Phyllergates cucullatus relictus, Rheindt & Prawiradilaga & Ashar & Lee & Wu & Ng, 2020

Rheindt, Frank E., Prawiradilaga, Dewi M., Ashar, Hidayat, Lee, Geraldine W. X., Wu, Meng Yue & Ng, Nathaniel S. R., 2020, A lost world in Wallacea: Description of a montane archipelagic avifauna (supplement), Science 36, pp. 1-104 : 51-56

SM8:

Phyllergates cucullatus relictus , subspecies nova

(Banggai Mountain Leaftoiler;

urn:lsid:zoobank.org:act:F1F92AB0-583D-4AA2-AEC1-8F47D4B8B7AA

) Frank E. Rheindt, Dewi M. Prawiradilaga, Hidayat Ashari, Suparno, Nathaniel S. R. Ng

Holotype

MZB.Ornit.34.442 ( fig. S12 ); adult male collected 20 Dec 2013 above Kokolomboi village (~ 950m) on Peleng Island (S 01⁰ 17.561 '; E 122⁰ 52.520 '). Collected by the Rheindt / LIPI field party, including tissue samples from breast muscle and liver; skin prepared by Suparno; field number Pel16; some molt; low fat; weight 7.5g; wing length 4.8cm; wing spread 15.3cm; total length 12.2cm; bill 1.3cm; tail 5cm; tarsus 2cm.

Description of holotype

Crown and nape rich rufous (2.5YR 4/10), slightly darker posteriorly, and not extending as far onto the nape as in the new Taliabu subspecies (P. c. sulanus; see SM7). Short blackish eyestripe. Facial region from auriculars to lores dusky-grey (N3) with an increasing rufous suffusion (concolorous with crown) towards the malar and moustachial regions. Mantle and scapulars to uppertail coverts olive with a slight bronzy hue (5Y 3/4), colder-colored than in the new subspecies from Taliabu (P. c. sulanus). Remiges and rectrices are darker and duskier, but with outer edging nearly concolorous with mantle. Underparts are bicolored, with a white chin to breast, and a lemon-yellow belly and vent (5Y 8/10), brighter centrally than laterally, and with a dusky olive suffusion on the flanks. Underwing concolorous with central belly on axillaries, with increasingly white suffusion towards the remainder of the underwing. Tarsus dark-yellow. On the live bird, the upper mandible was black with a yellow tip, and the lower mandible was black with a yellow base and tip. The iris color was not clearly discerned on the live bird.

Diagnosis

A distinct new subspecies of Mountain Leaftoiler P. cucullatus (or ‘Mountain Tailorbird’), differing from adjacent subspecies to the east and to the west in important discrete characters.

The lack of a supercilium and the posterior extension of the rufous crown coloration onto the mid-nape set this subspecies apart from most other subspecies, except those from Sulawesi and Taliabu, which have an equally or sometimes even slightly more extensive rufous crown. It further differs from cucullatus (Java, Bali, Sumatra), cinereicollis (Borneo), malayanus (Malay Peninsula) and all subspecies further west and north in the absence of a strong grey hindcollar band and/or strongly grey breast sides; from batjanensis (Bacan Island) in its lemon-yellow belly lacking a strong olive suffusion; and from dumasi (Seram and Buru) in its much less brown-colored upperparts. In many aspects, the new taxon is similar to the set of subspecies on Sulawesi (riedeli, stentor, meisei, hedymeles), but dramatically differs in its much more extensive yellow belly (versus yellow on the flanks only, or a light-yellow suffusion on the lowermost underparts, or a near-complete absence of yellow, respectively).

This new subspecies shares many unique traits with the new subspecies from Taliabu sulanus (see SM7), but differs significantly in its darker chestnut crown and its less reddish overall appearance, largely lacking a rufescent suffusion to the breast and flanks, and showing much less rufescent on the auriculars; its flanks are also much colder olive-washed (versus warmly rufescent-washed), and the upperparts and especially upper wings are colder bronze-olive. On live birds, the legs are much darker and less intensely colorful than those of birds from Taliabu.

Etymology

The subspecific epithet relictus, past participle of Latin ‘relinquere’ roughly translating as “the one left behind”, refers to the small size and isolated nature of the sole known population of this new subspecies, which is confined to a restricted area of montane forest on the island of Peleng.

Individual, sex and age-related variation within the taxon

The juvenile and immature plumages remain undocumented. There is a great deal of uniformity across the three adult specimens procured (two males and one female) except for differences in the intensity of a rudimentary degree of rufescent suffusion on the throat and breast sides.

History of discovery

FER and Filip Verbelen first encountered and documented the new subspecies during a visit to the highlands of western Peleng between 22-31 March 2009 ( 49). We found it again during our collecting expedition to Peleng between 18-23 Dec 2013, when three specimens were collected ( 19).

Distribution and status

Typical of Phyllergates leaftoilers, this new taxon is restricted to forest edge situations, treefall gaps and bamboo thickets in montane forest on the island of Peleng in the Banggai Archipelago. During our combined visits to the island ( 19, 49), we recorded this new taxon from 750m to the highest point at over 1000m elevation. It may, therefore, not range as low as the new taxon from neighboring Taliabu, although future fieldwork may well produce lower elevational records. Its presence on other islands in the Banggai Archipelago is unlikely given that only one of them, the small island of Bangkulu, slightly exceeds 600m in elevation, with only 5 ha of land lying above 600m, still well below the lowest known elevational occurrence of the new subspecies. Despite its very small range, its predilection for disturbed forest situations probably means that it is not particularly negatively affected by the current degradation that is impacting most highland forests of western Peleng.

Taxonomic rationale (combined for Phyllergates cucullatus sulanus and P. c. relictus)

The Mountain Leaftoiler P. cucullatus was previously thought to be an Orthotomus tailorbird and then called Mountain Tailorbird. We here acknowledge the distant relationship to Orthotomus tailorbirds (13 1) and therefore follow the recent trend of calling members of this species ‘leaftoilers’ rather than tailorbirds [e.g. ( 57)], a fitting translation from their re- instated scientific genus name Phyllergates . As for the species name cucullatus , we follow the recently proposed emendation ( 6) of the original spelling of the name (‘ cuculatus’) on the basis of information in the original description showing that the name was meant to refer to the birds’ hooded appearance (from Latin cucullus – hood).

Plumage evidence: The new subspecies sulanus from Taliabu is arguably one of the most distinctly-colored, if not the single most distinctly-colored subspecies of P. cucullatus (see Diagnosis) and is therefore well-deserving of subspecies status. Its reddish-suffused anterior body renders it instantly recognizable among any series of specimens. Although not as unique in morphology, we also describe relictus from Peleng at the subspecific level mainly on the basis of its distinct coloration. In plumage distinctness, relictus far exceeds several other previously recognized subspecies of P. cucullatus , such as P. c. cinereicollis.

Bioacoustic evidence: We have been unsuccessful in procuring a sufficiently large sample set of song recordings of the two new subspecies, precluding rigorous bioacoustic analysis. However, we note that the songs given by these two subspecies in the field did not strike us as very different from the songs of other subspecies we are familiar with. Song playback with recordings from several other islands elicited a ready response at least in P. c. relictus. Based on our bioacoustic experience with Indonesian passerines, we do not have the impression that song differences of the two new subspecies would warrant anything but a subspecific treatment at the present time.

Genomic evidence: We created a set of ~8,500 SNPs and a genome-wide sequence alignment of over 2 million base pairs (bp), along with an alignment of mitochondrial NADH dehydrogenase intron 2 (ND2) sequences, to investigate levels of differentiation among Phyllergates leaftoilers from Sulawesi, Peleng and Taliabu. Details on laboratory and analytical methods are given in a separate Methods paragraph below.

Each of the three subspecies (P. c. stentor from eastern Sulawesi, P. c. relictus from Peleng and P. c. sulanus from Taliabu) formed a spatially separate cluster in population- genomic space ( fig. S10 ). The main genomic division according to a PCA based on ~8,500 SNPs occurred between P. c. sulanus from Taliabu versus the other two subspecies (PC1 in fig. S10 ). In contrast to the leaf-warbler analysis (see SM6), this main genomic division among leaftoilers was also supported by the mitochondrial tree and the genomic ‘species tree’ ( fig. S11 ), consistently placing P. c. relictus from Peleng close to P. c. stentor from Sulawesi, although the concatenated tree built from genome-wide loci was in conflict, placing P. c. relictus closer to P. c. sulanus. Coincidentally, the majority tree with a basal placement of sulanus (topology 1 in fig. S11 ) is also the arrangement that would be supported by the extraordinarily divergent plumage of sulanus, making it unique among all leaftoiler subspecies.

Pairwise divergences between the subspecies (as determined by ND2 distances) were relatively low (0.3-1.7%; fig. S11 ), at levels generally accepted to be below the species threshold for birds [(~2-3%; (100, 10 1)], consistent with the current proposed subspecies status. These ND2 divergences further supported the majority tree (topology 1 in fig. S11 ) by consistently rendering P. c. sulanus as the most deeply diverged subspecies (up to ~1.7%), whereas P. c. relictus and P. c. stentor emerged as only 0.3% diverged.

In summary, mitochondrial sequence analysis, PCA of genome-wide SNPs and ‘species-tree’ analysis all agree in placing P. c. sulanus basal to the other two subspecies, an arrangement supported by its distinct plumage. Therefore, we have no reason to suspect bias in the mitochondrial divergence depth (unlike in Phylloscopus , see SM6), which supports our bioacoustic assessment that both relictus and sulanus are at the subspecies level. Future studies of the uniquely colored P. c. sulanus may yet challenge this assessment.

Methodology

Laboratory procedures: We extracted genomic DNA of all tissue material available for P. c. sulanus (n=5) and P. c. relictus (n=2), along with two samples of P. c. stentor that we had independently collected on Mt Tumpu on the adjacent eastern Sulawesi peninsula ( 19). Tissue of a single individual of Cettia parens from Makira in the Solomon Islands, provided by the American Museum of Natural History in New York, was also extracted to serve as an outgroup in phylogenomic rooting. Laboratory and analytical protocols followed our procedures outlined in SM6 (under Phylloscopus emilsalimi ), utilizing the same reference genome ( Phylloscopus trochiloides viridanus ), but using a minimum stack depth of 5 in STACKS 1.34 and a minimum required locus coverage of 5 in pyRAD due to differences in sequencing quality. The final filtered dataset for the Phyllergates leaftoilers totaled 8,515 SNPs and the final concatenated read supermatrix was 2,002,726 bp long, generated from 13,194 separate loci. For mitochondrial analysis, we sequenced ND2 using the primers L5219Met and H6313Trp (13 2) with 35 cycles of PCR performed at an annealing temperature of 50-53°C, but otherwise following the procedures as outlined in SM6. The final ND2 alignment for the leaftoilers was 1,015bp long, indel-free and fully translatable. All DNA data has been deposited with Genbank at accession number PRJNA566263 and MN518850 - MN518857 .

Figures

Fig. S12. Holotypes of Phyllergates cucullatus sulanus (MZB.Ornit.34.394) (top) and Phyllergates cucullatus relictus (MZB.Ornit.34.442) (bottom), respectively.

Fig. S10. Map of Sulawesi, Peleng, and Taliabu; principal component analysis (PCA) plots of genome-wide marker sets for Phyllergates leaftoilers and Phylloscopus leaf- warblers. Grey areas represent modern-day land extent; black lines off the coasts depict - 120m isobaths, indicating land extent during Quaternary glacial maxima. The triangle, circle and square symbols indicate collection localities on each of the islands (Sulawesi = A, Peleng = B, and Taliabu = C). The two PCA plots on the inset are based on genome-wide sets of 8515 and 4104 SNPs for the leaftoilers and leaf-warblers, respectively. Drawings of the birds are modified from Eaton et al. (57). PC1 and 2 account for more than 50% of observed variation in both taxa, and each island population occupies its own cluster in genomic space.

Fig. S11. Cladograms comparing different phylogenetic analyses for Phyllergates leaftoilers and Phylloscopus leaf-warblers. Topologies are depicted for trees resulting from the application of (1) mitochondrial tree inference (=mtDNA), (2) a coalescent species tree method based on genomic SNPs (=species tree), and (3) concatenation methods applied to genomic SNPs and sequence-based data (=concatenation). Outgroups used (not shown) were Cettia parens for the leaftoilers and Phylloscopus poliocephalus pallescens for the leaf warblers. Branch support values <75 not shown. In the mtDNA and species tree topologies, branch support values sequentially represent mitochondrial maximum likelihood (ML) bootstrap, mitochondrial maximum parsimony (MP) bootstrap, and coalescent species tree posterior probability (multiplied by 100). In the concatenation topologies, branch support values sequentially represent bootstrap from ML analysis on the concatenated read supermatrix and bootstrap from MP analysis on concatenated SNPs. Percentage values between clades denote mitochondrial raw pairwise p-divergences for the coding gene used.