Proposal (648) to South American Classification Committee
Revise the classification of the Phalacrocoracidae
Background: Our current SACC footnote is as follows:
8. Although the monophyly of the Phalacrocoracidae has never been questioned, treatment within the family has ranged from subfamilies and multiple genera, e.g., Hypoleucus, Stictocarbo, Leucocarbo, Notocarbo (Siegel-Causey 1988) to all species in a single genus, Phalacrocorax (e.g. Dickinson 2003). Kennedy et al. (2009) showed that the subfamilies and most genera of Siegel-Causey were not monophyletic. Dickinson & Remsen (2013), using the data in Kennedy et al. (2000, 2009), resurrected Microcarbo for a group of five Old World species, but all New World species remained in Phalacrocorax. Kennedy and Spencer (2014), using additional new genetic data, split Phalacrocorax into seven genera, restricting Phalacrocorax to a group of Old World species, and placing South American taxa into Nannopterum (for brasilianus and harrisi), Poikilocarbo (for gaimardi), and Leucocarbo (for magellanicus, bougainvillii, atriceps). SACC proposal badly needed.
New information: Kennedy and Spencer (2014) sampled 40 taxa of cormorants and sequenced over 8000 bp of mtDNA (5 loci) and nuDNA (5 loci). (However, except for a few samples obtained from LSU and AMNH, all samples are unvouchered blood or feather samples; the lack of anomalous results and Kennedy’s extensive experience with the family indicate no misidentifications).
Their Figure 1 is pasted in below (for better resolution see the original – pdf available from me if needed):
Kennedy and Spencer used the tree topology to recommend recognition of 7 genera (by resurrecting old generic names) for their 7 well-differentiated clades, as you can see from the figure, and the effect that adoption of their classification is reflected in the SACC note above.
Although estimated lineage ages are not included in the figure, from the text the estimates are as follows: (1) extralimital Microcarbo vs. the rest, 13-15 mya; (2) Poikilocarbo, 12-13.5 mya; (3) extralimital Urile vs. Phalacrocorax, 9-10 mya; and (4) Nannopterum vs. Leucocarbo, no figure given but crudely extrapolating from the other nodes, probably 6-7 mya. (Note the irony that Nannopterum, described solely on the basis of its flightlessness and reduced wings, is resurrected and survives as the oldest name for the two most widespread species in the W. Hemisphere; it is also of interest that N. harrisi is sister to the ancestor of olivaceus + auritus, as previously found by Kennedy et al. (2009); I would have predicted that it was recently derived from one of the two extant species.)
Analysis and recommendation: The genetic data look solid, and the 7 groups have been evolving as separate lineages for a long time. The Phalacrocoracidae must be one of the most homogenous families in terms of superficial external morphology, and so I suspect most were comfortable with but a single genus for the entire family, as in the Peters’ Check-list (1979) (and even the 1931 Peters’ CL recognized only 3 genera). (The tiny African Pygmy Cormorant looks to me basically like a dwarf P. olivaceus.) However, those who have studied cormorant skeletal morphology closely (Siegel-Causey 1990, Worthy 2011) have advocated multiple genera (although their groupings did not show much concordance with the Kennedy-Spencer tree).
If the 7 lineages were of comparatively recent origin, say within the last 5 million years, I would oppose elevating each of the groups to genus rank. However, because these lineages are old, all likely evolving independently since the Miocene, I personally favor following the Kennedy-Spencer recommendations exactly.
Converting their tree to a linear sequence with the usual sequencing conventions produces the following classification, with indentations used to signal nodes, with extralimital taxa in gray:
Many extralimital Leucocarbo
Let’s divide the proposal into two parts because even if one votes against the new classification, there remains the issue of linear sequencing of species taxa to match the tree topology.
Part A. Recognize the generic boundaries proposed by Kennedy and Spencer (2014), which would place all South American species in one of the three resurrected genera as per above. I recommend a YES.
Part B. Revise the linear sequence to reflect the phylogeny of Kennedy and Spencer (2014), as outlined above, regardless of passage of Part A. I recommend a YES on this.
KENNEDY, M., AND H. G. SPENCER. 2014. Classification of the cormorants of the world. Molecular Phylogenetics and Evolution 79: 249-257.
KENNEDY, M., C. A. VALLE, AND H. G. SPENCER. 2009. The phylogenetic position of the Galapagos Cormorant. Molecular Phylogenetics and Evolution 53: 94-98.
SIEGEL-CAUSEY, D. 1988. Phylogeny of the Phalacrocoracidae. Condor 90: 885–905.
WORTHY, T.H. 2011. Descriptions and phylogenetic relationships of a new genus and two new species of Oligo-Miocene cormorants (Aves: Phalacrocoracidae) from Australia. Zool. J. Linn. Soc. 163, 277–314.
Van Remsen, September 2014
Comments from Stiles: “Although the resulting genus name is rather unfortunate, the phylogenetic data look solid, so:
A. YES, as this does maintain consistent ages for the genera of cormorants.
B. YES, this follows from A.
Comments from Stotz: “A. Modified YES. Right now I can’t vote for a split into 7 genera. I would personally favor, Phalacrocorax for old world taxa (plus Urile) and Leucocarbo for New World taxa, recognizing Poikilocarbo for gaimardi and Microcarbo for Old World pygmy cormorants. The European Shag is a problem; I could go with Leucocarbo (not sure what the oldest name is), but I guess I am inclined to recognize Gulosus. So for SA taxa, I would say Yes to Poikilocarbo, and Leucocarbo, but NO to the splitting out of Nannopterum. B. YES. This seems straightforward.”
Comments from Nores: “NO. I prefer to be conservative. For this reason, I would place all South American cormorants, except gaimardi, in the genus Leucocarbo:
Comments from Zimmer: “Part (A): YES. Although the thought of 7 genera of cormorants is pushing it, even for someone like myself, who prefers more internally cohesive, narrowly defined genera. Uugh! Part (B): YES.”
Comments from Pacheco: “A – YES; Because the results of Kennedy/Spencer point to ancient lineages, I consider inescapable accept the arrangement proposed in three genera to the South American taxa.
B – YES”
Comments from Areta: “A-YES. Tough decision! To make genetic differentiation of clades including multiple species more consistent, Nannopterum should be merged with Leucocarbo, thus resembling differentiation within Phalacrocorax as defined by Kennedy & Spencer (2014). However, an alternative treatment would be to recognize Nannopterum and to split Phalacrocorax in two or three genera following the branching pattern, making the degree of differentiation within genera more consistent. I incline toward recognizing Nannopterum, given that morphological analyses have also recovered this clade, it is an old split and it provides interesting clues on the evolution of harrisi. Recognition of Poikilocarbo is also reasonable given its phylogenetic position and degree of differentiation. B-YES.”
Comments from Jaramillo: “A – NO but only with respect to Nannopterum, as others have suggested it is more internally consistent to include it with Leucocarbo -- at least to be consistent with the treatment of Phalacrocorax. Not sure which name is older, Leucocarbo or Nannopterum? I assume the former? Separating Poikilocarbo is fully justified. B – YES.”
Comments from Cadena: “NO. I am not sure I fully understand the situation here. Specifically, why exactly is it *necessary* to split the clade sister to Microcarbo into multiple genera? If I understand this correctly, all the taxa in this clade are recognized as members of a single genus by Dickinson and Remsen and in our baseline list; because all the taxa in this genus are descended from a single ancestor (i.e., the genus is monophyletic), I see no need to change. Sure, there are deep divisions within the genus, but this is true of many other genera. Van’s points about the ages of lineages are interesting, but as far as I know, clade age is not a criterion we have consistently followed to establish ranks above the species level. Absent a policy of naming/ranking clades based on their age, I think we should only fiddle with classification above the species level when absolutely necessary due to non-monophyly of taxa. Am I missing something?”