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(Sapheopipo Noguchii) Pecker

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(Sapheopipo Noguchii) Pecker J Ornithol (2005) 146: 103–110 DOI 10.1007/s10336-004-0063-4 ORIGINAL ARTICLE Hans Winkler Æ Nobuhiko Kotaka Æ Anita Gamauf Franziska Nittinger Æ Elisabeth Haring On the phylogenetic position of the Okinawa woodpecker (Sapheopipo noguchii ) Received: 23 March 2004 / Revised: 29 July 2004 / Accepted: 22 September 2004 / Published online: 17 February 2005 Ó Dt. Ornithologen-Gesellschaft e.V. 2005 Abstract The Okinawa woodpecker Sapheopipo noguchii would be Dendrocopos noguchii (Seebohm in Ibis is the rarest extant woodpecker species. The monotypic 5(5):173–182, 1887) in the tribe Campetherini rather than genus Sapheopipo was considered to be a representative of Picini. an old lineage of woodpeckers that led to the Eurasian genera Picus and the Blythipicus–Gecinulus species. This Keywords Picidae Æ Phylogeny Æ Island Æ view, based on similarities in color patterns, external Sapheopipo Æ Dendrocopos morphology and foraging behavior, has been adopted in all major accounts of the family. The alternative view, that this woodpecker may be related to the widespread white- backed woodpecker Dendrocopos leucotos, which evolved Introduction distinctive subspecies on other East Asian islands, has not been generally accepted. We analyzed partial sequences of Woodpeckers, despite their largely sedentary habits, the mitochondrial cytochrome b (cyt b) gene to test these colonized many islands and some species occupy vast hypotheses. The data suggest that the Okinawa wood- ranges. They successfully invaded the Antilles, Canary pecker is a member of the genus Dendrocopos, with white- Islands, the Sunda Archipelago west of the Wallace Line, backed woodpecker and great spotted woodpecker the Philippines, Japan and the Ryukyus. On many is- D. major as close relatives. Color patterns support the lands they evolved distinct subspecies and species. Some genetic results and indicate a closer relationship with the of these species are highly distinct and their relationships white-backed woodpecker. Consequently, the correct with continental woodpeckers are obscure (e.g., Xiphid- taxonomic designation of the Okinawa woodpecker iopicus, Nesoctites). Most island forms, however, repre- sent lineages that are widespread or derive from species with very large ranges (e.g., Melanerpes spp.; great spotted woodpecker Dendrocopos major, white-backed Communicated by A.J.Helbig woodpecker D. leucotos, gray-faced woodpecker Picus canus). Geographic variation within species is marked This revised version was published online in February 2005 with corrections to tables 1 and 2. and sometimes spectacular (e.g. island forms of the greater flameback Chrysocolpates lucidus; Winkler et al. H. Winkler (&) 1995) even if it is clinal (e.g., hairy woodpecker Picoides Konrad Lorenz Institute for Ethology, villosus). Austrian Academy of Sciences, Savoyenstraße 1A, 1160 Vienna, The Ryukyus form a chain of small islands between Austria Japan (Kyushu) and Taiwan. The Okinawa woodpecker E-mail: [email protected] or Pryer’s woodpecker, Sapheopipo noguchii (Seebohm Tel.: +43-1-4862121 1887), lives in the northern hills of the largest island, Fax: +43-1-486212128 Okinawa, in the subtropical Yambaru forest. Its N. Kotaka remaining population of about 150 individuals occupies Yambaru Wildlife Center, Ministry of the Environment, an area of some 20·30 km, and is critically endangered 905-1413 Hiji, Kunigami, Okinawa, Japan (BirdLife International 2000). First described by Seeb- ohm (1887)asPicus noguchii, it was later, because of its A. Gamauf Æ F. Nittinger Æ E. Haring distinct coloration, assigned by Hargitt (1890) to the Museum of Natural History, Burgring 7, 1014 Vienna, monotypic genus Sapheopipo, which was placed by Austria Peters (1948) between the three-toed woodpeckers of the 104 genus Picoides and the strange Cuban monotypic genus white-backed woodpecker live on islands north of Oki- Xiphidiopicus. Peters (1948) probably did not suppose nawa. They are all heavily streaked below while the that it is closely related to either of these genera. Okinawa woodpecker does not show such streaks. The Goodwin (1968) argued that this woodpecker is not a only author who argued strongly for the placement of Picus relative at all, but a Dendrocopos species derived the Okinawa woodpecker into Dendrocopos was Good- from D. leucotos. Short (1973, 1982), who based his win (1968). systematic review of the family mainly on color patterns, In this contribution, we analyse partial nucleotide dismissed Goodwin’s (1968) arguments. He argued that sequences of the mitochondrial cytochrome b (cytb) gene coloration, habits and vocalizations suggest that the to evaluate the relationships of the Okinawa wood- Okinawa woodpecker belongs to the tribe Picini without pecker. We specifically test whether the Okinawa close relatives, but possibly representing a specialized woodpecker is a relative of Picus or Blythipicus,orof relict related to Picus and the Blythipicus–Gecinulus line. Dendrocopos, and discuss the results with respect to He left the Okinawa woodpecker in its monotypic genus. coloration, morphology, behavior and conservation. This position (see also Short 1982) was later adopted by Sibley and Monroe (1990), Winkler et al. (1995) and Winkler and Christie (2002). The latter authors, how- Methods ever, noted that the view of Goodwin (1968) has some merits (Winkler and Christie 2002; Winkler et al. 1995). Sampling and DNA extraction Leaving aside the possibility that the Okinawa woodpecker is not closely related to any extant species, We derived tissues (muscle, skin, blood, feathers) for there are only a few species that one might suggest as its DNA extractions from various sources: museum speci- close relatives. They all belong either to the Campethe- mens, collected feathers, living birds, or birds found rini or the Picini in the current system of woodpeckers dead (e.g., the individual of the Okinawa woodpecker). (Short 1982; Winkler and Christie 2002; Winkler et al. Remaining tissue and/or DNA is stored at the Labora- 1995). Yamashina (1941) left the question open and tory of Molecular Systematics, Museum of Natural noted that the Okinawa woodpecker exhibits similarities History Vienna. Table 1 lists the specimens investigated to both, the Dendrocopos group (as defined now) and the and the GenBank sequences included in the analyses. Picus group. Structural traits of bill, feet, and wings are DNA extractions from museum material (skin from similar to those in Dendrocopos, while coloration and the foot pads of study skins) were performed in a 10% habits resemble those of Picus. Chelex (Biorad) solution containing proteinase K The first describers and some later authors (Short (0.5 mg/ml). After incubation (4 h, 50°C, with agitation) 1973, 1982) agree that the Okinawa woodpecker belongs solutions were heated to 95°C for 5 min and centrifuged to the Picini. They designated it originally as Picus,at for 1 min. For purification and to remove short frag- that time a genus into which most medium-sized ments of degraded DNA the supernatant was purified woodpeckers were placed. Short (1973) called attention using the QIA Quick PCR Purification Kit (QIAGEN) to the many resemblances of Sapheopipo to Picus. Par- with a final volume of 50 ll elution buffer. DNA was ticularly, the gray-faced woodpecker shows tremendous also extracted from muscle, blood or feathers (preserved variation and one of its subspecies, the Sumatran in ethanol, buffer or frozen) by overnight incubation at P. canus dedemi, strongly resembles Sapheopipo and 37°C in extraction buffer (10 mM Tris–HCl pH 8.0, could thus serve as an example of how easily the latter’s 10 mM EDTA, 50 mM NaCl, 40 mM dithiothreitol, color patterns could have been derived from a Picus-like 1% SDS, 0.5 mg/ml proteinase K). DNA was purified ancestor. Geographically somewhat more distant, picine by two PCI (phenol/chloroform/isoamylalcohol, woodpeckers of the genera Blythipicus and Gecinulus 25:24:1) and one CI (chloroform/isoamylalcohol, 24:1) occur with two species each. They exhibit some simi- extractions followed by precipitation with 1/10 vol. 3 M larities in coloration and habits, particularly the two NaAc, 3· vol. EtOH 96%. Control extractions with Blythipicus species resemble Sapheopipo in several as- pure extraction buffer (without tissue) were prepared for pects. Geographically closest are the bay woodpecker the PCR experiments. B. pyrrhotis and the pale-headed woodpecker G. grantia. However, it is the maroon woodpecker B. rubiginosus,a Sundaland woodpecker, that resembles the Okinawa Polymerase chain reaction (PCR), cloning woodpecker so much that it could allegedly be mistaken and sequencing for it in the field (Short 1973) were their ranges not separated by thousands of kilometers. Polymerase chain reaction was carried out with an Ep- There are two campetherine species, both belonging pendorf Thermocycler in a volume of 25 ll, containing to the genus Dendrocopos, that show some resemblance 1 U Dynazyme DNA polymerase (Finnzymes OY), with the Okinawa woodpecker and that are biogeo- 0.5 lM of each primer, and 0.2 mM of each dNTP. The graphically more or less close. These are the white- solutions were heated to 95°C (2 min) and then subjected backed woodpecker, D. leucotos, and the great spotted to 30 reaction cycles: 95°C (10 s), 59°C (10 s), 72°C (30 s), woodpecker, D. major. Dark, reddish subspecies of the followed by a final extension at 72°C (5 min). Since the 105 Table 1 Specimens of woodpeckers used in this study. Designation Zoologisches Forschungsinstitut und Museum A. Koenig). Se- of specimens (Code) is derived from abbreviations of taxon names. quences determined in the present study (ps) and sequences ob- Material for DNA-extraction (Tissue): mu muscle, sk skin from the taines from GenBank (GB) are listed. Sequence: c complete foot pads of study skins, bl blood, fe feather. Voucher numbers are section, m medium section, s short section. Accession no: aWeibel given for museum specimens (KLIVV Konrad Lorenz Institute for and Moore (2002), bZink et al. (2002), cEspinosa de los Monteros Ethology; NMW Museum of Natural History Vienna; ZFMK (2000) Taxon Code Tissue Source Voucher Geographic origin, Sequence Accesion No.
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