STOTEN-144061; No of Pages 10

Science of the Total Environment xxx (xxxx) xxx

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Function of restored wetlands for waterbird conservation in the Yellow Sea coast
Jun Fan a, Xiaodan Wang a, Wei Wu b, Weipin Chen b, Qiang Ma b, Zhijun Ma a,⁎
a
Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Coastal Ecosystems Research Station of the Yangtze River Estuary, Fudan University, Shanghai 200433, China
b
Shanghai Chongming Dongtan National Nature Reserve, Shanghai 202183, China

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• Restored wetlands support high water-

bird diversity
• Waterbird communities differ among
restored, natural, and artificial wetlands
• Restored wetlands are unlikely to re-
place the natural ones for waterbird
conservation
• Natural wetland conservation should be
the priority for waterbird conservation

a r t i c l e i n f o a b s t r a c t

Article history: To reduce the harm to wildlife caused by habitat loss and degradation, significant resources have been invested in
Received 4 August 2020 habitat restoration worldwide. However, whether restored habitats can support wildlife communities similar to
Received in revised form 10 November 2020 those natural ones remains unclear. Providing habitat for waterbirds, which are dependent on wetland for their
Accepted 22 November 2020
survival, is a major target in many wetland restoration practices. Here we conducted a year-round waterbird sur-
Available online xxxx
vey at Chongming Dongtan, a national nature reserve established for waterbird conservation in the south Yellow
Editor: Jan Vymazal Sea, in order to compare the characteristics of waterbird communities in four wetland types: restored wetlands,
natural tidal wetlands, and two artificial wetlands (fish ponds and farmlands). We determined whether water-
Keywords: bird diversity and species composition differed among the wetland types. The results indicated that waterbird di-
Artificial wetland versity, in terms of species richness, individual density, Shannon-Wiener diversity, functional diversity, and
Diversity phylogenetic diversity, was generally similar in the restored and natural wetlands and was higher in the restored
Habitat restoration and natural wetlands than in fish ponds or farmlands. Most threatened species and exclusive species occurred in
Natural wetland both natural and restored wetlands, but the overall species composition significantly differed between natural
Waterbird community
and restored wetlands. Non-metric multidimensional scaling analysis also indicated that waterbird community
significantly differed among the wetland types. The results suggest that restored wetlands support substantial
waterbird diversity but cannot replace natural wetlands because they lack the period tides that many tideland
specialists (shorebirds) depend on. This study highlights the importance of protecting natural wetlands for wa-
terbird conservation. We propose that both the diversity and species composition of wildlife communities should
be considered in evaluating the effectiveness of habitat restoration for wildlife.
© 2020 Elsevier B.V. All rights reserved.

1. Introduction

Wetlands provide a complex suite of ecosystem services including

flood mitigation, water quality improvement, providing food and habi-
⁎ Corresponding author. tats for wildlife, and supplying natural products for human use (Zedler,
E-mail address: zhijunm@fudan.edu.cn (Z. Ma). 2003; Jessop et al., 2015). Wetlands are greatly affected by human

https://doi.org/10.1016/j.scitotenv.2020.144061
0048-9697/© 2020 Elsevier B.V. All rights reserved.

Please cite this article as: J. Fan, X. Wang, W. Wu, et al., Function of restored wetlands for waterbird conservation in the Yellow Sea coast, Science
of the Total Environment, https://doi.org/10.1016/j.scitotenv.2020.144061
J. Fan, X. Wang, W. Wu et al.
activities. More than half of wetlands have disappeared or have been de-
graded over the past century (Davidson, 2014) and about 35% have
been destroyed since 1970 (Ramsar Convention on Wetlands, 2018).
This has negatively affected wildlife that live in wetlands, and has espe-
cially harmed those waterbirds that are highly dependent on wetland
habitats for their survival. Among all waterbird populations worldwide,
38% are declining (Wetland International, 2012), and the dramatic loss
and degradation of wetlands is the major cause of the population de-
clines (Kirby et al., 2008). How to provide suitable habitats for popula-
tion maintenance is a central challenge in waterbird conservation (Ma
et al., 2010; Jackson et al., 2020).
Because wetlands represent important natural capital and provide
essential ecological services, wetland restoration has become a global
concern (Wolters et al., 2005; Erwin and Beck, 2007; Moreno-Mateos
et al., 2012; Cui et al., 2016). Huge amounts of resources have been
invested and strict policies or laws, such as the ‘no net loss’ policy in
the USA and the Habitat Directive in the European Union, have been de-
veloped in some countries and regions to ensure the implementation of
wetland restoration (Copeland, 2010; De Groot et al., 2013; Ramsar
Convention on Wetlands, 2018). Providing habitats for waterbirds is
often a target of wetland restoration, and the responses of waterbirds
are indicators of habitat conditions and restoration trajectory (Erwin
and Beck, 2007; Bregnballe et al., 2014; Hagy et al., 2017; Tapp et al.,
2018). Many studies have found that restored wetlands can provide for-
aging, nesting, and roosting habitats and thus benefit diverse waterbird
species (Erwin and Beck, 2007, O'Neal et al., 2008, Sebastián-González
and Green, 2016; Morelli et al., 2017), suggesting that wetland restora-
tion is an effective approach for waterbird conservation in the face of
habitat loss and degradation.
Although former studies have indicated that restored wetlands can
support diverse waterbirds, the extent to which wetland restoration
can compensate for the loss of natural wetland habitat is unclear.
Some studies focused on the population recovery of special species or
groups and especially those are threatened (e.g., Armitage et al., 2007;
Jiang et al., 2016) but provided no information on other species and es-
pecially on common species that nevertheless provide important eco-
system functions. Some surveys focused on waterbirds in a specific
season (Bregnballe et al., 2014; Tapp et al., 2018; Luo et al., 2019), but
many waterbirds are migratory and have large seasonal differences in
their geographical distribution and habitat requirements. Some studies
only compared changes in bird diversity before and after wetland resto-
ration (Bregnballe et al., 2014). Because wetland restoration generally
improves habitat quality, it is not surprising that bird diversity increases
after restoration. Moreover, most studies focused on the number of spe-
cies and individuals among wetland types (Konisky et al., 2006) but fail
to consider the function of wetlands in supporting waterbirds. Wetlands
with low waterbird diversity, for example, might be important for spe-
cies with specific habits (Murillo-Pacheco et al., 2018) or with specific
habitat requirements (Jackson et al., 2019); such wetlands are therefore
indispensable for population maintenance even though their diversity is
low. Because of the differences in wetland properties and in the species
composition and habitat requirements of birds in different regions, wet-
land restoration efforts should be based on local conditions and should
have clearly defined restoration targets.
Species diversity is a common index used in the comparison of com-
munity characteristics (e.g., Armitage et al., 2007; O'Neal et al., 2008;
Bregnballe et al., 2014; Sievers et al., 2018). As an index, however, spe-
cies diversity treats all species as equally different from each other and
thus neglects the phylogenetic relationships and specific functions of
different guilds (Hooper et al., 2005). In contrast to species diversity,
phylogenetic diversity incorporates species evolutionary history; low
phylogenetic diversity suggests that a community is composed of
closely related species that may share similar ecological niches or habi-
tat requirements (Knapp et al., 2008). Similarly, functional diversity,
which represents differences in morphological and physiological fea-
tures related to the use of resources, reflects the adaptability of a
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community to environmental change (Petchey and Gaston, 2006).
When a habitat changes, species diversity, phylogenetic diversity, and
functional diversity can exhibit various trends (Frishkoff et al., 2014).
Diversity assessments also usually fail to account for differences in spe-
cies composition, i.e., communities with similar diversity may have
great differences in species composition. As a consequence, incorporat-
ing various measures of community diversity and species composition is
essential for comparing waterbird communities among wetland types
and for assessing management options.
Tidal wetlands along coasts provide habitats for the breeding, stop-
over, and wintering of diverse waterbirds. Tidal wetlands, however,
have suffered dramatic losses and degradation due to multiple factors,
such as reclamation, spread of invasive species, over-exploitation, pollu-
tion, and sea-level rise (Gedan et al., 2009; Murray et al., 2019). In the
Yellow Sea region in China, tidal wetlands are critical habitats for mil-
lions of waterbirds along the East Asian-Australasian Flyway, but more
than half of the total area of the tidal wetlands has been destroyed by
reclamation and exploitation in the past three decades (Murray et al.,
2014; Chen et al., 2019). In addition, the rapid spread of alien smooth
cordgrass (Spartina alterniflora) on tidal wetlands has degraded the hab-
itat for waterbirds (Gan et al., 2009). Smooth cordgrass is salt tolerant
and flood tolerant, and can spread over an entire tideland, from the
high-tide to the low-tide zone. In forming dense monocultures, smooth
cordgrass excludes native plants, including those that provide food for
birds, and generates a habitat that is unusable for most waterbirds
(Gan et al., 2009; Li et al., 2009a). As of 2015, > 40,000 ha of tidal wet-
lands in the Yellow Sea were occupied by smooth cordgrass (Liu et al.,
2018). The loss and degradation of tidal wetlands in the Yellow Sea
has caused a rapid decline of many waterbird populations and especially
of shorebirds that are highly dependent on tidal wetlands for refueling
during migration (Hua et al., 2015; Piersma et al., 2016; Studds et al.,
2017).
To mitigate the adverse effects on waterbirds of wetland loss and
degradation, the Chinese government, in addition to protecting natural
tidal wetlands, has invested significant resources in the restoration of
destroyed coastal wetlands (Stokstad, 2018). The waterbird habitat res-
toration project at Chongming Dongtan (31°25′–31°38′N, 121°50′–
122°05′E, Fig. 1) in the south Yellow Sea is the largest wetland restora-
tion project for waterbird conservation in China. Chongming Dongtan
has been designated as a national nature reserve and a wetland of inter-
national importance because it is essential for the conservation of mi-
gratory waterbirds along the East Asian-Australasian Flyway (Li et al.,
2009b; Choi et al., 2014). Since the 1990s, however, smooth cordgrass
has rapidly spread on the tidal wetlands at Chongming Dongtan and
now occupies >2000 ha of habitat for waterbirds. To remove smooth
cordgrass and reestablish wetland habitats for waterbirds, the govern-
ment has invested more than 180 million US dollar in a massive wetland
restoration project in 2013. The project had created 2400 ha of restored
wetlands with a mixed landscape of reed marsh, open water, shallow
shoals, and small islands (Ma, 2017; Kuang et al., 2019).
Understanding the effectiveness of wetland restoration can provide
a reference for management and habitat improvement. In the current
research, we attempted to answer the following questions: 1) Do the re-
stored wetlands at Chongming Dongtan support a high diversity of wa-
terbirds? 2) How do waterbird communities differ between wetland
types? and 3) Are restored wetlands good alternatives to natural wet-
lands? To answer these questions, we conducted a year-round water-
bird survey and compared waterbird communities in the restored
wetlands, in natural tidal wetlands, and in two artificial wetland types
(fish ponds and farmlands that are economic enterprises) at Chongming
Dongtan. The large areas of fish ponds and farmlands near the tidal wet-
lands and restored wetlands at Chongming Dongtan provide alternative
habitats to natural wetlands for waterbirds (Ma et al., 2004; Choi et al.,
2014; Kuang et al., 2019). Using the data from the survey, we compared
waterbird diversity (in terms of species richness, individual density,
Shannon-Wiener diversity, functional diversity, and phylogenetic
J. Fan, X. Wang, W. Wu et al.
Fig. 1. Location of Chongming Dongtan in the Yellow Sea (insert map) and distribution of major habitat types at Chongming Dongtan.
diversity) and species composition of waterbird community among
wetland types. We then discuss the implications of our results for wa-
terbird conservation and habitat management at Chongming Dongtan.
Because wetland restoration has been a global conservation action, re-
sults from this study should be applicable to habitat management in
other regions.
2. Materials and methods
2.1. Study area
Bared mudflat and vegetated saltmarsh are the major components of
the natural tidal wetlands at Chongming Dongtan (Fig. 1). With regular
and semi-diurnal tides, there are two distinct periods of ebb and flood
tides in a day. Most tidal flats are submerged by tidewater during the
high tide of the spring tide, while a large area of the tidal flats is exposed
during the low tide of the spring tide. Sea bulrush (Scirpus mariqueter) is
the dominant native plant on the saltmarsh, and its seeds and corms are
major foods for herbivorous waterbirds (Ma et al., 2004; Li et al., 2009b).
Migratory shorebirds are the dominant waterbirds on the tidal wetland
(Choi et al., 2009). They forage for macrobenthos when the tidal flats are
exposed, and they fly to nearby high-tide roosts when the tidal flats are
submerged by tidewater (Li et al., 2009b; Choi et al., 2014).
Restored wetlands are adjacent to natural tidal wetlands (Fig. 1).
Alien smooth cordgrass has been widely distributed in this area but has
been completely removed by the wetland restoration project. To remove
the smooth cordgrass and to restore habitats for waterbirds, the project
included the following actions: 1) constructing embankments to enclose
the tideland invaded by smooth cordgrass; 2) cutting the aboveground
vegetation of smooth cordgrass; 3) killing the underground organs of
smooth cordgrass by long-term flooding; 4) transforming the topogra-
phy and drawing water into the region to form open water areas, shoals,
and islands, and to thereby create diverse habitats for waterbirds; and
5) planting native plants (the reed Phragmites australis and the sea bul-
rush Scirpus mariqueter) that provide shelter and food for birds. To facil-
itate habitat management, the restored wetlands have been divided into
different zones of ~100 ha by dams. Each zone has a similar landscape
that includes open water, patchy reed marsh, shallow shoals, and small
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Science of the Total Environment xxx (xxxx) xxx
islands. Water depth in each zone is managed according to the seasonal
traits and habitat preference of major waterbird groups (Ma et al., 2009).
More specifically, the water level is raised to a mean depth of 30–100 cm
in the winter to provide additional open water areas for wintering ducks,
and the water level is lowered to a mean depth of 10–30 cm in spring,
summer, and autumn to provide the shallow water and exposed moist
shoals that are required by waders, and especially by migratory shore-
birds (Ma, 2017; Kuang et al., 2019).
Over the past several decades, Chongming Dongtan has experienced
many large-scale land reclamations. Some enclosed regions were con-
verted to artificial wetlands, such as fish ponds and farmlands (Li
et al., 2009b, Fig. 1). Most fish ponds are open water areas, with water
depth maintained at 50–70 cm when fish are being cultivated. In mid-
winter, the water level in the fish ponds is reduced for harvesting.
Once fish are harvested, the bottoms of the ponds are exposed to the
sun for 1–2 months. After that, water is drawn into the ponds, and fry
or juvenile fish are added for the next round of aquaculture (Ma et al.,
2004; Choi et al., 2014).
Farmlands are generally operated for two crops a year at Chongming
Dongtan. Fields are plowed and flooded in May, and rice (Oryza sativa)
is planted in June. After rice is harvested in October, wheat (Triticum
aestivum) is planted. The wheat is harvested in May of the next year. Ir-
rigation canals border farmlands and are connected to river channels
and thus contain standing water year round. Reeds and cattails (Typha
orientalis) are the common wetland plants along the irrigation canals
(Li et al., 2009b).
2.2. Waterbird surveys
Waterbird surveys were conducted at 16 areas, including three in nat-
ural wetlands (tidelands), four in restored wetlands, four in farmlands,
and five in fish ponds. Survey areas on natural wetlands were selected ac-
cording to their accessibility, while survey areas on other wetland types
were randomly selected. Each survey area in natural wetlands, restored
wetlands, and farmlands was about 100 ha (mean ± SD = 106 ±
14 ha), while the survey area of fish ponds was smaller (17 ± 10 ha).
A total of 17 bird surveys were conducted during the study period
from November 2016 to October 2017. Surveys were conducted twice
J. Fan, X. Wang, W. Wu et al. Science of the Total Environment xxx (xxxx) xxx

per month in spring (March–May) and autumn (September–October),
i.e., during the migration season when bird communities rapidly
change, and once per month in summer (June–August) and winter
(November–February) when bird communities are stable. The periods
of the four seasons were classified according to the phenology of at
Chongming Dongtan (Li et al., 2009b; Ma et al., 2009). The 16 areas
were surveyed in a random order during each survey. Waterbirds
were identified and counted using a binocular (8 ×) and a spotting
scope (20–60 ×). An experienced surveyor (JF) attended all of the sur-
veys. During surveys, observers rode electric bicycles or walked along
trails surrounding or inside the areas and stopped to record species,
number, and foraging behavior (foraging or not) of birds. Birds flying
over the areas were not recorded. All of the surveys were conducted
during the low tide of the spring tide when the tidelands were exposed
and thus were available for waterbirds. To detect the effects of tide on
habitat use by waterbirds, we also conducted surveys in restored
wetlands, fish ponds, and farmlands during the high tide (when most
tidelands were submerged by tidewater) on the same day after surveys
at low tide. Each survey lasted about 1 week to cover all the areas.
2.3. Data analysis
Because bird communities differed greatly among seasons at
Chongming Dongtan (Ma et al., 2009), we gathered and analyzed bird
survey data in each season. Surveys were conducted multiple times in
the same area in each season, and we therefore calculated the total spe-
cies and the mean numbers of individuals recorded in the same area in
each season for further analysis. Because wetlands that support threat-
ened or exclusive species (habitat specialists that are recorded in only
one wetland type) have high conservation value, we counted threat-
ened (listed as critically endangered, endangered, vulnerable, or near
threatened categories in IUCN's red lists; IUCN, 2019) and exclusive spe-
cies in each wetland type. Waterbird abundance did not significantly
differ between high tide and low tide in the restored wetlands, fish
ponds, and farmlands in any season (paired t-test, P ≥ 0.05 for all, Ta-
ble S1), We therefore used waterbird data collected at low tide for fur-
ther analysis of all four wetland types.
Waterbirds were classified into four groups according to their habitat
preference and ecological habits (Ma et al., 2010): (1) dabbling birds,
i.e., swimming birds that generally forage in shallow water (ducks,
geese, gulls, coots, moorhen, and terns); (2) diving birds, i.e., swimming
birds that generally forage in deep water (grebes, loons, divers, and cor-
morants); (3) large waders, i.e., large wading birds that generally forage
in shallow water and on moist soil (herons, egrets, storks, and cranes);
and (4) small waders, i.e., small wading birds that generally forage in shal-
low water and on moist soil (shorebirds). We determined waterbird spe-
cies and individual numbers in each waterbird group and wetland type
and season.
To compare waterbird diversity among wetland types, we calculated
species richness, abundance, individual density, Shannon-Wiener diver-
sity, functional diversity, and phylogenetic diversity for sum of total spe-
cies or species groups in each wetland type and each season. We used bill
length (mm), body mass (g), foraging style (pecking, plunging, diving,
sweeping, probing, routing, and flying), and food type (plants, inverte-
brates, vertebrates, both invertebrates and vertebrates, and omnivores)
as functional traits (Table S2) to calculate functional diversity using the
FD package in R (Laliberté and Legendre, 2010). Functional traits of wa-
terbirds were collected from HBW Alive (Del Hoyo et al., 2019).
We obtained a phylogenetic tree of all of the recorded species from
Birdtree (www.birdtree.org). We generated the original 5000 trees
and then used the TreeAnnotator package in BEAST software (ver.
1.10.0) to burn-in the first 10% (500) of the trees, and calculated the
maximum clade credibility (MCC) tree using mean heights. The mean
pairwise distance, representing phylogenetic diversity, was measured
based on the MCC tree using the Ape and Picante packages in R
(Webb et al., 2002; Kembel and Ackerly, 2012).
All of the diversity indices (richness, individual density, Shannon-
Wiener diversity, functional diversity, phylogenetic diversity) were
compared among wetland types for each season using one-way
analyses of variance (ANOVAs). As a post-hoc test, the Tukey honest
significant difference (HSD) test was used to determine pairwise
differences. Individual density was logarithmically transformed to
improve normality. Individual density in natural wetlands was not
included in the comparison because the area of tidal flats kept changing
with tide fluctuation.
We determined the similarity of waterbird communities between all
pairs of wetland types in the same season using the Jaccard coefficient of
similarity (C) as C = j / (a + b - j), where j is the number of common
species in the two communities, and a and b are the species number
in each of the two communities. A value of 0 indicates no similarity,
and a value of 1 indicates that the species are identical in the two
communities.
To further compare the species composition of waterbird communi-
ties among wetland types, we performed non-metric multidimensional
scaling (NMDS) using Vegan package in R (Oksanen et al., 2019) and vi-
sualized community similarity based on the Bray-Curtis distance calcu-
lated by the waterbird abundance matrix (Faith et al., 1987). A standard
deviation of 95% confidence interval was used to demonstrate the com-
position range of each wetland type. Analysis of similarity (ANOSIM)
was also used to measure the difference among wetland types
(Warton et al., 2012) using Vegan package in R (Oksanen et al., 2019).
A positive R value from the range between R = −1 and R = 1 indicates
that intergroup differences are greater than intragroup differences and
thus bird communities are dissimilar among wetland types. A larger R
value indicates a greater intergroup difference.
All analyses were conducted in R ver. 3.5.1 (R Development Core
Team, 2019). Results are reported as means ± SE.
3. Results
A total of 160,908 waterbirds representing 92 species were recorded
during the study period. Waterbird communities exhibited seasonal
variation: the number of species was highest in spring, the number of
individuals was highest in winter, and the numbers of species and indi-
viduals were lowest in summer (Table 1). Natural wetlands and re-
stored wetlands supported the most waterbirds, with 75.0% of the

Table 1
Numbers of species and individuals of waterbirds (all species, exclusive species, and threatened species) in each season in natural wetlands, restored wetlands, farmlands, and fish ponds.
Values in parentheses are percentages of the totals indicated in the last two columns on the right.

Natural wetlands Restored wetlands Farmlands Fish ponds Total

Species Individuals Species Individuals Species Individuals Species Individuals Species Individuals

Spring 51 (65.4%) 19,613 (63.0%) 52 (66.7%) 7612 (24.4%) 31 (39.7%) 2836 (9.1%) 26 (33.3%) 1076 (3.5%) 78 31,137
Summer 30 (62.5%) 7855 (61.2%) 28 (58.3%) 3047 (23.7%) 12 (25.0%) 1700 (13.2%) 12 (25.0%) 234 (1.8%) 48 12,836
Autumn 48 (75.0%) 28,841 (70.6%) 50 (78.1%) 10,138 (24.8%) 20 (31.3%) 419 (1.0%) 19 (29.7%) 1441 (3.5%) 64 40,839
Winter 35 (60.3%) 28,098 (36.9%) 36 (62.1%) 44,959 (59.1%) 16 (27.6%) 1370 (1.8%) 26 (44.8%) 1669 (2.2%) 58 76,096
Total 69 (75.0%) 84,407 (52.5%) 74 (80.4%) 65,756 (40.9%) 37 (40.2%) 6325 (3.9%) 45 (48.9%) 4420 (2.7%) 92 160,908
Threatened species 16 (84.2%) 17,572 (70.7%) 10 (52.6%) 6985 (28.1%) 2 (10.5%) 245 (1.0%) 4 (21.1%) 46 (0.2%) 19 24,848
Exclusive species 11 (55.0%) 415 (15.8%) 6 (30.0%) 2165 (82.2%) 1 (5.0%) 28 (1.1%) 2 (10.0%) 26 (1.0%) 20 2636

4
J. Fan, X. Wang, W. Wu et al. Science of the Total Environment xxx (xxxx) xxx

Table 2
Waterbird diversity in terms of species richness, individual density, Shannon-Wiener diversity (SD), phylogenetic diversity (PD), and functional diversity (FD) as affected by wetland type
and season. Different letters indicate significant differences calculated using Tukey test at 5% level.

Season Wetland type Richness Density (/km2) SD PD FD

Natural wetland 33.33 ± 3.06a – 1.62 ± 0.54ab 132.20 ± 8.04a 0.97 ± 0.02a
Restored wetland 30.50 ± 2.38a 181.48 ± 34.38a 2.38 ± 0.28a 154.41 ± 1.53a 0.81 ± 0.05a
Spring
Farmland 15.00 ± 6.73b 101.02 ± 114.02a 1.60 ± 0.34ab 129.36 ± 19.32a 0.76 ± 0.17a
Fish pond 7.80 ± 5.26b 127.30 ± 135.20a 1.14 ± 0.50b 142.93 ± 18.38a 0.82 ± 0.12a
Natural wetland 22.00 ± 2.65a – 1.40 ± 0.64a 123.49 ± 3.17a 0.94 ± 0.04a
Restored wetland 15.00 ± 2.94b 100.33 ± 58.44a 1.60 ± 0.38a 138.62 ± 4.16a 0.81 ± 0.06ab
Summer
Farmland 6.00 ± 0.82c 73.38 ± 24.01a 0.93 ± 0.33a 87.76 ± 21.47b 0.91 ± 0.07a
Fish pond 6.20 ± 1.92c 48.78 ± 16.04a 1.48 ± 0.25a 116.98 ± 30.05ab 0.75 ± 0.06b
Natural wetland 34.00 ± 3.46a – 2.31 ± 0.10a 121.36 ± 5.11ab 0.89 ± 0.03a
Restored wetland 22.00 ± 9.42a 161.76 ± 131.31a 1.98 ± 0.40ab 143.90 ± 6.61a 0.90 ± 0.04a
Autumn
Farmland 7.50 ± 3.70b 12.53 ± 3.36b 1.39 ± 0.47bc 94.27 ± 26.42b 0.78 ± 0.14a
Fish pond 7.40 ± 1.67b 240.74 ± 447.21a 1.12 ± 0.39c 118.91 ± 12.33ab 0.74 ± 0.12a
Natural wetland 22.67 ± 2.08a – 1.23 ± 0.46a 154.37 ± 3.26a 0.92 ± 0.10a
Restored wetland 22.75 ± 5.19a 1247.00 ± 95.88a 1.56 ± 0.30a 142.87 ± 8.88a 0.88 ± 0.07a
Winter
Farmland 9.25 ± 0.50b 60.10 ± 33.53b 1.38 ± 0.49a 157.84 ± 2.88a 0.92 ± 0.08a
Fish pond 9.00 ± 4.00b 246.38 ± 169.11b 1.21 ± 0.58a 148.37 ± 13.63a 0.78 ± 0.13a

total number of species and 52.5% of total number of individuals being
recorded in natural wetlands, and 80.4% of the total number of species
and 40.9% of total number of individuals being recorded in restored wet-
lands. Few waterbirds were recorded in fish ponds and farmlands
(Table 1). Waterbirds exhibited foraging behavior in all of the wetland
types where they occurred.
A total of 19 threatened species were recorded in the four wetland
types; most of these occurred in natural (16 species) and restored wet-
lands (10 species); few were recorded in fish ponds (4 species) or farm-
lands (2 species). Similarly, exclusive species were more evident in
natural (11 species) and restored wetlands (6 species) than in fish
ponds (2 species) and farmlands (1 species, Table 1). Most individuals
of threatened species (70.7% of the total) were recorded in natural wet-
lands, while most individuals of exclusive species (82.2% of the total)
were recorded in restored wetlands (Table 1).
Our analysis of diversity included 20 comparisons (five diversity in-
dices × four seasons) involving restored wetlands, farmlands, and fish
ponds, but only 16 comparisons involving natural wetlands because
one of the diversity indices (individual density) was not determined
for natural wetlands. Diversity indices did not significantly differ be-
tween natural and restored wetlands in any of the four seasons, except
that species richness was higher in natural than in restored wetlands in
summer (Table 2). Diversity indices also did not differ between farm-
lands and fish ponds in any of the seasons except that individual density
was higher in fish ponds than in farmlands in winter and functional
diversity was higher in farmlands than in fish ponds in summer. In six
comparisons, however, diversity indices were higher in natural wet-
lands than in farmlands and fish ponds, respectively, and in eight and
seven comparisons, diversity indices were higher in restored wetlands
than in farmlands and fish ponds, respectively (Table 2).
Waterbird groups differed among the four major habitats. Dabbling
and diving birds were dominant in restored wetlands; small waders
were mainly recorded in natural wetlands; and large waders used
diverse wetland types (Figs. 2 and 3). Considering food types of water-
birds (Table S2), although species with different food types can be
recorded in diverse wetland types, Individual numbers largely differed
among wetland types: Waterbirds that eat inveterbrate food were
dominant in natural wetlands, herbivorous and omnivorous birds
were dominant in restored wetlands. Waterbirds that eat animal food
(including invertebrate, vertebrate, and both) were mainly recorded
in natural and restored wetlands. Fish ponds and farmlands were
mainly used by waterbirds that eat vertebrate and both invertebrate &
vertebrate food (Fig. 4).
In the same season, Jaccard coefficients of waterbird communities be-
tween wetland types were always <0.5 (Table 3), suggesting large differ-
ences in species composition. NMDS analysis further indicated that the
species composition of waterbird communities significantly differed
among wetland types in each season. There was no overlap in the 95%
confidence interval among wetland types, except for fish ponds and
farmlands in spring (Fig. 5). ANOSIM also indicated significant differences

35 25
30 Spring Summer
Species number

20
25
20 15
15 10
10
5 5
0 0
Dabbling Diving Small Large Dabbling Diving Small Large
birds birds waders waders birds birds waders waders

35 25
Autumn Winter
Species number

30
20
25
20 15
15 10
10
5 5
0 0
Dabbling Diving Small Large Dabbling Diving Small Large
birds birds waders waders birds birds waders waders

Natural wetlands Restored wetlands Fish ponds Paddy fields

Fig. 2. Number of species of different waterbird groups in four wetland types.

5
J. Fan, X. Wang, W. Wu et al. Science of the Total Environment xxx (xxxx) xxx

Spring Summer
100% 100%
80% 80%
60% 60%

Percentage of individual numbers

40% 40%
20% 20%
0% 0%
Dabbling Diving Small Large Dabbling Diving Small Large
birds birds waders waders birds birds waders waders

Autumn Winter
100% 100%
80% 80%
60% 60%
40% 40%
20% 20%
0% 0%
Dabbling Diving Small Large Dabbling Diving Small Large
birds birds waders waders birds birds waders waders

Natural wetlands Restored wetlands Fish ponds Paddy fields

Fig. 3. Percentage of total numbers of individuals represented by different waterbird groups in four seasons in four wetland types.

in the species composition of waterbird communities among wetland support waterbird communities with high diversities. In addition,
types (spring: R = 0.54, summer: R = 0.95, autumn: R = 0.78, winter: more than 50% of the total numbers of individuals of threatened species
R = 0.89, p < 0.001 for all). and more than 80% of the total numbers of individuals of exclusive spe-
cies occurred in restored wetlands. Because numbers of waterbirds
4. Discussion were very low before wetland restoration, i.e., when dense smooth
cordgrass dominated the region (Gan et al., 2009), our results clearly
Wetland restoration has been implemented in many countries show that wetland restoration greatly improved the habitat for water-
worldwide (Moreno-Mateos et al., 2012). In China, with the support birds. Waterbird communities, however, significantly differed among
of wetland conservation policy, a huge amount of funding has been wetland types. Conditions similar to those documented here for
invested in wetland restoration along the coast including the Yellow Chongming Dongtan might also exist in other restored wetlands along
Sea region (Cui et al., 2016; Stokstad, 2018). This study indicated that China's coast (Li et al., 2011).
at Chongming Dongtan, restored wetlands targeted bird conservation Hydrologic regimes strongly affect the ecological processes and bio-
logical communities of wetlands (Ma et al., 2010; Howard et al., 2017),
and thus establishing appropriate hydrologic conditions is critical for
45 wetland restoration (Warren et al., 2002). Affected by periodic tides, a
40 natural tideland creates special habitats (mud and sandy flats) and
Species number

35 foods (macrobenthos) that are suitable for shorebirds (Jing et al.,

30 2007). In this study, restored wetlands were constructed by enclosing
25 the smooth cordgrass-invaded tideland with a solid embankment and
20 thus were unaffected by periodic tides (Ma, 2017). The region consisted
15 of natural tidal wetlands before the invasion of smooth cordgrass, while
10 the tideland condition was greatly altered by the spread of smooth cord-
5 grass. The dense vegetation and roots of smooth cordgrass promoted
0 the deposition of sediment, resulting in a rapid elevation of the tidal
Invertebrate Vertebrate Invetebrate Omnivores Plant flats (Li et al., 2009a). As a consequence, even if the embankments are
& vertebrate removed, most of the restored wetlands would not be periodically sub-
Percentage of individual numbers

merged by tidewater. This suggests that it is difficult to restore tidal

100%
wetlands to the conditions that prevailed before invasion by smooth
80% cordgrass. Although the habitat requirements of different waterbirds in-
cluding shorebirds were considered in the construction of the restored
60% wetlands at Chongming Dongtan (Ma, 2017), the hydrologic conditions
of the natural tideland are unlikely to be restored because of the lack of a
40% tidal effect. This has resulted in large differences in habitat conditions

20%
Table 3
Jaccard similarity of waterbird species between wetland types in each season. Numbers at
0% the lower left indicate the coefficient for spring and summer, and numbers at the upper
Invertebrate Vertebrate Invertebrate Omnivores Plant right indicate the coefficient for autumn and winter.
& vertebrate
Natural wetland Restored wetland Farmland Fish pond
Natural wetlands Restored wetlands Fish ponds Farmlands
Natural wetland – 0.07/0.03 0.05/0.04 0.12/0/03
Restored wetland 0.43/0.29 – 0.06/0.11 0.15/0.11
Fig. 4. Species number and percentage of individual numbers of different waterbird
Farmland 0.34/0.20 0.43/0.38 – 0.11/0.14
groups (classified according to food types) in four wetland types. Data in the four
Fish pond 0.24/0.11 0.44/0.29 0.36/0.09 –
seasons were combined.

6
J. Fan, X. Wang, W. Wu et al.
1.0
A
0.0 0.5
MDS2
-0.5
-1.0
-1.5 -1.0 -0.5 0.0
1.0
C D
0.0 0.5
MDS2
-1.0 -0.5
-1.0 -0.5 0.0 0.5
MDS1
Fig. 5. Difference in waterbird community composition based on Bray-Curtis distance among wetland types in spring (A), summer (B), autumn (C), and winter (D). Green dots represent
natural wetlands, dark blue dots represent restored wetlands, orange dots represent farmlands, and red dots represent fish ponds. The ellipse represents the 95% confidence interval.
NMDS stress: 0.13 in spring, 0.13 in summer, 0.16 in autumn, and 0.19 in winter. (For interpretation of the references to colour in this figure legend, the reader is referred to the web
version of this article.)
between restored and natural wetlands at Chongming Dongtan
(Shanghai Chongming Dongtan National Nature Reserve, 2019). Consis-
tent with this finding, many studies have found that abiotic condi-
tions in restored wetlands are difficult to return to their natural
state even many decades after restoration (reviewed by Moreno-
Mateos et al., 2012).
Habitat conditions determine the characteristics of biological
communities. At Chongming Dongtan, the main habitat types differed
among waterbird groups. This is closely related to the habitat require-
ments of waterbirds and the conditions of wetland types (Ma et al.,
2009; Tavares et al., 2015). Small waders are mainly tideland specialists
that feed on macrobenthos (e.g., mollusks, crustaceans, polychaetes and
other invertebrates), which are abundant on tideland with shallow
water or moist soil (Jing et al., 2007). Dabbling and diving birds require
large open water areas, which can be found in restored wetlands. Large
waders at Chongming Dongtan are mainly egrets and herons; they are
habitat generalists, are less sensitive to human disturbance, and can
therefore use diverse wetland types including artificial ones (Ma et al.,
2009). Distribution of waterbird groups that use different food types
also indicated that habitat use was closely related to the food resources
in different wetland types.
Our results indicated that after 3 years of wetland restoration, water-
bird diversity was generally similar between the restored and natural
wetlands. This is consistent with previous findings that vertebrate di-
versity (in terms of richness and density) in restored wetlands recovers
in a short time (reviewed in Moreno-Mateos et al., 2012). However, spe-
cies composition of waterbird communities significantly differed be-
tween restored and natural wetlands in the current study. Differences
in habitat conditions and species composition between restored and
natural wetlands mean that restored wetlands have changed to alterna-
tive states, i.e., they have not returned to the states of natural wetlands
before degradation (Hobbs et al., 2009; Moreno-Mateos et al., 2012).
Science of the Total Environment xxx (xxxx) xxx
1.0
B
0.0 0.5
MDS2
-0.5
-1.0
0.5 -1.0 -0.5 0.0 0.5 1.0
0.5
MDS2
0.0
-0.5
1.0 -1.0 -0.5 0.0 0.5 1.0
MDS1
With a variety of habitat types, restored wetlands have attracted di-
verse waterbirds at Chongming Dongtan. All of the recorded birds exhib-
ited foraging activities in the restored wetland, which is consistent with
the fact that restored wetlands have abundant food resources for water-
birds with different feeding habits (Shanghai Chongming Dongtan
National Nature Reserve, 2019). Moreover, some waterbirds, such as
black-winged stilts, pied avocets, Kentish plovers, and common terns,
built nests and bred successfully on the islands in the restored wetland,
while no waterbird was recorded building nests on natural wetlands (J
Fan, per. Observ.). A possible explanation is that the islands in restored
wetlands are surrounded by water, so that they are inaccessible to ter-
restrial predators. Natural tidal wetlands, in contrast, are unsuitable for
nesting because the intertidal zone is frequently submerged by tidewa-
ter and the supratidal zone is accessible to terrestrial predators (Gan
et al., 2009; Wang et al., 2019). As a consequence, restored wetlands
have different functions than natural wetlands in supporting waterbird
communities.
Because different diversity indices emphasize different aspects
of community composition, comparing multiple diversity indices
is helpful for understanding overall differences among communi-
ties. In our comparison of five diversity indices (species richness
and abundance, Shannon-Wiener diversity, phylogenetic diversity,
and functional diversity) among wetland types, we found that wa-
terbird diversity was generally similar in the restored and natural
wetlands and that waterbird diversity was higher in the restored
and natural wetlands than in the two artificial wetlands. This indi-
cates that the restored wetlands provided high-quality habitats for
waterbirds. However, there were large differences in the waterbird
species among wetland types in the same season. Although diver-
sity indices are commonly considered in comparing biological
communities (e.g., O'Neal et al., 2008; Moreno-Mateos et al.,
2012; Sebastián-González and Green, 2016), our results suggest
7
J. Fan, X. Wang, W. Wu et al.
that species composition should also be considered when assessing
the effectiveness of habitat restoration.
Although bird diversity was relatively low in fish ponds and farm-
lands, more than 40% of total number of species were found in the
two artificial wetland types at Chongming Dongtan. The significant dif-
ference in the waterbird communities among the wetland types suggests
that the different habitats at Chongming Dongtan are complementary in
supporting diverse waterbirds. This is consistent with previous findings
that artificial wetlands mainly constructed for economic purposes can
also be used as alternative or supplementary habitats for waterbirds
(e.g., Elphick, 2000; Ma et al., 2004; Green et al., 2015; Jackson et al.,
2020). At Chongming Dongtan, some production activities facilitate wa-
terbird foraging in artificial habitats. For example, the water level in fish
ponds is usually lowered in autumn or winter to facilitate harvest. By
concentrating fish and other prey in low-lying areas, the lowering of
the water level can increase the foraging efficiency of waders (Taft
et al., 2002; Ma et al., 2010) and can thus attract egrets and other waders
to the fish ponds. The moist-soil substrate after harvest also attracts
shorebirds for foraging in fish ponds (Ma et al., 2004; Choi et al., 2014).
However, the area of fish ponds in the study area was smaller than that
of other wetland types. This might be related to the less species and indi-
vidual numbers in fish ponds. Historically, there were large areas of fish
ponds at Chongming Dongtan, supporting high diversity and number of
waterbirds (Ma et al., 2004). The species and individual density of water-
birds in large-sized ponds were higher than those in small-sized ponds
(Hua et al., 2009).
The ploughing of farmlands at planting times exposes some soil inver-
tebrates, which attracts the Eastern cattle egret (Bubulcus coramandus),
whimbrels (Numenius phaeopus), and other insectivorous birds (Kuang
et al., 2019; Xie et al., 2019). Moreover, grain left in farmlands after har-
vest is an important food for waterbirds in winter (Miller et al., 2010). Be-
cause some waterbirds forage in artificial wetlands at night when human
disturbance is low (Márquez-Ferrando et al., 2014), our daytime surveys
may have underestimated the use of artificial wetlands by waterbirds.
Most shorebirds forage on tidelands but require a roosting site
nearby during high tide when tidelands are submerged (Jackson et al.,
2019). A recent study found that many artificial wetlands along
China's coasts are used by shorebirds as roosting sites during high tide
when tidelands are unavailable (Jackson et al., 2020). However, we
did not find significant differences in waterbird density in restored or
artificial wetlands between low tide and high tide periods, suggesting
that these wetlands were not used as major roosting sites during high
tide by shorebirds. This is probably because shorebirds can use the
supratidal zone, which is not submerged by tidewater during high
tide, as a roosting site at Chongming Dongtan. Over the past several de-
cades, however, the supratidal zone has disappeared as the result of rec-
lamation in most other regions along China's coast; as a result,
shorebirds in these other regions readily use nearby artificial wetlands
as roosting sites during high tide (Jackson et al., 2020).
The differences in the species composition of waterbird communi-
ties among wetland types suggest that an integrated landscape with
multiple wetland types can meet the habitat requirements of various
waterbirds and thus support high diversity. The relatively low bird di-
versity in the two artificial wetland types at Chongming Dongtan
might be due to our conducting this study in a nature reserve, where
waterbirds could use well-protected natural wetlands and well-
managed restored wetlands. In the regions that lack high quality natural
and restored wetlands, artificial wetlands likely provide important al-
ternative or supplementary habitats for waterbirds and other wildlife
(Jackson et al., 2020), besides their contribution to economic prosperity
and social well-being (Maltby, 2006).
Our results indicate that restored wetlands enclosed by solid em-
bankments can support high waterbird diversity but have limited func-
tion in supporting shorebirds, because wetlands enclosed by solid
embankments lack periodic tides. For former low-elevation tidelands
that have been recently enclosed by embankments, de-embankment
8
Science of the Total Environment xxx (xxxx) xxx
should be effective in restoring natural tides. De-embankment has
often been successfully used to restore tidal wetlands in Europe
(Wolters et al., 2005) and North America (Warren et al., 2002), but tide-
land restoration by de-embankment has yet to occur along China's
coast. Because a huge area of tideland has disappeared over the past
several decades due to excessive reclamation along China's coast (Ma
et al., 2014), de-embankment will be an important way to restore tide-
lands and to thereby provide habitat for shorebirds. Still, protection of
natural wetlands remains the best way to provide habitat for waterbirds
in general and shorebirds in particular.
5. Conclusion
Wetland restoration is an important conservation measure for wa-
terbirds that have suffered habitat loss and degradation worldwide.
This study revealed that at Chongming Dongtan, waterbird diversity in
restored wetlands was generally similar to that in natural wetlands,
and was higher than that in artificial wetlands (fish ponds and
farmlands). Moreover, many threatened species and exclusive species
occurred in restored wetlands. This is largely due to that diverse config-
uration (vegetation, waterbody, islands, and shoals) and water manage-
ment targeted to the habitat requirement of various waterbirds can
increase local waterbird diversity, which can be referred to in other wet-
land restoration projects for waterbird conservation.
Our results indicate that restored wetlands have important functions
in providing habitats for many waterbirds but cannot replace natural
wetlands for waterbird conservation. Considering the huge investment
required for wetland restoration, protecting existing natural tidelands is
cost-effective and should be the first consideration in waterbird conser-
vation. Because there are large differences in wetland conditions and
local bird communities among regions, regional comparison on habitat
use of waterbirds among wetland types can increase our understanding
on the function of wetland restoration for waterbird conservation.
CRediT authorship contribution statement
Jun Fan: Investigation, Formal analysis, Writing - original draft.
Xiaodan Wang: Formal analysis, Writing - review & editing. Wei Wu:
Investigation, Resources. Weipin Chen: Investigation, Resources. Qiang
Ma: Investigation, Resources. Zhijun Ma: Supervision, Conceptualiza-
tion, Methodology, Writing - review & editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
This study was financially supported by the National Key Research
and Development Program of China (2018YFC1406402) and the Na-
tional Natural Science Foundation of China (31830089 and 31772467).
We thank the Chongming Dongtan National Nature Reserve and World
Wide Fund for Nature Beijing Office for their assistance during the field-
work. We thank Kun Tan, Fenliang Kuang, and Wanjuan Ke for their ad-
vice on experimental design, data analysis, and paper writing, and
Binbin Zhu, Hengchi Chen, Xuesong Feng, Wenjie Xue, Jieyun Liu, Esther
Li, Katherine Leung, and Xuelian Shi for their assistance in field surveys.
We would like to thank Bruce Jaffee for English language editing.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2020.144061.
J. Fan, X. Wang, W. Wu et al.
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