Environmental Management

, Volume 43, Issue 6, pp 1187–1200

Waterbird Population Changes in the Wetlands at Chongming Dongtan in the Yangtze River Estuary, China

Authors

    • Coastal Ecosystems Research Station of Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science Fudan University
    • School of Life SciencesFudan University
  • Yong Wang
    • Coastal Ecosystems Research Station of Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science Fudan University
    • Center for Forestry, Ecology and Wildlife Alabama A&M University
    • College of Life SciencesBeijing Normal University
  • Xiaojing Gan
    • Coastal Ecosystems Research Station of Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science Fudan University
  • Bo Li
    • Coastal Ecosystems Research Station of Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science Fudan University
  • Yinting Cai
    • Coastal Ecosystems Research Station of Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science Fudan University
  • Jiakuan Chen
    • Coastal Ecosystems Research Station of Yangtze River Estuary, Ministry of Education Key Laboratory for Biodiversity Science and Ecological Engineering, Institute of Biodiversity Science Fudan University
Article

DOI: 10.1007/s00267-008-9247-7

Cite this article as:
Ma, Z., Wang, Y., Gan, X. et al. Environmental Management (2009) 43: 1187. doi:10.1007/s00267-008-9247-7

Abstract

We studied the changes in wetland habitats and waterbird communities between the 1980s and the 2000s at Chongming Dongtan, a Ramsar site in the Yangtze River estuary, an ecologically important region. This region is an important stopover site for shorebirds along the East Asian–Australasian flyway and is extensively used by waterfowl. A net loss of 11% of the wetland area was estimated during study periods at Chongming Dongtan. The change was dependent on wetland types: while the area of artificial habitats such as paddy fields and aquacultural ponds more than doubled, more than 65% of natural habitats including sea bulrush (Scirpus mariqueter) and common reed (Phragmites australis) marshes were lost over the two decades. An exotic plant species introduced from North America, smooth cordgrass (Spartina alterniflora), occupied 30% of the vegetated intertidal zone by the 2000s. Although waterbird species richness did not change between the 1980s (110) and the 2000s (111), 13 species found in 1980s were replaced by 14 newly recorded species. Moreover, there were more species with declining trends (58) than with increasing trends (19). The population trends of species were affected by residential status and habitat types. Transients, wintering migrants, and habitat specialists were more likely to show declining trends compared to those breeding at Dongtan (including year-round and summer residents) and habitat generalists. Furthermore, species associated mainly with natural wetlands were more likely to decline than those associated mainly with artificial wetlands. These patterns suggest that the loss and change of wetland habitats at Chongming Dongtan adversely affected local population dynamics and might have contributed to the global decline of some waterbird species. Because Chongming Dongtan provides stopover and wintering habitats for many migratory waterbirds, protection and restoration of natural wetlands at Chongming Dongtan are urgently needed.

Keywords

Chongming DongtanCoastal wetlandsHabitat usePopulation trendsWaterbirdsWetlands

Introduction

Coastal wetlands are important breeding, stopover, and wintering habitats for waterbirds. With nearly half of the world’s human population living in coastal regions, coastal wetlands are under great pressure from anthropogenic impacts (Adam 2002). Over the past century, loss and degradation of coastal wetlands have been a common phenomenon globally, and have had detrimental effects on waterbirds during all stages of their life cycles (Schekkerman and others 1994; Weber and others 1999; Erwin and others 2003).

The coastal wetlands in China provide habitats for more than 200 waterbird species, including millions of migratory shorebirds along the East Asian-Australasian Flyway and hundreds of thousands of wintering waterfowl (China Forestry Bureau 2000; Barter 2002). Unfortunately, to meet the needs for land resources for economic development, the coastal wetlands in China have been lost or degraded considerably. From the 1960s to the 1990s, a total of 2.19 × 106 ha, or 50%, of coastal wetlands was enclosed by the construction of seawalls and used for agricultural or industrial purposes (China Forestry Bureau 2000). Anthropogenic activities in wetlands and surrounding areas have also had a negative impact on waterbirds and their habitats. Over the past decades, there has been a rapid spread of the exotic plant, smooth cordgrass (Spartina alterniflora), on tidal flats, which has changed the composition of plant communities and landscapes of coastal wetlands in eastern China (Wang 2007). However, the effects of these habitat changes on the waterbird communities in coastal wetlands of China are largely unknown.

Studies of avian community dynamics in response to habitat changes in terrestrial landscapes have shown that mixed responses to anthropogenic changes are species dependent (Boulinier and others 1998; Chamberlain and others 2000; Lindsay and others 2002) and are also affected by avian guild composition and structure (Cueto and de Casenave 2000). Waterbirds are key indicators of the quality and importance of wetlands (Erwin and Custer 2000; Wetlands International 2006). However, most studies of wetland habitat changes and waterbird responses are based largely on population status and modeling (e.g., Goss-Custard and others 1994, 2002; Sutherland 1996; Burton and others 2006). The spatiotemporal dynamics of waterbird communities in relation to habitat changes influenced by urbanization and economic development remains largely unexplored.

We here examine wetland habitat changes and waterbird species richness and population trends associated with these habitats at Chongming Dongtan (hereafter Dongtan) in the Yangtze River estuary of eastern China between the 1980s and the 2000s. The area is a Ramsar site which is used extensively by waterbirds (Xu and Zhao 2005). The Yangtze River delta is one of the most important economic zones in China and Asia. It accounts for 1% of the land mass of China but holds 6% of the human population in China and produces 20% of China’s GDP (National Bureau of Statistics of China 2003). To meet the increasing demands for land to support economical development and rapid urbanization, coastal wetlands in the Yangtze estuary have been converted. For example, about 84,300 ha of coastal wetlands near Shanghai has been transformed for agricultural purposes during the past half-century (Xie 2004), which altered coastal wetland landscapes of the estuary (Ma and others 2004; Xie 2004).

We studied the changes in wetland habitats and waterbird communities between the 1980s and the 2000s at Dongtan in the Yangtze River estuary. Our specific objectives were to examine (1) the changes in wetland area and types, (2) the changes in waterbird community composition and population trends, and (3) the factors that contributed to the changes in waterbird populations at Dongtan. It is hoped that this study will increase the current understanding of the effects of wetland habitat changes on waterbird communities and provide insights into and suggestions for the conservation of waterbirds and their associated habitats in the Yangtze River estuary, China.

Methods

Study Area

Dongtan (31°25′–31°38′N, 121°50′–122°05′E; Fig. 1) is located at the east end of Chongming Island in the Yangtze River estuary (Fig. 1) and encompasses a total area of 32,600 ha (Fig. 1). Sediment input from the Yangtze River results in continuous growth of the intertidal zones (Xu and Zhao 2005). However, converting the intertidal zones to agricultural (e.g., farmlands and vegetable fields) and aquacultural (e.g., fish and crab ponds) systems has taken place at a rate faster than that of natural formation. More than 15,000 ha of intertidal zones has been developed at Dongtan over the past half-century. Most of the area reclaimed before the 1990s is currently being used as farmlands, vegetable gardens, orchards, and nursery gardens, while the area reclaimed since then has mainly been transformed into aquacultural ponds (Ma 2006).
https://static-content.springer.com/image/art%3A10.1007%2Fs00267-008-9247-7/MediaObjects/267_2008_9247_Fig1_HTML.gif
Fig. 1

Map of Chongming Dongtan with insets showing its location on Chongming Island in the Yangtze River estuary. The dikes were constructed for the development of the intertidal zones during the past four decades

Dongtan encompasses both natural estuarine wetlands outside dikes and artificial wetlands inside. The natural wetlands include the intertidal zones (between the mean high-water and the mean low-water marks) and coastal shallow-water zones (below the mean low-water marks). The artificial wetlands include aquacultural ponds and paddy fields. The dominant native plants in the intertidal zones include common reed (Phragmites australis) and sea bulrush (Scirpus mariqueter) (Xu and Zhao 2005). Smooth cordgrass (Spartina alterniflora), originating from North American, was introduced at Dongtan in the middle 1990s and has spread rapidly in intertidal zones in the past decades (Wang 2007).

Dongtan is an important stopover site for at least 250,000 shorebirds annually for replenishing energy stores and avoiding unfavorable weather conditions (Barter 2002). Dongtan is also an important wintering site for waterbirds (Xu and Zhao 2005). Because of its importance in waterbird conservation, Dongtan was recognized as a Ramsar site in 2002, and designated a national nature reserve in 2005. Historically, bird hunting (especially for shorebirds and waterfowl) was common at Dongtan. It was estimated that tens of thousands waterbirds were killed annually in the 1990s (Xie 2004). After establishment of the reserve, strict protection measures for waterbirds were taken at Dongtan. Hunting for birds has been strictly banned in recent years. However, there are still human activities, such as eel fry harvesting, buffalo grazing, and shellfish collecting, in the intertidal zones of the reserve (Xu and Zhao 2005).

Wetland Classification

Dongtan wetlands were classified using the Landsat Thematic Mapper (TM) image of January 1988 and the Landsat Enhanced Thematic Mapper (ETM) image of November 2002. The 2002 ETM image was georeferenced to a digital topographic map of Dongtan (Universal Transverse Mercator [UTM] coordinate system) using prominent features visible on the image. The 1998 TM image was rectified and resampled using the 2002 ETM image. An average error (root mean square) of <0.5 m was achieved for both images, and the pixel size was kept at 30 × 30 m.

According to field surveys and interviews of local farmers, we identified seven wetland categories at Dongtan, including aquacultural ponds, paddy fields, reed zone, sea bulrush zone, smooth cordgrass zone, bare intertidal zone, and coastal shallow-water zone, in the 1980s and 2000s. We adopted a combination of unsupervised and supervised classification to group the Landsat data into the seven land use categories based on expert knowledge. Thirty training locations identified using Global Position Systems (GPS) were collected in different land use types (three to six locations in each) for ground truth of the Landsat images. The classification accuracies were >90% according to resampling of known habitats (>30 locations) to test the model. All classifications were conducted using IDRISI software (Eastman 1997).

Waterbird Surveys

To assess the waterbird community of the 1980s, we used reported data from two comprehensive waterbird surveys conducted at Dongtan between October 1986 and December 1989 (Huang and others 1993) and between September 1986 and December 1988 (Zhang and Yuan 1989). Both studies conducted surveys once every 1–2 months in summer and winter, and at about 10-day intervals in spring and autumn, to capture the migration peak (the coastal shallow-water zone was investigated once every season); each survey lasted 3–5 days. For intertidal zones, the investigators (two to four persons) counted waterbirds by walking over the intertidal zones at low tide (the tidal difference was about 0.3–4.5 m at spring tide and 1.5–2.2 m at neap tide) using 10 × 42 binoculars and 20–60 × spotting scopes. Surveys on water areas were conducted by boat. More than 20 surveys were conducted during the study periods. Species were classified into four abundance categories according to their maximum number of individuals: abundant (>1000 birds), common (100–1000 birds), rare (<100 birds), and absent (Huang and others 1993). Unfortunately, we could not obtain the raw data for these two studies.

We resurveyed waterbirds between February 2001 and December 2004 in the same areas as in the 1980s bird surveys, including areas that had been converted to other uses. We used the same protocol as in the 1980s surveys. A total of 26 surveys were conducted during this period. For each bird encounter, we recorded the species, abundance, and wetland type the birds used. For areas that were wetlands in 1980 but were converted after the 1980s, we rode a bicycle along fixed routes and stopped to record data when waterbirds were encountered.

Statistical Analyses

We classified bird species into four residential status classes based on the time of year that the birds used the site (Xu and Zhao 2005): transients that occurred only during migration seasons (mid-March to mid-May and early August to late October), summer breeders during the summer breeding season (mid-May to late July), winter migrants that used the site during winter (early November to mid-March), and residents. Based on their major habitats at Dongtan in the 2000s, the species were also classified into three groups, including species associated mainly with habitats in natural wetlands (with more than two thirds of individuals recorded in coastal wetlands), species associated mainly with habitats in artificial wetlands (with more than two-thirds of individuals recorded in artificial wetlands), and species with major habitats in both natural and artificial wetlands (with more than one-third of the individuals in both natural and artificial wetlands) (Appendix). Based on the surveys of 2000s, a habitat diversity index (HDI) was calculated for each bird species as
$$ HDI = - \sum\limits_{i = 1}^{s} {p_{i} \log_{e} p_i} $$
where pi is the proportion of individuals of a species that occurred in the ith habitat, and s is the total number of habitat types. The minimum HDI value of 0 is obtained when a bird species occupies only a single habitat type (habitat specialist) and the value increases as the number of habitat types and evenness of the distribution across habitats increase (habitat generalist). Estimation of habitat association for rare species is not always representative, and thus HDI was calculated only for bird species that were recorded more than three times during field surveys in the 2000s. The HDI calculated in this study only assessed the habitat associations of each waterbird species at Dongtan because habitat availability and composition might vary among study sites across the distribution range.

We used the maximum observed number of birds of a given species during the study as an abundance index. The maximum observed number is a better estimation of species abundance, particularly during nonbreeding seasons, when the number of birds varied considerably among repeated surveys (Goss-Custard and others 2002). Waterbirds recorded in the 2000s were classified into four abundance categories (abundant, common, rare, and absent) according to their maximum observed numbers in the same way as in the 1980s study. The abundance categories (abundant, common, rare, and absent) were transformed to classes 3, 2, 1, and 0, respectively. The transformed abundance classes approximated the log function. Change in abundance was calculated as the abundance class in the 2000s minus the abundance class in the 1980s. The negative, zero, and positive values indicated declining, relatively stable, and increasing population trends, respectively. We used chi-square to test the hypothesis that the distribution of species among abundance classes was not different between the two study periods. The HDI values among different waterbird groups were compared using analysis of variance (ANOVA), followed by Tukey multiple comparisons if the ANOVA was significant.

To investigate the relative importance of habitat type, residential status, and HDI to the bird population trends, we performed logistic regression analyses (Hosmer and Lemeshow 2000) with population change (decline or increase) as the dependent variables and major habitat type, residential status, and HDI as the independent variables. Probability (p) of population decline or increase was calculated as
$$ p = e^{{(\beta_{0} + \beta_{1} x_{1} + \beta_{2} x_{2} + \ldots \beta_{k} x_{k} )}} \left( {1 + e^{{(\beta_{0} + \beta_{1} x_{1} + \beta_{2} x_{2} + \ldots \beta_{k} x_{k} )}} } \right)^{ - 1} $$
where e = 2.718, and βi is the regression coefficient for independent variable xi. Akaike’s Information Criterion (AIC) (Burnham and Anderson 2004) was used to select the best-fit model. We used the second-order bias correction (AICc) because sample size and variable ratio are <40 for most models:
$$ AIC_{c} = - 2\ln (L) + 2Kn(n - K - 1)^{ - 1} $$
where ln(L) is the log-likelihood derived from binary logistic regression analyses, K is the number of parameters in the model including the slope (Burnham and Anderson 2004), and n is the sample size. AICc scores were then rescaled to remove constants following
$$ \Updelta {\text{AIC}}_{i} = \,{\text{AIC}}_{i} - {\text{AIC}}_{min } $$
where AICi is the AIC value for model i, and AICmin is the AIC value from the model with the lowest value. This transforms the ∆AICi of the best model to 0. Generally, models with ∆i  ≤ 2.0 imply substantial support (Burnham and Anderson 2004). Evidence ratios, or the likelihood that model i is better than model j, was adjusted to Akaike weights (wi) using
$$ w_{i} = \exp ( - 0. 5\Updelta_{i} ) \left(\sum\limits_{i = 1}^{R} {\exp ( - 0. 5\Updelta_{i} )} \right)^{ - 1} $$
where R is the total number of models included for comparison. This ‘weight of evidence’ displays a model’s strength as a probability with the highest ratio equating to the best-fit model (Burnham and Anderson 2004). A significant level (α) of 0.05 was used for all statistical tests and results are reported as mean ± SD. All analyses were performed using SPSS 12.0 (SPSS 2003).

Results

Wetland Structure

Total area of wetlands declined from 41,310 to 36,660 ha from 1988 to 2002 at Dongtan, with the 11% loss mostly attributable to agricultural uses (dry farmland, vegetable gardens, etc.). Although the area of artificial wetlands (aquaculture ponds and paddy fields) more than doubled and the area of the coastal shallow-water zone remained basically constant, nearly 50% of the intertidal zones were lost during the study period. In the 1980s, the dominant plants in the intertidal zones were common reed and sea bulrush, which covered 4870 and 4670 ha, respectively. With the development of the intertidal zones and the spread of smooth cordgrass, more than two-thirds of these habitats were lost by the 2000s. Smooth cordgrass now accounts for approximately 30% of the vegetated area of the intertidal zones (Table 1).
Table 1

Area (thousands of hectares) of wetland habitats for waterbirds at Chongming Dongtan in 1988 and 2002

Wetland category

1988

2002

Change in area

%Change

Intertidal zones

22.20

11.86

−10.34

−46.6

    Sea bulrush habitat

4.67

1.50

−3.17

−67.8

    Common reed habitat

4.87

1.14

−3.73

−76.5

    Smooth cordgrass habitat

0

1.14

+1.14

    Bare intertidal zone

12.66

8.08

−4.58

−36.2

Aquaculture ponds

1.14

3.29

+2.15

+188.6

Farmland (paddy fields)

3.47

7.01

+3.54

+102.0

Coastal shallow-water zone

14.50

14.50

0

0

Total

41.31

36.66

−4.65

−11.3

Waterbird Communities and Population Trends

A total of 124 waterbird species were recorded during the 1980s and 2000s surveys (Appendix). Although a similar number of species was found in the 1980s (110 species) and 2000s (111 species), 13 species found during the 1980s were replaced by 14 newly recorded species during the 2000s. The locally missing species included winter migrants (9 species) and transients (4 species), and the newly occurring species included summer breeders (5 species), transients (5 species), and winter migrants (4 species; Appendix). Of the 124 waterbird species, transients (52 species) and winter migrants (54 species) accounted for 86% of all species. Transients and winter migrants were also dominant taxa, as all of the abundant species recorded in both the 1980s and the 2000s were transients or winter migrants except for little egret (Egretta garzetta) (Table 2).
Table 2

Numbers of waterbird species in abundant, common, and rare abundance classes at Chongming Dongtan in the 1980s and 2000s, which were classified according to their residential status, and percentage species numbers with increasing (PI) and decreasing (PD) population trends in each residential status

Residential status

Abundant

Common

Rare

Total species

PI (%)

PD (%)

1980s

2000s

1980s

2000s

1980s

2000s

1980s

2000s

Residents

0

1

6

4

0

1

6

6

16.7

16.7

Summer breeders

0

0

3

1

4

11

7

12

50.0

25.0

Winter migrants

14

5

21

13

15

27

50

45

9.3

55.6

Transients

8

3

27

16

12

29

47

48

13.5

48.1

Total

22

9

57

34

31

68

110

111

15.3

47.6

Note: See the Appendix for the change in abundance classes of each species

In the 1980s, 22, 57, and 31 waterbird species were classified as abundant, common, and rare, respectively; and these numbers were changed to 9, 34, and 68, respectively, in the 2000s (χ2 = 25.1, df = 2, P < 0.001) (Table 2). The changes amounted to a 50% reduction in the number of species that were in the abundant and common classes and a 100% increase in the number of species in the rare class.

Population trends between the two study periods appeared to be species-specific. Fifty-nine species (48% of the total species) showed declining trends (negative change) in abundance, 19 species (15% of the total species) showed increasing trends (positive change), and the remaining species were stable (Fig. 2). Population trends (increasing, deceasing, and stable) were also affected by resident status (χ2 = 16.0, df = 6, P < 0.05). Proportionally, winter migrants and transients were more likely to decline (56% and 48%, respectively), while 50% of the 12 summer breeder species increased (Table 2).
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Fig. 2

Number of waterbird species in different abundance change classes at Chongming Dongtan. Abundance change classes were calculated based on the difference between the abundance categories—abundant (3), common (2), rare (1), and not detected (0)—between the 2000s and the 1980s surveys. The negative, zero, and positive values indicate declining, relative stable, and increasing population trends, respectively

Of the 111 species recorded in the 2000s, most species were found in the sea bulrush zones (69 species; 62% of the total), followed by the aquacultural ponds (64 species; 58%) and bare intertidal zone (51 species; 46%). Fewer species were recorded in the coastal shallow-water zone (30 species; 27%), common reed zone (26 species; 23%), paddy fields (15 species; 14%), and smooth cordgrass zone (13 species; 12%). Meanwhile, 90 species (81%) were recorded in natural wetlands (intertidal zones and coastal shallow water area), and 66 (59%) in artificial wetlands (aquacultural ponds and paddy fields). Forty-five (41%) and 21 (19%) species were found exclusively in natural and artificial wetlands, respectively. Population trends were significantly affected by habitat categories (χ2 = 13.4, df = 4, P < 0.01), and species with artificial or natural wetlands as their major habitats were more likely to decrease in abundance than those in both artificial and natural wetlands (Fig. 3).
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Fig. 3

Percentage of waterbird species with natural wetlands (filled bar), artificial wetlands (open bar), and both artificial and natural wetlands (dotted bar) as their major habitats, which were classified according to their population trends at Chongming Dongtan between the 1980s and the 2000s. Numbers in parentheses are the total numbers of species with declining, stable, and increasing trends

Among the 124 waterbird species, 12 species were listed as threatened by BirdLife International, of which 4 species were endangered and 8 vulnerable (Appendix). Compared with the 1980s, four threatened species (swan goose [Anser caerulescens], Baikal teal [Anas formosa], Baer’s pochard [Aythya baeri], and Saunders’ gull [Larus saundersi]) showed decreasing trends, while Chinese egret (Egretta eulophotes) set a new record (rare species) in the 2000s. Ten of the 12 threatened species (all except for Baikal teal and Baer’s pochard) were recorded in natural wetlands and 4 (black-faced spoonbill [platalea minor], Baikal teal, Baer’s pochard, and hooded crane [Grus monacha]) were recorded in artificial wetlands.

Determinants of Waterbird Population Trends

A total of 91 bird species were recorded more than three times during the 2000s surveys and the average HDI of these species was 0.79 ± 0.64. There was a significant difference in HDI among bird groups with increasing, decreasing, and stable population trends (ANOVA, F2,88 = 7.4, P = 0.001). Post hoc comparisons indicated that the HDI of species with decreasing trends (0.55 ± 0.54; n = 40) was significantly lower than that of species with relatively stable (0.90 ± 0.67; n = 40) or increasing (1.27 ± 0.53; n = 11) trends, while the difference between the latter two was not significant. This indicates that the species which were found to have declined most were those with relatively specialized habitat requirements.

Among the residential status groups, residents and summer breeders tended to have higher HDIs (1.59 ± 0.95 [n = 6] and 1.00 ± 0.48 [n = 9], respectively) and increasing population trends (50% species showed increasing population trends), while winter migrants and transients had lower HDIs (0.55 ± 0.61 [n = 38] and 0.85 ± 0.52 [n = 38], respectively), which were unlikely to show increasing trends (14% and 18% showed increasing population trends, respectively).

Logistic regression analyses showed that the model with HDI and habitat type as the predictors was the best among the six a priori selected models (Table 3). This model accounted for 49% of the variation in population trends (Nagelkerke R2 = 0.49, χ2 = 19.4, P < 0.001). The overall predictive accuracy was 86%, with 95% and 55% being declining and increasing species, respectively. These results suggested that species with lower HDIs were more likely to show a decreasing trend. Moreover, population trends also depended on the major habitat types: species with both natural and artificial wetlands as their major habitats were more likely to increase in abundance than species in only natural or artificial wetlands; and those with natural wetlands as their major habitats were more likely to decrease in abundance than species with artificial wetlands as their major habitats, even with the same HDI (Fig. 4).
Table 3

Assessment of logistic regression models for estimating the relationship between waterbird population trends (decline or increase) and major habitat types (HT), residential status (RS), and habitat diversity index (HDI) of waterbirds at Chongming Dongtan, China

Model(s)

L

K

AICc

∆AICc

Wi

HDI, HT

33.77

4

42.64

0

0.58

HDI

39.57

2

43.82

1.19

0.32

HT

40.42

3

46.93

4.30

0.07

RS, HDI

38.63

5

49.97

7.33

0.01

HT, RS, HDI

33.55

7

50.15

7.52

0.01

HT, RS

39.86

6

53.77

11.13

0.00

Note: Models were ranked by the second-order Akaike’s information criterion (AICc). L is the likelihood value from the logistic regression analysis. K is the number of parameters used. AICc\( - 2\ln (L) + 2Kn(n - K - 1)^{ - 1}, \) where n is the sample size. ∆AICc = AICc − the lowest AICc value. Wi (Akaike weights) \( = \exp ( - 0. 5\Updelta_{i} )(\sum\limits_{i = 1}^{R} {\exp ( - 0. 5\Updelta_{i} )} )^{ - 1}, \) where R is the number of models being evaluated

https://static-content.springer.com/image/art%3A10.1007%2Fs00267-008-9247-7/MediaObjects/267_2008_9247_Fig4_HTML.gif
Fig. 4

Relationships between waterbird habitat characteristic (habitat diversity index and major habitat types) and probability of population increase at Chongming Dongtan between the 1980s and the 2000s based on logistic regression analysis

Discussion

The wetlands at Dongtan have undergone considerable change over the last two decades, with substantial loss of natural wetlands overrunning the creation of artificial wetlands. Simultaneously, the spread of invasive smooth cordgrass has largely changed the vegetated habitats in the intertidal zones. Comparison of the species composition and abundance of waterbird communities during the study periods showed that there were more abundance-declining species than abundance-increasing ones, suggesting that waterbird abundance has decreased markedly at Dongtan over the past two decades. The population trends of waterbirds were also species-specific. In general, habitat specialists, migrants, and species with natural wetlands as their major habitats were more likely to show declining trends than habitat generalists, local breeders (residents and summer breeders), and species with artificial wetlands as their major habitats.

Although several studies have found that the estimates of bird abundance can be influenced by observer differences (Morin and Conant 1994; Sauer and others 1994), others have found this effect to be minor relative to among-site or interannual variation (Smith 1984). In this study, the absence of quantitative data on waterbirds of the 1980s precluded detailed analysis of abundance change of each species during the study periods. However, the analysis based on the changes in abundance helped to detect major changes and avoid minor changes resulting from observer-related variation. Moreover, our results are consistent with other independent studies on the population dynamics of some waterbird species at Dongtan, such as the declining abundance of whistling swan, Baikal teal, and mallard and the increasing abundance of little egret and cattle egret (Xie 2004; Xu and Zhao 2005). Therefore, the methodology- or observer-related biases are relatively limited relative to the magnitude of actual changes in bird abundance during study periods.

Relationship Between Wetland Habitat Change and Waterbird Population Trends

Several factors might have contributed to the population trends of waterbirds at Dongtan. One such factor suggested by this study is the dramatic change in area and types of wetlands at Dongtan. Such reduction and change of habitats could result in the variation in waterbird communities as suggested by other long-term studies of avian population trends (e.g., Kingsford and Thomas 2004; Rendon and others 2008).

Our results show that 81% of the waterbird species inhabited natural wetlands, including 62% in sea bulrush and 46% in bare intertidal zones. Former studies have shown that the sea bulrush habitats were foraging sites of waterbirds, especially those depending on seeds and corms of sea bulrush as major food, such as herbivorous ducks and cranes (Yu and others 1995; Ma and others 2003). The bare intertidal zone was largely used as a foraging site by shorebirds during migration (Jing and others 2007). The decline in area of the sea bulrush and bare intertidal zones might imply a reduction in foraging sites for most waterbird species at Dongtan, which could have contributed to the general decline in abundance of many waterbird species during the study periods.

The smooth cordgrass marsh at Dongtan is typically composed of tall and dense cordgrass monocultures, which might make birds’ foraging and predator detection difficult (Ma 2006; Wang 2007). Our results showed that the smooth cordgrass zone could be used by only a very few waterbird species at Dongtan. Studies in San Francisco Bay have shown that the replacement of native habitats by exotic smooth cordgrass is disadvantageous to local bird communities due to the loss of key trophic supports (Levin and others 2006). Since smooth cordgrass can outcompete the native sea bulrush and spread in all types of intertidal zones (Wang 2007), the establishment and expansion of smooth cordgrass greatly threaten the habitats of bird communities in natural wetlands.

Over recent decades, the profits associated with economic consumptive activities such as eel fry harvesting, buffalo grazing, and shellfish collecting have encouraged local people to be engaged in these activities in the intertidal and coastal shallow-water zones. For example, the number of boats and shacks in the coastal shallow-water zones increased from several dozens in the 1980s to about 1000 in recent years, primarily from December through the following April each year (Xie 2004). The coastal shallow-water zones have been the roosting sites of wintering waterfowl including thousands of whistling swans (Yu and others 1995). The potential effects of such activities on waterbirds were illustrated by the decline in wintering whistling swans from 3000 to 3500 individuals annually in the 1980s (Huang and others 1993) to fewer than 10 in the 2000s at Dongtan. Although the area of coastal shallow-water zones has been relatively stable during the past two decades, intensive human disturbance in those zones might have led some birds to shift their habitat use from the coastal shallow-water zones to aquacultural ponds (Ma 2006).

Our results indicate that habitat specialists were more likely to decline in population size than habitat generalists at Dongtan during the study periods. This suggests that habitat specialists are more sensitive to the loss and change of wetland habitats, while habitat generalists might adjust their habitat use and emigrate from degraded or unusable habitats. This pattern has also been observed in other animal taxa, with resource specialists being more sensitive to being adversely affected by environmental changes than resource generalists (e.g., reptiles [Waldron and others 2006], fish [Feary 2007], and insects [Franzen and Johannesson 2007]).

Many studies have shown that artificial wetlands can provide wintering, stopover, and even breeding habitats for waterbirds (e.g., Sanchez-Guzman and others 2007; Yasue and others 2007; Rendon and others 2008). The artificial aquacultural ponds at Dongtan have become important habitats for waterbirds, supporting about 60% waterbird species in the 2000s. However, recent studies have shown that aquacultural ponds are only roosting habitats for most waterfowl, the major waterbird groups there. A majority of waterbirds still depend on the bare intertidal and sea bulrush habitats for food (Ma and others 2004; Ma 2006). Consequently, artificial wetlands may be able to compensate only partially for the loss of natural coastal wetlands at Dongtan. Their function in supporting waterbirds might differ greatly from that of natural wetlands.

Species richness is a state variable for ecosystems and is largely used in management and conservation efforts (Nichols and others 1998). However, Sax and Gaines (2003) indicate that species richness can remain stable or even increase along with the loss and degradation of habitats at local and regional scales. Our results show that the species richness of waterbirds has been stable at Dongtan over the last two decades, though dramatic change and loss of wetland habitats have occurred. We recommend that more ecological parameters, such as species composition, species abundance, and guild structure and dynamics, need to be considered to obtain an integrated index for assessing the effects of environmental changes on biodiversity.

Waterbird Population Changes at Dongtan: A Global or a Local Phenomenon?

Globally, the proportion of waterbird populations exhibiting a decreasing trend markedly exceeds that exhibiting an increasing trend (Wetlands International 2006). Many studies have suggested that local, regional, and global factors could account for the changes in bird abundance (Schekkerman and others 1994; Holmes and Sherry 2001; Valiela and Bowen 2003). Although we cannot directly answer the question of which factors affect the population changes of waterbirds at Dongtan, the observed patterns probably reflect consequences of the changes at multiple scales. Given the large scale and fast pace of habitat changes at Dongtan, it is likely that the changes in waterbird communities were partially the consequence of intensive local habitat and environmental changes, including the loss of intertidal zones due to reclamation, increased human economic activities, and spread of invasive exotic plants.

To determine whether or not population changes in one region are representative of broader trends, information on the population dynamics of a species at a much larger spatial scale is required (Virkkala 1991). Although bird population dynamics at the local scale does not necessarily reflect patterns over large areas (Blake and others 1994), the waterbird population trends we observed at Dongtan are typical throughout the coastal areas of eastern China based on the similar patterns of wetland loss and degradation (China Forestry Bureau and others 2000; Ma and others 2008). Moreover, because of the close linkages among the breeding, stopover, and wintering stages in the life history of birds, the performance of birds in one stage of their life history could profoundly affect their population dynamics in the future (Baker and others 2004; Keller and Yahner 2006). Our results suggest that the population changes at Dongtan due to the loss and conversion of wetland habitats might have contributed to the global decline in some waterbird species. Presently, little is still known about the mechanisms and processes through which waterbird species are affected by habitat changes. Further studies of behavior, ecology, and demography are needed to address these questions. Such data will be essential to understanding how habitat changes affect waterbird community dynamics and developing evidence-based conservation and management plans (Holmes and Sherry 2001).

Implications for Conservation

Although the deposition of silt in the estuary increases the intertidal zone area, development of the intertidal zones has occurred at a rate faster than that of natural formation, which has ultimately caused a net loss of natural coastal wetlands at Dongtan. Because of the importance of natural wetlands in providing habitats, especially foraging sites, for most waterbirds at Dongtan, we suggest that reclamation programs should not be developed further until the intertidal zones reach a certain width, so that the speed of reclamation can be lower than that of intertidal sedimentation. In this way, tidelands can be reclaimed to meet the land demands for economic activities in an appropriate way, with a stable area of intertidal zones being maintained as waterbird habitats.

The spread of smooth cordgrass in intertidal zones causes a reduced quality of habitats for waterbirds. It is critical that the spread of smooth cordgrass in intertidal zones be controlled and replaced with native vegetation to restore the native habitats for waterbirds. Successful practices in controlling smooth cordgrass, including physical, chemical, and biological measures, in North America are good examples for Dongtan (reviewed by Hedge and others 2003).

Human economic activities in coastal wetlands are important to the economic development of local communities. However, these activities have severely disturbed the foraging and roosting of waterbirds in intertidal zones. To decrease the conflicts between economic activities and the conservation of waterbird habitats, we suggest that these activities should be regulated temporally and spatially according to the habitat use and resident status of waterbirds, which can reduce the conflicts between waterbird habitat use and human activities. The aim would be to minimize disturbance in the most important areas for migratory waterbirds during the spring and autumn migration periods and to permanently control human activities in certain areas of natural wetlands in order to provide undisturbed havens for waterbirds.

Acknowledgments

This study was supported by the National Basic Research Program of China (No. 2006CB403305), National Natural Science Foundation of China (No. 30670269), and Shanghai Scientific and Technology Foundation (No. 07DZ12038). We are grateful to Zhengyi Huang, Kai Jing, Shimin Tang, Fenghui Yang, and Qing Wang for helping with data collection and field surveys and to Chongming Dongtan Nature Reserve for facilitating our fieldwork. We thank Andrew Watkinson, Mark Barter, Zachary Felix, Dawn Lemke, and Kathy Robert for their comments and suggestions on early versions of the manuscript. The three anonymous reviewers and the editor provided constructive suggestions for improvement of the manuscript. Yong Wang’s research in China was partially supported by funds from the U.S. National Science Foundation (HRD-0420541), Fudan University, Beijing Normal University, and Alabama A&M University.

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