Habitat Use and Its Implications for the Conservation of the Overwintering Populations of Bean Goose Anser Fabalis and Greater White-Fronted Goose A

Ornithol Sci 15: 141 – 149 (2016)

ORIGINAL ARTICLE Habitat use and its implications for the conservation of the overwintering populations of Bean Goose Anser fabalis and Greater White-fronted Goose A. albifrons in South Korea

Min Kyung KIM1, Sang-im LEE2 and Sang Don LEE1,#

1 Department of Environmental Science and Engineering, College of Engineering, Ewha Womans University, Seoul 120–750, Korea 2 Institute of Advanced Machinery and Design, Seoul National University, Seoul 151–742, Korea

ORNITHOLOGICAL Abstract The Korean peninsula is geographically important for the migration of geese. Several thousand geese visit South Korea every winter, but currently it is SCIENCE unclear which habitats are preferred by the geese. Understanding patterns of habitat © The Ornithological Society usage is important for establishing conservation strategies, as some habitats may of Japan 2016 be disappearing more rapidly than others making it critical to know whether or not a disappearing habitat is crucial to certain birds. In this study, we investigated the habitat use of the wintering populations of Bean Goose Anser fabalis and Greater White-fronted Goose A. albifrons. We found that the wintering populations of these two geese species in South Korea have stabilized after sudden increases during the mid and late 2000s. Both species formed larger wintering populations at coastal lakes, on reclaimed lands, and at estuaries than on freshwater habitats, which may be related to the availability and/or diversity of food items. Considering that environmental changes resulting from development and climate change are reducing the inshore areas and estuaries, the role of artificial wetlands, such as reclaimed areas that are used as rice fields, is important for conservation of geese that overwinter in Korea.

Key words Bean goose, Conservation strategy, White-fronted goose, Wintering habitat

Historically the Korean peninsula supports large areas provide major habitats for wintering migratory areas of tidal flats particularly along the western and waterbirds (Ministry of Environment 2000). southern coastlines, it also has many rivers, streams, In this study, we investigated the habitat use and reservoirs and considerable areas of agricultural wintering status of the Bean Goose Anser fabalis and land widely distributed inland. Thus, the penin- Greater White-fronted Goose A. albifrons in South sula provides important habitats at which migratory Korea. These two Palearctic species are the dominant waterbirds may rest and forage (Ministry of Envi- wintering geese in Korea (Park & Won 1993) and ronment 2010) during their journeys along the East are known to breed in Siberia (Won & Kim 2012). Asia-Australasian Flyway (Mackinnon 2012). How- Goose populations have been in rapid decline for ever, in Korea, severe industrial development and centuries and some East Asian goose populations urbanization are ongoing and many of the habitats have reached critically low levels (Syroechkovskiy used by migratory waterbirds are being impacted by 2006). Two subspecies of the Bean Goose are known such human-oriented activities. Reclamation projects to overwinter in Korea A. f. middendorffii and A. f. along the western and southern shorelines to produce serrirostris, with approximately 80,000 of the former rice fields, industrial land and housing areas threaten and 70,000 of the latter and are known to be declin- avian habitats because the shoreline and near shore ing globally (Wetlands International 2006). Despite the Bean Goose being designated as an Endangered (Received 27 October 2014; Accepted 16 January 2016) species level 2 in Korea (Rho et al. 2010), no detailed # Corresponding author, E-mail: [email protected] investigation of its habitat preferences have been con-

141 M. K. KIM et al. ducted so far. Such information is crucial in order to Won 1993), it is highly likely that both roosting and be able to establish suitable conservation strategies. foraging geese were all included in the data. As it was This study, the first of its kind in Korea, -was con not possible to distinguish between counts of roost- ducted with the aim of providing the following: (i) ing and of foraging geese, we regarded the data as a data on the size of the wintering populations of Bean representation of the overall activities of the geese. Goose and Greater White-fronted Goose in Korea from 1999 to 2013 and a distribution map of their 2) Types of habitat wintering sites, in order to help our understanding of We followed the categorization of habitat types their current status; (ii) suitable conservation strate- made in the Winter Migratory Bird Census (Min- gies for goose populations in Korea, based on analy- istry of Environment 2004). Based on the descrip- ses of habitat types in the areas where the majority tions of census sites, study areas were divided into of the geese overwinter. five habitat types: (1) seashore, (2) coastal lakes and reclaimed land, (3) rivers, (4) estuaries, and (5) MATERIALS AND METHODS dam, lakes and reservoirs. Habitat type 1 includes islands and bay areas where ocean currents directly 1) Population size wash the shoreline. Type 2 includes rice fields, arti- We extracted contemporary count data for the pop- ficial land or lakes formed by reclamation projects ulations of Bean Goose and Greater White-fronted or breakwater construction. Due to extensive rec- Goose from the Winter Migratory Bird Census Data lamation activities around the West Sea in recent collected from 1999 until 2013 (Ministry of Environ- years (such as the Saemangeum project from 1991 ment 1999-2013). The Winter Migratory Bird Cen- to 2006; Saemangeum Developmental Agency 2013), sus, begun in 1999, entails an annual count of all bird there has been a huge increase in the total area of species at each site in late January or early February, type 2 (401 km2 was reclaimed by the Saemangeum done quickly over a period of 2–3 days to avoid dou- project alone; Ministry of Agriculture, Food and ble counting. The data are published by the National Rural Affairs 2013) while other habitat types did not Ministry of the Environment of Korea (Ministry of change much in total area. Habitat type 3 includes Environment 2004) and are known to be suitable for riverine areas. Type 4 corresponds with the brackish establishing current habitat usage of birds winter- water zone where seawater and freshwater meet. In ing in South Korea (Moores et al. 2010). The data many cases, type 4 includes areas where saltmarsh include a list of species and their abundance, but do vegetation grows. Habitat type 5 includes freshwater not include time and habitat use (roosting/foraging). lakes and inland reservoirs. The habitat type of each The number of sites surveyed increased from 69 survey site was fixed over the study years. in 1999 to 195 in 2013, reflecting a growing aware- In this study, we analyzed the types of habitats ness of the importance of the Korean peninsula for that supported large numbers of geese. We conducted migratory bird conservation (Ministry of Environ- frequency analysis with SPSS 12.0 to investigate ment 1999, 2013). Since the number of census sites the relevance between variables of the five habitat has increased over the years, we could not use the types concerning sites with a large goose population total number of geese counted because this would (>1,000), and sites with a small population (<1,000) very likely have increased in line with the addition of from 1999 to 2013. In our dataset, a thousand (log new monitoring sites over the years. Therefore, of the number 3) is located near the median of the abun- 69 sites that were monitored in 1999 we selected 42 dance for both species (median for log number: sites for Bean Goose and 39 sites for Greater White- 2.701 for Bean Goose and 2.947 for Greater White- fronted Goose, where more than one individual was fronted Goose). Thus, we used 1,000 as the threshold recorded between 1999 and 2013, and we analyzed between small and large flocks of geese. the data collected from these sites only. The distance between the closest neighboring census sites aver- RESULTS aged 13.89±6.46 km (mean±SD). Considering that Greater White-fronted Geese forage near their roost- 1) Population size ing sites (Cramp & Simmons 1977), and in the case Compared with the early 2000s, the numbers of of those overwintering in Korea confine their activi- Bean Goose and Greater White-fronted Goose over- ties within 5 km radius of their roosting sites (Park & wintering in South Korea in January had nearly dou-

142 Habitat use of two wintering geese in Korea bled by the mid and late 2000s (Fig. 1). Since 2010, species showed a positive correlation (coefficient of the total sizes of the overwintering goose populations correlation=0.706, P=0.003), suggesting that any seem to have declined, nevertheless they are still environmental change on their breeding or wintering larger than in the early 2000s. Based on population grounds would affect both species. This correlation trends, we recognize the period 1999–2004 as when is also visible in the distribution map showing the geese populations were small, 2005–2009 as the average population size recorded at each site (Fig. period when goose populations suddenly increased, 2); the geese mainly formed wintering flocks along and 2010–2013 as the period during which the the western and southern coasts where estuaries and wintering populations seem to have stabilized or reclaimed land were abundant. Both goose species reduced. The overwintering populations of the two showed similar patterns of distribution.

Fig. 1. Variation in the numbers of overwintering Bean Goose and Greater White-fronted Goose in Korea (data from Ministry of Environment, 1999–2013). The data are from 42 sites for Bean Goose and 39 sites for Greater White-fronted Goose.

Fig. 2. The annual average numbers of wintering Bean Goose (a) and Greater White-fronted Goose (b) in South Korea, 1999–2013.

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2) Analysis of habitat types uted across habitat types, larger populations mostly We conducted frequency analysis in order to exam- gathered at either coastal lakes and reservoirs (ii) or ine which types of habitat are used by geese. The fre- estuaries (iv) (Fig. 3 (a) and (b)). Among the five quencies of habitat use over the entire study period habitat types, the habitat least used by geese was (1999–2013) did not differ significantly between rivers. bean and white-fronted geese (χ2=4.410, P=0.346), In order to investigate the annual variation in the seemingly indicating their ecological similarities, par- usage of the five habitat types by geese, we compared ticularly with regards to preferred food sources. The habitat usage during the three time periods. Habi- types of habitat that harbored large numbers of win- tat usage was not constant during the three periods tering geese (≥1,000 individuals) differed from those (χ2=31.433, P<0.000 for bean; χ2=20.820, P<0.01 that harbored small numbers (<1,000 individuals) for white-fronted) (Fig. 4). The use of some habitats (χ2=32.914, P<0.000 for bean; χ2=22.585, P<0.000 increased gradually (seashore (i)) or decreased (dams, for white-fronted). Analysis revealed that whereas lakes, and reservoirs (v)). During the period when smaller populations were more or less evenly distrib- the wintering populations of both species increased

(a) Bean Goose Anser fabalis

(b) Greater White-fronted Goose Anser albifrons

Fig. 3. Comparisons of habitat types that harbored small (<1,000) and large (≥1,000) wintering flocks of Bean Goose (a), and Greater White-fronted Goose (b) during 1999–2013. The five habitat types are: (i) seashore, (ii) coastal lakes and reclaimed land, (iii) rivers, (iv) estuaries, and (v) dams, lakes and reservoirs.

144 Habitat use of two wintering geese in Korea

(a) Bean Goose Anser fabalis

(b) Greater White-fronted Goose Anser albifrons

Fig. 4. Annual variation in the usage of five types of habitat by Bean Goose (a) and Greater White-fronted Goose (b) between 1999 and 2013. Values on the Y axes are the average percentage of the number of individuals observed at each habitat. The categories of habitat types are the same as in Fig. 3. n represents the sample size of each habitat category. (1999–2004: Bean Goose 29,104 individuals/yr, Greater White-fronted Goose 32,683 individuals/yr. 2005–2009: Bean Goose 56,660 individuals/yr, Greater White-fronted Goose 59,158 individuals/ yr. 2010–2013: Bean Goose 36,910 individuals/yr, Greater White-fronted Goose 43,404 individuals/yr.) During 2005–2009, when there was a sudden increase in the overwintering populations in South Korea, the usage of estuaries (iv) greatly increased in both species. The categories of habitat types are the same as in Fig. 3.

145 M. K. KIM et al. suddenly (2005–2009), the usage of estuaries (iv) ily to the area as it appears to provide them with greatly increased. This analysis is based on the data more feeding opportunities on farmland. from 42 sites for Bean Goose and 39 sites for Greater Although habitat simplification due to reclamation White-fronted Goose; the pattern was similar when causes the decline of habitat quality for many species we only used data from those sites where more than of migratory birds (Donald et al. 2001), it has been 1,000 geese were recorded. suggested that herbivorous migratory waterbirds, such as geese, may have benefited from the spread DISCUSSION of recent changes in agriculture (Fox et al. 2005; Gauthier et al. 2005; but also see below). Much (44%) Our results show that the wintering populations of of the reclaimed area at Saemangeum was converted both Bean Goose and Greater White-fronted Goose to rice fields for human food resources (Ministry of in South Korea increased suddenly during the mid Agriculture, Food and Rural Affairs 2013), but coin- and late 2000s. This increase is consistent with a cidentally may have provided certain birds with rest- parallel increase in the Greater White-fronted Goose ing areas and food resources such as grains or inver- population in Japan until 2006/2007 (Shimada 2009), tebrates that are important for their winter survival but is in contrast to Syroechkovskiy’s (2006) report and possibly for their next breeding performance that goose breeding populations in the Russian Far (Robb et al. 2008). This hypothesis implies that due East had declined greatly prior to 2005. Based on to the increase in their preferred habitat, previously Syroechkovskiy’s (2006) report, it seems that while separate wintering populations in other neighboring the number of geese wintering in Korea suddenly regions, such as China, may have temporarily joined increase during the mid 2000s, that may have been the wintering population in Korea. A similar shift in the result of geese from different breeding popula- wintering locations has been reported for the Greater tions converging to winter in South Korea. As pre- White-fronted Goose in Europe, where a decrease in viously suggested (Syroechkovskiy 2006; Shimada the wintering population in the UK and Ireland coin- 2009), we can assume that the habitat conditions in cided with an increase in the Netherlands (Pollit et Korea were sufficiently favorable to support this sud- al. 2003). With the exception of Japan (see Shimada den increase in the size of the overwintering geese 2009), we do not have any data indicating whether populations. Syroechkovskiy (2006) suggested that (or how) the sizes of wintering goose populations in on the west coast of South Korea the conversion of neighboring regions has changed in recent years. In inter-tidal mudflats and saltmarshes into rice fields order to understand the composition and the variation had benefitted wintering geese, attracting them to on in size of the wintering goose populations in South the post-harvest waste grain left on the fields. Our Korea, long-term international collaboration span- analysis also shows that coastal lakes and reclaimed ning the geographic regions in neighboring countries land accounted for more than 50% of the habitat types where geese overwinter is necessary to monitor fluc- where large wintering populations of geese gathered. tuations in goose numbers over time. The timing of the increase in the overwintering The number of geese overwintering in Korea geese population in Korea coincided with the com- seems to have decreased in recent years, follow- pletion of the Saemangeum Seawall Project, suggesting the sudden increase around 2005, but the rea- ing that the geese may have used the newly reclaimed sons for their decline is not clear. If we compare area formed along the west coast. In total, 40,100 the number of geese observed in a specific habitat ha were reclaimed, and 28,300 ha will be converted type over the periods 2005–2009 and 2010–2013, into rice fields, corresponding roughly to 3% of then the greatest difference is observed in estuaries. South Korea’s total rice field area (Statistics Korea This implies that degradation in quality or reduction 2014). Before reclamation, the estuarine wetlands of in the area of estuarine habitat in Korea occurred as Saemangeum provided important feeding grounds for extensive construction took place in estuaries. If the very large numbers of migratory birds, with an esti- increase in potential foraging sites resulting from the mated 400,000 shorebirds dependent on the particular Saemangeum reclamation project played an impor- habitat there during their migration between Asia and tant role in the sudden increase in geese populations Alaska or Asia and Russia (Birds Korea 2005). The during the mid 2000s, then the subsequent population reclamation of Saemangeum, while deleterious for decline may indicate that the quality of the reclaimed shorebirds, may have attracted waterbirds temporar- area deteriorated, as documented by Moores et al.

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(2008). Furthermore, the Four Rivers Project is also strategy, this includes: (i) reducing the usage of agri- considered to have led to deterioration in the quality cultural pesticides, (ii) flooding rice paddies in winter of estuarine habitat (Moores et al. 2010). In order instead of keeping them dry, or (iii) leaving certain to discern whether this recent decrease in wintering amounts of grain as food for the geese. Pesticides, geese is a consequence of a more general decline although used in spring and summer, are known to in goose populations or due to degradation of their cause mortality in wintering waterbirds (Hobaugh preferred habitat in Korea, systematic monitoring of et al. 1989; Wilson et al. 1996). Winter-flooded rice the status of breeding populations in the Far East is paddies can serve as roosting and foraging sites for necessary. waterbirds (Brouder & Hill 1995; Elphick & Oring Our results suggest that the geese prefer coastal 2003; Nishimiya 2010). Considering that the other lakes, reclaimed land and estuaries as overwintering types of habitat that the geese prefer (shores and sites rather than shores and freshwater habitats such estuaries) are likely to decrease in area with anthro- as rivers, lakes and reservoirs. This is consistent with pogenic activities (such as development and urban- Moriguchi et al.’s (2013) recent findings concerning ization) and climate change (Galbraith et al. 2002), Greater White-fronted Goose in Japan forming over- protecting and maintaining artificial wetlands as win- wintering populations in the agricultural plains along tering grounds for geese will be very important for the western and eastern coasts of Honshu. Although the conservation of these species. Bean Goose and Greater White-fronted Goose differ slightly in their patterns of habitat usage, they ACKNOWLEDGMENTS seemed to prefer similar types of habitat. During the years when goose numbers increased, more geese We are deeply grateful to all of the researchers who partici- converged on estuaries, perhaps indicating a rela- pated in the winter migratory bird censuses. The authors wish tionship between this habit and the increase in their to thank NRF (2015M3C8A6A06012735, 2009–0083527, 2014–048162) and KEITI (2014000130010) for financial numbers. Since the census data that we analyzed for support. this study was collected in a site-specific manner, the habitat types recorded may represent both foraging REFERENCES and roosting sites for geese. Thus, we must be care- ful in drawing conclusions based on how the geese Birds Korea (2005) A web-report on the Saemangeum utilized each habitat type and what resources they reclamation project: A symbol of South Korea in the used in each habitat type. Nevertheless, based on world. Available at http://www.birdskorea.org/Habi- other reports of their preference for estuarine habitat tats/Wetlands/Saemangeum/BK-HA-Saemangeum- (Williams & Forbes 1980; Stroud et al. 2001) and Reclamation-Project-2005-04-01.shtml (Accessed on GreenKorea’s (2003) observation that geese in Korea 15 June 2015). forage on the roots or fruits of plants growing in estu- Brouder SM & Hill JE (1995) Conjunctive use of farm- aries, we can infer that their preference for estuaries land adds value: Winter flooding of ricelands pro- as wintering sites may be due to the high primary vides waterfowl habitat. Calif Agric 49: 58–64. productivity of those areas that provide a wide range Cramp S & Simmons KEL (1977) Handbook of the of food items for them. Wilson and Jefferies (1996) Birds of Europe the Middle East and North Africa: The Birds of the Western Palearctic. Volume I. Ostrich suggested that the amount of nitrogen mineralized to Ducks. Oxford University Press, Oxford. in intertidal marshes such as estuaries was higher Donald PF, Green RE & Heath MF (2001) Agricultural than inland marshes thus the preference of intertidal intensification and the collapse of Europe’s farmland marshes for foraging may be linked to the availability bird populations. Proc R Soc Lond B Biol Sci 268: of nitrogen for plant growth. It is also possible that 25–29. geese prefer the estuarine environment because it is Elphick CS & Oring LW (2003) Conservation implica- relatively less disturbed than inland habitats. Further tions of flooding rice fields on winter waterbird com- observations are necessary in order to understand the munities. Agric Ecosyst Environ 94: 17–29. factors underlying the preference for estuarine habi- Fox AD, Madsen J, Boyd H, Kuijken E, Norriss DW, tats among the geese. Tombre IM & Stroud DA (2005) Effects of agricul- Considering their habitat preferences, we suggest tural change on abundance, fitness components and that managing the man-made wetlands used by the distribution of two Arctic-nesting goose populations. overwintering geese can be an efficient conservation Glob Change Biol 11: 881–893.

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