Treat Snowy Plover Charadrius nivosus as a separate species from Kentish Plover C. alexandrinus
Proposal (482) to South American Classification Committee
[Note from Remsen: this proposal passed the North American Classification Committee (8 to 3) and is posted here with the permission of the senior author. Because there was significant disagreement among NACC members, I also post their comments here, at the end]:
Despite their distinct geographic distributions, Palearctic and Nearctic populations of Snowy Plover Charadrius alexandrinus are currently considered to be a single species. Snowy Plovers in America were first described as Aegialitis nivosa by Cassin in 1858 (cited by Oberholser 1922), but the differences in adult plumage to Eastern Snowy Plovers were not deemed to be consistent enough to warrant full species status (Oberholser 1922).
Genetic differences between Eurasian and American populations of Snowy Plovers are substantial (Küpper et al. 2009). Mitochondrial DNA sequences of ND3 and ATPase differ by more than 6% between American and Eurasian populations. Φst values for North American and Eurasian populations are large (all population comparisons ≥ 0.95). Autosomal and sex chromosomal markers show distinct alleles for Eurasian and American Snowy Plovers. Fst values based on microsatellite analyses are above 0.25 for all population comparisons between Eurasian and North American Snowy Plovers. The American and Eurasian Snowy Plovers are more genetically differentiated than the Eurasian Snowy Plovers and African White-fronted Plovers C. marginatus (described by Vieillot 1818).
Genetic differences are also reflected in morphological and behavioural differences. Eurasian Snowy Plovers are larger than American Snowy Plovers. There are also differences in chick plumage and male advertisement calls (Küpper et al. 2009).
The North American subspecies nivosus, tenuirostris and occidentalis show genetic structuring, but mitochondrial sequence differences between subspecies are comparatively low (< 1%, Funk et al. 2007).
1. Split Kentish Plover from Snowy Plover and adopt ‘Kentish Plover’ for Palearctic populations
2. Change scientific name of Snowy Plover to Charadrius nivosus (Cassin 1858) with three subspecies: C. nivosus nivosus (currently C. alexandrinus nivosus), C. nivosus tenuirostris (currently C. alexandrinus nivosus) and C. nivosus occidentalis (currently C. alexandrinus occidentalis)
3. Keep scientific name Charadrius alexandrinus (Linnaeus 1758) for Kentish Plover
Funk, W. C., T. D. Mullins, and S. M. Haig. 2007. Conservation genetics of snowy plovers (Charadrius alexandrinus) in the Western Hemisphere: population genetic structure and delineation of subspecies. Conservation Genetics 8:1287-1309.
Küpper, C., J. Augustin, A. Kosztolányi, J. Figuerola, T. Burke, and T. Székely. 2009. Kentish versus Snowy Plover: Phenotypic and genetic analyses of Charadrius alexandrinus reveal divergence of Eurasian and American subspecies. Auk 126:839−852.
Linnaeus, C. 1758. Systema naturae per regna tria naturae: secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. 10th edition
Oberholser, H. C. 1922. Notes on North American birds. XI. Auk 39:72-78.
Vieillot J. 1818. Ornithologie.
Clemens Küpper, and Tamás Székely (Department of Biology and Biochemistry, University of Bath, UK) & Terry Burke (Department of Animal and Plant Sciences, University of Sheffield, UK)
Comments from NACC members:
Banks: YES. This seems to be well documented.
Barker: YES. Kentish and snowy plovers are reciprocally monophyletic in mtDNA, which suggests that these two taxa have already met a fairly high bar for species recognition. Under a simple divergence model, nuclear Fst of >0.2 implies less than one migrant per generation, which is inadequate to maintain genetic continuity in the face of genetic drift, let alone selection. Küpper et al. found Fst between Kentish and snowy plovers of 0.26-0.38, suggesting much less than one migrant per generation. Funk et al.'s work on New World populations establishes that none of them are nearly so divergent. I agree with Van that given the poor population sampling the size differences don't mean much, but for me the multilocus genetic data are convincing. If Kentish and White-fronted plovers intergrade genetically in Africa, does that affect species status of the snowy? I don't think so. I know that the genetic arguments above are a simplification, and that more sophisticated analyses, better population sampling, etc. could refine this estimate, but I think the burden of proof now rests with the single species side of the argument.
Cicero: YES. The combination of mtDNA and nuclear genetic data provide good evidence in favor of a split between Eurasian and American populations of C. alexandrinus. I would vote no if this were based solely on mtDNA, but the authors analyzed 21 microsatellite loci and a sex-specific marker for 166 individuals - a nice data set that supports the genetic differences. The lack of samples from populations of other subspecies is a definite weakness of this study, as the authors admit, and further sampling might reveal additional species within this complex. However, I think that the data are still strong enough to move forward with this split. Although the vocal differences are only suggestive (no quantitative analyses, only 2 sonograms presented), the courtship calls do appear to be quite distinct.
Dunn: YES. I’m a bit puzzled on this. The NACC has been quick to correct the lumping craze from the 1960’s-early 1980’s period and has done so even in one case when there wasn’t a good published paper rebutting the lump (Rosy Finches). But, what about the lumping errors of the 1930’s-early 1940’s? Why is one more sacrosanct than the other?
The history of these taxa is well detailed. They were regarded as separate species through the third edition of the Check-List (1931), then were lumped in the 19th Supplement (first Supplement since the Check-List) in 1944 (Auk 61:441-464). The AOU cited Peters (1934,Volume 2, page 250) in the lump, but Peters offers no rationale. Perhaps he followed Oberholser’s (1922) recommendation (citation in the current motion) in lumping New and Old World taxa. Oberholser’s conclusion was based on the similarity in plumage, and that even the supposed characters (crown color, more rufous in alternate Old World birds) and lore color (darker in Old World birds) overlapped. Obviously there was no analysis of vocalizations in Oberholser’s study or in the decisions by Peters and the AOU.
Those that do know the calls hear no similarity between New and Old World birds. Old World birds, at least those that I know well in Asia, give “kip” notes, much as the call of a Sanderling, or a Red-necked Phalarope, totally different from the buzzy type calls in New World birds.
Even beyond that, as Pam notes the two ranges are separated by thousands of miles (Japan and Washington) and have likely been separated by eons. I’m not the least bit surprised that the initial genetic studies indicate they are quite different. It’s not like Bar-tailed Godwits and Whimbrels where the species are circum polar. Is there any other case where New and Old world populations of the same species (but different subspecies) are so separated by range?
So, my rationale in voting yes is based mainly on the basis that there was no justification (either by AOU in 1944, or Peters earlier) for the lump, that the two have very different vocalizations, and they are well isolated by range (continents apart!). The genetic studies support this as well.
Kratter: NO. The authors never give what definition of species they used. Presumably it’s PSC, because there is no discussion of reproductive isolation. There are several subspecies of alexandrinus not analyzed that could alter the results. What if eastern Asian subpp. of alexandrinus are more closely related to nivosus? The authors do not present this possibility, and state only that greater geographical representation could find additional cryptic spp. Definitely should have included rubricapilla in the analyses. It does not seem that microsatellites would be the best nuclear marker for this type of study. Level of morphological and plumage differences is fine for spp (A good comparison is mongolus & leschenaultii). Too bad the authors do not even mention plumage differences.
Rasmussen: YES. Although there are weaknesses with the case presented in the paper, as pointed out by others, clearly these are better considered two distinct species, very likely not each other’s closest relatives. There is no geographical approach between Palearctic and Nearctic birds (since the Snowy Plover doesn’t breed north of Washington) and no indication of introgression, and birds in the Far East are the same race as those in Europe. In a good sample of several different types of vocalizations from both from various commercially available sources, none of their vocalizations are very similar, and some are markedly distinct, such as the sweet prolonged upslurred note of Snowy Plover, which is not matched by anything in the Kentish Plover’s repertoire according to the available sources. I already advocated this split in my book---the available evidence overall is too strong to ignore, and we may wait many years for someone to produce a paper pulling it all together.
Remsen: NO. This vote is cast from the perspective that I am certain that actual analyses of vocalizations will show that the two groups are separate BSC species. As is, the Küpper et al. paper provides data consistent with species rank but not sufficient for a yes vote at this time. The authors argue that alexandrinus and marginatus are more closely related than either is to nivosus. However, this is only with respect to two mitochondrial genes and rests, as far as I can tell, largely on their text statement “Differences between mtDNA sequences and CHD-Z genotypes were larger between Kentish and Snowy plovers (6%) than between Kentish and White-fronted plovers.” The haplotype tree presented (Fig. 2) actually provides no support for the node that links marginatus and alexandrinus, or even support for the monophyly of alexandrinus itself. All the tree shows is that there is strong support that the 13 individuals of nivosus and the 4 marginatus each form a monophyletic group. Further, the authors themselves point out that a weakness of their study is that not all of the taxa assigned to the alexandrinus group have been sampled. Also, they only sampled the most geographically remote subspecies (Madagascar) of C. marginatus, which is widespread in Africa and possibly is in contact with unsampled alexandrinus populations on the African coasts. Finally, I find no mention of “gene tree” in the text (quick skim – may have missed it?).
The authors assign importance to the low variation within nivosus compared to alexandrinus. However, that variation within nivosus is based on only 13 individuals, from only 2 localities yet -- how do we know with such a sampling regime?
As for non-genetic data, the discrete biometric differences are biologically interesting and not inconsistent with species rank. However, by themselves they are basically irrelevant to taxon rank unless one adopts a species concept that does not allow for discrete geographic variation within a species. Many populations of birds that no one would claim should be treated as separate species differ significantly in mean measurements among populations. Note (Table 4) that the differences between the one breeding population of Snowy and four Kentish populations analyzed are highly statistically significant but nonetheless overlap in all measurements except tarsus length. However, with only one population of Snowy Plovers analyzed, we actually do not know how broadly this applies. The difference in plumage pattern of chicks (Fig. A1) is also of interest, but whether the difference shown in the photos applies broadly is uncertain because are no actual data to evaluated (N=1 of each taxon).
The vocal differences are indeed important. Every pair of sister populations in shorebirds ranked as separate species also differs, as far as I can tell, in vocalizations. In fact, those differences in vocalizations have been the nail-in-coffin evidence for recent splits. Strong empirical evidence indicates that barriers to gene flow are associated with discrete differences in vocalizations. However, the paper only presents two sonograms from two individuals and thus is totally insufficient for assessment of individual and geographic variation.
The lead sentence in the final paragraph of the published paper claims: “we have shown that Kentish and Snowy plovers should no longer be considered to constitute a single cosmopolitan species.” Really? One sonogram of each, non-overlapping tarsus length (based on small N and without good geographic sampling), and a suggestive mtDNA gene tree should not be considered sufficient in my opinion. I strongly suspect that the vocal differences, widely known to birders, once adequately documented, will be sufficient evidence for species rank; in fact, I think that there are already enough publicly available recordings that a simple presentation of sonograms from multiple individuals without much additional work.
Rising: YES. These have been begging to be split for a long time, and many have proposed it, although I don't think that it has formerly been done. Sort of the "I think that the Kentish and American Snowy plovers are different species," stuff. I'm happy with the proposed nomenclature.
Stotz: YES. The information presented by Kupper et al is generally strong. Their vocal information is a bit marginal in terms of sample size, bit it is clear from other literature that the voices of Snowy and Kentish plovers are substantially different.
Winker: NO. On the whole, I suspect that they will eventually be proven correct. But I am not convinced mostly for sample size issues, with genetics (13 Snowy Plovers is too small a sample size) and especially with the sample sizes for chick plumage and vocalizations in the Appendix in the 2009 Auk publication. This seems like too much of a minimalist approach to documenting phenotypic differences (body size is not a useful species limits character) and species limits using genetics. With real population samples (and better geographic coverage in Snowys), their preliminary data suggest that they could eventually make a convincing case, but until those data are available I do not think a change is warranted.
Comments from Remsen: “NO. I’ll stick with what I said in my NACC vote. With a decent sample of published sonograms, I would instantly change to a YES vote, but I think the published data so far are insufficient for the split. On the other hand, Jon Dunn does have a valid point that the “data” for the original lump are lacking.”
Comments from Stiles: “YES. The sticking point here seems to be the possible heterogeneity among the Old World subspecies; those most closely approaching the New World in E Asia apparently remain distinct morphologically from nivosus suggest no major problem – further splits among these forms are not our problem. Considering the evidence as it stands, that favoring this split, although imperfect, clearly trumps that for the original lumping with alexandrines, which is essentially nil.”
Comments from Robbins: “YES. As pointed out by members of the NACC committee sampling of other populations/taxa could have been more extensive, but the authors did demonstrate significant genetic differences between New World and Old World taxa. Morphological and vocal differences have been documented as well. Issues associated with possible gene flow in African taxa really have no bearing on whether Snowy Plover deserves species status. Given current data I believe recognizing alexandrinus as a species is warranted.”
Comments from Nores: “YES. As indicated by Küpper et al. (2009), the genetic differences (mtDNA and nuclear genetic) between Eurasian and American populations of Snowy Plovers are substantial, and recognizing them as two species is warranted. Although their vocal information is a bit poor in relation to sample size, it is clear from other sources that the voices of Snowy and Kentish plovers are quite different. As indicated by Cicero, the lack of samples of other subspecies is a definite weakness of this study.”
Comments from Pacheco: “YES. Defendo que em casos como este – no qual as razões para o lumping não foram demonstrados – o tratamento original pode ser restaurado a partir das informações disponíveis.”
Comments from Zimmer: “YES. Van’s comments are all spot-on with respect to the inadequacy of the published non-genetic data, and I share the concerns regarding geographic breadth of taxon and geographic sampling as it relates to some of the genetic data. However, I think that the vocal differences between the two groups are well known, even if not properly documented in a published format, and the genetic distance between the two groups is substantial (and with no prospects for introgression). Given that, the tipping point for me is Jon’s argument that the true status quo should be the pre-Peters treatment, in which Kentish and Snowy plovers were treated as distinct species. I’ve maintained all along that the quality of the published evidence for recognizing a split should be lower if the “split” is merely restoring a Peters lump that was made without justification. I think the burden of proof should be placed on those that would follow Peters’ unjustified lump, not on those that would restore the original status.”
Comments from Pérez-Emán: “NO for now to be consistent with previous proposal’s votes in which decision is not based in thoroughly analyzed published data. Genetic data published by Küpper et al. (2009) and Funk et al. (2007) suggest these taxa are largely differentiated (though largely homogeneous within each “species”). These data coupled with the few available morphological data (especially plumage pattern) and published and unpublished vocal evidence (as commented by both Dunn and Rasmussen) should be more than complete evidence for this split. However, I agree with Van that a more thorough evaluation should be completed before accepting this change.”
Comment from Thomas Donegan: “In connection with the recent update to the Colombian checklist (Donegan et al. 2011), we inspected recordings we could get our hands on of Snowy and Kentish Plovers and presented some sonograms and discussion of the vocal differences observed. We tentatively adopted this split, in line with some committee members’ comments and the AOU-NACC. Although the vocal sample we had remains very small and may not satisfy the requirements of those who have voted against the proposal, this discussion provides additional information compared to the two sonograms and assertion in Krupper et al. that the songs are different, so this paper may be of interest.
“Reference: Donegan, T.M., Quevedo, A., McMullan, M. & Salaman, P. 2011. Revision of the status of bird species occurring or reported in Colombia 2011. Conservación Colombiana 15: 4-21. http://www.proaves.org/IMG/pdf/CC15/Conservacion_Colombiana_15_4-21.pdf.”