Revised Proposal (589) to South American Classification Committee
Split Epinecrophylla
haematonota into four species
Effect on SACC: If adopted, three
species would be added to the South American checklist by splitting Epinecrophylla haematonota into four
species as recommended by Whitney, Isler, Bravo, Aristizábal, Schunck,
Silveira, and Piacentini (2013). Following a comment to the original proposal
and the ensuing discussion amended herein, this revision is split into two
parts for the committee's consideration as follows:
A. E. amazonica (Ihering, 1904), E.
haematonota (Sclater, 1857), E.
pyrrhonota (Sclater and Salvin, 1873),
and
B. the newly described E. dentei.
Background: The Stipple-throated
Antwren is a widespread denizen of western Amazonia, occurring both south and
north of the Amazon. During survey work in the Aripuanã-Machado interfluvium,
Amazonas, Brazil, in 2000-2003, Bret Whitney noted that the vocalizations of E. haematonota antwrens were audibly
distinct from those on the opposite side (left bank) of the Rio Madeira.
Newly
Published information
A.
To provide a foundation for evaluating the taxonomic status of the
Aripuanã-Machado population, molecular and vocal analysis of currently
recognized subspecies of E. haematonota was undertaken,
Maximum-likelihood and Bayesian analyses of mtDNA showed that the
Aripuanã-Machado population was
embedded within a large well-supported clade containing four distinctive
lineages comprising taxa currently known as E.
spodionota, E. h. haematonota
(including E. fjeldsaai), E. h. pyrrhonota, and a fourth lineage
including E. h. amazonica and the
Aripuanã-Machado population. The relationships among the four lineages are not
well resolved, and they are ~5–6 % divergent. E. spodionota has previously been recognized as a distinct species,
and differences in loudsong pace support the acknowledgement of the remaining
lineages as distinct species. The slowest paced loudsongs are delivered by amazonica, the fastest by nominate haematonota and pyrrhonota, and the pace of the loudsong of the Aripuanã-Machado
population is intermediate. All pace
comparisons were significant statistically except for between h. haematonota and pyrrhonota. The latter two taxa, however, are distinguished
morphologically, especially as the female plumage of pyrrhonota is most distinct in the complex. Given vocal and
morphological differences, the extent of genetic diversity among the lineages
and the inability to resolve their relationships, even though not a direct
basis for species consideration, indicates that the evolution of the four clades,
spodionota, pyrrhonota, haematonota,
and the clade containing amazonica
and the Aripuanã-Machado population has proceeded to the species level.
B.
The phylogeny showed that the Aripuanã-Machado population was sister to E. h. amazonica, its neighbor to the
west on the opposite bank of the Rio Madeira. Differences in vocalizations and
morphology support its description as a new species. The new species, E. dentei, differs vocally by the
significantly faster pace of its loudsong and by a diagnosable distinction in
note shape which produces loudsongs of a subtlety different quality to the
human ear. Adult females of dentei
are readily distinguished from those of amazonica
by color of the throat and of the belly. Maximum-likelihood and Bayesian
analysis showed that dentei and amazonica were ~3% divergent. Phenotypic
differences of vocalizations and plumage supported by genetic results meet
previously established guidelines for species consideration in thamnophilids in
parapatry (Isler et al. 1998).
Recommendation: I recommend a
"YES" vote on accepting all four species, including Epinecrophylla dentei, in the list,
based on morphology, vocalizations, and genetic distinctions. The status of fjeldsaai is considered in a separate
recommendation.
Literature
cited:
Isler, M. L., P. R.
Isler, and B. M. Whitney. 1998. Use of vocalizations to establish species
limits in antbirds (Passeriformes; Thamnophilidae). Auk 115:577–590.
Whitney, B. M., M. L.
Isler, G. A. Bravo, N. Aristizábal, F. Schunck, L. F. Silveira, and V. de Q.
Piacentini. 2013. A new species of Epinecrophylla
antwren from the Aripuanã-Machado interfluvium in central Amazonian Brazil with
revision of the “stipple-throated antwren” complex. In: del Hoyo, J., Elliot, A., Sargatal, J., & Christie, D.A.
(Eds.), Handbook of the Birds of the
World. Special Volume: New Species
and Global Index. Lynx Edicions, Barcelona, Spain, pp. 263–267.
Morton Isler,
November 2013
______________________________________________________________________________________________
Further comments:
Comments
from Thomas Donegan: Our team who works on the Colombian checklist is presently
considering the various HBW splits and new species, such as this. Proposal 589 refers to splitting E. haematonota into 4 species, i.e.
treating pyrrhonota, dentei and amazonica each as species when they were previously considered
subspecies or undescribed. I had some
queries with the vocal data supporting this approach which have been discussed
offline with Mort Isler and Bret Whitney, and we agreed to include an edited
version of this discussion here:
At the
outset, I should note great appreciation for the work that Bret Whitney and
colleagues put into getting all these Amazonian species "out there"
in such an informative volume; and in particular for this interesting paper on
ex-Myrmotherulas. I apologise for what may be perceived as a
negative tone of commentary. One of the most depressing things about
publication is the (generally only) negative feedback one tends to receive in
return. To redress that here:
congratulations for such a mammoth and impressive effort and piece of work,
which will surely put the taxonomy of Amazonian birds on a surer footing; and
in particular for a very interesting review of these antwrens. I would though raise the following issues on
this proposal:
1. The only claimed differences in
voice between the four proposed species in this group are in song speed. The populations postulated for species rank (haematonota, pyrrhonota, amazonica and
dentei) are claimed to differ from
one another "significantly" in song speed (except pyrrhonota vs. haematonota). However, the
wording used is confusing: “Isler et al. (1998, 2007)” (who published a test of
diagnosability) are cited in the introduction to the section, as a test that
two species “differed significantly”. Then when discussing song speed, the paper
states that the “average pace of the
four populations differ significantly”. This wording suggests usage of a Student's t-test or similar (tests of statistical
significance) rather than diagnosability.
The authors cited only means for a single variable, with no standard
deviation data or information about upper and lower bounds of this variable
presented and no information about other variables, so it is not possible to
work out whether diagnosis is likely.
Whitney et al. (2013) did not state any other quantitative vocal
differences (except near-diagnostic note interval length differences between amazonica and dentei). Subjective differences in note shape are also cited but
were considered diagnostic only “almost” (i.e. not entirely?) perfectly.
2. If the single variable cited is
diagnostic between some populations, this level of differentiation falls below
that recommended for diagnosing antbird species – where three diagnosable differences (not a single one) in variables for calls or songs is the usual benchmark
for sympatric species (Isler et al. 1998).
(Calls were not studied here.)
3. Any splitting then relies
heavily on molecular data. The molecular
study concludes impressive (>5%) differentiation between various groups in a
polytomy: spodionota; amazonica+dentei; haematonota+fjeldsaai; and pyrrhonota. However, splitting based on molecular
data does not adopt a minimalistic approach to resolving the polytomy, because dentei groups with vocally similar amazonica and is not in any separate
part of the polytomy but is proposed here for species rank.
There is
then a highly favourable factor towards most of the splits advocated in this
paper and proposal, which is almost entirely overlooked. Two members of the polytomy, spodionota and pyrrhonota, are fully sympatric in the East Andes of Colombia. Salaman et al. (2002) noted as follows:
"Myrmotherula spodionota, FOOTHILL ANTWREN: Ten birds were caught
(one collected) in both primary and secondary growth at Alto Río Hornoyaco;
five were captured and collected at Fragua (1000-1400 m); one female and 3
males were caught and collected at 1000-1460 m on the Río Rumiyaco. These are
the first specimen records from Colombia; Willis (1988) reported sightings at
El Paraíso, Dpto Huila in Apr 1962. The species is otherwise known from the
Andean East Slope of Ecuador and Peru from 600-1300 m (Hilty & Brown 1986).
Interestingly, extensive data from Ecuador indicate an elevational segregation
of M. spodionota from its close relative, the Stipple-throated Antwren M.
haematonota (Krabbe et al. 1999). However, both were captured in the same
mist-nets at 1100 m at Alto Río Hornoyaco although they were not observed
foraging together."
As part of
the team that captured and processed these two species following simultaneous
capture in the same mist-net, I can confirm the accuracy of the notes in this
paper! Interestingly, some Colombian
East slope specimens referred to by Salaman et al. (2002) from the contact zone
were among those sampled for mtDNA by Whitney et al. (2013). Consistent with observations at sites of
sympatry and a lack of noted intergradation in the above study, the molecular
differentiation between these forms was supported. (E.
spodionota is already recognised as a separate species by the SACC.)
Lumping all
of members of the polytomy is not a viable proposition, due to spodionota and pyrrhonota being sympatric and demonstrably good species. The logical next step to analyse species
limits would be to determine vocal differentiation between the two sympatric
members of the polytomy, and compare these differences to pairwise differences between
other taxa in the polytomy. However, the
authors did not do this: no vocal data on spodionota
is included. We therefore do not know if
this polytomy shows atypically low vocal variation but in a way consistent with
the vocal variation between sympatric related antbirds.
Reading the
data as its stands, splitting the polytomy does not have basis in the vocal
data presented using the Isler et al. (1998) model. Splitting of the polytomy is, however,
supported by molecular results, assuming that recognising monophyletic species
is virtuous, because lumping sympatric spodionota
with haematonota is not viable. New taxon dentei
then emerges as a weaker candidate for species rank, as a result of it being
grouped with amazonica in molecular
data (and not an independent part of the polytomy), parapatric in its
distribution with respect to amazonica
(these replacing one another on different sides of an Amazonian river, a
typical subspecies distribution pattern) and not demonstrating the level of
vocal variation from amazonica as is
demonstrated by sympatric antbirds.
I would
therefore like to propose splitting this proposal into Part A (splitting haematonota into three species: (haematonota, pyrrhonota, and amazonica), for which I see no
reasonable alternative even based on the limited vocal data in Whitney et al.
(2013), due to the molecular data and sympatry between two forms in the
polytomy and the similar divergence of all of them. Part B (splitting dentei from amazonica)
should be considered separately and does not seem at all clear-cut based on the
data that are currently available.
Additional literature
cited:
Isler, M. L., P. R.
Isler, and B. M. Whitney. 1998. Use of vocalizations to establish species
limits in antbirds (Passeriformes; Thamnophilidae). Auk 115:577–590.
Salaman PGW, Stiles FG, Bohórquez CI, Alvarez M, Umaña AM, Donegan TM
& Cuervo AM. 2002. New
and noteworthy records from the east slope of the Andes of Colombia. Caldasia
24(1): 157-189.”
Comments from Bret
Whitney:
“I just read [the comments above] and it makes a lot of sense to look into each
of the arguments raised. E. dentei is not a strongly
differentiated species, it's a weakly differentiated species. It shows weak diagnosability morphologically
and vocally (note structure being "almost" diagnostic means one
sample failed perfect taxon allocation), genetic divergence is not huge, and it
possesses some ecological characteristics that appear to be unique, but the
fact remains that the population was well-sampled (relative to many other
phylogeographic studies) and shows near-perfect consistency in all of the above
character sets throughout its range. As
explained in the paper, one taxonomic treatment option would be to recognize haematonota, spodionota, pyrrhonota, and
amazonica as species with dentei as a subspecies of amazonica. If the committees decide that's the way to
go, so be it, you will get no further explanation from me. That said, I continue to believe that the
best course, the one most indicative of speciation in this group of birds, be
it of long-standing or relatively incipient, is to call them all separate
species. It is not possible to make a
truly strong case for either species or subspecies rank in this case.
Comments from Mort
Isler: “As the author who was responsible for the
vocal analysis recommending that dentei
be considered distinct at the species level, I will respond to Thomas Donegan's
comments. Before I do, let me say that I thought Donegan's comments to be well
thought out and considered, and I greatly appreciate the time and energy that
they involved. It is great to have a community of individuals, like Thomas and
SACC members, who carefully examine species-level recommendations.
In response to Donegan
comment 1, I can confirm that tests of diagnosability were performed on the
data. Unfortunately, space limitations of the HBW volume did not allow the
inclusion of the description of the methodology employed nor the results of the
test as we have done in all of our previous papers. Pace, a ratio, is not
normally distributed, and consequently our test (using the t distribution) for
likelihood of overlap with larger samples could not be employed. The
statistical test employed was a non-parametric bootstrap simulation (see Isler
and Whitney 2011, p. 4 for more description).
The Difference Between Means (DBM) of dentei and amazonica
resulting from this test was five standard deviations, which is well above an
acceptable level for considering the difference to be diagnostic. Results of
other pairwise comparisons of taxa in the group were diagnostic at a similar
level except for between pyrrhonota
and haematonota as noted in the
paper.
In response to Donegan
comments 2 and 3, the following recommendation in Isler et al. 1998 (p. 586) is
sometimes overlooked: "However, three diagnosable differences in vocal
characters, as defined herein, should be considered a point of reference, not a
requirement----for parapatric taxa, fewer than three diagnosable vocal
characters might be considered an appropriate threshold for species
recognition." With regard to dentei
and amazonica, a question can be
raised as to whether they are parapatric and gene flow between them is possible
or whether the rivers that appear to separate them geographically are a sufficient
barrier. The answer to that question is not known, but we do know that these
headwaters rivers provide a less formidable obstacle than those downstream; how
much of an obstacle is the issue. Other considerations supporting the
recommendation for species status include the almost perfect distinction in
note shape (see Whitney comments), ecological distinctions, and genetic
diversity. Although I agree with the Donegan comment on the last named, I think
it appropriate to keep genetic distance in mind when the decision is
borderline, as it is with the current example.
For all the reasons
expressed by Donegan and expanded above, when the paper was being written, I
struggled with the recommendation, and (obviously) came down on the side of a
species recommendation for dentei). But Bret Whitney, in his response, put it
perfectly: although dentei is a
clearly differentiated population, arguments can be made for either species or
subspecies rank; and although we came down on the species side, and whatever
the committee decides will be acceptable.
On the second issue
(Part A in the Donegan statement) regarding haematonota,
pyrrhonota, and amazonica, I
would only add one observation. The
geographic pattern provided by loudsong pace is informative. The slower paced
loudsongs of amazonica are juxtaposed
in between the fastest paced loudsongs of haematonota
(and pyrrhonota) and the intermediate paced ones of dentei. This pattern clearly obviates the possibility of west to
east clinality, and although it is not directly relevant to the amazonica/dentei species rank issue, it
seems to add support that haematonota
and amazonica be considered
specifically distinct.
Additional literature
cited:
Isler, M. L., and B. M.
Whitney. 2011. Species limits in antbirds (Thamnophilidae): the Scale-backed
Antbird (Willisornis poecilinotus)
complex. Wilson Journal of Ornithology 123: 1–14.”
Additional
Comment from Thomas Donegan: As to falling back
to lack of gene flow, supported by c 3% mtDNA variation and good sampling, many
diagnostic subspecies could be subjected to this sort of argumentation. If
subspecies are to be a valid category based on diagnosability but small
differences, then one has to draw the line somewhere between those showing
smaller and larger differences. I have
found Isler et al.'s "point of reference" a good basis for this in
suboscine birds. E. dentei is
borderline in this respect, but falls the wrong side of the standard
suggested. I am not particularly trying
to push subspecies treatment versus species as cases like this end up being
pretty subjective, but as the other proposed splits within the proposal are
much more certain, I do feel they should at least better be unbundled in this
committee process.
Additional
Comment from Bret Whitney: The yardstick
suggested by Isler et al. 1998 continues to be a conservative standard, but as
Mort pointed out, we never imagined that it would become a requirement, and we
included statements to that effect. To
the contrary, we knew full well that some well-differentiated, universally
recognized groups with very simple vocalizations (e.g. Grallaricula
flavirostris complex) were definitely not going to display three diagnostic
vocal characters. In Hypocnemis,
we documented fairly extensive syntopy of subflava and peruviana
in Brazil and Peru, but there is only one diagnostic character separating the
vocal repertoires of these birds (that fact will no doubt come into play in the
SACC proposal dealing with newly described H. rondoni).”
Additional Comment from
Mort Isler: I hesitate to extend the discussion further,
but I think it should be emphasized that the three-character yardstick
continues to provide a valuable insight into whether the vocalizations of
allopatric thamnophilid populations have diverged sufficiently to facilitate
reproductive isolation. After many years of use, the consistency of results
derived from its use with the results of molecular studies is especially
informative. But it remains a yardstick, to be used in conjunction with other
considerations.
______________________________________________________________________________________________
Comments from Zimmer: “YES on both
parts. I would concur that E. dentei is weakly differentiated from E. amazonica, and that it really comes
down to a judgment call as to whether to consider them as species or
subspecies. However, given the
distribution of the two taxa across the Madeira, and given the stronger case
for species treatment of the other taxa in the complex, I think it makes the
most biogeographic sense to treat dentei
and amazonica as species – it
certainly seems that they are on independent evolutionary trajectories, even if
that has not yet translated to more than weak vocal differentiation.”
Additional comments from Thomas Donegan:
“We have now published our treatments for the Colombia
checklist including on the various HBW splits for species that occur in
the country. On this species, we adopted Part A and needed to express no view
on Part B.
Stipple-throated
Antwren Epinecrophylla haematonota
"Negro
Stipple-throated Antwren" Epinecrophylla
pyrrhonota
“Whitney et al. (2013) have proposed treating E.
pyrrhonota, and others as species separate from E. haematonota based
on impressive molecular differentiation and some vocal and plumage
differences. Differences in loudsongs appear to fall a little below those
generally regarded as necessary for recognition of species in antbirds (Isler et
al. 1998, Remsen et al. 2013). Molecular results included
impressive (>5%) differentiation between various groups in a polytomy
comprising: spodionota, dentei+amazonica, haematonota+fjeldsaai
and pyrrhonota. Because spodionota and pyrrhonota are
fully sympatric in the East Andes of Colombia (Salaman et al. 2002) and because
specimens from the zone of sympatry were sampled in the molecular study,
lumping the polytomy is not a viable proposition. Proposed new species E.
(amazonica) dentei is a weaker candidate for species rank but extralimital
for Colombia so its status does not require consideration here.
Recognition of this split results in a change of the name for populations
occurring in Colombia from haematonota to pyrrhonota. Reference: Donegan, T.M., McMullan,
W.M, Quevedo, A. & Salaman, P. 2013. Revision of the status of bird species occurring or
reported in Colombia 2013. Conservacion Colombiana 19: 3-10. http://www.proaves.org/wp-content/uploads/2013/12/Checklist-Update-2013-Conservacion-Colombiana-19-3-10.pdf.”
Comments
from Robbins: “[YES on
A and B]. This is clearly a subjective
call as all parties acknowledge. For now, I’ll side with the majority in
recognizing these as species.”
Comments
from Pérez-Emán: “This is not an easy proposal to vote,
particularly Part B, as it could go either way based on available information.
I vote YES in Part A, based on molecular phylogenetic results (polytomy
including spodionota) and,
particularly, in this context, evidence of sympatry of spodionota and pyrrhonota.
For Part B, I agree with most of Thomas’ comments and, certainly, a subspecific
distinction for dentei seems the
appropriate decision. Differences between dentei
and amazonica are weak compared to
differences between other lineages within the group and are based on morphology
(mostly female plumage differences), vocalizations (faster pace of loudsong and
note structure, this last one representing a consistent difference except for
one sample) and genetic distance (3% genetic divergence from amazonica). Vocal differences are lower
than usually considered in species level differences (yardstick of three vocal
differences for allopatric populations) and genetic divergence is the lower
among these groups of lineages. Although these yardsticks (as well as the
commonly, even abused, 2% difference in genetic distance) have been useful to
evaluate species status in allopatric populations, instead of just phenotypic
differences in plumage, these are just reference thresholds to evaluate
population differences and are based on the need to use surrogate characters
for reproductive isolation. In the case of dentei
vs. amazonica, these populations are
parapatric and a large sample of the former, taken from throughout its
distribution and compared to other described taxa within haematonota, did not show any evidence of hybridization (and no
evidence of intermediates). Thus, based on what we know right now, in the case
of this weakly differentiated taxon, I would lean toward recognizing species
level of dentei voting YES for Part
B.”
Comments
from Remsen: “A. YES. What we know for certain is that spodionota and haematonota are syntopic without signs of gene flow and must be
treated as separate species under any criteria.
Therefore, we can extrapolate, for better or worse, from the differences
between these two as a yardstick for assigning taxon rank to other members of
the group, in terms of the potential significance of voice or plumage as
indicating that other members of the complex have diverged to the level
associated with known species-level differences. Thus, in combination with the polytomy in the
tree, treatment of pyrrhonota and amazonica is justified.
“B. NO. As widely acknowledged above, this one is
definitely borderline, and thanks to Thomas for catalyzing the subdivision of
this proposal. First, a rant on use of
genetic distance in assessing taxon rank in allopatric taxa. Genetic distance, in my opinion, is highly
over-rated and abused metric in assigning taxon rank at the
species-subspecies-population level, even in a comparative context. Why would relative degree of difference in
loci selected specifically for analysis because of their presumed neutrality be
interpreted as relevant to anything having to do with potential gene flow? This would depend entirely on the almost
certainly erroneous assumption that degree of difference in these loci is
somehow related to differences in those loci that are relevant to gene
flow. Why would that be the case for
neutral loci vs. loci potentially under strong selection? For parapatric taxa, however, genetic
distance IS critical in assigning taxon rank because as long as samples come
from adjacent populations, then any genetic distance at all indicates an
absence of gene flow. Now, for dentei.
Isolated from the rest of the group by major rivers, the Madeira and the
Amazon, it must be regarded as an allopatric taxon. Not known farther south than Brazil, to
contact amazonica in the headwaters
would require its presence into Bolivia as far SW perhaps as the Amazonian
foothills in Beni/La Paz, something like 1000 km SW of current southernmost
records … I really cannot see any chance
for true geographic contact between it and other members of the group, and
thus, in my view, genetic distance is irrelevant. Further, if genetic distance were used, dentei would fall squarely within the
levels shown by populations ranked as subspecies within tropical forest
undergrowth birds. Although only
intended as a guideline by Isler et al. (1998), the 3-character standard is
really the only thing we have to go on for dentei,
and therefore I think that it is best treated as a subspecies.”
Comments
from Cadena: “YES to A, based on
the rationale provided by Van, and NO to B.
I agree with
comments by Donegan and Van that dentei,
based on the available information, is best considered a subspecies of amazonica. I agree that the
three-character difference standard need not be required in all cases,
especially when taxa are in geographic contact. However, although the ranges of
dentei and amazonica appear parapatric, they are actually allopatric, separated
by a major river.”
Comments
from Jaramillo: “A –
Yes B – Much more difficult, but I will listed to those who are most intimate
with the issue, and although borderline, trust that their opinion that this is
a good species is the way to vote on this one. I think it is equivocal, and
admittedly a subjective call on how to go on this one.”
Comments from Pacheco: “An easy YES on A;
however, difficult to decide on B. Although the arguments of Donegan and Van
are appropriate, I recognize subjectivity in the decision and vote YES on B
believing that E. dentei have their
independent evolutionary path.”
Comments
from Stiles: “A.
definitely YES. B. a very difficult
borderline case; I prefer to be conservative on this one, and hope that some
playback experiments can be conducted to clinch the case with dentei one way or the other – so for
now, NO.”
Additional
comments from Pérez-Emán:
“Certainly, a difficult proposal. As you pointed out, if those taxa were
parapatric I would keep my vote. Considering them as allopatric, given the
current distribution, decision is based on the weight we should o not give to
yardsticks. The speciation process is seen as a continuous in nature, some taxa
well differentiated, others not, even when they are already isolated
reproductively. The problem is that the only thing we have to infer the process
is the use of character differentiation relative to sympatric taxa. I am not
completely convinced that three-character difference in vocalizations should be
a rigid one. However, this would create certain inconsistencies with previous
proposals. So, after this long chat, I would be willing to change my vote to NO
instead of YES, but just as a matter to be consistent with previous proposals.”