Skip to main content

Advertisement

Identification of coastal wetlands of international importance for waterbirds: a review of China Coastal Waterbird Surveys 2005–2013

Abstract

Background

China’s coastal wetlands belong to some of the most threatened ecosystems worldwide. The loss and degradation of these wetlands seriously threaten waterbirds that depend on wetlands.

Methods

The China Coastal Waterbird Census was organized by volunteer birdwatchers in China’s coastal region. Waterbirds were surveyed synchronously once every month at 14 sites, as well as irregularly at a further 18 sites, between September 2005 and December 2013.

Results

A total of 75 species of waterbirds met the 1 % population level Ramsar listing criterion at least once at one site. The number of birds of the following species accounted for over 20 % of the total flyway populations at a single site: Mute Swan (Cygnus olor), Siberia Crane (Grus leucogeranus), Far Eastern Oystercatcher (Haematopus osculans), Bar-tailed Godwit (Limosa lapponica), Spotted Greenshank (Tringa guttifer), Great Knot (Calidris tenuirostris), Spoon-billed Sandpiper (Calidris pygmeus), Saunders’s Gull (Larus saundersi), Relict Gull (Larus relictus), Great Cormorant (Phalacrocorax carbo), Eurasian Spoonbill (Platalea leucorodia), Black-faced Spoonbill (Platalea minor) and Dalmatian Pelican (Pelecanus crispus). A total of 26 sites supported at least one species of which their number met the 1 % criterion. Forty-two species met the 1 % criterion in the Yellow River Delta, Shandong; 29 at the Cangzhou coast, Hebei and 26 species at the Lianyungang coast, Jiangsu.

Conclusions

The results highlight the international importance of China’s coastal wetlands for waterbirds. This study also demonstrates that participation of local birdwatchers in waterbird surveys results in data that are invaluable not only for understanding the current status of waterbirds in China’s coastal regions but also for waterbird conservation and management.

Background

China’s coastal wetlands provide critical breeding, stopover and wintering sites for millions of waterbirds along the East Asian-Australasian Flyway. Unfortunately, coastal wetlands have been severely altered through reclamation, pollution, the spread of invasive species and over-harvesting of marine organisms (MacKinnon et al. 2012; Ma et al. 2014; Hua et al. 2015). Waterbirds are not only conservation targets, but also indicators of the quality and importance of wetlands. Over the past several decades, waterbird surveys have been conducted along China’s coasts. For example, between 1996 and 2005, Mark Barter and colleagues conducted surveys of migrating shorebirds in the Yellow Sea region (Barter 2002) and wintering bird surveys were conducted in Fujian (Barter et al. 2007). Waterbirds were also surveyed in nature reserves, especially focusing on threatened species such as the Red-crowned Crane (Grus japanensis) (Su and Zou 2012) and the Chinese Crested Tern (Sterna bernsteini) (Fan et al. 2011), while synchronous waterbird surveys have been conducted in some reserves continuously throughout the years. All these surveys have provided basic data for conservation and management measures.

However, the current population status of most waterbird species is still largely unclear, especially outside nature reserves where waterbird surveys have seldom been conducted. More recently, birdwatching has become increasingly popular in China; over 30 birdwatching societies have been established and the number of birdwatchers continues to increase (Ma et al. 2013). Since 2005, birdwatchers in China’s coastal regions have organized and conducted synchronous waterbird surveys once every month (China Coastal Waterbird Census Group 2009, 2011). These provide basic data in order to understand the status of waterbirds in coastal regions. Our surveys complement those of wintering waterbirds reported by Cui et al. (2014).

The criteria for the identification of ‘wetlands of international importance’ under the Ramsar Convention on Wetlands of International Importance Especially as Waterfowl Habitat include two that relate specifically to waterbirds: criterion 5 states that a site should regularly support 20000 or more waterbirds, while criterion 6 insists that the site should regularly support 1 % of the number of individual birds in a population of a species or subspecies of waterbirds (Ramsar Convention Secretariat 2010). Wetlands International regularly reviews waterbird populations and publishes the number of birds meeting the 1 % criterion for different populations (Wetlands International 2014). In this review, we identify sites of international importance using the Ramsar 1 % population criterion and highlight several species for which population estimates apparently require revision. This will be helpful for conservation and management measures of waterbirds and their wetland habitats.

Methods

The China Coastal Waterbird Census Group was established in 2005, training birdwatchers in bird identification and counting methods. Surveys have been conducted monthly since September 2005.

Because most of the surveyors are volunteers, surveys are conducted at weekends. To facilitate bird counts, surveys are generally conducted at high tide during periods of spring tides (China Coastal Waterbird Census Group 2009, 2011).

During surveys, surveyors walk along fixed routes and record waterbirds using binoculars and telescopes. Surveys of most sites can be finished in one day, whereas some larger sites need at least two days, e.g., along the Yalu Jiang, which covers some 60 km of coastline with multiple roost sites (Choi et al. 2015). Surveys at this site usually need at least two days to count different sections; at this site it is known that two sections for counting birds contain, essentially, discrete populations with little movement of birds between the two sections on consecutive days. Therefore, different sections at Yalu Jiang were counted on consecutive days, combining the number of birds of the two sections. This method was also used in the wider Rudong area. To ensure consistency of the survey methods, every site had a survey coordinator as the main investigator and team leader and surveys were arranged to minimize the risk of double-counting within the site on the same and consecutive days.

From September 2005 to December 2013, waterbirds were counted at 32 sites: 14 sites were surveyed each month and a further 18 sites at irregular intervals. At least one site was surveyed in each coastal province (Fig. 1). Some nature reserves were not covered in our surveys; however, there have been previous waterbird surveys in these coastal nature reserves (Barter et al. 2002).

Fig. 1
figure1

Survey sites along China’s coasts. The dark grey shows the regular survey sites and light grey the occasional survey sites. NR: Nature Reserve

The number of birds of each species recorded during every census were compared with the 1 % population estimates published in Waterbird Population Estimates (Wetlands International 2014).

Results and discussion

Species

A total of 75 species, including 33 shorebirds, 19 ducks and geese, 5 terns, 5 cranes, 4 gulls, 2 storks, 2 egrets, 2 spoonbills, 1 cormorant and 1 pelican, were recorded in numbers that met the 1 % criterion at least once at a single site during each census from September 2005 to December 2013 (Table 1). Among these species, the numbers of Mute Swan (Cygnus olor), Siberian Crane (Grus leucogeranus), Far Eastern Oystercatcher (Haematopus osculans), Bar-tailed Godwit (Limosa lapponica), Spotted Greenshank (Tringa guttifer), Great Knot (Calidris tenuirostris), Spoon-billed Sandpiper (Calidris pygmeus), Saunders’s Gull (Larus saundersi), Relict Gull (Larus relictus), Great Cormorant (Phalacrocorax carbo), Eurasian Spoonbill (Platalea leucorodia), Black-faced Spoonbill (Platalea minor), and Dalmatian Pelican (Pelecanus crispus) exceeded 20 % of the total flyway population estimate at a single site (Table 1). The numbers of Spotted Greenshank and Dalmatian Pelican exceeded the estimated numbers of the entire flyway population, suggesting an underestimate of the total population.

Table 1 Waterbird species at sites that meet the Ramsar 1 % criterion (Wetlands International 2014)

Some waterbird species exceeded the 1 % criterion at more than one site (Table 1). For example, the Saunders’s Gull was recorded as exceeding the 1 % criterion at 12 sites, the Spotted Redshank (Tringa erythropus) and Kentish Plover (Charadrius alexandrinus) both at 11 sites and the Eurasian Curlew (Numenius arquata) at 10 sites.

Among the 75 waterbird species that met the 1 % criterion, shorebirds were the most abundant group. This reflects the fact that millions of shorebirds in the East Asian-Australasian Flyway depend on China’s coastal wetlands for their stopover and wintering sites (Barter 2002; Bamford et al. 2008; Conklin et al. 2014). The surveys provided important data for understanding the number of shorebird populations at China’s coasts, especially for those species for which data in earlier times were absent or insufficient , such as for the Spoon-billed Sandpiper and the Spotted Greenshank.

The Spoon-billed Sandpiper is a critically endangered species (IUCN 2014), endemic to the East Asian-Australasian Flyway and dependent on coastal wetlands for much of its life cycle, with an estimated population of 140–480 individuals (Wetlands International 2014). The Rudong and Dongtai mudflats in Jiangsu are the most important areas along the flyway, an important and key stopover site for refuelling and moulting on both their northward and southward migration (Tong et al. 2012). On 12 October 2011, 103 Spoon-billed Sandpipers were recorded at Rudong alone. In October 2012 and 2013, over 100 individual sandpipers were recorded in the Rudong area (including Dongling and Dongtai coasts), Jiangsu (Tong et al. 2013, 2014). The maximum number (143 individuals) was recorded in October 2013. Both adults and juvenile birds have been recorded in the autumn, including some adults moulting their primaries (Tong 2012). This is the only known moulting ground and it appears that most of their adult population moults here. Moreover, our surveys revealed that the Min Jiang estuary in Fujian, is a regular wintering site for the Spoon-billed Sandpiper.

The estimated total flyway population of the Spotted Greenshank was 400–600 individuals (Wetlands International 2014). However, a total of 1117 individuals was recorded at the Dongtai and Rudong (including Dongling) coasts, Jiangsu Province, between 15 and 19 October 2013 (Tong et al. 2014), of which 940 were found at the Tiaozini reclamation district, Dongtai. Moreover, a total of 112 Dalmatian Pelicans was recorded at Tiaozini reclamation district, the Dongtai coast, Jiangsu in November 2013 which exceeds the former estimated total number of 100 individuals, in East Asia (Wetlands International 2014). These results provide the basis for updating the total population of these waterbirds in the flyway.

Sites

Of the 32 sites surveyed, 26 supported at least one species that met the 1 % criterion for recognition as a site of international importance (Table 2, Fig. 2). Previously, Barter (2002) listed 10 sites along the Yellow Sea coast as being internationally important for shorebirds (two of which, Yancheng and Dong Sha, were not included in our surveys). Our surveys identified additional sites for shorebirds, as well as new sites for other waterbird taxa.

Table 2 The 26 sites where waterbird species meeting the Ramsar 1 % population criterion have been recorded at least once during the 2005–2013 surveys
Fig. 2
figure2

The 26 sites supporting at least one species for which the number of birds met the 1 % criteria. NR: Nature Reserve

Among the 26 sites identified as being of international importance 13 are currently under some form of protection (Table 3), of which 8 are National Nature Reserves, 4 are Provincial Nature Reserves, and 1 Wetland Park. The other 13 sites currently have no legal protection. Four of the sites (Shuangtaizihekou National Nature Reserve, the Yellow River Delta National Nature Reserve, the Chongming Dongtan National Nature Reserve, as well as Mai Po and the Inner Deep Bay in the Hong Kong SAR) are currently designated by the Chinese government as Ramsar sites.

Table 3 Sites of international importance for waterbirds and their current protection status

Among the sites of international importance that currently are without any form of legal protection, a number are of particular importance for conservation. For example, the mudflats in the Rudong area in Jiangsu, stretch for 120 km between Tiaozini, Dongtai in the north and Dongling in the south. This area was divided into three count sections: the Tiaozini reclamation district of Dongtai (DT), Rudong (RD) and Dongling (DL). At these three sites, a total of 19 waterbird species, including 16 shorebird species, met the 1 % criterion since 2010, including the critically endangered Spoon-billed Sandpiper and the endangered Spotted Greenshank (Table 2). As well, 112 Dalmatian Pelicans were recorded at the Tiaozini reclamation district, Dongtai.

A total of 26 waterbird species, including 20 species of shorebirds, met the 1 % criterion at the Lianyungang coast, Jiangsu, in 2010–2013 (Table 2). The Far Eastern Oystercatcher had a stable winter population at Lianyungang, with a peak number of 2806 in 2013, which is about 25 % of the total flyway population estimate and the largest known wintering congregation in China (Melville et al. 2014). In addition, 8 % of the total flyway population of the Asian Dowitcher was recorded during the southward migration in 2012 and 12 % in the northward migration in 2013. Nine per cent of the total flyway population of the Grey Plover (Pluvialis squatarola) was also recorded in 2013.

Xitou, Guangdong has ‘only’ two species that met the 1 % criterion, but this includes the ‘critically endangered’ Spoon-billed Sandpiper. At Quanzhou Bay, Fujian, the population of the Grey-tailed Tattler (Heteroscelus brevipes) met the 1 % criterion in May 2011; this is the first internationally important site for the Grey-tailed Tattler in China.

Many sites identified as being of international importance to waterbirds along the Chinese coast currently lack any formal protection and many are immediately threatened by reclamation projects (Ma et al. 2014). In particular, the Jiangsu coast is undergoing rapid development as the provincial government hopes to complete reclamation of 1800 km2 of intertidal flats by 2020 — including much of the areas currently used by Spoon-billed sandpipers and Spotted Greenshanks, as well as many other species. Tianjin is soon to lose most of its remaining intertidal areas and the northern Bohai coast is being reclaimed for infrastructure development and aquaculture (Yang et al. 2011; Murray et al. 2014).

In view of the extent of approved and planned coastal reclamation projects and the speed with which many are being implemented, there is an urgent need to prioritise the designation of new protected areas to safeguard sites of international importance for waterbirds. Additionally, even sites that are currently reserves often suffer from a variety of management problems, including the invasion of exotic species, such as cordgrass (Spartina) which covers tidal flats (Gan et al. 2009), as well as boundary changes to accommodate new development projects. There is an urgent need to strengthen the management of existing reserves, as well as designating new ones.

Conclusions

Globally, citizen science is making an increasing contribution to scientific research, especially in bird studies (Greenwood 2007; Ma et al. 2013). The China Coastal Waterbird Census is a typical case of citizen science in China: all the surveys over the past eight years were conducted by volunteer birdwatchers in their spare time. Information from the surveys is vital for understanding waterbird populations and their dynamics along China’s coasts and critical for conservation strategies.

Over the past three decades, China’s coastal wetlands have been subject to intensive development and the rate of wetland loss is still accelerating (Ma et al. 2014; Murray et al. 2014). The loss and degradation of coastal wetlands have become the most serious threats to waterbirds (Hua et al. 2015), which might be the major causes for the decrease in the number of waterbirds at some survey sites, e.g., the Tianjin coast (Yang et al. 2011).

Coordinated and regular waterbird surveys over the long-term, covering China’s coasts, will continue to provide baseline data for understanding the effects of habitat changes on waterbirds.

Our data will contribute to the demarcation of ‘ecological red lines’ (Li 2014) in order to maintain biodiversity in China. It must be recognised, however, that our surveys are not comprehensive and many coastal areas remain unsurveyed, which potentially could support important waterbird populationsFootnote 1.

Notes

  1. 1.

    As this paper was being finalized we discovered two further sites that support internationally important number of waterbirds, i.e., Yingkou, Liaoning (Great Knot, Far Eastern Curlew, Saunders’s Gull, Relict Gull) and Qingduizi, Dalian, Liaoning (Great Knot, Far Eastern Curlew, Far Eastern Oystercatcher, Saunders’s Gull).

References

  1. Bamford MJ, Watkins DG, Bancroft W, Tischler G, Wahl J (2008) Migratory Shorebirds of the East Asian-Australasian Flyway: Population Estimates and Internationally Important Sites. Wetlands International Oceania, Canberra, Australia

  2. Barter M (2002) Shorebirds of the Yellow Sea: Importance, Threats and Conservation Status. Wetlands International. Global Series 9, International Wader Studies 12, Canberra, Australia

  3. Barter MA, Du JJ, Wang H, Chen Y, Gao Z, Cheng H et al (2002) Shorebird numbers in the Yancheng National Nature Reserve during the 2001 northward migration. Stilt 41:27–34

  4. Barter M, Yu X, Cao L (2007) Wintering Waterbird Survey of the Coastline of Fujian Province. China Forestry Publishing House, Beijing, China

  5. China Coastal Waterbird Census Group (2009) China Coastal Waterbird Census Report (Sep. 2005–Dec. 2007). Hong Kong Bird Watching Society, Hong Kong

  6. China Coastal Waterbird Census Group (2011) China Coastal Waterbird Census Report (Jan. 2008–Dec. 2009). Hong Kong Bird Watching Society, Hong Kong

  7. Choi CY, Battley PF, Potter MA, Rogers KG, Ma ZJ (2015) The importance of Yalu Jiang wetland in the north Yellow Sea to Bar-tailed Godwits Limosa lapponica and Great Knots Calidris tenuirostris during northward migration. Bird Conserv Int 25:53–70

  8. Conklin J, Verkuil Y, Smith B (2014) Prioritizing Migratory Shorebirds for Conservation Action in the East Asian-Australasian Flyway. WWF Hong Kong, Hong Kong

  9. Cui P, Wu Y, Ding H, Wu J, Cao MC, Chen L et al (2014) Status of waterbirds at selected locations in China. Waterbirds 37:402–409

  10. Fan ZY, Chen CS, Chen SH, Chan S, Lu YW (2011) Breeding seabirds along the Zhejiang coast: diversity, distribution and conservation. Chinese Birds 2:39–45

  11. Gan X, Cai Y, Choi C, Ma Z, Chen J, Li B (2009) Potential impacts of invasive Smooth Cordgrass Spartina alterniflora spread on bird communities at Chongming Dongtan, a Chinese wetland of international importance. Est Coast Shelf S 83:211–218

  12. Greenwood JJD (2007) Citizens, science and bird conservation. J Ornithol 148:S77–S124

  13. Hua N, Tan K, Chen Y, Ma ZJ (2015) Key research issues concerning the conservation of migratory shorebirds in the Yellow Sea region. Bird Conserv Int 25:38–52

  14. IUCN (2014) The IUCN Red List of Threatened Species. Version 2014.3, www.iucnredlist.org

  15. Li G (2014) Drawing a red line for ecological protection. Qiushi J 6(3). [http://english.qstheory.cn/2014-08/14/c_1111963598.htm]

  16. Ma Z, Cheng Y, Wang J, Fu X (2013) The rapid development of birdwatching in mainland China: a new force for bird study and conservation. Bird Conserv Int 23:259–269

  17. Ma Z, Melville DS, Liu J, Chen Y, Ren W, Zhang Z et al (2014) Rethinking China’s new great wall. Science 346:912–914

  18. MacKinnon J, Verkuil YI, Murray N (2012) IUCN Situation Analysis on East and Southeast Asian Intertidal Habitats, with Particular Reference to the Yellow Sea (including the Bohai Sea). IUCN, Gland, Switzerland and Cambridge, UK

  19. Melville DS, Gerassimov YN, Moores N, Yu Y, Bai Q (2014) Conservation assessment of Far Eastern Oystercatcher Haematopus [ostralegus] osculans. Int Wader Stud 20:129–154

  20. Murray NJ, Clemens RS, Phinn SR, Possingham HP, Fuller RA (2014) Tracking the rapid loss of tidal wetlands in the Yellow Sea. Front Ecol Environ 12:267–272

  21. Ramsar Convention Secretariat (2010) Designating Ramsar Sites: Strategic Framework and Fuidelines for the Future Development of the List of Wetlands of International Importance. In: Ramsar Handbooks for the Wise Use of Wetlands. 4th ed. Vol. 7. Ramsar Convention Secretariat, Gland, Switzerland

  22. Su L, Zou H (2012) Status, threats and conservation needs for the continental population of the Red-crowned Crane. Chinese Birds 3:147–164

  23. Tong M, Zhang L, Li J, Zockler C, Clark NA (2012) The critical importance of the Rudong mudflats, Jiangsu Province, China in the annual cycle of the Spoon-billed Sandpiper Calidris pygmeus. Wader Study Group Bull 119:208–211

  24. Tong M (2012) 2012 Spring spoon-billed sandpiper survey of Rudong, Dongtai and Wenzhou (Jiangsu and Zhejiang Provinces, Eastern China). Spoon-billed Sandpiper Task Force News Bull 8:15–19

  25. Tong M, Zhang L, Jing L, Zöckler C, Clark NA (2013) Record count of the critically endangered Spoon-billed Sandpipers on Rudong mudflats, Jiangsu, China. Spoon-billed Sandpiper Task Force News Bull 9:3–5

  26. Tong M, Clark N, Zhang L, Jing L, Zöckler C (2014) The autumn Rudong SBS Survey 2013. Spoon-billed Sandpiper Task Force News Bull 11:9–10

  27. Wetlands International (2014) Waterbird Population Estimates, 5th Edition. Summary Report. Wetlands International, Wageningen, The Netherlands, http://www.wpe.wetlands.org/

  28. Yang H, Chen B, Barter M, Piersma T, Zhou C, Li F et al (2011) Impacts of tidal land reclamation in Bohai Bay, China: ongoing losses of critical Yellow Sea waterbird staging and wintering sites. Bird Conserv Int 21:241–259

Download references

Acknowledgements

This paper was written with the help of Prof. Zhijun Ma and Kun Tan at Fudan University, and David Melville. We thank Paul Holt and Xiaodong Li for providing waterbird data from Zhuanghe in Liaoning Province and Wenzhou in Zhejiang Province. We greatly appreciate all the volunteers who have participated in the census.

Author information

Correspondence to Qingquan Bai.

Additional information

Competing interests

The authors declare they have no competing interests.

Authors’ contributions

All authors guided and participated in waterbird surveys at different sites along China’s coast. All authors contributed to this work. The initial draft was prepared by QQB and all authors read and approved the final manuscript.

Rights and permissions

This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Keywords

  • 1 % criterion
  • Citizen science
  • Coastal wetlands
  • Ramsar site
  • Waterbirds