How many Toucanets? (Part 2)

I covered the Central American species in the Aulacorhynchus ‘prasinus’ (Emerald Toucanet) species complex in Part 1. Here, I cover the South American forms.

Edit: See excellent comments by Rasmus at Birdforum regarding the situation below. On a number of points, including the subspecies distributions and interpretations of figures, Rasmus has clarified the situation. Thanks!

The distribution and relationships of different subspecies populations of ‘prasinus’ toucanets is less well resolved in South America. I have no firsthand experience with the group, but I've done the best I could to sort out these groups based on the literature and present some kind of unified picture here, highlighting areas needing further study. Sampling is the big problem and the morphology and coloration studies (Navarro-Siguenza et al. 2001, hereafter just Navarro-Siguenza) do not precisely match up with the genetic work (Puebla-Olivares et al. 2008, hereafter just Puebla-Olivares) because of the incomplete sampling in both. Each paper proposes slightly different taxonomic groupings based on their incomplete work, but they do state the need for more focused work on the South American members of the ‘prasinus’ complex.

There are seven subspecies in the South American clade, ranging along mid-slopes of the Andes from their northernmost extent in Colombia and Venezuela south to Peru and Bolivia. The field guides, and the two papers examining them, agree on their rough distribution as follows:

A.p. lautus (Colombia)
A.p. phaeolaemus (Colombia)
A.p. griseigularis (Colombia)
A.p. albivitta (Colombia,Venezuela, Ecuador)
A.p. cyanolaemus (Ecuador and Peru)
A.p. atrogularis (Peru)
A.p. dimidiatus (Bolivia)

Here is a composite figure approximately depicting their ranges and appearance based on multiple sources (see full citation below). Throat color ranges from white to gray to blue-gray to black, roughly in a northward to southward progression. The extent of yellow in the bill varies regionally. No distinct population breaks jump out. A large population stretching from Bolivia to southwest Ecuador includes the black-throated forms dimidiatus, atrogularis, and the blue-throated cyanolaemus. In the north, blue-gray-throated phaeolaemus, gray-throated griseigularis, and white-throated albivitta inhabit parallel north-south branches of the Andes, roughly in that west-to-east order. Gray-throated lautus is found on the disjunct mountain range on the Colombian coast, the Sierra de Santa Marta.

(click to view large)

Sources disagree on whether some of these populations are disjunct or continuous and in some cases there is no data on whether or where some subspecies make contact with one another. The following map is how most field guides depict the range of Emerald Toucanet in the Andes, and shows in more detail how the populations follow narrow elevation gradients along the Andes (it is pieced together from two field guides, don’t mind the color change – green in the north, blue in Peru, see citation below). This map also shows the basal Central American Darien population, A. cognatus, on the border with Panama.

Specifically, when I say sources disagree, I mostly mean the two papers I’ve been discussing disagree with the field guides. Here are the population maps from those two sources, Navarro-Siguenza on the left and Puebla-Olivares on the right:

(click to view large)

You’ll notice that these maps give away the taxonomic conclusions of each paper, so allow me to step through those conclusions before trying to reconcile them with the information in the field guides.

The Puebla-Olivares phylogeny breaks down into two groups – one group composed solely of albivitta from the eastern Colombian Andes, and its two northern forks (Merida, Perija). This group is divergent from the remaining South American lineages by about 5% sequence divergence. The authors recommend splitting it as the monotypic species, the White-throated Toucanet (A. albivitta).

The remaining group contains the birds from the central Colombian Andes southward to Bolivia. Of these, the central Colombian Andes birds are basal and most divergent, by about 1.5%, and the authors recommend splitting this as the Grey-throated Toucanet (A. griseigularis).

All of the remaining populations fall into one closely-related, poorly resolved group, including the blue-throated cyanolaemus and the black-throated atrogularis and dimidiatus. The authors recommend splitting this last group as the Black-throated Toucanet (A. atrogularis), an odd name for a species including multiple throat colors.

Here is a summary of the Bayesian tree, with approximate mtDNA divergences:

(click to view large)

The Puebla-Olivares phylogeny is missing two subspecies in their sampling – lautus from the Sierra de Santa Marta, and phaeolaemus from the western Colombian Andes. We can only hypothesize where these taxa fit into the phylogeny. If I had to guess, based on coloration and range, phaeolaemus would be closely allied to its close neighbors, griseigularis. Lautus is more distinctive as a disjunct population and in coloration, and I would expect it to fall out as a basal group, or perhaps with its closest neighbor, albivitta. These are just my speculations, however, and only completing the molecular work will tell us for sure.

Using their color and morphology analysis, Navarro-Siguenza split the South American toucanets into three species: A. lautus, A. albivitta (including griseigularis and phaeolaemus), and A. atrogularis (including cyanolaemus and dimidiatus). The phylogeny tells us that lumping the three Colombian Andes subspecies based on similarity in pattern wasn’t correct, as griseigularis is actually closer to the southern atrogularis group than the other sampled northern subspecies. On the other hand, the phylogeny actually confirms the morphology assessment that the blue-throated birds in the south are in the same species as the black-throated birds. Based on how complex the situation is, we really need to get lautus and phaeolaemus sampled to fully sort out the evolutionary history of the ‘prasinus’ complex in South America.

Two main problems exist in the analysis of this species complex that also need to be addressed before the evolutionary history of the group can be fully figured out. There is some confusion in the Navarro-Siguenza analysis of the color patterns in the northern subspecies, and confusion in sampling in Ecuador in Puebla-Olivares, where the white-throated albivitta meets the southern blue-throated cyanolaemus.

Take a look at the Ecuadorian population in the maps from the two papers above – the ‘disjunct’ Ecuadorian birds are assigned to albivitta in the coloration paper, but cyanolaemus in the phylogeny paper. So, specifically where do albivitta and cyanolaemus occur in Ecuador? Ridgely and Greenfield (2001), in their Ecuador field guide, illustrate the population distribution quite clearly – albivitta comes down the east slope of the Andes from Colombia, and cyanolaemus comes up the east slope from Peru. They give the known southern limit of albivitta as the Napo region, and the known northern limit of cyanolaemus as Morona-Santiago, but state that it is unclear whether the two forms meet in central Ecuador:

Puebla-Olivares illustrate a disjunct population in SW Ecuador and NW Peru - cyanolaemus. They illustrate another disjunct population in NE Ecuador, which is labeled on their specimen list as albivitta. Navarro-Siguenza et al. (2001) show the same disjunct populations, and label the NE Ecuador population as albivitta. All field guide range maps I’ve seen show the NE Ecuador population as continuous with the Northern Andes, so I would believe that birds in the northern half of the Ecuadorian Andes are indeed white-throated albivitta birds as Navarro-Siguenza labels them and Puebla-Olivares does in their specimen list.

So what? Well, the Puebla-Olivares phylogeny puts this population solidly within the southern dimidiatus-atrogularis-cyanolaemus group! Puebla-Olivares label the NE Ecuador birds as atrogularis-group on their map with no clarification in the text on this switch. Their map shows albivitta populations as restricted to Colombia. The birds sampled from NE Ecuador are labeled as albivitta in their specimen list, and are sampled from Napo, within the range of albivitta as in Ridgely and Greenfield (2001). Puebla-Olivares et al. (2008) make no mention of this crazy result, and I can’t figure out what is the most likely hypothesis – A) there is some gross error in the paper, B) the exact range divide between albivitta and cyanolaemus in Ecuador is unclear and the paper actually sampled cyanolaemus or C) albivitta birds in Ecuador are really a disjunct population allied with cyanolaemus and not with Colombian populations of albivitta! If the white-throated Ecuadorian birds are in the southern atrogularis group, then this species is remarkable among all in the ‘prasinus’ species complex as it includes birds with three major throat colors – white, blue, and black. I think only clarification from the authors will help us figure this one out - I may try to contact them soon.

Taking a detailed look at the Colombian populations analyzed by color pattern in Navarro-Siguenza et al. (2001), I realized that the color patterns they report don’t reconcile with those depicted in the field guides. In analyzing this paper, I must first point out a gross error – figure 3, the frequencies of different color and pattern traits in the various populations, has been mislabeled. Instead of an AB/CD pattern in labeling the four components, it goes AD/BC – this isn’t important unless you’re looking at the figure yourself, then you’ll see what I mean. It is also possible I have a pdf copy that has since had its errors corrected by the journal.

In the following map, lautus is found in the Sierra de Santa Marta, the large triangular coastal range in northern Colombia. albivitta inhabits the Eastern Cordillera, including the northwest fork (Sierra de Perija) and the northeast fork into Venezuela (Cordillera de Merida). griseigularis inhabits the Central Cordillera, and the east slope of the Western Cordillera. phaeolaemus inhabits the western slope of the Western Cordillera.

The field guides are abundantly clear – phaeolaemus is blue-gray-throated, griseigularis is gray-throated, and albivitta is white-throated. My confusion originated from the face pattern labeled “I” in Navarro-Siguenza - a gray-throated bird with reduced yellow on the bill, makes up about 80% of Eastern Andes birds sampled and appearing in no other population. However, if one refers back to the face pattern legend, pattern “I” is located from Cauca in the Western Andes. Pattern “I” resembles no population of toucanet as depicted in the field guides. The explanation for this remains a mystery to me – the eastern albivitta is supposed to be white-throated with no variation, while the westernmost phaeolaemus is supposed to be blue-gray throated. Neither greseigularis nor phaeolaemus is ever depicted with reduced yellow on the bill. I can’t make sense out of this – there must be some error, as pointed out by the difference in labeling of “I” between two figures, and I’m not sure what the correct result should be. Because I can’t make any sense out of this, I don’t trust any of the rest of the analysis of the albivitta-griseigularis-phaeolaemus group in their data (lautus and the southern group seem okay and don’t conflict with other sources).

To illustrate what I am talking about, here are the author’s different face patterns, with the throat color labeled and the approximate percentage of each pattern found in each population. Note particularly how the only gray or blue-gray throated population in the Colombian Andes is the pattern "I", in the Eastern Andes. This makes no sense at all when you refer back to the subspecies depicted above. The authors do not make mention of these significant differences except to suggest that the variation in pattern is due to frequent contact between populations, which doesn't make sense when the populations don't have the patterns they 'should' have.

(click to view large)

The worst problem I see in Navarro-Siguenza is not the gross errors (mislabeling figures, misidentifying the population of face pattern “I”) but the lack of data given allowing others to sort out their results. They lump their specimens into broadly defined localities (see the paper’s map above, and compare with the more detailed field guide maps). If the variation and confusion in the albivitta group is due to previously undepicted regional variation, no deciphering of it is possible from this lumping of source data. Most frustratingly, the authors does not give precise locality data for any specimens used, preventing any further attempt to understand their data. To see how useful providing specific locality data, look how I used the specimen list in Puebla-Olivares above.

Summary

Puebla-Olivares and Navarro-Siguenza both state that the systematics of the South American ‘prasinus’ complex are under need of more serious work, and I couldn’t agree more. While I am convinced by their work on the Central American group, leading to four species splits, I can’t say I am convinced by the splits in South America (although I don’t doubt that there are splits to be made) and I think more data should be obtained from all populations before a reasoned decision can be made. Too much information is missing to properly delineate which populations belong to which species.

Here are all of the putative species splits identified by the Puebla-Olivares et al. phylogeny:

Aulacorhynchus wagleri (Wagler’s Toucanet)
A. prasinus (Emerald Toucanet)
Incl: prasinus, warneri, chiapensis, virescens, stenorhabdus, volcanius
A. caeruleogularis (Blue-throated Toucanet)
Incl: caeruleogularis, maxillaris
A. cognatus (Goldman’s Blue-throated Toucanet)
A. albivitta (White-throated Toucanet)
A. griseigularis (Grey-throated Toucanet)
A. atrogularis (Black-throated Toucanet)
Incl: atrogularis, dimidiatus, cyanolaemus

Populations not assignable to species based on the molecular work so far:
lautus
phaeolaemus
Ecuadorian populations of albivitta

You’ll have to check out both papers yourself for discussion of the biogeography of the group as we understand it so far, although a detailed analysis of the causes of diversification in this group is lacking. They do note that the patterns in distribution of toucanet lineages is similar to other Andean species, so perhaps a broad-scale comparative work is possible as we examine more groups in as much detail as the toucanets. Puebla-Olivares mention that they are going to analyze the rest of the Aulacorhynchus toucanets in this manner – I hope their further work lends a lot of clarity to both the evolutionary history and taxonomic clarity of all of the toucanets. They’re just fantastic birds.

Finally, if you were wondering about this picture, it is A. atrogularis from Peru:


References

Subspecies depictions:
Map - Puebla-Olivares et al. 2008
cyanolaemus, atrogularis, dimidiatus - Schulenberg et al. 2007
lautus - Short and Gilbert 2002
albivitta, griseigularis, phaeolaemus - Restall et al. 2007

Combined map:
Peru - Shulenberg et al. 2007
Northern South America - Restall et al. 2007

Population maps:
Puebla-Olivares et al. 2008 (right)
Navarro-Siguenza et al. 2001 (left)

Phylogeny based on Bayesian tree in Puebla-Olivares et al. 2008

Ecuador map - Ridgely and Greenfield 2001

Colombia map - Source

face patterns - from figs. 1 and 3 of Navarro-Siguenza et al. 2001

A. atrogularis photo - Source

Hilty, S.L., and W.L. Brown. 1986. A Guide to the Birds of Colombia. Princeton University Press.

NAVARRO S., A.G., PETERSON, A.T., LÓPEZ-MEDRANO, E., BENÍTEZ-DÍAZ, H. (2001). SPECIES LIMITS IN MESOAMERICAN AULACORHYNCHUS TOUCANETS. The Wilson Bulletin, 113(4), 363. DOI: 10.1676/0043-5643(2001)113[0363:SLIMAT]2.0.CO;2

Puebla-Olivares, F., E. Bonaccorso, A.E. de los Monteros, K.E. Omland, J.E. Llorente-Bousquets, A.T. Peterson, and A.G. Navarro-Siguenza. 2008. Speciation in the Emerald Toucanet (Aulacorhynchus prasinus) complex. The Auk. 125(1): 39-50.

Restall, R., C. Rodner, and M. Lentino. 2007. Birds of Northern South America: An Identification Guide, Volume 2. Yale University Press.

Ridgely, R.S., and P.J. Greenfield. 2001. The Birds of Ecuador Field Guide. Comstock Publishing.

Schulenberg, T.S., D.F. Stotz, D.F. Lane, J.P. O'Neill, and T.P. Parker III. 2007. Birds of Peru. Princeton University Press.

Short, L, J Horne, and AE Gilbert. 2002. Toucans, Barbets, and Honeyguides. Oxford University Press, USA.