4032 (3): 251 263 …...subtropical lowland South America, except for Amazonia (Figure 1). Recently a cis-Andean population tentatively Recently a cis-Andean population tentatively

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

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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


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.


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.


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


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


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).

References

Alonso, J.A. & Whitney, B.M. (2001) A new Zimmerius tyrannulet (Aves: Tyrannidae) from white sand forests of northern

Amazonian Peru. Wilson Bulletin, 113, 1–9.

http://dx.doi.org/10.1676/0043-5643(2001)113[0001:ANZTAT]2.0.CO;2

Alström, P. & Ranft, R. (2003) The use of sounds in bird systematics, and the importance of bird sound archives. Bulletin of the

British Ornithologists’ Club (Supplement), 123A, 114–135.

Bates, J.M., Tello, J.G. & Cardoso da Silva, J.M. (2003) Initial assessment of genetic diversity in ten bird species of South

American cerrado. Studies on Neotropical Fauna and Environment, 38, 87–94.

http://dx.doi.org/10.1076/snfe.38.2.87.15924

Boesman, P. (2006) Birds of Venezuela MP3 Sound Collection. Peter Boesman and Birdsounds.nl, Belgium and Netherlands.

[DVD-ROM]

Brumfield, R.T. & Capparella, A.P. (1996) Historical diversification of birds in northwestern South America: A molecular

perspective on the role of vicariant events. Evolution, 50, 1607–1624.

http://dx.doi.org/10.2307/2410897

Chesser, R.T. (2000) Evolution in the High Andes: the phylogenetics of Muscisaxicola ground-tyrants. Molecular

Phylogenetics and Evolution, 15, 369–380.

http://dx.doi.org/10.1006/mpev.1999.0774

Clement, M., Posada, D. & Crandall, K.A. (2000) TCS: a computer program to estimate gene genealogies. Molecular Ecology,

9, 1657–1660.

http://dx.doi.org/10.1046/j.1365-294x.2000.01020.x

Coopmans, P. & Krabbe, N. (2000) A new species of flycatcher (Tyrannidae: Myiopagis) from eastern Ecuador and eastern

Peru. Wilson Bulletin, 112, 305–312.

http://dx.doi.org/10.1676/0043-5643(2000)112[0305:ANSOFT]2.0.CO;2

Driskell, A.C. & Christidis, L. (2004) Phylogeny and evolution of the Australo-Papuan honeyeaters (Passeriformes,

Meliphagidae). Molecular Phylogenetics and Evolution, 31, 943–960.

http://dx.doi.org/10.1016/j.ympev.2003.10.017

Drummond, A.J. & Rambaut, A. (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary

Biology, 7, 214.

http://dx.doi.org/10.1186/1471-2148-7-214

Fitzpatrick, J.W. (2004) Family Tyrannidae (tyrant-flycatchers). In: del Hoyo, J., Elliott, A. & Christie, D.A. (Eds.), Handbook

of the Birds of the World. Vol. 9. Cotingas to Pipits and Wagtails. Lynx Edicions, Barcelona, pp. 170–462.

García-Moreno, J., Arctander, P. & Fjeldså, J. (1998) Pre-Pleistocene differentiation among chat-tyrants. Condor, 100, 629–

640.

http://dx.doi.org/10.2307/1369744

Gascuel, O. (1997) BIONJ: an improved version of the NJ algorithm based on a simple model of sequence data. Molecular

Biology and Evolution, 14, 685–695.

http://dx.doi.org/10.1093/oxfordjournals.molbev.a025808

Gemmel, N. & Akiyama, S. (1996) An efficient method for extraction of DNA from vertebrate tissues. Trends in Genetics, 12,

338–339.

http://dx.doi.org/10.1016/S0168-9525(96)80005-9

Hackett, S.J. (1996) Molecular phylogenetics and biogeography of tanagers in the genus Ramphocelus (Aves). Molecular

Phylogenetics and Evolution, 5, 368–382.

http://dx.doi.org/10.1006/mpev.1996.0032

Herzog, S.K., Kessler, M. & Balderrama, J.A. (2008) A new species of tyrannulet (Tyrannidae: Phyllomyias) from Andean

foothills in northwest Bolivia and adjacent Peru. Auk, 125, 265–276.

http://dx.doi.org/10.1525/auk.2008.07038

Hosner, P.A. (2004) Genus Elaenia. In: del Hoyo, J., Elliott, A. & Christie, D.A. (Eds.), Handbook of the Birds of the World.

Vol. 9. Cotingas to Pipits and Wagtails. Lynx Edicions, Barcelona, pp. 267–274.

Johnson, N.K. & Jones, R.E. (2001) A new species of tody-tyrant (Tyrannidae: Poecilotriccus) from northern Peru. Auk, 118,


http://dx.doi.org/10.1676/0043-5643(2001)113[0001:ANZTAT]2.0.CO;2http://dx.doi.org/10.1676/0043-5643(2001)113[0001:ANZTAT]2.0.CO;2http://dx.doi.org/10.1676/0043-5643(2000)112[0305:ANSOFT]2.0.CO;2http://dx.doi.org/10.1676/0043-5643(2000)112[0305:ANSOFT]2.0.CO;2http://dx.doi.org/10.1642/0004-8038(2001)118[0334:ANSOTT]2.0.CO;2

334–341.

http://dx.doi.org/10.1642/0004-8038(2001)118[0334:ANSOTT]2.0.CO;2

Johnson, N.K. & Cicero, C. (2002) The role of ecologic diversification in sibling speciation of Empidonax flycatchers

(Tyrannidae): multigene evidence from mtDNA. Molecular Ecology, 11, 2065–2081.

http://dx.doi.org/10.1046/j.1365-294X.2002.01588.x

Joseph, L. & Wilke, T. (2004) When DNA throws a spanner in the taxonomic works: testing for monophyly in the Dusky-

capped Flycatcher, Myiarchus tuberculifer, and its South American subspecies, M. t. atriceps. Emu, 104, 197–204.

http://dx.doi.org/10.1071/MU03047

Joseph, L., Wilke, T. & Alpers, D. (2003a) Independent evolution of migration on the South American landscape in a long-

distance temperate-tropical migratory bird, Swainson’s Flycatcher (Myiarchus swainsoni). Journal of Biogeography, 30,

925–937.

http://dx.doi.org/10.1046/j.1365-2699.2003.00841.x

Joseph, L., Wilke, T., Bermingham, E., Alpers, D. & Ricklefs, R. (2003b) Towards a phylogenetic framework for the evolution

of shakes, rattles and rolls in Myiarchus tyrant-flycatchers (Aves: Passeriformes: Tyrannidae). Molecular Phylogenetics

and Evolution, 31, 139–152.

http://dx.doi.org/10.1016/S1055-7903(03)00259-8

Kirchman, J.J., Hackett, S.J., Goodman, S.M. & Bates, J.M. (2001) Phylogeny and systematics of the ground rollers

(Brachypteraciidae) of Madagascar. Auk, 118, 849–863.

http://dx.doi.org/10.1642/0004-8038(2001)118[0849:PASOGR]2.0.CO;2

Krabbe, N. & Nilsson, J. (2003) Birds of Ecuador. Sounds and Photographs. Bird Songs International, Westernieland,

Netherlands. [DVD-ROM]

Lanyon, W.E. (1978) Revision of the Myiarchus flycatchers of South America. Bulletin of the American Museum of Natural

History, 161, 4.

Mayer, S. (2000) Birds of Bolivia. Sounds and Photographs. 2nd edition. Bird Songs International, Westernieland. [DVD-ROM]

Moore, J.V., Krabbe, N. & Jahn, O. (2013) Bird Sounds of Ecuador. John V. Moore Nature Recordings, San José, California.

[DVD-ROM]

Norman, J.A., Rheindt, F.E., Rowe, D.L. & Christidis, L. (2007) Speciation dynamics in the Australo-Papuan Meliphaga

honeyeaters. Molecular Phylogenetics and Evolution, 42, 80–91.


Posada, D. (2008) jModelTest: Phylogenetic Model Averaging. Molecular Biology and Evolution, 25, 1253–1256.

http://dx.doi.org/10.1093/molbev/msn083

Remsen, J.V. (2005) Pattern, process, and rigor meet classification. Auk, 122, 403–413.

http://dx.doi.org/10.1642/0004-8038(2005)122[0403:PPARMC]2.0.CO;2

Reynard, G.B., Garrido, O.H. & Sutton, R.L. (1993) Taxonomic revision of the Greater Antillean Pewee. Wilson Bulletin, 105,

217–227.

Rheindt, F.E., Norman, J.A. & Christidis, L. (2008a) DNA evidence shows vocalizations to be a better indicator of taxonomic

limits than plumage patterns in Zimmerius tyrant-flycatchers. Molecular Phylogenetics and Evolution, 48, 150–156.


Rheindt, F.E., Christidis, L. & Norman, J.A. (2008b) Habitat shifts in the evolutionary history of a Neotropical flycatcher

lineage from forest and open landscapes. BMC Evolutionary Biology, 8, 193.

http://dx.doi.org/10.1186/1471-2148-8-193

Rheindt, F.E., Norman, J.A. & Christidis, L. (2008c) Genetic differentiation across the Andes in two pan-Neotropical tyrant-

flycatcher species. Emu, 108, 261–268.

http://dx.doi.org/10.1071/MU08020

Rheindt, F.E., Norman, J.A. & Christidis, L. (2008d) Phylogenetic relationships of tyrant-flycatchers (Aves; Tyrannidae), with

an emphasis on the elaeniine assemblage. Molecular Phylogenetics and Evolution, 46, 88–101.


Rheindt, F.E., Christidis, L. & Norman, J.A. (2009a) Genetic introgression, incomplete lineage sorting and faulty taxonomy

create multiple polyphyly in a montane clade of Elaenia flycatchers. Zoologica Scripta, 38, 143–153.

http://dx.doi.org/10.1111/j.1463-6409.2008.00369.x

Rheindt, F.E., Christidis, L., Cabanne, G.S., Miyaki, C. & Norman, J.A. (2009b) The timing of Neotropical speciation dynamics

in the late Neogene: a reconstruction of Myiopagis flycatcher diversification using phylogenetic and paleogeographic data.

Molecular Phylogenetics and Evolution, 53, 961–971.


Rheindt, F.E., Cuervo, A.M. & Brumfield, R.T. (2013) Rampant polyphyly indicates cryptic diversity in a clade of Neotropical

flycatchers (Aves: Tyrannidae). Biological Journal of the Linnean Society, 108, 889–900.

http://dx.doi.org/10.1111/j.1095-8312.2012.02036.x

Ridgely, R.S. & Tudor, G. (1994) The Birds of South America. Vol. II. The Suboscine Passerines. Oxford University Press,

Oxford, 814 pp.

Ridgely, R.S. & Greenfield, P.J. (2001) The Birds of Ecuador. Cornell University Press, Ithaca, NY, 848 pp.

Ronquist, F. & Huelsenbeck, J.P. (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics,


http://dx.doi.org/10.1642/0004-8038(2001)118[0334:ANSOTT]2.0.CO;2http://dx.doi.org/10.1642/0004-8038(2001)118[0849:PASOGR]2.0.CO;2http://dx.doi.org/10.1642/0004-8038(2001)118[0849:PASOGR]2.0.CO;2http://dx.doi.org/10.1642/0004-8038(2005)122[0403:PPARMC]2.0.CO;2http://dx.doi.org/10.1642/0004-8038(2005)122[0403:PPARMC]2.0.CO;2

19, 1572–1574.

http://dx.doi.org/10.1093/bioinformatics/btg180

Ronquist, F., Huelsenbeck, J.P. & van der Mark, P. (2005) MrBayes 3.1 Manual. Online manual. Available from: http://

mrbayes.csit.fsu.edu/manual.php (accessed 2 July 2013)

Saitou, N. & Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular

Biology and Evolution, 4, 406–425.

Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular evolutionary genetics

analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony methods. Molecular Biology and

Evolution, 28, 2731–2739.

http://dx.doi.org/10.1093/molbev/msr121

Tello, J.G. & Bates, J.M. (2007) Molecular phylogenetics of the tody-tyrant and flatbill assemblage of tyrant flycatchers

(Tyrannidae). Auk, 124, 134–154.

http://dx.doi.org/10.1642/0004-8038(2007)124[134:MPOTTA]2.0.CO;2

Traylor, M.A. (1982) Notes on tyrant-flycatchers (Aves: Tyrannidae). Fieldiana Zoology, 13, 1–22.

Vielliard, J. (1995) Guia Sonoro das Aves do Brasil. CD 1. Campinas, UNICAMP Departamento de Zoologia, Säo Paulo.

[Audio CD]

Zimmer, J.T. (1941) Studies of Peruvian birds. No. XXXVI. American Museum Novitates, 1108, 1–23.

Zimmer, K.J. & Whittaker, A. (2000) Species limits in Pale-tipped Tyrannulets (Inezia: Tyrannidae). Wilson Bulletin, 112, 51–

66.

http://dx.doi.org/10.1676/0043-5643(2000)112[0051:SLIPTT]2.0.CO;2

Zimmer, K.J., Whittaker, A. & Oren, D.C. (2001) A cryptic new species of flycatcher (Tyrannidae: Suiriri) from the cerrado

region of central South America. Auk, 118, 56–78.

http://dx.doi.org/10.1642/0004-8038(2001)118[0056:ACNSOF]2.0.CO;2

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.


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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4032 (3): 251 263 …...subtropical lowland South America, except for Amazonia (Figure 1). Recently a cis-Andean population tentatively Recently a cis-Andean population tentatively