage, vocalizations and habits from Periporphyrus.