Habitat modification in relation to coastal reclamation and its impacts on waterbirds along China's coast

Global Ecology and Conservation 17 (2019) e00585

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Original Research Article

Habitat modification in relation to coastal reclamation and its impacts on waterbirds along China's coast Tiantian Ma, Xiaowen Li*, Junhong Bai**, Baoshan Cui State Key Laboratory of Water Environment Simulation, School of Environment, Beijing Normal University, Beijing, 100875, PR China

a r t i c l e i n f o

a b s t r a c t

Article history: Received 14 October 2018 Received in revised form 1 March 2019 Accepted 1 March 2019

The eastern coast of China provides a network of Important Bird Areas (IBAs) as feeding and breeding habitats, as well as migratory corridors for a large variety of waterbirds. However, long-term coastal reclamation has greatly encroached on coastal wetlands and undermined their functions as waterbird habitats. To identify the impacts of coastal reclamation on waterbird habitats in 2014, we analyzed coastal wetland modifications that have been caused by various reclamation types in 38 IBAs along China's coastline by using remotely sensed data. The distribution data of major waterbird families in 15 IBAs were collected to explore their population responses to habitat modification. The densities of their population were calculated to compare the habitat preferences to the natural and modified habitats. In addition, the index of Reclamation Intensity was used to evaluate the comprehensive impacts of coastal reclamation on waterbirds. The results show that more than half of the wetland areas in the 38 IBAs have undergone modification from various types of land use. The different habitat preferences indicate that the original habitat suitability for waterbirds has been perturbed considerably by the coastal reclamation. Our findings revealed that there are still notable conservation gaps for waterbirds along China's coastline and the opportunity exists for trading off waterbird conservation versus socioeconomic benefits by wise use of artificial wetlands as alternative and provisional habitats for waterbirds. © 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Keywords: Habitat modification Coastal reclamation Waterbird distribution Habitat preference Important bird area

1. Introduction Coastal wetlands are among the world's most productive ecosystems, acting as habitats for millions of migratory birds and as nurseries for amphibians and fishes, with considerable biodiversity supported by both terrestrial- and marine-derived nutrients (Barbier et al., 2011; Jaramillo et al., 2018; Kirwan and Megonigal, 2013). Coastal wetlands, such as the Important Bird Areas (IBAs) in the East Asian-Australasian Flyway (EAAF), are threatened by ever-increasing anthropogenic activities; however, they support a greater number of globally threatened waterbirds than any other flyway in the world (MacKinnon et al., 2012; Lei et al., 2018; Wetlands International, 2012). As the core part of the EAAF, China's coastal wetlands provide important stopover, breeding and wintering habitats for a huge number of endangered waterbirds (China Coastal Waterbird Census Group et al., 2015; Yang et al., 2017), and many coastal wetlands have been identified as Important Bird Areas (IBAs),

* Corresponding author. ** Corresponding author. E-mail addresses: [email protected] (X. Li), [email protected] (J. Bai). https://doi.org/10.1016/j.gecco.2019.e00585 2351-9894/© 2019 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/ licenses/by-nc-nd/4.0/).

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playing key roles in conserving the biodiversity of waterbirds. Every year, millions of waterbirds (e.g., shorebirds constitute the majority) have utilized these IBAs as resting areas when migrating between Australia and Siberia (Bai et al., 2015; Chan et al., 2009; Xia et al., 2017); but these coastal wetlands along China's coastline have undergone extensive modification from the intensive land use and coastal reclamation driven by rapid economic development (Ma et al., 2014). Some recent works have noted that the waterbird habitat in the EAAF has been seriously degraded by reclamation along China's coastal region, particularly in the coastal areas around the Yellow Sea (Cui et al., 2016; Ma et al., 2019; Murray and Fuller, 2015; Murray et al., 2014; Studds et al., 2017), and there is urgent need to safeguard those remaining waterbird habitat along China's coastline by strictly controlling ongoing coastal reclamation activities. Investigating the modified habitats relative to the distributions of waterbirds can provide fundamental knowledge for use in mitigating the impacts of coastal reclamation on waterbirds (Antoniazza et al., 2018; MacKinnon et al., 2012; We et al., 2017). Previous studies have compared the properties of natural and artificial habitats at local scales to reveal the impacts of anthropogenic activities on waterbird distribution (Bellio et al., 2009; Li et al., 2013; Marquez-Ferrando et al., 2014; SebastianGonzalez et al., 2015). Migratory waterbirds are the major populations in the IBAs along China's coast, with different species spreading across the diverse habitats (Bai et al., 2015; Xia et al., 2017). Thus, investigations of species distribution without considering landscape perspectives would insufficiently to reveal the spatial distribution patterns of migratory and mobile species at a regional scale (Martin et al., 2007). The importance and habitat functioning of China's coastal wetlands for waterbirds have been limited by the shortage of protected coastal sites (Yang et al., 2017). The 38 IBAs along China's coastline are crucial habitat nodes for maintaining biodiversity and viability of waterbirds in the EAAP by sustaining migratory population flows, and their supportive functions for waterbird populations are critically undermined when key habitats are destroyed. Ma et al. (2014) used the expression “New Great Wall” to describe the impacts of the continuous seawall associated with coastal reclamation along China's coast, particularly in waterbird habitats (Miller, 2015). Currently, some focal areas for waterbird conservation along China's coastline have been identified according to their considerable decline in population sizes, still, little is known about the different waterbird population dynamics that exist in response to the modification of natural habitats by coastal reclamation at the regional scale along migratory routes (Xia et al., 2017). Effective habitat conservation should spatially capture the shifting geographical distribution ranges of species due to the varied habitat preference during different periods in the life history of species (del Rosario Avalos and Hernandez, 2015). Many studies have demonstrated that waterbird populations tend to shift their habitats when resting or breeding (Barshep et al., 2017; Green et al., 2015), and artificial wetlands (e.g., salt fields and shrimp and fish ponds) can potentially function as alternative habitats for some waterbird populations when their populations winter, migrate and even breed (Li et al., 2012; Marquez-Ferrando et al., 2014; Scarton and Montanari, 2015). Although artificial wetlands can act as alternative habitats for waterbirds, they are still inadequate replacements for the loss of natural wetlands (Bellio et al., 2009; Ma et al., 2004). For the IBAs along China's coast, studies that explore how the waterbird populations respond to various modified artificial habitat types by land reclamation are lacking. Therefore, exploration of the responses of waterbirds to those modified habitats is necessary to balance the need for waterbird conservation with those of socioeconomic development. The objective of our study was therefore set to demonstrate the spatial distribution patterns of the major waterbird groups in natural and artificial habitats and to quantify the responses of waterbird populations to the reclamation intensity in the 38 IBAs along China's coast. The results of our study support implications for the tradeoff that exists between the need for waterbird conservation and socioeconomic activities such as coastal reclamation. 2. Materials and methods 2.1. Study area: IBAs along China's coast The coastal wetlands of China function as the key part of the East Asian-Australasian Flyway and link the habitats for a huge number of waterbirds that migrate between Australia and Siberia (Fig. 1) (Bai et al., 2015; Murray and Fuller, 2015). The coastal areas of the nine provinces (i.e., Liaoning, Hebei, Shangdong, Jiangsu, Zhejiang, Fujian, Guangdong, Guangxi and Hainan) and two cities (i.e., Shanghai and Tianjin), extend for nearly 18,000 km and constitute the coastline of mainland China (Wang et al., 2014). These regions contain numerous coastal wetlands formed by estuaries from river-derived sedimentation, providing globally important wetlands for a great number of migratory waterbirds, particularly in the 38 IBAs, with a total area of 32,018 km2, of which 5 IBAs are designated as Ramsar Sites (i.e., Shuangtai Hekou NNR, Yellow River Delta NNR, Yancheng NNR, Chongming Dongtan NNR and Dongzhaigang NNR) (Murray and Fuller, 2015). However, more than 50% of the coastal wetlands have been modified dramatically by intensive land reclamation in the past half century (An et al., 2007), and the socioeconomic development in the coastal region has contributed more than 60% of the total GDP in China in recent decades (He et al., 2014). The shrinkage and fragmentation of coastal wetlands has exacerbated the ecological integration and functioning of the coastal ecosystem and habitats and poses great threats to local livelihoods and coastal biodiversity (An et al., 2007; Cui et al., 2016; He et al., 2014; Wang et al., 2014). 2.2. Data on coastal wetlands and land reclamation Remote sensing images were used in our study to extract data on coastal wetlands and land reclamation in the nine coastal provincial unites and two cities; these images were obtained from the United States Geological Survey website (www.usgs.

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Fig. 1. The locations of 38 Important Bird Areas along China's coastline and their waterbird distributions.

gov), including the images of Enhanced Thematic Mapper in 2014 (with spatial resolution of 30 m
30 m). Through visual interpretation based on ENVI 4.4, land use and land cover maps were obtained, and the natural coastal wetlands (i.e., tidal flats, salt marsh, estuarine water, and estuarine alluvium) and coastal reclamation types (i.e., mariculture, cropland and constructed area) were extracted and highlighted. 2.3. Data on distribution of waterbirds According to the Dictionary of Important Bird Area (mainland) published by BirdLife International in 2009, 38 Important Bird Areas (IBAs) have been identified along China's coast (Table 1) (Chan et al., 2009), and these are delineated by circles with the same area (Chan et al., 2009) (Fig. 1). The data on the waterbird distributions and population sizes in the IBAs were sourced from the Institute of remote sensing applications, Chinese academy of sciences and updated according to the reports of China's coastal waterbird census group, which included the point-counting distribution data of 133 species of the five major taxonomic assemblages (families) from field survey, i.e., Shorebirds, Anatidae, Gulls, Ardeidae and Cranes, accounting

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Table 1 The geographic positions and conservation status of 38 IBAs along China's coast. No.

Code

Name

Area (ha)

Centroid

Conservation status

Province

1 2 3 4 5 6 7 8 9

CN063 CN062 CN059 CN058 CN055 CN052 CN311 CN312 CN317 CN320 CN319 CN327 CN328 CN331 CN332 CN365 CN367 CN373 CN374 CN375 CN376 CN377 CN382 CN385 CN388 CN391 CN394 CN395 CN396 CN397 CN410 CN411 CN416 CN417 CN498 CN486 CN487 CN500 CN501 CN502

Shuifeng Reservoir and middle reaches of Yalu Jiang Yalu Jiang Estuary Zhuanghe coast Laotieshan Wafangdian Fuzhou Wan Shuangtai (Shuangtaizi) Estuary and Inner Gulf of Liaodong Beidaihe Luan He Estuary Tianjin Coast

30,000 200,000 22,070 17,000 30,000 130,000 7000 20,000 148695

40 300 N 125 00 E 39 530 N 123 350 E 39 350 N 122 450 E 38 460 N 121 110 E 39 400 N 121 350 E 41 00 N 121 450 E 39 490 N 119 300 E 39 250 N 119 150 E 39 200 N 117 400 E

Unprotected Partially protected Unprotected Protected Unprotected Partially protected Protected Protected Partially protected

Liaoning Liaoning Liaoning Liaoning Liaoning Liaoning Hebei Hebei Tianjin

Yellow River Delta Nature Reserve Laizhou Wan Rongcheng Swan Nature Reserve Qingdao-Rizhao coastal wetland and islands Lianyungang saltworks Yancheng Nature Reserve Qidong Northern Yangtze Estuary Nature Reserve Coastal Wetlands of Northern Chongming Dao Island Chongming Dongtan Nature Reserve Jiuduansha Nature Reserve Eastern Tidal Flat of Nanhui Hangzhou Wan Yong Jiang Estuary Wuyumen Taizhou Wan Yueqing Wan Xuanmen Wan Wenzhou Wan Coast between Ao Jiang and Feiyun Jiang Funing Wan Min Jiang Estuary Quanzhou Wan and Jin Jiang Estuary Dongshan Wan Rong Jiang Estuary Nanliu Jiang Estuary Shankou Mangroves Nature Reserve Dongzhaigang Nature Reserve Qinglangang Nature Reserve Houshui Wan

153,000 10,000 10,500 1,063,000 7000 453,300 21,491 6060 32,610 42,320 12,250 37,100 2200 5400 10,200 22,000 4300 12,400 18,400 5000 730,000 7093 21,400 2000 5500 8000 3337 2800 5000

37 500 N 119 00 E 37 120 N 119 100 E 37 120 N 122 300 E 36 00 N 120 200 E 34 420 N 119 140 E 33 350 N 120 300 E 31 490 N 121 270 E 31 470 N 121 270 E 31 300 N 121 570 E 31 300 N 121 540 E 30 580 N 121 540 E 30 180 N 120 450 E 30 00 N 121 390 E 29 90 N 121 420 E 28 370 N 121 350 E 28 140 N 121 100 E 28 90 N 121 170 E 27 530 N 120 510 E 27 370 N 120 410 E 26 540 N 120 30 E 26 100 N 119 300 E 24 520 N 118 410 E 23 420 N 117 230 E 23 170 N 116 430 E 21 360 N 109 30 E 21 320 N 109 450 E 19 580 N 110 350 E 19 370 N 110 520 E 19 530 N 109 280 E

Protected Unprotected Protected Unprotected Unprotected Protected Protected Unprotected Protected Protected Partially protected Unprotected Unprotected Unprotected Unprotected Unprotected Unprotected Unprotected Unprotected Unprotected Partially protected Protected Partially protected Unprotected Partially protected Protected Protected Protected Partially protected

Shandong Shandong

10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38

Shandong Jiangsu Jiangsu Jiangsu Shanghai Shanghai Shanghai Shanghai Zhejiang Zhejiang Zhejiang Zhejiang Zhejiang Zhejiang Zhejiang Zhejiang Fujian Fujian Fujian Fujian Guangdong Guangxi Guangxi Hainan Hainan Hainan

for 96% of the total number of waterbird species along China's coast (China Coastal Waterbird Census Group et al., 2015). In particular, Shorebirds accounted for approximately 80% of the total number of the migratory waterbirds. 2.4. Measuring impacts of habitat modification on waterbird population All the data sets of land use and land cover, IBAs and waterbird distribution were geographically registered and transformed into vectorized GIS data layers by ArcGIS 10.1, and the distribution of natural wetlands and reclamation types in IBAs were clipped and extracted from land use and land cover in coastal region by using spatial boundary of IBAs. Further, the waterbird population size on the different habitat types were measured by overlaying point-counting data on waterbird population size with land use land cover data in IBAs. The waterbird populations in a habitat type (i.e., habitat affinity to natural wetland or reclamation type) were calculated by summing up all the point-counting data of waterbirds within this habitat type, and used to quantify the impacts of habitat modification on the population dynamics of waterbird. 2.5. Statistical analysis The waterbirds were distributed in natural coastal wetlands and four types of artificial habitats that were modified by reclamation (i.e., mariculture field, cropland, enclosed water and constructed area), of which the natural coastal wetlands were used as the baseline for comparing the population distributions of five waterbird assemblage responses to those four types of habitats modified by reclamation. To measure the habitat modifications along China's coast, the percentages of the four artificial habitat types altered by coastal reclamation in the 38 IBAs were calculated, and the population percent of each assemblage of waterbirds was calculated in all natural and artificial types of habitats to compare the supportive functions of the habitats. In addition, the trends in population distribution within the natural and artificial habitats were further explored

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by regression analysis to quantify the impacts of coastal reclamation on waterbirds. The population density for each assemblage in all IBAs was also calculated to reveal the preferences of the waterbirds for natural and artificial habitats. The index of Reclamation Intensity was introduced and used to evaluate the integrated impacts of various land use types on the natural coastal wetlands based on their magnitudes in habitat modification, and this index was calculated as follows:

P Ri ¼

Wj HAj TAi

where Ri is the reclamation intensity for a certain IBA (i), Wj is the weight set for a specific habitat type (j), HAj refers the area of habitat type (j) within a certain IBA (i), and TAi means the total area of IBA (i). Analytic Hierarchy Process (AHP) can be used to quantify the magnitude of land use/land cover in coastal management (Xu et al., 2017). In this study, the ornithological experts and local managers of the IABs were consulted extensively to obtain knowledge for the AHP judgment matrixes. Finally, the weights of natural wetlands, mariculture field, cropland, enclosed water and constructed area were identified as 0.0388, 0.0694, 0.1089, 0.2898 and 0.4931, respectively. Finally, the relationships between the different population densities and the Reclamation Intensity indexes were presented to demonstrate the impacts of land reclamation on the waterbirds. 3. Results 3.1. Habitat modification Approximately 52% of the total area of all IBAs was altered by coastal reclamation, but the contributions of the reclamation types presented regional variations (Fig. 2), of which mariculture fields accounted for the largest contribution (30.85%) compared with the least percentage (2.21%) of the croplands. Six IBAs (No. 2, 17, 23, 26, 30, and 32) were almost completely transformed into mariculture fields, and another six (No. 3, 7, 11, 15, 27, and 28) had been more than 50% reclaimed for mariculture. In addition, 6.54% of the coastal wetlands had been converted into constructed area in all IBAs, of which the coastal wetlands around Bohai Sea (No. 4, 6, 9 and 13) showed relatively higher percentages of conversion; however, these areas provided key stopover sites for waterbirds in the EAAP. In addition, the enclosed water was mainly distributed in four IBAs (No. 9, 11, 22 and 24), where the coastal wetlands are only partially protected or unprotected (Table 1). The completely transformed IBAs, such as No. 2, 17, 23, 30 and 32, were also partially protected or unprotected (Fig. 2 and Table 1). Although 8 IBAs (i.e., No. 8, 19, 20, 31, 34, 35, 37, and 38) remained intact and covered by natural reserves, the other 8 IBAs (4, 7, 10, 12, 15, 16, 18, and 36) were still being encroached upon by reclamation even though they had already been protected. 3.2. Population distribution The natural wetlands across all IBAs were inhabited by more than 50% of the population of all waterbirds, and approximately 95% of Anatidae and 93% of Ardeidae were recorded in the natural wetlands, showing the key role of natural wetlands in providing intact habitats for the waterbirds (Fig. 3). Next to the natural wetlands, the mariculture fields were the secondmost important habitats for Shorebirds, Anatidae, Gulls and Cranes, supporting 48% of the gull population in particular. The croplands attracted less than 10% Ardeidae, whereas the enclosed water had the least number of waterbirds recorded, including a very few shorebirds. The total number of waterbirds showed a significant positive relationship with the area of the natural wetlands, showing “S-curve” growth with the increased area of the natural wetlands (Fig. 4). Due to the expansion of artificial wetlands, the

Fig. 2. The percentages of natural coastal wetlands and four reclamation types in 38 Important Bird Areas (from left to right: No. 1 to 38) along China's coast.

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Fig. 3. The population percentages for bird families inhabiting the different types of habitats. SH: Shorebirds; AN: Anatidae; GU: Gulls; AR: Ardeidae; CR: Cranes.

Fig. 4. The distribution trends of waterbirds inhabiting natural and artificial habitats. The regression analysis of total waterbirds is shown at a significance level of P < 0.05.

waterbird number grew slightly at first, then sharply increased to the peak and quickly decreased with a relatively stable shrinkage afterwards (Fig. 4). 3.3. Population density The different waterbird assemblages showed variation in their population densities in the habitat types (Fig. 5). Shorebirds exhibited the broadest habitat suitability, with relatively higher population densities in all habitat types; however, the population density of Shorebirds in the mariculture fields (2.8/ha) was nearly twice that in the natural habitats and enclosed water. In contrast, the Cranes showed the narrowest habitat distribution, with lower population density, and they occurred only in natural wetlands. Anatidae was observed aggregated in enclosed water, with the highest population density (nearly 10.0/ha) among the all waterbird groups, compared with a very tiny portion of their population being recorded in natural wetlands and mariculture fields at much lower population densities. The mariculture fields were mostly preferred by the gulls, with the highest population density, whereas no records of gulls were made in the enclosed waters. The population densities of Ardeidae were lower in natural wetlands (0.03/ha) and enclosed water (0.04/ha) and higher in croplands (0.12/ha), with no distribution in mariculture; however, their population densities were generally lowest among the waterbird groups in all habitat types. Although natural wetlands with vast areas were preferred by most waterbird populations, the population densities, however, were always lower; only the cranes showed higher population density in the natural wetlands than in the reclamation types. 3.4. Population response to reclamation intensity Population density showed a general continuous decline with the increase in Reclamation Intensity (RI), which dramatically decreased during a very narrow RI threshold (0.02e0.05) in particular and remained nearly stable outside this

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Fig. 5. The mean density of different bird families in different habitats. The population density in each type of habitat was the average value for all observed IBAs. NH: Natural habitats; MF: Mariculture field; CR: Cropland; EW: Enclosed water.

threshold (Fig. 6). Since most of the waterbirds inhabited natural wetlands, their population densities decreased dramatically at first, indicating the great impact of the essential changes of habitats from natural to artificial habitats for waterbirds. However, when the artificial habitats reached a certain size, reclamation types such as mariculture or croplands became alternative habitats for waterbirds, which resulted in small-scale increases in population density. Finally, the population

Fig. 6. Change in density in waterbird families with increasing reclamation intensities. The relationship of total waterbird number and reclamation intensity by regression analysis is shown at a significance level of P < 0.05.

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density became stable, showing a slight decrease with increasing reclamation intensities. As the major families with the larger population sizes, the Shorebirds and Anatidae showed trends similar to that of the total waterbirds to reclamation intensity. However, obvious trends were not exhibited by Gulls, Ardeidae and Cranes probably due to their smaller population sizes. 4. Discussion Our study indicated that large-scale coastal reclamation threatened the population of waterbirds by the conversion of more than half of the natural wetlands into artificial wetlands (e.g., mariculture fields and enclosed water) or constructed areas in all IBAs along China's coast. In particular, 6.05% of the area of natural habitats in all IBAs has been converted into impervious constructed area, where the waterbird can hardly inhabit, as well as 45.16% into reclaimed artificial wetlands, which are used only as alternative habitats by waterbirds. Our research revealed that only 34.22% of the area of the IBAs is effectively protected by the national nature reserves, with 21.05% being partially protected. However, 44.73% of the area of the IBAs is not included in the extant conservation system, indicating obvious conservation gaps for waterbird habitats in these IBAs along China's coast. Among these conservation gaps, some act as key stopover habitats for migratory waterbirds in the EAAP, particularly in the IBAs around the Bohai Sea (No. 4, 6, 9 and 13). These areas have become bottlenecks in the EAAP, as their key habitat functions have been undermined greatly by the coastal reclamation (Hua et al., 2015; Murray et al., 2015; Studds et al., 2017), and the conservation gaps therefore need to be filled in these IBAs by incorporating the areas into the existing conservation system. In addition, we found considerable reclaimed wetlands within nearly half of the protected IBAs, indicating the urgent need to strengthen the effective conservation of coastal wetlands and to strictly manage the land reclamation in these sites. Habitat modifications have fundamentally impacted the abundance and distribution of waterbird species, as well as the ecological integration of the coastal wetland ecosystem. Understanding the variations in population size and density in the different habitats is crucial when predicting species distributions for conservation actions (Ehrlen and Morris, 2015). In this study, the population size of waterbirds showed a positive relation to the area of natural wetlands, whereas the responses of waterbirds to areas of coastal reclamation were nonlinear and mostly depended on the sitespecific habitat types, implying that some waterbirds were forced to adapt and change their habitat preferences from natural wetlands to artificial wetlands resulting from coastal reclamation. The much greater percentage of waterbird populations observed in natural wetlands still indicated the necessity to conserve and restore natural wetlands (Bellio et al., 2009; Ma et al., 2004). Some waterbirds showed higher population affinities for specific artificial wetlands, such as mariculture fields and enclosed water, as these modified habitats still retained key physical elements of the natural habitats and the associated habitat functions (Lei et al., 2018; Green et al., 2015; Marquez-Ferrando et al., 2014). Despite the greater human disturbance with high reclamation intensity, the mariculture fields were the most attractive habitats for Shorebirds and Gulls, with the highest population densities because of the rich food resources provided (e.g., fish, shrimp and crab). Similarly, Anatidae and Ardeidae were densely populated in the enclosed waters and croplands because of both the relatively abundant food resources and less human disturbance. The variations in habitat preferences by waterbirds provided nonlinear response curves to the reclamation intensity, which created opportunities for a trade-off in the conflicting land resource uses of waterbird habitat versus the economic benefits by considering that those habitable reclaimed areas served as potential alternative habitats. This trade-off should be made by identifying those sites, evaluating the population dynamics and distribution patterns of the waterbirds, and developing temporal-spatially shifting management measures to maximize the habitable functions of the areas while minimizing their socioeconomic cost. As one of the most endangered waterbird species protected at the national level, the crane has a population distribution that is exclusively within natural wetlands in the IBAs, indicating the extreme sensitivity of the crane to human-induced habitat modifications. Thus, the crane can be used as an excellent indicator species to inform habitat change for waterbird conservation (Li et al., 2017). The total number of waterbirds generally declined with the increased RI and mostly declined in the very narrow threshold of the RI (0.02e0.05), remaining nearly stable outside of this threshold. The sharp decrease in most waterbird populations might indicate the fundamental impacts of habitat transformation from natural to artificial habitats during the narrow transitional threshold and indicate the necessity of identifying and setting a rigorous RI threshold. Our study suggests that, when considering integrated conservation and restoration strategies for waterbird habitats in coastal regions under unavoidable reclamation, the potential tradeoffs between anthropogenic activities and waterbird conversation need to be explored for ecological coastal management (Bellio et al., 2009; Ma et al., 2004). In addition to the wise use and management of alternative habitats caused by the coastal reclamation, measures for wetland restoration should be carefully considered to mitigate the degradation and the loss in natural habitats and to maintain “no net loss” for the natural wetlands (Murray and Fuller, 2015; Athearn et al., 2012; Li et al., 2012). This may involve in situ offset by restoring local natural wetlands from these modified habitats (e.g., mariculture field, cropland and enclosed water) within the IBAs. To compensate for the loss in natural wetlands to impervious constructed areas and hard infrastructure (e.g., industrial ports, roads and the seawall system), the ex situ offset can be employed to incorporate sufficient natural habitat restored outside the IBAs to ensure “no net loss” of the natural wetlands in the IBAs (Yu et al., 2017). Furthermore, the restoration sites and pattern should be systematically prioritized and optimized to achieve the most cost-efficient conservation outcome by trading off between the ecological benefits versus the socioeconomic costs.

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Although the scarcity of data on the distribution of waterbird populations probably led to biased results for such a large area across all the IBAs along China's coast, our study is still valuable to explore the distributions of waterbird populations in response to modified habitats by land reclamation, which has rarely been documented in previous research. Our study highlighted the need to ensure the effective habitat conservation for the IBAs by strictly controlling coastal reclamation and human activities; however, this approach would be time- and resource-consuming (Liang and Li, 2012; Studds et al., 2017). Hence, future research is needed to prioritize a cost-efficient spatial pattern for wetland conservation within the IBAs along China's coast based on a systematic conservation framework, and this conservation pattern should be tailored with an optimized restoration pattern to acquire the integrated conservation efficacy as well as to adapt the impacts of the coastal squeeze driven by both land reclamation and rising sea levels (Dias et al., 2017; Maleki et al., 2016; Yang et al., 2017; Li et al., 2017). 5. Conclusions More than one-half of the wetland area in the 38 IBAs along China's coast has been transformed into artificial habitat by intensive coastal reclamation and relevant land use development, even in the nearly one-half that are in protected IBAs. Of the natural habitats in all IBAs, 6.05% has been converted into impervious constructed area, where the waterbirds can hardly inhabit. Only 34.22% of the area of the IBAs was effectively protected by the national nature reserves, with 21.05% partially protected, and 44.73% of the area of the IBAs not included in the extant conservation system, resulting in notable conservation gaps for the waterbirds. Most of waterbirds still inhabit the natural wetlands with large population sizes; however, they also used some specific artificial wetlands as alternative or provisional habitat (e.g., mariculture field, enclosed water) with much smaller numbers but relatively higher densities, showing distinct habitat preferences to the different artificial habitats. The total number of waterbirds generally declined with the increased RI and mostly declined in the narrow RI threshold (0.02e0.05), indicating the impacts of habitat transformation from natural to artificial habitats during the transitional threshold. The variations in habitat preferences by waterbirds contributed to the nonlinear response curves to the reclamation intensity, and create an opportunity for a trade-off in the conflict between the different land resource uses, i.e., waterbird habitats versus economic benefits.

Acknowledgments This work was supported by the National key R&D program of China (2017YFC0505906), the National Natural Science Foundation of China (No. 31770576 and No. 31370535) and the National Key Basic Research Program of China (2013CB430406). The authors would also extend appreciation to all the anonymous reviewers and editors for their constructive comments that improved the paper.

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