Improvement on molecular sex identification primers for Passeriform bird species

Introduction

The coastline of the Chinese mainland stretches 18000 km and spans temperate, subtropical and tropical regions, but seabirds along the coastline have seldom been studied in China prior to the last decade (Melville, 1984; Hsu and Melville, 1994). Approximately 33 species of seabirds were believed to be breeding in China, but little was known of their distribution and populations, especially for those species breeding offshore (Melville, 1984). This situation has gradually changed since 2000, when the critically endangered Chinese Crested Tern (Thalasseus bernsteini) was rediscovered on Matzu Island off the coast of Fujian Province (Liang et al., 2000). The coastlines of Shandong, Zhejiang and Fujian provinces drew the most attention due to the presence of the Chinese Crested Tern and other breeding seabirds (Chen et al., 2005, 2009; Jiang et al., 2005; Liu et al., 2009).

There are 3061 islands off the Zhejiang coast, constituting 43.9% of all islands in China. Ornithological studies in Zhejiang, as in the rest of China, have long focused on terrestrial avifauna. Most of the information about seabirds in Zhejiang came from early museum collections (Shaw, 1934; Zhuge, 1990). Many species were again ignored during terrestrial wildlife surveys conducted from 1995 to 2000 throughout Zhejiang Province (Tao, 2002). A few surveys were conducted on avifauna on several larger islands, most of which were inhabited (Zhuge et al., 1986; Zhu, 1990; Zhu et al., 1991; Tao, 2002) and in two newly created marine nature reserves (Chen et al., 2007; Liang et al., 2007; Wang et al., 2008). Zhou (1998) indicated that a few islands, reported by fishermen and other non-experts, had breeding seabirds. The situation of most of the uninhabited islands off the Zhejiang coast remained unknown.

From 2003 to 2006, we conducted breeding seabird surveys along the Zhejiang coast, with the aim to search for new breeding colonies of the critically endangered Chinese Crested Tern and investigate the species, population size, distribution of and threats to other breeding seabirds on the islands off the Zhejiang coast. In 2004, we found a small breeding colony of Chinese Crested Terns on the Jiushan Archipelago (Chen et al., 2005).

Study area and methods

The Zhejiang coastline stretches over 6500 km (Fig. 1), from about 27°06′N to 31°11′N and is bordered by the East China Sea. The southern part of the coast meets Fujian Province, which is adjacent to the Taiwan Strait. Of all the islands off the Zhejiang coast, 2886 uninhabited islands account for 94.3%. About 1383 islands are situated off the northern coastline, forming the Zhoushan island region.

Figure  1.  Zhejiang coast and islands surveyed for breeding seabirds. 1, Shengsi; 2, Qiqu; 3, Huoshan; 4, Qushan; 5, Changtu; 6, Zhongjieshan; 7, Wuzhishan; 8, Putuo; 9, Meisan; 10, Jiushan; 11, Nantian; 12, Yushan; 13, Taizhou; 14, Luxi; 15, Dongtou; 16, Beiji; 17, Nanji.

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The breeding season of seabirds in Zhejiang lasts from May to September (Zhuge, 1990; Yan et al., 2006). We conducted our surveys from June to August, when breeding colonies are relatively stable. During 6–18 June 2003, we surveyed the northern Zhejiang coast, including the Shengsi, Qiqu and Huoshan archipelagos, as well as Qushan and adjacent islands. From 14 June to 1 August 2004, we surveyed the northern and central Zhejiang coast, including the Wuzhishan, Zhongjieshan and Changtu archipelagos, Putuo and adjacent islands as well as the Jiushan Archipelago. From 12 July to 11 August 2005, the Zhongjieshan, Wuzhishan and Jiushan archipelagos were revisited for Chinese Crested Terns and from 9 June to 4 August 2006, we surveyed the central and southern Zhejiang coast, including the Meisan and Yushan archipelagos, Nantian and adjacent islands, the Taizhou Archipelago, Luxi and adjacent islands, as well as the Dongtou, Beiji and Nanji archipelagos.

Since no seabirds had been found breeding on inhabited islands, we focused our efforts on uninhabited ones. In total, we surveyed 2740 islands, comprising 95% of the uninhabited islands and reefs along the Zhejiang coast. Some remote islands were excluded, such as the Langgan Archipelago, Haijiao island in the Shengsi Archipelago, the Liangxiongdi and Sijiemei islets in the Zhongjieshan Archipelago and the islands in Hangzhou Bay. During each survey, we interviewed local fishermen about breeding seabirds and islands beforehand and then visited all uninhabited islands and reefs in each area, paying special attention to the areas mentioned by the fishermen.

Each survey team generally consisted of 3–5 members. Our transportation vehicles were mainly rented fishing boats. When the boat approached an island where breeding seabirds inhabited, the birds would fly upward due to the noise from the motor. Once a breeding colony was detected, we would observe with binoculars and take photographs to identify the breeding species and estimate their population size. We generally counted birds in the air and corroborated the count with photographs. For small colonies of fewer than 20 birds, we would count all individual birds. For larger colonies, we adopted the method of estimating the number of birds in densely packed flocks, as described by Bibby et al. (2007), i.e., we counted the flock by tens or even hundreds according to the size of the flock. Then we reached an estimated population size by taking the mean of independent counts by different observers. Finally, we landed on each island to confirm whether it was a breeding site or just a roosting site and to investigate and confirm the island characteristics listed in Zhejiang Islands (Zhou, 1998). We remained on a breeding island as little time as possible, usually no more than 20 min to avoid further disturbance (Gaston, 2004).

Results

During our surveys conducted over four breeding seasons, we recorded 11 species of seabirds: Great Frigatebird (Fregata minor), Great Cormorant (Phalacrocorax carbo), Swinhoe's Storm Petrel (Oceanodroma monorhis), Black-tailed Gull (Larus crassirostris), Bridled Tern (Sterna annethetu), Roseate Tern (S. dougallii), Black-naped Tern (S. sumatrana), Sooty Tern (S. Fuscata), Little Tern (S. albifrons), Greater Crested Tern (Thalasseus bergii) and Chinese Crested Tern (T. bernsteini) (Plate I). Among these, six species, i.e., Larus crassirostris, Sterna annethetu, S. dougallii, S. sumatrana, Thalasseus bergii and T. bernsteini were documented as breeding in 49 colonies on 28 islands off the coast of Zhejiang Province (Table 1).

  Plate I.  Breeding seabirds along the Zhejiang coast. (a) The Black-tailed Gulls; (b) The Black-tailed Gulls on the Jiushan Archipelago; (c) The Bridled Tern; (d) The Bridled Terns on the Beiji Archipelago; (e) The Chinese Crested Tern and the Greater Crested Tern; (f) The breeding ground of Chinese Crested Terns and Greater Crested Terns on the Jiushan Archipelago; (g) The Roseate Tern; (h) The Roseate Terns on the Taizhou Archipelago. Photos by Shuihua Chen.

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Table  1.  Breeding seabirds and their distributions along the Zhejiang coast

Archipelago	Island	Latitude	Longitude	Species and population size (mean ± SE) a
				BTG	BT	RT	BNT	GCT	CCT b
Qushan	Huangzexiaoshan	30°31′02″	122°18′43″	307 ± 30
Zhongjieshan	Shizhushan	30°11′07″	122°42′45″		1367 ± 153	170 ± 10	173 ± 6
	Xiaopanjiao	30°08′08″	122°45′14″				27 ± 1
	Yezishan	30°10′19″	122°39′51″		2467 ± 153	303 ± 21	97 ± 6
Changtu	Wujiao	30°14′30″	122°28′26″			10 ± 1	38 ± 3	18 ± 1
	Xiaomeimeijiao	30°13′43″	122°33′25″				10 ± 0
Huoshan	Dongkuaijiao	30°19′52″	121°52′08″				11 ± 0
Wuzhishan	Mantoushan	30°13′56″	121°53′49″	850 ± 50
	Longdongshan	30°13′40″	121°53′24″	483 ± 76
	Yaqueshan	30°13′34″	121°53′43″	103 ± 15
	Wumaoshan	30°13′51″	121°53′38″				18 ± 1
Meisan	Xiexuantou	29°36′10″	122°08′25″	65 ± 5
Jiushan	Jiangjunmao	29°22′47″	122°13′54″					4000 ± 200	15 ± 5
	Nanerduo	29°22′34″	122°13′35″	197 ± 25
	Xiaoqingshan	29°27′40″	122°14′49″	193 ± 15
	Qilingtou	29°22′45″	122°15′19″	497 ± 45			12 ± 1
	Mabushan	29°22′52″	122°11′23″	283 ± 15
Yushan	Fuhujiao	28°53′18″	122°16′25″		900 ± 100			15 ± 0
Nantian	Shamaoyu	29°06′15″	122°01′46″	367 ± 15	350 ± 50
	Youcaihuayu	29°01′44″	122°01′30″	187 ± 6	187 ± 12
Taizhou	Niaodao	28°23′53″	121°54′53″		93 ± 6	18 ± 1
	Zhunandao	28°25′42″	121°51′16″			36 ± 2	29 ± 1
	Shewei	28°32′15″	121°55′10″		197 ± 6	80 ± 5	47 ± 3	19 ± 1
Luxi	Nanpanshanyu	28°00′20″	121°15′42″	1400 ± 100
Dongtou	Shuangfengshan	27°41′50″	121°08′21″	537 ± 32			28 ± 3
Beiji	Xiaoxiaojiyu	27°40′01″	121°11′39″		1367 ± 58		19 ± 1
Nanji	Xiamaan	27°25′13″	121°00′50″	467 ± 15			17 ± 1
	Xiaochaiyu	27°25′20″	121°05′33″	19 ± 1	29 ± 1		7 ± 1
Total	28 islands			15 colonies	9 colonies	6 colonies	14 colonies	4 colonies	1 colony
a 1) BTG, Black-tailed Gull; BT, Bridled Tern; RT, Roseate Tern; BNT, Black-naped Tern; GCT, Greater Crested Tern; CCT, Chinese Crested Tern. These abbreviations also apply to Table 2. 2) Wuzhishan, Zhongjieshan and Jiushan were visited twice. This table only lists data from the first survey in 2004. b This data had been separately reported in Chen et al. (2005).

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All the breeding colonies were located on uninhabited small islands. The major characteristics of seabird breeding islands are presented in Table 2.

Table  2.  Characteristics of seabird breeding islands along the Zhejiang coast ^a

Species	Area (m2)				Elevation (m)				Distance to continent (km) b			Vegetation type
	Min.	Max.	Mean		Min.	Max.	Mean		Min.	Max.	Mean
BTG	5697	136746	33540		18.5	87.9	41.6		4.7	51.0	25.5	Grass; Grass and shrub
BT	3649	73655	30641		32.4	58.0	42.7		4.7	64.0	33.7	Grass
RT	4891	44075	17350		12.0	58.0	34.3		19.5	64.0	41.3	Grass
BNT	3596	136764	26928		9.4	87.9	35.2		19.5	65.5	41.6	No vegetation; Grass
GCT	4891	22101	12320		12.0	46.6	32.5		25.6	50.9	35.1	No vegetation; Grass; Grass and shrub
CCT	15247	15247	15247		40.9	40.9	40.9		25.6	25.6	25.6	Grass and shrub
Total	3596	136764	24420		9.4	87.9	35.7		4.7	65.5	32.8
a Data of area and elevation are from Zhejiang Islands (Zhou, 1998). b Distances to mainland were measured using Google Earth.

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Discussion

The Great Frigatebird, Swinhoe's Storm Petrel, the Bridled Tern, the Sooty Tern and the Chinese Crested Tern were new additions to the records of Zhejiang avifauna from these surveys (Zhuge et al., 1986; Tao, 2002; Chen et al., 2005). Among the 11 species of seabirds recorded, only six species were documented as breeding in this area. Only one bird from each of four species, i.e., the Great Frigatebird, the Great Cormorant, Swinhoe's Storm Petrel and the Sooty Tern, was recorded, which were probably vagrants led astray by typhoons. The results of our surveys were consistent with the findings of Hsu and Melville (1994), Cao et al. (2007) and Chen (2010) that the Great Cormorant and Swinhoe's Storm Petrel bred further north in Jiangsu and Shandong provinces and that the Great Frigatebird and Swinhoe's Storm Petrel bred further south, in the South China Sea. The Little Tern was recorded at sea in a small colony and probably breeds on mainland beaches (Zhuge et al., 1986).

Previous studies (Zhuge et al., 1986; MacKinnon et al., 2000; Tao, 2002) have indicated that Bulwer's Petrel (Bulweria bulwerii), the Streaked Shearwater (Calonectris leucomelas), the Brown Noddy (Anous stolidus), the Common Tern (Sterna hirundo), the Gull-billed Tern (Gelochelidon nilotica) and the Caspian Tern (Sterna caspia) might be summer residents along the Zhejiang coast, but these species were not observed during our surveys. These historical records suggest that some species were either extirpated from historical breeding sites or simply passengers or vagrants at sea during the summer season. Nevertheless, their breeding status along Zhejiang coast needs further study.

Of the species found breeding, the Black-tailed Gull and the Black-naped Tern were relatively abundant and widely recorded in most survey areas. The Chinese Crested Tern, a critically endangered species with an estimated global population of no more than 50 birds and only two small breeding populations, was found on the Matzu Archipelago in Fujian Province and the Jiushan Archipelago in Zhejiang Province (Liang et al., 2000; Chen et al., 2009).

According to the "1% of biogeographic population thresholds" that govern the selection of Important Bird Areas (IBAs) under criterion A4i, i.e., for 1600 Black-tailed Gulls, 1000 Bridled Terns, 200 Roseate Terns, 150 Black-naped Terns, 200 Greater Crested Terns and 1 Chinese Crested Tern in East Asia (BirdLife International, 2004), the Zhongjieshan, Jiushan and Beiji archipelagos meet the IBA criterion, while the Wuzhishan, Yushan and Taizhou archipelagos are close to the threshold. These areas are important breeding sites for seabirds in Zhejiang.

Chen et al. (2009) reported that egg collection, disturbance, sea water pollution and over-fishing are major threats to the survival of the critically endangered Chinese Crested Terns and other breeding seabirds along the Zhejiang coast. Of these factors, egg collection is thought to be the most severe threat and is very common in the coastal regions surveyed. The situation has deteriorated along with recent rapid economic development. The results of our surveys also indicate that most breeding sites of seabirds suffer, to varying extent, from egg collection.

The creation of nature reserves is one of the major measures of wildlife conservation in China. Among these seabird breeding sites, three nature reserves have been established, i.e., the Wuzhishan Islands Bird Provincial Nature Reserve in Zhoushan, the Jiushan Archipelago Oceanic National Nature Reserve in Ningbo and the Nanji Archipelago Oceanic National Nature Reserve in Wenzhou. Most breeding sites of seabirds are not protected by legislation. This situation might be caused by the lack of detail information of breeding seabirds for these islands. Although forestry administrations are supposed to be responsible for the conservation of terrestrial wildlife, including seabirds, these administrations usually do not have the jurisdiction and ability to enforce laws at sea. In contrast, oceanic administrations, which take responsibility for the management, monitoring and conservation of aquatic wildlife, do not have jurisdiction over the conservation of seabirds. The recently enacted Law of the People's Republic of China on Island Protection emphasizes the conservation of biodiversity on uninhabited islands. We hope that the situation will improve in the near future.

Acknowledgments

This study was funded by the National Natural Science Foundation of China (No. 30570251), Zhejiang Provincial Natural Science Foundation (No. Y5090070) and a WWF China Small Grant.