Decrease in population of swans (Cygnus spp.) due to the development of areas adjacent to the wintering site

This study aimed to analyze the relationship between Cygnus spp. population trends and land-use changes and artificial development activities in the Nakdonggang Estuary for the necessity of management to the buffer area outside the protected area boundary in Korea. Analysis of the 15-year population change revealed a sharp decline in the Cygnus columbianus population in the winter, which could be attributed to the Nakdonggang Estuary becoming unfeasible as their wintering site. In contrast, there was no sharp decline in the Cygnus cygnus population, although a moderate decline was identified. Over the past 30 years, farmland activities decreased by approximately 10% in the areas adjacent to the protected area resulting from the expansion of the urbanized area. The rate of decrease in the water body area was high, attributed to urban development through reclamation. The correlation analysis between the area (ha) of paddy fields and the monthly (Nov.–Feb.) population of C. columbianus indicated that the populations in December (R2 = 0.768) and January (R2 = 0.743) were more correlated with the change in paddy field areas than those in the early winter (November: R2 = 0.457) and at the end of winter (February: R2 = 0.582). In the case of C. cygnus, the population tended to increase with increases in the areas of paddy fields, but the statistical explanatory power was low. We identified a distinct difference in that C. columbianus was more sensitive to urbanization than C. cygnus in the Nakdonggang Estuary.


Introduction
The Global Wetland Outlook (Ramsar Convention on Wetlands 2018) of the Ramsar Convention reported, with great concern, on the continued decline in wetland areas around the world. According to the report, about 35% of natural wetlands had declined as of 2015. In addition, it was reported that biodiversity is also being greatly affected by the decline in wildlife habitats. Compared with 1970, wetland-dependent species, such as waterfowl, are said to be exhibiting a serious decline, with decreases of 81% of inland wetland species and 36% of coastal and marine species. This rapid decrease in waterfowl is reported to be directly affected by changes in their habitats due to land-use change and the lack of food resources due to habitat damage (Burton et al. 2006).
In the case of migratory birds, management of both wintering and breeding areas is an important issue for ensuring waterfowl habitat stability, as the success rate in breeding areas increases only if the birds can maintain adequate body condition with sufficient food resources (Inger et al. 2010). Located on the East Asian oceanic migratory bird movement route, Korea hosts 40 key biodiversity areas nationwide, which are important internationally as major migratory bird destinations. Most of them are concentrated in the estuaries of large-scale rivers, and that of the Nakdonggang River is Korea's representative Migratory Bird Sanctuary, Natural Monument Area and National Wetland Protected Area. Due to the characteristics of the estuary, wild birds congregate in the area during the winter due to the formation of brackish water and tidal flats.
Three species of Cygnus spp. in Korea: Cygnus cygnus, C. columbianus, and C. olor, all of which are classified as being of the least concern (LC) ). However, when limited to the Korean Peninsula, the winter habitat disturbance and population decline of Cygnus spp. are evident, and C. cygnus and C. columbianus are classified as vulnerable (VU), while C. olor is classified as endangered (EN) on the national red list. In addition, it is legally designated and managed as an Endangered Species and Natural Monument. Among these species, a relatively large number of individuals winter across the country; therefore, it is important to examine the changes in the number of individuals by region. In the research by Choi et al. (2018) on the changes in the numbers of large Cygnus spp. in 112 locations nationwide, the Nakdonggang Estuary was the site with the largest decrease among all surveyed districts. The proportion of wintering individuals at the mouth of the Nakdonggang River has decreased by about 10% from a quarter of those wintering nationwide. Nevertheless, the largest number of Cygnus spp. winter at the mouth of the Nakdonggang River historically and today among monitoring sites nationwide. Considering the decrease in the distribution ratio of wintering individuals at the mouth of the Nakdonggang River, it is a highly important wintering site for Cygnus spp. in Korea, but the wintering environment is rapidly deteriorating.
Since 1999, the Ministry of Environment and the National Institute of Environmental Research has formed the Winter Waterbird Census Program to collect winter bird information throughout the country (National Institute of Biological Resources; NIBR 2020). The simultaneous collection of national data does not have a long history compared with that in other countries; therefore, long-term studies related to migratory populations and habitats have not yet been conducted (Kim et al. 2017). Although the period is relatively short, the results of a survey (NIBR 2020) conducted at the mouth of the Nakdonggang River for about 20 years (1999-2019) from 1999, when the national simultaneous census began, are considered important as data that can accurately reflect the changing trend of the number of Cygnus spp. individuals according to habitat changes. Previous studies have been conducted on the analysis of the distribution trend of Cygnus spp. in Korea, and Kang et al. (2008) confirmed the trend of a rapid decrease in the population of Cygnus spp. from 1999 to 2007 by analyzing field survey results. Regarding the decreasing number of Cygnus spp., Hong (2020) reported that the Nakdonggang Estuary and Junam Reservoir, the largest wintering area of Cygnus spp. in Korea, are threatened by various developments. Kim and Won (1994) also reported that several natural wetlands and reservoirs are being damaged by various development projects. Kim et al. (2018) reported a decrease in the area of farmland in Korea from 24.2 to 22.9% between 1990 and 2000 due to rapid urbanization. Wintering Cygnus spp. in Northeast Asia reportedly use paddy fields as feeding and roosting areas (Watanabe et al. 2008;Fujioka et al. 2010;Shimada et al. 2014). In addition, Wang et al. (2021) investigated the behavior of Cygnus spp. in wintering sites by categorizing their behaviors as resting, vigilance, maintenance, and movement, and reported frequent movements in wintering sites with limited space from early November to late February according to the deterioration of the environment. Wood et al. (2021) reported that food competition among Cygnus spp. is a cause of such movement in feeding areas. Eventually, if certain habitats are damaged, the species outcompeted for food among Cygnus spp. may disappear faster. Regarding the behavior of Cygnus spp. in wintering areas, Weathers et al. (1984) also confirmed that they attempted to effectively maintain food acquisition efficiency and energy consumption, and Powell and Engelhardt (2000) reported that Cygnus spp. engaged in short-distance foraging flights between 2 and 10 km to conserve food and increase their energy consumption efficiency. However, such short-distance movement is only possible in wintering areas with good environments, and in poor environments, it is inevitable that they will travel longer distances (Van Gils and Tijsen 2007). In this regard, Hahm and Kim (2001) revealed that if the environment of their feeding area deteriorates, Cygnus spp. will move between the Junam Reservoir and Nakdonggang Estuary, a distance of about 35 km, during the wintering period. Although the period was relatively short, the results (NIBR 2020) of a national simultaneous census conducted at the mouth of the Nakdonggang River for about 20 years from 1999 showed that the overall population of Cygnus spp. decreased, and in particular, the population of swans (C. columbianus) decreased sharply. Korea achieved rapid economic development in a short period of time, and during this period, farmlands and natural areas quickly developed into urbanized areas. The estuary of the Nakdonggang River is located in Busan Metropolitan City, the second-largest city in Korea; therefore, the winter feeding site was rapidly damaged by the development of the surrounding area. Thus, this study aimed to analyze whether land use changes around the wetland and artificial development activities have affected the decrease in the wintering populations of Cygnus spp. in the Nakdonggang Estuary, Korea's representative wintering area, over time.

Study area
The estuary of the Nakdonggang (35° 05′ 14″ N, 128° 55′ 32″ E), the longest river in Korea, is located at the southeastern tip of the Korean Peninsula and connects to the Pacific Ocean. Due to its location at the northeastern tip of the Eurasian continent, the area is used as an intermediate or wintering site by many migratory birds. Owing to its ecological characteristics, it has been designated as an Important Migratory Habitat (EAAF097) on the East Asian-Australasian Flyway. Owing to its national importance, the site has been designated and managed as a Cultural Heritage Protection Zone (Natural Monument No. 179) and a Wetland Protected Area (since 1999).
Although wild wintering birds do not recognize the boundaries of protected areas, this study examined the changes in land use in the region adjacent to the Wetland Protected Area (37.718 km 2 ) at the mouth of the Nakdonggang. Generally, large migratory birds attempt to reduce their energy expenditure to ensure survival; therefore, their habitat boundary in the winter is smaller than that in the breeding season. Powell and Engelhardt (2000) monitored wintering C. columbianus's short-range route to its feeding ground and confirmed the distance to be up to 10 km. Therefore, the destruction of the habitat near their main sleeping site would affect their selection of wintering sites. Here, we selected up to 10 km outside the boundary of the Wetland Protected Area as the study area ( Fig. 1).
Owing to the characteristics of the estuary, such as the brackish water formed in the area, with the development of sand bars and mudflats, the sand bars around Eulsukdo were distributed on the western side of the island group (Daemadeung, Jangjado, and Sinjado) and eastern side of the island group (Menggeummeorideung, Baekhabdeung, Doyodeung, etc.). The study area, which includes both the resting places and feeding ground of Cygnus spp., has been changing rapidly, with various developments occurring around it. On land, which mainly serves as a feeding ground, notable development has occurred in the areas where wide rice paddies were traditionally cultivated. In the water area, estuary banks, constructed from 1983 to 1987 to prevent salt damage to agricultural and industrial water and aid the transportation network, have significantly changed the characteristics of the brackish area. Furthermore, the reclamation of mudflats for the development of industrial (1990)(1991)(1992)(1993)(1994)(1995)(1996)(1997)(1998)(1999)(2000)(2001)(2002)(2003)(2004)(2005)(2006)(2007) and residential complexes (1990-2007), large bridge penetrating the protected area (2005)(2006)(2007)(2008)(2009)(2010), constructed coastline (1990s-2000s), and sediment changes due to dredging are continuously changing the shape of and depth of water in the protected area (Kim et al. 2005).
Population changes of Cygnus spp.
In the case of C. olor, very few birds spend the winter in Korea (Meng et al. 2020); therefore, in this study, we only analyzed the changes in the populations of C. cygnus and C. columbianus. The wintering status of wild birds in this area has been monitored since 1999 through a national winter waterbird census (conducted once in January every year). However, in this survey, limited survey points within the Wetland Protected Area have been considered. Regarding the distance traveled by the birds for their feeding activities, the analysis of population changes from the data could not comprehensively represent this behavior in a wintering site. Wintering wild birds have, therefore, been monitored throughout the Nakdonggang Estuary protected area by WETLANDS & BIRDS KOREA (NGO), who aim to protect wild birds in Busan. In collaboration with experts, a survey of major inland points was conducted throughout the estuary (since 2004-2005), and a survey of the sand bars and blind spots was conducted by boat. To prevent overlapping, the teams were divided into groups of two, and then the survey areas were set for each team to conduct a simultaneous investigation. The survey areas were divided into five zones and the surveys were conducted. If a group of Cygnus spp. moving around the area was identified during the survey, the population calculation was adjusted through contact with the researchers in the relevant position. The survey was conducted four times per year, once a month from November to the February of the following year, when most of the wintering birds left the site. The largest population size was determined as the number of birds recorded in the year. For detailed analysis, the population sizes observed monthly were used. The Cygnus spp. population data from 2004-2005 to 2019-2020 were used in this study and the change trends of the populations of C. cygnus and C. columbianus were analyzed in SPSS 26. The data from January were used for comparison with the national census data using the linear regression model. A comprehensive analysis was conducted considering the explanatory power (R 2 ) and autocorrelation based on residuals (Durbin-Watson), and the change tendency was determined using the trend line. The Durbin-Watson statistic ranges from 0 to 4, with the midpoint (2) representing the absence of correlation among the residuals. Therefore, a value of 1.5 to 2.5 is favorable for obtaining proper models (Chithra et al. 2016).
Change in land-cover types according to the time-series analysis Focusing on the Wetland Protected Area, land-use changes were examined in the surrounding areas within 10 km of the protected boundary, which are potential spaces for Cygnus spp. to engage in feeding activities. The land-use changes in surrounding potential habitats were analyzed over time using the 1:50,000-scale land-coverage map from the late 1980s to the end of the 2010s provided by the Ministry of Environment (2020). A total of seven large categories, including urbanized and dried areas, farmlands, forests, grasslands, wetlands (waterside vegetation), bare lands, and water areas, were identified. ArcGIS 10.8 and QGIS 3.16 were used for the spatial analysis. In ArcGIS 10.8, the buffer settings and area calculations were analyzed for each type of land cover, and raster image files were extracted to fit the buffer range using the "clip raster by mask layer" function in QGIS 3.16. To examine the characteristics of the changes, depending on the distance from the protected area, the buffer was set and analyzed at intervals of 2 km. The change in the cumulative land coverage area ratio (%) was analyzed up to 10 km, expanding to 2 km. The analysis of land cover focused on the characteristics of the change in the area ratio (%) of wetlands, water areas, and farmlands as potential habitats of Cygnus spp. across landuse types. In addition, the change tendency between the area (ha) of paddy fields from 2004 to 2019 in Gangseo-gu and Saha-gu, Busan, located 5 to 10 km from the Nakdonggang Estuary, and the monthly population of Cygnus spp. was analyzed through a scatter plot constructed in SPSS, considering the explanatory power and trend line.

Cygnus spp. population changes
The results of linear regression analysis for comparing the simultaneous census results of major migratory bird destinations in Korea over the past 16 years are as shown in Figs. 2 and 3. In the case of C. cygnus, the Durbin-Watson coefficient (1.700) and explanatory power (0.561) were suitable for linear regression analysis, and a continuously increasing trend was observed. In the case of C. columbianus, the Durbin-Watson coefficient (2.27) and explanatory power (0.518) were also suitable for linear regression analysis, and a continuously declining trend was identified. However, as a result of the linear regression analysis of the target site, the explanatory power for C. cygnus was low, at 0.206, and in the case of C. columbianus, the Durbin-Watson coefficient was 0.98, which was not suitable for linear regression analysis. According to the trend line of the graph, both C. cygnus and C. columbianus were declining. The sizes of the C. cygnus and C. columbianus populations searching for and arriving at the estuary of Nakdonggang were not consistent; the winter populations showed significant changes between years. However, a certain pattern of arrival was noted. If many birds wintered in a certain year, the number decreased significantly in the following year, and then restored in the next year, occurring in two-year cycles. While C. cygnus maintained this pattern until recently, the population of C. columbianus has declined sharply since 2007, with few reaching Nakdonggang Estuary since 2015. The migration pattern for C. cygnus has also not recovered since 2017. The 15-year population record showed that the winter population of C. columbianus has sharply declined, which could be attributed to the Nakdonggang Estuary being no longer feasible as their wintering site. There was, however, no sharp decline in the C. cygnus populations; rather, only a moderate decline was observed. The largest winter population of C. cygnus was 4219 individuals in 2011, whereas the smallest was 783 in 2009. The wintering population of C. columbianus plummeted from 181 individuals in 2006 to only 8 in 2019. Although the tendency of the population decline between the two species was very different, the pattern of population increase and decrease, compared with that in the previous year, was similar. Despite these characteristics, both species showed the same trend in response to changes in the overall habitat of the wintering site. However, C. columbianus could still be much more sensitive to changes than C. cygnus. The analysis of various records that indirectly indicated the cause underlying the change in the wintering population showed that damage to the food supply at the estuary was the most relevant.
The wintering populations from 2004-2005 to 2019-2020 were analyzed monthly from November to February (Figs. 4, 5). Based on the annual population changes, a very important aspect of the change in the wintering population of Cygnus spp. was observed. The total wintering population did not decrease sharply until 2019; rather, it had been declining moderately since 2006. For three years from 2006, the initial wintering population remained intact; however, since January, the population started to decline rapidly. This may be because the birds moved due to a lack of food in the middle of the wintering period. This phenomenon was consistent in 2010, 2011, 2013, and 2014. The early wintering population had disappeared.

Changes in land-cover types according to time-series analysis
In the late 1980s, Cygnus spp. concentrated in the Wetland Protected Area of the Nakdonggang Estuary for wintering, as is evident from the time-series analysis of the changes in the surrounding land coverage by the end of 2010 (Table 1, Fig. 6). Of the seven types of land coverage, including urbanized areas, farmlands, forests, grasslands, wetlands (waterside vegetation), bare land, and water areas, there was a sharp change in the ratio of more than 5% compared with that at the end of the 1980s.
Considering the distance, within 2 km of the protected boundary, the urbanized area increased by 19.6% from 9.1% in the late 1980s to 28.7% in the late 2010s, and farmland decreased by 17.8% from 21.6 to 3.9%. The water area also decreased by 7.6%   from 52.1 to 44.5%. If the distance was extended to 4 km, the increase in the urbanized area was 15.3%, which was slightly lower than that of the area within 2 km. The rate of increase in urbanized areas was low, although the changes were sufficient to threaten the habitat. However, the trend of the change in farmland was opposite of that of the urbanized area, suggesting that the farmland mainly changed into urbanized areas. The rate of decrease in the water area was also notable, represented by urban development through reclamation. Busan is the second-largest city in Korea. In the past, there was very little urban development around the Nakdonggang River as it was a floodplain; however, the urbanization of this area progressed quickly due to the expansion of the city and creation of embankments to prevent flooding.
Correlation between the population of Cygnus spp. and area of paddy fields According to the results of the time-series analysis on the relationship between the winter populations of C. cygnus and C. columbianus and the area of paddy fields, the two species exhibited different tendencies in dependence on paddy fields. C. columbianus was relatively sensitive to changes in the area of paddy fields according to the graph, but C. cygnus was not. The correlation between the number of C. columbianus arriving and the area of farmland (Fig. 7) was demonstrated in the monthly appearance of the population from November to February. The correlations in December (R 2 = 0.768) and January (R 2 = 0.743) with the change in the area of paddy fields were stronger than those in the early winter (November: R 2 = 0.457) and the end of the winter (February: R 2 = 0.582). Regarding the correlation between the number of C. cygnus and the area of paddy fields (Fig. 8), the population tended to increase with increases in the areas of paddy fields from November to January, but the statistical explanatory power was low. For February, there was no trend of population increase with the increase in area. The decrease in the number of wintering C. cygnus was also not highly sensitive, but the graph showed that it was related to the decrease in the area of paddy fields. The maintenance and expansion of paddy fields around the wetland are important to protect the Cygnus spp. population at the mouth of the Nakdonggang River.

Discussion
Population changes of Cygnus spp.
Migratory birds generally exhibit philopatry to their breeding (Blums et al. 2002) and wintering sites (Robertson and Cooke 1999); however, they are sensitive to changes in the environment (Lameris et al. 2017;Nuijten et al. 2020). In particular, low temperatures in winter directly affect their survival because they are sensitive to variations in food sources for securing energy (Stillman et al. 2015). The populations of wild birds that visited the mouth of the Nakdonggang in the winter did not show a consistent pattern, according to the time-series analysis. Although there was an overall tendency to decrease in the linear regression analysis, the size of the population that arrived every year tended to fluctuate. Based on the development history, habitat deterioration in certain areas has led to an increase in the population in other areas, which is relatively small scale and tends to deviate from the same habitat range. The Nakdonggang Estuary area is closely related to the populations of Upo Wetland and Junam Reservoir, other representative wintering areas of wild birds nearby. If the population at the mouth of the Nakdonggang decreases, that in the nearby habitats increases, and vice versa (Hahm and Kim 2001). This trend is clear even if the region is expanded to East Asia; in a study on Grus vipio (Jinming et al. 2012), the populations showed a distinct relationship with the habitats in Korea, China, and Japan. In particular, the decline in the population of C. columbianus was confirmed. Between 100 and 200 C. columbianus individuals consistently wintered until the mid-2000s, after which, however, the size of the wintering population decreased sharply and did not recover. It is important to consider the phenomenon confirmed from 2006 to 2008 and the phenomenon that has occurred since. During those years, the initial wintering populations presented similar numbers; however, they rapidly decreased after the middle half of the wintering period. This phenomenon corroborated the hypothesis that C. columbianus had initially settled there as a wintering habitat but subsequently had to move for other reasons. Therefore, C. columbianus took three consecutive years to decide to change its initial wintering site. Unlike the sharp decrease in the wintering populations of C. columbianus, the C. cygnus populations tended to decrease relatively smoothly, which was related to the winter feeding activities of the two species. Based on studies (Fujioka et al. 2010;Wood et al. 2019) on their feeding habits, this tendency can be indirectly understood. The two species initially chose a similar wintering environment, but C. columbianus tends to use rice paddies, which is the main type of agriculture in East Asia, to a greater extent than C. cygnus (Fujioka et al. 2010); therefore, the land-use changes in the surrounding areas were inferred to have different effects on their wintering site selection. An analysis of the detailed food preferences of both species, along with those of all other Cygnus spp., which are known to share similar food sources, would be required in the future.
Changes in land-cover types according to time-series analysis The Cygnus spp. are among of largest wild birds on Earth and are bound to be sensitive to food availability in the wintering period. Therefore, the security of food resources significantly impacts the wintering populations in certain areas. Although the scarcity of food resources could only be inferred indirectly, the changes in land use around the wintering site, where the Cygnus spp. can acquire food, are expected to be vital factors affecting their choice of habitat. During the wintering period, the changes in the type of land use in the region in which C. columbianus travels to acquire food were similar to those reported by Fujioka et al. (2010). Most of the land at the mouth of the Nakdonggang is a large-scale low-lying flatland formed by flooding and has long been a very advantageous area for rice paddies. The changes in the use of rice paddies have occurred quite rapidly, as rice consumption has decreased sharply due to the changes in traditional rice-cultivation areas and recent changes in the food culture of the country. The development pressure in the area located outside Busan was very high and a large area developed very quickly. The sharp decline in rice paddies occurred mainly between 2000 and 2010; the rice paddies closer to the areas where the birds would obtain their food were more likely to disappear. Although the sharp decline in C. columbianus cannot be explained simply by the reduction in rice paddies, it supports a deep relationship between the timing of the sharp decline in rice paddies and the decrease in the wintering population of C. columbianus. Notably, the changes in the C. columbianus population were clearly different to the changes in the C. cygnus population, which has relatively low dependence on rice paddies (Fujioka et al. 2010). Although C. cygnus and C. columbianus, whose individual characteristics have not been specifically studied, generally share the same habitat, we observed a distinct difference in terms of habitat sensitivity. C. columbianus was found to be more sensitive to development around its wintering site than C. cygnus. Our findings indicate that restoration of the wintering area of C. columbianus requires not only the maintenance of a core wintering site, but also the maintenance and restoration of rice paddies, which could serve as feeding grounds. In this study, the capacity to analyze the correlation directly and statistically between the changes in land cover, including farmlands, and Cygnus spp. populations was limited due to the absence of population surveys in remote agricultural areas. However, notable rapid reductions were observed in agricultural areas, which are important feeding areas, and could have had considerable impacts on Cygnus spp. over time, causing the decline in the populations of the wintering sites.

Conclusion
It was confirmed that the Wetland Protected Area at the Nakdonggang Estuary, a representative wintering site of Cygnus spp., designated with the second class of National Endangered Species, is continuously being developed. Long-term monitoring for 15 years (2005)(2006)(2007)(2008)(2009)(2010)(2011)(2012)(2013)(2014)(2015)(2016)(2017)(2018)(2019) confirmed that the populations of C. cygnus and C. columbianus rapidly decreased, and the trend was clear as a result of a time-series analysis of farmland in the Nakdonggang Estuary based on the 10-km wintering area proposed in a previous study. The decrease in farmland within a radius of 2 km of the protected site was the most severe. In parallel with GIS spatial analysis, the correlation between the change in the area ratio of paddy fields and the C. cygnus and C. columbianus monitoring results was affected by the decrease in paddy fields, and the dependence of C. columbianus on paddy fields was relatively high, consistent with the results of previous studies. The Wetland Protected Area at the Nakdonggang Estuary is a large-scale wintering site for Cygnus spp. adjacent to large cities, and it is urgent that paddy fields, which are major feeding sites, are managed through the establishment of buffer zones outside the protected areas, based on the results of this study. This study identified the trend of the change in the population of Cygnus spp. through long-term monitoring, and it was meaningful to explore the correlation between the trend of the change in the population and the decrease in paddy fields. However, there was a limit to the extent to which other variables could be explored, except for the change in the area ratio of paddy fields for the analysis of the decreasing tendency of the population, and sufficient statistical data could not be analyzed due to the deficiency of spatial data. In the future, it is necessary to continuously monitor the population of Cygnus spp. based on the detailed distribution map considering land use and investigate an additional influencing factor such as vegetation changes including food resources by water flow, water depth and salinity according to the development of surrounding areas. In addition, it is needed to conduct social discussions regarding the necessity of establishing a buffer zone outside the protected area boundary in Korea.