Spatiotemporal Distribution and Habitat Characteristics of Shorebirds in the Coastal Wetlands of Dalian, Liaoning, China

Abstract

The coast of Dalian in Liaoning Province, China, is one of the most important habitats for migratory shorebirds along the East Asia–Australasian Flyway. However, the coastal areas of Dalian have been modified extensively by various projects, including reclamation and the construction of aquaculture and port facilities, embankment buildings, cross-sea passages, and wind farms, which have led to significant damage to the coastal habitats of shorebirds. Assessing the spatiotemporal distribution and habitat characteristics of shorebirds is of great importance to biodiversity conservation. The present study involved a 15-month-long survey of shorebirds in nine coastal wetlands of Dalian from August 2021 to October 2022. In total, 31 species of shorebirds, belonging to five families, were recorded. Migratory shorebirds were the most frequently observed, accounting for 77% of the recorded shorebirds. Dunlin (Calidris alpina), Kentish plover (Charadrius alexandrinus), Eurasian curlew (Numenius arquata), and Far Eastern curlew (Numenius madagascariensis) were the most abundant species. Both species richness and species abundance peaked in May and again in September. The Zhuanghe Estuary boasted the highest species diversity, while the Huli Estuary wetland exhibited the greatest species abundance. The type of habitat and the spatial extent of natural wetlands were the main variables influencing the spatial distribution of waterbirds. By identifying the population characteristics and habitat status of shorebirds in Dalian, the results provide support for shorebird conservation and habitat management.

1. Study Methods

1.1. Survey Areas

Coastal birds are near the top of the marine food chain. Nonetheless, they face numerous anthropogenic threats caused by profound human impacts on their shoreline habitat. For instance, human activity on beaches can negatively affect halophytic dune plants [1,2,3], which provide important resources for nesting plovers, such as shading, shelter, and nesting materials. Therefore, these activities affect coastal bird behavior and breeding ecology [4] and also lead to the destruction of nests and eggs [5,6,7,8]. Domestic dogs can act as predators of eggs and chicks or may disturb egg-incubating adults. For example, when dogs are present near plover nests, plovers may move away from the nest, exposing eggs/chicks to predation or excessive sunlight, which can compromise successful hatching and fledging [9]. Fishermen often cause an accumulation of fishing lines and hooks on beaches, creating a type of litter that can entrap birds [10]. Mechanical beach cleaning also poses another threat to shorebirds that is linked to the need to keep beaches aesthetically attractive for human visitors while incidentally negatively impacting coastal biodiversity [11,12]. During the breeding (nesting) period, nests may be disturbed by trampling, motor vehicle traffic, and the generation of plastic litter by people [13]. When shorebirds react to people with alarm behavior, this leads to an energy cost and reduces the time available to birds for feeding, preening, or resting. More seriously, the presence of people may prevent chicks from being fed because they hide in response to alarm calls, and it certainly prevents the adults from brooding their chicks. In addition, persistent alarm calls by parent birds may attract the attention of predators, such as raptors or corvids [14].

Hence, the current status and comprehensive changes in the marine environment caused by humans can be evaluated by surveying the birds in coastal wetlands. A remarkable feature of the life history of shorebirds is their reciprocating migration between the northern and southern hemispheres [15,16]. Many factors influence the dynamic spatiotemporal distribution of populations during migration, such as climatic change, predation, competition, and food supply [17,18]. However, the most important factor affecting the distribution of migrating birds is the habitat change in breeding, wintering, and food supply habitats along the migration route [19,20]. Because shorebirds primarily stay in coastal (inland) wetlands, the changes in shorebird populations can reflect the status of wetland ecosystems [21]. Past research on shorebirds in China has mainly focused on species composition [22], the frequency and distribution of species [23,24], dynamic situations occurring during migration [25], selection and use of habitats, carrying capacity of habitats [26], and feeding habits of the birds [27].

Dalian is located in Liaoning Province in the southernmost part of Northeast China on the Liaodong Peninsula; it is surrounded by the Bohai Sea to the west and the Yellow Sea to the south and east. It is located in the warm temperate zone of the northern hemisphere and has a temperate monsoon climate with maritime characteristics. Dalian features plentiful wetland resources, including natural estuaries, mudflats, and estuary deltas along with anthropogenic wetlands including salt and aquaculture farms. The coastal wetlands are mainly distributed in the coastal section along the Yellow Sea on the north of the Qingyun Estuary and the areas around Jinpu Bay and Changxing Island of the Bohai Sea, with a total area of about 1400 km² of wetlands [28]. These wetlands provide ideal breeding, resting, and wintering grounds for wading birds. As a result, tens of millions of birds that migrate long distances in the East Asia–Australasia Flyway use these important shorebird habitats of China with major stopovers located on the Northeast Asian Flyway [29]. Birds are highly sensitive to changes in habitat; shorebirds are widely used in research to document human interference in these landscapes or changes in habitat quality [30,31]. At present, few studies have addressed the populations of shorebirds in the coastal wetlands of Dalian. Especially in the coastal areas of China, few studies have reviewed the timing of regional shorebird migration, shorebird population structure, or the direction of migration in different ecological land types. Some scholars have conducted research using correlation analysis to document links between dominant passeriform species and climatic factors in Laotie Mountain of Dalian [32]. Consequently, the present study on the shorebirds of the coastal wetlands of Dalian was conducted. The goals of this study are (1) to gather foundational information about the community structure and spatial–temporal distribution of shorebirds in the study area and (2) provide scientific evidence to support the understanding of shorebird migration patterns, the impacts of climate change and human activities on these birds, and the conservation and management of Dalian’s coastal wetlands.

Based on the field surveys, coupled with previous field surveys [33], nine representative coastal wetland areas were selected as the survey areas for shorebirds. These areas include Haidao village and Anzi estuary along the Bohai Sea coast as well as Qingyun, Dengsha, Huayuankou, Zhuanghe, Yingna, Huli, and Diyan estuaries along the coast of the Yellow Sea (Figure 1).

The types of coastal wetlands of Dalian in the survey areas mainly included salt farms and aquaculture farms, and the seacoast wetlands mainly included estuaries, mudflats, and estuary deltas (as shown in Figure 2).

1.2. Field Sampling Techniques

From August 2021 to October 2022, an extensive 15-month field survey was conducted in the coastal wetlands of Dalian to study shorebirds. This survey was systematically carried out on the 1st or 15th day (during the spring tide period) of each lunar month. For data collection, a combination of sample points and sample lines was adopted in every survey area [34]. Continuous observation and recording were carried out for the birds in the wetlands using the direct count method. During each survey, the surveyors counted the birds in their fields of view with 15 × 56 binoculars (Swarovski Optic, Tyrol, Austria) and 20–75 × 85 spotting scopes (Zeiss, Oberkochen, Germany) on the mudflats. Additionally, digital cameras (Nikon D5, Chiyoda-ku, Tokyo, Japan) equipped with 800 mm fixed-focus lenses were used to assist in recording the observations. For highly alert waterbird species, covert surveys were conducted using camouflage nets and vehicle-mounted equipment to minimize disturbance. In determining the numbers of individuals present, the maximum value retention method was adopted, effectively calculating the cumulative maximum abundance of each across all surveyed areas [35].

1.3. Data Analysis and Statistics

For birds with large numbers of individuals or those birds that flew away quickly, numbers were estimated by units of 5, 10, 50, or 100 birds. The numbers of migratory birds were recorded by observing in a single direction to avoid repeated recording as birds arrived and departed the area of the observer.

The diversity ($H^{\prime }$) of shorebirds at each survey site was calculated with the Shannon–Wiener Index [36]:

$$H^{\prime }=-\sum _{i=1}^S{P}_i\ln P_i$$

where $S$ is the number of species present in a survey area and $P_i$ is the ratio of the number of individuals of the $i$th species in a survey area to the total number of individuals of birds of all species observed in the survey area.

The present study employed satellite remote sensing image data from 36 scenes, including 24 scenes with medium resolution and 12 scenes with high resolution; these data were acquired from the China Center for Resources Satellite Data and Application (https://www.cresda.com/zgzywxyyzx/index.html, accessed on 18 October, 2022). Satellite remote sensing images acquired during low tide were chosen as often as possible, and all images fully covered the survey areas. The cloud coverage rate was limited to less than 10%, and adjacent images were limited to an overlap of no less than 5% of image width. Clear images with rich hierarchies were chosen. The image preprocessing process was completed mainly using remote sensing image preprocessing methods such as radiation, atmospheric, and geometric correction along with image fusion. The high-resolution remote sensing images were processed with applications such as ArcGIS (Environmental Systems Research Institute, Redlands, CA, USA), the Earth Resource Data Analysis System, and the Environment for Visualizing Images. Based on the site surveys, important bird habitats were classified primarily through manual visual interpretation assisted by the classification results of coastal wetland ecosystems. Using this method, a map of the distribution of important bird habitats in coastal wetlands was obtained, and a bird habitat factor was extracted. The anthropogenic threat types in the coastal wetlands were complex and diverse, so the survey indices were designed based on the anthropogenic perturbations. The survey results of anthropogenic threat types in the study areas in 2010, 2015, and 2020 were obtained using the method of simultaneous remote sensing analysis with manual visual interpretation and computer image automatic interpretation processing. In addition, special information such as that related to roads and wind farms was extracted at the ecosystem scale based on the survey content.

The statistical analysis of data was conducted using SPSS 20.0, and plotting was carried out using Excel software (Microsoft Corp., Redmond, WA, USA). Pearson correlation analysis was used to analyze the relationships between the lengths and areas of different types of coastlines, the landscape area, and the mean patch area of habitats with the species present and abundance of waterbirds. Polynomial regression analysis was used to analyze the relationships between the lengths of muddy and reclaimed coastlines with the species present and the abundance of waterbirds.

2. Results

2.1. Species Composition

In total, 30,933 shorebirds belonging to 31 species were recorded including 1, 2, 5, and 23 species of the families Haematopodidae, Recurvirostridae, Charadriidae, and Scolopacidae, respectively (

Table 1. Overview of the survey areas.

No.	Station	Latitude and Longitude	Overview of Area
1	Haidao Village	39°35′12.7″ N, 121°35′35.9″ E	Near the Fuzhou River estuary, with large area of distributed paddy fields and aquaculture ponds.
2	Anzi River estuary	39°24′7.5″ N, 121°55′40.1″ E	Located in the east of Pulandian Bay, with salt fields and aquaculture ponds on both estuary banks.
3	Qingyun River estuary	39°7′22.8″ N, 122°2′14.6″ E	Located in the northeast of Dalian Jinshitan National Tourist Resort. There were abandoned aquaculture ponds on both banks of the Qingyun River estuary, and strip observation was conducted along the river banks.
4	Dengsha River estuary	39°10′43.2″ N, 122°6′25″ E	Located in the south of Dengshahe Subdistrict, Jinzhou District, Dalian City. There were hard covering green belts on both banks of the river course at the estuary, and there were aquatic plants, e.g., reeds, distributed in the river course, so the ecological landscapes were relatively complex.
5	Huayuankou	39°31′24.3″ N, 122°39′18.2″ E	Located in Zhuanghe Huayuankou Economic Zone. It was a muddy mudflat, flat and broad, with an area up to 40 km2. There was a dam constructed along the coast at Huayuankou, and there were aquaculture ponds distributed along the estuary banks.
6	Zhuanghe River estuary	39°40′3.4″ N, 123°0′7.5″ E	Located in the south of the urban area of Zhuanghe City, and formed by the convergence of three rivers, i.e., the Zhuanghe River, the Reshui River, and the Baoma River, in the estuary area. The estuary area was a muddy and sandy mudflat, with crisscrossing tidal creeks.
7	Yingna River estuary	39°44′24.3″ N, 123°13′13″ E	Located in the west of the Qingduizi Bay, Zhuanghe. There were aquaculture ponds on both banks of the river course at the estuary, and the estuary mudflat was broad, with Suaeda glauca distributed.
8	Huli River estuary	39°47′34.6″ N, 123°16′45.7″ E	Located in the bottom of the Qingduizi Bay, Zhuanghe. There was a muddy mudflat at the estuary, with breakwaters constructed on the coast.
9	Diyan River estuary	39°48′2.7″ N, 123°24′40.2″ E	Located in the east of Qingduizi Bay, Zhuanghe. There were aquaculture ponds, nursery rooms, and fish meal processing plants, etc., on both banks of the river course at the estuary.

). The International Union for the Conservation of Nature lists the Mongolian plover (Anarhynchus mongolus) as a globally endangered species and the Far Eastern curlew (Numenius madagascariensis) as a globally threatened species. In addition, 22 and 25 species are currently covered by the China–Australia Migratory Bird Agreement and the China–Japan Migratory Bird Agreement, accounting for 71 and 81% of all shorebird species observed, respectively. All shorebird species found in the survey were listed on the “List of terrestrial wildlife under state protection, which are beneficial or of important economic or scientific value” of China. Shorebirds image in a survey area was shown in Figure 3.

From the perspective of the sedentary type, migratory birds had the most species, i.e., 24 species, accounting for 77% of the total bird species. Summer migratory birds and passing (or summer migratory) birds had six species and two species, respectively, accounting for 16%, and 6% of the total bird species, respectively.

2.2. Dominant and Rare Species

Generally, the abundance of a species making up more than 10% of the total abundance of all species is considered to be a dominant species, while a species with an abundance of less than 1% of the total abundance of all species is considered to be a rare species [34]. Based on this method the coastal wetlands of Dalian had four dominant shorebird species including Dunlin (Calidris alpina), Kentish plover (Charadrius alexandrinus), Eurasian curlew (Numenius arquata), and Far Eastern curlew. Dunlin was the most abundant with 4898 birds or 31% of all shorebirds, followed by Kentish plover, Eurasian curlew, and Far Eastern curlew, which accounted for 18, 17, and 10%, of all shorebirds, respectively. The seven common species included bar-tailed godwit (Limosa lapponica), whimbrel (Numenius phaeopus), grey plover (Pluvialis squatarola), great knot (Calidris tenuirostris), terek sandpiper (Xenus cinereus), Mongolian plover (Anarhynchus mongolus), and greenshank (Tringa nebularia), listed in frequency of occurrence. The 20 rare species included red knot (Calidris canutus), Pacific golden plover (Pluvialis fulva), and green sandpiper (Tringa ochropus), among others.

From the perspective of the range of distribution of each species, grey plover, whimbrel, Far Eastern curlew, greenshank, and pratincole (Tringa glareola) were widely distributed, and all were found in eight out of the nine survey areas. Little ringed plover (Charadrius dubius), Kentish plover, terek sandpiper, Dunlin, Eurasian oystercatcher (Haematopus ostralegus), and black-winged stilt (Himantopus himantopus) were distributed in five to seven of the nine survey areas. Common snipe (Gallinago gallinago), green sandpiper, marsh sandpiper (Tringa stagnatilis), common sandpiper (Actitis hypoleucos), ruddy turnstone (Arenaria interpres), and broad-billed sandpiper (Limicola falcinellus) were found in only one survey area each (

Table 2. Quantity and distribution of shorebirds in coastal wetlands of Dalian.

No.	Order	Family	Species	Latin Name	Quantity (Birds)	Protection Level	IUCN2024	RDB	CJMBA	CAMBA	Sedentary Type (Month)	Distribution
1	Charadriiformes	Haematopodidae	Oyster catcher	Haematopus ostralegus	53	△			○		Summer (March–October)	Dengsha River estuary, Huayuankou, Zhuanghe River estuary, Yingna River estuary, Diyan River estuary
2		Recurvirostridae	Black-winged stilt	Himantopus himantopus	36	△			○		Summer (April, May, August)	Anzi River estuary, Qingyun River estuary, Dengsha River estuary, Huayuankou, Huli River estuary
3			Avocet	Recurvirostra avosetta	11	△			○		Passing, summer (May)	Qingyun River estuary, Diyan River estuary
4		Charadriidae	Pacific golden plover	Pluvialis fulva	2	△			○		Passing (April, September)	Dengsha River estuary, Huli River estuary
5			Grey plover	Pluvialis squatarola	612	△			○	●	Passing (April–May, August–November)	Anzi River estuary, Qingyun River estuary, Dengsha River estuary, Huayuankou, Zhuanghe River estuary, Yingna River estuary, Huli River estuary, Diyan River estuary
6			Little ringed plover	Charadrius dubius	31	△				●	Summer (April, May, June, August)	Anzi River estuary, Qingyun River estuary, Dengsha River estuary, Huayuankou, Zhuanghe River estuary, Diyan River estuary
7			Kentish plover	Charadrius alexandrinus	2911	△					Passing, summer (March–July, September–Octobert)	Anzi River estuary, Qingyun River estuary, Dengsha River estuary, Huayuankou, Zhuanghe River estuary, Huli River estuary, Diyan River estuary
8			Mongolian plover	Charadrius mongolus	219	△	E		○	●	Passing (May, September)	Huayuankou, Zhuanghe River estuary, Huli River estuary, Diyan River estuary
9		Scolopacidae	Common snipe	Gallinago gallinago	4	△					Passing (September)	Huli River estuary
10			Black-tailed godwit	Limosa limosa	28	△		I	○	●	Passing (May, September, October)	Songmudao Bridge at Anzi River estuary, Huayuankou, Diyan River estuary
11			Bar-tailed godwit	Limosa lapponica	859	△			○	●	Passing (April, May, July, August, September)	Huayuankou, Zhuanghe River estuary, Huli River estuary, Diyan River estuary
12			Whimbrel	Numenius phaeopus	708	△			○	●	Passing (April–September)	Anzi River estuary, Qingyun River estuary, Dengsha River estuary, Huayuankou, Zhuanghe River estuary, Yingna River estuary, Huli River estuary, Diyan River estuary
13			Eurasian curlew	Numenius arquata	2663	△			○	●	Passing (February–May, July–November)	Haidao Village, Dengsha River estuary, Yingna River estuary
14			Far Eastern curlew	Numenius madagascariensis	1544	△	E			●	Passing (March–November)	Anzi River estuary, Qingyun River estuary, Dengsha River estuary, Huayuankou, Zhuanghe River estuary, Yingna River estuary, Huli River estuary, Diyan River estuary
15			Spotted redshank	Tringa erythropus	28	△			○		Passing (May, July, September–November)	Dengsha River estuary, Anzi River estuary, Zhuanghe River estuary
16			Redshank	Tringa totanus	8	△			○	●	Passing (April–June, September)	Zhuanghe River estuary, Diyan River estuary
17			Greenshank	Tringa nebularia	192	△			○	●	Passing (May, July–November)	Anzi River estuary, Qingyun River estuary, Dengsha River estuary, Huayuankou, Zhuanghe River estuary, Yingna River estuary, Huli River estuary, Diyan River estuary
18			Green sandpiper	Tringa ochropus	1	△			○		Summer (September)	Zhuanghe River estuary
19			Marsh sandpiper	Tringa stagnatilis	7	△			○	●	Passing (September)	Huli River estuary
20			Pratincole	Tringa glareola	71	△			○	●	Passing (April, May, August, September)	Anzi River estuary, Qingyun River estuary, Dengsha River estuary, Huayuankou, Zhuanghe River estuary, Yingna River estuary, Huli River estuary, Diyan River estuary
21			Common sandpiper	Actitis hypoleucos	4	△			○	●	Summer (August)	Dengsha River estuary
22			Terek sandpiper	Xenus cinereus	318	△			○	●	Passing (April–October)	Dengsha River estuary, Huayuankou, Zhuanghe River estuary, Yingna River estuary, Huli River estuary, Diyan River estuary
23			Grey-tailed tattler	Tringa brevipes	18	△				●	Passing (May, August, September)	Qingyun River estuary, Shahe River estuary, Zhuanghe River estuary
24			Ruddy turnstone	Arenaria interpres	11	△			○	●	Passing (May)	Huayuankou
25			Great knot	Calidris tenuirostris	455	△	E			●	Passing (April, May, September)	Huayuankou, Zhuanghe River estuary, Huli River estuary
26			Red-necked stint	Calidris ruficollis	63	△			○	●	Passing (May, October)	Zhuanghe River estuary, Diyan River estuary
27			Sharp-tailed sandpiper	Calidris acuminata	19	△			○		Passing (May)	Qingyun River estuary, Dengsha River estuary, Huayuankou, Diyan River estuary
28			Curlew sandpiper	Calidris ferruginea	8	△			○	●	Passing (May)	Zhuanghe River estuary, Diyan River estuary
29			Dunlin	Calidris alpina	4898	△			○	●	Passing (March–May, August–November)	Anzi River estuary, Huayuankou, Zhuanghe River estuary, Yingna River estuary, Huli River estuary, Diyan River estuary
30			Red knot	Calidris canutus	3	△			○	●	Passing (May)	Zhuanghe River estuary, Huli River estuary
31			Broad-billed sandpiper	Limicola falcinellus	9	△			○	●	Passing (May)	Diyan River estuary

Notes: “△” denotes important migratory bird and waterbird with protection significance or important economic or scientific value listed in the “List of terrestrial wildlife under state protection, which are beneficial or of important economic or scientific value”; “IUCN2024” denotes threat level by the International Union for Conservation of Nature, VU—vulnerable, EN—endangered, CR—critically endangered; “RDB” denotes China Red Data Book of Endangered Animals, R—rare, E—endangered, V—vulnerable, I—indeterminate; “summer” denotes summer migratory bird; “winter” denotes winter migratory bird; “○” denotes bird under CJMBA; “●” denotes bird under CAMBA; “resid.” denotes resident bird; “passing” denotes passing bird; and the contents in the brackets denote residing months.

).

2.3. Spatiotemporal Distribution and Diversity

The number of shorebird species present in the Dalian region exhibited an obvious seasonal pattern with shorebird populations mainly concentrated in spring, summer, and autumn; none were observed in winter. The number of species present peaked in May and September, with the number of species present being relatively small in March, June, July, and October. The number of shorebird species in the Diyan River estuary, Huayuankou, and the Zhuanghe River estuary in May were the largest at 18, 17, and 17, respectively. Relatively large numbers of shorebird species (12) were also observed in both the estuaries of the Huli and Zhuanghe rivers in September. Meanwhile, relatively small numbers of birds were observed in the estuaries of the Yingna and Qingyun rivers as well as those of Haidao Village in all seasons (Figure 4).

The seasonal variation in the number of shorebird individuals was similar to that of the number of species present, with peaks occurring in spring and autumn, as would be expected of birds during migration. The populations of shorebirds were highest in the Huli River estuary, Huayuankou, and the Zhuanghe River estuary. A peak of 4600 birds was observed in the Huli River estuary in September, with the largest numbers of individuals seen for Dunlin, Eurasian curlew, Far Eastern curlew, and grey plover, listed from larger to smaller numbers. The number of individuals peaked at 2720 birds in Huayuankou in April, including many Dunlins and Eurasian curlews. The number of individuals peak at 1952 birds in the Zhuanghe River estuary in May, including many Far Eastern curlew, Eurasian curlew, and bar-tailed godwit (Figure 5).

The seasonal variation in biodiversity exhibited two peaks, occurring in May (1.81) and August (1.41), with relatively low biodiversity in the other months. From the perspective of spatial distribution, the biodiversity was relatively high in Huayuankou (1.43), the Zhuanghe River estuary (1.42), and the Diyan River estuary (1.42), and relatively low in the estuaries of the Qingyun and Yingna rivers. The biodiversity peaked in Dengsha River estuary in August (2.70), followed by the Zhuanghe River estuary in May (2.64), as shown in

Table 3. Spatiotemporal variation in the biodiversity of shorebirds in the coastal wetlands of Dalian.

Area	Haidao Village	Anzi River Estuary	Qingyun River Estuary	Dengsha River Estuary	Huayuankou	Zhuanghe River Estuary	Yingna River Estuary	Huli River Estuary	Diyan River Estuary	Mean
January	-	-	-	-	-	-	-	-	-	-
February	-	-	-	-	-	-	-	-	-	-
March	-	0	0	0	1.22	1.68	0	0	1.06	0.49
April	-	1.49	1.91	2.07	1.87	1.82	0	0	1.49	1.33
May	-	1.96	-	2.08	2.31	2.64	2.16	1.50	1.80	1.81
June	-	0.97	0	0	0.99	0.92	0	-	1.49	0.55
July	-	0.98	-	0	1.27	1.63	0	-	1.62	0.69
Augst	-	0.88	0	2.70	0.86	1.39	1.25	2.14	2.07	1.41
September	-	1.36	1.00	1.00	1.37	1.17	0	1.97	1.80	1.21
October	-	1.70	-	0.65	1.54	0.14	0	1.15	0	0.65
November	-	-	-	-	-	-	-	-	-	-
December	-	-	-	-	-	-	-	-	-	-
Mean	-	1.17	0.36	1.06	1.43	1.42	0.43	0.85	1.42

“-” denotes no effective value obtained.

.

2.4. Variations in Numbers of the Main Migratory Species

The main migratory shorebirds in the Dalian coastal region included Kentish plover, bar-tailed godwit, Eurasian curlew, Far Eastern curlew, and Dunlin, which accounted for 88% of the total number of birds observed. From March to October 2021, a total of 19,595 Dunlin individuals were observed in six areas including the estuaries of the Anzi and Dengsha rivers, Huayuankou, and the estuaries of the Zhuanghe, Yingna, Huli, and Diyan rivers, accounting for 34% of the total number of observed shorebirds. The largest numbers of individual shorebirds were observed in May, and the area with the largest number of individuals was the Zhuanghe River estuary. In August, the number of Eurasian curlews peaked at 7132 birds, accounting for 23% of the total number of shorebirds observed (Figure 6).

2.5. Status of Changes in Habitat

The present study documented surveys of habitat change that were primarily related to the following three aspects: road construction, urban construction, and agricultural use. The survey indices included road length and density along with the areas and spatial extent of residential zones, industrial and mining lands, tourism facilities, wind farms, farmlands, and aquaculture farms (

Table 4. Survey results of habitat changes.

Survey Indices			2010	2015	2020
Road construction	Road	Length	289,990	395,495	544,752
		Density	1.05	1.43	1.97
Urban construction	Residential zones	Area	13,591	14,068	14,544
		Percentage	4.92	5.10	5.26
	Industrial and mining lands	Area	4884	4882	5205
		Percentage	1.77	1.77	1.88
	Tourism facilities	Area	81	127	227
		Percentage	0.03	0.05	0.08
	Wind farms	Area	-	2117	2117
		Percentage	-	0.77	0.77
Agricultural exploitation	Farmlands	Area	5539	4505	4369
		Percentage	2.01	1.63	1.58
	Aquaculture farms	Area	43,126	43,813	44,986
		Percentage	15.63	15.87	16.28

(Notes: length is in m, density is in m/ha, and area is in ha).

). From 2010 to 2020, both the length and density of road networks at different levels exhibited gradually increasing trends, with road length increasing by 87.9% and road density increasing from 1.05 to 1.97. The increases in road length and density caused increased degrees of fragmentation of patches, patch types, and landscapes. The areas and spatial extent of residential zones, industrial and mining lands, and tourism facilities exhibited gradually increasing trends. The tourism facilities covered a relatively small area and had a maximum percentage of only 0.08%. From 2015 to 2020, a total of 28 wind-driven generators were observed in the wind farms of the survey areas; the quantity of wind-driven generators remained unchanged over time. Based on a 1 km area of impact radius for a single wind-driven generator, the wind-driven generators impacted 2117 ha, which remained unchanged within these five years. The percentage of farmland area decreased gradually, with a decrease of up to 21.1%; the farmlands were mainly transformed into forest lands, grasslands, and residential lands. Overall, the range and strength of anthropogenic perturbations increased gradually, and the impact of anthropogenic threats on habitats became stronger and stronger. The variation in the habitats would inevitably have an important impact on the behavior of the waterbirds, including effects on migration, reproduction, and wintering.

2.6. Relationship between Habitat Status and Waterbird Populations

The landscape patterns of habitat can be divided into spatial and spatiotemporal patterns, which are crucial to understanding the impact of fragmentation on biodiversity [37]. Spatial pattern analysis is helpful in understanding the distribution of biodiversity and its relationship with habitat characteristics. By analyzing spatial and temporal patterns, we can reveal the specific mechanism of the fragmentation process on biodiversity, including changes in species richness, population dynamics, and community structure. In general, no correlation was found between the area of natural wetlands and species richness (Figure 7), and no correlation was found between the total landscape area of habitats and species richness (Figure 8). The species–area relationship of bird communities is not purely linear, and a small island effect may be present [38].

3. Discussion

3.1. Community Characteristics

The city of Dalian has rich coastal wetland resources, which provide important stopover sites for shorebirds along the Northeast Asian Flyway. In this survey, 31 species of shorebirds were found in Dalian, with the species of the family Scolopacidae being the most frequently observed. Compared with the survey results obtained in 1987 [39], six of those species were not observed in the present study, including lapwing (Vanellus vanellus), little curlew (Numenius minutus), far eastern curlew, green sandpiper, pintail snipe (Gallinago stenura), and woodcock (Scolopax rusticola). In contrast, the present study observed eight species in this region that were not found in the 1987 survey mentioned above, including Eurasian oystercatcher, black-winged stilt, avocet, redshank, greenshank, great knot, red knot, and broad-billed sandpiper. The species composition of shorebirds in the coastal wetlands of Dalian has changed over 30 years.

The structure of the shorebird community is closely related to the availability of suitable habitats for shorebirds, with different environments showing different species compositions [40]. The species composition of shorebirds in the Dalian coastal areas is basically similar to that of shorebirds in Tianjin and Qinghai Lake, which lie at the same latitude as Dalian [22]. However, the main migratory shorebirds in Qinghai Lake are redshank, Kentish plover, black-tailed godwit, Temminck’s stint (Calidris temminckii), Mongolian plover, pratincole, and avocet, which are different from those in Dalian and Tianjin (Kentish plover, bar-tailed godwit, Eurasian curlew, Far Eastern curlew, and Dunlin) [41,42], with the numbers of individuals of various species differing greatly. This may be related to the adverse climate and scarce food resources for shorebirds in winter at Qinghai Lake. In addition, Dalian and Tianjin serve as hubs of the Northeast Asian Flyway, unlike Qinghai Lake, which is located on the inland Chinese–Indian Flyway, with respect to the selectivity of migration.

The species composition of shorebirds in Dalian is generally similar to that of shorebirds in other coastal areas such as the coastal areas of Zhejiang and Fujian provinces [43], the Yangtze River estuary [44], and Yancheng City in Jiangsu Province [45]. This is related to the fact that both the coastal wetlands of Dalian and the above-mentioned coastal areas are located along the Australian–Siberian Flyway. However, slight differences are known in the dominant migratory species, with the largest difference embodied by the number of individuals observed. For example, hundreds of bird species pass through the Yangtze River estuary in the spring and autumn migratory seasons [26].

3.2. Spatiotemporal Distribution of and Habitat Selection by Shorebirds

All shorebirds in the Dalian region are seasonal migrants or summer residents. The variation in the number of species present exhibits obvious seasonal characteristics, with shorebirds mainly concentrated in the spring, summer, and autumn seasons. This is related to the climatic conditions in the Dalian region. In January in Dalian, the mean daily temperature is −4.8 °C [46]; icing occurs in the water systems of the coastal wetlands and in the nearshore sea areas, so shorebirds are unable to feed on the benthos in intertidal zones [47].

The Dalian coastal wetlands host significant numbers of species of shorebirds, primarily concentrated in the following four areas: Huayuankou and the estuaries of the Diyan, Zhuanghe, and Huli rivers (Figure 3, Figure 4 and Figure 5); this is mainly related to the quality of shorebird habitats. All these areas are river estuaries with large expanses of mudflats, which provide wide foraging space and rich food resources for shorebirds after ebb tide and are relatively ideal feeding and perching places for shorebirds [48]. Moreover, the Dengsha River estuary has relatively high biodiversity, especially in two migration seasons, i.e., spring and autumn, which is related to complex habitats and landscapes. Not only does the Dengsha River estuary feature downstream mudflats, but it also has rich natural marshes and artificial aquaculture ponds along both banks of the upstream watercourse. These varied habitats are suitable for use by a diverse array of shorebirds. The diversity of habitats also results in a diverse array of species; for example, species such as Pacific golden plover and spotted redshank were found in this area.

The area of natural wetland exhibits positive correlations with both the number of species and the abundance of shorebirds; the habitats scattered across the entire landscape exhibit a positive correlation with species richness, indicating that the percent cover of natural wetland exhibits a positive correlation with the richness of shorebirds [15,16,49]. The type of habitat and the coverage of natural wetlands are the main variables influencing the spatial distribution of waterbirds. A larger wetland area usually provides more food and has higher habitat stability and connectivity, which can better meet the habitat needs of migratory shorebirds and support more migratory shorebird species [40]. However, the total landscape area of habitats exhibited no significant correlation with the numbers of individual bird species. Some research has shown that when the coverage of wetlands is >70%, this has a negative effect on waterbird communities. Waterbirds that are highly sensitive to the spatial characteristics of habitats select habitats with concentrated patches and strong connectivity, while species with low spatial sensitivity select habitats with fragmented patches and diverse habitat types [50]. From another perspective, the diversity, abundance, and interactions within bird communities, as well as their ability to adapt to changes in the environment, are all clear indicators of the quality of the local habitat. These bird communities reflect the overall health and stability of the ecosystem, providing valuable insights for conservation efforts.

3.3. Migration Characteristics

The migration of shorebirds in the coastal wetlands of Dalian is primarily concentrated in spring and autumn, which is basically synchronized with the migration time in other areas of the Yellow and Bohai seas [25]. The northward migration in spring starts in March and peaks in May. The number of species and the abundance of shorebirds decreases sharply in June and rises again in July–August. After the number of shorebirds migrating southward peaks in autumn (September), the number of species and the abundance of shorebirds start to decrease in October, while southward migration is completed in November. With respect to the variations in migratory patterns, the number of species of shorebirds migrating north is higher than that of those migrating south (Figure 2), but the number of individuals migrating south in autumn is larger than those migrating north in spring (Figure 3). With respect to the main migratory species, the Kentish plover was found to be more abundant during southward migration in autumn than in spring, while the bar-tailed godwit exhibited a reverse phenomenon (Figure 4). This may be related to the fact that a large number of subadult birds born in a given year join in the birds migrating south, while some of the birds migrating sound are long-distance migrants that can fly across this area without stopping and directly reach their destinations [51].

Humans have impacted the coastal areas of Dalian quite extensively. The habitats for shorebirds in this region adjoin multiple important development zones, such as the Dalian Changxing Island Lingang Industrial Zone, the Puwan New Zone, the Dalian Economic and Technological Development Zone, and the Huayuankou Economic Zone. The increasing impacts on coastal wetland resources have led to a significant reduction in the size and quality of shorebird habitats and related food resources [52]. The migration of shorebirds is a systematic process, and any change in any link may greatly impact their migration activity. Therefore, it is necessary to review and analyze the intensive use of coastal wetland resources, consider the need to protect these areas, and restore and maintain the important function of Dalian as a part of the East Asian–Australasian Flyway, ensuring the normal migration of shorebirds.

3.4. Habitat Characteristics

The status of avian habitats influences the distribution, abundance, and diversity of birds in an area [53], and the conditions of habitats and surrounding areas have significant impacts on the selection of habitats by birds [54]. On the whole, the coastal wetlands of Dalian are characterized by complex types and structures, fragmented landscape patterns, and a complex pattern of transformation among landscape types. Figure 7 and Figure 8 show that no correlation was found between the number of individuals of shorebird species and landscape patches. One occurred because of the small sample size and because each estuarine area had complex ecological types that varied greatly from one area to another. In fragmented habitats, small patches and anthropogenic green spaces play the role of providing “transit stations” or “stepping stones” in bird activities, which may lead to an increase in bird species richness in some small patches, weaken the area effect, and result in the small island effect [55,56]. This was especially true in the Yingna River estuary mainly because the large number of reeds created a type of habitat that is unsuitable for most shorebirds; as a result, the shorebirds are unable to live and feed on the mudflats. Habitats with high heterogeneity generally have high biodiversity [57]. In the study of bird density and individual species, it was found that the high landscape and biological diversity of habitats resulted in a relatively high density and abundance of bird communities. Compared with a core area of a habitat, edge habitats can create more diverse avian habitats that attract more bird species [58]. The main factor that attracts these waterbirds is the high structural heterogeneity in these artificial wetlands (such as fish ponds and crab ponds), which have abundant aquatic plants and varying depths of water, making them favored by birds because of the diverse habitat types [59,60]. Considering the diverse ecosystem of bird habitats in Dalian coastal wetlands, it is necessary to reduce or even avoid further fragmentation of habitat patches in order to maintain or even increase patch connectivity in the region [61].

However, recent urbanization along with related social and economic development have combined with the following natural factors such as coast erosion to threaten the diversity of shorebirds in Dalian [62]. (1) Global warming has strongly impacted the stability and ecological functions of wetlands, while sea level rise is leading to a retreat of coastal wetlands toward inland areas [63,64]. The shrinkage of coastal wetlands has had a devastating impact on migratory birds that rely on them for survival, reproduction, and wintering. (2) Reclamation and aquaculture in coastal zones are important anthropogenic factors causing wetland loss and degradation [65,66]. Various large-scale embankment and pond creation activities have directly led to significant losses of natural coastal wetlands. Furthermore, even the areas of coastal wetland zones that have not undergone reclamation and aquaculture are also adversely affected by production activities in nearby reclamation and aquaculture areas. Excessive reclamation fragments waterbird habitats, ultimately resulting in a loss of biodiversity. (3) The implementation of coastal works such as port facilities, embankment structures, and cross-sea passages will significantly impact natural coastal wetlands by changing various aspects of the landscape including changes in sedimentation characteristics, landforms, hydrological dynamics, and ecological structure. This leads to a series of problems, including a decrease in the area of natural wetlands, habitat fragmentation, environmental degradation, resource overloading, and species invasion, all of which have contributed to the loss of habitats and alterations in migration routes for birds. (4) The construction of wind farms will result in the loss of habitats for animals; meanwhile, collisions with wind turbines may create more serious hazards by causing the injury and death of birds. The construction and operation of wind farms will undoubtedly have a certain impact on the habitats, flight patterns, and migration of birds. Leddy et al. pointed out that wind turbines and related equipment on wind farms will influence the selection of habitats by birds [66]. The population density of birds in grasslands without wind turbines or located at least 80 m from wind turbines was significantly higher than that in areas with wind farms.