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A phylogeographic break and bioacoustic intraspecific differentiation in the Buff-barred Warbler (Phylloscopus pulcher) (Aves: Passeriformes, Phylloscopidae)
© Päckert et al.; licensee BioMed Central Ltd 2014
Received: 1 August 2014
Accepted: 6 August 2014
Published: 30 September 2014
According to current taxonomy only three out of 27 Sinohimalayan leaf warbler species (Phylloscopidae) are considered genetically uniform across their entire breeding range along the Southeastern margin of the Qinghai-Tibetan Plateau, the Buff-barred Warbler (Phylloscopus pulcher) being one of them. Because marked differentiation among Himalayan and Chinese populations has been recently demonstrated for a number of Phylloscopus species (or sister species) we investigated the intraspecific variation of a mitochondrial gene, songs and morphology of P. pulcher in a phylogeographic approach.
We sequenced a fragment of the mitochondrial cytochrome b, reconstructed haplotype networks and analyzed DNA polymorphism among Himalayan and Chinese populations. We measured time and frequency parameters of two distinct song types and analyzed among population-differentiation in a principal component analysis and a discriminant analysis. We also compared measurements of body size dimensions taken from museum specimens.
The mitochondrial haplotype network (cytb) was divided into two distinct clusters corresponding to geographic origin of samples. Pairwise genetic distances among Himalayan and Chinese mtDNA lineages account for 1.3% which coincides with Pleistocene lineage separation at roughly 650,000 years ago. Genetic diversity is slightly higher in the Chinese part of the species’ range with respect to haplotype and nucleotide diversity while the less diversified Himalayan population lineage shows signs of recent range expansion. The vocal repertoire of P. pulcher comprises two distinct verse types that are combined with short interspersed click notes to long continuous song displays. Trill verse types showed significant differences among regions in almost all measured frequency and time parameters: Chinese males displayed more rapid and more broad-banded trills at a lower pitch. In contrast, warbling verse types showed a distinctively different structure among regions: Himalayan songs consisted of repeated syllables while Chinese songs comprised repetitions of single, long and strongly modulated elements. Subtle morphological differences among specimens from the two study regions could only be confirmed for plumage coloration but not for metric characters.
Based on the genetic and bioacoustic distinctiveness of Chinese Buff-barred Warbler populations, we recommend that the name Phylloscopus pulcher vegetus Bangs, 1913 should be re-validated for this taxon.
Phylogeographic patterns of Sino-Himalayan forest passerines are widely congruent for terminal sister taxa equally on the species level as well as on the subspecies level (Martens et al. ; Päckert et al. ). The consistency of these patterns across different passerine families implies a common onset and cause of differentiation among the extant taxa concerned: Of many Chinese bird species (particularly of those occupying subalpine breeding habitats) their closest relative inhabits the corresponding elevational forest belt of the Himalayas and/or the adjacent Indo-Burmese mountain ranges. In many cases the origin of the respective sister lineage split and extant vicariance could be dated back to Pleistocene range fragmentation (Päckert et al. [2009a], ). So far, information on the extent of secondary contact zones among such close, but genetically distinct relatives is scarce except for several sister taxa in the Himalayas (Martens and Eck ; Martens et al. ; Päckert et al. ). Recent phylogeographic studies on Chinese bird populations even located some areas of range overlap at the south-eastern margin of the Qinghai-Tibetan Plateau (QTP) in the Hengduan mountain range that in some cases well correspond with the postulated Mekong-Salween divide (Dai et al. ; Zhao et al. ). Likewise, similar phylogeographic breaks have been found across the Himalayas at the southern QTP margin, e.g. between Himalayan and Indo-Burmese sister lineages (Päckert et al. ) and even for Central Nepal four distinct subspecies transition areas were defined by (Martens and Eck (); (Figure Forty-one)).
Phylogeographic breaks among Himalayan and Chinese sister taxa of Old World warblers ( Phylloscopus ) indicated by mtDNA genetic distances (cytochrome b , in %)
Taxon 1 Himalayas
Taxon 2 China
Phylloscopus trochiloides trochiloides
Phylloscopus trochiloides obscuratus
Phylloscopus trochiloides ludlowi Wa
Phylloscopus t. ludlowi E/P. t. trochiloides
Phylloscopus fuligiventer fuligiventer
Phylloscopus fuligiventer weigoldi
Martens et al. 
Phylloscopus ricketti/P. calciatilis
Phylloscopus reguloides reguloides b
Phylloscopus reguloides ticehursti
Phylloscopus xanthoschistos c
Phylloscopus chloronotus d
Martens et al. 
Martens et al. 
Phylloscopus humei humei
Phylloscopus humei mandellii
The Buff-barred Warbler (Phylloscopus pulcher; sometimes also named Orange-barred Leaf Warbler) occupies a wide breeding distribution from the NW Himalayas along the southern margin of the Qinghai-Tibetan Plateau to the Hengduan Mountains and stretching to N and E Myanmar and to SW and C China (map with detailed records in von Vietinghoff-Scheel ; Cheng ; Clement ; Martens ). Within the wide breeding range two subspecies are currently accepted (Clement ; Martens ): Phylloscopus pulcher kangrae in the NW Himalayas to Kashmir and nominate P. p. pulcher covering the whole remaining eastward range (Hartert ; Vaurie ). Forest breeding habitats of the species cover a broad altitudinal range from median elevations up to subalpine forests occasionally above 4000 m including some downhill movements outside the breeding season (Clement ). Local breeding records from Nepal cover a rather narrow range from between 3250 up to 4100 m a.s.l. and wintering records suggest local movements from beginning of October down to 1400–2700 m a.s.l. (Martens and Eck ). For the drier western Himalayas, Price et al. () give breeding range limits at slightly lower elevations between 3050 and 3500 m a.s.l (for the western subspecies kangrae a breeding range between 3250 and 3960 m is given in Hartert ). In Sikkim, the species is highly abundant in conifer and dwarf rhododendron association up to 3960 m during breeding season with downhill movements in winter (between 1220 and 2130 m; Hartert ; Ali ). During the breeding season Buff-barred Warblers occupy the coniferous forest belt with Abies, Tsuga and Picea intermixed with Quercus and Rhododendron at the lower limit up to subalpine birch and juniper with some dwarf-rhododendron undergrowth as well as semi-open bush vegetation above treeline (Martens and Eck ; Clement ).
Presently, nominate P. p. pulcher is considered morphologically uniform with respect to plumage coloration or proportions throughout its entire Sino-Himalayan breeding range (e.g. Clements et al. ). However, there was first evidence of subtle differentiation of territorial songs among populations from the Himalayas and from China based on a limited number of sound recordings (Fischer et al. ). Accordingly, we at least expect a subtle phylogeographic break between Himalayan and adjacent Chinese populations of Phylloscopus pulcher as found in many other leaf warbler species, too. We test this hypothesis using one molecular marker (mitochondrial cytochrome b) and sonagraphic analysis of an extended data set of song recordings.
2.1 Molecular genetics and voucher specimen morphology
A minimum spanning haplotype network was constructed using TCS (Clement et al. ) and pairwise distances were computed using MEGA 4 and genetic diversity parameters and mismatch distributions were estimated using DnaSP v5.1 (Librado and Rozas ). Cytochrome-b sequences were deposited on GenBank under accession numbers KJ567540–KJ567596 (Additional file 1: Appendix).
For potential phenotypic distinction among Himalayan and Chinese birds we took morphological measurements from specimens available to us (compare Additional file 1: Appendix) of wing length, tail length, beak length and tarsus length according to the methods given in Eck et al. (): wing length (Wmax) maximum chord, ruler with zero-stop; tail length (T1) taken with divider from the point where the central rectrices meet the skin to longest rectrix tip; tarsus length (Tar1) taken with calipers according to Eck et al. (); beak length (Bsk) with divider from tip to skull front.
Buff-barred Warbler songs are quite stereotypic and are usually displayed in a song continuum of distinct verses which are connected by short high-pitched (call like) notes.
Prior to sonagraphic analyses all original recordings were converted to wave format with a sampling rate of 22.1 kHz and in 16 bit mono and analyzed with Avisoft SASLab Light v3.74 (Specht ). Sonagraphic measurements were taken for individual verse types (trills and warbles) excluding the introductory click note. The following parameters were measured (compare Figure 2): maximum frequency of the whole verse, of the first and the last note (F max, F max1, F maxend), minimum frequency and frequency span of verse (F min, Δf = F max – F min), frequency course of verse from the first to the last element (ΔF max = F maxend – F max1), total duration of verse (t) plus maximum and minimum duration of longest and shortest element (t max, t min), maximum and minimum frequency bandwidth of broadest and narrowest element (Δf max, Δf min), total number of elements (z) and of different element types (z el). Tempo of verses was calculated as a function of a) total number of elements per time unit (z/t; speed) or b) number of repeated units (elements or syllables) per time unit (repetition rate). A maximum of five verses per type (trills and warbles) were measured for the individual male and means were calculated separately for each the two verse types of each male. Among- and within-species differentiation of verse types was analyzed using principal-component analysis and discriminant analysis with SPSS 11.5.
3.1 Mitochondrial DNA
The Himalayan cluster was separated by a minimum of six substitutions from a second cluster including all sequences from Chinese samples and two samples from Myanmar (the maximum difference among tip haplotypes was 15 substitutions; Figure 3). The latter Burmese birds were captured in March and must be considered winter visitors/spring migrants from a Chinese population (Figure 1). Genetic diversity of the Chinese cluster is somewhat higher compared to the Himalayan ones (Figure 3): Among all Chinese samples, 20 haplotypes were found and most common haplotypes were present in six, four and three individuals, respectively. Haplotype diversity (HD) and nucleotide diversity (π) were both higher in the Chinese population than in the Himalayan population: HDChina = 0.947 ± 0.023, HDNepal = 0.717 ± 0.103; π China = 0.0037 ± 0.0004, π Nepal = 0.0016 ± 0.0004. Both geographical subsamples showed strictly unimodal mismatch distributions corresponding to a growth-decline model, but only the Nepal-Himalayan population had a significantly negative Tajima’s D indicating past population expansion (Figure 3). However, both Fu and Li’s D and F statistics were significantly negative for the Chinese population, too (D = −3.025, p < 0.05; F = −3.052, p < 0.05). The mean genetic distance between the Himalayan and the Chinese cluster was 1.2% compared to within-group distances of 0.4% for each of both clusters. The mean genetic distance between one sample of subspecies kangrae and the samples of nominate pulcher from Nepal ranged at 0.3%.
We compared 19 specimens from the Himalayas (W to E Nepal, 1999–2003) to 11 from China (Sichuan, Gansu; 5 from 1914, 6 from 1998–2007), all from the breeding season (May to early July). Except for one Chinese bird (from 30 July) all birds were adults and not in moulted plumage. Specimens from both regions were pretty similar in plumage coloration of underpart and identical in upperpart coloration. Slight differences are only noticeable in a series. Nepal: Throat and breast light grey noticeably interspersed with scattered yellow feathers causing patchy ornamentation, towards broad middle of belly vividly yellowish-greenish, sides of belly, flanks, in continuation of throat and belly light greyish. China: Similar to nominate pulcher from Nepal, throat and breast grey but distinctly more homogeneously darker stone grey with hardly any yellow feathers, no patchy distribution of greyish-greenish markings like in specimens from Nepal; middle of belly less vividly yellowish-green than in Himalayan specimens, flanks similar in specimens from both regions.
Body size dimensions of Buff-barred Warblers ( Phylloscopus pulcher ) from the Himalayas and China (all in mm); means and standard deviations [range of individual measures]
Nepal/males (n = 14)
59.4 ± 1.8 [56.0–62.5]
43.1 ± 1.9 [40.0–45.8]
19.1 ± 1.2 [16.4–20.0]
11.3 ± 0.7 [10.0–13.0]
Nepal/females (n = 5)
53.0 ± 2.9 [50.0–58.0]
40.2 ± 1.0 [38.5–41.0]
18.4 ± 1.3 [17.0–20.2]
10.4 ± 0.6 [9.5–10.8]
China/males (n = 7)
59.6 ± 1.8 [58.0–62.0]
44.0 ± 1.4 [42.5–46.5]
18.7 ± 1.1 [17.0–20.0]
11.0 ± 0.7 [10.0–12.0]
China/females (n = 3)
55.5 ± 1.3 [55.0–57.0]
40.7 ± 2.0 [39.0–43.0]
17.9 ± 0.2 [17.7–18.0]
10.0 ± 0,06 [10.0–10.1]
3.3 Territorial songs
Mean values (plus standard deviations) of frequency and time parameters of trill song and warbling song of Phylloscopus pulcher
3.25 ± 0.42
96.4 ± 13.5
29.6 ± 1.4
1.4 ± 0.5
0.03 ± 0.004
0.01 ± 0.001
9.77 ± 0.71
2.93 ± 0.23
7.00 ± 0.74
5.64 ± 0.87
0.87 ± 0.37
−1.9 ± 0.71
3.32 ± 0.92
70.6 ± 20.7
21.4 ± 2.1
1.0 ± 0.1
0.05 ± 0.012
0.02 ± 0.016
9.37 ± 0.51
3.56 ± 0.58
5.81 ± 0.77
4.97 ± 0.88
0.73 ± 0.27
−0.9 ± 0.83
Δf min **
1.76 ± 0.24
12.1 ± 3.0
6.9 ± 1.3
2.5 ± 0.7
0.13 ± 0.009
0.09 ± 0.028
7.46 ± 0.38
2.42 ± 0.26
5.04 ± 0.44
4.75 ± 0.44
3.36 ± 0.62
−0.4 ± 0.32
1.61 ± 0.27
15.9 ± 6.2
9.7 ± 2.3
3.4 ± 0.9
0.11 ± 0.028
0.05 ± 0.009
7.72 ± 0.60
2.43 ± 0.44
5.30 ± 0.99
4.36 ± 0.91
2.05 ± 0.76
−0.3 ± 0.41
Warbling verses of Himalayan males (Figure 4) were structurally complex including steady repetitions of one syllable (syntax: AB AB AB AB), two syllables (AB AB AB CD CD CD) and even three syllables (AB AB AB CD CD CD EF EF EF). Despite very similar auditory impression, Chinese warbles were distinctive against those from the Himalayas comprising only repeated single elements instead of syllables (syntax: AAAAA, AAA BBB or AAA BBB CCC; Figure 4d). The strong frequency modulation of the single element in Chinese verse types (v-shaped or w-shaped in the sonagram) is the reason for their warbling sound quality, although these song types do not contain syllables of alternating notes. No repetitions of syllables were found in Chinese warbles and no repetitions of single elements were found in Himalayan warbles, respectively. In contrast to trill verse types, warbling verse types did not show strong differences of continuous frequency and time parameters among regions. Only four out of twelve parameters differed between Chinese and Himalayan warbles and all of these corresponded to the more complex structure of the latter including syllables of alternating short and long elements. Compared to Himalayan populations, warbling songs from Chinese populations are significantly slower and less variable with respect to different element types per single verse (Table 3). Note types of Chinese verses are significantly longer (only t min) and cover a significantly broader frequency range (only Δf min) compared to Nepalese note types (Table 3).
Rarely, mixed verse types have been found in single individuals combining trills followed by a short warbling part in both regions (Figure 4h, i).
According to our expectations we confirmed a Sino-Himalayan East–West divide in the Buff-barred Warbler, P. pulcher. Assuming an empirical substitution rate of 0.0105 substitutions per lineage, site and million years (approximately 2% among lineages for cytochrome b, Weir and Schluter ) the respective genetic distance of 1.2% corresponds to a late Pleistocene separation among Himalayan and Chinese mtDNA lineages roughly 650000 years ago. This value compares to intraspecific distances in other leaf warbler taxon pairs showing the same phylogeographic break (e.g. P. f. fuligiventer/P. f. weigoldi: Table 1; Martens et al. ) and even to interspecific distances among sister species of leaf warblers: Phylloscopus ogilviegranti and P. hainanus; Seicercus grammiceps and S. castaniceps (both pairs having a cytochrome-b distance of 1.5%; Olsson et al. , ; Päckert et al. , [2009b]).
East–West divides across the southern and south-eastern QTP margin are a quite general pattern in forest-dwelling passerines and many of them date back to Pleistocene impact on differentiation processes in disjunct forest refuges (Martens et al. ; Päckert et al. ). Typically, Himalayan taxa might be genetically less diverse than their respective Chinese counterparts due to a loss of genetic variation in smaller, strongly isolated Himalayan refuge populations (Päckert et al. [2009a]). This is partly reflected by slight differences of genetic diversity parameters and haplotype network structure in P. pulcher, but a broader sampling would be required to substantiate these findings. Likewise, the eastward extent of the Himalayan haplogroup of P. pulcher and possible secondary contact with the Chinese haplogroup cannot be reliably confirmed due to a wide sampling gap in the eastern Himalayas and southern China. Thus further study of material particularly from south-western Chinese provinces (particularly SW Yunnan and SE Tibet) and adjacent areas in N Myanmar and NW India is required. In fact, secondary overlap of distinct mtDNA lineages in the latter region has been demonstrated for tits and long-tailed tits, Paridae and Aegithalidae (Dai et al. ; Zhao et al. ; Wang et al. [2013a], [2013b]) and can be hypothesized for other leaf warbler taxa, too (e.g. for P. xanthoschistos and P. davisoni, P. r. reguloides (incl. assamensis) and P. r. ticehursti; Olsson et al. ; Päckert et al. [2009b], ).
Along the southern QTP margin in the Himalayas, East–West divides and secondary contact between mtDNA lineages were documented for different regions and at different degrees of genetic divergence. In the Central Himalayas, Martens and Eck () defined four subspecies transition areas that largely correspond to intraspecific splits among mtDNA sister lineages, e.g. in Periparus tits (P. ater in the Dhaulagiri transition area and P. rubidiventris in the Kathmandu transition area). In contrast, secondary overlap in the Western Himalayas often corresponds to a faunal transition among Central Asian and Himalayan faunal elements that correspond to deeper and older phylogenetic splits (and do not even represent sister clades); e.g. Periparus rufonuchalis/P. rubidiventris (Martens et al. ); Aegithalos leucogenys/Ae. concinnus, Ae. niveogularis/Ae. iouschistos (Päckert et al. ).
To date only a few Asian passerine species were shown to have a homogeneous mitochondrial gene pool across the entire southern and south-eastern QTP margin, e.g. Pyrrhula nipalensis (Töpfer et al. ). Intraspecific mtDNA differentiation might also be absent in two further leaf warbler species (P. maculipennis, P. magnirostris), but this remains to be verified. Furthermore, mtDNA phylogeographies have limited explanatory power, because nuclear gene flow might widely extend beyond the limits of phylogeographic mtDNA divides as in the Green-backed Tit (Parus monticolus) (Wang et al. [2013a], [2013b]).
For the Chinese populations of the Buff-barred Warbler the name Reguloides pulcher vegetus Bangs  is available. The original description was based on three specimens from W Sichuan collected by W. R. Zappey. The holotype was collected at Yachiakun on July 14, 1908, by W. R. Zappey on 3810 m a.s.l. Bangs later compared the material from Zappey with two specimens from Sikkim which he considered to be “very different from the Chinese bird” (Bangs ). According to Bangs’ description his newly described P. p. vegetus should be “much paler and duller in color throughout” compared to nominate pulcher from the Himalayas with some slight differences in yellow underpart and rump patch coloration, too. Later on, Chinese P. p. vegetus received a tentative treatment only by taxonomists (e.g. Hartert ), presumably due to a lack of significant material for comparison. Riley () considered all Chinese specimens belonging to subspecies vegetus until further revisiting of specimens from Nepal. Greenway () analysed seven Buff-barred Warbler specimens from Yunnan and Tibet and considered them even “slightly darker and greener below than the type of vegetus” and concluded that for the time being he had insufficient Indian material at hand for comparison. Most subsequent taxonomic authorities synonymized that taxon with the nominate form P. p. pulcher (Ticehurst ; Vaurie ) and, in his field guide, Williamson () considered the Chinese form vegetus “not separable from the typical race”. Thus, in current taxonomy P. p. vegetus is not recognized as a valid subspecies anymore (Cheng ; Dickinson ; Clements et al. ). In fact, we could confirm morphological distinctiveness of Chinese P. p. vegetus only for subtle differences from Himalayan birds in plumage coloration but not by metric morphological traits of specimens examined. Our mean values of morphological parameters were fully congruent with body size dimensions listed for birds from Sikkim by Ali () and for birds from Nepal by Martens and Eck (). Differences among sexes were already documented for Nepal birds by Eck and Martens () but based on different material than analyzed here.
Compared to Himalayan populations of subspecies P. p. pulcher and P. p. kangrae, Chinese P. p. vegetus has more homogeneously dark greyish throat and breast plumage with hardly any yellow feathers and underparts less vividly yellowish-green. In addition, warbling song types provide a diagnostic character for subspecies distinction of Chinese vegetus populations for their unique syntax pattern of repeated single notes (AAA BBB CCC) instead of repeated syllables in the Himalayan part of the species breeding range (ABABAB CDCDCD). Apart from subspecies diagnosability solely by song pattern, pairwise distances between Himalayan and Chinese populations notably exceed the intraspecific distance value among NW Himalayan P. pulcher kangrae and nominate P. p. pulcher from the Central Himalayas.
We therefore recommend revalidation of the name Phylloscopus pulcher vegetus Bangs  for Chinese populations of the Buff-barred Warbler. We refrain from assigning cytochrome-b hapotypes as diagnostic characters and restrict subspecies diagnosis to its subtle phenotypic characteristics and to song pattern of single note repetitions as outlined above. According to our data, the Chinese breeding area of P. pulcher vegetus extends from the provinces Gansu and Qinghai in the North across Shaanxi and Sichuan to Yunnan in the South – and possibly even to adjacent sub-Himalayan N Myanmar in the Southwest (breeding records from this region remain to be confirmed, since our own field records were made outside the breeding season). During the breeding season the birds occupy broad-leaf and mixed forests from mean elevations at 2350 m to mountain summits at 3200 m (at Lianhua Shan, Gansu).
Though slight differences between P. p. pulcher and P. p. vegetus are obvious, the original description of vegetus by Banks differed from the judgment of later authors as outlined above. Though we generally agree with the original morphological diagnosis by Bangs () and use the name vegetus here, a re-examination of the type material is advisable.
Chinese populations of the Buff-barred Warbler (Phylloscopus pulcher) turned out to be distinctive against their Himalayan counterparts by the structural pattern of warbling song types and by slight differences in plumage colouration. That distinctiveness is backed by a genetic distance of 1.3% among two separate mitochondrial lineages (cytochrome b) from the Himalayas and China, respectively, and by significant differentiation of frequency and timely dimensions of trill song types. Based on the notable differentiation of three independent character sets outlined here (morphology, acoustics, genetics) we recommend the revalidation of the taxon name Phylloscopus pulcher vegetus Bangs, 1913 for Chinese populations of the Buff-barred Warbler.
This study was performed within the scope of the Deutsche Forschungsgemeinschaft project funding for PA 1818/3-1 (M.P.) and was supported by further grants to Y.-H. Sun from the National Natural Science Foundation of China, project No. 31272286. J. Martens received annual travel grants from Feldbausch Foundation and Wagner Foundation at Fachbereich Biologie of Mainz University for field research in Asia. Additional samples from Nepal were provided by M. Fischer and M. Hartmann, Naturkundemuseum Erfurt. A. Rauh assisted with molecular lab work. We thank all colleagues for kind support and all institutions for project funding.
Results of the Himalaya Expeditions of J. Martens, No. 279. – For No. 278 see: ZooKeys 339: 55–65, 2013.
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