Review of recent seabird taxonomy papers, from Steve N. G. Howell

Two recent (2004) papers on seabird taxonomy should be of interest to all seabirders, and also raise some other general issues about taxonomic concepts: one was in Emu 104:125-147, by Penhallurick and Wink (P & W), and is a genetic-based taxonomic overhaul of the Procellariiformes as a whole; the other was in Auk 121:847-864, by Austin et al. (A et al.), and is a molecular phylogeny of the Little/Audubon’s Shearwater complex. Here I’d like to review findings that may be of interest to ID Frontiers, and discuss some issues of method and philosophy; persons with a deeper interest should obviously find and read these papers for themselves.

First off, P & W is generally well written and, unlike so many papers in Auk and the like, is quite user friendly to the more general reader. It takes time to overview and explain several aspects that relate to genetic studies, species concepts, problems that remain unresolved (molecular clocks, for example), etc., and I for one really appreciate this approach. P & W also argue for the inclusion of pairwise distance matrix data in such papers, rather than simply phylogenetic trees statistically generated from the data, and this seems like a good suggestion.

P & W make a number of recommendations from higher level to species-level, all of which are worthy of consideration and many of which make intuitive sense. Others are more radical (such as uniting albatrosses and two subfamilies of storm-petrels in a single family) – but this highlights an issue that genetics can, in theory, resolve: the dim-distant-past relatedness of groups despite millions of years of subsequent modification and divergent and convergent evolution. For example, with small shearwaters, features such face pattern, foot color, undertail covert color, and such may not be taxonomically informative, as the results of A et al. indicate. (Why colder-water taxa such as Manx and the traditional Little Shearwater group have shorter tails with white undertail coverts whereas warmer-water taxa such as Townsend’s and the Audubon’s complex have longer tails and dark undertail coverts is an interesting point of conjecture.)

Besides the possible merger of albatross and storm-petrels, the diving-petrels clump closer to other petrels, shearwaters, etc., and together these might comprise a second family – thus we would have only two families of tubenoses versus the familiar four:
a) Diomedidae (albatrosses, storm-petrels); and b) Procellariidae (everything else). However, P & W are suitably and commendably cautious in this (“radical”) proposal and note that corroborating evidence should be sought.

What about lower levels? FYI, at the species level, P & W work within what they call the “multidimensional Biological Species Concept,” and their introduction offers a helpful and concise overview of relevant species concepts.

Albatrosses. The split into four genera is again supported and this split, which was adopted by the AOU a while back, makes good sense from every angle. At the species level, P & W reject all the new splits and further suggest that Amsterdam Albatross be lumped in with Wandering. Thus we would revert to 13 well-defined albatross species, several with two or more subspecies that all correspond to the terminal taxa (no new subspecies) that are familiar to albatross people.

Storm-Petrels. No species-level changes are proposed but the generic-level taxonomy is thrown into chaos, with two new genera proposed, the familiar Oceanodroma sunk, and Halocyptena (the old genus for Least Storm-Petrel) rejuvenated. I doubt that anyone familiar with storm-petrels at sea would have guessed how the species supposedly fall into these new divisions, so here goes:
Hydrobates: British and Fork-tailed!
Cymochorea: Leach’s, Swinhoe’s, Tristram’s, (Markham’s).
Halocyptena: Least, Wedge-rumped, Black, (Matsudaira’s).
Thalobata: Band-rumped, so distinctive that it gets its own genus!

Note that Ashy and Hornby’s were not dealt with because of no real evidence for their affinities. However, the same is true for Markham’s and Matsudaira’s, for which P & W note that their placement is provisional. This sloppy “science” should have been avoided, given the so-called evidence used (e.g., an unreferenced statement in Sibley & Monroe 1990 that Markham’s may be conspecific with Tristram’s – which is unlikely, at best!). Regardless, there is a lot of food for thought here. The well-marked southern hemisphere storm-petrel genera were not altered, although Nesofregetta (White-throated) was not included.

Petrels and Shearwaters. 
The Fulmar clade (Fulmarini) is well defined and comprises Antarctic, Snow, and Pintado petrels, both fulmars, and giant-petrels. However, Northern and Southern giant-petrels differed from each other by less than did the North Atlantic (nominate glacialis) and North Pacific (rodgersi) Northern Fulmars (0.61% for giant-petrels; 1.92% for fulmars). P & W recommend lumping the giant-petrels into a single species, presumably called Giant Petrel.

Shearwaters. The genus Calonectris (Cory’s and Streaked) is retained as distinct, while traditional Puffinus is split into two genera: Puffinus (small shearwaters, basically) and Ardenna (large shearwaters, with Buller’s and Wedge-tailed distinct enough to warrant their own subgenus, Thyellodroma). No surprises here from the perspective of the field birder. At the species level, however, Flesh-footed and Pink-footed differ by 0.70% and P & W recommend lumping these two taxa. The two Cory’s (Atlantic borealis and Mediterranean diomedea) differ by 0.96%, but no samples of Cape Verde Shearwater were included.
Within the small shearwaters the paper starts to unravel in its organization. The only small shearwater taxa analyzed were: Little (but no mention of which subspecies! See later discussion of A et al. paper), Hutton’s, Audubon’s (but no mention of which subspecies!, cf. A et al.), Christmas, Black-vented, Manx, Mediterranean (aka Yelkouan), and Balearic (last two differing from each other by 2.2% and retained as species).
Now, within the text discussion, SPECIES proposed and listed (without comment) in the restricted genus Puffinus (small shearwaters) also include: Persian (persicus), Newell’s, Townsend’s, Fluttering, Heinroth’s, and Bannerman’s (bannermani)... and yet no data are provided. I don’t argue that any of these may be undeserving of species status, but throwing them in without comment seems unscientific, at best. For example, in other worlds the taxa bannermani and persicus are traditionally subspecies of Audubon’s Shearwater (e.g., see review by A et al.).

Prions, which are extralimital to North America (but won’t the first one here, if at sea, be a wet nightmare). P & W recommend the rather radical lumping down to two species of prions, which they call Broad-billed Prion (ironically including the present-day Slender-billed Prion!) and Fairy Prion. That would certainly make it easier in the field... but is quite contrary to other studies that recommend recognizing six or more species of prions. Blue Petrel is also included in this grouping.

Procellarini. Includes the genera Procellaria (Spectacled Petrel was not sampled) plus Bulweria and, provisionally, Pseudobulweria (Tahiti Petrel etc.), for which no complete sequences were available. Bulwer’s Petrel has traditionally been considered a gadfly petrel, closer to the Pterodroma petrels, so this is a marked shift that may draw comment.

Pterodromini. The Pterodroma petrels (once Tahiti Petrel et al. are excluded) form a monophyletic group, thank goodness, but so few samples were available that subdivisions within the genus are uncertain. A tentative analysis is offered, however, with Pterodroma (in the restricted sense) involving only North Atlantic species plus Soft-plumaged (4.55% different from Fea’s – called deserta not feae in Fig. 2 by the way – which is only 2.9% different from Bermuda Petrel) and the Great-winged group (Great-winged, White-headed, Magenta, and Atlantic). Three other provisional genera are discussed. Zino’s Petrel was unavailable for study, and the taxon for the single sample of Dark-rumped Petrel was “not established” – perhaps collected at sea (?) but no elucidation is offered for this odd statement.

Pelecanoidini. Diving Petrels. The four widely recognized species are retained.

So that’s it for a possible revision of tubenoses...

At a different level, A et al. review the “Global molecular phylogeny” of the Little/Audubon’s Shearwater cluster. Despite calling their paper (p. 855) “the first comprehensive phylogenetic assessment of this complex...” A et al. did not analyze gunax, bannermani, or heinrothi (the first two taxa samples did not yield DNA, the last was not available); and, unfortunately, their sample of Townsend’s Shearwater failed to yield DNA. Still, they did have samples of almost all taxa, many derived from samples of skin cut from the foot webbing of museum specimens. They used 1-10 individuals of each taxon, whereas samples for the P & W paper seemed to be one individual per taxon (which generously assumes each sample was correctly identified and labeled, and that the taxa show no significant internal variation).

Strong support was found for three biogeographically defined groups: a) North Atlantic; b) Southern Oceans and Australasia; and c) tropical Indian and Pacific oceans. But the 
proposed (re)classification is not congruent with any traditional taxonomy. 

Revised species limits proposed by A et al. are:
Puffinus bailloni (Tropical Shearwater), ranging from tropical Indian Ocean through the western Pacific Ocean (including the taxa nicolae, polynesiae, and dichrous, which together form a “lower-level taxon” P. dichrous; plus bailloni, persicus, and temptator, all three of which are their own “lower-level taxon”).
Puffinus assimilis (Little Shearwater), ranging in the southern oceans from the South Atlantic to New Zealand, and probably Chile (including the taxa assimilis, tunneyi, kermadecensis, haurakiensis, and elegans).
Puffinus lherminieri (Audubon’s Shearwater) of the North Atlantic (including lherminieri, loyemilleri, boydi, and baroli, with the last two being their own “lower-level taxa”).
Puffinus subalaris (Galapagos Shearwater) of the Galapagos (monotypic).

One other enigmatic taxon, myrtae, of the central Pacific, was found to be closer to Newell’s Shearwater, and was lumped with it as P. newelli (which implies Townsend’s and Newell’s are considered separate species). The controversial taxa atrodorsalis and colstoni from the Indian Ocean are both sunk, and several other taxa (such as S Caribbean loyemilleri) are weakly defined.

The separation of Galapagos Shearwater is no real surprise, but the other groupings are rather a shake-up, mainly the split of North Atlantic populations as one species, thus cleaving apart both the traditional Little and Audubon’s shearwaters in one cut.

So, these two papers give us a lot to think about. This is where the discussion gets fuzzy. As Mark Twain said, he’d rather have his ignorance than another man’s knowledge, for his ignorance was much greater – and this is where I may get to demonstrate my profound ignorance.

One point that emerges from these papers, among others, is the apparent inability (to my mind) of these molecular approaches to resolve species-level divisions. But this comes down to what we call a species; where we draw the lines (humans and chimps apparently share 98% of their genes...). 

A et al. note that their analysis calls for detailed studies of morphology, life history, vocalizations, and additional molecular markers to resolve some of the terminal taxa issues. And the introduction to P & W notes that “it cannot be said that molecular data have resolved the problem of establishing boundaries between genera, subgenera, species, and subspecies unambiguously.” For example, in the albatrosses, Black-browed Albatross and Campbell Albatross have been separate for an estimated 2.6 million years – seems like a long time to me. The paradoxical human seemingly loves consistency and the ability to say: the division happens at a value of 5.6734%, or some such. And yet every molecular taxonomy paper, computer program, whatever, is just a little bit different (some say better) than the previous one, and thus inconsistency reigns. Which means it is all very difficult for those of us ignorant of genetics to make consistent judgements and comparisons. 
	For example, P & W used complete mitochondrial cytochrome b sequences largely obtained from GenBank, whereas A et al. based their phylogeny on 917 base pairs of the mitochondrial DNA cytochrome b gene. The pairwise distance matrices of P & W feature uncorrected ‘p’ distances and corrected amino acid distances, whereas those of A et al. feature Tamura-Nei corrected distances. Because of these method differences, it is unclear to me whether a 2.3% difference in one paper is identical to a 2.3% difference in the other (can anyone help?). Are the distances and thus results of the two papers directly comparable? This human tendency – different methods, different statistics, no consistency – appears to be true of perhaps every single genetic-based taxonomy paper I have read; and this seems rather unscientific...

On p. 133, P & W note that “although clear differences in appearance mean that there must be differences elsewhere in their genomes, the near identity of the cytochrome b sequences...” This is where I can’t help feel there is a difference between statistical “significance” and biological significance – a huge one. Just looking at the North Atlantic Puffinus, for whatever reason the colder-water baroli has evolved to look like more like a southern ocean Little than its closest relative, warmer-water boydi, which looks and behaves like an Audubon’s. Based on series of specimens I measured last week at USNM, there is no overlap in, e.g., wing or tail measurements, between boydi and lherminieri; and none in tail length between baroli and boydi. Using the “common sense Biological Species Concept” I would argue these are three valid species-level taxa that exhibit significant biological differences in morphology and ecology (and probably voice, I’d guess). They diverged a hell of a long time ago and do not interbreed. 

To this end, it is good to see that A et al. (p. 859) note “the taxonomic decision with regard to species versus subspecies status will depend on other characters” – which implies they accept the limits of their DNA data.

Conversely, P & W combine seemingly radical higher level taxonomy with very conservative species-level taxonomy based simply on numbers. It is common sense that some species and species-groups diverged longer ago than others, some maybe 10 million years ago, others 5 million, others 1 million... where to draw the line?

Regardless of one’s taxonomic philosophy, the two papers discussed here make huge progress in what has remained for too long an area of smoke and mirrors. With more papers (hopefully using directly comparable methodology...) and more field data, the taxonomy of tubenoses should become much clearer.

Steve N. G. Howell