Proposal (388) to South American Classification Committee
Split Diomedea exulans
into four species
Effect on SACC: This
would divide an existing species, Diomedea exulans (Wandering
Albatross), into four species, at least three of which have been recorded in
South American waters.
Background: The Wandering
Albatross (Diomedea exulans) as currently defined by SACC consists of
four taxa:
(1) nominate exulans
(Linnaeus, 1758) of circumpolar distribution across the Southern Ocean (e.g.
South Georgia, Kerguelen, Heard, Macquarie),
(2) dabennena (Mathews,
1929) from the temperate-zone island group of Tristan da Cunha and Gough,
(3) antipodensis (Robertson
& Warham 1992) from the sub-polar Antipodes and Campbell Islands off New
Zealand,
(4) gibsoni (Robertson
& Warham 1992) from the sub-polar Auckland Islands off New Zealand.
The four taxa are characterized by a trend of
neoteny and decreasing size towards the north, with an all-white adult plumage
in the circumpolar exulans giving way to a complex pattern of brown
immature plumage retention in the temperate and New Zealand taxa. The
morphological distinctness between the two New Zealand taxa gibsoni and antipodensis
is in question, and many adult individuals cannot be unequivocally identified,
although adult gibsoni is generally paler (=less neotenous) and somewhat
approaches exulans (Tickell 2000; Brooke 2004; Onley and Scofield 2007).
In 1983, a fifth taxon was described from the
temperate Indian Ocean island of Amsterdam (Roux et al. 1983). This new taxon –
breeding at equal latitudes as dabennena – displays the most extreme
form of neoteny with an all-brown adult plumage. Therefore, Roux et al. (1983)
decided to award it species status: D. amsterdamensis. However, this
treatment is not universally accepted, and some authors have proposed the
inclusion of D. amsterdamensis in D. exulans (e.g. Penhallurick
and Wink 2004).
New Information: In a
controversial book chapter, Robertson and Nunn (1998) put forth a revised
albatross taxonomy in which they elevated all nominal subspecies to species
rank. Consequently, they recognized five Wandering Albatross species. Their
proposal was only partly based on published phylogenetic evidence and was
therefore rejected by some subsequent authors (e.g. Penhallurick and Wink 2004;
Christidis and Boles 2008). However, despite widespread criticism in scientific
circles, the new Robertson and Nunn classification has been widely adopted by
authors of popular bird books (Tickell 2000; Brooke 2004; Onley and Scofield
2007) and by the conservation community (e.g. Birdlife International).
Penhallurick and Wink (2004) employed GenBank
sequences of albatrosses and other seabirds to construct phylogenetic trees and
to compute cyt-b divergences. They found divergences between the five Wandering
Albatross taxa to be well below their 3.2% “cut-off” for species status and
concluded that all five taxa be lumped into a single species. Penhallurick and
Wink’s (2004) work came under criticism for analytical flaws and the rigid use
of cyt-b divergences as a species threshold (Rheindt and Austin 2005).
Burg and Croxall (2004) examined sequences of
the mitochondrial control region in four Wandering Albatross taxa (exulans,
antipodensis, gibsoni, dabennena). They found that exulans,
dabennena, and a clade comprising the two New Zealand taxa (gibsoni and
antipodensis) were separated from one another by 4.5 – 5.2% divergence.
The New Zealand taxa gibsoni and antipodensis were
little differentiated between each other and shared several haplotypes,
although there was one near-fixed difference. Additionally, Burg and Croxall
(2004) analyzed nine microsatellite loci in most samples. They were unable to
detect differentiation between any of their exulans populations,
even between individuals from different oceans, while there were significant
levels of population differentiation between antipodensis and gibsoni.
Based on their genetic data, Burg and Croxall (2004) proposed a three-species
treatment under which the taxon gibsoni is subsumed
under D. antipodensis, while D. dabennena and a
monotypic D. exulans are also viewed as distinct species. Please
note that Burg and Croxall (2004) did not address P. (e.) amsterdamensis.
Burg and Croxall’s (2004) results agree with
phylogenetic studies on other Antarctic sub-polar seabirds that have
demonstrated strong latitudinal differentiation in the absence of longitudinal
differentiation. For instance, Jouventin et al. (2006) detected pronounced
phylogenetic differences in rockhopper penguins and elevated the northern taxon
from the temperate zone to species level (Eudyptes moseleyi), even
though geographic distances between some northern and southern populations are
much smaller than towards their conspecifics. This finding suggests that global
sea currents of different temperature play an important role in seabird
speciation.
Analysis and Recommendation: The
biological species status of the five Wandering taxa must be assessed in the
light of two types of considerations:
(1) The relevance of sequence
divergence: A vast and growing body of literature shows that many avian
biological sister species are generally differentiated by at least c. 2-3%
divergence in a number of widely used mitochondrial coding genes (ND2, cyt-b,
COI), although this figure can be substantially lower on account of rapid
speciation (Johnson and Cicero 2004) or can be skewed by genetic introgression
following hybridization (e.g. Funk and Omland 2003). Albatrosses in general and
the five Wandering taxa in particular are characterized by low divergences
(<1% cyt-b; Penhallurick and Wink 2004). These minute values led
Penhallurick and Wink (2004) to unite the five taxa into a single species.
Although Burg and Croxall (2004) found c. 5% divergence
between Wandering taxa in the mitochondrial control region, this locus is known
to evolve much faster than the widely used coding genes (ND2, COI, cyt-b) and,
therefore, cannot be compared.
The use of mtDNA divergences as a species
indicator intersects the barcoding debate and the molecular clock debate, and
remains controversial. The latest studies seem to show that a homogeneous rate
of c. 2.1% mtDNA divergence per million years may apply across a
wide range of bird families for comparisons below the genus level (e.g. Weir
and Schluter 2008). This would indicate that Wandering taxa are very young.
However, important differences between rates of mtDNA evolution among bird
families cannot be ruled out (Pereira and Baker 2006) and have even been
detected within the Procellariiformes (Nunn and Stanley 1998).
There are other aquatic bird clades
characterized by tiny interspecific mtDNA divergences (e.g. Anas ducks –
Johnson and Sorenson 1999; Larus gulls – Liebers et al. 2004)
possibly related to frequent hybridization and mtDNA introgression in these
groups. Therefore, past introgression events may have artificially reduced
divergences between Wandering taxa and may explain why some researchers
perceive these divergences to be too low for the generally high level of
morphological differentiation.
On the other hand, Friesen et al. (2007) have
shown that speciation in pelagic seabirds may proceed at a much faster time
scale than in most other tetrapods. Their demonstration that a speciation event
between two biological species of storm-petrel dates back only 110,000 –
180,000 years opens up the possibility that the Wandering taxa may also have
attained biological species status in a shorter timeframe than generally
expected.
In summary, tiny mtDNA divergences among
Wandering taxa may be an artifact of introgression. Even if not, the
potentially young age of Wandering taxa does not rule out biological species
status, because even more rapid speciation has been documented in other
seabirds. Therefore, other data sources must be consulted to obtain evidence
for or against the biological species status of Wandering taxa.
(2) The question of taxon allopatry:
Akin to Proposal on Shy
Albatrosses, it is relevant to examine whether the Wandering taxa are
allopatric in essence. One sub-polar taxon (exulans) stretches around
the globe and closely approaches the range of the other three taxa at its
breeding colonies in Macquarie Island (620 km to nearest gibsoni, 700 km
to nearest antipodensis) and South Georgia (2500 km to nearest dabennena).
In contrast, the Atlantic breeding colonies of exulans (South
Georgia) are 5100 km removed from the nearest colony in the Indian Ocean
(Prince Edward Island), and the minimum distance between its Indian Ocean
breeding grounds at Kerguelen and its New Zealand colony at Macquarie is 5800
km. Although Macquarie was not sampled
by Burg and Croxall (2004), their microsatellite data show a panmictic
population structure of exulans between South Georgia and
Crozet across 6000 km. The uniform plumage reflects this lack of
genetic differentiation across the range of exulans and
contrasts with the distinct neotenous adult plumages of the other taxa.
The lack of genetic data on Macquarie
notwithstanding, the small exulans colony on this island only numbers c. 10
birds and is subject to current immigration and emigration to/from the Indian
Ocean (de la Mare and Kerry 1994). It can, therefore, not be very different
from Indian Ocean colonies in terms of population genetics. In fact, exulans is a widespread
visitor to New Zealand and Australian waters in numbers that exceed the size of
the Macquarie colony. The fact that exulans has colonized an
island within the range of gibsoni and antipodensis,
but fails to interbreed with them, suggests that they may have attained
prezygotic isolation mechanisms.
Recommendations: Based
on the above considerations, I suggest the following three options for
treatment:
(1) One
species: Lump all five taxa into D. exulans. This is the status
quo, although I am not sure about SACC’s current stance on the extralimital
taxon amsterdamensis.
(2) Four
species: Recognize all taxa as distinct species, except for gibsoni,
which is retained in D. antipodensis. This is Burg and Croxall’s (2004)
proposal, though – here again – they did not comment on amsterdamensis.
(3) Five
species: Recognize all taxa as distinct species. This is Robertson and Nunn’s
(1998) treatment.
I advise against Option 3, because gibsoni
and antipodensis are poorly differentiated morphologically and
genetically (Burg and Croxall 2004). The significant microsatellite structure
between both taxa is consistent with subspecies treatment.
As far as Options 1 and 2 are concerned, I do
not feel that there is overwhelming evidence for either treatment. However, if
I were forced to make a recommendation, I would advocate Option 2, because
distributional data indicate that the New Zealand taxa don’t interbreed with exulans
even though they could. By yardstick analogy, the temperate-zone dabennena
(which may have a different life-history owing to its warm-current environment)
would be at the species level because its control-region differentiation
towards the other taxa is even more pronounced than that of the New Zealand
clade (Burg and Croxall 2004). Data on the extralimital amsterdamensis are
lacking, but on account of its high level of morphological differentiation
(=extreme neoteny) it may be best to go with the describers’ recommendation for
species status (Roux et al. 1983) until and unless other data have been
presented.
Literature Cited:
Brooke M (2004) Albatrosses and Petrels
across the World. Oxford University Press.
Burg TM, Croxall JP
(2004) Global population structure and taxonomy of the wandering
albatross species complex. Mol. Ecol. 13, 2345–2355.
Christidis L, Boles WE (2008) Systematics
and Taxonomy of Australian Birds. CSIRO Publishing, Canberra.
de la Mare WK, Kerry KR (1994) Population
dynamics of the Wandering Albatross (Diomedea exulans) on Macquarie
Island and the effects of mortality from longline fishing. Polar Biology 14,
231-241.
Friesen VL, Smith AL, Gómez-Díaz E, Bolton M,
Furness RW, González-Solís J, Monteiro LR (2007) Sympatric speciation by
allochrony in a seabird. Proc. Natl. Acad. Sci. U S A 104,
18589–18594.
Funk DJ, Omland KE (2003) Species-level
paraphyly and polyphyly: Frequency, Causes, and Consequences, with Insights
from Animal Mitochondrial DNA. Annual Review of Ecology, Evolution and
Systematics 34, 397-423.
Johnson NK, Cicero C
(2004) New mitochondrial DNA data affirm the importance
of Pleistocene speciation in North American birds. Evolution 58,
1122–1130.
Johnson, K.J. & M.D.
Sorenson. 1999. Phylogeny and biogeography of the dabbling ducks
(Genus: Anas): A comparison of molecular and morphological
evidence. Auk 116: 792-805.
Jouventin P, Cuthbert RJ, Ottvall R (2006)
Genetic isolation and divergence in sexual traits: evidence for the northern
rockhopper penguin Eudyptes moseleyi being a sibling species. Mol. Ecol.
15 (11), 3413-3423.
Liebers D, de Knijff P, Helbig AJ (2004) The
herring gull complex is not a ring species. Proc. R. Soc.
Lond. B 271, 893–901.
Nunn GB, Stanley
SE (1998) Body size effects and rates of cytochrome b evolution
in tube-nosed seabirds. Mol. Biol. Evol. 15:1360-1371.
Onley D, Scofield P (2007) Albatrosses, Petrels
and Shearwaters of the World. Princeton University Press, Princeton.
Penhallurick J, Wink M (2004) Analysis
of the taxonomy and nomenclature of the Procellariiformes based on complete
nucleotide sequences of the mitochondrial cytochrome b gene. Emu 104,
125-147.
Pereira SL, Baker AJ (2006) A mitogenomics
timescale for birds detects variable phylogenetic rates of molecular evolution
and refutes the standard molecular clock. Mol Biol Evol 23, 1731-1740.
Rheindt FE, Austin J (2005) Major analytical
and conceptual shortcomings in a recent taxonomic revision of the
Procellariiformes - A reply to Penhallurick and Wink (2004). Emu 105:
181–186.
Robertson CJR, Nunn GB
(1998) Towards a new taxonomy for albatrosses. Pages
13-19 in Albatross Biology and Conservation. G. Robertson and R.
Gales, Eds. Surrey Beatty, Chipping Norton.
Roux JP, Jouventin P, Mougin JL, Stahl JC,
Weimerskirch H (1983) Un nouvel albatros Diomedea amsterdamensis n. sp. decouvert
sur L'ile Amsterdam (37°50'S, 77°35'E). Oiseau et la Revue Francaise
d'Ornithologie 53 (1), 1-11.
Tickell WLN (2000) Albatrosses. Yale University
Press, New Haven, Connecticut.
Weir JT, Schluter, D (2008)
Calibrating the avian molecular clock. Mol. Ecol. 17, 2321–2328.
Frank
Rheindt, January 2009
Remsen addendum: Thus,
a YES vote would indicate favoring a four species treatment, and no would favor
single species (status quo). If you favor a 5-way split, then vote YES on this
one, indicate that you would favor 5, and if there is enough support, I’ll
create a new proposal to go from 4 to 5 species.
_________________________________________________________________________
Comments from Robbins: “YES, given
the current state of knowledge, Frank’s suggestion of recognizing four species
seems the best course of action.”
Comments from Zimmer: “YES. I find the Burg & Croxall (2004) proposal
to be the most compelling. I can’t
support treating gibsoni/antipodensis as separate species, and
based on current evidence, I’m willing to give amsterdamensis the
benefit of the doubt.“
Comments from Jaramillo: “YES –
This is a subject I have been following for a while, and certainly the
treatment of polytypic Wandering, and a separate Amsterdam didn’t jive with me.
Certainly, if Amsterdam was a species, the other group that shows considerable
neoteny in plumage, particularly that of females (the NZ group, gibsoni and
antipodensis) seemed to warrant species status too, for example. The
issue of latitude and water temperature is indeed of considerable importance in
the argument to separate these taxa, and fortunately it is finally being given
the consideration it deserves. We think it logical to separate closely related
yet different (voice, display, morphology, genetics) species east of the Andes
and west of the Andes, well the same is true of temperate vs. Subantarctic
seabirds, water temperature differences may be a barrier as great as a mountain
range or broad river to a landbird. I have not seen any work that analyzes the
displays of these different forms. It
would be nice to have that data to work with as well, but alas it is not out
there in a manner that we can use to assess behavioral barriers to
reproduction. But as the proposal states, the potential for mixing is there,
because many of these forms overlap in the broad sense that the at sea range
may include breeding islands of members of other taxa in the complex. Finally,
it may not sit well with some people that some of these taxa are extremely
similar to each other, or even possibly unidentifiable other than at the
breeding island (at least some individuals of the population); however. this is
common in Procellariiformes. Divergence in plumage coloration is not great in
seabirds, and sometimes within-species plumage variation is greater than
between-species plumage variation (observed in various polymorphic Pterodroma,
or even Leach’s Storm-Petrel). Four species seems like a reasonable course of
events. Although there are some clear differences between gibsoni and
antipodensis, there are also greater similarities between these two than
with the rest.
“Finally, three of the four have occurred
within our waters: exulans broadly in the southern oceans; antipodensis off
Chile (photos and satellite tracked individuals); dabennena in
Argentina – Uruguay and I assume Brazil.”
Comments from Pacheco:
"YES. Diante do exposto, eu creio que o melhor arranjo seja
aquele que contempla a adoção de 4 espécies, tal qual recomendado por Burg e
Croxall (2004).”
Comments from John Penhallurick:
“Frank Rheindt discusses the taxonomy of
five taxa, four of which (nominate exulans, dabennena, antipodensis
and gibsoni) have been traditionally treated as subspecies of Diomedea
exulans; and one (amsterdamensis) which was originally described as
a separate species (Roux et al. 1983), but which a number of recent
publications (Bourne, 1989; Vuilleumier et al. 1992; Dickinson, 2003;
Penhallurick and Wink, 2004; Christidis and Boles 2008) have treated as a
subspecies of D. exulans. Rheindt
appears to recommend recognising four species: exulans, dabennena, antipodensis (including
gibsoni) and amsterdamensis.
“Rheindt writes relatively approvingly of
Robertson and Nunn (1998), who announced that all terminal albatross taxa
(monotypic species and what had previously been considered subspecies) should
be considered species in terms of the Phylogenetic Species Concept (PSC), to
which they indicated their allegiance. He notes that the Robertson
and Nunn classification “has been widely adopted by authors of popular bird
books (Tickell 2000; Brooke, 2004 Onley and Scofield 2005) and by the
conservation community (Birdlife International).” It should be remembered that Robertson and
Nunn’s treatment was published as an unrefereed book chapter, not in a refereed
journal. Furthermore, Robertson and Nunn adduced no evidence at all
in support of their proposal: it was simply a matter of fiat in
terms of the PSC.
“Rheindt also writes approvingly of Burg
and Croxall (2004), and notes that his final preference, that is, recognising
four species, agrees with Burg and Croxall’s conclusion. It must be
remembered that both papers by Burg and Croxall (2001, 2004) wrote not in terms
of the multidimensional Biological Species Concept (BSC Mayr 1996). In terms of
what species concept they were using, Burg and Croxall cite Moritz (1994a and
1994b), who described the differences between management units (MU) and evolutionary
significant units (ESU): ESUs are two groups that show reciprocal monophyly of
mtDNA haplotypes and significant differences in allele frequencies at nuclear
loci. MUs on the other hand show significant differences in allele
frequencies without regard to the phylogeny of the markers. They
also cite Avise & Wollenberg (1997), who endorsed the Phylogenetic Species
Concept (PSC), which emphasizes the criteria of phylogenetic relationships, and
not reproductive relationships. Thus, it appears that they are using either the
ESU model, which stresses conservation values, or the PSC, which treats all
subspecies as good species. Burg &
Croxall’s discussion is irrelevant to any discussion of albatross taxonomy in
terms of the multidimensional BSC.
“It should be remembered that many
recently discussions of albatross taxonomy have widely relied on conservation
values. This is understandable: there are severe threats to many
albatross taxa from practices like long-line fishing. It is extremely regrettable that much
conservation legislation is written in terms of species, not subspecies, the
latter of which, being geographical representatives of species, are often at
risk. As Schodde and Mason (1999) have
stated: “ ‘subspecies’, as genetically distinct regional populations, are the
building blocks of evolution and the ‘real’ units of biodiversity, and…many
more of them are and endangered than ‘biological species’.” Schodde and Mason
proposed a new term “ultrataxon” to refer to all terminal taxa, the second
reason for doing so being that it averts a re-circumscribing of Australian bird
fauna under alternative definitions of species, which would lead to ambiguity
and confusion in classification. However, in the body of their book,
Schodde and Mason continued to classify birds in terms of species and
subspecies in the fashion of the multidimensional BSC.
“Rheindt, correctly, recognises the role
of neoteny in the differentiation of these taxa, although it is unclear exactly
what he means when he cites dabennena as displaying “the most
extreme form of neoteny”. The plumage of gibsoni, antipodensis and amsterdamensis
recalls stages 1-3 of nominate exulans. Such changes probably
reflect epigenetic change, and specifically gene silencing, in that the one or
more of the genes that are responsible for the change from juvenile or immature
plumage are switched off. Neoteny is also apparently responsible for the
differences between the two taxa in Diomedea epomophora, in that sanford
retains black upperwings. The juvenile stages of both taxa appear to
be almost identical, involving some black speckling on the back, slightly more
in sanfordi, and largely black upperwings; the nominate shows more
white, although the juvenile sanfordi also shows “fine white
fringing to greater median and some lesser secondary coverts” (Marchant &
Higgins 1990: 282). The fact that the cytochrome-b Tamura-Nei
distance between these two taxa is 0.0000% suggests that they diverged very
recently. This suggests that the epigenetic factors involved in such
plumage differences can evolve very quickly indeed, and morphological
differences due to such factors should not, of themselves, be claimed as
evidence of species status.
“In their critique of Penhallurick and
Wink (2004), Rheindt and Austin (2005) cite specifically Abbott and Double
(2003 a, b) as well as Burg and Croxall (2001,2004) as studies that have
uncovered new evidence for the species status of at least some of these
forms. I have explained above why I do not consider Burg and
Croxall’s papers as relevant to the question of species concepts under the
multidimensional BSC. Similarly, I do not believe that anything in Abbott and
Double’s two papers is relevant to the question we address here: should a
number of taxa traditionally treated as subspecies within a single species be
treated as comprising two or more species. Of critical importance in
this discussion are the species concepts utilised in these studies.
“Abbott and Double (2003a) initially
stated that they were adopting the species nomenclature suggested by Robertson
& Nunn (1998). Since Robertson and Nunn (1998) explicitly said
that they were working within the Phylogenetic Species Concept, and since
Robertson and Nunn’s paper was not published in a refereed journal, this is not
a promising beginning for any discussion in accordance with the
Multidimensional BSC. In their abstract, Abbott and Double (2003a)
stated that their analysis confirmed the separation of the shy/white-capped
pair and the Salvin’s/Chatham pair but did not provide species-level
resolution (Emphasis added).
“An admitted limitation of Penhallurick
& Wink (2004) was that it relied on a single gene: cytochrome-b,
which was criticised by Rheindt and Austin (2005) and also in Rheindt’s
Proposal 388. And it is obviously desirable to confirm these
findings with studies of other, particularly nuclear,
genes. However, it should be remembered that many studies have
confirmed the utility of both cytochrome-b and Bayesian
inference. For example, May-Collado & Agnarsson (2006), in a
study of cetacean phylogeny, stated in their abstract:
‘Until
more genes are available for a high number of taxa, can we rely on readily
available single gene mitochondrial data? Here, we estimate the phylogeny of 66
cetacean taxa and 24 outgroups based on Cyt-b sequences. We judge
the reliability of our phylogeny based on the recovery of several deep-level
benchmark clades. A Bayesian phylogenetic analysis recovered all benchmark
clades and for the first time supported Odontoceti monophyly based exclusively
on analysis of a single mitochondrial gene. The results recover the monophyly
of all but one family-level taxa within Cetacea, and most recently proposed super-
and subfamilies. In contrast, parsimony never recovered all benchmark clades
and was sensitive to a priori weighting decisions. These results provide the
most detailed phylogeny of Cetacea to date and highlight the utility of
Bayesian methodology in general, and of Cyt-b in cetacean
phylogenetics. They furthermore suggest that dense taxon sampling, like dense
character sampling, can overcome problems in phylogenetic reconstruction.’
“What Penhallurick & Wink (2004) said
in relation to Diomedea exulans and Diomedea epomophora was
as follows:
‘We provide a
distance matrix for albatrosses as Table 2. In the text that
follows, nucleotide distances are given, with amino acid distances following in
brackets. Considering the distances in the Table 2, those between
the species that were split by Robertson and Nunn (1998) are much smaller than
those between previously recognised "good" species of
albatross. For example, within the D. exulans complex,
the distance between Robertson and Nunn's D. chionoptera [=
nominate exulans] and D. antipodensis is 0.52
% (0.00 %); in the case of their D. exulans [= dabennena],
0.87 % (0.00 %); and in the case of gibsoni, 0.52 % (0.00
%). D. gibsoni shows a percentage difference of 0.00 %
(0.00 %) from D. antipodensis and 0.70 % (0.00 %) from dabennena. Compare these distances, all of less than 1.0
%, with the distances ranging from 3.2 % to 3.6 % between both D. e.
epomophora and D. e. sanfordi from all of the taxa in the exulans complex.
We conclude that gibsoni, antipodensis and dabennena
are better recognised as subspecies of D. exulans than as good
species in their own right. We note that in the case of antipodensis and
gibsoni, both were described as a subspecies of D. exulans in
their original description by Robertson and Warham (1992: 74 and 76).’
“Somewhat surprising is the distance
evidence relating to D. amsterdamensis, which has sometimes been treated
as a good species since its description by Roux et al. (1983),
although Bourne (Table 4 1989: 112) treated it as a subspecies of D.
exulans. The fact that it is only 0.52 % (0.00 %) distant from antipodensis,
gibsoni and exulans, and only 0.87 % (0.00 %) removed from dabennena strongly
suggests that it belongs among the subspecies of exulans.
“In our unpublished reply to Rheindt and
Arndt (2005), which was, I believe very unfairly, denied publication, we made
the following point:
‘The Tamura-Nei
distance between nominate epomophora and sanfordi is
0.0000%, and the same distance is found between D. e. gibsoni and D.
e. antipodensis. This figure suggests that the divergence
between these taxa was very recent. Whereas Burg and Croxall (2004),
in terms of ‘ESUs’, suggested splitting exulans from antipodensis/
gibsoni and both from dabennena, the TN distances of
0.902% between nominate exulans and dabennena; of
0.539% between exulans and antipodensis; of 0.539% between exulans and gibsoni;
of 0.540% between exulans and amsterdamensis; are well below the
TN distance between exulans and epomophora of
3.797. These data suggest that in terms
of the Multidimensional BSC, we have only two species: D. exulans and
D. epomophora, although it would seem appropriate to class dabennena as
a semi-species.’
“On
the question of taxon allopatry, Rheindt concludes “The fact that exulans has
colonized an island within the range of gibsoni and antipodensis,
but fails to interbreed with them, suggests they may have attained
prezygotic isolation mechanisms.”(Emphasis added). To claim that because a
small number of birds (ca. 10) on Macquarie Island have failed to interbreed
with birds on islands 620 km north in the case of gibsoni and 700
km north in the case of antipodensis proves or even strongly suggests
that they could never interbreed again stretches the imagination.
“Rheindt
concludes “tiny MtDNA divergences among Wandering taxa may be an
artifact of introgression…”(Emphasis added). Introgression refers to the
movement of a gene from one species into the gene pool of another by
backcrossing an interspecific hybrid with one of its parents (Dowling and Secor
1997). It is a long-term process; it may take many hybrid
generations before the backcrossing occurs. Given the extreme
philopatry of all Diomedea albatross taxa, the idea of such lengthy
processes of hybridisation, of which there is no evidence whatsoever, seems
implausible. I conclude that mention of two possibilities, without any evidence
for the reality of either, does not amount to any kind of proof.
“In
Proposal 388, Rheindt refers to criticism of Penhallurick and Wink (2004) for
“rigid use of cyt-b divergence as a species threshold (Rheindt and
Austin 2005).” Yet Rheindt himself cites
as authoritative a study by Burg and Croxall which appeals to “c.5% divergence
between Wandering taxa in the mitochondrial control region”, although he
concedes “this locus is known to evolve much faster than the widely used coding
genes (ND2, COI, Cyt-b)”….” There
is an obvious contradiction here.
“Rheindt
and Austin (2005) identified several problems under this heading. Firstly, saturation and multiple
substitutions are a serious problem as one goes deeper in the phylogeny.’ I agree. Because of its fast rate
of mutation, cytochrome-b would be unsuitable for investigating
relationships at the order level. But most of the taxonomic issues
Penhallurick and Wink were addressing in their 2004 paper concerned levels of
divergence of 5% or less. And it is highly unlikely that multiple
substitutions, which require two or more changes at a single site, are going to
be a problem at that level. The use of Tamura-Nei weighted distances
also reduces potential saturation problems.
“A
second problem identified by Rheindt and Austin (2005) is “the difference in
rates of molecular evolution among bird lineages’’. They made the
mistake of assuming that Penhallurick and Wink were applying a universal rate
of evolution: specifically, that we ‘tend to reject separate species status for
any taxon pair with a divergence of <2%.’
What we were actually trying to apply was the principle enunciated by
Helbig et al. (2002) in discussing the types of evidence that might be applied
to determine the species status of allopatric taxa. They referred
to: DNA sequences, and the sum of the character differences corresponding to or
exceeding the level of divergence seen in related species that
coexist in sympatry. Throughout, when
dealing with possible species, we used the distance between well-established
species in the same group as a measuring stick. And it was this
judgement that guided our decisions on status.
“I
believe that is both unfair and incorrect of Rheindt and Arndt (2005) to say
that Penhallurick and Wink (2004) propose to ‘once again revise’ the albatross
taxonomy. In relation to albatrosses, we
supported the analysis contained in Mayr & Cottrell (1979) and in Marchant
& Higgins (1990, vol. 1. Part A: 264-354, except that that source treated
the taxon we call dabennena as the nominate of D. exulans, and
referred to the taxon we call exulans as D. e. chionoptera);
and also in del Hoyo, Elliott and Sargatal (1992); Dickinson (2003) and more
recently Christidis and Boles (2008). Diomedea exulans gibsoni and Diomedea
exulans antipodensis were both described as a subspecies by Robertson
& Warham (1992). Since Robertson & Nunn (1998) claimed to be relying on
genetic distances, our main concern was to point out that a more reasonable
view of distances supported the traditional analysis.
“Finally,
I would like to point to a glaring lack in relation to proposals submitted to
the SACC: specifically, the lack of any criteria for making judgments about
whether the difference between taxa should be at the species or subspecies
level. In the absence of such criteria, one does not know how to
evaluate proposals such as 388. Nowhere in his proposal does Rheindt
explicitly state in terms of what species concepts he is making his proposal.
It does not appear to be the strictest form of the PSC, which views all
terminal taxa as species, since he proposes to treat antipodensis and gibsoni as
conspecific. Perhaps he, like Burg and Croxall, is working in terms of the ESU
or MU concepts of Moritz (1994a and 1994b). But if the multidimensional BSC is
at least implicitly the standard by which such proposals must be judged, I
submit that Proposal 388 fails the test.
“References
Abbott,
C. L. and Double, M. C. (2003a). Phylogeography of shy and white-capped
albatrosses inferred from mitochondrial DNA sequences: implications for
population history and taxonomy. Molecular
Ecology 12: 2747-2758.
Abbott,
C. L. and Double, M. C. (2003b). Genetic structure, conservation genetics and
evidence of speciation by range expansion in shy and white-capped albatrosses. Molecular
Ecology 12: 2953-2962.
Avise
J. C. and Wollenberg, K. (1997). Phylogenetics and the origin of species. Proceedings
of the National Academy of Sciences of the USA 94: 7748-7755.
Bourne,
W. P. (1989) The evolution, classification and nomenclature of the great
albatrosses. Le Gerfaut 79: 105-116.
Burg,
T. M. and Croxall, J. P. (2001). Global relationships amongst black-browed and
grey-headed albatrosses: analysis of population structure using mitochondrial
DNA and microsatellites. Molecular
Ecology 10: 2647-2660.
Burg,
T. M. and Croxall, J. P. (2004). Global population structure and taxonomy of
the wandering albatross species complex.
Molecular Ecology 13: 2345-2355.
Christidis,
L. and Boles, W. E. (2008). Systematics and Taxonomy of Australian
Birds. CSIRO Publishing, Collingwood, Victoria.
Dickinson,
E. C. (2003) The Complete Howard and Moore Checklist of the Birds of
the World. Rev and enlarged 3rd edn. Princeton University
Press, Princeton, New Jersey.
Dowling,
T. E. and Secor. C. L. (1997). The role of hybridization and introgression in
the diversification of animals. Annual Review of Ecology and
Systematics. 28: 593-619.
Helbig,
A. J., Knox, A. G., Parkin, D. T., Sangster, G. and Collinson, M. (2002)
Guidelines for assigning species rank. Ibis 144: 518-525.
del
Hoyo, J., Elliott, A. and Sargatal, J. eds. (1992) Handbook of the
Birds of the World, Vol. 1. Lynx Edicions, Barcelona.
Marchant,
S. and Higgins, P. J. (1990) Handbook of Australian, New Zealand and
Antarctic Birds. Vol. 1. Oxford U. P., Melbourne.
May-Collado,
L. M. and Agnarsson, I. (2006) Cytochrome b and Bayesian
inference of whale phylogeny. Molecular Phylogenetics and Evolution 38,
344-354.
Mayr,
E. (1996). What is a species and what is not? Philosophy of Science 63,
262-77.
Mayr,
E. and Cottrell, G. W. (1979) 'Checklist of Birds of the World'. Vol. 1, 2nd
edn. Museum of Comparative Zoology, Cambridge, Mass.
Moritz,
C. (1994a). Defining ‘evolutionarily significant units’ for conservation. Trends
in Ecology and Evolution 9: 373-374.
Moritz,
C. (1994b). Applications of mitochondrial DNA analysis in conservation: a
critical review. Molecular Ecology 3: 401–411.
Penhallurick,
J. M and Wink, M. (2004) Analysis of the taxonomy and nomenclature of the
Procellariiformes based on complete nucleotide sequences of the mitochondrial
cytochrome-b gene. Emu 104: 125-47.
Rheindt,
F. E. & Austin, J. J. (2005) Major analytical and conceptual shortcomings
in a recent revision of the Procellariiformes – a reply to Penhallurick and
Wink (2004). Emu 105: 181-186.
Robertson,
C. J. R. and Nunn, G. B. (1998) Towards a new taxonomy for albatrosses In Albatross
biology and conservation (Eds. G. Robertson and R. Gales) pp. 13-19.
Beatty and Sons, Chipping Norton.
Robertson,
C. J. R. and Warham, J. (1992) Nomenclature of the New Zealand Wandering
Albatrosses. Bulletin of the British Ornithologists' Club. 112 (2):
74 - 81.
Roux,
J.-P., Jouventin, P., Mougin, J.-L., Stahl, J.-C., and Weimerskirch, H. (1983)
Un nouvel albatros Diomedea amsterdamensis n. sp. découvert sur l'Ile
Amsterdam (37o50'S,77o35'E). Oiseau 53: 1-11.
Schodde,
R. and Mason, I. J. (1999) The directory of Australian birds:
passerines. CSIRO Publishing, Collingwood, Vic.
Vuilleumier,
F., Le Croix, M. and Mayr, E. (1992) New species of birds described from
1981-1990. Bulletin of the British Ornithologists’ Club, Centenary
Supplement, 112A: 267-309.”
Rheindt’s response to the comments by
Penhallurick:
“Penhallurick’s comments are rather antagonistic and
suggest my proposal seeks to establish one taxonomic treatment of Wandering
Albatross at the expense of the other. However, my main conclusion states that
– as far as the “1-species” or “4-species” solutions are concerned – “…I do not
feel there is overwhelming evidence for either treatment…” So essentially, I
concur with Penhallurick to the point that his favored “1-species solution” may
well turn out to be the best treatment at some point in the future when more evidence
is available. However, with the current evidence at hand, I believe that the
4-species solution would make more sense within the framework of the Biological
Species Concept, for reasons expounded in the proposal.
“In his interpretation of my proposal, Penhallurick has
misunderstood a number of important points and missed the significance of
others. He dwells on particulars of a scientific debate carried out in the
journal Emu in 2004/05 (Penhallurick and Wink 2004; Rheindt and Austin 2005)
that – in my opinion – has only marginal relevance to the current proposal,
resulting in the mix-up of a number of unrelated issues. For instance, Burg and
Croxall’s (2004) incidental finding of 5% control region divergence is not the
reason why my proposal cites this study as supporting BSC species status of
Wandering taxa. Rather, the phylogenetic structure these authors found among
Wandering taxa is used in conjunction with ecological observations (range
sympatry) to advance this case.
“I do wish to offer a clarification on four central
points brought forth by Penhallurick.
“(1) Penhallurick asks SACC members to
disregard some of the most pertinent research carried out on Wandering
Albatross systematics because the authors phrased their results under a
different species concept. I believe we should not throw out these detailed
studies on Wandering Albatross phylogenetic structure only because their
authors opt to describe their findings in terms of “ESUs” rather than
biological species. Despite Penhallurick’s concern, SACC members have the
ability of re-interpreting those results under their own species concept.
“(2) Similarly, Penhallurick is confused about which
species concept underlies the present proposal. In line with SACC’s adoption of
the multi-dimensional BSC, my proposal followed the other 387 SACC proposals in
utilizing this species concept. This is obvious by mention of such terms as
“essential allopatry”, which would be immaterial to a debate within the
confines of most other species concepts widely used in ornithology.
(3) Penhallurick states that I write “approvingly” of
Robertson and Nunn (1998) and Burg and Croxall (2004). Apart from being
irrelevant, this is not true. In fact, if anything, I wrote disapprovingly of
Robertson and Nunn’s (1998) “controversial book chapter”. Penhallurick then
goes into a lengthy discussion on how the conservation community has welcomed
or pushed the treatment of Wandering taxa as separate species. Here again, I
fail to see the relevance to the current SACC discussion. Just as conservation
concerns should not motivate a split in albatross taxa, the illegitimacy of
this interference should not be used as an argument to motivate a lump.
“(4) Most significantly, I take issue with
Penhallurick’s portrayal of genetic introgression in albatrosses as an
“…implausible…” and “…lengthy process of hybridization of which there is no
evidence whatsoever…” Introgression rather than conspecificity as a cause of
near-zero mtDNA divergences among Wandering taxa is not just a theoretical
exercise, but also a plausible scenario. The following three points
are meant to illustrate that genetic introgression is not a marginal process,
but an all-encompassing phenomenon:
“a. MtDNA introgression is
pervasive in the biological world and greatly diminishes the utility of low
mtDNA divergences as a true yardstick of taxon divergence. (Note that high
divergences are less gravely affected). Judging by the inflationary number of
studies reporting on introgression, it seems to occur in most animal species in
one form or the other. In birds alone, patterns of genetic introgression have
been detected across the whole taxonomic spectrum, from passerines to
Galloanseres. A small number of example studies include the following (full
citation not provided): Gill 1997; Brumfield et al. 2001; Helbig et al. 2001,
2005; Rohwer et al. 2001; Bensch et al. 2002; Sætre et al. 2003;
Lovette 2004; Kulikova et al. 2004; Mank et al. 2004; Shapiro et al. 2004;
Grant et al. 2004; Dabrowski et al. 2005; Borge et al. 2005; Secondi et al.
2006; Kvist and Rytkönen 2006; Vallender et al. 2007; Peters et al.
2007; Martínez-Cruz and Godoy 2007; Rheindt et al. 2009; Carling and Brumfield
2008, 2009; Gay et al. 2008.
“b. As pointed out in the
original proposal, mtDNA introgression can affect all/most members of entire
radiations, such as Anas ducks (Johnson and Sorenson 1999,
Peters et al. 2007) and Larus gulls (Liebers et al. 2004).
Plumage differences between various Larus gulls are arguably
smaller than between an adult male Snowy Albatross (D. exulans) and his
neotenous cousin from the north (e.g. D. amsterdamensis). While
introgression is widely accepted as the cause for near-zero mtDNA divergences
in Larus, why should it not be plausible in Diomedea?
If we were to subscribe to Penhallurick’s “divergence-only” approach, we would
also have to be prepared to challenge the biological species status of Greater
and Lesser Black-backed Gulls based on their near-zero mtDNA divergence
(Liebers et al. 2004).
“c. Penhallurick paints
genetic introgression as a long-term process requiring many generations, and
thus finds it to be an “implausible” phenomenon in albatrosses. Penhallurick
errs on two accounts. Firstly, genetic introgression can be extremely fast. For
an avian example, take Mank et al.’s (2004; Conservation Genetics 5) research
showing how Mottled Duck and Mallard microsatellites went from distinct to
almost identical within only 58 years. Secondly, Penhallurick’s statement
belies the vast time scales of the evolutionary process. Why – in the last tens
of thousands of years – could there not have been, say, a climate-induced
500-year period (or repeated episodes of such periods) during which exulans expanded
into the ranges of the other Wandering taxa and occasionally hybridized with
them, leading to introgression from one taxon into the other and a “re-setting”
of mtDNA divergence to zero… There is no reason to presume introgression in
Wandering Albatrosses must have happened fast and now.
“Based on these considerations, I re-iterate my view
that near-zero mtDNA divergences in Wandering Albatross taxa may not be too
informative to this taxonomic debate, and that other lines of enquiry (e.g.
their essentially sympatric occurrence around New Zealand) may provide more
information on their BSC status.
Comments from Stiles: “YES.
I think that the 4-species treatment is the best way to express what we know
about these birds, and I think that Rheindt has satisfactorily answered the
objections of Penhallurick.”
Additional comments from Penhallurick: “Some
final comments on Rheindt’s Proposal. If we consider Rheindt’s
proposal, and ignore the appeals to irrelevant papers, the core of his proposal
comes down to two statements of “possibilities”. He states that
introgression “may” explain the low DNA distances. He offers no
actual evidence that this has occurred. And he needs to explain not
just how introgression occurred between two Wandering Albatross taxa but
between all of them. This beggars the imagination. Secondly,
we are invited to assume that because a small number of exulans are
present on Macquarie Island, this represents breeding isolation between that
taxon and taxa on Subantarctic Islands some 700 km away. Think about this! It
would be laughable in any serious discussion. Again, Rheindt
presents no evidence that this most unlikely convergence ever
occurred. I thought science was about evidence. And
Rheindt has presented none!”
Additional comments from Rheindt: Please see Liebers et al.
(2004; Proc. R. Soc. Lond. B) for a well-documented example of a species swarm
of approximately a dozen BSC species of Larus gull that all share
near-identical mtDNA, presumably as a result of introgression. Similar patterns
(but with less comprehensive documentation) have been detected in Anas duck
mtDNA - see previous contribution. It is questionable why such a pattern should
‘...beggar imagination...’ in albatrosses."
Comments from John Croxall (12 Jan. 2010): “I was
recently informed of the existence of this proposal and although I would not
normally get involved in such issues, I felt that the SACC might find a few
comments useful to help it reach a decision. (For the record: (a) I
have undertaken research on albatrosses and petrels for some 30 years to
my retirement in 2006; (b) I am not a taxonomist; such work on albatrosses that
I have co-published were by-products of studies on population genetics and
parentage largely conducted by Theresa Burg; (c) I have never met, or
refereed papers by, Rheindt or Penhallurick!).
Additional published material
“There are at least 4 supplementary sources of
information that are relevant to your deliberations:
“1. The very
recent paper (despite its June 2009 date, the issue only appeared in November)
by Chambers et al. (2009) Phylogenetic analysis of the 24 named albatross taxa
based on full mitochondrial cytochrome b DNA sequences. Notornis 56:
82-94. To me, on a quick perusal (and despite its abundant
typographic errors), this provides a good and pragmatic overview of many of the
issues, not least those involved in considering the approach and conclusions
propounded by Penhallurick and Wink (2004). While the paper does not
consider relevant biological (especially ecological) information (see
below), I believe the essence of its conclusions in respect to the taxa
relating to your proposal are entirely realistic and would support the proposal
for splitting. I attach a copy of the paper.
“2. The paper by Techow et al. (2010) Speciation and
phylogeography of giant petrels Macronectes. Molecular Phylogenetics
and Evolution 54: 472-487, as this has considerable bearing on
the issue of cytochrome b sequence divergence (see below). I
attach a copy.
“3. The publications of the Taxonomic Working Group of
the Agreement on the Conservation of Albatrosses & Petrels (ACAP), which
has reviewed several of the Diomedea issues relevant to your
proposal, specifically Diomedea antipodensis and gibsoni at
its 2006 meeting and D. exulans and D. amsterdamensis at
the 2008 meeting. They have not yet reviewed D. exulans/D.
dabennena. However, given the principles and precedents involved
and that Burg and Croxall (2004) found there was more genetic distinction
between dabennena and exulans (sensu
stricto) than between exulans and antipodensis/gibsoni,
it would seem unlikely that the ACAP Taxonomic Working Group would not support
this split (it is the existing ACAP position). I attach the
documents (AC2, AC3, AC4) from
to the relevant meetings of this Working Group; these are available publicly
through the ACAP website. I am not a member of this Taxonomic
Working Group but its discussions are relevant
to BirdLife International (see below), for which I am the ACAP
representative to its Advisory Committee and Meeting of Parties.
“4. In respect of Diomedea dabennena, the
publication by Cuthbert et al. (2003) Separating the Tristan albatross and the
wandering albatross using morphometric measurements. Waterbirds 26:
338-344, is also relevant. Tristan albatross, although showing reasonable
genetic divergence, is not easy to distinguish in the field from D. exulans,
without considerable experience of age and sex-related plumage patterns of the
latter. In essence, their ranges overlap at sea only in the
wintering grounds, particularly in the Brazilian and Benguela Current systems
where Tristan albatross may co-occur with D. exulans from
South Georgia towards the northern limits of the latter’s wintering range.
There are numerous recent observations and uplinks from tracking studies
confirming the regular occurrence of Tristan albatross in the SACC area.
“5. SACC also raises the issue of D. amsterdamensis,
material of which was unavailable to Burg and Croxall (2004); some relevant
data were provided in Milot et al. (2007) Proc. Roy. Soc. Lond. Series B 274:
1779-1787 and I understand there is a paper forthcoming which summarises all
data relevant to its distinctiveness at the species level. However,
this species is, to date, unrecorded for the SACC area (indeed it has quite a
restricted (at all seasons) main distribution at sea in the Indian Ocean).
Comments on the proposal to SACC
Background
“1. The statement (New Information para 1) that “despite
widespread criticism … popular bird books” is incorrect. First,
while Penhallurick and Wink (2004) – on rather tendentious grounds – and
Christidis & Boles (2008) – on grounds which may equally reflect lack of
any real experience of the taxa involved (and both representing at most
personal/ regional perspectives on this complex)- were critical of the adoption
of the Diomedea “splits”, the vast majority of the scientific community
has accepted them, as evidenced by references in the reports of the ACAP
Taxonomic Working Group. Second, this acceptance extends to recent
monographic treatments, e.g. Tickell (2000); Brooke (2004); Onley and Scofield
(2007). The authors of these works would be somewhat dismayed to be
regarded as non-scientists! Tickell was
a pioneer researcher on albatrosses as long ago as 1958; Brooke has published
for over 20 years on avian ecology, especially with respect to seabirds,
including describing new procellariiform taxa; Scofield is a leading New
Zealand museum-based researcher with wide field experience of albatrosses and
petrels. Thus, all recent global reviews have chosen to maintain
most of the splits in Diomedea taxa that are the subject of
your proposal.
“2. The BirdLife International position is as follows. As the authority for the IUCN Red
List, BirdLife maintains a Taxonomic Working Group (BTWG). For regions with authoritative
checklist/classification committees, these are very closely followed
by BirdLife. However, for taxonomic groups of more global
distribution, BirdLife prefers to use the latest authoritative global
review. For Procellariiformes, the
default authority is Brooke (2004), with updates as determined by BTWG in its
annual review process. For albatrosses, however, BirdLife currently follows the
advice of the ACAP Taxonomic Working Group, regarding this as the most appropriate taxonomic
authority for the species covered by this Agreement.
Sequence Divergence
“1. It is increasingly recognised that, compared with
most avian taxa, Diomedeidae, probably Procellariidae and possibly
Procellariiformes, show unusually low levels of sequence divergence even
between well-established species.
“2. This topic is reviewed and discussed for albatrosses
by Milot et al. (2007). The difficulty, of course, is how to compare
distances between taxa that are mainly (indeed entirely for all problematic
cases) allopatric, given the limited guidance available from congeneric
sympatric taxa. For me, there are two main guidelines here. First, Black-browed and Campbell
Albatross, which now breed sympatrically at Campbell Island, are separated by
0.8%. Second, the two giant petrels are
separated by about 0.4%. The latter is quite an important result
because we know from extensive (multi-year of banded individuals) field studies
of these cryptic sibling species that hybridisation is almost non-existent (the
few cases are invariably Southern males with Northern females), especially
noteworthy considering that the loose breeding aggregations of both species
often overlap spatially, that the observable discriminating morphological
characteristics are essentially only in bill colour and that their annual
cycles are only staggered temporally by some 5-6 weeks. Everyone who has worked in the field with
these two species where they breed sympatrically recognises the correctness of
their discrimination by Bourne and Warham (1966) as distinct species. It is remarkable that Penhallurick and Wink
(2004) chose to ignore the wealth of biological and ecological data on these
taxa – literally a dozen or more publications whereby species distinctiveness
had not only never been questioned but invariably clearly substantiated- in
favour of applying some arbitrary genetic distance standard.
“Even recognising that Macronectes is in a
different family of the Order, it nevertheless has many biological and
ecological similarities to albatrosses (diurnal, surface breeders with vocal
and plumage characteristics highly conserved), and emphasises that
procellariiform taxa which may look almost identical to us and which have very
low cytochrome b divergence, may still behave as perfectly good
biological species.
“This is not the place to rehearse the arguments for the
taxonomic status of the Diomedea and Thalassarche taxa, perhaps
beyond recognising that there are probably three difficult cases, for most of
which more data would be useful:
“(a) Diomedea
antipodensis/gibsoni, discussed in some detail by Chambers et al (2009),
where the ACAP TWG decision (in AC2 paper) was to retain as subspecies,
the identical cytochrome b sequences and limited
microsatellite differences finding more favour than the plumage differences at
most ages and the very distinct foraging areas and migrations outside the
breeding season (the former taxon occurring regularly (annually on migration)
in the SACC area; the latter mainly restricted to the Tasman Sea when not
breeding)).
“(b) D.
epomophora/sanfordi (both of which occur in the SACC region), whose
distinctive plumages render them diagnosable at almost all ages and stages, yet
cytochrome b differences are very low (0.08%) and hybridisation does
occur (albeit at the not entirely “natural” site of Taiaroa Head). The ACAP TWG
addressed this species pair in its AC4 paper and maintained full species status
for both. [For the record, based on my experience with Thalassarche
melanophrys and T. chrysostoma, hybridisation events
can occasionally take place between species which are as different as these
two, if there are mixed colonies with substantially disproportionate
numbers of the two species involved. In Diomedea, the
relatively high frequency of extra-pair copulations, including forced
copulations, may also lead to hybrid pairs at sites where individuals of one
species are sometimes attracted to breeding sites populated by another
species].
“(c) Thalassarche
cauta and T. steadi (the latter occurring in the SACC
region) which currently lack 100% reliable morphometric or plumage diagnostics
for all ages and stages (but bill colour allows discrimination in almost all
cases and breeding seasons differ by about 8 weeks) and have cytochrome b distances
of about 0.2%. However, these two taxa have been the subject of a
dedicated phylogeographic PhD thesis and the ACAP Taxonomic Working
Group (in its AC3 paper) reached a unanimous decision based on the
published papers there from; consequently, BirdLife has followed this
decision.
“I do not wish to extend these comments to address issues
raised by Penhallurick. However, I would simply observe that,
whatever the merits of the higher order taxonomic and nomenclatural
modifications suggested in the Penhallurick and Wink (2004) paper, over 100
albatross and petrel scientists, meeting at the Fourth International Albatross
and Petrel Conference in Uruguay in 2004, were unanimous in agreeing that most,
if not all, of the conclusions relating to the species status of albatrosses,
giant petrels, and prions were in direct disagreement with the experience of
those scientists who had worked most extensively with these species in the
field. It is evident that the
Penhallurick and Wink (2004) conclusions disregarded the substantial body of
biological and ecological information available on the distinctiveness of most
of the taxa in the above groups, where modern data on genetics, vocalisations,
ecology, core foraging areas etc. are demonstrating the distinctiveness of
these mainly allopatric taxa in ways consistent with their recognition at
species level under all of the currently accepted concepts.”
Additional comments from Robbins: “Given
Rheindt and Croxall’s comments, I see no reason to change my original vote of
supporting recognition of four species.”
Additional comments from Stiles: “Here,
I merely reiterate my YES vote, especially in view of Croxall’s reply to
Penhallurick’s latest salvo. The fact
that a group of world experts on the albatrosses has collectively supported
species status for these forms is not to be lightly dismissed. As a definite non-expert I am strongly
inclined to accept their verdict.”
Comments from Schulenberg: “YES. As several have noted, this case is a tough
nut to crack, as the biological species concept is poorly suited to treat
essentially allopatric taxa, and other taxonomies are reasonable. All that
said, similar as all these taxa are, I am impressed by the differences among
them, both in terms of genetic structure between populations, and in terms of
trends towards neoteny in plumages (correlated with latitude). Therefore, I
think that recognizing four species (including the extralimital amsterdamensis)
is the best approach. Also, while fully aware of the distance between Macquarie
Island (breeding site for exulans) and Campbell and Auckland islands
(breeding sites for antipodensis/gibsoni), I'm more impressed by
the relative proximity of these sites. Low genetic distances notwithstanding,
the morphological and ecological differences point to me towards recognizing
these taxa as species.
“The question of English names is not, to my
knowledge, before us. But if SACC accepts the split, then I foresee issues with
English names. The name "Wandering Albatross" has long standing, and
maybe there will be resistance to changing it. But the name "Wandering
Albatross" would prove useful for (the great many) individuals of the
complex (sensu lato) that might not be identifiable in the field. In turn, a
different English name would be called for to use for Diomedea exulans (sensu
stricto). Onley and Scofield (2007) use "Snowy Albatross" for exulans.
I don't think that this has been followed by other authors, but ... they may be
on to something.”
Comments from Remsen: “NO. My
understanding of these albatrosses is that they will breed in subadult plumages
with fully adult-plumaged individuals. If
that is incorrect, please let me know. If
this is true, then the neotenic plumage differences among island populations
seem unlikely to act as any barrier to gene flow, consistent with the low
degrees of genetic divergence. The
correlation with latitude suggests an ecological response among the populations
rather than any intrinsic biological difference that indicates that they are
lineages that have reached levels of divergence associated with species rank in
other birds. As for differences among
island populations in timing of breeding, migration routes, and wintering
areas, such differences occur among island populations of many seabirds that no
one would consider to consist of multiple species, and are therefore not really
persuasive on their own. To a
non-seabird biologist such as myself, all I see is discrete geographic
variation in plumage characters correlated with an ecological variable. Vocal differences are alluded to, but I would
like to see published data on this. Seabird
biologists working with shearwaters have been tuned in to vocal differences and
their importance for some time, but I am not aware of a parallel emphasis in
albatrosses – if this only reveals my ignorance, someone please correct me.
“Having discussed species limits with a number
of seabird biologists, they have openly lobbied me for species rank for
population because that would
increase their status in terms of conservation.
Thus, their taxonomy has an agenda, driven by politics, and this arouses
my suspicions. I do not want to accuse
any of the 100 albatross and petrel scientists (mentioned by Croxall) of such
non-scientific, subjective reasoning, but I am concerned that such reasoning
may enter their decision of endorsement of narrower species limits, if only
subconsciously. I’d also like to know
how many of them have training in systematics rather than just ecology. Such comments will undoubtedly insult this
active and extensive community of researchers, but I only mean to provoke
production of the sort of data that will fortify these taxonomic decisions …
particularly in this case data on actual isolating mechanisms (voice and
display?). Finally, I want to emphasize that my vote on this has nothing to do
with degree of genetic (mtDNA) differentiation.”
Comments from Cadena: “[NO].
I have remained on the sideline
regarding this proposal because I know close to nothing about the biology of
these birds and wanted to have comments from most committee members and others,
hoping they would illustrate me. I am
actually uncertain as to how to vote, so hopefully the following comments will
stimulate some additional discussion that may finally lead us to reach a
decision soon. What I see here is that much of the Rheindt vs. Penhallurick
discussion boils down to a rather simple issue: Rheindt is only saying that
there are various reasons why low (or no) mtDNA differentiation need not imply
conspecificity and that because of those reasons one ought to look at other
sources of data to decide how to rank all these forms. I have to say I agree
with Rheindt on this 100%. Then, what else do we have? I am not certain about
all the details, but as Van puts it, the strongest evidence for splitting these
forms are differences in plumage and, based on his first remark, plumage
variation is unlikely to be a barrier to gene flow (right?). To me, differences
in timing of breeding are persuasive arguments for species status for sympatric
populations, but not for populations existing in allopatry that may be tracking
changes in e.g. resource availability and lack fixed genetic differences in
genes controlling breeding behavior, such that they would mate if they were to
come into contact (e.g. Ecuadorian populations of Zonotrichia capensis separated
by 25 km differ drastically in breeding seasons as a result of climatic
differences between sites, but nobody seems to have claimed these should be
considered different species). Alvaro mentioned differences in water
temperature between sites as a possible isolating factor, but this to me seems
like a difference in the environment, not a difference in the organisms, so
using it as an indication of reproductive isolation (following the BSC) appears
problematic as essentially all biological species show some ecological
discontinuities in their ranges and comprise populations occupying ecologically
different environments (take again the Zonotrichia case, with
populations occurring from sea level to very high-elevation areas). Is there
anything else? If not, I think my vote would lean towards NO. I realize this
might challenge the opinion of albatross experts mentioned in the proposal, but
if these experts were not weighting the evidence for reproductive isolation
following the criteria we try to follow here, then I would be fine with
reaching a different conclusion.”