Introduction
Coastal areas provide important habitats for many waterbird species, especially shorebirds, wildfowl, gulls and terns (van de Kam et al. Reference van de Kam, Ens, Piersma and Zwarts2004, Reference van de Kam, Battley, McCaffery, Rogers, Hong, Moores, Ki, Lewis and Piersma2008, Wetlands International 2006, Bamford et al. Reference Bamford, Watkins, Bancroft, Tischler and Wahl2008). Despite their importance as providers of marine food resources and livelihoods for fishing communities, intertidal areas for centuries have been converted into land for agricultural and residential use, port construction and industrial estates (Dalby Reference Dalby1957, Glue Reference Glue1971, Davidson et al. Reference Davidson, Lafoley, Doody, Way, Gordon, Key, Drake, Pienkowski, Mitchell and Duff1991, Suchaneck Reference Suchaneck1994, BirdLife International 2004). Whereas reclamation activities have now ceased in north-west Europe (Piersma Reference Piersma, Reinhard and Folmer2009), the conversion of intertidal flats into fish- or salt ponds, agricultural, recreational, or industrial land has accelerated in eastern Asia, especially in the Yellow Sea region, in order to accommodate the pressure of increasing human populations and economic growth (Barter Reference Barter2002, Moores Reference Moores2006, van de Kam et al. Reference van de Kam, Battley, McCaffery, Rogers, Hong, Moores, Ki, Lewis and Piersma2008, SOAPRC 2009, Wan et al. Reference Wan, Li and Lei2009). The populations of migrating waterbirds that depend on coastal wetlands have declined in parallel with the losses of intertidal areas, in extreme cases leading to threatened or nearly extinct populations (Syroechkovskiy Reference Syroechkovskiy and Straw2004, Crosby and Chan Reference Crosby, Chan, Boere, Galbraith and Stroud2006, Wetlands International 2006, Moores et al. Reference Moores, Rogers, Kim, Hassell, Gosbell, Kim and Park2008, van de Kam et al. Reference van de Kam, Battley, McCaffery, Rogers, Hong, Moores, Ki, Lewis and Piersma2008, Amano et al. Reference Amano, Székely, Koyama, Amano and Sutherland2010, Zöckler et al. Reference Zöckler, Syroechkovskiy and Atkinson2010). In view of the rapid decrease of intertidal habitats, the safeguarding of the remaining intertidal flats from further losses and degradations must become a global priority.
Here we present the case of Bohai Bay in the north-west Yellow Sea, China, strategically located in the middle of the East Asian-Australasian Flyway (hereafter EAAF). The coast of Bohai Bay is crucial to waterbirds, especially shorebirds and gulls that make stopovers there during northward and southward migration, or winter there, including Relict Gull Larus relictus, listed as ‘Vulnerable’ by IUCN (2010) and BirdLife International (2010a), Saunders’s Gull L. saundersi, Eurasian Curlew Numenius arquata, Red Knot Calidris canutus, Curlew Sandpiper C. ferruginea and Marsh Sandpiper Tringa stagnatilis (Li et al. Reference Li, Qian, Liu, Zhang and Wang1996, Barter Reference Barter2002, Battley et al. Reference Battley, Rogers, van Gils, Piersma, Hassell, Boyle and Yang2005, Minton et al. Reference Minton, Wahl, Jessop, Hassell, Collins and Gibbs2006, Yang and Zhang Reference Yang and Zhang2006, Liu et al. Reference Liu, Holt and Zhang2007, Yang et al. Reference Yang, Chen and Zhang2008). The majority of Red Knot during northward migration, and the largest wintering populations of Eurasian Curlew and Relict Gull, were counted in Bohai Bay along the EAAF (Barter et al. Reference Barter, Li and Xu2001, Reference Barter, Riegen and Xu2003, Liu et al. Reference Liu, Holt, Lei, Zhang and Zhang2006, Cao et al. Reference Cao, Tang, Wang and Barter2009). Concerns about the accelerating tidal flat reclamation along the Bohai Bay coast, and the potential effects on waterbirds dependent on the bay, have been voiced earlier (Barter et al. Reference Barter, Riegen and Xu2003, Liu et al. Reference Liu, Holt, Lei, Zhang and Zhang2006, Yang et al. Reference Yang, Chen and Zhang2008). No evidence on the impacts of the land reclamation in recent decade has so far been provided.
Bohai Bay sits next to a densely human-populated and rapidly developing region. Two industrial developments have been under construction on the western and northern coasts of Bohai Bay since 1994 (Table 1): Tianjin Binhai New Area, located in the municipality of Tianjin, western Bohai Bay, and Caofeidian New Area, in the city of Tangshan, Hebei Province, northern Bohai Bay, started in 1994 and 2002, respectively (Fig. 1). In the past decade, the developments have turned large areas of sea into industrial land and the rate of land reclamation has accelerated (this study). In future, the planned development will lead to a continuing reduction of both land and shallow sea habitats (Table 1).
Figure 1. Location of study sites and reclaimed areas of the Tianjin Binhai and Caofeidian New Area industrial reclamation projects in Bohai Bay by 2010.
Table 1. Details of the industrial reclamation projects in Bohai Bay.Footnote a
Loss of waterbird habitats can lead to a decline in waterbird numbers (e.g. Moores et al. Reference Moores, Rogers, Kim, Hassell, Gosbell, Kim and Park2008, Kraan et al. Reference Kraan, van Gils, Spaans, Dekinga, Bijleveld, van Roomen, Kleefstra and Piersma2009, Catry et al. in press), or to the movement of birds to nearby suitable habitats (Burton et al. Reference Burton, Rehfisch, Clark and Dodd2006); the latter can lead to increased densities on other sites and consequent increase in mortality of the displaced birds, thus leading to an overall loss of birds (Goss-Custard Reference Goss-Custard1980). The reclamation of the two major industrial developments has changed, and will further change, waterbird habitats along the Bohai Bay coast. The aim of this study was to determine if waterbirds have declined already, or have become concentrated in the remaining suitable areas. We conducted surveys of migratory and wintering waterbirds along the coasts of Tianjin and Tangshan during 2006–2010, and were fortunate to have concentrated most survey efforts in an area relatively little impacted so far. We interpret these counts in the light of the historical extent of land reclamation, reconstructed on the basis of satellite photographs.
Methods
Study area and study sites
The study area focused on the coasts of Tianjin (38º45’–39º12’N, 117º34–57’E) and Tangshan (39º01–10’N, 118º07–21’E). The area has a typical temperate climate with cold, dry winters and hot, humid summers. The average temperature in January is -4°C and in July 26°C (HPDLR 2007). The intertidal area remains frozen from December for three months. The main habitats are tidal mudflats, saltpans and shrimp ponds; a sea wall separates the saltpans and shrimp ponds from the mudflats. Tides have an average range of 2.5 m (HPDLR 2007). The intertidal flats outside the dykes are 1–3 km wide at low tide (see Fig. 2) and completely submerged from about 2 hrs before time of high tide. There are salt works, wharfs, oil fields and industrial areas along the coast. Local people collect shellfish and catch fish on the mudflats from spring to autumn.
Figure 2. Changes in reclaimed offshore areas in the Tianjin Binhai and Caofeidian New Areas over years. The lined areas are intertidal flats, the area in the circle is the core study area in Tangshan (Beipu, Nanpu and Zuidong), the dark grey areas present the cumulative extent of previously reclaimed areas and the black areas show the new reclaimed areas between years, including new land, sea walls and mudflats or shallow water within closed sea walls. (The data set is provided by International Scientific Data Service Platform, Computer Network Information Center, Chinese Academy of Sciences. (http://datamirror.csdb.cn))
We worked at seven study sites in Tianjin: Duliujian estuary, Haibinyuchang, Lujuhe, Dagukou, Chengtougu, Haiyan and Dashentang, and four in Tangshan: Heiyanzi, Beipu, Nanpu and Zuidong (Fig. 1). The sites in Tangshan were situated between Tianjin Binhai New Area and Caofeidian New Area, but closer to the latter. However, during the study period, most study sites in Tianjin were lost gradually to land reclamation by the Tianjin Binhai New Area. The order in which the mudflats were enclosed by sea walls was: from east of Haiyan to Dashentang in October 2007, from Lujuhe to Dagukou in December 2007, from east of Haibinyuchang to Lujuhe and Chengtougu in September 2008. In Tangshan, the core study sites Beipu, Nanpu and Zuidong were only a little affected by land reclamation until late 2009, with partial land loss in Zuidong in 2010.
Remote sensing data collection and processing
To document the extent of loss of sea areas, especially of the intertidal zone, we acquired a set of Landsat MSS/TM/ETM+ images which covered a period of 36 years: 1974, 1984, 1993, 2000, 2002–2010. Land cover in the study area was classified into land, intertidal area and water, using visual interpretation and digitalization with technical support from ArcMap 9.3 (ESRI Inc. 2008). We estimated the total area of tidal flats at low tide in spring along the Tianjin and Tangshan coasts in each year, measured the tidal flats at each study site and the total offshore area, including tidal flats and shallow water, to be reclaimed according to project plans, and calculated the changes in land-use within industrial developments between years using ArcMap 9.3.
Survey methods
Surveys were conducted along the seawall at each study site. Survey lengths were: Duliujian estuary–1.5 km, Haibinyuchang to Lujuhe–3 km, Lujuhe to Dagukou–6.5 km, Chengtougu–2.5 km, Haiyan to Dashentang–6 km, Heiyanzi–2 km, Beipu–4 km, Nanpu–10 km, and Zuidong–6 km.
From September 2006 to December 2008, we carried out surveys during three periods each year: one survey in September, three (2007) or six (2008) surveys in May, and monthly surveys from December to February. In 2009, surveys were conducted monthly in Tangshan except in May, when eight surveys were carried out. In Tangshan in 2010, one survey was conducted in January, one in February and seven surveys during May. Waterbirds on the intertidal mudflats were counted using telescopes (25–60x) and/or binoculars (10x40) during the outgoing tide. We recorded air temperatures during survey periods, as temperature can affect the distribution of wintering waterbirds (Liu et al. Reference Liu, Holt, Lei, Zhang and Zhang2006). Combinations of sites (e.g. Haibinyuchang to Dagukou, Haibinyuchang to Lujuhe, Haiyan to Dashentang) were each usually surveyed within one day, with additional sites requiring extra counting days. Study site surveys were adjusted when necessary to account for habitat loss, but also occasionally due to bad weather or access problems caused by bad road conditions.
Internationally important species
Internationally important species are defined as those which were present in numbers ≤ 1% of their flyway populations at least once during the study period according to the Convention on Wetlands (Ramsar, Iran, 1971); shorebird flyway populations follow Bamford et al. (Reference Bamford, Watkins, Bancroft, Tischler and Wahl2008) except for Red Knot and Eurasian Curlew flyway population sizes where we used the update by Rogers et al. (Reference Rogers, Yang, Hassell, Boyle, Rogers, Chen, Zhang and Piersma2010) and Cao et al. (Reference Cao, Tang, Wang and Barter2009) respectively. For other waterbird species we followed Wetlands International (2006), IUCN (2010) and BirdLife International (2011).
Data collection and analysis
In order to compare annual numbers between regions and annual changes in abundance within the regions, we organised the data as follows:
(1) Surveys were carried out during May, the peak period of northward migration in the study area, from 2007 to 2010. Mean waterbird densities were calculated to show population trends of waterbirds during northward migration in different areas.
(2) Monthly surveys were conducted in every winter month from 2006/2007 to 2009/2010. Trends in wintering waterbird populations were determined by comparing the means of waterbird densities counted in December, January and February between years.
(3) To assess changes in shorebird populations in the study area before and after tidal land reclamation, we used the data from Zuidong. This was the only site within the core study area in Tangshan that had a series of comparable monthly surveys conducted since 2004, when land reclamation activities had not yet started.
(4) To verify whether this increase in waterbirds at the core study sites is indeed mainly due to habitat loss elsewhere in Bohai Bay, we used all information on known numbers of Red Knot and Curlew Sandpiper, the two most common migrant shorebirds, in combination with the known land reclamation. Assuming the staging populations in northern Bohai Bay to have remained stable, we predicted the yearly peak numbers based on the sum of the peak numbers counted in the core study area during the previous year plus the known number of birds that occurred in the reclaimed intertidal flats elsewhere in Tianjin and Tangshan along western and northern Bohai Bay in that year (Barter et al. Reference Barter, Li and Xu2001, Reference Barter, Riegen and Xu2003). The observed peak numbers of Red Knot and Curlew Sandpiper in 2004 and 2006 were calculated on the assumption that peak numbers counted only at Zuidong represented a third of the staging population in the entire core study area (of which Zuidong is approximately one third). We also assumed that 2004 followed on 2000–2002 and that 2006 followed on 2004.
Results
The recent history of loss of intertidal land
According to analysis of the remote sensing images from 1974 to 1993, a total of 313 km2 of intertidal area was reclaimed mainly for salt works in Tianjin and Tangshan along western and northern Bohai Bay. In the following 16 years (1994–2010), approximately 450 km2 of offshore area, including 218 km2 of intertidal mudflats (34% of the total intertidal area in 1993 in western and northern Bohai Bay) was reclaimed for the Tianjin Binhai and Caofeidian New Areas (Figs. 2 and 3). Notably, reclamation accelerated during the past five years (2005–2010) with a removal of 78% of the total reclaimed tidal area for the two developments (Figs. 2, 3 and 4). The Tianjin Binhai and Caofeidian New Areas had reclaimed a total of 110 km2 and 108 km2 intertidal lands, respectively, by 2010.
Figure 3. Changes in the available intertidal area in Tianjin and Tangshan along western and northern Bohai Bay from 1974 to 2015 (above) and changes in the reclaimed intertidal area due to the Tianjin Binhai and Caofeidian New Areas respectively from 1994 to 2015 (below). The dotted lines present the possible situation according to the plan of the Tianjin Binhai and Caofeidian New Areas.
Figure 4. Land reclamation activity on the mudflats in Caofeidian New Area in spring 2007.
Abundance of waterbirds in Tianjin and Tangshan
A total of 58 waterbird species were recorded in the study areas of Tianjin and Tangshan during the study (Fig. 1, Table 2). Sixteen of them occurred in internationally important concentrations in the study region: 14 species during northward migration and four species during southward migration and winter. During the survey periods, shorebirds and gulls comprised most of the waterbirds occurring in the intertidal area. Shorebirds clearly formed the great majority, accounting for 99% of all waterbirds in May, 75% in winter and 66% in September.
Table 2. Waterbird species and their maximum numbers recorded in Tianjin and Tangshan during the study. Species are listed in order of abundance. “IUCN” shows the conservation status of each species; “1%” indicates species whose maximum number was more than 1% of their estimated flyway population (Wetlands International 2006, Bamford et al. Reference Bamford, Watkins, Bancroft, Tischler and Wahl2008, Cao et al. Reference Cao, Tang, Wang and Barter2009, Rogers et al. Reference Rogers, Yang, Hassell, Boyle, Rogers, Chen, Zhang and Piersma2010, IUCN 2010 and BirdLife International 2011).
a W, M and B are winter, migration and breeding period respectively
b LC - Least Concern, NT - Near Threatened , VU – Vulnerable, EN - Endangered, as listed by IUCN (2010)
c the flyway population is the world population.
Spring counts (2007–2010)
At the beginning of the survey period in 2006/2007, the spring density of waterbirds on mudflats in Tangshan was higher than that in Tianjin (Table 3). With the ongoing losses of intertidal habitats in western and northern Bohai Bay, densities of waterbirds increased dramatically during the subsequent springs, while densities in the rapidly disappearing study area in Tianjin declined from 2007 to 2008 (Table 3). Red Knot, Curlew Sandpiper, Broad-billed Sandpiper Limicola falcinellus and Sanderling Calidris alba increased rapidly at the study sites in Tangshan over the years, as the loss of intertidal mudflats in Bohai Bay continued.
Table 3. Changes in the available intertidal area along western and northern Bohai Bay and waterbird densities in May in the study areas in Tianjin and Tangshan from 2007 to 2010.
a Average temperature in May in Tangshan (CMDSSS 2010)
Winter counts (2006/2007 to 2009/2010)
Since the start of winter counts in 2006/2007, the density of waterbirds underwent a rapid increase in both Tianjin and Tangshan, concurrent with the rapid loss of tidal flats in the surrounding area (Table 4, Fig. 2). Although waterbird densities in Tangshan were relatively stable from 2007/2008 to 2008/2009, they decreased during 2009/2010, a rather severe winter (Table 4). With the exception of this last cold winter, waterbird populations increased at the study sites, mainly due to the large influx of Eurasian Curlews and Relict Gulls, which were the most common wintering waterbirds (Fig. 5). The peak count of wintering Eurasian Curlews in the core study area in Tangshan increased from 6% of the flyway population in 2006 to 17% in 2009; for Relict Gull the proportion of the global population increased from 6% in 2006 to 61% in 2009.
Figure 5. Monthly numbers of Eurasian Curlew and Relict Gull, two main species, at study sites in Tianjin and Tangshan during winter months from 2006 to 2010 (the remaining study sites in Tianjin were not surveyed in the last winter). Average mudflats surveyed in Tianjin and Tangshan in each winter showed in Table 4. 1% of the flyway population of Eurasian Curlew is 1,000 birds (Cao et al. Reference Cao, Tang, Wang and Barter2009) and that of the world population of Relict Gull is 120 birds (Wetlands International 2006, BirdLife International 2010a). D, J and F are December, January and February, respectively.
Table 4. Changes in the available intertidal area along western and northern Bohai Bay, densities of waterbirds and of the two main groups (shorebirds and gulls) in winter (December, January and February) in the study areas in Tianjin and Tangshan from 2006 to 2010.
a Average temperature in winter months (December, January and February) in Tianjin and Tangshan (CMDSSS 2010)
Seasonal changes in shorebird numbers in Tangshan between 2004 and 2009
The only count sector that was comprehensively covered by monthly surveys in both 2004 and 2009 was Zuidong (Fig. 1). The seasonal pattern of change in shorebird abundance was similar in 2004 and 2009, with a large peak occurring during northward migration in both years (Fig. 6). However, compared to the 2004 survey, which was carried out before the tidal flat reclamation in Tangshan, the densities of shorebirds in this sector substantially increased during northward migration 2009 (Fig. 6), especially in the three species for which this area is of special importance in flyway terms: Sanderling (11% of their flyway population on 24 May 2009), Eurasian Curlew (8.7% on 3 February 2009) and Red Knot (8.5% on 10 May 2009); the 1% criterion of Eurasian Curlew and Red Knot follow Bamford et al. (Reference Bamford, Watkins, Bancroft, Tischler and Wahl2008) to compare with the percentage in 2004 (Yang et al. Reference Yang, Chen and Zhang2008).
Figure 6. Maximum monthly numbers of shorebirds at Zuidong in Tangshan (including 22 km2 of intertidal flats) in 2004 and 2009 (2004 data from Yang et al. Reference Yang, Chen and Zhang2008).
Changes in predicted and observed numbers of Red Knot and Curlew Sandpiper in Tangshan between 2002 and 2010
In the core study area in Tangshan, the peak counts of Red Knot and Curlew Sandpiper increased dramatically from 13% and 3% of their flyway populations in 2007 to 62% and 23% in 2010, respectively. As shown in Fig. 7, increasing numbers of Red Knot and Curlew Sandpiper, the two most common migrant shorebirds during northward migration, could partially be accounted for by displacement of birds from lost areas. That the predicted increases are smaller than the actual increases should not surprise us, as many areas were not counted previously at the peak period (Barter et al. Reference Barter, Li and Xu2001, Reference Barter, Riegen and Xu2003). The general pattern of increase is consistent with the idea that over the course of the years, as more mudflat areas in Bohai Bay were reclaimed, the staging populations became ever more concentrated in what remained, as shown directly for Red Knot (Fig. 8). In 2010, with 970 birds km–2, the density of Red Knot was four times higher than in the years up to 2007 (211 birds km–2) in the core study area.
Figure 7. Predicted and counted peak numbers of Red Knot (A) and Curlew Sandpiper (B) in the core study area (Beipu, Nanpu and Zuidong) (including 67 km2 of tidal flats) in Tangshan during northward migration from 2000 to 2010. The white and black bars give the predicted and counted peak numbers at the core study sites in 2000-2002, 2004 and 2006-2010 respectively.
Figure 8. Changes in peak numbers of Red Knot in the core study area in Tangshan (Beipu, Nanpu and Zuidong) in parallel with changes in the available intertidal area in Tianjin and Tangshan along western and northern Bohai Bay during northward migration from 2000 to 2010.
Discussion
The Yellow Sea is a critical stopover site for waterbirds in the EAAF (Barter Reference Barter2002, Minton et al. Reference Minton, Wahl, Jessop, Hassell, Collins and Gibbs2006). The large numbers and diversity of waterbirds in the present study area during migration periods (especially during northward migration) and in winter confirm the critical importance of the Bohai Bay coast for migrating waterbirds. Bohai Bay supports high proportions of the flyway populations of Relict Gull, Red Knot, Broad-billed Sandpiper, Curlew Sandpiper and Eurasian Curlew (Table 2). With the current rapid economic growth in China leading to increasing human populations and industrial projects in coastal areas, habitat loss resulting from wetland reclamation remains a major threat for biodiversity conservation.
During 1994-2010 one third of the intertidal mudflats in the western and northern Bohai Bay system were lost to industrial development, with the speed of land reclamation actually accelerating since 2006. What would happen if the intertidal habitats continued to decrease? Would the number of waterbirds in Bohai Bay be reduced or would they move to nearby remaining wetland? From 2007 to 2010 the populations of waterbirds, especially shorebirds, noticeably increased in the core study sites in Tangshan (Beipu, Nanpu and Zuidong) that were not much affected by reclamation schemes (Tables 3, 4). The increase in shorebird numbers at Zuidong has been going on since at least 2004 when the main reclamations began (Fig. 6; Yang et al. Reference Yang, Chen and Zhang2008). Meanwhile, Red Knot and Curlew Sandpiper, the two main species during northward migration, continued to concentrate in the core area in Tangshan as land reclamation continued in Bohai Bay (Figs. 7 and 8). This suggests that birds moved from the lost mudflats to what was left nearby; it may also mean that they have nowhere else to go.
Two subspecies of Red Knot, C. c. piersmai and C. c. rogersi, stage at the intertidal mudflats of Bohai Bay. According to the peak counts, by 2010 at least 67% of the world population of C. c. piersmai and 57% of C. c. rogersi, based on the figures in Rogers et al. (Reference Rogers, Yang, Hassell, Boyle, Rogers, Chen, Zhang and Piersma2010) refuelled at the core study sites for several weeks in April and May. The increase in Red Knot numbers counted is actually accompanied by decreases in the total flyway population of the two subspecies, from c.222,000 birds in 2000 (Bamford et al. Reference Bamford, Watkins, Bancroft, Tischler and Wahl2008) to 130,000 birds in 2007 (Piersma Reference Piersma2007) to 105,000 birds in 2009 (Rogers et al. Reference Rogers, Yang, Hassell, Boyle, Rogers, Chen, Zhang and Piersma2010). Similarly, Curlew Sandpiper on their wintering grounds in Australia have also shown decreasing numbers over 30 years (Gosbell and Clemens Reference Gosbell and Clemens2006, Rogers and Gosbell Reference Rogers and Gosbell2006a, C. Minton unpubl. data). Therefore, our study confirms the prediction that birds are forced into ever smaller areas of tidal flat in Bohai Bay during northward migration.
A large proportion of the world’s declining population of Relict Gull numbering 12,000 birds (BirdLife International 2010a, IUCN 2010) winters in Bohai Bay. The Tianjin coast was previously the most important known wintering ground, especially for adults (Liu et al. Reference Liu, Holt, Lei, Zhang and Zhang2006). Interestingly, the largest number of Relict Gulls occurred in Tianjin (8,230 birds, of which 7,880 birds were found in the Jingqu sub-area, south of the Duliujian estuary and not part of our study area; Fig. 1) on 17 December 2005 at the beginning of the severe 2005/2006 winter (Fig. 9) when exposed mudflats were still available (Y. Liu unpubl. data). However, the importance of Tianjin has decreased since late 2007, as much of the traditional wintering habitat has been converted into land for industrial development. In the 2008/2009 winter they had apparently moved to Tangshan where they were found in good numbers (7,318 birds, 61% of their global population, in January 2009), coinciding with habitat loss in Jingqu (Fig. 2), which held the largest number of Relict Gulls counted in Tianjin. The number of Relict Gulls present in our remaining study sites in Tianjin and Tangshan in the 2008-2009 winter (8,477 birds) matched the previous maximum winter count in Tianjin (8,230 birds in 2005, Y. Liu unpubl. data). That Relict Gull numbers were so much lower during the following winter (Fig. 5) must have been due to this winter being the most severe in Bohai Bay for 30 years (Fig. 9). Weather conditions have previously affected the winter distribution of Relict Gull (Liu et al. Reference Liu, Holt, Lei, Zhang and Zhang2006, BirdLife International 2010a). We suggest that the Tangshan intertidal area has become the most important wintering ground for Relict Gull in normal winters.
Figure 10. Reclamation activities at Zuidong, one of the core study sites in Tangshan, since 2009 for industry. A shows land reclamation on the mudflats. B and C are the pumping of sand from the mudflats (B) to fill-in near-shore saltpans (C).
Eurasian Curlew is now listed as ‘Near Threatened’ (BirdLife International 2010b, IUCN 2010) and according to an updated estimate, their EAAF population is now 100,000 birds (Cao et al. Reference Cao, Tang, Wang and Barter2009). The difference between the new estimate and the old one of 40,000 birds (Bamford et al. Reference Bamford, Watkins, Bancroft, Tischler and Wahl2008) can be explained by the inclusion of previously unknown numbers of birds wintering in China but not an increase in the flyway population. Eurasian Curlew winter on the coasts of the EAAF and the most northerly and abundant area is Bohai Bay (Cao et al. Reference Cao, Tang, Wang and Barter2009). In normal winters from 2006/2007 to 2008/2009, Eurasian Curlew numbers increased rapidly in the Tangshan study area (Fig. 5), possibly because previously important wintering areas nearby were reclaimed by Caofeidian New Area (H.Y. Yang unpubl. data; Fig. 2). That 4,000–5,000 Eurasian Curlews stayed for the whole of the coldest winter in 30 years shows that this small area of intertidal mudflats in Tangshan is very attractive (Figs. 5 and 9).
Ongoing land developments and predicted effects on waterbirds
A new big industrial development, Cangzhou Bohai New Area, has been under development in south-western Bohai Bay since 2007, with 3,321 km2 of planned developments including a 117 km2 offshore area (SOAPRC 2009). According to the land reclamation plans (Table 1) and the presence of sea walls still to be closed (pers. obs.), more marine habitats, including large areas of intertidal mudflat, will soon be lost at all three development project sites. In addition, the local government has started other small reclamation projects in the core study area, which affect intertidal areas by direct land conversion as well as the pumping of sand to fill-in near-shore saltpans (Fig. 10).
We suggest that waterbird densities at the remaining coastal sites in Bohai Bay, especially in Tangshan, will continue to increase as intertidal flats are lost. As a result, the survival of birds forced to congregate together or to relocate is likely to decrease, leading to a decline in their flyway populations (Evans et al. Reference Evans, Knights and Pienkowski1979, Goss-Custard Reference Goss-Custard1980, Baker et al. Reference Baker, González, Piersma, Niles, de Lima Serrano do Nascimento, Atkinson, Collins, Clark, Minton, Peck and Aarts2004, Burton et al. Reference Burton, Rehfisch, Clark and Dodd2006, Goss-Custard et al. Reference Goss-Custard, Burton, Clark, Ferns, McGrorty, Reading, Rehfisch, Stillman, Townshend, West and Worrall2006).
If the entire intertidal area in Bohai Bay disappears, what will happen to the waterbirds that depend on it now? Along the Yellow Sea coastline, mudflats are being lost at great speed (Barter Reference Barter2002, Moores Reference Moores2006, Moores et al. Reference Moores, Rogers, Kim, Hassell, Gosbell, Kim and Park2008, SOAPRC 2009, Wan et al. Reference Wan, Li and Lei2009), and it is believed that declines in migratory shorebird populations in Australia and New Zealand over the last 30 years (Gosbell and Clemens Reference Gosbell and Clemens2006, Southey Reference Southey2009, C. Minton unpubl. data, AWSG and Arthur Rylah Institute unpubl. data) are due to the loss of feeding habitat at stopovers along the Yellow Sea coast (Barter 2005, Gosbell and Clemens Reference Gosbell and Clemens2006, C. Minton and D. Rogers pers. comm.). That the Yellow Sea may well be filled to capacity is demonstrated by the declines between 2006 and 2008 in 19 of the most abundant shorebird species at Saemangeum (137,000 shorebirds in total; Moores et al. Reference Moores, Rogers, Kim, Hassell, Gosbell, Kim and Park2008), a recently reclaimed intertidal area in South Korea that was previously the premier shorebird site in the Yellow Sea (Moores Reference Moores2006, Rogers et al. Reference Rogers, Moores and Battley2006b). Among them was the Great Knot Calidris tenuirostris, endemic to this flyway, of which 23% of the population depended on Saemangeum during northward migration (Rogers et al. Reference Rogers, Moores and Battley2006b, Moores et al. Reference Moores, Rogers, Kim, Hassell, Gosbell, Kim and Park2008). Since the Saemangeum mudflats were closed off, the world population has declined by 20% (Moores et al. Reference Moores, Rogers, Kim, Hassell, Gosbell, Kim and Park2008) resulting in Great Knot now being assessed as ‘Vulnerable’ by IUCN (2010) and BirdLife International (2010c). Apparently, this unique shorebird species had nowhere else to go.
In view of the agreements between China and Japan (Beijing–1981), and China and Australia (Canberra–1988) to safeguard migratory birds and their environments (Anon. Reference Anon1981, Reference Anon1988), China should protect the remaining intertidal areas within Bohai Bay to limit further declines in waterbird populations within the EAAF. Additionally, in order to monitor the effects of tidal flat reclamation on waterbirds, systematic surveys should be conducted, especially during the winter and northward migration periods. Also, more research should be carried out to develop a good understanding of the relationship between mudflats, benthos and waterbirds to understand the unique ecosystem in Bohai Bay that supports such large waterbird numbers. It is also important that decision makers and the public are made fully aware of the great importance of Bohai Bay for waterbirds, and of the potential environmental disaster for all those that rely on the tidal flats as a food source, including the many human beings that harvest the Bay’s finfish and shellfish (Kim et al. Reference Kim, Choi and Lee2006, Sato Reference Sato2006, Nie and Tao Reference Nie and Tao2008, Wan et al. Reference Wan, Li and Lei2009).
Acknowledgements
This project was supported by National Basic Research Program of China (Grant No. 2006CB403305), National Natural Science Foundation of China-Guangdong Joint Fund (Grant No. U0833005) and the National Fish and Wildlife Foundation-ConocoPhillips SPIRIT of Conservation Migratory Bird Program and the International Crane Foundation. We acknowledge the support for our field research from Ming-Lu Wu, Section Chief of the Forestry Department, Hebei Province, China. We thank Ru-Lin Gao for his enthusiastic guiding to most of the study sites in Tangshan and his generosity in sharing his local knowledge . We thank Rui-Ding Zhao, Biao Wang, Xue-Song Feng, Dong-Lai Li, Si-Hang Chen, Jian-Qiang Li, Ning Wang, Lei Guan, Yang Qiu, Wei-Pan Lei, Si-Hai Yan, Tian Fang, Lan Zhang and Xiao-Jing Li for field assistance and Dong-Lai Li for helping draw the map of study sites. The manuscript was improved with help from anonymous reviewers, Phil Battley, Clive Minton and Phil Atkinson.
