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Variations in fish habitat fragmentation caused by marine reclamation activities in the Bohai coastal region, China
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Variations in fish habitat fragmentation caused by marine reclamation activities in the Bohai coastal region, China Xiaosong Ding a, b, Xiujuan Shan b, c, *, Yunlong Chen b, Miao Li a, b, Jiajia Li a, d, Xianshi Jin b, c a
College of Marine Sciences, Shanghai Ocean University, Shanghai, 201306, China Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs; Shandong Provincial Key Laboratory of Fishery Resources and Eco-environment; Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China c Laboratory for Marine Fisheries Science and Food Production Processes; Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China d Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Qingdao Key Laboratory for Marine Fish Breeding and Biotechnology, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China b
A R T I C L E I N F O
A B S T R A C T
Keywords: Marine reclamation Fish habitat fragmentation Fish recruitment Coastal wetland
Due to the development of the social economy and population density pressure, coastal reclamation activities have rapidly increased throughout coastal regions in China and have had a significant negative impact on fish habitat fragmentation (especially on the habitat of the early life history stage of fish, ELHSF). However, few studies have focused on the negative ecological impacts of reclamation patches on ELHSF habitats (such as spawning, nursery, and feeding grounds). Data on marine reclamation were extracted from 49 Landsat remote sensing images from 7 different periods from 1985 to 2015, and ichthyoplankton data from 1982 to 2014 were compiled. The trend of fragmentation showed that the number of artificial heterogeneous patches significantly increased, and the isolation of habitat landscape became more intense. As a result, the spatial patterns of ich thyoplankton habitat rapidly transformed from a continuous and integral distribution to a divided and frag mented distribution, which drastically changed numerous environmental factors and deeply reshaped normal fish recruitment activities by impacting the number and abundance of ELHSF.
1. Introduction Due to the limited urban land area and the sharp increase in the population density in coastal zones, low-cost, short-cycle and high-profit marine reclamation projects have rapidly increased in prevalence throughout coastal regions in China (Yang et al., 2011; Wang et al., 2010, 2014). Four stages of large-scale marine reclamation activities have occurred since the establishment of the People’s Republic of China (after 1949) (Liu et al., 2008; Wang et al., 2014; Zhu et al., 2016): (1) The first stage (1949–1960): salt grounds were spread throughout the coastal region for the extraction of salt from seawater. The Changlu salt ground was built and expanded into the largest salt area in China at this stage (Liu et al., 2008). (2) The second stage (1960–1980): agricultural developments were implemented to increase the food and agricultural resources in the coastal region. Due to the increase in agricultural land, the coastal tidal flat disappeared (Liu et al., 2008; Tian et al., 2016). (3)
The third stage (1980–1990): marine aquaculture quickly spread throughout the coastal wetland to meet the needs of society for aquatic foods. Marine aquaculture has led to severe eutrophication in coastal waters (Liu et al., 2008; Wang et al., 2014). (4) The fourth stage (1990-present): reclamation activities mainly included those for harbor, industry, and urbanization land use in the coastal zone. Currently, the different land use types that were developed in the four periods coexist and affect the coastal environment. With the development of reclama tion activities, fish habitat is undergoing severe fragmentation (espe cially for spawning, nursery and feeding grounds) (Bakker et al., 2009; Wang et al., 2010; Yu et al., 2016). Fragmented habitat will lead to negative effects on the normal activities of fish migration, reproduction and population replenishment (Bakker et al., 2009; Wu et al., 2002; Yang et al., 2011; Zhao et al., 2004). However, quantitative and sys tematic studies on the effects of marine reclamation on the early life history stage of fish (ELHSF) are lacking.
* Corresponding author. Laboratory for Marine Fisheries Science and Food Production Processes; Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China. E-mail address: [email protected] (X. Shan). https://doi.org/10.1016/j.ocecoaman.2019.105038 Received 5 May 2019; Received in revised form 9 October 2019; Accepted 23 October 2019 0964-5691/© 2019 Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article as: Xiaosong Ding, Ocean and Coastal Management, https://doi.org/10.1016/j.ocecoaman.2019.105038
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Fig. 1. Spatial distribution of reclamation projects in the Bohai coastal region, China. Table 1 Fragmentation indexes and their significance in this study. No.
Index
Significance
1
AI (aggregation index)
A small AI indicates that the patch is made up of many small patches; thus, the spatial aggregation is not strong.
Formula
2
MPA (mean patch area)
A small MPA indicates that the landscape is highly fragmented, and vice versa.
3
MPFD (mean patch fractal dimension)
A MPFD value close to 1 indicates that the degree of similarity is high in the same patch type and the spatial distribution of the patches is regular.
I ¼ 2 lnðnÞ þ 100%
A MSI value of 1 indicates that all patches are square, and a high index indicates that the shape of the patch is irregular.
5 6
NP (number of patches) PD (patch density)
A large NP corresponds to a high degree of fragmentation, and vice versa. A high PD corresponds to a high degree of fragmentation in the landscape pattern, and vice versa.
Habitat fragmentation (HF) is a very useful way to study the rela tionship between reclamation patches and ELHSF habitat (Forman, 1995; Nadzir et al., 2014; Wu et al., 2002). However, current studies have been limited to analyzing the characteristics of HF, and discussions of fish habitat isolation under the impacts of reclamation activities are lacking (XU et al., 2015; Yang et al., 2018; Zhang et al., 2016). Habitat isolation and environmental factor changes are the main negative im pacts of reclamation activities on ELHSF habitat. Based on the fish HF characteristics and the ELHSF data, the relationship between reclama tion activities and fish habitat can be systematically discussed (Li et al., 2018; Rendenieks et al., 2017; XU et al., 2015). In this paper, we study the impact of coastal wetland fragmentation resulting from marine reclamation and discuss the relationship with the
ðPij Þ � lnðPi Þ �
0 < AI�100
MPA>0 1 � MPFD�2
MPDF ¼ � 2 lnð0:25Lij Þ lnðAreaij Þ Pm Pn i¼1 j¼1 NPij ! Pm Pn 0:25Lij i¼1 j¼1 pffiffiffiffiffiffiffiffiffiffiffiffi Areaij Pm Pn MSI ¼ i¼1 j¼1 NPij — Pn NPi PD ¼ Pni¼1 i¼1 Areai i¼1
MSI (mean shape index)
i¼1 j¼1
NPi MPA ¼ Pn i¼1 NPi
Pm Pn 4
Others m P n P
�
j¼1
MSI�1
NP � 1 PD � 0
ELHSF. The results of this study will support marine reclamation man agement and fish habitat protection in the future. 2. Materials and methods 2.1. Study area The Bohai Sea (37� 070 -41� 000 N, 117� 350 -121� 100 E, Fig. 1) is a semienclosed inland sea in China that has an area of approximately 7.7 � 104 km2. The Bohai coastal region is an important habitat for the ELHSF and represents important spawning, nursery and feeding grounds for fishery resources in the Yellow Sea and Bohai Sea (Jin, 2004; Yang et al., 2011; Zhang et al., 2007). Inputs from many rivers, such as the 2
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Fig. 2. Changes in the areas of reclamation projects in the bays of the Bohai coastal region from 1985 to 2015. Table 2 Dynamics of the AI, MPA, MPFD, MSI, NP and PD indicators for different types of reclamation projects. Time
Type
AI
MPA (1 � 106)
MPFD
MSI
NP
PD (1 � 10 8)
1985–1990
Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land
92.00 83.73 85.33 94.16 90.72 93.62 85.14 89.82 95.60 92.79 93.73 86.55 80.68 96.01 93.02 94.36 90.46 91.64 96.15 95.94 95.63 93.19 96.47 96.17 95.69 96.38 93.89 96.54 96.83 96.68
2.13 0.22 0.33 3.75 1.84 3.17 0.43 0.35 6.65 2.04 3.63 0.64 0.56 7.82 2.99 4.12 0.91 1.62 8.48 6.01 7.99 1.53 7.43 9.62 6.81 11.00 2.14 11.60 16.70 10.50
1.06 1.05 1.04 1.05 1.04 1.06 1.06 1.04 1.05 1.04 1.07 1.06 1.06 1.05 1.05 1.07 1.06 1.06 1.05 1.06 1.07 1.06 1.07 1.05 1.06 1.07 1.06 1.07 1.06 1.06
1.53 1.32 1.30 1.48 1.38 1.55 1.46 1.31 1.48 1.42 1.61 1.47 1.41 1.50 1.46 1.67 1.49 1.52 1.52 1.48 1.72 1.51 1.60 1.54 1.50 1.73 1.52 1.75 1.63 1.51
135 20 6 6 30 144 21 9 30 41 158 31 20 31 33 205 46 23 37 56 141 64 73 47 51 123 103 90 33 26
3.60 3.04 0.26 0.97 0.76 5.46 3.06 0.89 1.82 28.70 13.10 3.07 0.90 2.37 3.59 16.80 3.29 1.05 3.29 3.51 19.20 3.77 1.20 3.99 1.97 5.46 4.25 1.28 4.00 6.38
1990–1995
1995–2000
2000–2005
2005–2010
2005–2010
3
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Fig. 3. Characteristics of the fragmentation indexes from 1985 to 2015.
Yellow River, Haihe River, Weihe River, and Liaohe River, have enriched the abundance of bait organisms and have made the offshore waters important spawning and habitat grounds for many fishery groups, such as fish, shrimp, crab, shellfish and cephalopods. The coastal area of the Bohai Sea covers 4 provinces (Liaoning Province, Hebei Province, Tianjin City and Shandong Province). The coastal area has a high population density and a high density of social and economic activities. The spatial density of reclamation projects, such as large ports, aquaculture, and tourism infrastructure, is very high (Pelling et al., 2013; Duan et al., 2016; Wang et al., 2014).
Bohai coastal region. 2.2.2. Extraction method for reclamation projects After geometric correction and coordinate transformation, the coastline in 1985 (denoted coastline1985) was extracted via visual interpretation and used as the benchmark to extract land reclamation projects. The extraction rules for the reclamation projects were as fol lows: all of the extracted reclamation projects must refer to the bench mark (Shoreline1985) and the texture, shape, color, etc., during the historical periods (1985–1990, 1990–1995, 1995–2000, 2000–2005, 2005–2010, 2010–2015). The reclamation project must be compared to Google Maps (GM) via overlapping to ensure the precision of the extracted area; otherwise, the project must be re-extracted from the image. Using this procedure, we acquired the spatiotemporal distribution of marine reclamation projects for different periods. The marine reclama tion types were divided into Aquaculture Land (land used for marine aquaculture), Harbor Land (land used for harbor), Industrial Land (land used for industrial and urban), Salt Land (land used for saltern) and Unused Land (land that has been reclaimed but not used). The preprocessing of Landsat images was performed using ENVI (ENVI 5.2 SP1, ITT Visual Information Solutions, Boulder, CO, USA, 2015), and the reclamation projects were extracted based on visual
2.2. Extraction method for reclamation projects 2.2.1. Satellite data The Landsat remote sensing data used in this article were from the official USGS website (https://earthexplorer.usgs.gov/), and they included 7 periods (1985, 1990, 1995, 2000, 2005, 2010 and 2015) and 7 images per period for a total of 49 images. Each image had limited cloud coverage to ensure that the accuracy of the subsequent image interpretation was not impacted. The additional data included China’s administrative division map (spatial scale: 1:4,000,000), a topographic map (spatial scale: 1:4,000,000), a nature reserve map of the Bohai coastal region, and the regional economic statistics yearbook for the 4
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Fig. 4. Fragmentation trends of coastal wetland landscape patterns.
interpretation by experts in ArcGIS (ESRI ArcGIS Desktop 10.2) software.
Table 3 Evaluation parameters and score coefficients of the principal components. Index
PC1
PC2
PC3
PC4
PC5
PC6
AI MPA MPFD MSI NP PD Std. Deviation (SD) Proportion of Variance (%) Cumulative Proportion (%)
0.44 0.50 0.49 0.57 0.03 0.01 1.74 51
0.39 0.01 0.22 0.08 0.71 0.53 1.06 20
0.08 0.11 0.03 0.04 0.57 0.81 0.98 16
0.59 0.14 0.68 0.01 0.35 0.23 0.63 7
0.47 0.79 0.33 0.03 0.19 0.04 0.61 6
0.28 0.31 0.39 0.82 0.06 0.08 0.12 0
51
71
87
94
100
100
2.3. Ichthyoplankton data The ichthyoplankton data were from a historical survey of the Bohai Sea by the Fishery Resources and Eco-environment Lab (Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences). The data included the species number of fish eggs (SNFE), species number of fish larvae (SNFL), abundance index of fish eggs (AIFE), and abundance index of fish larvae (AIFL). The data were obtained by horizontally towing a zooplankton net (mouth diameter 80 cm, length 270 cm, mesh size 0.50 mm) in the Bohai Sea. The survey periods included 1982–1983, 1992–1993, 2013–2014, and 2014–2015. 2.4. Fragmentation index To quantitatively study HF, 6 indexes were used to study the land scape fragmentation characteristics along the coastal region at the 5
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Fig. 5. Variations in SNFE, SNFL, AIFE, AIFL, and FPC from 1982 to 2015.
spatiotemporal scale (Table 1) (McGarigal et al., 2002; Rendenieks et al., 2017; Yan et al., 2017). The “SDMTools” package (Jeremy et al., 2014) was used to calculate the marine reclamation fragmentation index, and the data were visual ized using the “ggplot2” (Hadley, 2009) and “sp” packages (Pebesma et al., 2005) in R software.
The area of Unused Land fluctuated throughout the study period. 3.2. HF variation The patches created by the reclamation projects extensively altered the landscape patterns in the coastal wetland region from 1985 to 2015 (Table 2, Fig. 3). The main fragmentation characteristics of the patches were as follows: highly aggregative and exhibiting increasing area, increasing MPFD, increasing MSI, increasing NP, and increasing PD. However, different patch types exhibited different characteristics in different regions. The largest increase in the AI occurred in the Industrial Land patches (increase units: 11.21), and the smallest increase occurred in the Salt Land patches (increase units: 2.67). The largest increase in the MPA index was found in the Salt Land patches (increase units: 1.29 � 107), and the smallest was found in the Unused Land patches (increase units: 8.68 � 106). The largest increase in the MPFD index was found in the Industrial Land patches (increase units: 0.03), and the smallest increase was found in the Salt Land patches (increase units: 0.01). The largest increase in the MSI was found in the Industrial Land patches (increase units: 0.45), and the smallest was found in the Unused Land patches (increase units: 0.12). A significant increase in the NP index was observed for all reclamation types, although the Aquaculture Land patches showed a decreasing trend in NP after 2000. The PD index showed a significant increasing trend, which was closely related to the rapid increase in MPA.
3. Results 3.1. Dynamics of reclamation patches The analysis of the changes in the proportions of marine reclamation types from 1985 to 2015 indicated that all of the patch areas showed increasing trends (Figs. 1 and 2). Among these areas, the Unused Land, Industrial Land and Salt Land patches showed significant increasing trends, while the Aquaculture Land patch areas increased at a slower rate than the other patch types. The increasing trend was not uniform throughout the Bohai coastal region and varied during the different time periods (Fig. 2). The area of Aquaculture Land showed rapid growth from 1995 to 2005 in the coastal regions of Laizhou Bay and Bohai Bay, and the growth rate slowed after 2005. The area of Harbor Land showed a sig nificant increasing trend from 2000 to 2005, and the growth rate was highest near Bohai Bay, followed by the Laizhou Bay coastal region and the Liaodong Bay coastal region. The area of Salt Land exhibited sig nificant increases in the coastal regions of all three bays. In the Laizhou Bay coastal region, the Salt Land area showed a significant increasing trend throughout the study period. In the Bohai Bay coastal region, the Salt Land area reached its highest value in 2000–2005, and in the Liaodong Bay coastal region, it reached its highest value in 1990–2005.
3.3. Trend of fragmentation of coastal wetlands The fragmentation characteristics of the marine reclamation patches 6
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Fig. 6. Relationship between coastal wetland reclamation and ELHSF.
showed the following characteristics (Fig. 4): 1) The AI showed a rapidly increasing trend, indicating that the spatial aggregation of various patches was strong. 2) The MPA index showed a rapidly increasing trend, indicating an increase in large patch areas. 3) The MPFD index was concentrated from 1.05–1.065, indicating a significant increase in the degree of similarity. 4) The MSI showed a rapidly increasing trend, indicating that the geometric shapes of the patches deviated from a square and increased in complexity. 5) The NP index showed a rapidly increasing trend, indicating that the number of patches increased rapidly. 6) The PD index showed a rapidly increasing trend in the patch density, which was closely related to the rapid increase in large-area patches. Over the past 30 years, the landscape characteristics of coastal wetlands showed (a) significant increasing trends in the number of large-area patches and total patches, (b) more complex and regular distributions of patch shapes over time, and (c) a more cohesive distri bution of patches over time.
second principal components (FPC and SPC, respectively) was 71%, and the FPC explained 51% of the variation in HF. To analyze the relation ship between HF and ELHSF, the FPC was used to represent HF; SNFE, SNFL, AIFE, and AIFL were used to represent ichthyoplankton; and the relationships between HF and ichthyoplankton were investigated. HF and ichthyoplankton showed diametrically opposite trends (Fig. 5). The FPC showed a strong increasing trend from 1985 to 2015 (Slope: 247000), but the SNFE, SNFL, AIFE and AIFL showed significant decreasing trends from 1982 to 2014 (Slope(SNFE): -0.831, Slope(SNFL): -0.524, Slope(AIFE): -0.0109, Slope(AIFL): -0.0474). Driven by land recla mation activities, the landscape pattern of coastal wetland habitats showed a severe fragmentation trend. As a result, the environmental factors of the ichthyoplankton spawning ground and nursery ground have changed drastically and profoundly, affecting the biomass and biodiversity of ichthyoplankton (Fig. 6). 4. Discussion 4.1. Impact of marine reclamation on the coastal environment
3.4. Relationships between HF and ichthyoplankton
Over the past 10 years, nearly ~1000 km2 or ~50% of the coastal wetlands in China have been lost due to marine reclamation (Liu et al.,
We analyzed the variables by performing principal component analysis (PCA) (Table 3). The cumulative proportion of the first and 7
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Fig. 7. Spatial characteristics of marine reclamation activities and spawning grounds in the Shandong Peninsula during two historical periods (1990 and 2008–2009).
As many key fish habitats (especially ELHSF habitats) surround reclamation regions, reclamation activities will directly lead to a decline in fish habitat and deeply reshape ecological connectivity, ultimately leading to the disappearance of the original habitat (Bian et al., 2018; Jin et al., 2015; Xu et al., 2018; Zhang et al., 2012). After studying the changes in the habitat of Chinese mitten crabs (Eriocheir sinensis) in the Yangtze River Estuary, Xue et al. (2016) showed that the original ecological functions of suitable habitat areas and habitat connectivity have been drastically destroyed because of the pressure from reclama tion activities. The spatial distribution characteristics of the reclamation and spawning grounds in the offshore area of Shandong Peninsula in 1990 and 2008–2009 were compared, which indicated that the scale of reclamation in 2010 was stronger than that in 1990, with a larger patch area and more concentrated spatial distribution. However, the spawning grounds showed larger areas and greater spatial continuity in 1990 than in 2008–2009 (Fig. 7). HF will impact ELHSF recruitment by reshaping the quality and distribution to the fish spawning ground (Figs. 5 and 7). Under the impact of reclamation activities on the ELHSF habitat in the Pearl River Delta, the number of fish species, habitat density and biomass decreased by more than 70% compared with historical fishery stock assessments (Yu et al., 2016).
2008; Tian et al., 2016; Wang et al., 2014). As a result, the land use and land cover changes (LUCCs) in coastal zones have rapidly transformed from natural to artificial landscapes, which has led to many environ mental problems (Guo et al., 2007; Shi et al., 2010) (Fig. 6). The reclamation projects weakened the exchange rate between seawater and freshwater and reduced self-purification and nutrient cycling (Wang et al., 2014), which led to generally declining trends in the stability of phytoplankton and zooplankton density. Furthermore, the dominant species and community structure underwent dramatic ecological suc cession to suit the new habitats (Li et al., 2010; Yang et al., 2011). However, reclamation activities still had a positive ecological effect in some coastal regions. Chen et al. (1998) noted that reclamation projects had a positive effect on maintaining the stability of the intertidal ecological environments of the coastal zones in the Yangtze River Delta. 4.2. Negative impacts of marine reclamation patches on fish habitat Reclamation activities will not only shrink the spatial distribution of ELHSF but also deeply change ecological factors. The negative impacts of reclamation projects on coastal fish habitats mainly include water pollution and HF (Fig. 6). Water pollution in reclamation regions mainly includes high concentrations of suspended sediment material, eutrophic substances, heavy metal pollution, and microplastics. High concentra tions of suspended sediment materials prohibit light propagation and reduce net primary productivity (NPP). Eutrophic substances are the main driving factor of large algal blooms and are also important factors that indirectly lead to hypoxia in coastal regions (Cosme et al., 2016; Shi et al., 2017). Heavy metals are a special type of pollution that can become enriched in the muscles and organs of shellfish and fish and pose a great risk to human health through the food chain (Hou et al., 2018; Lv et al., 2014; Mcleod et al., 2011; Yang et al., 2011).
5. Summary In summary, coastal wetland landscapes have been deeply reshaped by reclamation activities, and these areas show (a) significant increasing trends in the number of large-area patches and total patches, (b) more complex and regular distributions of patch shapes, and (c) more cohe sive distributions of patches. As a result, the environmental factors of ichthyoplankton spawning and nursery grounds have changed drasti cally, which has profoundly affected the biomass and biodiversity of 8
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ichthyoplankton. Future studies on the effects of marine reclamation activities on ELHSF habitat should focus on investigating and exploring the underlying biological mechanisms in the spawning grounds and nursery grounds.
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Declaration of competing interest We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled. Acknowledgments Funding for this work was provided by the National Research Pro gram of China, No. 2017YFE0104400, the National Basic Research Program of China under contract (No. 2015CB453303), the Taishan Scholar Project Special Fund, the “Aoshan Talent” Project Financially Supported by Pilot National Laboratory for Marine Science and Tech nology (Qingdao) (No. 2017ASTCP-ES07), and the National Natural Science Foundation of China (No. 41506168). The authors also thank the editor and reviewers for their thoughtful and thorough reviews, which greatly improved the manuscript. References Bakker, M.M., Doorn, A.M.V., 2009. Farmer-specific relationships between land use change and landscape factors: introducing agents in empirical land use modeling. Land Use Policy 26 (3), 809–817. https://doi.org/10.1016/j. landusepol.2008.10.010. Bian, X.D., Wan, R.J., Jin, X.S., et al., 2018. Ichthyoplankton succession and assemblage structure in the Bohai Sea during the past 30 years since 1980s. Prog. Fish. Sci. 39 (2), 1–15. https://doi.org/10.19663/j.issn2095-9869.20170911001 (In Chinese). Chen, X., Zong, Y., 1998. Coastal erosion along the Changjiang deltaic shoreline, China: history and prospective. Estuarine. Coast Shelf Sci. 46 (5), 733–742. https://doi.org/ 10.1006/ecss.1997.0327. Cosme, N., Hauschild, M.Z., 2016. Effect factors for marine eutrophication in LCIA based on species sensitivity to hypoxia. Ecol. Indicat. 69, 453–462. https://doi.org/ 10.1016/j.ecolind.2016.04.006. Duan, H., Zhang, H., Huang, Q., et al., 2016. Characterization and environmental impact analysis of sea land reclamation activities in China. Ocean Coast Manag. 130, 128–137. https://doi.org/10.1016/j.ocecoaman.2016.06.006. Forman, R.T.T., 1995. Some general principles of landscape and regional ecology. Landsc. Ecol. 10 (3), 133–142. https://doi.org/10.1007/BF00133027. Guo, H., Jiao, J.J., 2007. Impact of coastal land reclamation on ground water level and the sea water interface. Gr. Water 45 (3), 362–367. https://doi.org/10.1111/j.17456584.2006.00290.x. Hadley, W., 2009. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York. Hou, X.Y., Zhang, H., Li, D., et al., 2018. Development trend, environmental and ecological impacts, and policy recommendations for Bohai Sea reclamation. Acta Ecol. Sin. 38 (9), 3311–3319. https://doi.org/10.5846/stxb201706261145 (in Chinese). Jeremy, V.D., Lorena, F., Stephanie, J., et al., 2014. SDMTools: Species Distribution Modeling Tools: Tools for Processing Data Associated with Species Distribution Modeling Exercises. R Package Version 1.1-221. https://CRAN.R-project.org/pack age¼SDMTools. Jin, X.S., 2004. Long-term changes in fish community structure in the Bohai Sea, China. Estuarine. Coast Shelf Sci. 59 (1), 163–171. https://doi.org/10.1016/j. ecss.2003.08.005. Jin, X.S., Dou, S.Z., Shan, X.J., et al., 2015. Hot spots of frontiers in the research of sustainable yield of Chinese inshore fishery. Prog. Fish. Sci. 36 (01), 124–131. https://doi.org/10.11758/yykxjz.20150119 (in Chinese). Li, K., Liu, X., Zhao, X., et al., 2010. Effects of reclamation projects on marine ecological environment in Tianjin Harbor Industrial Zone. Procedia Environ. Sci. 2, 792–799. https://doi.org/10.1016/j.proenv.2010.10.090. Li, J., Liu, Y., Yang, Y., 2018. Land use change and effect analysis of tideland reclamation in Hangzhou Bay. J. Mt. Sci. 15 (2), 394–405. https://doi.org/10.1007/s11629-0174542-5. Liu, W., Liu, B.Q., 2008. Current situation and countermeasures of sea reclamation in China. J. Guangzhou Environ. Sci. 23 (2), 26–30 (in Chinese).
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Variations in fish habitat fragmentation caused by marine reclamation activities in the Bohai coastal region, China Xiaosong Ding a, b, Xiujuan Shan b, c, *, Yunlong Chen b, Miao Li a, b, Jiajia Li a, d, Xianshi Jin b, c a
College of Marine Sciences, Shanghai Ocean University, Shanghai, 201306, China Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs; Shandong Provincial Key Laboratory of Fishery Resources and Eco-environment; Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China c Laboratory for Marine Fisheries Science and Food Production Processes; Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China d Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture and Rural Affairs, Qingdao Key Laboratory for Marine Fish Breeding and Biotechnology, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China b
A R T I C L E I N F O
A B S T R A C T
Keywords: Marine reclamation Fish habitat fragmentation Fish recruitment Coastal wetland
Due to the development of the social economy and population density pressure, coastal reclamation activities have rapidly increased throughout coastal regions in China and have had a significant negative impact on fish habitat fragmentation (especially on the habitat of the early life history stage of fish, ELHSF). However, few studies have focused on the negative ecological impacts of reclamation patches on ELHSF habitats (such as spawning, nursery, and feeding grounds). Data on marine reclamation were extracted from 49 Landsat remote sensing images from 7 different periods from 1985 to 2015, and ichthyoplankton data from 1982 to 2014 were compiled. The trend of fragmentation showed that the number of artificial heterogeneous patches significantly increased, and the isolation of habitat landscape became more intense. As a result, the spatial patterns of ich thyoplankton habitat rapidly transformed from a continuous and integral distribution to a divided and frag mented distribution, which drastically changed numerous environmental factors and deeply reshaped normal fish recruitment activities by impacting the number and abundance of ELHSF.
1. Introduction Due to the limited urban land area and the sharp increase in the population density in coastal zones, low-cost, short-cycle and high-profit marine reclamation projects have rapidly increased in prevalence throughout coastal regions in China (Yang et al., 2011; Wang et al., 2010, 2014). Four stages of large-scale marine reclamation activities have occurred since the establishment of the People’s Republic of China (after 1949) (Liu et al., 2008; Wang et al., 2014; Zhu et al., 2016): (1) The first stage (1949–1960): salt grounds were spread throughout the coastal region for the extraction of salt from seawater. The Changlu salt ground was built and expanded into the largest salt area in China at this stage (Liu et al., 2008). (2) The second stage (1960–1980): agricultural developments were implemented to increase the food and agricultural resources in the coastal region. Due to the increase in agricultural land, the coastal tidal flat disappeared (Liu et al., 2008; Tian et al., 2016). (3)
The third stage (1980–1990): marine aquaculture quickly spread throughout the coastal wetland to meet the needs of society for aquatic foods. Marine aquaculture has led to severe eutrophication in coastal waters (Liu et al., 2008; Wang et al., 2014). (4) The fourth stage (1990-present): reclamation activities mainly included those for harbor, industry, and urbanization land use in the coastal zone. Currently, the different land use types that were developed in the four periods coexist and affect the coastal environment. With the development of reclama tion activities, fish habitat is undergoing severe fragmentation (espe cially for spawning, nursery and feeding grounds) (Bakker et al., 2009; Wang et al., 2010; Yu et al., 2016). Fragmented habitat will lead to negative effects on the normal activities of fish migration, reproduction and population replenishment (Bakker et al., 2009; Wu et al., 2002; Yang et al., 2011; Zhao et al., 2004). However, quantitative and sys tematic studies on the effects of marine reclamation on the early life history stage of fish (ELHSF) are lacking.
* Corresponding author. Laboratory for Marine Fisheries Science and Food Production Processes; Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao, 266237, China. E-mail address: [email protected] (X. Shan). https://doi.org/10.1016/j.ocecoaman.2019.105038 Received 5 May 2019; Received in revised form 9 October 2019; Accepted 23 October 2019 0964-5691/© 2019 Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
Please cite this article as: Xiaosong Ding, Ocean and Coastal Management, https://doi.org/10.1016/j.ocecoaman.2019.105038
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Fig. 1. Spatial distribution of reclamation projects in the Bohai coastal region, China. Table 1 Fragmentation indexes and their significance in this study. No.
Index
Significance
1
AI (aggregation index)
A small AI indicates that the patch is made up of many small patches; thus, the spatial aggregation is not strong.
Formula
2
MPA (mean patch area)
A small MPA indicates that the landscape is highly fragmented, and vice versa.
3
MPFD (mean patch fractal dimension)
A MPFD value close to 1 indicates that the degree of similarity is high in the same patch type and the spatial distribution of the patches is regular.
I ¼ 2 lnðnÞ þ 100%
A MSI value of 1 indicates that all patches are square, and a high index indicates that the shape of the patch is irregular.
5 6
NP (number of patches) PD (patch density)
A large NP corresponds to a high degree of fragmentation, and vice versa. A high PD corresponds to a high degree of fragmentation in the landscape pattern, and vice versa.
Habitat fragmentation (HF) is a very useful way to study the rela tionship between reclamation patches and ELHSF habitat (Forman, 1995; Nadzir et al., 2014; Wu et al., 2002). However, current studies have been limited to analyzing the characteristics of HF, and discussions of fish habitat isolation under the impacts of reclamation activities are lacking (XU et al., 2015; Yang et al., 2018; Zhang et al., 2016). Habitat isolation and environmental factor changes are the main negative im pacts of reclamation activities on ELHSF habitat. Based on the fish HF characteristics and the ELHSF data, the relationship between reclama tion activities and fish habitat can be systematically discussed (Li et al., 2018; Rendenieks et al., 2017; XU et al., 2015). In this paper, we study the impact of coastal wetland fragmentation resulting from marine reclamation and discuss the relationship with the
ðPij Þ � lnðPi Þ �
0 < AI�100
MPA>0 1 � MPFD�2
MPDF ¼ � 2 lnð0:25Lij Þ lnðAreaij Þ Pm Pn i¼1 j¼1 NPij ! Pm Pn 0:25Lij i¼1 j¼1 pffiffiffiffiffiffiffiffiffiffiffiffi Areaij Pm Pn MSI ¼ i¼1 j¼1 NPij — Pn NPi PD ¼ Pni¼1 i¼1 Areai i¼1
MSI (mean shape index)
i¼1 j¼1
NPi MPA ¼ Pn i¼1 NPi
Pm Pn 4
Others m P n P
�
j¼1
MSI�1
NP � 1 PD � 0
ELHSF. The results of this study will support marine reclamation man agement and fish habitat protection in the future. 2. Materials and methods 2.1. Study area The Bohai Sea (37� 070 -41� 000 N, 117� 350 -121� 100 E, Fig. 1) is a semienclosed inland sea in China that has an area of approximately 7.7 � 104 km2. The Bohai coastal region is an important habitat for the ELHSF and represents important spawning, nursery and feeding grounds for fishery resources in the Yellow Sea and Bohai Sea (Jin, 2004; Yang et al., 2011; Zhang et al., 2007). Inputs from many rivers, such as the 2
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Fig. 2. Changes in the areas of reclamation projects in the bays of the Bohai coastal region from 1985 to 2015. Table 2 Dynamics of the AI, MPA, MPFD, MSI, NP and PD indicators for different types of reclamation projects. Time
Type
AI
MPA (1 � 106)
MPFD
MSI
NP
PD (1 � 10 8)
1985–1990
Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land Aquaculture Land Harbor Land Industrial Land Salt Land Unused Land
92.00 83.73 85.33 94.16 90.72 93.62 85.14 89.82 95.60 92.79 93.73 86.55 80.68 96.01 93.02 94.36 90.46 91.64 96.15 95.94 95.63 93.19 96.47 96.17 95.69 96.38 93.89 96.54 96.83 96.68
2.13 0.22 0.33 3.75 1.84 3.17 0.43 0.35 6.65 2.04 3.63 0.64 0.56 7.82 2.99 4.12 0.91 1.62 8.48 6.01 7.99 1.53 7.43 9.62 6.81 11.00 2.14 11.60 16.70 10.50
1.06 1.05 1.04 1.05 1.04 1.06 1.06 1.04 1.05 1.04 1.07 1.06 1.06 1.05 1.05 1.07 1.06 1.06 1.05 1.06 1.07 1.06 1.07 1.05 1.06 1.07 1.06 1.07 1.06 1.06
1.53 1.32 1.30 1.48 1.38 1.55 1.46 1.31 1.48 1.42 1.61 1.47 1.41 1.50 1.46 1.67 1.49 1.52 1.52 1.48 1.72 1.51 1.60 1.54 1.50 1.73 1.52 1.75 1.63 1.51
135 20 6 6 30 144 21 9 30 41 158 31 20 31 33 205 46 23 37 56 141 64 73 47 51 123 103 90 33 26
3.60 3.04 0.26 0.97 0.76 5.46 3.06 0.89 1.82 28.70 13.10 3.07 0.90 2.37 3.59 16.80 3.29 1.05 3.29 3.51 19.20 3.77 1.20 3.99 1.97 5.46 4.25 1.28 4.00 6.38
1990–1995
1995–2000
2000–2005
2005–2010
2005–2010
3
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Fig. 3. Characteristics of the fragmentation indexes from 1985 to 2015.
Yellow River, Haihe River, Weihe River, and Liaohe River, have enriched the abundance of bait organisms and have made the offshore waters important spawning and habitat grounds for many fishery groups, such as fish, shrimp, crab, shellfish and cephalopods. The coastal area of the Bohai Sea covers 4 provinces (Liaoning Province, Hebei Province, Tianjin City and Shandong Province). The coastal area has a high population density and a high density of social and economic activities. The spatial density of reclamation projects, such as large ports, aquaculture, and tourism infrastructure, is very high (Pelling et al., 2013; Duan et al., 2016; Wang et al., 2014).
Bohai coastal region. 2.2.2. Extraction method for reclamation projects After geometric correction and coordinate transformation, the coastline in 1985 (denoted coastline1985) was extracted via visual interpretation and used as the benchmark to extract land reclamation projects. The extraction rules for the reclamation projects were as fol lows: all of the extracted reclamation projects must refer to the bench mark (Shoreline1985) and the texture, shape, color, etc., during the historical periods (1985–1990, 1990–1995, 1995–2000, 2000–2005, 2005–2010, 2010–2015). The reclamation project must be compared to Google Maps (GM) via overlapping to ensure the precision of the extracted area; otherwise, the project must be re-extracted from the image. Using this procedure, we acquired the spatiotemporal distribution of marine reclamation projects for different periods. The marine reclama tion types were divided into Aquaculture Land (land used for marine aquaculture), Harbor Land (land used for harbor), Industrial Land (land used for industrial and urban), Salt Land (land used for saltern) and Unused Land (land that has been reclaimed but not used). The preprocessing of Landsat images was performed using ENVI (ENVI 5.2 SP1, ITT Visual Information Solutions, Boulder, CO, USA, 2015), and the reclamation projects were extracted based on visual
2.2. Extraction method for reclamation projects 2.2.1. Satellite data The Landsat remote sensing data used in this article were from the official USGS website (https://earthexplorer.usgs.gov/), and they included 7 periods (1985, 1990, 1995, 2000, 2005, 2010 and 2015) and 7 images per period for a total of 49 images. Each image had limited cloud coverage to ensure that the accuracy of the subsequent image interpretation was not impacted. The additional data included China’s administrative division map (spatial scale: 1:4,000,000), a topographic map (spatial scale: 1:4,000,000), a nature reserve map of the Bohai coastal region, and the regional economic statistics yearbook for the 4
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Fig. 4. Fragmentation trends of coastal wetland landscape patterns.
interpretation by experts in ArcGIS (ESRI ArcGIS Desktop 10.2) software.
Table 3 Evaluation parameters and score coefficients of the principal components. Index
PC1
PC2
PC3
PC4
PC5
PC6
AI MPA MPFD MSI NP PD Std. Deviation (SD) Proportion of Variance (%) Cumulative Proportion (%)
0.44 0.50 0.49 0.57 0.03 0.01 1.74 51
0.39 0.01 0.22 0.08 0.71 0.53 1.06 20
0.08 0.11 0.03 0.04 0.57 0.81 0.98 16
0.59 0.14 0.68 0.01 0.35 0.23 0.63 7
0.47 0.79 0.33 0.03 0.19 0.04 0.61 6
0.28 0.31 0.39 0.82 0.06 0.08 0.12 0
51
71
87
94
100
100
2.3. Ichthyoplankton data The ichthyoplankton data were from a historical survey of the Bohai Sea by the Fishery Resources and Eco-environment Lab (Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences). The data included the species number of fish eggs (SNFE), species number of fish larvae (SNFL), abundance index of fish eggs (AIFE), and abundance index of fish larvae (AIFL). The data were obtained by horizontally towing a zooplankton net (mouth diameter 80 cm, length 270 cm, mesh size 0.50 mm) in the Bohai Sea. The survey periods included 1982–1983, 1992–1993, 2013–2014, and 2014–2015. 2.4. Fragmentation index To quantitatively study HF, 6 indexes were used to study the land scape fragmentation characteristics along the coastal region at the 5
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Fig. 5. Variations in SNFE, SNFL, AIFE, AIFL, and FPC from 1982 to 2015.
spatiotemporal scale (Table 1) (McGarigal et al., 2002; Rendenieks et al., 2017; Yan et al., 2017). The “SDMTools” package (Jeremy et al., 2014) was used to calculate the marine reclamation fragmentation index, and the data were visual ized using the “ggplot2” (Hadley, 2009) and “sp” packages (Pebesma et al., 2005) in R software.
The area of Unused Land fluctuated throughout the study period. 3.2. HF variation The patches created by the reclamation projects extensively altered the landscape patterns in the coastal wetland region from 1985 to 2015 (Table 2, Fig. 3). The main fragmentation characteristics of the patches were as follows: highly aggregative and exhibiting increasing area, increasing MPFD, increasing MSI, increasing NP, and increasing PD. However, different patch types exhibited different characteristics in different regions. The largest increase in the AI occurred in the Industrial Land patches (increase units: 11.21), and the smallest increase occurred in the Salt Land patches (increase units: 2.67). The largest increase in the MPA index was found in the Salt Land patches (increase units: 1.29 � 107), and the smallest was found in the Unused Land patches (increase units: 8.68 � 106). The largest increase in the MPFD index was found in the Industrial Land patches (increase units: 0.03), and the smallest increase was found in the Salt Land patches (increase units: 0.01). The largest increase in the MSI was found in the Industrial Land patches (increase units: 0.45), and the smallest was found in the Unused Land patches (increase units: 0.12). A significant increase in the NP index was observed for all reclamation types, although the Aquaculture Land patches showed a decreasing trend in NP after 2000. The PD index showed a significant increasing trend, which was closely related to the rapid increase in MPA.
3. Results 3.1. Dynamics of reclamation patches The analysis of the changes in the proportions of marine reclamation types from 1985 to 2015 indicated that all of the patch areas showed increasing trends (Figs. 1 and 2). Among these areas, the Unused Land, Industrial Land and Salt Land patches showed significant increasing trends, while the Aquaculture Land patch areas increased at a slower rate than the other patch types. The increasing trend was not uniform throughout the Bohai coastal region and varied during the different time periods (Fig. 2). The area of Aquaculture Land showed rapid growth from 1995 to 2005 in the coastal regions of Laizhou Bay and Bohai Bay, and the growth rate slowed after 2005. The area of Harbor Land showed a sig nificant increasing trend from 2000 to 2005, and the growth rate was highest near Bohai Bay, followed by the Laizhou Bay coastal region and the Liaodong Bay coastal region. The area of Salt Land exhibited sig nificant increases in the coastal regions of all three bays. In the Laizhou Bay coastal region, the Salt Land area showed a significant increasing trend throughout the study period. In the Bohai Bay coastal region, the Salt Land area reached its highest value in 2000–2005, and in the Liaodong Bay coastal region, it reached its highest value in 1990–2005.
3.3. Trend of fragmentation of coastal wetlands The fragmentation characteristics of the marine reclamation patches 6
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Fig. 6. Relationship between coastal wetland reclamation and ELHSF.
showed the following characteristics (Fig. 4): 1) The AI showed a rapidly increasing trend, indicating that the spatial aggregation of various patches was strong. 2) The MPA index showed a rapidly increasing trend, indicating an increase in large patch areas. 3) The MPFD index was concentrated from 1.05–1.065, indicating a significant increase in the degree of similarity. 4) The MSI showed a rapidly increasing trend, indicating that the geometric shapes of the patches deviated from a square and increased in complexity. 5) The NP index showed a rapidly increasing trend, indicating that the number of patches increased rapidly. 6) The PD index showed a rapidly increasing trend in the patch density, which was closely related to the rapid increase in large-area patches. Over the past 30 years, the landscape characteristics of coastal wetlands showed (a) significant increasing trends in the number of large-area patches and total patches, (b) more complex and regular distributions of patch shapes over time, and (c) a more cohesive distri bution of patches over time.
second principal components (FPC and SPC, respectively) was 71%, and the FPC explained 51% of the variation in HF. To analyze the relation ship between HF and ELHSF, the FPC was used to represent HF; SNFE, SNFL, AIFE, and AIFL were used to represent ichthyoplankton; and the relationships between HF and ichthyoplankton were investigated. HF and ichthyoplankton showed diametrically opposite trends (Fig. 5). The FPC showed a strong increasing trend from 1985 to 2015 (Slope: 247000), but the SNFE, SNFL, AIFE and AIFL showed significant decreasing trends from 1982 to 2014 (Slope(SNFE): -0.831, Slope(SNFL): -0.524, Slope(AIFE): -0.0109, Slope(AIFL): -0.0474). Driven by land recla mation activities, the landscape pattern of coastal wetland habitats showed a severe fragmentation trend. As a result, the environmental factors of the ichthyoplankton spawning ground and nursery ground have changed drastically and profoundly, affecting the biomass and biodiversity of ichthyoplankton (Fig. 6). 4. Discussion 4.1. Impact of marine reclamation on the coastal environment
3.4. Relationships between HF and ichthyoplankton
Over the past 10 years, nearly ~1000 km2 or ~50% of the coastal wetlands in China have been lost due to marine reclamation (Liu et al.,
We analyzed the variables by performing principal component analysis (PCA) (Table 3). The cumulative proportion of the first and 7
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Fig. 7. Spatial characteristics of marine reclamation activities and spawning grounds in the Shandong Peninsula during two historical periods (1990 and 2008–2009).
As many key fish habitats (especially ELHSF habitats) surround reclamation regions, reclamation activities will directly lead to a decline in fish habitat and deeply reshape ecological connectivity, ultimately leading to the disappearance of the original habitat (Bian et al., 2018; Jin et al., 2015; Xu et al., 2018; Zhang et al., 2012). After studying the changes in the habitat of Chinese mitten crabs (Eriocheir sinensis) in the Yangtze River Estuary, Xue et al. (2016) showed that the original ecological functions of suitable habitat areas and habitat connectivity have been drastically destroyed because of the pressure from reclama tion activities. The spatial distribution characteristics of the reclamation and spawning grounds in the offshore area of Shandong Peninsula in 1990 and 2008–2009 were compared, which indicated that the scale of reclamation in 2010 was stronger than that in 1990, with a larger patch area and more concentrated spatial distribution. However, the spawning grounds showed larger areas and greater spatial continuity in 1990 than in 2008–2009 (Fig. 7). HF will impact ELHSF recruitment by reshaping the quality and distribution to the fish spawning ground (Figs. 5 and 7). Under the impact of reclamation activities on the ELHSF habitat in the Pearl River Delta, the number of fish species, habitat density and biomass decreased by more than 70% compared with historical fishery stock assessments (Yu et al., 2016).
2008; Tian et al., 2016; Wang et al., 2014). As a result, the land use and land cover changes (LUCCs) in coastal zones have rapidly transformed from natural to artificial landscapes, which has led to many environ mental problems (Guo et al., 2007; Shi et al., 2010) (Fig. 6). The reclamation projects weakened the exchange rate between seawater and freshwater and reduced self-purification and nutrient cycling (Wang et al., 2014), which led to generally declining trends in the stability of phytoplankton and zooplankton density. Furthermore, the dominant species and community structure underwent dramatic ecological suc cession to suit the new habitats (Li et al., 2010; Yang et al., 2011). However, reclamation activities still had a positive ecological effect in some coastal regions. Chen et al. (1998) noted that reclamation projects had a positive effect on maintaining the stability of the intertidal ecological environments of the coastal zones in the Yangtze River Delta. 4.2. Negative impacts of marine reclamation patches on fish habitat Reclamation activities will not only shrink the spatial distribution of ELHSF but also deeply change ecological factors. The negative impacts of reclamation projects on coastal fish habitats mainly include water pollution and HF (Fig. 6). Water pollution in reclamation regions mainly includes high concentrations of suspended sediment material, eutrophic substances, heavy metal pollution, and microplastics. High concentra tions of suspended sediment materials prohibit light propagation and reduce net primary productivity (NPP). Eutrophic substances are the main driving factor of large algal blooms and are also important factors that indirectly lead to hypoxia in coastal regions (Cosme et al., 2016; Shi et al., 2017). Heavy metals are a special type of pollution that can become enriched in the muscles and organs of shellfish and fish and pose a great risk to human health through the food chain (Hou et al., 2018; Lv et al., 2014; Mcleod et al., 2011; Yang et al., 2011).
5. Summary In summary, coastal wetland landscapes have been deeply reshaped by reclamation activities, and these areas show (a) significant increasing trends in the number of large-area patches and total patches, (b) more complex and regular distributions of patch shapes, and (c) more cohe sive distributions of patches. As a result, the environmental factors of ichthyoplankton spawning and nursery grounds have changed drasti cally, which has profoundly affected the biomass and biodiversity of 8
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ichthyoplankton. Future studies on the effects of marine reclamation activities on ELHSF habitat should focus on investigating and exploring the underlying biological mechanisms in the spawning grounds and nursery grounds.
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Declaration of competing interest We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled. Acknowledgments Funding for this work was provided by the National Research Pro gram of China, No. 2017YFE0104400, the National Basic Research Program of China under contract (No. 2015CB453303), the Taishan Scholar Project Special Fund, the “Aoshan Talent” Project Financially Supported by Pilot National Laboratory for Marine Science and Tech nology (Qingdao) (No. 2017ASTCP-ES07), and the National Natural Science Foundation of China (No. 41506168). The authors also thank the editor and reviewers for their thoughtful and thorough reviews, which greatly improved the manuscript. References Bakker, M.M., Doorn, A.M.V., 2009. Farmer-specific relationships between land use change and landscape factors: introducing agents in empirical land use modeling. Land Use Policy 26 (3), 809–817. https://doi.org/10.1016/j. landusepol.2008.10.010. Bian, X.D., Wan, R.J., Jin, X.S., et al., 2018. Ichthyoplankton succession and assemblage structure in the Bohai Sea during the past 30 years since 1980s. Prog. Fish. Sci. 39 (2), 1–15. https://doi.org/10.19663/j.issn2095-9869.20170911001 (In Chinese). Chen, X., Zong, Y., 1998. Coastal erosion along the Changjiang deltaic shoreline, China: history and prospective. Estuarine. Coast Shelf Sci. 46 (5), 733–742. https://doi.org/ 10.1006/ecss.1997.0327. Cosme, N., Hauschild, M.Z., 2016. Effect factors for marine eutrophication in LCIA based on species sensitivity to hypoxia. Ecol. Indicat. 69, 453–462. https://doi.org/ 10.1016/j.ecolind.2016.04.006. Duan, H., Zhang, H., Huang, Q., et al., 2016. Characterization and environmental impact analysis of sea land reclamation activities in China. Ocean Coast Manag. 130, 128–137. https://doi.org/10.1016/j.ocecoaman.2016.06.006. Forman, R.T.T., 1995. Some general principles of landscape and regional ecology. Landsc. Ecol. 10 (3), 133–142. https://doi.org/10.1007/BF00133027. Guo, H., Jiao, J.J., 2007. Impact of coastal land reclamation on ground water level and the sea water interface. Gr. Water 45 (3), 362–367. https://doi.org/10.1111/j.17456584.2006.00290.x. Hadley, W., 2009. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York. Hou, X.Y., Zhang, H., Li, D., et al., 2018. Development trend, environmental and ecological impacts, and policy recommendations for Bohai Sea reclamation. Acta Ecol. Sin. 38 (9), 3311–3319. https://doi.org/10.5846/stxb201706261145 (in Chinese). Jeremy, V.D., Lorena, F., Stephanie, J., et al., 2014. SDMTools: Species Distribution Modeling Tools: Tools for Processing Data Associated with Species Distribution Modeling Exercises. R Package Version 1.1-221. https://CRAN.R-project.org/pack age¼SDMTools. Jin, X.S., 2004. Long-term changes in fish community structure in the Bohai Sea, China. Estuarine. Coast Shelf Sci. 59 (1), 163–171. https://doi.org/10.1016/j. ecss.2003.08.005. Jin, X.S., Dou, S.Z., Shan, X.J., et al., 2015. Hot spots of frontiers in the research of sustainable yield of Chinese inshore fishery. Prog. Fish. Sci. 36 (01), 124–131. https://doi.org/10.11758/yykxjz.20150119 (in Chinese). Li, K., Liu, X., Zhao, X., et al., 2010. Effects of reclamation projects on marine ecological environment in Tianjin Harbor Industrial Zone. Procedia Environ. Sci. 2, 792–799. https://doi.org/10.1016/j.proenv.2010.10.090. Li, J., Liu, Y., Yang, Y., 2018. Land use change and effect analysis of tideland reclamation in Hangzhou Bay. J. Mt. Sci. 15 (2), 394–405. https://doi.org/10.1007/s11629-0174542-5. Liu, W., Liu, B.Q., 2008. Current situation and countermeasures of sea reclamation in China. J. Guangzhou Environ. Sci. 23 (2), 26–30 (in Chinese).
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