A panel of polymorphic microsatellites in the Blue Eared Pheasant (Crossoptilon auritum) developed by cross-species amplification

Introduction

Jankowski's Bunting (Emberiza jankowskii) (Passeriformes: Embrizidae) was named by Taczanowski (1888). It is a small-sized grassland passerine with a body length (from bill to tail) ranging from 14.8 to 15.5 cm for males and from 14.5 to 15.5 cm for females (Gao, 2002) and can be distinguished easily from other buntings by its distinctive oval blackish-chestnut belly patch (Fig. 1a, b). It has been recently up-graded to Endangered in the IUCN Red List of globally threatened species since it is experiencing a drastic population decline (BirdLife International, 2010).

Figure  1.  Jankowski's Bunting and its habitats. (a) male, (b) female, (c) female and nestlings in the nest, (d) nest parasitized by the Common Cuckoo, (e) current breeding habitat at the Dagang Forest Farm, (f) current breeding habitat at Keerqinyouyiqian Qi, (g) historic breeding habitat at Xianghai, (h) historic breeding habitat at Hunchun. a, photo by Wenshi Qi; b–d, photos by Guohai Yu; e–h, photos by Haitao Wang.

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It has long been clear that the status of Jankowski's Bunting is in urgent need of re-evaluation. We provide updated information on its distribution and population trends at known breeding sites, based on unpublished data of field surveys conducted by us. We also describe the primary characteristics of breeding habitats, breeding biology of the remaining population at the Dagang Forest Farm and the threats faced by this bird, based mainly on our published data.

Distribution

Historically, two breeding populations of this species have been known: an eastern population, with recorded breeding sites located at Dongning in Heilongjiang Province, in the Yanbian area in eastern Jilin, the extreme south of the Russian Far East and the boundary region between Russia, China and D.P.R. Korea (Yamashina, 1957; Fu and Chen, 1966; Panov, 1973; Stresemann and Portenko, 1981; Zhao et al., 1994; Fig. 2). A western population has its recorded breeding sites at Siping, Baicheng and Songyuan cities in western Jilin Province and adjacent areas of Inner Mongolia (Fu and Chen, 1966; Zhao et al., 1994; Gao, 2002). No Jankowski's Buntings were found to breed in the middle areas between the eastern and western breeding distributions. The distribution of the bunting was described as "island-like" within its rather small breeding range (Fu and Chen, 1966).

Figure  2.  Distribution of Jankowski's Bunting. 1, breeding sites in Russia, i.e. Ussuriysk, Erdmana peninsula, Murav'yev-Amurskiy peninsula, Sedimi, Kraskino, Nagornaya, Pos'yeta bay, Krabbe peninsula, Sakpau lake and Tal'mi lake; 2, Manpo; 3, Samjiyon; 4, Hunchun; 5, Dongning; 6, Helong; 7, Antu; 8, Dunhua; 9, Nonnan; 10, Shuangliao; 11, Changling; 12, Daan; 13, Tongyu; 14, Taonan; 15, Yuquan; 16, Zhenlai; 17, Keerqinyouyiqian Qi; 18, Zhalaite Qi; 19, Qiqihaer; 20, Zhaodong; 21, Harbin; 22, Acheng; 23, Mudanjiang River; 24, Lishu; 25, Liaoyang; 26, Linxi; 27, Beidaihe; 28, Beijing.

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Jankowski's Bunting has vanished from most of its historic breeding sites during the past 40 years (Gao, 2002; Jiang et al., 2008). For the eastern population, no information has been reported in Russia since the early 1970s (Litvinenko, 1989; Litvinenko and Shibaev, 1999; BirdLife International, 2001). As well, no surviving birds were found during field surveys conducted by Wang et al. in 1997, 1999, 2004–2006 and 2010 in eastern Jilin and Dongning in Heilongjiang (unpublished data), with the last record for the eastern population in China occurring in 1980 (Fu et al., 1984). In the past, this species was recorded at Manpo and Samjiyon in the D.P.R. Korea, but no documentation is available of more recent information. Thus, the eastern population may already be extinct. The western population suffered a similar fate as the eastern population. Fu and Chen (1966) reported that the breeding range of the western population covered Taonan, Tongyu, Changling, Zhenlai in western Jilin and Tuquan in Inner Mongolia. After this, no subsequent information on the species within its breeding range has been reported for over 30 years. In 1994, Zhao et al. reported that the breeding population at Yushutai, Yaotuo and Xianghai still existed (Zhao et al., 1994); however, no birds could be found at the three breeding sites nor at most other historic breeding sites in western Jilin and Inner Mongolia during irregular field surveys conducted by Wang et al. from 1999 to 2010 (unpublished data). Its currently known breeding distribution is restricted to Xiergen and Xinjiamu of Keerqinyouyiqian Qi, Tumuji and Maanshan of Zhalaite Qi in Inner Mongolia and the Dagang Forest Farm of Zhenlai County in western Jilin (Jiang et al., 2008; Fig. 2).

The bunting is resident at most recorded breeding sites (Yamashina, 1957; Fu and Chen, 1966). Occasionally, the species makes some migratory movements during non-breeding seasons, and sporadic wintering populations or individuals were also recorded in several regions of Inner Mongolia, Heilongjiang, Liaoning, Hebei, Beijing and the D.P.R. Korea (Morrison, 1948; Su, 1963; Stresemann and Portenko, 1981; Cheng, 1987; Huang, 1989; Fig. 2). The precise migration pattern, selection of wintering habitats and distribution for the species are still unclear.

Population size

The remaining population of Jankowski's Bunting in the Dagang Forest Farm grassland has undergone a dramatic decline in numbers from c. 60 pairs in 1999 to c. 10 pairs in 2010 (Fig. 3). The population size at Tumuji has remained relatively constant at about three pairs (ranging from one to five pairs; Fig. 4). The breeding population at Maanshan has been monitored since 2001. Its population declined from c.11 pairs in 2001 to around three pairs in 2008 and no birds were detected in 2010 (Fig. 5). Xiergen and Xinjiamu of Keerqinyouyiqian Qi are new, recently found breeding sites for the Jankowski's Bunting. The observed maximum population size at Xiergen was 39 (25 males) in 2008, 47 (26 males) in 2009 and 53 (29 males) in 2010; for the Xinjiamu population it was 4 (2 males) in 2008, 8 (all males) in 2009 and 13 (9 males) in 2010 (unpublished data).

Figure  3.  Population size of Jankowski's Bunting detected in 1999–2010 (except for 2003) surveys at the Dagang Forest Farm grassland in western Jilin

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Figure  4.  Population size of the Jankowski's Bunting detected in 2001–2010 (except for 2003) surveys at the Tumuji National Nature Reserve in Inner Mongolia

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Figure  5.  Population size of the Jankowski's Bunting detected in 2001–2010 (except for 2003, 2006 and 2009) surveys at Maanshan in Inner Mongolia

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Breeding biology

The breeding season of the western population located at the Dagang Forest Farm extends from late April to late July, earlier than that of the eastern population (Yamashina, 1957; Jiang et al., 2008), which is likely caused by geographical differences. The buntings build nests under dense grass on the ground, sometimes at the base of Armeniaca sibirica or other small trees. The internal direction of the nests is mostly oriented to 45° southeast and externally 45° southwest nest building lasts for around 6–11 days (Gao et al., 2002; Jiang et al., 2008), with clutch size decreasing with nest-initiation date. The following breeding parameters were observed or measured: mean clutch size 5.26 ± 0.76 eggs (ranging from 4–7 eggs), egg laying period 5.57 ± 1.04 days (ranging from 4–8 days), incubation period 12.17 ± 0.87 days (ranging from 11–14 days), nestling period 11.45 ± 1.04 days (ranging from 10–13 days). The overall probability of Mayfield nest success to fledging is 0.218 ± 0.007 (Jiang et al., 2008). Incubation is carried out exclusively by females, with 35.0%, 74.5% and 67.6% of daytime spent for incubation during the early, middle and late incubation period respectively, while both sexes participate in building the nest, feeding the young and defending the nest (Tong et al., 2002a; Bai et al., 2003a; Jiang et al., 2008; Fig. 1a, c). Young have been observed being brought grasshoppers, caterpillars and spiders and their cocoons as food (Byers et al., 1995). Several investigators considered that Jankowski's Bunting may raise two broods per breeding season (Stresemann and Portenko, 1981; Tong et al., 2002a); however, no detailed investigations have been conducted so far on the subject.

The reproductive progress of Jankowski's Bunting is vulnerable to disturbance. A low reproductive success may be a factor causing a decline in the number of populations and the slow recovery of populations from low reproductive periods. Known causes leading to low nest success include nest parasitization by the Common Cuckoo (Cuculus canorus) (Fig. 2c), nest predation by snakes and ants or potential nest predators such as the European Suslik (Citellus citellus) and the Amur Falcon (Falco amurensis), anthropological activities such as grazing and nest-robbing by fruit-pickers and shepherds, disease or sibling competition, nest abandonment, a lack of fertilization or embryo death (Cheng et al., 2002; Tong et al., 2002b; Bai et al., 2003a; Jiang et al., 2008).

Habitats

Jankowski's Bunting breeds in a variety of open habitats at low elevations. The western population occupies mainly the Mongolian steppes or low hills with grass species dominated by Filifolium sibiricum, Stipa baicalensis and Spodiopogon sibiricus, interspersed by Armeniaca sibirica (Gao, 2002; Gao et al., 2003). The currently known population still breeds in such habitats (Fig. 1e, f). The western population was reported to breed in savanna-like habitats with mixed shrubs of A. sibirica, Ulmus macrocarpa and U. pumila at Xianghai (Gao et al., 2002; Fig. 1g), and in afforested habitats with young Pinus sylvestris mongolica and Populus at Yaotuozi of Changling (Zhao et al., 1994). The eastern population once bred on low hills, in meadows or on coastal plains with xerophilous grass species and scattered young oak bushes, where the vegetation structure was distinct from the surrounding habitats (Yamashina, 1957; Stresemann and Portenko, 1981; Fig. 1h).

Threats

The main reason for the possible extinction of the eastern population and drastic reduction of breeding distribution in the western population in China is the conversion of its suitable habitats into cultivated areas and possibly forest plantations. In western Jilin, over 70% native grasslands have been lost since the 1960s (Jiang et al., 2008). In Russia, Shulin (1928 in Stresemann and Portenko, 1981) reported that fires, started for agricultural purposes, affected the habitat of the bunting adversely and thus prevented its breeding. Potentially suitable habitats remaining in Russia (and presumably also in the D.P.R. Korea) are threatened by the implementation of the large-scale Tumangan Development Project (BirdLife International, 2010). These changes may lead to reduced re-colonization of its suitable habitats. In addition, unduly grazing severely destroyed the suitable microhabitats of Jankowski's Bunting, particularly grassland with Armeniaca sibirica (Gao et al., 2003; Jiang et al., 2008). Other factors such as drought and balefires may also pose a severe threat to the breeding and survival of the species, e.g., the annual average rainfall during 1999–2001 was only 235.3 mm, far below the average of 434.8 mm during 1981–1998 (Cheng et al., 2002; Bai et al., 2003b; Jiang et al., 2008).

Conservation

The preferred habitats of Jankowski's Bunting are grasslands with stunted shrubs (especially A. sibirica). The bird is sensitive to habitat loss and changes of vegetation (Gao et al., 2002). Protecting the availability and structure of its remaining breeding habitats, as well as restoring parts of its historical breeding habitats are important to ensure the continued presence of this species. The breeding habitats of Tumuji and Xiergen are well kept because they are shaded in the Tumuji and Kerqin National Nature Reserve. The current status of three other known breeding sites of Jankowski's Bunting is not encouraging. At the Dagang Forest Farm, the natural vegetation is seriously destroyed by excessive grazing (Jiang et al., 2008). At Maanshan, the suitable habitat is reduced in area and degraded in quality due to cultivation and grazing. The population at Xiergen is distributed in a small area encircled by rail fences, but the site would be unworkable if the rail fences were demolished. The Maanshan is adjacent to the Tumuji National Nature Reserve and the Xiergen borders the Keerqin National Nature Reserve. We suggest therefore that responsibility for these breeding sites should be taken over by the two Nature Reserve administrations.

Jankowski's Bunting is a species of which few in-depth investigations have been carried out and factors that may potentially affect its survival remain largely unknown. Therefore, beside protecting the remaining breeding habitats of the bunting, we suggest that: 1) persistent surveys covering its historic distribution and potential distribution should be undertaken to obtain more reliable data on its population size, breeding distribution and wintering habitat; 2) studies on genetic population structures and diversity of the species should be conducted to obtain theoretical references and some genetic background information and 3) studies on dispersal patterns should be conducted to obtain data on its ability of re-colonizing or supplying individuals to more distant sites, which might be important for making suitable and effective management decisions and measures to protect Jankowski's Bunting.

Acknowledgements

We thank Guohai Yu for providing some of the photos of the Jankowski's Bunting (Fig. 1b, d), Zhenxin Li for assistance in preparing the distribution map. We also thank professor Zhengwang Zhang for his helpful remarks on this paper. The work on the Jankowski's Bunting was supported by the National Natural Science Foundation of China (Grants 30370183, 39870117).