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Molecular evidence suggests radical revision of species limits in the great speciator white-eye genus Zosterops

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Abstract

White-eyes (Zosterops spp.) are a group of small passerines distributed across the Eastern Hemisphere that have become a textbook example of rapid speciation. However, traditional taxonomy has relied heavily on conservative plumage features to delimit white-eye species boundaries, resulting in several recent demonstrations of misclassification. Resolution of confused taxonomy is important in order to correctly delimit species and identify taxa which may require conservation, particularly in Asia where the songbird trade is decimating wild populations. In this study, we aim to untangle multiple instances of confused taxonomic treatment in three large, widespread Asian wastebasket species complexes of white-eye (Oriental White-eye Zosterops palpebrosus, Japanese White-eye Zosterops japonicus and Mountain White-eye Zosterops montanus) renowned for their conservative morphology. Using mitochondrial DNA from 173 individuals spanning 42 taxa, we uncovered extensive polyphyly in Z. palpebrosus and Z. japonicus and propose some radically revised species limits under which former members of Z. palpebrosus and Z. japonicus would be reassigned into four and two different species, respectively. The revised taxonomy results in a net loss of two previously recognized species and a net gain of two newly recognized species, leading to significant taxonomic change but a lack of additional species-level diversity. One of the newly elevated species, Zosterops melanurus from Java and Bali, is also the world’s most heavily traded songbird and requires urgent conservation attention.

Zusammenfassung

Molekulare Belege erfordern eine radikale Revision der Artgrenzen innerhalb der „Superartbildner“-Brillenvogelgattung Zosterops

Brillenvögel (Zosterops spp.) sind eine Gruppe kleiner Singvögel der östlichen Hemisphäre, die zu einem Paradebeispiel für schnelle Artbildung geworden sind. Allerdings stützte sich die traditionelle Taxonomie bei der Abgrenzung der Brillenvogelarten bisher vorwiegend auf konservative Gefiedermerkmale, was zu verschiedenen in neuerer Zeit aufgedeckten Falschklassifikationen führte. Eine Entwirrung der Taxonomie ist wichtig für eine korrekte Artabgrenzung und die Ermittlung von Taxa mit besonderem Schutzbedarf, speziell in Asien, wo der Handel mit Singvögeln die Wildpopulationen stark dezimiert. Ziel dieser Untersuchung war es, verschiedene Fälle verworrener taxonomischer Einordnung bei drei großen, weitverbreiteten asiatischen “Sammelsurium-Artkomplexen” von Brillenvögeln (Gangesbrillenvogel Z. palpebrosus, Japanbrillenvogel Z. japonicus und Gebirgsbrillenvogel Z. montanus) aufzulösen, welche für ihre konservative Morphologie bekannt sind. Anhand von mitochondrialer DNA von 173 Individuen aus 42 Taxa entdeckten wir ein beträchtliches Maß an Polyphylie bei Z. palpebrosus sowie Z. japonicus und empfehlen eine radikale Revision einiger Artgrenzen, durch welche vormalige Angehörige der Arten Z. palpebrosus und Z. japonicus neu zu jeweils vier beziehungsweise zwei verschiedenen Arten gerechnet würden. Diese überarbeitete Taxonomie resultiert insgesamt in dem Verlust zweier vormals anerkannter Arten sowie einem Hinzugewinn von zwei neu etablierten Arten, was zwar zu einer signifikanten taxonomischen Veränderung, jedoch nicht zu zusätzlicher Diversität auf Artebene führt. Eine der neu anerkannten Arten, Z. melanurus von Java und Bali, ist zudem der meistgehandelte Singvogel der Welt und bedarf dringender Schutzmaßnahmen.

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Acknowledgements

We thank C. Y. Gwee, N. S. R. Ng, E. Y. X. Ng, Q. Tang, G. W. J. Low, P. Baveja, J. Y. Lim, H. Z. Tan, D. Y. J. Ng, R. Y. C. Teo, Y. F. Chung, J. E. H. Ang, A. Y. H. Tan and J. S. M. Soh for field support, lab support and/or valuable feedback on this manuscript. We acknowledge grants from Wildlife Reserves Singapore (R-154-000-A05-592) and Wildlife Reserves Singapore Conservation Fund (R-154-000-A99-592) for funding this project. We are indebted to Wildlife Reserves Singapore, the Lee Kong Chian Natural History Museum (Singapore), the Burke Museum of Natural History and Culture (Seattle, WA), Museum Zoologicum Bogoriense (Cibinong, West Java, Indonesia) and the Hong Kong Bird Watching Society Ringing Team for providing samples for this study. The National Parks Board of Singapore is acknowledged for facilitating fieldwork. The experiments comply with the laws of the Republic of Singapore and Hong Kong.

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  1. Bryan T. M. Lim and Keren R. Sadanandan contributed equally to this work.

Authors and Affiliations

  1. Department of Biological Sciences, National University of Singapore, 16 Science Drive 4, Singapore, 117558, Singapore

    Bryan T. M. Lim, Keren R. Sadanandan & Frank E. Rheindt

  2. School of Biological Sciences, Kadoorie Biological Sciences Building, University of Hong Kong, Pok Fu Lam Road, Hong Kong SAR, China

    Caroline Dingle & Yu Yan Leung

  3. Research Center for Biology-LIPI, Cibinong, West Java, Indonesia

    Dewi M. Prawiradilaga, Mohammad Irham & Hidayat Ashari

  4. Wildlife Reserves Singapore, 80 Mandai Lake Road, Singapore, 729826, Singapore

    Jessica G. H. Lee

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  1. Bryan T. M. Lim
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Correspondence to Frank E. Rheindt.

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Communicated by M. Wink.

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Lim, B.T.M., Sadanandan, K.R., Dingle, C. et al. Molecular evidence suggests radical revision of species limits in the great speciator white-eye genus Zosterops. J Ornithol 160, 1–16 (2019). https://doi.org/10.1007/s10336-018-1583-7

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