Zosterops consobrinorum

Z. consobrinorum View in CoL

‘mainland’ Z. consobrinorum Z. consobrinorum ‘Wangi-wangi ‘Buton/Muna’ ‘Kabaena’ White-eye’ populations of this species do not show consistent variation between genetic and phenotypic measures.

ZOSTEROPS SP. NOV. – THE ‘ WANGI-WANGI WHITE-EYE’

Due to its unique biogeographic position ( Esselstyn et al., 2010), Sulawesi has particularly high endemism ( Michaux, 2010). It also remains relatively poorly studied ( Cannon et al., 2007) and novel taxa have been found on Sulawesi in recent years ( Indrawan & Rasmussen, 2008; Esselstyn et al., 2012; Harris et al., 2014). However, these taxa were found in remote forested areas or on more isolated islands. The fact that the ‘Wangi-wangi white-eye’ occurs on a densely populated, environmentally degraded island is particularly remarkable. Most Wakatobi bird species descriptions date from the expedition of Heinrich Kühn (1901–02; Hartert, 1903). This single island endemic must have been overlooked.

The ‘Wangi-wangi white-eye’ occurs in mixed-species flocks with Z. c. flavissimus on Wangi-wangi Island and exhibits the same generalist foraging habits common to Zosterops ( Van Balen, 2008; Kelly, 2014). The ‘Wangi-wangi white-eye’ is a much larger bird than Z. chloris (Supporting Information, Tables S9, S11), likely facilitating niche partitioning between these congeneric species. It is relatively common on Wangi-wangi: in the 18 mist-netting sessions conducted on that island, 20% of birds caught were ‘Wangi-wangi white-eyes’ and 39% were Z. chloris . All netting was carried out in the scrub and forest edge habitats, which are the most common ecosystems on the island. ‘Wangi-wangi white-eyes’ shows tolerance of disturbed habitats, although they do not show the flexibility in habitat preference of Z. c. flavissimus (present in all habitats on the Wakatobi Islands) and were not present in mangroves. Concern for the future of the ‘Wangi-wangi white-eye’ is amplified by the small size of Wangi-wangi Island (155 km 2) and that extensive surveys in south-east Sulawesi have shown it to be the only home of the ‘Wangi-wangi white-eye’ (it is absent from Oroho and Kapota, the satellite islands of Wangi-wangi). The authors recommend the collection of type specimens so that this species can be officially named and recognized, coupled with detailed surveys of Wangi-wangi Island to assess its distribution and density, and any conservation action required. A series of photos of this species are supplied in the Supporting Information to aid future field identification of this new taxon (Supplementary information, Tobias scoring, Table S19).

The provisional classification of the ‘Wangi-wangi white-eye’ as a population of Z. consobrinorum ( Van Balen, 2018c) is understandable. Both are pale-chested Zosterops separated by a short geographical distance (27 km between Buton and Wangi-wangi). Our work shows the closest relatives of the ‘Wangi-wangi white-eye’ are found in the Solomon Islands: Z. murphyi and Z. rennellianus (single island endemics) and Z. griseotinctus , a ‘supertramp’ species restricted to a series of small islands ( Van Balen, 2018a). These taxa are all> 3000 km distant from Wangi-wangi and are phenotypically distinct, all having yellow/green chests. The nodes placing the ‘Wangi-wangi white-eye’ in this clade have low support ( Fig. 3 View Figure 3 ), so its evolutionary origins remain uncertain. Sequencing of other Indo-Pacific Zosterops species that have not yet had their genetic data assessed, such as the black-ringed white-eye Zosterops anomalus (Meyer & Wiglesworth, 1896) from south Sulawesi, may shed light on this situation. The ‘Wangi-wangi white-eye’ may be a remnant of an older Zosterops radiation and represent the remaining relict taxon.

ZOSTEROPS CHLORIS – INDEPENDENT COLONIZATIONS AND THE ‘ WAKATOBI WHITE-EYE’

This study clarifies a number of features about Sulawesi Z. chloris populations, while raising further questions. It appears from our data that white-eyes from the south-east Sulawesi mainland and its continental islands form a continuous population, rather than Z. c. intermedius being present on the continental islands and Z. c. mentoris on the mainland, as was suggested by Trochet et al. (2014). The mainland south-east Sulawesi population of Z. chloris is closely related to the south Sulawesi population (Z. c. intermedius), but shows sufficient divergence (ND2: 1.22%) that further investigation is required to clarify their taxonomy. Currently there is insufficient genetic or phenotypic data to classify Z. chloris from the mainland south-east Sulawesi population as either Z. c. intermedius or Z. c mentoris. Zosterops c.intermedius as currently defined includes populations from south Sulawesi, the continental islands of south-east Sulawesi and much of the Lesser Sunda Islands ( Van Balen, 2018a). An assessment of the different populations currently assigned to Z. c. intermedius and Z. c. mentoris (isolated populations in central and northern Sulawesi) is needed to clarify the taxonomy of Z. chloris on mainland Sulawesi .

Within south-east Sulawesi, the Runduma population of Z. chloris (first noted by this study) represents a recent independent colonization from a mainland south-east Sulawesi source population ( Fig. 5 View Figure 5 ), not from the Wakatobi Islands. This was an unexpected discovery, because the shortest distance between Runduma and the closest mainland population (Buton) is 123 km ( Fig. 1 View Figure 1 ). The distance between Runduma and its nearest Wakatobi Island neighbour is only 61 km. The Runduma population of another small passerine, the olive-backed sunbird Cinnyris jugularis (Linnaeus, 1766) , appears to have colonized Runduma via the shorter distance from the Wakatobi Islands ( Kelly, 2014). Given the isolation of Runduma and its tiny size (c. 5.5 km 2), it was unsurprising that it was colonized much later than the Wakatobi Islands ( Fig. 5 View Figure 5 ). Runduma Z. chloris are morphologically distinct from other Z. chloris populations, showing the largest body size and longest bill length ( Fig. 6 View Figure 6 ; Supporting Information, Table S8). Larger bill and body size has been repeatedly observed to evolve in bird populations as an adaptation to a more generalist niche on small islands ( Grant, 1965; Clegg & Owens, 2002; Clegg et al., 2002; Scott et al., 2003). Runduma Island is almost entirely covered in coconut plantations and the Z. chloris population has been observed to feed on coconut nectar more regularly on Runduma than elsewhere (DJK, pers. obs.). Thus, the longer bill may be an adaptation allowing the population to take advantage of an abundant resource in an ecologically constrained habitat. Such changes can be rapid and quickly come to fixation in a population ( Bosse et al., 2017). This morphometric difference, coupled with the pairwise genetic distance (ND2: 0.73%, COI: 2.22%), between mainland Sulawesi and Runduma populations indicates there may be a subspecies level difference between them ( Hebert et al., 2004). Future collection of song recordings and type specimens for assessment of more subtle plumage differences might prove useful in determining the taxonomic status of this population.

Zosterops View in CoL c. flavissimus (Wakatobi Islands) proved the most distinct of the Z. chloris View in CoL populations sampled. It appears to have diverged much earlier (0.38–0.8 Mya) than any of the other Sulawesi populations of Z. chloris View in CoL ( Fig. 5 View Figure 5 ). This was an older date of divergence than that of several recognized Zosterops species ( Fig. 5 View Figure 5 ). Zosterops View in CoL c. flavissimus is morphometrically distinct from other Z. chloris View in CoL populations ( Fig. 6 View Figure 6 ; Supporting Information, Tables S8, S9), being significantly smaller. Its song is highly distinct from mainland south-east Sulawesi Z. chloris View in CoL ( Fig. 8 View Figure 8 ), with a generally higher maximum frequency and number of notes (Supporting Information, Tables S13, S14), which would be expected for a population with a smaller body size (Potvin, 2013). Zosterops View in CoL c. flavissimus is also distinct from mainland south-east Sulawesi Z. chloris View in CoL in plumage, with a more vibrant yellow head and paler bill (Supporting Information, Tobias scoring, Table S18). The pairwise difference between Z. c. flavissimus and mainland south-east Sulawesi Z. chloris View in CoL (ND2: 2.5%, COI: 4.9%) is much larger than the average species difference (COI: 2.7%) that Hebert et al. (2004) found between North American birds, and is much more than 10 times the intra-group variation. In addition, our molecular species delimitation analyses (ABGD) highlights Z. c. flavissimus as a separate species. All of this evidence makes a strong case for the recognition of Z. c. flavissimus as a full species. While the gap between the Wakatobi Islands and Buton is small (27 km), differentiation over small, open-water gaps has been noted many times in the genus Zosterops View in CoL ( Mayr, 1942; Diamond, 1998; Mayr & Diamond, 2001). The isolation of the Wakatobi population may have been helped by a loss of dispersal ability during adaptation to the Wakatobi Islands (Supporting Information, assessment of dispersal ability, Fig. S5 View Figure 5 ). Several type specimens of the Wakatobi Zosterops View in CoL currently designated as Z. c. flavissimus are in the American Museum of Natural History’s collection (Supporting Information, Table S20) from the expedition of Heinrich Kühn (1901–02; Hartert, 1903), which should facilitate the promotion of this population to a full species as Z. flavissimus .

Zosterops View in CoL c. maxi from Lombok is also significantly different in song from other Z. chloris View in CoL populations, although with a tiny sample size (N = 2). A much larger sample size and investigation of further traits would be needed to form a greater understanding of the relationship of Z. c. maxi to other Z. chloris View in CoL populations.

ZOSTEROPS CONSOBRINORUM – INCONSISTENT VARIATION BETWEEN MEASURES

By providing the first detailed assessment of Z. consobrinorum , this study gives a first insight into its evolutionary history and emphasizes the need to use a combined approach when studying systematics and evolution. The fact that Z. atrifrons is the closest relative of Z. consobrinorum among the species sampled is not surprising. Zosterops atrifrons is a pale-chested, white-eye endemic to central and northern Sulawesi, showing geographic and phenotypic similarity ( Van Balen, 2008). The unusual patterns of divergence between Z. consobrinorum populations emphasize how incorrect inferences can easily be drawn in phylogenetic studies, particularly when using a small number of mitochondrial genes. Due to unavoidable logistical constraints, many phylogeographic studies have relied on a small number of museum specimens from each individual population, or a single line of evidence, for assessing populations (genetic, phenotypic or acoustic). While phenotypic and genetic measures often provide the same answer ( García et al., 2016), there are cases where they have been shown to differ ( Phillimore et al., 2008; Potvin et al., 2013). While the Kabaena population of Z. consobrinorum is distinct in morphometrics and song ( Figs 7 View Figure 7 , 9 View Figure 9 ), it is almost inseparable from the mainland Sulawesi population in mitochondrial DNA ( Figs 3 View Figure 3 , 4 View Figure 4 ). This population has only been separated from mainland Sulawesi since the last glacial maximum ( Voris, 2000). Kabaena is the smallest island (873 km 2) that Z. consobrinorum was found on. This may have presented a more ecologically constrained environment for the Kabaena Z. consobrinorum population in comparison to the mainland ( Lomolino & Weiser, 2001). The larger body size of the Kabaena Z. consobrinorum population ( Fig. 7 View Figure 7 ) may have been an adaptation to life on a smaller island ( Clegg & Owens, 2002). Morphological adaptation to new environmental conditions can occur rapidly in birds and may not be related to change in neutral genetic markers like mitochondrial DNA, particularly over the short time -span Kabaena has been isolated ( Nussey et al., 2005; Charmantier et al., 2008; Lande, 2009). As well as adaptation to local conditions, genetic drift can play a role in phenotypic change in island populations and may lead to rapid change in small populations on islands (Clegg et al., 2002; Runemark et al., 2010).

The unusual population structure of the Buton/ Muna Z. consobrinorum is more difficult to explain. Initial observations of the song and phenotype of the Buton population prompted suggestions it could be an independent subspecies ( Wardill, 2003). This would be unexpected for an island only 6 km from Sulawesi, but not unprecedented ( Mayr, 1942; Mayr & Diamond, 2001). This study finds no such differences, but there is strong genetic divergence in ND2 / ND 3 in half of the Buton birds and the single Muna bird sampled. That such genetically divergent individuals could be found at the same site on Buton (Kusambi, 5.153 °S, 122.895 °E) seems strange. The regular trading of Zosterops species as pets in Indonesia ( Harris et al., 2017) may also have confused the pattern. Zosterops consobrinorum sing the most readily of our study species (pers. obs.) and are popular pets for that reason. It is entirely possible that the Buton/Muna population was originally more genetically distinct, but escaped Z. consobrinorum pets with mainland Sulawesi heritage may have bred with the local population, reducing any genetic divergence between Buton and Sulawesi ( Laikre et al., 2010). There is no morphological distinction between Sulawesi, Buton or Muna birds, and a deeper genomic sampling would be needed to understand this pattern. The lack of morphometric divergence between the Buton and Muna populations may reflect the fact that they inhabit larger, more diverse islands than Kabaena (Buton– 4408 km 2; Muna– 2890 km 2), which are only separated by 0.6 km at their closest point. These two diverse islands may provide a less ecologically constrained environment ( Lomolino & Weiser, 2001). Sampling from a larger number of sites, in a wider diversity of habitats, would allow greater understanding of the Buton and Muna populations and assess whether they are uniform in morphometrics throughout those islands. Considering all traits, together with ABGD classification of Z. consobrinorum as one species, we recommend no change to the taxonomy of Z. consobrinorum .