ZOOTAXA
ISSN 1175-5326 (print edition)
ISSN 1175-5334 (online edition)Copyright © 2015 Magnolia Press
Zootaxa 4032 (3): 251–263 www.mapress.com/zootaxa/
Article
http://dx.doi.org/10.11646/zootaxa.4032.3.1
http://zoobank.org/urn:lsid:zoobank.org:pub:14CEC95F-B541-4E89-A4C4-2F7306884DE7
Cryptic speciation in the Lesser Elaenia Elaenia chiriquensis
(Aves: Passeriformes: Tyrannidae)
FRANK E. RHEINDT1,4, NIELS KRABBE2, ALISON K.S. WEE1 & LES CHRISTIDIS3
1Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 1175432Zoological Museum, University of Copenhagen, Universitetsparken 15, DK-2100, Copenhagen, Denmark3National Marine Science Centre, Southern Cross University, Coffs Harbour, NSW Australia 24504Corresponding author. E-mail: [email protected]
Abstract
Tyrant-flycatchers (Tyrannidae) are a taxonomically confusing bird group containing a large degree of cryptic diversity
that has only recently begun to be unraveled through the application of acoustic and molecular methods. We investigated
all three subspecies of the Lesser Elaenia, Elaenia chiriquensis Lawrence, across their range using sound recordings as
well as nuclear and mitochondrial markers. We show that two of the three subspecies, the nominate race from southern
Central America and the widespread South American subspecies E. c. albivertex Pelzeln, have undergone very low levels
of vocal and molecular differentiation across their fragmented range. In contrast, the isolated taxon E. c. brachyptera Ber-
lepsch, endemic to the western and also, as recently shown, eastern slopes of the northern Andes, is phylogenetically and
vocally distinct from other Lesser Elaenias, indicating that it constitutes a separate biological species.
Key words: Neotropics, Elaeniinae, diversification, cryptic differentiation, bioacoustics, Andes, Panamá, vocalization,
mitochondrial DNA, nuclear DNA, Coopman’s Elaenia
Introduction
With 300–400 species in approximately 70 genera, the tyrant-flycatchers (Tyrannidae) are one of the richest bird
families worldwide, but equally one of the least understood in terms of taxonomy (Fitzpatrick 2004). With
generally inconspicuous plumage that often looks near-identical even across generic boundaries, many species
have evaded formal recognition until recently (Fitzpatrick 2004), and additional cryptic species continue to be
discovered (e.g. Coopmans & Krabbe 2000; Alonso & Whitney 2001; Johnson & Jones 2001; Zimmer et al. 2001;
Herzog et al. 2008). Moreover, new insights into the importance of vocalizations for species recognition (Alström
& Ranft 2003), especially in tyrannid flycatchers (Rheindt et al. 2008a), have revealed further tyrannid species
diversity (e.g. Lanyon 1978; Reynard et al. 1993; Zimmer & Whittaker 2000). The rapid advancement of
molecular methods in the field of phylogenetics over the past decade has also added to our knowledge of alpha
taxonomy in tyrant-flycatchers (García-Moreno et al. 1998; Chesser 2000; Johnson & Cicero 2002; Joseph et al.
2003a, b; Joseph & Wilke 2004; Rheindt et al. 2008a, b, c; 2009a, b; 2013).
The genus Elaenia is a fairly homogeneous group of tyrant-flycatchers comprising 18 currently recognized
species distributed mostly throughout drier and scrubbier parts of the Neotropics (Hosner 2004). The identification
of Elaenia flycatchers requires extreme care, as some species are challenging to distinguish even in the hand; this
has created widespread confusion over distributional boundaries, vocalizations and even species limits within the
genus (Zimmer 1941; Traylor 1982; Ridgely & Tudor 1994; Fitzpatrick 2004; Hosner 2004).
The Lesser Elaenia Elaenia chiriquensis is one of the most widespread members of the genus, occurring in
open country throughout much of the Neotropics (Figure 1). The three subspecies are distributed as follows:
nominate chiriquensis in Panama and Costa Rica; E. c. brachyptera in the border region between Ecuador and
Colombia on the west slope of the Andes in the Chocó Region; E. c. albivertex throughout much of tropical and
subtropical lowland South America, except for Amazonia (Figure 1). Recently a cis-Andean population tentatively
attributed to brachyptera has been documented (Moore et al. 2013).
Accepted by P. Rasmussen: 16 Sept. 2015; published: 16 Oct. 2015 251
The three subspecies of E. chiriquensis differ in the hues of their body colouration, with brachyptera
additionally being slightly smaller (Hosner 2004). Otherwise, they appear to differ little from one another. Within
widespread E. c. albivertex, Zimmer (1941) found no clear plumage distinctions in a series of over 240 specimens
from different parts of South America, and Bates et al. (2003) demonstrated comparatively low levels of
mitochondrial divergence (c. 0.25% cytochrome-b and 0.28% ND2) between populations from the savannahs of
Amapá, Brazil, in the Guianan Shield and the cerrado regions of Dpto. Santa Cruz, Bolivia. They concluded that
cerrado birds such as E. chiriquensis must have maintained higher levels of gene flow than Neotropical forest
understorey birds with similarly wide distributions, or that cerrado may have expanded to parts of its present-day
distribution fairly rapidly. Ridgely & Greenfield (2001) reported that the vocalizations of E. c. brachyptera differ
from those of widespread E. c. albivertex, suggesting that the former taxon may deserve to be elevated to species
rank.
As part of an on-going wider study on the evolutionary dynamics of the flycatcher genus Elaenia, we
generated nuclear and mitochondrial DNA sequences for all three subspecies from across their range. Additionally,
we analysed sound recordings of all three subspecies. We here present our molecular and vocal data on taxon
differentiation within E. chiriquensis and discuss their taxonomic implications.
FIGURE 1. Distribution map of the E. chiriquensis complex roughly following Hosner (2004) with minor modifications; red:
nominate subspecies (chiriquensis); blue: brachyptera; purple: albivertex; note that the eastern Andean population from the Río
Maranon drainage of southern Ecuador into Peru is here shown to belong to albivertex.
Material and methods
Molecular sampling regime. We generated full-length sequences of the mitochondrial gene NADH
dehydrogenase subunit 2 (ND2) for five samples of E. c. albivertex from large parts of its distribution, two samples
of E. chiriquensis from Panama, and two samples of a population from the eastern Andean slope of Ecuador
tentatively assigned to brachyptera by Moore et al. (2013; Table 1). Sequence data were also obtained for the
nuclear β-fibrinogen intron 5 (Fib5) for the latter two Ecuadorian samples (Table 1). Our dataset was
complemented by ND2 and Fib5 sequences of an additional E. c. albivertex reported by Tello & Bates (2007), and
two E. c. albivertex individuals and one E. c. brachyptera from the west slope of the Andes as reported by Rheindt
RHEINDT ET AL.252 · Zootaxa 4032 (3) © 2015 Magnolia Press
et al. (2008b). ND2 and Fib5 sequences of two E. mesoleuca (Deppe) individuals were used as outgroups to root
the trees. The latter species was identified as the sister taxon of the E. chiriquensis complex in phylogenetic
analyses including all but one Elaenia species (Rheindt et al. 2008b).
Extraction, sequence generation and alignment. For most samples, we extracted genomic DNA from frozen
and ethanol-preserved tissue following standard extraction procedures as outlined by Gemmel & Akiyama (1996).
For the two Ecuadorian east-slope samples, we extracted genomic DNA from ethanol-preserved tissue using the
Exgene Clinic SV Genomic DNA Purification kit (GeneAll Biotechnology Co., Ltd, Seoul) following the
manufacturer’s protocol. The complete ND2 gene (and partial sequence of the adjacent tRNA-Met) was amplified
and sequenced in two overlapping fragments of approximately 370 and 750 base pairs (bp), using the primer pairs
L5215 with H5578 (Hackett 1996) and FRND2.1 (Rheindt et al. 2008d) with H6315 (Kirchman et al. 2001),
respectively. Additional sequences were amplified as a single fragment using L5215 and H6315. The Fib5 intron
was amplified and sequenced using primer pairs Fib5 and Fib6 (Driskell & Christidis 2004). PCR conditions for
both gene regions were similar to those described by Driskell & Christidis (2004). Amplified fragments were
purified using the GFX Gel Band and PCR purification Kit (Amersham Bioscience Corp., Piscataway, New
Jersey), the AMPure reagent (Agencourt Bioscience Corp., Beverly, Massachusetts), or ExoSAP-IT PCR cleanup
reagent (Affymetrix, Inc., California). Purified PCR products were sequenced by cycle sequencing and dye
terminator methods with BigDye Terminator v3.1 Cycle Sequencing Kit (Applied Biosystems, California) on an
automated sequencer (ABI 3130xl Genetic Analyzer, Applied Biosystems, California) or on a MegaBACE 1000
capillary DNA sequencer utilising the methods described by Norman et al. (2007).
We aligned and edited sequences using the program CodonCode Aligner 4.2.5 (CodonCode Corp.,
Massachusetts). All sequences were double-checked by eye. We used ORF Finder (www.ncbi.nlm.nih.gov/gorf/
orfig.cgi) to check for internal stop codons, reading frame shifts, anomalous substitution patterns, and deviant base
composition.
Phylogenetic analysis. Phylogenetic inference was conducted using maximum parsimony (MP), maximum
likelihood (ML) and Bayesian inference methods. MP and ML analyses were carried out in MEGA 5.2.2 (Tamura
et al. 2011). We analyzed each data partition (ND2 and Fib5) separately. MEGA 5.2.2 was also used to perform raw
‘p’ sequence divergence calculations using the pairwise deletion option.
MP analyses were performed using a heuristic search of tree space with tree-bisection-reconnection branch
swapping. Parsimony bootstrap tests were conducted with 10,000 replicates of full heuristic searches. For ML
analyses, we used the software jModelTest (Posada 2008) to evaluate the likelihoods of 88 models of nucleotide
sequence evolution using default settings. The best-fitting model was chosen according to the Bayesian
Information Criterion. The optimal model selected for ND2 was the Hasegawa-Kishino-Yano model with invariant
sites, and we also used this model for the concatenated dataset given that the ND2 partition is about twice as large
and 5–6 times as variable as the Fib5 partition. ML bootstrap tests were performed with 10,000 replicates and
heuristic searches of tree space, with initial trees generated either by neighbor-joining (Saitou & Nei 1987) or
BIONJ, a modified neighbor-joining method (Gascuel 1997). Subtree-pruning-regrafting branch swapping was
conducted on the dataset.
Bayesian inference was performed with BEAST v1.8 (Drummond & Rambaut 2007). Markov Chain Monte
Carlo (MCMC) chains were run with a Hasegawa-Kishino-Yano model of nucleotide substitutions with invariant
site and Yule tree prior. Four runs were completed with a randomly generated starting-tree topology. For each run,
posterior estimates were obtained by sampling every 1000th MCMC step from a total of 10,000,000 steps. Using
Tracer, we determined a reasonable burn-in for our runs of 200,000, with the corresponding ESS value >200,
confirming that our runs had reached convergence. The remaining sampled trees were used to build a maximum
clade credibility tree with TreeAnnotator v.1.8 (Drummond & Rambaut 2007) with a 2% burn-in.
Acoustic Sampling Regime and Analyses. Our vocal dataset consisted of 10 recordings of vocalizations of
nominate E. c. chiriquensis, 109 recordings of E. c. albivertex, 19 recordings of E. c. brachyptera (7 of which are
from its western Andean range, and 12 are from the eastern Andean slope population), 49 recordings of the
outgroup species Elaenia mesoleuca, and 93 recordings of various other Elaenia species, for a total of 280
recordings. For the exact identity of recordings and their accession numbers in public sound libraries, see Appendix
1.
For spectrographic analysis, we used Cool Edit Pro (Syntrillium Software). Because vocalizations of
brachyptera differ so strikingly from other E. chiriquensis groups, we struggled to assign call types to their
Zootaxa 4032 (3) © 2015 Magnolia Press · 253ELAENIA ELAENIA CHIRIQUENSIS
TA
BL
E 1
. Vou
cher
or s
ampl
e nu
mbe
rs, n
ames
of i
nstit
utio
ns, G
enB
ank
acce
ssio
n nu
mbe
rs, t
axon
iden
tity
and
colle
ctio
n lo
calit
ies o
f all
E. c
hiriq
uens
is sp
ecim
ens
and
two
outg
roup
sam
ples
; sa
mpl
es f
or w
hich
bot
h N
D2
and
Fib5
wer
e ge
nera
ted
are
prin
ted
in b
old;
abb
revi
atio
ns: F
MN
H—
Fiel
d M
useu
m o
f N
atur
al H
isto
ry (
Chi
cago
); U
SNM
—U
nite
d St
ates
Nat
iona
l Mus
eum
(W
ashi
ngto
n, D
.C.);
AM
NH
—A
mer
ican
Mus
eum
of
Nat
ural
His
tory
(N
ew Y
ork)
; M
ECN
—M
useo
Ecu
ator
iano
de
Cie
ncia
s N
atur
ales
(Q
uito
); M
G—
Mus
eu G
oeld
i (B
elem
); U
FP—
Uni
vers
idad
e Fe
dera
l de
Per
nam
buco
; LS
UM
Z—Lo
uisi
ana
Stat
e U
nive
rsity
Mus
eum
of
Nat
ural
Sci
ence
; ZM
UC
—Zo
olog
ical
Mus
eum
at
the
Uni
vers
ity o
f C
open
hage
n; L
GEM
A—
Labo
rató
rio d
e G
enét
ica
e Ev
oluç
ão M
olec
ular
de
Ave
s (Sã
o Pa
ulo)
; USP
—U
nive
rsid
ade
de S
ão P
aulo
.
Inst
itutio
n an
d vo
uche
r or s
ampl
e nu
mbe
r G
enba
nk a
cces
sion
num
ber
Taxo
n na
me
Col
lect
ion
loca
lity
Vou
cher
skin
MG
535
32 (f
ield
num
ber
MG
CH
-245
);
tissu
e FM
NH
391
476
**
ND
2: E
U31
0947
, Fib
5:
EU
3109
40
E. c
. alb
iver
tex
Bra
zil:
Am
apá,
Faz
. Cas
imir
o
Vou
cher
skin
UFP
unc
atal
ogue
d (fi
eld
num
ber U
FP M
TE-
084)
; tis
sue
FMN
H 3
9257
4 EU
3109
49E.
c. a
lbiv
erte
x B
razi
l: Pa
rá, M
onte
Ale
gre
Vou
cher
skin
USN
M 6
2596
8; ti
ssue
USN
M B
1234
3 EU
3109
42E.
c. a
lbiv
erte
x G
uyan
a
Vou
cher
skin
USN
M 6
4900
4; ti
ssue
USN
M B
4398
EU
3109
46E.
c. a
lbiv
erte
x G
uyan
a
Vou
cher
skin
AM
NH
831
265
(fiel
d nu
mbe
r GFB
285
4);
tissu
e D
OT
4789
EU
3109
43E.
c. a
lbiv
erte
x V
enez
uela
: Bol
ivar
, Auy
an T
epui
Vou
cher
skin
LSU
MZ
1509
66**
N
D2:
EU
3109
48, F
ib5:
E
U31
0941
E
. c. a
lbiv
erte
x B
oliv
ia: S
ta. C
ruz,
Vel
asco
Vou
cher
skin
ME
CN
636
3 (fi
eld
num
ber
NK
2-20
.8.9
2);
tissu
e ZM
UC
125
668
**
ND
2: E
U31
0951
, Fib
5:
EU
3109
39
E. c
. bra
chyp
tera
E
cuad
or: E
smer
alda
s, 10
km
W L
ita
Vou
cher
skin
ME
CN
874
0 (fi
eld
num
ber
NK
1-16
.8.1
2);
tissu
e ZM
UC
148
519
ND
2: K
P696
505
Fib5
:KP9
3899
3E
. c. b
rach
ypte
ra
Ecu
ador
: E A
ndea
n sl
ope
at R
ío Q
uijo
s, N
apo
Vou
cher
skin
ZM
UC
138
277
(fiel
d nu
mbe
r N
K2-
16.8
.12)
; tis
sue
ZMU
C 1
4852
0 N
D2:
KP6
9650
6Fi
b5:K
P938
994
E. c
. bra
chyp
tera
E
cuad
or: E
And
ean
slop
e at
Río
Qui
jos,
Nap
o V
ouch
er sk
in U
FP u
ncat
alog
ued
(fiel
d nu
mbe
r UFP
MTE
-01
7); t
issu
e FM
NH
392
559
EU31
0950
E. c
. alb
iver
tex
(mus
eum
skin
err
oneo
usly
la
bele
d as
E. f
lavo
gast
er)
Bra
zil:
Pará
, Mon
te A
legr
e
Vou
cher
skin
UFP
535
25 (f
ield
num
ber
MG
CH
-217
);
tissu
e FM
NH
391
472
* N
D2:
DQ
2945
43; F
ib5:
D
Q29
4455
E
. c. a
lbiv
erte
x B
razi
l: A
map
á, F
az. C
asim
iro
Vou
cher
skin
USP
unc
atal
ogue
d; ti
ssue
LG
EM
A P
2177
**
ND
2: E
U31
0945
, Fib
5:
EU
3109
37
E. m
esol
euca
(out
grou
p)
Bra
zil
Vou
cher
skin
USP
unc
atal
ogue
d; ti
ssue
LG
EM
A P
2176
**
ND
2: E
U31
0944
, Fib
5:
EU
3109
38
E. m
esol
euca
(out
grou
p)
Bra
zil
* se
quen
ce fr
om T
ello
& B
ates
(200
7)
** se
quen
ce fr
om R
hein
dt e
t al.
(200
8b)
RHEINDT ET AL.254 · Zootaxa 4032 (3) © 2015 Magnolia Press
homologous counterparts in sister taxa. Therefore, our bioacoustic analysis is largely qualitative and aims at the
documentation of different call types within each taxon.
Results
Molecular characterization. We did not detect any stop codons or indels (insertions or deletions) in the ND2 gene
or indels in Fib5. Consequently, alignments were straightforward. The ND2 fragment was 1066 bp long and
contained 118 variable sites (=11.1%), whereas the Fib5 fragment was 544 bp long and contained 23 variable sites
(=4.2%). Fib5 had a noticeably smaller proportion of variable sites as compared to ND2, and is therefore
presumably of less value in phylogenetic inference at this taxonomic level.
Uncorrected ND2 sequence divergence (shown across taxa in Table 2) ranged from 7.9–8.3% between
members of the E. chiriquensis complex and the outgroup E. mesoleuca. Within E. chiriquensis, the two
individuals from the eastern Andean slope in Ecuador were characterized by very low (0.6%) ND2 divergence
from the brachyptera sample from the western Andean Chocó region, suggesting a close affinity of east-slope birds
not with the widespread taxon albivertex, but with brachyptera from west of the Andes. In contrast, the group
comprising brachyptera (from Chocó) and Ecuadorian Andean east-slope individuals exhibited ND2 divergences
of 3.7–4.3% from the other two taxa (albivertex and nominate chiriquensis). ND2 differentiation between the latter
two subspecies was low (0.8–1.2%). Within widespread albivertex, divergences ranged from 0.1–0.6% despite the
pronounced geographic separation of some of these samples.
Sequence divergence in the more slowly-evolving nuclear Fib5 intron (Table 2) ranged from 0.2–2.3%
between the E. chiriquensis complex and the outgroup E. mesoleuca. Comparable levels of divergence were also
recorded within the E. chiriquensis complex, with 0.2–3.1% between E. c. brachyptera and the other two taxa, and
0–1.9% between albivertex and nominate chiriquensis.
TABLE 2. Uncorrected ND2 and FIB5 p-divergences between and within taxa in the E. chiriquensis complex and the
outgroup E. mesoleuca; bold print indicates intra-taxon divergences.
Molecular phylogenetics. MP, ML and Bayesian analyses of the ND2 dataset all recovered a deep division of
the complex into a clade containing the three brachyptera samples versus a clade consisting of all albivertex and
nominate chiriquensis samples with high branch support for each clade (Figure 2). Within each of these two clades,
there was only shallow differentiation among samples. Apart from variations in the exact branch support values,
there were limited differences among trees resulting from different analytical modes.
The same topology and general branch support were recovered in MP, ML and BI analyses of the concatenated
dataset (Figure 3). This may reflect a lack of phylogenetic resolution in the Fib5 partition, which produced
completely unresolved and polytomous trees with all analytical modes (not shown). Given the limited phylogenetic
utility of Fib5 in Elaenia flycatchers at this taxonomic level, subsequent discussions are based on analysis of the
ND2 sequences only.
albivertex chiriquensis brachyptera mesoleuca
ND2
albivertex 0.1–0.6
chiriquensis 0.8–1.2 0.2
brachyptera 3.9–4.3 3.7–3.9 0.0–0.6
mesoleuca 7.9–8.3 8.1–8.2 8.3 0.4
FIB5
albivertex 0.4–1.7
chiriquensis 0.0–1.9 0.4
brachyptera 0.9–3.1 0.2–1.3 0.0–0.2
mesoleuca 0.4–1.3 0.2–1.1 1.7–2.3 0.8
Zootaxa 4032 (3) © 2015 Magnolia Press · 255ELAENIA ELAENIA CHIRIQUENSIS
FIGURE 2. Bayesian tree of the ND2 partition; numbers at nodes indicate MP bootstrap support / ML bootstrap support /
Bayesian posterior probability. Support values below 90 not shown.
FIGURE 3. Bayesian tree of the concatenated dataset (using both partitions); for explanation of nodal support values, see
Figure 2.
RHEINDT ET AL.256 · Zootaxa 4032 (3) © 2015 Magnolia Press
Zootaxa 4032 (3) © 2015 Magnolia Press · 257ELAENIA ELAENIA CHIRIQUENSIS
Bioacoustic analysis. The vocalizations of E. c. chiriquensis and E. c. albivertex were found to be strikingly
similar (Figure 4a–d). Vocalizations of E. c. brachyptera, on the other hand, differed from the former two taxa as
much as from any other species of Elaenia (Figures 4–5). Dawn song of brachyptera differed distinctly in the
number and quality of its elements (easily recognizable units); one call type, a simple up-down-stroke (rise and fall
in pitch) (Figure 6), differed in pitch and relative volume, and another call (Figure 7f), perhaps best described as a
rattle, differed in so many respects that no homologous call of chiriquensis or albivertex was apparent. A simple
up-down-stroke call is generally widespread in the genus, in some species including E. mesoleuca and E.
flavogaster only given as a burred note (i.e. a rapid series of alternating up- and down-strokes), in others, such as E.
albiceps and E. pallatangae, both in a burred and a pure whistled form. Therefore, its absence or presence in a taxon
may not provide much phylogenetic information. The rattle call of brachyptera, however, was not detected in any
other taxon in the genus and must be considered tentatively a vocal autapomorphy.
Dawn song: The most complex tyrannid vocalization is the dawn song, which is normally only given by the
male for a brief period at predawn and early dawn and occasionally at dusk, but only very rarely during the day
(Ridgely & Tudor 1994). We suspect that in some species the dawn song may be a pair duet. The dawn song is
rarely heard outside the breeding season. Most tyrannid dawn songs, including those of Elaenia mesoleuca and all
three forms of E. chiriquensis, consist of two phrases, one fairly simple and the other more complex. Typically, the
simple phrase is repeated several times before the song is terminated with a complex phrase. At the peak of song
activity, pauses between songs may be so brief that it is difficult to determine when one song ends and the next
begins. The number of times the simple phrase is repeated varies from song to song, and sometimes the complex
phrase may be repeated a few times. Occasionally an individual may repeat only one of the two phrases for
extended periods of time.
An examination of available dawn songs in xeno-canto (www.xeno-canto.org) and Macaulay Library of
Natural Sounds (www.macaulaylibrary.org) showed that for the genus Elaenia as a whole, the introductory phrase
of the dawn song is usually rather stereotyped throughout the range of a species except for slight differences in
pitch among individuals, whereas the more complex termination may be subject to some variation, not only among
individuals and regions, but also by the same individual during a bout of songs. Unless occasional call notes are
included, variations of complex phrases usually only involve a change in the order of the elements in the phrase; a
new element is almost never included.
In the dawn songs examined of nominate Elaenia chiriquensis (n=2) and E. c. albivertex (n=31), structure
varied little, and in 25 dawn song recordings of E. mesoleuca the only structural variation was omission (n=8) of
the first element of the complex phrase, and replacement (n=1) of the second element with a call note.
In dawn songs of E. c. chiriquensis and E. c. albivertex (Figures 4a–d and 5b) the complex phrase consisted of
three elements. The first element was identical to the simple phrase and was a double-noted tirí, the higher first
note a pure up-downstroke whistle and the second note a rising burred note. The second element of the complex
phrase was usually given twice but sometimes thrice and rarely just once, varying even within the same individual.
It also had two components: (1) the first an up-down-up-downstroke, and the initial upstroke usually brief and
faint, with peak volumes at first peak frequency as well as in the middle of the second upstroke; (2) the second
component was a low and evenly pitched sound composed of 4–6 identical notes with loud first three or four
harmonics. The third element was identical to the burred part of the first element.
FIGURE 4. Complex (terminal) phrase in dawn songs of three subspecies of Elaenia chiriquensis. a: E. c. chiriquensis; b–d: E.
c. albivertex (b from Venezuela, c from southeastern Brazil, d from the Río Marañón drainage, southernmost Ecuador); e: E. c.
brachyptera (from eastern Ecuador). Note the similarity of E. c. chiriquensis and E. c. albivertex and the difference of E. c.
brachyptera. In chiriquensis and albivertex the number of times the mid-element was repeated varied even in the same
individual; it was usually repeated once, but sometimes twice, and was occasionally just given once. There was minor variation
in the length and quality of mid-notes between individuals.
FIGURE 5. Complex (terminal) phrase in dawn songs of three closely related forms of the genus Elaenia. A: E. mesoleuca; B:
E. chiriquensis albivertex; C : E. chiriquensis brachyptera. Note the peak volume at high pitch, the fewer elements in
brachyptera, and the differences in quality of the elements between all three taxa.
FIGURE 6. Whistled calls of Elaenia chiriquensis. a: E. c. chiriquensis; b–d: E. c. albivertex (b from Venezuela, c from
Bolivia, d from the Río Marañón drainage in southernmost Ecuador); e–f: E. c. brachyptera (e from eastern, f from western
Ecuador). Note the higher pitch and the asymmetry in e and f. This is the most commonly heard call of these forms.
FIGURE 7. Other calls of Elaenia c. chiriquensis (a), E. c. albivertex (b–c), and E. c. brachyptera (d–f). The “rattle” of
brachyptera (f) is quite unlike calls of other taxa in the genus.
RHEINDT ET AL.258 · Zootaxa 4032 (3) © 2015 Magnolia Press
In E. mesoleuca (Figure 5A) the complex phrase was usually also composed of three elements, but it was the
second element that is identical to the simple phrase. The first element (omitted in 8 of 25 recordings) was a sharp,
high-pitched, rising (1.1–5 kHz) pure note, 0.03–0.05 s long, occasionally ending with a faint down-stroke, quite
unlike any call given by the species or related forms. The second element was a rising (1–4 kHz), burred note, the
first half of which was composed of fast-paced strokes, the second half of slow-paced strokes. The third element
was a low and evenly pitched (2–3 kHz) burred note fairly constant in length (0.12–0.15 s) but subject to
considerable individual variation in the number of strokes (4–11).
Owing to the scarcity of the taxon, only a single dawn song recording was available for brachyptera (Figures
4e and 5c). It differed distinctly from nominate chiriquensis and albivertex in three respects: (1) by having only two
elements in the complex phrase, none repeated; (2) by the quality, very high pitch, and relative volume of the first
element; (3) and by the sound quality of the second element. The first element was a sharply rising and high-
pitched whistle similar to the simple phrase, beginning at c. 2.5 kHz and suddenly rising to over 6 kHz with most
volume at high pitch. The second element was double-noted, beginning with a burred note of 5–6 up-down-strokes
and continuing into a single, equally long down-up-stroke with lowest pitch four semitones below the burred note.
It differed as much from dawn song of E. c. chiriquensis and E. c. albivertex as dawn songs of other species of
Elaenia did from each other. Several individuals were heard to give similar dawn songs when the existing
recording was made, so the recording was presumed to be representative, an assumption also supported by birds at
two different localities in eastern Ecuador reacting to playback of this recording during the day by approaching
closely, calling, and spreading their crest.
Calls: The recorded calls of E. c. chiriquensis from Panama and Costa Rica could be divided into two different
call types: “whistled” calls (7 recordings), and “burred” calls (1). The whistled calls of E. c. chiriquensis (Figure
6a) were almost identical to whistled calls on 39 recordings of E. c. albivertex (Figure 6b–d). They averaged 2–3
semitones higher-pitched but did not differ in any other aspect, and only two of them exceeded the highest-pitched
call recorded in albivertex, and then only by one and two semitones. The single recording of a burred call of
nominate chiriquensis (Figure 7a) was fairly similar to one of the calls given by albivertex (Figure 7b). A variety of
burred calls of E. c. albivertex ranged from whistled calls with a small burred section to entirely burred calls of
various lengths and pitches (some shown in Figure 7b–c), all differing from the most commonly given calls of E.
mesoleuca in both pitch and quality.
The recorded calls of E. c. brachyptera (Figures 6e–f and 7d–f) were from at least 18 different individuals (12
from east and 6 from west of the Andes) and could be divided into three different types: “whistled call” (15),
“burred call” (10), and “rattle” (5), besides chase calls and begging calls. All differed in at least two aspects from
vocalizations of chiriquensis and albivertex as well as from the outgroup E. mesoleuca. The whistled call was the
commonest call recorded. It is presumed to be homologous to the whistled call of albivertex, but averages 7–8
semitones higher and is distinctly asymmetrical, with the peak volume extending to the down-stroke rather than
being evenly placed around the peak frequency (Figure 6). This call led Bret Whitney (pers. comm.) to suggest that
brachyptera should be treated as a distinct species, which led NK to collect a specimen for molecular and
morphological comparisons. Burred calls of brachyptera averaged 1–2 semitones lower than the whistled calls but
still six semitones higher than in chiriquensis and albivertex, and most showed a tendency to asymmetrical volume
around the peak frequency (Figure 7d–e) as did the whistled call (Figure 6e–f). The “rattle” call of brachyptera
(Figure 7f) was distinctly different from calls of all other taxa in the genus examined and was the vocalization that
led the late Paul Coopmans (pers. comm.) to suggest that brachyptera should be elevated to species rank even
before its distinctive dawn song was recorded. It was a 0.3–1.0 s long series of 5–15 notes with peak frequency
around 5.2 kHz (4.6–6.0 kHz), usually slightly rising at first and falling at the end, notes given at a fairly even pace
of about 20 (16–23) notes per s, with each note composed of two or three connected up-down-strokes, the first and
last notes often of fewest strokes.
Discussion
Analyses of the mitochondrial ND2 gene corroborate that the subspecies albivertex is monophyletic, with shallow
differentiation over its large range (Figures 1–3), despite the wide distribution of its savannah habitat along the
margins of the Amazonian rainforest bloc. The data provide no evidence of obvious phylogeographic structuring
Zootaxa 4032 (3) © 2015 Magnolia Press · 259ELAENIA ELAENIA CHIRIQUENSIS
within this taxon (Figures 2, 3). This result is in agreement with Bates et al. (2003), who also found comparably
low ND2 divergences (0.1–0.5%) over the whole of this taxon’s range, and lower divergences between some
samples from opposite ends of the range than between samples of the same provenance.
Despite their geographic separation across the Darién Gap and northern central Colombia, albivertex and the
nominate subspecies chiriquensis were relatively poorly differentiated in terms of mitochondrial DNA. Their
conspecific treatment is further supported by our detection of limited acoustic differentiation at best (Figures 4, 7,
8).
South American populations of E. chiriquensis east of the Andes have invariably been attributed to the taxon
albivertex (e.g. Hosner 2004). However, vocal encounters with populations along the east slope of the Ecuadorian
Andes cast this attribution in doubt (Moore et al. 2013). Here, our vocal and molecular analyses unequivocally
demonstrate that these populations form a tight-knit group with brachyptera, which had heretofore been assumed
to be endemic to the western Andean Chocó region.
The genetic differentiation between brachyptera (here including samples from east of the Andes) and other
subspecies of the E. chiriquensis complex is at the same level as or exceeds that between recognized species of
Elaenia (e.g. E. dayi and E. obscura in Rheindt et al. 2008b). Although not in itself sufficient for a change in taxon
rank, this deep genetic differentiation suggests that brachyptera might best be treated as a biological species.
Vocalizations are often a more important taxonomic indicator in tyrant-flycatchers than morphological characters
(see Introduction). Therefore, vocal differentiation between brachyptera and other taxa can provide further insights
into its biological species status.
Our vocal analyses of brachyptera showed that its song and calls (Figures 5C, 6EF, 10) differ as much or more
from vocalizations of E. c. chiriquensis and E. c. albivertex as do other species of the genus from each other,
suggesting that brachyptera is more appropriately classified as a biological species than as a subspecies of E.
chiriquensis. More research is needed to establish morphological and ecological differences between brachyptera
and related taxa.
Remsen (2005) called for caution in the elevation of avian subspecies to species level in acoustic and
phylogenetic investigations, arguing that studies of limited sampling may easily overlook intermediate populations.
We deem this possibility unlikely, as our DNA and vocal samples of albivertex cover a considerable part of its
range without showing any character approximation to brachyptera wherever the ranges come close. It is currently
unknown whether the ranges of these two taxa meet at all (Ridgely & Greenfield 2001; Hosner 2004), and records
of ‘E. chiriquensis’ from eastern Peru and eastern Colombia will need to be closely assessed in the future to
establish the exact range boundaries between E. c. albivertex and E. brachyptera. So far, east slope records of birds
that exhibit either a brachyptera-like vocalization or mtDNA genotype are limited to three localities in Ecuador,
two of them in Napo Province (Río Quijos at 0.185°S, 77.682°W, 1300 m and Cosanga at 0.5777°S, 77.868°W,
1930 m: present study) and one in Morona-Santiago Province (Río Upano at Macas at ca. 2.301°S, 78.107°W, 930
m: P. Coopmans unpublished, also XC116575). The southernmost of these (Macas) is located 315 km north of the
nearest record of albivertex (SSE of Zumba, Río Marañón drainage: e.g. XC105974).
We propose the English name “Coopmans’s Elaenia” for E. brachyptera, in honour of the late Paul
Coopmans’s important contributions to Neotropical ornithology, and in recognition of the fact that it was through
his ears that this taxon’s presence in eastern Ecuador first came to be recognised.
Acknowledgements
This contribution is dedicated to the memory of Paul Coopmans, who met his untimely death in January 2007. His
suggestion that brachyptera is vocally distinct was the primary trigger for FER to pursue DNA material of the
taxon. We owe a special deal of gratitude to John Moore and Robert Ridgely for helpful suggestions and
comments. We thank Bret M. Whitney for first pointing out, in 1992, the distinctive vocalizations of brachyptera,
and Dusan Brinkhuizen and Luis Salagaje for help in field identification or locating of brachyptera in eastern
Ecuador. We thank the following people and institutions for kindly lending us Elaenia tissue for DNA analysis:
Donna Dittmann and Robb Brumfield (Louisiana State University Museum of Natural Sciences), David Willard
and Shannon Hackett (Field Museum of Natural History), Paul Sweet (American Museum of Natural History),
Christopher Huddleston (Smithsonian National Museum of Natural History), Cristina Miyaki and Gustavo
RHEINDT ET AL.260 · Zootaxa 4032 (3) © 2015 Magnolia Press
Sebastián Cabanne (Laboratório de Genética e Evolução Molecular de Aves, Universidade de São Paulo) and Jon
Fjeldså (Zoological Museum, University of Copenhagen). This work was supported by the following grants to
FER: a National University of Singapore Department of Biological Sciences start-up grant (WBS R-154-000-583-
651) and Faculty of Science start-up grant (WBS R-154-000-570-133); the Joseph Grinnell Student Research
Award awarded by the Cooper Ornithological Society; Sigma Xi Grant-in-Aid of Research; and Museum Victoria
1854 Student Scholarship. Labwork was partly funded by the Ian Potter Foundation and Amersham Biosciences
(now GE Healthcare).
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APPENDIX 1. Recordings examined.
E. chiriquensis chiriquensis: 10 (ML 7426, 46397, 165831, 165856, 165862–165863, 184520, 184527; XC 2816, 53709).
E. chiriquensis albivertex: 110 [ML 7409–7425, 10622, 11649, 14500, 14503, 19888, 34111–34112, 34120, 34131, 59344,
60919, 68141, 69886–69887, 69889–69893, 72305, 77958, 89812, 89824, 98619, 105973, 106480, 111828, 111844,
114670, 114882, 117144, 120826, 134797, 134804, 140444, 140467, 144369, 144427, 144430, 144988, 144991, 145000,
145031, 145040, 145083, 145146, 145180, 145205, 145220, 145225, 145229, 168083; XC 1774, 5575, 5732, 7304, 9466,
12220, 14237, 15285, 15444, 18520, 18914, 41704, 49373, 59343, 59384, 59385, 60390–60391, 73540, 74403, 76345,
81526–81528, 105953–105957, 105973–105975, 106224, 128654, 246362; also four recordings published by Boesman
(2006), one by Mayer (2000), and one by Vielliard (1995)].
E. chiriquensis brachyptera: 19 [7 from western Colombia and Ecuador and 12 from eastern Ecuador: XC 85110, 116575,
157107, 157133–34, 157138–40, 157189–90, 157195, 158215, 169413, 169417; also a recording published by Krabbe &
Nilsson (2003; cut 3), one by Moore et al. (2013; cut 3), an unpublished recording by Dušan Brinkhuizen, and two
unpublished recordings by Paul Coopmans].
E. mesoleuca: 49 (ML 19568–78, 20050, 22170, 56344, 56348, 85625, 88083, 103881, 103886, 103903, 103906, 143848,
178137, 178166, 178168–69, 178177; XC 10454, 13510, 16330, 23765, 30466, 33238, 41818, 42051, 59830, 60392,
81538–40, 81543–44, 93328, 93406, 98813, 103906, 118643, 144990, 153670).
Examined recordings in ML and XC of other species of Elaenia (primarily dawn songs): E. albiceps 30; E. cristata 3; E. dayi 2;
E. fallax 1; E. flavogaster 13; E. frantzii 6; E. gigas 4; E. martinica 1; E. obscura 5; E. pallatangae 3; E. parvirostris 7; E.
pelzelni 1; E. ridleyana 1; E. ruficeps 3; E. spectabilis 10; E. strepera 3.
Zootaxa 4032 (3) © 2015 Magnolia Press · 263ELAENIA ELAENIA CHIRIQUENSIS
http://dx.doi.org/10.1642/0004-8038(2007)124[134:MPOTTA]2.0.CO;2http://dx.doi.org/10.1642/0004-8038(2007)124[134:MPOTTA]2.0.CO;2http://dx.doi.org/10.1676/0043-5643(2000)112[0051:SLIPTT]2.0.CO;2http://dx.doi.org/10.1676/0043-5643(2000)112[0051:SLIPTT]2.0.CO;2http://dx.doi.org/10.1642/0004-8038(2001)118[0056:ACNSOF]2.0.CO;2http://dx.doi.org/10.1642/0004-8038(2001)118[0056:ACNSOF]2.0.CO;2
AbstractIntroductionMaterial and methodsResultsDiscussionAcknowledgementsReferences
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