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Current Status of the Northern Goshawk Accipiter Gentilis in Japan Based on Mitochondrial DNA

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Current Status of the Northern Goshawk Accipiter Gentilis in Japan Based on Mitochondrial DNA Ornithol Sci 7: 143–156 (2008) ORIGINAL ARTICLE Current status of the Northern Goshawk Accipiter gentilis in Japan based on mitochondrial DNA Shigeki ASAI1,#, Daisuke AKOSHIMA2, Yoshihiro YAMAMOTO3, Yoshimitsu SHIGETA1, Masahiko MATSUE4 and Hiroshi MOMOSE4,* 1 Yamashina Institute for Ornithology, 115 Konoyama, Abiko, Chiba 270–1145, Japan 2 Laboratory of Wild Animals, Department of Applied Biophilia, Faculty of Agriculture, Tokyo University of Agriculture, 1737 Funako, Atsugi, Kanagawa 243–0034, Japan 3 Department of Genetics, Hyogo College of Medicine, 1–1 Mukogawa, Nishinomiya, Hyogo 663–8501, Japan 4 Landscape and Ecology Division, Environment Department, National Institute for Land and Infrastructure Management, 1 Asahi, Tsukuba, Ibaraki 305–0804, Japan Abstract Although the Northern Goshawk Accipiter gentilis is not designated a ORNITHOLOGICAL threatened species in Japan, it is thought that its population once experienced a de- SCIENCE crease. To evaluate the current status of the goshawk, we sequenced the mitochondrial © The Ornithological Society DNA control region and determined its variation among individuals. Considering that of Japan 2008 part of the Japanese population migrates or moves seasonally, we divided the samples into two categories (breeding and non-breeding season, based on sampling dates) and then calculated indices of genetic diversity and statistics for each category. Among 145 samples, we found ten haplotypes, of which two were dominant in both fre- quency and range. Haplotype diversity and nucleotide diversity were 0.63Ϯ0.04SD and 0.0018Ϯ0.0014SD, respectively. Comparing this diversity with those of other species, we concluded that the status of the Northern Goshawk in Japan is neither urgent nor secure. Significant genetic distance was not detected between the breeding and non-breeding groups, thus we could find no evidence of seasonal movement. The long-term effective female population size was estimated at 3,000 to 30,000 individu- als. A recent population decline was not detected from the mismatch distribution. Therefore, the past population decline of the goshawk may not have been very seri- ous. Future studies should consider the genetic structure of goshawks that inhabit other areas near Japan. Key words Accipiter gentilis, Control region, Genetic diversity, Goshawk, Mito- chondrial DNA The Northern Goshawk Accipiter gentilis was des- result of urbanization of this species, or true growth ignated a threatened species in the Red Data Book of (e.g. Research Division, Wild Bird Society of Japan Japan (Ministry of the Environment 2002). However, 1984; Ohba 1988; Endo 1989; Koita et al. 1997; the government of Japan eliminated this species from Kawakami & Higuchi 2003). It is unknown to what the threatened species list in 2006, because the popu- extent the goshawk declined in the past, due to a lack lation size was estimated to be sufficiently larger than of comparable data on population sizes. Nevertheless, it was two or three decades ago. The growth in the many researchers believe that this species was rare in estimated population size could result from previous the past (Ohba 1988; Endo 1989; Koita et al. 1997). underestimations due to insufficient questionnaire In general, it is assumed that genetic diversity in a surveys, recent high incidences of observation as a diminished population of a threatened species is low due to genetic drift. A decline in genetic diversity (Received 18 June 2008; Accepted 29 October 2008) would reduce the adaptability of a population to envi- # Corresponding author, E-mail: [email protected] ronmental fluctuation (Primack & Kobori 1997; * Present Address: Eastern Region Research Subteam for Wildlife Management, National Agricultural Research Center, 3–1–1 Frankham et al. 2002). If the Goshawk had under- Kannondai, Tsukuba, Ibaraki 305–8666, Japan gone a population decline with reduced genetic diver- 143 S. ASAI et al. sity, it could still be considered threatened. Therefore, variation (Baker & Marshall 1997). A primer set to it is necessary to determine genetic diversity to assess amplify the CR is a prerequisite for genetic studies, the true current status of this species. Our aim is to and thus we first had to sequence a region of mtDNA document the genetic structure of the goshawk in containing the CR in a preliminary experiment to de- Japan, based on variation among mitochondrial DNA sign the primers (unlike the cytochrome b region, for sequences. which universal primers can be used). We determined In Japan, the goshawk is a resident of Hokkaido, the complete DNA sequence of the mitochondrial Honshu, Shikoku, and Kyushu (Committee for genome. Check-list of Japanese Birds 2000). However, in the Total cellular DNA was extracted from a tissue southwestern part of the range, breeders are uncom- sample of a goshawk preserved at the Yamashina In- mon while wintering birds are common (Morioka et stitute for Ornithology (Accession ID: 1999-0198). al. 1998; Committee for Check-list of Japanese Birds The complete 18,266-bp nucleotide sequence (DDBJ 2000). In addition, this species is observed annually Accession No. AP010797) was determined using de- at Cape Irago, a famous stopover point over which scribed procedures (Yamamoto et al. 2000). The PCR raptors migrate (e.g. Tsuji 1988; Kawakami & primers AG50 (5Ј-GGC GGT TGC TAT GAG GGT Higuchi 2003). Kudo (2008) reported that two satel- TAG AAG GAG AAT GAT GC-3Ј) and AG30 (5Ј- lite-tracked individuals migrated from Hokkaido to CAG AAT GAT ATT TCC TAT TCG CAT ACG Honshu. In Europe and North America, Northern CTA TCC TAC-3Ј) were made from the cytochrome Goshawks move southward in winter, even if they are b sequences of a goshawk previously registered in the not always migratory (Cramp & Simmons 1979; DDBJ (Accession No. X86738), in order to amplify Kenward 2006). Some goshawks that breed in Utah the rest of the mitochondrial genome. The total se- migrate there from 100–613 km away (Sonsthagen et quence was then determined using the M13 shotgun al. 2006), whereas other birds are considered resi- method. dents (Underwood et al. 2006). From the data avail- In contrast to the gene order of Gallus gallus (Oki- able it seems that at least part of the goshawk popula- moto et al. unpublished), the CR of the goshawk is tion in Japan moves seasonally. located between tRNA-thr and tRNA-pro. At the po- Genetic structure may reveal seasonal movements. sition where the CR is found in many other birds, the For example, if haplotypes found in the breeding sea- goshawk has a non-coding region (pseudo-CR) be- son are replaced by others in the non-breeding sea- tween tRNA-glu and tRNA-phe, as in other raptors son, it is plausible that breeders emigrate and individ- including Common Buzzard Buteo buteo (Haring et uals breeding elsewhere immigrate. Regarding ge- al. 1999), Peregrine Falcon Falco peregrinus (Min- netic diversity, we must also discriminate wintering dell et al. 1998), and Mountain Hawk Eagle Spizaetus birds; not doing so could lead to overestimates of ge- nipalensis (Asai et al. 2006). netic diversity of the original Japanese population. We discuss the seasonal movement of the goshawk 2) DNA samples and determination of haplo- based on sampling dates and the phylogeny of each types haplotype. Samples were mainly collected from four sources: If the Japanese goshawk experienced a relatively 29 blood samples collected by the National Institute recent bottleneck, this should be evident in its genetic for Land and Infrastructure Management from structure. We also discuss a recent demographic event Ichikai-machi, Tochigi Prefecture, between 1999 and in the Japanese population, by calculating the effec- 2001 (two of them were considered as one sample be- tive population size and depicting the frequency of cause the two individuals were deemed to be broth- pairwise sequence differences. ers); 37 feathers collected by the River Bureau, the Ministry of Land, Infrastructure, Transport, and MATERIALS AND METHODS Tourism, and the Incorporated Administrative Agency, Japan Water Agency, between 2000 and 1) Determination of the complete mtDNA se- 2006; tissues from carcasses deposited at the Ya- quence mashina Institute for Ornithology; and blood samples Due to its high variability, the control region (CR) from injured birds at conservation centers. Because of mitochondrial DNA (mtDNA) is thought to be some feathers collected at the same time resulted in most appropriate for detecting intraspecific genetic the same haplotype, we considered them to be from 144 Status of Goshawk based on mtDNA the same individual, and thus dealt with them as one wood et al. 2006). Therefore, it is reasonable to as- sample. Excluding samples whose collecting sites sume that samples collected from March to July rep- and dates were unknown, we analyzed a total of 145 resent the breeding distribution in Honshu. We then samples. calculated indices of genetic diversity and statistics We extracted DNA from the samples using a for each category. We considered samples from Sep- DNeasy Tissue Kit (QIAGEN) according to the man- tember in Hokkaio to represent breeding distribution ufacturer’s guidelines. We designed a primer set (Ag- (no samples were collected during either March or ContRegFa 5Ј- TCT TCC CAC TAA CCG GAG April in Hokkaido). We considered three categories CCC -3Ј and AgContRegRa 5Ј- CCT GAA GCT of breeding season: long (February to July), standard GGG AAC GTA GGG -3Ј) to amplify a 625-bp frag- (March to July), and short (April to July). ment containing a highly variable part (domain I; de- fined as a 448-bp region from the 5Ј-end of the CR to 4) Haplotype analysis the 5Ј-adjacent site of the F box, a conserved se- To construct phylogenetic trees, appropriate substi- quence block in the CR; see Baker & Marshall 1997), tution models for the datasets were determined based based on the complete mtDNA sequence. PCR was on the Akaike Information Criterion (AIC; Akaike conducted following standard procedures using Ex 1974) calculated using MrModeltest2 (Nylander Taq (TaKaRa) at an annealing temperature of 62°C.
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