Yanlin Cui, Yanan Tang, Sen Yang, Wei Wu, Xuesong Feng, Qiang Ma, Dongliang Niu, Jun Ma, Zhijun Ma. 2023: Changes in wintering Hooded Cranes and their habitats at Chongming Dongtan over the past 20 years. Avian Research, 14(1): 100083. DOI: 10.1016/j.avrs.2023.100083
Citation: Yanlin Cui, Yanan Tang, Sen Yang, Wei Wu, Xuesong Feng, Qiang Ma, Dongliang Niu, Jun Ma, Zhijun Ma. 2023: Changes in wintering Hooded Cranes and their habitats at Chongming Dongtan over the past 20 years. Avian Research, 14(1): 100083. DOI: 10.1016/j.avrs.2023.100083

Changes in wintering Hooded Cranes and their habitats at Chongming Dongtan over the past 20 years

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  • Corresponding author:

    E-mail address: ma_jun@fudan.edu.cn (J. Ma)

    E-mail address: zhijunm@fudan.edu.cn (Z. Ma)

  • Received Date: 18 Nov 2022
  • Rev Recd Date: 04 Feb 2023
  • Accepted Date: 05 Feb 2023
  • Available Online: 14 Apr 2023
  • Publish Date: 13 Feb 2023
  • The Hooded Crane (Grus monacha) is listed as a Vulnerable species in the IUCN red list. Tidal wetland (tideland), the major habitat for wintering Hooded Cranes at East China's Chongming Dongtan, has dramatically changed in the past two decades, but there is limited knowledge about the population and habitat changes of the Hooded Cranes. This study investigated the population size and distribution of wintering Hooded Cranes at Chongming Dongtan from 2000 to 2021. We used remote sensing images combined with a vegetation classification algorithm to analyse the distribution of saltmarsh vegetation. The quadrat method was used to investigate the density and weight of the underground corms of Sea Bulrush (Scirpus mariquter), the main food on tideland for the Hooded Cranes. From 2000 to 2021, the population number of wintering Hooded Cranes at Chongming Dongtan remained stable at approximately 100. In 2000, the area of Scirpus spp. and Common Reed (Phragmites australis) accounted for approximately half of the total saltmarsh area at Chongming Dongtan, respectively. The invasive Smooth Cordgrass (Spartina alterniflora) rapidly expanded on tideland in the 2000s while the Scirpus spp. was competed out and thus significantly reduced in area. After the implementation of an ecological project to control Smooth Cordgrass and to restore Scirpus spp. in the 2010s, the area of the Smooth Cordgrass decreased considerably while the area of Scirpus spp. increased. The corms of Sea Bulrush decreased on the southeastern tideland during the study period, which might be the cause of the northward movement of the foraging Hooded Cranes on tideland. We also found Hooded Cranes foraged crops in the nearby farmland in mid-winter, causing human-bird conflicts in the recent decade. Our results found that changes in habitat and food conditions on tideland impacted wintering Hooded Cranes. Foraging in farmland with human disturbance in the recent decade might be related to insufficient food on tideland. We suggest active intervention to accelerate the restoration of Sea Bulrush on tideland and reduce human disturbance in farmland to improve the habitat quality of the wintering Hooded Crane at Chongming Dongtan.

  • Habitat quality is the key factor affecting the survival and fitness of animals (Block and Brennan, 1993). Many migratory birds stay in wintering grounds for nearly half a year. The habitat quality of wintering grounds affects the body condition, migration timing, and reproductive success of migratory birds, all of which are closely related to the population maintenance of migratory birds in return (Johnson et al., 2006). Food resources are a crucial factor affecting wintering habitat quality (Ling et al., 2015). Migratory birds consume a large amount of energy during migration and thus need to ingest a large amount of food after arriving at the wintering ground to restore body conditions (Myers et al., 1987). Most migratory birds molt at the wintering ground, which also requires the support of a large number of nutrients (Kjellen, 1994). Moreover, before spring migration, migratory birds need to accumulate fuel in the wintering ground, preparing for the migratory flights to their breeding grounds (Lindström and Piersma, 1993). Therefore, understanding the quality of wintering habitat is essential for bird conservation and habitat management.

    The Hooded Crane (Grus monacha) is a Vulnerable species in the IUCN Red List (BirdLife International, 2016). As migratory birds, the main wintering grounds for Hooded Cranes are located in Kagoshima of Japan, Suncheon Bay of South Korea, inland lakes in the middle and lower reaches of the Yangtze River in China (Wang et al., 2021), such as Shengjin Lake, Caizi Lake and Poyang Lake, and Chongming Dongtan in the Yangtze estuary (BirdLife International, 2016). The number of wintering Hooded Cranes at Chongming Dongtan was approximately 100. Hooded Cranes mainly stay on tidal wetlands and are highly dependent on the underground corms of Sea Bulrush (Scirpus mariquter), a dominant saltmarsh plant, as their major food (Jing et al., 2002a; Ma et al., 2003). This suggests that they are sensitive to tidal wetland changes at Chongming Dongtan.

    Over the past 20 years, tidal wetlands have changed significantly at Chongming Dongtan. Reduction of sediment input from the runoff of the Yangtze River to the estuary has caused a slowdown of tideland expansion and even erosion of tidal flats in some regions; rapid spread of the exotic plant Smooth Cordgrass (Spartina alterniflora) in the 2000s and then eradication of Smooth Cordgrass in the 2010s have caused dramatic changes in tidal vegetation (Gan et al., 2009; Ma et al., 2017; Hu, 2020). Many waterbird populations have changed over the past decades, including some populations that decreased in the early 2000s (Ma et al., 2009) and then increased with the implementation of wetland restoration (Fan et al., 2021). However, the impacts of environmental changes on the population and habitat conditions of the Hooded Cranes remain unknown.

    The Hooded Crane is a flagship species for tidal wetland conservation at Chongming Dongtan. Understanding its population dynamics and habitat changes provides the basis for making conservation measures. In this study, we investigated the population number and distribution of wintering Hooded Cranes and analysed the areal changes in salt marsh vegetation and the biomass changes in the underground corms of Sea Bulrush, the main food for Hooded Cranes, during the past 20 years. This study aims to reveal the responses of Hooded Cranes to habitat changes at Chongming Dongtan and to provide scientific references for wetland conservation and restoration practices.

    Chongming Dongtan (31°25ʹ‒31°28ʹ N, 121°50ʹ‒122°05ʹ E) is located at the eastern end of Chongming Island, Shanghai, China. It is an estuarial tidal wetland formed by sediment from the Yangtze River runoff under sea‒land interactions (Cao and Xue, 2016). The main salt marsh plants at Chongming Dongtan include Common Reed (Phragmites australis), Sea Bulrush, and Smooth Cordgrass (Zhang et al., 2020). Among them, Common Reed and Sea Bulrush are the native plants at Chongming Dongtan. These two species were the major salt marsh plants at Chongming Dongtan before the 20th century (Han et al., 2009). As the pioneer species of the tidal flat, Sea Bulrush is mainly distributed in low tide flats, while Common Reed is mainly distributed in medium and high tide flats. In the 1990s, Chongming Dongtan experienced large-scale land claims many times (Li et al., 2022), causing a reduction in the area of natural tidal flats (Han et al., 2009). The enclosed land was mainly transformed into aquaculture ponds or farmland (Fan et al., 2021).

    The invasion of an alien species, Smooth Cordgrass, in the early 2000s changed the plant community at Chongming Dongtan (Li et al., 2022; Gao and Zhang, 2006). Under the combined effect of cordgrass invasion and tidal flat reclamation, the distribution area of Sea Bulrush at Chongming Dongtan declined dramatically. This negatively affected waterbirds that are dependent on Sea Bulrush for their food and habitat (Gan et al., 2009). Since 2013, an ecological project has been implemented at Chongming Dongtan aiming to control Smooth Cordgrass. The main distribution area of Smooth Cordgrass in the eastern and northern tidal flat has been enclosed by constructed dikes. Then, the cordgrass inside the dikes was eliminated using mowing, flooding, and replacement of native plants (Fan et al., 2021). With a length of 24 ​km, the constructed dike inevitably affected sediment deposition and tidal flat development of Chongming Dongtan (Ding, 2016).

    The tidal flat is the main foraging habitat for the Hooded Cranes at Chongming Dongtan (Jing et al., 2002b), so our fieldwork focused on the tidal flat. Hooded Cranes generally forage on Sea Bulrush habitat and rarely use reed and cordgrass habitats on tidal flats due to their dense vegetation, which is unsuitable for large-sized birds (Gan et al., 2009). From 2000 to 2021, crane surveys were generally conducted once every month since late October, when the wintering cranes arrived at Chongming Dongtan. Surveys are performed in the weather without strong wind, rain, and fog. During the surveys, investigators walked along the dikes close to the tidal flat, searching for cranes with a monocular (60 ​× ​). The number of Hooded Cranes was recorded, and their locations were documented according to the geomorphological features of tidal flats. Because the tidal flat is open and cranes are large enough to observe from far away, the accuracy of the record can be guaranteed. We used the largest numbers in a single survey in each season, mianly in January when the population number was stable, as the population size of wintering Hooded Cranes at Chongming Dongtan.

    To identify the changes in salt marsh vegetation over the past two decades, salt marsh vegetation in 2000, 2005, 2010, 2015, and 2020 was interpreted based on Landsat 5/7/8 remote sensing images combined with a vegetation classification algorithm. The coastline was first delineated by manual digitization and visual interpretation on high spatial resolution Google imageries. The inland areas were excluded by constructing an intertidal buffer zone. The identification algorithm of the distribution range of salt marsh vegetation is as follows:

     Vegetation =NDVI0.2EVI0.1LSWI>0;VF=Nvegetation /Ngood 

    where NDVI is the normalized difference vegetation index; EVI is the enhanced vegetation index; LSWI is the land surface water index; VF is the green vegetation frequency per pixel in a year (range 0–1). Nvegetation is the number of observations identified as green vegetation in a year; Ngood is the number of good observations in a year. A frequency threshold of 0.5 was used to classify pixels as vegetated (VF ​≥ ​0.05) or nonvegetated (VF ​ < ​0.05) (Wang et al., 2020a).

    To identify different salt marsh vegetation types, a vegetation classification algorithm based on pixels and phenology was constructed (Zhang et al., 2020; Wang et al., 2020b) as follows:

    Smooth Cordgrass ​= ​LSWI mean(Apr‒May) ​ < ​0 ∩ VF(Dec‒Jan) ​ > ​0;

    Common Reed ​= ​NDVImean(Apr‒May) ​ > ​0.20 ∩ EVImean(May‒Jun) ​≥ ​0.30;

    Scirpus spp. ​= ​LSWImean(Sep‒Oct) ​ < ​−0.05.

    Both Sea Bulrush and Common Bulrush (S. triqueter) were widely distributed on the tidal flat at Chongming Dongtan. However, they cannot be distinguished using remote sensing images due to their similar vegetation features. As a consequence, Sea Bulrush and Common Bulrush were combined and recorded as Scirpus spp.

    To understand the food conditions of the Hooded Cranes, we sampled the underground corms of Sea Bulrush in December 2000 and 2021. In 2000, we randomly set thirty 50 ​cm ​× ​50 ​cm Sea Bulrush plots along the elevation direction (from the high tide zone to the low tide zone) with an interval of about 100 ​m at the main foraging areas of the Hooded Cranes on the southeastern tidal flat (Ma et al., 2003). In 2021, we set sampling areas in the northeastern and eastern Sea Bulrush zones on the tidal flats where cranes foraged and a sampling area on the southeastern zone on the tidal flat where cranes generally foraged in 2000. Two parallel transects were set at an interval of 200 ​m at each sampling area along the elevation direction. We set a sampling site with three 15 ​cm ​× ​15 ​cm Sea Bulrush plots every 50 ​m along each transect until the edge of the Sea Bulrush. At the plots, we collected the underground corms of Sea Bulrush by taking a soil core of 15 ​cm depth and sieved the soil core with a 30-mesh sieve in water. We took the corms to the laboratory to wash, count, and measure their fresh weight and then put them in a 60 ​℃ oven to dry to constant weight and measure the dry weight.

    The number, dry weight, and fresh weight of underground corms of Sea Bulrush in each plot were divided by the plot area to convert them into density data. One-way ANOVAs were applied to compare the number, total weight, and weight of individual corms of the underground corms of Sea Bulrush among the southeastern zone of the tidal flat in 2001 and the northeastern, eastern, and southeastern zones of the tidal flat in 2021. Then, a Tamhane's T2 test was used for post-hoc multiple comparisons.

    From 2000 to 2021, the number of wintering Hooded Cranes at Chongming Dongtan remained at approximately 100, with fluctuations in different years. The maximum number was 147 in 2003 (Fig. 1).

    Figure  1.  Population numbers of wintering Hooded Cranes at Chongming Dongtan from 2000 to 2021.

    In 2000, Hooded Cranes exclusively foraged on tidal flats, with foraging sites located in the southeastern region. When the tidal flat was submerged by tidewater during high spring tide, the Hooded Cranes temporarily rested in the inland area near the dikes and returned to the tidal flat to forage after the tide receded. Since the late 2000s, apart from foraging on the tidal flat, approximately half of the number of Hooded Cranes foraged on farmland near the tidal flat, where they fed on grain leavings, wheat seeds and seedlings, in January and February. Cranes generally returned to forage on tidal flats around late February. The main foraging sites on the tidal flat also moved northwards and were located at the east of the tidal flat in the recent years (Fig. 2).

    Figure  2.  Kernel density map of the main distribution area of the wintering Hooded Cranes at Chongming Dongtan in 2000 (A), 2010 (B), and 2021 (C). The dashed lines illustrate the boundaries of the 1 km buffer area.

    In 2000, the total area of salt marsh vegetation at Chongming Dongtan was 1281.2 ​ha. The distribution area of reed was the largest (approximately 674.6 ​ha), accounting for 52.7% of the total salt marsh vegetation area, mainly distributed in the southern and northern tidal flats with relatively higher elevations. The distribution area of Scirpus spp. was approximately 596.1 ​ha, accounting for 46.5% of the total area of salt marsh vegetation, mainly in the eastern tidal flat. The distribution area of Smooth Cordgrass was approximately 10.5 ​ha, accounting for 0.8% of the total area of salt marsh vegetation, and was scattered on the tidal flats (Fig. 3).

    Figure  3.  Salt marsh vegetation distribution (A, B, C, D, E) and vegetation area on tidal flats (F) at Chongming Dongtan in 2000 (A), 2005 (B), 2010 (C), 2015 (D), and 2020 (E). The red lines in (E) illustrate Scirpus sampling zones in the northeastern, eastern, and southeastern tidal flat. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

    In 2005, the total area of salt marsh vegetation was 1482.4 ​ha. The distribution area of Scirpus spp. increased to 756.1 ​ha, accounting for 51% of the total salt marsh vegetation, mainly distributed in the southeastern tidal flats. The reed had the second largest distribution (approximately 490.5 ​ha), accounting for 33.1% of the total area of salt marsh vegetation, mainly in the higher elevated tidal flat. The distribution area of Smooth Cordgrass increased to approximately 235.8 ​ha, accounting for 15.9% of the total area of salt marsh vegetation, mainly in the northeastern and northern tidal flats (Fig. 3).

    In 2010, the total area of salt marsh vegetation increased to 2443.8 ​ha. Smooth Cordgrass became the largest salt marsh vegetation, with a distribution area of approximately 1418.3 ​ha, accounting for 58% of the total area of salt marsh vegetation. Smooth Cordgrass was dominant in the northern and northeastern parts of the tidal flat. The area of reed was approximately 731.9 ​ha, accounting for 30% of the total area of salt marsh vegetation, mainly in the southern and eastern parts of the tidal flat. The area of Scirpus spp. largely decreased to 293.7 ​ha, accounting for 12% of the total vegetation area, and was mainly distributed in the southeastern and eastern tidal flats. The Scirpus vegetation that dominated in the northern and northeastern tidal flat in 2000 has been replaced by Smooth Cordgrass vegetation (Fig. 3).

    In 2015, the total area of salt marsh vegetation on the tidal flat was 1381 ​ha. The distribution area of Scirpus spp. increased to 909.8 ​ha, accounting for 65.9% of the total salt marsh vegetation, mainly distributed in the northern and southeastern tidal flat. The area of reed was approximately 373.1 ​ha, accounting for 27.0% of the total area of salt marsh vegetation, mainly in the higher elevated tidal flats. The area of Smooth Cordgrass (98.1 ​ha) largely decreased compared to that in 2010, accounting for 7.1% of the total area of salt marsh vegetation, mainly distributed in the northern tidal flat. In addition to the vegetation on the tidal flat, there was 696.8 ​ha of Scirpus spp., 132.2 ​ha of reed, and 286.5 ​ha of Smooth Cordgrass in the wetland restoration zone of Chongming Dongtan (Fig. 3).

    In 2020, the total area of salt marsh vegetation was 2345.3 ​ha. Reed became the major salt marsh vegetation, covering an area of approximately 1690.8 ​ha, accounting for 72.1% of the total area of salt marsh vegetation, and was widely distributed in the southern and southeastern tidal flats. The area of Scirpus spp. was 541.1 ​ha, accounting for 23.1% of the total area, and was mainly distributed in the northern, eastern, and southeastern tidal flats. The area of Smooth Cordgrass decreased further, accounting for 4.8% of the total area of salt marsh vegetation, mainly distributed in the northern tidal flat. In addition to the vegetation on the tidal flat, there was 244.2 ​ha of Scirpus spp. and 708.1 ​ha of reed in the wetland restoration zone of Chongming Dongtan in 2020 (Fig. 3).

    The density, total weight, and individual weight of corms of Sea Bulrush from the southeastern zone in 2021 were significantly lower than those in 2000. The corms collected from the northeastern and eastern zones in 2021, where Hooded Cranes mainly foraged in that year, had significantly higher corm density and total weight than those in the southeastern zone in 2021. When comparing the corms from the main foraging sites in the two different years, namely, the southeastern zone in 2000 and the northern and eastern zone in 2021, corm density displayed a significant increase, while the total weight showed a significant decrease. This might be caused by the shrinkage of corm size, as the weight of individual corms from the northeastern and eastern zones in 2021 was significantly lower than that in 2000 (Table 1).

    Table  1.  Density and weight of the underground corms of Scirpus mariquter in the northeast (NE), east (E), and southeast (SE) zones on the tidal flat in 2000 and 2021.
    SE zone in 2000 (n = 30) SE zone in 2021 (n = 24) NE zone in 2021 (n = 12) E zone in 2021 (n = 16)
    Density of corms (individual/m2) 504.8 ± 36.9a 13.0 ± 37.4b 1770.4 ± 424.3c 1538.9 ± 842.4c
    Total fresh weight (g/m2) 139.3 ± 20.8a 1.6 ± 5.3b 232.5 ± 97.2a 157.3 ± 93.6a
    Total dry weight (g/m2) 0.4 ± 1.3a 69.0 ± 31.6b 60.1 ± 36.2b
    Fresh weight of individual corms (g) 0.28 ± 0.03a 0.10 ± 0.05b 0.13 ± 0.04c 0.10 ± 0.02c
    Dry weight of individual corms (g) 0.02 ± 0.01a 0.04 ± 0.01b 0.04 ± 0.01b
    One-way ANOWA post-hoc test was used to determine the differences between zones. The same letter means insignificant, and different letters mean significant.
     | Show Table
    DownLoad: CSV

    This study indicates that the population size of Hooded Cranes remained stable while the foraging sites have changed at Chongming Dongtan over the past 20 years. Different from their exclusive foraging on the tidal flat in 2000, some Hooded Cranes foraged in farmland since the late 2000s, and the foraging site on the tidal flat has moved northwards in recent years. The distribution area of Sea Bulrush, the main food source of Hooded Cranes, significantly reduced in 2010 but has nearly recovered in recent years. We found a significant decrease in the underground corms of the Sea Bulrush on the southeast tidal flat, the main foraging sites of the Hooded Cranes in 2000. All these results suggest that the changing food conditions have impacted the foraging habitat use of wintering Hooded Cranes at Chongming Dongtan.

    The environmental conditions changed considerably at Chongming Dongtan during the study period. The deposition of sediments transported by the Yangtze River at the east of Chongming Island caused the tidal flat at Chongming Dongtan to extend eastwards in the twentieth century. Over the past 20 years, however, the dramatic reduction in sediments transported by the Yangtze River has caused expansion of tidal flat slowdown and even erosion in some areas (Guo et al., 2021). A dike 24 ​km in length, constructed to eliminate Smooth Cordgrass at Chongming Dongtan, has also affected the hydrology and sedimentation in the surrounding area (Hu, 2020). Both of these factors have affected the physical conditions of the tidal flat and thus impacted the vegetation distribution on the tidal flat (Ge et al., 2019). As a pioneer plant on the tidal flat, the distribution of Sea Bulrush is strongly affected by changes in the tidal flat. We found that in 2020, Sea Bulrush was distributed on the tidal flat outside the new dike constructed to eliminate Smooth Cordgrass (Fig. 3C), where no higher plants used to grow due to the low elevation. This suggests that the new dike caused rapid sediment deposition nearby, thus raising the tidal flat to be suitable for the colonization of Sea Bulrush.

    Habitat change in wintering Hooded Cranes at Chongming Dongtan is closely related to the changes in food availability. Affected by the runoff of the Yangtze River and ocean currents, the deposition speed of sediments on tidal flats was fast in the northern part and slow in the southern part in the early 2000s (Jia et al., 2001). The corms of Sea Bulrush in some regions in the southeastern tidal flat can be washed out from the soil and exposed on the surface of the tidal flat, which is convenient for Hooded Cranes to forage. However, the corms of Sea Bulrush in the northern tidal flat were buried deeper due to continuous sediment deposition, making it unavailable for Hooded Cranes (Ma et al., 2003). Therefore, although Sea Bulrush was widespread on the tidal flats in 2000, Hooded Cranes mainly foraged at the southeastern part of the tidal flat.

    However, we found that at the southern part of the tidal flat where cranes forged in 2000, the corms of Sea Bulrush in 2021 were smaller and in lower density, thus causing a reduced fresh weight in 2021 compared with that in 2000. This may be related to the different growth conditions of Sea Bulrush. Over the past two decades, the area of the southeastern tidal flat has remained stable while the elevation has increased (Chen et al., 2021). Our fieldwork recorded a newly constructed plank road of approximately 1 ​m above the surface of the tidal flat in the region in 2009, while in 2020, the plank road was as high as the surface of the tidal flat, suggesting rapid deposition of sediments during the period. Although there is still a large area of Sea Bulrush vegetation, the elevated tidal flat caused a succession of Sea Bulrush vegetation from the outer zone with sparse plants to the inner zone with dense plants. The corms of Sea Bulrush tend to be underdeveloped when plant density is high (Huang et al., 1993), which might cause a reduced fresh weight of corms in the southeastern tidal flat in 2021.

    In the 2000s, along with the rapid expansion of the invasive Smooth Cordgrass on the tidal flat, Sea Bulrush was competed out and thus significantly reduced in the distribution area, especially in the northern tidal flat where Smooth Cordgrass seriously invaded (Chen et al., 2008). After the implementation of the Smooth Cordgrass elimination project in 2013, the spread of cordgrass on the tidal flat was curbed, while Sea Bulrush gradually recovered. However, the total area of Sea Bulrush in 2021 was still less than that in 2000. We found that the density and weight of the corms of Sea Bulrush in the eastern tidal flat were significantly higher than those in the southeastern tidal flat in 2021. This might be the leading cause for the northwards movement of the foraging cranes on the tidal flat during the study period. Although the potential food, in terms of density and fresh weight of the corms of Sea Bulrush, in the eastern and northeastern part of the tidal flat in 2021 was similar to that at the foraging sites of Hooded Cranes on the southeastern tidal flat in 2000, the corms were buried deeply in the soil due to deposition of sedimentation, which is inconvenient for the forging of cranes (Ma et al., 2003). Actually, in the early 2000s, although Sea Bulrush was widely distributed on the tidal flat, the Hooded Cranes only foraged at the southeastern region, where the scouring of tidewater exposed some corms of Sea Bulrush on the surface of tidal flats and made it convenient for cranes to find food (Ma et al., 2003).

    A total of 244.2 ​ha of Sea Bulrush was recorded inside the wetland restoration zone in 2021, which was formed by artificial planting and germination of soil seed banks. We did not record Hooded Cranes in the wetland restoration zone, likely because this area was managed to be covered by water to provide suitable habitat for waterfowl, and thus, the corms are unavailable for the Hooded Cranes, which prefer to forage on the exposed ground at Chongming Dongtan. However, the Sea Bulrush in the wetland restoration zone has provided food for many herbivorous waterfowl, including the Tundra Swans (Cygnus columbianus) in winter. The corms of Sea Bulrush were the main food for wintering Tundra Swan at Chongming Dongtan (Huang et al., 1993). Unlike Hooded Cranes forging for the corms of Sea Bulrush when the tidal flat was exposed, Tundra Swans foraged for the corms when the tidal flat was submerged by tidewater (Huang et al., 1993). The number of Tundra Swans was more than 3000 around 1990 but decreased to a dozen in the 2000s, mainly due to the reduction in Sea Bulrush and the increase in human disturbance on tidal flats (Ma et al., 2009). Benefiting from the corms of Sea Bulrush in the wetland restoration zone, the population size of wintering Tundra Swans has increased to over 1000 in 2021 at Chongming Dongtan. Tundra Swans mainly forage in the wetland restoration zone and thus reduce food competition with Hooded Cranes (Zhao et al., 2013), which cannot use the corms of Sea Bulrush in the wetland restoration zone.

    The use of farmland near the tidal flat by the Hooded Cranes might be closely related to the local agricultural activities at Chongming Dongtan. In 2000, tidal flats had just undergone a new round of land claiming. The soil salinity in the newly enclosed area was high, which was unsuitable for crop growth. The primary land use type of the enclosed area was aquaculture ponds, which can be used as high tide roosts but not as foraging habitats for Hooded Cranes (Ma et al., 2004). As a consequence, Hooded Cranes were recorded exclusively foraging on tidal flats. Along with the desalination of the soil inside the enclosed region for several years, some aquaculture ponds were transformed into farmland, and crops such as wheat and rice were planted. Hooded Cranes started to forage for grain leavings or wheat seeds and seedlings in farmland. The foraging cranes peaked in January and February, likely because food is abundant in farmland along with sowing and seed germination. As the wheat grew, the seedlings were no longer suitable for Hooded Cranes to eat, so Hooded Cranes mainly foraged for corms of Sea Bulrush on the tidal flats in March until departure from Chongming Dongtan. When Hooded Cranes forage in farmlands, despite farmers using firecrackers to drive them out some still foraged in the farmland, suggesting that food resources might be insufficient on tidal flats. The consumption of grains in farmland at Chongming Dongtan is similar to the cases of Hooded Cranes in other wintering grounds (Ohsako, 1989; Liu et al., 2001). The human-bird conflicts caused by crane forging in farmland, which is common in human-dominated landscapes (Cheng et al., 2022, Wang et al., 2022), deserve attention in the future.

    Both Sea Bulrush and Common Bulrush are distributed on the tidal flat of Chongming Dongtan. Previous investigations found that the northern and northeastern tidal flats mainly distributed Sea Bulrush, while the southeastern tidal flat had both plants. This may be related to the higher salinity of the water in the northern part of Chongming Dongtan, and Sea Bulrush is relatively more tolerant to high salinity (Ding et al., 2015). Unlike the Sea Bulrush with developed underground corms, the corms of Common Bulrush are underdeveloped all the time (Huang et al., 1993), making Common Bulrush rarely used by the Hooded Cranes. However, it is difficult to distinguish them from remote sensing data due to the similarity in appearance and phenology between Sea Bulrush and Common Bulrush. Therefore, this study overestimated the distribution area of Sea Bulrush. More field investigations are needed to determine the actual distribution area and location of the two different bulrushes on the tidal flat.

    Hooded Cranes have two populations worldwide. One population has over 10,000 individuals wintering in Japan and South Korea, and the other has approximately 1000 individuals wintering in the middle and lower reaches of the Yangtze River in China (BirdLife International, 2016). Although habitat conditions largely changed over the past two decades, the number of wintering Hooded Cranes at Chongming Dongtan remained stable. The migration patterns of Hooded Cranes in Japan have been identified by satellite tracking (Mi et al., 2018). Tracking the annual movements of Hooded Cranes at Chongming Dongtan and other wintering areas in mainland China in the future would help to reveal the linkages between the flocks at different wintering sites.

    Over the past two decades, although population number of the wintering Hooded Cranes remained stable, the distribution, habitat, and food of the Hooded Cranes largely changed at Chongming Dongtan, which is closely related to the changes of local environment conditions. In view of the limited natural food resources on the tidal flat for wintering Hooded Cranes and the intense human disturbance on Hooded Cranes foraging on farmland, we suggest speeding up the recovery of the Sea Bulrush community on the tidal flat by artificial planting and other auxiliary measures. Publicity and education should be carried out to local farmers to reduce the disturbance on Hooded Cranes foraging in farmland. Specific economic compensation is also needed to compensate for farmers' losses caused by Hooded Cranes. In addition, long-term monitoring of the dynamics of the Hooded Crane population and Sea Bulrush distribution is required to understand the changes in Hooded Cranes and their habitat on longer time scales.

    ZM, JM and YC conceived the idea. YC, ZM, SY, WW, XF, QM and DN organized and conducted the fieldwork. YC and YT analyzed the data. YC and ZM led the writing of the manuscript. YC, YT, JM, ZM participated in writing and editing the manuscript. All authors read and approved the final manuscript.

    The authors confirm that all the fieldwork was conducted with the permission and support of the Management Office of Chongming Dongtan Nature Reserve and was strictly complied with the requirement of Chinese Wild Animal Protection Law.

    The authors declare that they have no competing interests.

    We thank the Chongming Dongtan National Nature Reserve for support of this study. This study was financially supported by the National Key Research and Development Program of China (2022YFF1301004), the Science and Technology Department of Shanghai (21DZ1201902), and the Shanghai Landscaping and City Appearance Administrative Bureau (G201610).

  • Block, W.M., Brennan, L.A., 1993. The habitat concept in ornithology. Curr. Ornithol. 11, 35-91.
    BirdLife International, 2016. Grus monacha. The IUCN Red List of Threatened Species 2016: e. T22692151A93337861. doi: .(Accessed2November2022).
    Cao, M., Xue, J.H., 2016. Review of service function and value research on Chongming Dongtan wetland ecosystem. J. Nanjing Forest. Univ. Nat. Sci. 40(5), 163-169.
    Chen, J.Q., Zhao, B., Ren, W.W., Saunders, S.C., Ma, Z.J., Li, B., et al., 2008. Invasive Spartina and reduced sediments: Shanghai's dangerous silver bullet. J. Plant Ecol. 1, 79-84.
    Chen, X.H., Zhang, G.A., Zhang, W.D., Li, M.T., 2021. Influence of sediment transport reduction in the Yangtze River on sediment transport in typical shoal sections of the estuary. J. Sediment Res. 46(6), 44-50.
    Cheng, C.Y., Liu, J.J., Ma, Z.J., 2022. Effects of aquaculture on the maintenance of waterbird populations. Conserv. Biol. 36, e13913.
    Ding, W.H., 2016. The Effects of Spartina Ecological Management Project on the Tidal Flat Habitat of Grus monacha in Chong-Ming Dongtan. Master's Thesis. East China Normal University, Shanghai.
    Ding, W.H., Jiang, J.Y., Li, X.Z., Huang, X., Li, X.Z., Zhou, Y.X., et al., 2015. Spatial distribution of species and influencing factors across salt marsh in southern Chongming Dongtan. Chin. J. Plant Ecol. 39, 704-716.
    Fan, J., Wang, X.D., Wu, W., Chen, W.P., Ma, Q., Ma, Z.J., 2021. Function of restored wetlands for waterbird conservation in the Yellow Sea coast. Sci. Total Environ. 756, 144061.
    Gao, Z.G., Zhang, L.Q., 2006. Multi-seasonal spectral characteristics analysis of coastal salt marsh vegetation in Shanghai, China. Estuar. Coast. Shelf Sci. 69, 217-224.
    Gan, X. J, Cai, Y. T, Choi, C.Y., Ma, Z.J., Chen, J.K., Li, B., 2009. Potential impacts of invasive Spartina alterniflora on spring bird communities at Chongming Dongtan, a Chinese wetland of international importance. Estuar. Coast. Shelf Sci. 83, 211-218.
    Ge, Z.M., Li, S.H., Tan, L.S., Li, Y.L., Hu, Z.J., 2019. The importance of the propagule-sediment-tide "power balance" for revegetation at the coastal frontier. Ecol. Appl. 29, e01967.
    Guo X.J., Fan, D.D., Zheng, S. W, Wang, H.M., Zhao, B.C., Qian, C.J., 2021. Revisited sediment budget with latest bathymetric data in the highly altered Yangtze (Changjiang) Estuary. Geomorphology 391, 107873.
    Han, Z., Liu, Y., Yun, C.X., Zheng, J.H., 2009. Spatial and temporal dynamics of vegetation community in Chongming Dongtan based on remote sensing and GIS. In: Proceedings of the 14th China Ocean (Coastal) Engineering Symposium. China Ocean Press, Beijing, pp. 280–284.
    Hu, M.Y., 2020. Study on the synergistic dynamics of frontier vegetation and sedimentation in the intertidal zone of Chongming Dongtan. Master's thesis. East China Normal University, Shanghai.
    Huang, Z.Y., Sun, Z.H., Yu, K, Zhou, M.Z., Zhao, R.Q., Gao, J., 1993. Bird Resources and Habitats in Shanghai. Fudan University Press, Shanghai.
    Jia, H.L., Liu, C.Y., Yang, O., 2001. Dynamic sediment environment of the north branch of Changjiang estuary. J. East China Normal Univ. Nat. Sci. 1, 90-96.
    Jing, K., Tang, S.M., Chen, J.K., Ma, Z.J., 2002a. Wintering ecology of the Hooded Crane in the eastern tideland of Chongming Island. Chin. J. Zool. 37(6), 29-34.
    Jing, K., Tang, S.M., Chen, J.K., Ma, Z.J., 2002b. Primary research on the characteristics of feeding sites of Grus monacha in the east tide flat of Chongming. Zool. Res. 23(1), 84-88.
    Johnson, M.D., Sherry, T.W., Holmes, R.T., Marra, P.P., 2006. Assessing habitat quality for a migratory songbird wintering in natural and agricultural habitat. Conserv. Biol. 20, 1433-1444.
    Kjellen, N., 1994. Moult in relation to migration in birds ‒ a review. Ornis Svecica 4, 1-24.
    Li, S., Dong, B., Gao, X., Xu, H.F., Ren, C.Q., Liu, Y.R., et al., 2022. Study on spatio-temporal evolution of habitat quality based on land-use change in Chongming Dongtan, China. Environ. Earth Sci. 81(7), 1-12.
    Lindström, Å., Piersma, T., 1993. Mass changes in migrating birds: the evidence for fat and protein storage re-examined. Ibis 135, 70-78.
    Ling, Y., Zhou, L., Song, A.Y., 2015. The effects of food abundance and disturbance on foraging flock patterns of the wintering Hooded Crane (Grus monacha). Avian Res. 6, 15.
    Liu, Z.Y., Xu, W.B., Wang, Q.S., Shi, K.C., Xu, J.S., Yu, G.Q., 2001. Study on the environmental capacity of Crane in Shengjin Lake during overwintering period. Resour. Environ. Yangtze Basin 10, 454-459.
    Ma, Q., Wu, W., Tang, C.D., Niu, D.L., Wu, J.H., Ma, Z.J., 2017. Effects of habitat restoration on the diversity of bird and macrobenthos in the Chongming Dongtan wetland. J. Nanjing Forest. Univ. Nat. Sci. 41(1), 9-14.
    Ma, Z.J., Li, B., Jing, K., Zhao, B., Tang, S.M., Chen, J.K., 2003. Effects of tidewater on the feeding ecology of hooded crane (Grus monacha) and conservation of their wintering habitats at Chongming Dongtan, China. Ecol. Res. 18, 321-329.
    Ma, Z.J., Li, B., Zhao, B., Jing, K., Tang, S.M., Chen, J.K., 2004. Are artificial wetlands good alternatives to natural wetlands for waterbirds? A case study on Chongming Island, China. Biodiver. Conserv. 13, 333-350.
    Ma, Z.J., Wang, Y., Gan, X.J., Li, B., Jing, K., Tang, S.M., Chen, J.K. 2009. Change and loss of wetland habitats and waterbird population trends at Chongming Dongtan of the Yangtze River estuary, China. Environ. Manag. 43, 1187-1200.
    Mi, C., Møller, A.P., Guo, Y., 2018. Annual spatio-temporal migration patterns of Hooded Cranes wintering in Izumi based on satellite tracking and their implications for conservation. Avian Res. 9, 23.
    Myers, J.P., Morrison, R., Antas, P., Harrington, B., Lovejoy, T.E., Sallaberry, M., et al., 1987. Conservation strategy for migratory species. Am. Sci. 75, 19-26.
    Ohsako, Y., 1989. Flock, organization, dispersion and territorial behaviour of wintering Hooded Cranes Grus monacha in Izumi and Akune, Kyushu. Jpn. J. Ornithol. 38, 15-29.
    Wang, W., Zhou, L.Z., Fu, R., Cheng, L., Yan, S.F., Mahtab, N., et al., 2021. Effects of foraging site distances on the intestinal bacterial community compositions of the sympatric wintering Hooded Crane (Grus monacha) and Domestic Duck (Anas platyrhynchos domesticus). Avian Res. 12, 20.
    Wang, X.D., Li, X.H., Ren, X.T., Jackson, M.V., Fuller, R.A., Melville, D.S., et al., 2022. Effects of anthropogenic landscapes on population maintenance of waterbirds. Conserv. Biol. 36, e13808.
    Wang, X.X., Xiao, X.M., Zou, Z.H., Hou, L.Y., Qin, Y.W., Dong, J.W., et al., 2020a. Mapping coastal wetlands of China using time series Landsat images in 2018 and Google Earth Engine. ISPRS J. Photogram. Remote Sens. 163, 312-326.
    Wang, X.X., Xiao, X.M., Zou, Z.H., Chen, B.Q., Ma, J., Dong, J.W., et al., 2020b. Tracking annual changes of coastal tidal flats in China during 1986-2016 through analyses of Landsat images with Google Earth Engine. Remote Sens. Environ. 238, 110987.
    Zhang, X., Xiao, X., Wang, X., Xu, X., Chen, B., Wang, J., et al., 2020. Quantifying expansion and removal of Spartina alterniflora on Chongming island, China, using time series Landsat images during 1995-2018. Remote Sens. Environ. 247, 111916.
    Zhao, F.T., Zhou, L.Z., Xu, W.B., 2013. Habitat utilization and resource partitioning of wintering Hooded Cranes and three goose species at Shengjin Lake. Chinese Birds 4, 281-290.
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