Community structure, abundance variation and population trends of waterbirds in relation to water level fluctuation in Poyang Lake

JGLR-01505; No. of pages: 10; 4C: Journal of Great Lakes Research xxx (xxxx) xxx

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Community structure, abundance variation and population trends of waterbirds in relation to water level fluctuation in Poyang Lake Yankuo Li a,⁎, Fawen Qian b, Janet Silbernagel c, Hannah Larson c a b c

College of Life Sciences, Jiangxi Normal University, Nanchang 330022, China Key Laboratory of Forest Ecology and Environment of State Forestry Administration Institute of Forestry Ecology, Environment and Protection, CAF, Beijing 100091, China Nelson Institute for Environmental Studies, University of Wisconsin-Madison, 550 N. Park St., Madison, WI 53706, USA

a r t i c l e

i n f o

Article history: Received 29 November 2018 Accepted 18 July 2019 Available online xxxx Communicated by Craig Hebert Keywords: Community structure Waterbird abundance Population trend Water level fluctuation Poyang Lake

a b s t r a c t Poyang Lake is China's largest freshwater lake, and it has been an internationally important wintering ground for migratory waterbirds. Based on waterbird censuses from 2001 to 2016, community structure and abundance trends of waterbirds were analyzed, as well as the potential correlations with the water level of Poyang Lake. The results showed that the annual average number of waterbirds in Poyang Lake was 426,707 ± 150,170, with 111 species from 17 families. Waterfowl was the most abundant family accounting for 74.4 ± 8.8% of all individuals, followed by shorebirds (14.8 ± 8.5%), wading birds (6.5 ± 1.8%) and open-water/waterbirds (4.4 ± 1.9%). Although waterbird abundance fluctuated dramatically, there were no significant trends in the abundance of most guilds or in total waterbird abundance; only geese significantly increased among the eight groups. Analysis of trends of 37 relatively abundant or regularly occurring species indicated that population trends appeared to be species-specific. As for the correlations between water level and waterbird abundance, only shorebirds showed significant correlations with average July water level, average water level, and high water level duration in wet season among four guilds, i.e. waterfowl, wading bird, shorebird and, open-water and waterbird. At the group level, abundances of swans, geese, and ducks were significantly correlated with monthly average water level during the wet season, and wader abundance was significantly correlated with average water levels and high water level duration during the wet season. Correlations between population abundance and monthly water level also exhibited species-specific patterns. © 2019 Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.

Introduction As a natural resource of global significance, wetland ecosystems have been widely recognized as playing a key role in supporting global biodiversity by providing vital habitat for numerous wildlife species (Balian et al., 2008). However, wetlands across the world have generally been subjected to major alterations to their natural status by human activities over the last century (Gardner et al., 2015). Habitat loss and degradation driven by land use change have pushed approximately 30% of freshwater species to the verge of extinction around the world (Collen et al., 2014). Likewise, China's wetlands have also undergone rapid loss and degradation from the late 20th century up until recent years (He and Zhang, 2001; Niu et al., 2012). Although climatic factors are important reasons for wetland change, human activities, such as reclamation, agriculture, urban sprawl, road construction, drainage, diking and damming, eutrophication, and pollution, have been recognized as the key drivers of China's wetland loss (An et al., 2007; Zhang et al., 2010). In recent years, the impact of human activities on wetland ⁎ Corresponding author. E-mail address: [email protected] (Y. Li).

ecosystems has been increasingly important as hydrological regimes are even more profoundly modified, especially through the operation or construction of large dams (Zhang et al., 2012). Poyang Lake is the largest freshwater lake in China, playing a crucial role in flood control and reduction for the middle and lower Yangtze River. Known for its extraordinary biodiversity, the Poyang Lake wetland is also one of the largest overwintering grounds for migratory birds in the world. An estimated 352 bird species inhabit Poyang Lake, with 16 of these species listed as threatened in the International Union for Conservation of Nature (IUCN) Red List of Threatened species. Poyang Lake is home to 99% of the world's critically endangered Siberian cranes (Leucogeranus leucogeranus) and over 95% of endangered oriental white storks (Ciconia boyciana) (Huang et al., 2016; Ji et al., 2007). A major reason for Poyang Lake's high biodiversity is its dramatic water level variations over both short-term (weeks to months) and longterm (years) periods, resulting in a remarkable lake size change from approximately 3000 km2 during the wet season to b500 km2 in winter, i.e., the dry season (Andreoli et al., 2007). The significant seasonality and inter-annual fluctuations in water levels create extensive wetland complexity in the Poyang Lake, which provides vital wintering habitats for hundreds of thousands of migratory birds (Liu et al., 2011).

https://doi.org/10.1016/j.jglr.2019.08.002 0380-1330/© 2019 Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.

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However, it is well understood that Poyang Lake water levels and area have been declining significantly over the last decade (Feng et al., 2012; Liu et al., 2013). Poyang Lake experienced its most severe drought in the 2000s (Li et al., 2016). The increasing area of grassland and consequent prairie-like landscape raised public awareness about the fact that the dry season of Poyang Lake was getting much longer and earlier. Researchers have shown that alterations to the Yangtze River flows from the Three Gorges Dam play a vital role in causing the seasonal dryness of Poyang Lake (Li and Zhang, 2015). In recent years, with an evergrowing body of literature detailing the effects on the hydrologic regime of Poyang Lake from the Three Gorges Dam, increasing attention is also being paid to its potential effect on migratory waterbirds (Jia et al., 2013; Mei et al., 2015). This subject has been given greater urgency because of a proposed dam for maintaining water levels in Poyang Lake, resulting in concern over the dam's potentially disastrous effects on the wetland ecosystem and migratory birds (Jiao, 2009). Undoubtedly, improving our knowledge about the effects of water level fluctuations on migratory bird communities is critical to understanding the role of human water control in structuring bird communities in Poyang Lake. However, the lack of long-term temporal data and broad spatial coverage impedes the understanding of the relationship between water level fluctuation and migratory bird community dynamics. Until now, long-term trends of migratory bird populations in the whole of Poyang Lake have not been available nor correlations between water level fluctuation and migratory bird abundance. In this study, the characteristics of waterbird communities, variations of waterbird abundance, population trends, and water level fluctuations were analyzed in Poyang Lake. The main objectives were to: (1) understand the community structure of wintering waterbirds in Poyang Lake; (2) estimate waterbird abundance change and population dynamics in the Poyang Lake wetland from 2001 to 2016 and examine whether there are significant trends in waterbird abundance and population size of dominant, rare or endangered species; and (3) analyze the correlations between bird abundance variation, population dynamics, and water level fluctuations of Poyang Lake as well as the implications of the results for waterbird conservation and ecological assessment of the proposed dam construction at Poyang Lake.

level usually between 10 and 16 m above msl and, a lowest recorded level of 5.90 m above msl in 1963 (Shankman et al., 2009). These seasonal water level dynamics in Poyang Lake have fostered abundant species diversity, developed diverse bottomland and lakeshore wetland vegetation, and formed a complex wetland landscape in flux. Poyang Lake was identified as a Ramsar wetland site in 1996. Every year, N500,000 waterbirds winter at Poyang Lake (Zhu et al., 2012). Eighteen nature reserves have been established to protect the wetland ecology, wildlife, and fish, covering an area of 2,006 km2. However, migratory birds still face increasing threats resulting from wetland loss, habitat degradation, poaching, and an intensive fishery (Huang et al., 2016). Bird census A wintering waterbird census was conducted once a year across the entire Poyang Lake wetland from 2001 to 2016 (Fig. 1). Under the guidance of ornithologists, this waterbird monitoring project was organized by the Wildlife Service of Jiangxi Province beginning in 1998. Bird census data before 2001 were not included in our study and were treated instead as preliminary studies. The study area covered the vast majority of lakes potentially used by waterbirds in 13 counties. All surveys adopted a synchronous survey counting method to avoid repeating or omitting counts because of the frequent movement of waterbirds (Wei et al., 2016). The middle of the winter was preferred for surveys because the waterbird community is most stable during this period; thus, surveys were conducted in December, January, or early February in most years. Bird species identification and counts were performed by investigators whenever they encountered waterbirds along transects at designated areas. The research teams were composed of ornithologists, local wildlife service staff, nature reserve technicians, and birdwatching volunteers using binoculars and telescopes. A total count method was used to estimate the numbers of waterbirds assembling in small flocks. We used a “group counting method” to count waterbirds in larger colonies, namely, we estimated bird numbers by counting groups and multiplied the number of groups by the average number of birds in one group (Howes, 1989; Qian et al., 2009). If some sites were not accessible by foot, boats were used. Statistical analyses

Materials and methods Study area Poyang Lake is located in the middle and lower reaches of the Yangtze River, in the northern part of Jiangxi Province, China (115°49′ to 116°36′E, 28°11′ to 29°51′N, see Fig. 1), with a total watershed area of 162,000 km2. The length of the lake is approximately 173 km from south to north and its maximum width is 74 km from east to west, with an average width of 16.9 km. Poyang Lake's primary water sources are from five major tributaries: the Ganjiang River, Xiuhe River, Fuhe River, Xinjiang River, and Raohe River. The lake's water typically discharges into the Yangtze River from its northern part, but sometimes there is a reverse flow resulting from elevated water levels in the Yangtze River. The Poyang Lake region has a subtropical wet climate characterized by mean annual precipitation of 1,680 mm and an annual average temperature of 17.5 °C. Precipitation shows marked seasonal fluctuations and can be divided into a wet season (April–September) and a dry season (October–March) (Wang, 2004). Accordingly, there is a dramatic seasonal change in water level and water surface area. In the wet season, the lake's highest water level generally ranges from approximately 18 to 21 m above mean sea level (msl), with a highest recorded level of 22.59 m above msl in 1998; the floodplains are inundated during this period, forming a large lake of over 3,000 km2 (Shankman et al., 2009). In the dry season, the lake shrinks to b1,000 km2 and forms a narrow meandering channel, with a water

We assessed temporal trends in waterbird abundance for 37 regularly occurring species as well as bird groups (goose, swan, duck, crane, wader, gull, spoonbill, and others; see Electronic Supplementary Material (ESM) Table S1). For each species and group, trends in abundance from 2001 to 2016 were examined by least squares curve fits and smoothing curve fits (Bolduc and Afton, 2008). The census data from winter 2009 were not included in our study because this census was conducted in late winter. Additionally, we classified all waterbird species into four guilds based on feeding niche, habitat preference, and taxonomy: (1) waterfowl, including Anatidae; (2) wading birds, including cranes, storks, herons, egrets, bitterns, and Rallidae species; (3) shorebirds, including waders of Recurvirostridae, Scolopacidae, Charadriidae, and Jacanidae; and (4) open-water and waterbirds, including gulls, grebes, kingfishers, cormorants, and pelicans. We used a curve smoothing approach to assess population size change patterns and then applied curvilinear regression to test whether there were significant trends. Daily water level was collected by the Hydrology Bureau of Jiangxi Province at the Wucheng hydrology station. A general linear modeling method was used to examine relationships between water level and waterbird abundance and population size. The hydrology parameters involved in the correlation analyses included monthly average water level, average water levels in wet season and dry season, and flood duration (i.e., days of high water level N17 m and N18 m) which can affect wetland biomass. Statistical results were determined using P b 0.05. General linear modeling was conducted using SPSS 18.0 (SPSS

Please cite this article as: Y. Li, F. Qian, J. Silbernagel, et al., Community structure, abundance variation and population trends of waterbirds in relation to water le..., Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2019.08.002

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Fig. 1. Map showing the study area, Poyang Lake. The symbols show the waterbird monitoring locations where waterbird censuses were conducted from 2001 to 2016. The black grid area was covered by rice fields.

Inc., 2009); curvilinear regression and graphic plots were done using R 3.5.0 (R Core Team, 2013). Results Community structure and waterbird abundance We recorded 6,400,607 individuals from 111 species of waterbirds from 17 families during the 15 years from 2001 to 2016 (ESM Table S1). The annual average number of waterbirds was 426,707 ± 150,170, with a maximum of 725,760 in 2005 and a minimum of 264,859 in 2012. The waterbird community was dominated by waterfowl, which comprised 74.4% of the individuals and 29.7% of the species (Table 1). Shorebirds had the second-highest number of individuals (14.8%) and species (28.8%), followed by wading birds, which represented 6.5% of individuals and 25.2% of species. The open-water and waterbird guild contained the fewest species (16.2%) and individuals (4.4%).

Waterfowl This group included Anatidae. Swans, geese, and ducks comprised 15.6 ± 5.5%, 41.1 ± 13.4%, and 17.6 ± 7.4% of all individuals, respectively. Swan goose (Anser cygnoides), bean goose (A. fabalis), greylag goose (A. anser), greater white-fronted goose (A. albifrons), and lesser white-fronted goose (A. erythropus) were dominant species, while the other five goose species occurred infrequently or only several individuals were recorded (Table 2, ESM Table S1). Twenty-two duck species were detected, including ten diving ducks species of the genus Aythya, Mergellus, and Mergus, and twelve dabbling duck species of Anas, Tadorna, Nettapus, and Aix (ESM Table S1). Dabbling ducks constituted the majority of overall duck abundance, on average accounting for 97.4% of the identified ducks. The most abundant duck species were spot-billed duck (Anas zonorhyncha) and common teal (A. crecca), followed by mallard (A. platyrhynchos), Eurasian wigeon (A. penelope), ruddy shelduck (Tadorna ferruginea), northern pintail (A. acuta), and falcated duck (A. falcata), in descending order (Table 2). In contrast,

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most diving ducks occurred infrequently. Baer's pochard (Aythya baeri), tufted duck (A. fuligula), and northern pochard (A. ferina) were relatively abundant diving duck species and were frequently recorded, but had smaller populations, with an average number of 325, 218, 510, respectively. Given their diving habit for feeding, mergansers were classified as diving ducks. Three merganser species occurred in Poyang Lake. The common merganser had a small, stable population, with an annual average of 63 individuals. The scaly-sided merganser (Mergus squamatus) and smew (Mergellus albellus) occurred occasionally, having been observed twice and four times in our study period, respectively, with b20 individuals recorded. Wading birds We recorded 388,695 wading birds composed of cranes (four species), storks (two species), herons (eleven species), spoonbills (two species), crakes (eight species), and bustard (one species). Crane and spoonbill abundance represented 2.1% and 1.9% of all waterbirds, respectively. Grey heron (Ardea cinerea) was the most abundant species (5232 ± 2283) in this guild; the second most abundant was Eurasian spoonbill (Platalea leucorodia) (5137 ± 2620), followed by common crane (Grus grus) (3117 ± 3289), Siberian crane (3150 ± 788), and oriental white stork (2882 ± 1297) (Table 2). Among the four crane species, the abundance of hooded crane (Grus monacha) (362 ± 181) and white-naped crane (Grus vipio) (1499 ± 988) was clearly less than that of Siberian cranes and common cranes. Compared with closely allied species in this area, black stork (Ciconia nigra), great egret (Ardea alba), and intermediate egret (Egretta intermedia) had small populations. Other species in this guild were all recorded occasionally with few individuals, especially the great bustard (Otis tarda), for which only one individual was detected, in 2005. Shorebirds We recorded 32 species in this guild, which was dominated by a small number of species; most species occurred infrequently or were not abundant. The top seven shorebirds by abundance were pied avocet (Recurvirostra avosetta), spotted redshank (Tringa erythropus), dunlin (Calidris alpina), black-tailed godwit (Limosa limosa), northern lapwing (Vanellus vanellus), common greenshank (Tringa nebularia), and common redshank (T. totanus), which collectively accounted for 96.2 ± 6.8% of all identified shorebirds. Five species were rarely recorded: Swinhoe's snipe (Capella megala), lesser sandplover (Charadrius mongolus), long-billed plover (C. placidus), Temminck's stint (Calidris temminckii), sanderling (Crocethia alba), greater painted-snipe (Rostratula benghalensis), Eurasian woodcock (Scolopax rusticola), and Nordmann's greenshank (Tringa guttifer). Open-water and waterbirds We grouped 18 species, including gulls (eight species), terns (three species), cormorants (one species), grebes (two species), kingfishers (three species), and pelicans (one species), into the open-water and waterbird guild. However, 93.5 ± 15.1% of individuals in this guild consisted of six species: black-headed gull (Larus ridibundus), European herring gull (L. argentatus), little grebe (Tachybaptus ruficollis), great cormorant (Phalacrocorax carbo), Eurasian coot (Fulica atra), and great crested grebe (Podiceps cristatus). Other gull species as well as terns were rare. The three kingfisher species were all resident species and contained the fewest individuals in this guild.

Waterbird abundance trends Total waterbird abundance showed no evident trend but annual abundance fluctuated dramatically, ranging from 264,589 to 725,760 individuals. Of the four guilds, only waterfowl, open-water and waterbirds had positive trends, but these were not statistically significant. Of the 111 waterbird species, only relatively abundant and regularly occurring species were examined for abundance trends. Population trends during the 2001–2016 period were species-specific. For the wading bird guild, significant increases were found in common crane (R2 = 0.35, F = 7.43, P = 0.016) and oriental white stork (R2 = 0.27, F = 4.72, P = 0.049), while other crane species showed negative trends in abundance (Fig. 2). White-naped cranes decreased significantly (R2 = 0.47, F = 11.65, P = 0.005), and the decreasing trend of Siberian cranes was weakly significant (R2 = 0.26, F = 4.64, P = 0.051). Of the remaining species, grey herons also showed a significant decreasing trend (R2 = 0.29, F = 5.24, P = 0.039). As for waterfowl, abundance of Anatidae showed no significant trends, but goose abundance showed a significant linear increase (R2 = 0.27, F = 4.70, P = 0.049), which was mainly due to increases in bean goose and swan goose (Fig. 3). Swan goose abundance during 2010–2016 was significantly larger than that in 2001–2008 (F = 6.15, df = 13, P = 0.028), and bean goose showed a significant exponential increase (R2 = 0.65, F = 27. 60, P = 0.000). There was no significant trend in abundance of dabbling ducks, diving ducks, or ducks overall, but significant short-term increases were found for both dabbling ducks (R 2 = 0.76, F = 15.45, P = 0.011) and diving ducks (R 2 = 0.79, F = 18.60, P = 0.008) from 2001 to 2007, followed by different trends (Fig. 3). As for specific species, significantly negative trends were found for gadwall (R2 = 0.37, F = 6.95, P = 0.022) and northern pintail (R2 = 0.34, F = 6.55, P = 0.024), while a positive trend occurred for spot-billed duck abundance (R2 = 0.44, F = 10.21, P = 0.007). Eurasian wigeon significantly decreased after 2008 (F = 15.03, df = 13, P = 0.014), and the average number of individuals during the 2001–2008 period was eight times that of during 2010–2016. For shorebirds, open-water and waterbirds, only three species presented significant trends: common redshank significantly decreased (R2 = 0.33, F = 6.38, P = 0.025); little grebe (R2 = 0.27, F = 5.24, P = 0.038) and crested grebe (R2 = 0.69, F = 18.53, P = 0.001) significantly increased. Correlations between water level and waterbird abundance Average monthly water level Abundance of total waterbirds, wading birds, waterfowl, and openwater birds was not correlated with monthly average water level (above msl) of Poyang Lake. However, there was a significant negative correlation between shorebird abundance (ln-transformed) and average water level in July (R2 = 0.30, F = 5.50, P = 0.036). Among seven waterbird groups, swan abundance was negatively correlated with August average water level (R2 = 0.30, F = 5.43, P = 0.037) and goose abundance (ln-transformed) was positively correlated with June water level (R2 = 0.27, F = 4.80, P = 0.047) (Fig. 4). Total duck abundance was significantly negatively correlated with average water level of May (R2 = 0.37, F = 7.67, P = 0.016), June (R2 = 0.29, F = 5.22, P = 0.040), and July (R2 = 0.41, F = 9.10, P = 0.010) because of the negative correlation of dabbling duck abundance with monthly water level in

Table 1 Number of species and total number of waterbirds recorded in Poyang Lake wetland, based on land surveys between 2001 and 2016. Guild Wading bird Waterfowl Shorebird Open-water and waterbird

# Species

% Total species

28 33 32 18

25.2 29.7 28.8 16.2

Totals

% Total

25,912 ± 6,767 315,359 ± 110,260 67,401 ± 62,775 18,035 ± 8,459

6.5 ± 1.8 74.4 ± 8.8 14.8 ± 8.5 4.4 ± 1.9

Please cite this article as: Y. Li, F. Qian, J. Silbernagel, et al., Community structure, abundance variation and population trends of waterbirds in relation to water le..., Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2019.08.002

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Table 2 Relative abundance of numerous or regularly occurring species in Poyang Lake, including relative percentage (Rel.%) of each species compared to guilds (Rel.%-G) and total abundance (Rel. %-T). Guild

Waterfowl

Wading birds

Shorebirds

Open-water and waterbirds

Species

Mean ± SD

Rel.%-G

Rel.%-T

Tundra swan (Cygnus columbianus) Swan goose (Anser cygnoides) Bean goose (Anser fabalis) Greylag goose (Anser anser) Greater white-fronted goose (Anser albifrons) Lesser white-fronted goose (Anser erythropus) Ruddy shelduck (Tadorna ferruginea) Spot-billed duck (Anas poecilorhyncha) Eurasian wigeon (Anas penelope) Mallard (Anas platyrhynchos) Common teal (Anas crecca) Northern pintail (Anas acuta) Falcated duck (Mareca falcata) Gadwall (Mareca strepera) Siberian crane (Leucogeranus leucogeranus) Hooded crane (Grus monacha) White-naped crane (Grus vipio) Common crane (Grus grus) Oriental white stork (Ciconia boyciana) Eurasian spoonbill (Platalea leucorodia) Grey heron (Ardea cinerea) Little egret (Egretta garzetta) Great egret (Ardea alba) Intermediate egret (Ardea intermedia) Common moorhen (Gallinula chloropus) Pied avocet (Recurvirostra avosetta) Spotted redshank (Tringa erythropus) Dunlin (Calidris alpina) Black-tailed godwit (Limosa limosa) Northern lapwing (Vanellus vanellus) Common greenshank (Tringa nebularia) Common redshank (Tringa totanus) Black-headed gull (Larus ridibundus) European herring gull (Larus argentatus) Little grebe (Tachybaptus ruficollis) Great cormorant (Phalacrocorax carbo) Great crested grebe (Podiceps cristatus). Eurasian coot (Fulica atra)

66,393 ± 30,065 85,098 ± 42,515 39,590 ± 32,159 4923 ± 3776

21.0 ± 7.3 26.1 ± 6.5 11.9 ± 7.5 1.6 ± 1.4

15.6 ± 5.5 19.7 ± 6.0 9.2 ± 6.3 1.1 ± 0.8

31,630 ± 18,808

10.4 ± 5.8

7.7 ± 4.6

1302 ± 1602 4182 ± 2131 12,825 ± 882 4033 ± 5046 7244 ± 5043 12,476 ± 13,010 3726 ± 3270 3124 ± 3105 1642 ± 2147 3150 ± 788 362 ± 181 1499 ± 988 3117 ± 3289 2882 ± 1297 5137 ± 2620 5232 ± 2283 1321 ± 746 170 ± 218 93 ± 123 606 ± 1076 17,258 ± 14,484 17,020 ± 14,008 10,768 ± 25,406 3938 ± 4852 1864 ± 1717 1331 ± 1271 542 ± 720 7766 ± 8761 2912 ± 3,132 2314 ± 984 3396 ± 3449 667 ± 677 1808 ± 2315

0.4 ± 0.4 1.4 ± 0.6 4.0 ± 2.3 1.6 ± 2.1 2.5 ± 1.8 4.3 ± 4.1 1.4 ± 1.6 1.0 ± 1.1 0.5 ± 0.6 13.9 ± 4.2 1.6 ± 0.8 6.6 ± 4.5 12.4 ± 10.9 12.3 ± 5.2 21.7 ± 9.4 23.1 ± 10.3 5.6 ± 2.7 0.8 ± 1.1 0.4 ± 0.6 0.2 ± 0.3 29.0 ± 20.1 23.8 ± 17.7 6.5 ± 9.1 9.5 ± 14.9 2.9 ± 1.9 2.7 ± 2.6 1.3 ± 2.2 34.2 ± 24.5 18.1 ± 16.3 24.2 ± 21.3 18.1 ± 16.3 34.2 ± 24.5 3.6 ± 3.4

0.3 ± 0.3 1.0 ± 0.5 3.0 ± 1.8 1.1 ± 1.5 1.9 ± 1.4 3.0 ± 2.9 1.0 ± 1.1 0.7 ± 0.8 0.4 ± 0.5 0.8 ± 0.3 0.1 ± 0.1 0.4 ± 0.3 0.8 ± 0.9 0.7 ± 0.3 1.3 ± 0.6 1.4 ± 0.8 0.3 ± 0.2 0.04 ± 0.07 0.01 ± 0.04 0.1 ± 0.2 3.9 ± 3.9 3.3 ± 2.9 1.5 ± 3.2 1.1 ± 1.7 0.4 ± 0.3 0.3 ± 0.3 0.1 ± 0.2 1.6 ± 1.4 0.8 ± 0.9 1.0 ± 1.1 0.8 ± 0.9 1.6 ± 1.4 0.1 ± 0.1

general (February: R2 = 0.37, F = 7.71, P = 0.016; April: R2 = 0.36, F = 7.15, P = 0.019; May: R2 = 0.61, F = 20.60, P = 0.001; June: R2 = 0.34, F = 6.79, P = 0.022; and December: R2 = 0.34, F = 6.60, P = 0.023), while diving duck abundance contributed little. None of the abundances of waders, cranes, gulls or spoonbills were significantly correlated with monthly water levels. Correlations between population abundance and monthly water levels were species-specific. Among Anatidae, ruddy shelduck (ln-transformed) was significantly negatively correlated with average March water level (R2 = 0.34, F = 6.60, P = 0.023), and the same was true for Eurasian wigeon with average May water level (R2 = 0.26, F = 4.64, P = 0.051); common teal was significantly negatively correlated with water levels in April (R2 = 0.34, F = 6.56, P = 0.024), May (R2 = 0.45, F = 10.68, P = 0.006). For wading birds, only little egret (Egretta garzetta) was significantly positively correlated with monthly water level, specifically January (R2 = 0.48, F = 12.15, P = 0.004) and March (R2 = 0.41, F = 9.11, P = 0.010). Among shorebirds, blacktailed godwit was positively correlated with average water level in August (R2 = 0.35, F = 6.31, P = 0.027); spotted redshank showed a weakly significant negative correlation with water level in July (R2 = 0.29, F = 4.57, P = 0.056), while northern lapwing (ln-transformed) was significantly negatively correlated with water level in November (R2 = 0.30, F = 5.43, P = 0.037) and December (R2 = 0.28, F = 5.09, P = 0.042). Water level in wet and dry season Of the four guilds, only shorebirds showed significant negative correlations with average water level (R2 = 0.36, F = 6.67, P = 0.024),

high water level (N18 m) duration (R2 = 0.40, F = 8.07, P = 0.015), and high water level (N17 m) duration (R2 = 0.53, F = 13.74, P = 0.003) during the wet season. As for eight groups of waterbirds, only waders presented significant negative correlations with water levels during the wet season including average water level (R2 = 0.37, F = 6.94, P = 0.022), high water level (N18 m) duration (R2 = 0.40, F = 8.11, P = 0.015), and high water level (N17 m) duration (R2 = 0.54, F = 14.25, P = 0.003) (Fig. 5). For specific species, only northern lapwing showed a significant negative correlation with average water level in the dry season (ln-transformed, R2 = 0.38, F = 7.88, P = 0.015) (Fig. 5). Discussion As part of China's largest freshwater lake ecosystem, the Poyang Lake wetland supports rich species diversity and numerous wintering birds. High waterbird species richness and abundance revealed in our long-term monitoring from 2001 to 2016 provides good evidence of the wetland's importance for migratory birds. The average annual number of waterbirds was estimated to be about 426,707, with a maximum of 725,760 waterbirds belonging to 111 species. Diverse habitats such as deep water areas, shallow water areas, marsh, mudflat, sandy land, and grassland coexisted in the wetland during the entire dry season, which provided suitable habitats for different guilds of waterbirds. Meanwhile, large areas of habitat and consequently high carrying capacity ensured the survival of hundreds of thousands of waterbirds in this wetland (Liu et al., 2011). Compared with bird species richness 15 years before (Wu and Ji, 2002), there was no distinct change. However, more casual

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species were recorded, such as Canada goose (Branta canadensis), brant goose (Branta bernicla), ferruginous duck (Aythya nyroca), and blackfaced spoonbill (Platalea minor). On the other hand, some species have become rare, such as great bustard, which had a small, stable population in Poyang Lake during 1983–2000, with an annual average of 111 ± 98 individuals (Wu and Ji, 2002), but only one individual was detected during 2001–2016 in this study. Although there were fluctuations in annual waterbird abundance during 2001–2016, total waterbird abundance did not show a significant trend, nor did abundance of the four bird guilds defined here. It seems that during the study period, no significantly large effect of changing environmental conditions on waterbird abundance occurred in the Poyang Lake, even as the hydrological regime experienced significant change (Liu et al., 2013). One potential reason for this is that the diverse, unique landscape has, in some ways, buffered adverse effects of a prolonged dry season on waterbirds. A great number of inner lakes separated from the Poyang Lake were formed in the dry season, with their water level changing independently, and these were important wintering habitats for waterbirds (Qi et al., 2011). However, species specific analyses revealed significant population trends during the study period for a variety of species, including common crane, oriental white stork, white-naped crane, grey heron, bean goose, gadwall, northern pintail, spot-billed duck, Eurasian wigeon, common redshank, little grebe, and crested grebe. For migratory birds, population fluctuations can be the result of factors on breeding areas, wintering grounds, or stopover sites (Xu et al., 2015a). Thus, it is difficult to identify specific determining factors for the population fluctuations observed at Poyang Lake. Nonetheless, populations of some species, e.g. oriental white stork, have likely benefitted from habitat improvements stemming from the China National Wetland Conservation Action Plan (Wang et al., 2012). Numerous wetlands in the middle-

lower Yangtze River region can provide waterbirds with many options for wintering grounds (Cao et al., 2010), which could contribute to annual fluctuations in waterbird abundance. Finally, large areas of rice cultivation near the Poyang Lake wetland provide some waterbirds with suitable feeding habitat, which may increase the carrying capacity of the Poyang Lake wetland but which could also result in substantial dispersal of waterbirds. As for crane species, hooded crane, white-naped crane and Siberian crane all showed significant or weakly significant decreasing trends. The population trends of crane species do not seem to be a result of the lower water levels of Poyang Lake. In another study, food shortage caused by abnormal flooding was demonstrated to be a determining factor for a shift to alternative foraging habitats in the Poyang Lake (Burnham et al., 2017). Vallisneria plants are usually recognized as the major food for cranes in Poyang Lake; they grow well when water levels are lower than 17 m during the wet season and are suppressed when water levels are higher than 18 m (Li et al., 2011). As a result of the collapse of Vallisneria following abnormal wet season flooding, food deficits in winter forced Siberian cranes to switch feeding strategies and habitat (Burnham et al., 2017; Jia et al., 2013). Abnormal flooding has driven Siberian cranes and white-naped cranes to heavily cultivated rice paddies in recent years, which could partly explain population decreases in their traditional foraging habitats in natural wetlands (rice paddies were not included in our survey). Common cranes have frequently used rice paddies in the Poyang Lake area (Shan, 2013), which may be the reason for their population increase regardless of the food shortage after abnormal flooding. Hooded cranes were seldom found to use rice paddies, and thus, would be more vulnerable to the effects of wet season flooding. Interestingly, outside of our study areas we observed an increasing number of cranes foraging in rice paddies in recent years. However, the importance of agricultural fields to cranes was not realized until the winter of 2016, when approximately 1000 Siberian

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cranes fed in a small lotus pond near Poyang Lake in early winter and 300 individuals used this pond throughout the winter. For waterfowl, goose abundance significantly increased, which mainly resulted from the significant increase in abundance of bean goose and swan goose. Although swan goose did not show a significant trend, its abundance during 2010–2016 was significantly greater than that in 2001–2008. Coincidentally, 2008 and 2009 were critical years when the Three Gorges Dam started to operate with significant impacts on the hydrological regime of Poyang Lake. Further study is needed to explore the effect of the Three Gorges Dam operation on the distributions of tundra swan, geese, and ducks in the middle and lower Yangtze River as well as on Poyang Lake. We found that water levels during the wet season showed significant correlations with waterfowl abundance. Both the total abundance of swans and ducks were significantly correlated with average monthly water levels during the wet season, while goose abundance showed a significant positive correlation with average June water level. Presumably these significant correlations were due to the influence of water levels during the wet season on food availability for waterbirds in winter. As key drivers of the wetland system, even slight changes in water levels and inundation period may change wetland plant communities (David, 1996), and flooding can have a particularly profound impact (Toogood and Joyce, 2009). Water levels during the wet season have been found to have a significant influence on vegetation growth in Poyang Lake, especially species diversity, abundance, and distribution of aquatic macrophytes in the wetland (Dai et al., 2016; You et al., 2015; Tan and Jiang, 2016). Overly high water levels could cause lower plant biomass (Xu et al., 2015b). Massive flooding could cause extensive death of submerged plants and reduce the density and biomass of aquatic plants in Poyang Lake (Cui et al., 2000). Therefore, higher

water levels in wet season may mean lower availability of food resources or even a food shortage for swans and ducks which are highly dependent on submerged plants in winter. Conversely, geese are heavily reliant on plants in grasslands emerging after water recession; therefore higher water levels during wet season may result in expanded habitat and more abundant food resources for geese. Similarly, numerous cranes in rice fields offer convincing evidence of a shift in foraging strategy or habitat selection of cranes. Shorebird abundance was also negatively correlated with water levels during the wet season and with flood duration. Although much less is known about shorebird ecology in Poyang Lake, the negative correlations may be related to food availability. Biomass of benthic invertebrates is known to decrease with increasing water depth and distance from the shore (Saiz-Salinas and Ramos, 1999; Soltwedel, 1997). In Poyang Lake, accelerated dryness converted the shallow water area into grassland and was typically accompanied by human disturbances such as tourism and livestock grazing. Habitats available for shorebirds were limited to areas distant from the shore. Thus, increased water level and extended flood duration probably significantly reduced habitat availability and food abundance for shorebirds. It is not unexpected to find a negative correlation between northern lapwing abundance and dry season water level. Water level fluctuations during the dry season can influence habitat availability and distribution of wintering birds at Poyang Lake (Chen et al., 2016). Suitable habitat for waterbirds shrinks with rising water level in the dry season and virtually disappears when water levels are higher than 14 m (Xia et al., 2010). In addition, water levels can also influence the degree of human disturbance experienced by waterbirds. At lower water levels, appropriate habitats are available in areas surrounded by extensive mud flats, which make human access difficult (Barzen et al., 2009). As

Please cite this article as: Y. Li, F. Qian, J. Silbernagel, et al., Community structure, abundance variation and population trends of waterbirds in relation to water le..., Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2019.08.002

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Fig. 4. Significant correlations between abundance of swan, goose, duck, and dabbling duck and monthly average water level (above msl) of Poyang Lake.

Fig. 5. Wader abundance was significantly correlated with average water level (above msl) and high water level duration during the wet season. Northern lapwing abundance was significantly correlated with average dry season water levels.

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dry season water levels rise, the land-water ecotone – the most important habitat for migratory birds – shifts towards human settlements, which causes waterbirds to be more vulnerable to human disturbance and poaching (Liu et al., 2011).

Conservation implications As a wintering ground of international importance for waterbirds, the Poyang Lake wetland supports hundreds of thousands of migratory waterbirds. Habitat availability and quality in this wetland could directly affect Asian waterbird abundance, community structure, and the survival of endangered species. Severe drought caused such concern about the survival of waterbirds in Poyang Lake that a controversial hydrological structure was proposed to control the water level in dry season. However, our study indicates that water levels in the wet season can also have profound effects on waterbirds, which is easy to overlook compared to the immediate adverse effects of winter drought. Increased water levels and flood duration during the wet season may become the new norm for Poyang Lake because of the Three Gorges Dam. The dam may increase water discharge from the Yangtze River into Poyang Lake, raising the lake's water level and worsening flooding (Wang et al., 2011). Considering the increasing trend of high flood stages and duration in Poyang Lake (Li et al., 2015), food deficits resulting from increased water level and prolonged inundation raises new challenges for waterbird conservation, especially endangered species. Thus, we suggest further research is necessary to more comprehensively understand the effects of altered hydrology on wintering waterbirds. We argue that any proposals designed to control water levels during the dry season should be modeled to project and evaluate effects on waterbird habitats. Meanwhile, rice fields near Poyang Lake should be included in the ongoing monitoring project for the wintering waterbird census, and future habitat modeling studies. Supplementary data to this article can be found online at https://doi. org/10.1016/j.jglr.2019.08.002.

Acknowledgements This study was supported financially by the National Natural Science Foundation of China (No. 31660618 and No. 31460107). We are grateful to the leaders and workers in local wildlife services and nature reserve management bureaus, and birdwatching volunteers who graciously contributed their time and effort in helping us complete this field study. We thank Nathan Schulfer and, Sulong Zhou for their support in writing and reviewing the manuscript, and the Nelson Institute for Environmental Studies for hosting Li Yankuo's visiting fellowship to the University of Wisconsin-Madison in the U.S. from February to August 2017. References An, S.Q., Li, H.B., Guan, B.H., Zhou, C.F., Wang, Z.S., Deng, Z.F., Zhi, Y.B., Liu, Y.H., Xu, C., Fang, S.B., Jiang, J.H., Li, H.L., 2007. China's natural wetlands: past problems, current status, and future challenges. Ambio 36 (4), 335–342. Andreoli, R., Yésou, Y., Li, J., Desnos, Y.L., Shifeng, H., De Fraipont, P., 2007. Poyang Hu (Jiangxi Province, PR of China) area variations between January 2004 and June 2006 using ENVISAT low and medium resolution time series. Int. J. Geogr. Inf. Sci. 13 (1–2), 24–35. Balian, E.V., Segers, H., Lévêque, C., Martens, K., 2008. The freshwater animal diversity assessment: an overview of the results. Hydrobiologia 595 (1), 627–637. Barzen, J.A., Engels, M., Burnham, J., Harris, J., Wu, G.F., 2009. Potential impacts of a water control structure on the abundance and distribution of wintering waterbirds at Poyang Lake. In: International Crane Foundation (Ed.), Unpublished Report Submitted to Hydro-Ecology Institute of the Yangtze Water Resources Commission. Bolduc, F., Afton, A.D., 2008. Monitoring waterbird abundance in wetlands: the importance of controlling results for variation in water depth. Ecol. Model. 216 (3–4), 402–408. Burnham, J., Barzen, J.A., Pidgeon, A.M., Sun, B.T., Wu, J.D., Liu, G., Jiang, H.X., 2017. Novel foraging by wintering Siberian Cranes Leucogeranus leucogeranus at China's Poyang Lake indicates broader changes in the ecosystem and raises new challenges for a critically endangered species. Bird. Conserv. Int. 27 (2), 204–223.

9

Cao, L., Zhang, Y., Barter, M., Lei, G., 2010. Anatidae in eastern China during the nonbreeding season: geographical distributions and protection status. Biol. Conserv. 143 (3), 650–659. Chen, B., Cui, P., Xu, H.G., Lu, X.Q., Lei, J.C., Wu, Y., Shao, M.Q., Ding, H., Wu, J., Cao, M.C., Liu, G.H., 2016. Assessing the suitability of habitat for wintering Siberian cranes (Leucogeranus leucogeranus) at different water levels in Poyang lake area, China. Pol. J. Ecol. 64 (1), 84–97. Collen, B., Whitton, F., Dyer, E.E., Baillie, J.E.M., Cumberlidge, N., Darwall, W.R., Pollock, C., Richman, N.I., Soulsby, A.M., Böhm, M., 2014. Global patterns of freshwater species diversity, threat and endemism. Glob. Ecol. Biogeogr. 23 (1), 40–51. Cui, X.H., Zhong, Y., Chen, J.K., 2000. Influence of a catastrophic flood on densities and biomasses of three plant species in Poyang Lake, China. J. Freshw. Ecol. 15 (4), 537–541. Dai, X., Wan, R.R., Yang, G.S., Wang, X.L., Xu, L.G., 2016. Responses of wetland vegetation in Poyang Lake, China to water-level fluctuations. Hydrobiologia 773 (1), 35–47. David, P.G., 1996. Changes in plant communities relative to hydrologic conditions in the Florida Everglades. Wetlands 16 (1), 15–23. Feng, L., Hu, C.M., Chen, X.L., Cai, X.B., Tian, L.Q., Gan, W.X., 2012. Assessment of inundation changes of Poyang Lake using MODIS observations between 2000 and 2010. Remote Sens. Environ. 121, 80–92. Gardner, R.C., Barchiesi, S., Beltrame, C.M., Finlayson, M., Galewski, T., Harrison, I.J., Paganini, M., Perennou, C., Pritchard, D.E., Rosenqvist, A., Walpole, M., 2015. State of the world's wetlands and their services to people: a compilation of recent analyses. Ramsar Briefing Note No. 7. Ramsar Convention Secretariat, Gland. He, Y., Zhang, M.X., 2001. Study on wetland loss and its reasons in China. Chin. Geogr. Sci. 11 (3), 241–245. Howes, J., 1989. Shorebird Studies Manual (No. 55). Asian Wetland Bureau, Kuala Lumpur, Malaysia. Huang, Y., Li, Y.K., Ji, W.T., Xu, P., Wang, Z.G., 2016. Bird diversity and conservation status in Poyang Lake Area. Wetland Sci. 14 (3), 311–327 (In Chinese). Ji, W.T., Zen, N.J., Wang, Y.B., Gong, P., Xu, B., Bao, S.M., 2007. Analysis of the waterbirds community survey of Poyang Lake in winter. Ann. GIS 13 (1), 51–64. Jia, Y.F., Jiao, S.W., Zhang, Y.M., Zhou, Y., Lei, G.C., Liu, G.H., 2013. Diet shift and its impact on foraging behavior of Siberian crane (Grus leucogeranus) in Poyang Lake. PLoS One 8 (6), e65843. Jiao, L., 2009. Scientists line up against dam that would alter protected wetlands. Science 326 (5952), 508–509. Li, X.H., Zhang, Q., 2015. Variation of floods characteristics and their responses to climate and human activities in Poyang Lake, China. Chin. Geogr. Sci. 25 (1), 13–25. Li, F.S., Liu, G.H., Wu, J.D., Zeng, N.J., Harris, J., Jin, J.F., 2011. Ecological Study of Wetlands and Waterbirds at Poyang Lake. Popular Science Press, Beijing. Li, X.H., Zhang, Q., Xu, C.Y., Ye, X.C., 2015. The changing patterns of floods in Poyang Lake, China: characteristics and explanations. Nat. Hazards 76 (1), 651–666. Li, M., Zhang, Q., Li, Y.L., Yao, J., Tan, Z.Q., 2016. Inter-annual variations of Poyang Lake area during dry seasons: characteristics and implications. Hydrol. Res. 47 (S1), 40–50. Liu, C., Tan, Y.J., Lin, L.S., Tao, H.N., Tan, H.R., 2011. The wetland water level process and habitat of migratory birds in Lake Poyang. J. Lake Sci. 23 (1), 129–135 (in Chinese). Liu, Y.B., Wu, G.P., Zhao, X.S., 2013. Recent declines in China's largest freshwater lake: trend or regime shift? Environ. Res. Lett. 8 (1), 014010. Mei, X.F., Dai, Z.J., Du, J.Z., Chen, J.Y., 2015. Linkage between Three Gorges Dam impacts and the dramatic recessions in China's largest freshwater lake, Poyang Lake. Sci. Rep. 5, 18197. Niu, Z.G., Zhang, H.Y., Wang, X.W., Yao, W.B., Zhou, D.M., Zhao, K.Y., Zhao, H., Li, N.N., Huang, H.B., Li, C.C., Yang, J., Liu, C.X., Liu, S., Wang, L., Li, Z., Yang, Z.Z., Qiao, F., Zheng, Y.M., Chen, Y.L., Sheng, Y.W., Gao, X.H., Zhu, W.H., Wang, W.Q., Wang, H., Weng, Y.L., Zhuang, D.F., Liu, J.Y., Luo, Z.C., Cheng, X., Guo, Z.Q., Gong, P., 2012. Mapping wetland changes in China between 1978 and 2008. Chin. Sci. Bull. 57 (22), 2813–2823. Qi, S.H., Liu, Y., Yu, X.B., Liao, F.Q., 2011. Effect of “Lake enclosed in autumn” on the habitat of winter bird in Poyang Lake. Res. Environ. Yangtze Basin 20 (Z1), 18–21 (In Chinese). Qian, F.W., Yu, C.H., Jiang, H.X., 2009. Ground and Aerial Surveys of Wintering Waterbirds in Poyang Lake Basin. In Proceedings of the UNEP/GEF Siberian Crane Wetland Project, Project Completion Workshop, Harbin. R Core Team, 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria Available from. http://www.R-project.org/. Saiz-Salinas, J.I., Ramos, A., 1999. Biomass size-spectra of macrobenthic assemblages along water depth in Antarctica. Mar. Ecol. Prog. Ser. 178, 221–227. Shan, J.H., 2013. The Bird Species Diversity, Population Dynamics of the Endangered Bird Species and Conservation Gap Analysis in the Poyang Lake. (Ph.D. Dissertation). Northeast Forestry University, Harbin, China. Shankman, D., Davis, L., De Leeuw, J., 2009. River management, land use change, and future flood risk in China's Poyang Lake region. Int. J. River Basin Manag. 7 (4), 423–431. Soltwedel, T., 1997. Temporal variabilities in benthic activity and biomass on the western European continental margin. Oceanol. Acta 20 (6), 871–879. SPSS Inc. Released, 2009. PASW Statistics for Windows, Version 18.0. SPSS Inc., Chicago. Tan, Z.Q., Jiang, J.H., 2016. Spatial–temporal dynamics of wetland vegetation related to water level fluctuations in Poyang Lake, China. Water 8 (9), 397. Toogood, S.E., Joyce, C.B., 2009. Effects of raised water levels on wet grassland plant communities. Appl. Veg. Sci. 12 (3), 283–294. Wang, X.H., 2004. Evaluation on Poyang Lake Wetland Ecosystem. Science Press, Beijing (In Chinese). Wang, Y.C., Lai, X.J., Jiang, J.H., Huang, Q., 2011. Effect of the Three Gorges Reservoir on the water regime of the Lake Poyang wetlands during typical water regulation period. J. Lake Sci. 23, 191–195 (In Chinese). Wang, Z.M., Wu, J.G., Madden, M., Mao, D., 2012. China's wetlands: conservation plans and policy impacts. Ambio 41 (7), 782–786.

Please cite this article as: Y. Li, F. Qian, J. Silbernagel, et al., Community structure, abundance variation and population trends of waterbirds in relation to water le..., Journal of Great Lakes Research, https://doi.org/10.1016/j.jglr.2019.08.002

10

Y. Li et al. / Journal of Great Lakes Research xxx (xxxx) xxx

Wei, Z.H., Li, Y.K., Xu, P., Qian, F.W., Shan, J.H., Tu, X.B., 2016. Patterns of change in the population and spatial distribution of oriental white storks wintering in Poyang Lake. Zool. Res. 37 (6), 338–346. Wu, Y.H., Ji, W.T., 2002. Study on Jiangxi Poyang Lake National Nature Reserve. Forestry Press, Beijing (In Chinese). Xia, S.X., Yu, X.B., Fan, N., 2010. The wintering habitats of migrant birds and their relationship with water level in Poyang Lake, China. Res. Sci. 32 (11), 2072–2078 (In Chinese). Xu, C.L., Barrett, J., Lank, D.B., Ydenberg, R.C., 2015a. Large and irregular population fluctuations in migratory Pacific (Calidris alpina pacifica) and Atlantic (C. a. hudsonica) dunlins are driven by density-dependence and climatic factors. Popul. Ecol. 57 (4), 551–567. Xu, X., Zhang, Q., Tan, Z.Q., Li, Y.L., Wang, X.L., 2015b. Effects of water-table depth and soil moisture on plant biomass, diversity, and distribution at a seasonally flooded wetland of Poyang Lake, China. Chin. Geogr. Sci. 25 (6), 739–756.

You, H.L., Xu, L.G., Liu, G.L., Wang, X.L., Wu, Y.M., Jiang, J.H., 2015. Effects of inter-annual water level fluctuations on vegetation evolution in typical wetlands of Poyang Lake, China. Wetlands 35 (5), 931–943. Zhang, J.Y., Ma, K.M., Fu, B.J., 2010. Wetland loss under the impact of agricultural development in the Sanjiang Plain, NE China. Environ. Monit. Assess. 166 (1–4), 139–148. Zhang, Q., Li, L., Wang, Y.G., Werner, A.D., Xin, P., Jiang, T., Barry, D.A., 2012. Has the ThreeGorges Dam made the Poyang Lake wetlands wetter and drier? Geophys. Res. Lett. 39 (20), L20402. Zhu, Q., Zhan, Y.H., Liu, G.H., Wu, J.D., Zhan, H.Y., Huang, Y.Z., Huang, J., Zhang, B., Hu, B.H., Li, Y., 2012. Investigation of number and distribution of the waterfowl of Poyang Lake in the winter of 2011. Jiangxi Forestry Sci. Technol. 3, 1–9 (In Chinese).

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