The Distribution, Abundance and Conservation of Avian Biodiversity in Yellow Sea Habitats in the Republic of Korea

NIAL MOORES BA (Hons.), Hull University (UK) and Master‘s Degree (Ecological Planning), Kyushu Institute of Design and Technology, Kyushu University (Japan)

University of Newcastle, Australia

A thesis submitted to the University of Newcastle for the degree of Doctor of Philosophy

April 2012

Principal Supervisor: Professor Phil Hansbro Associate Supervisor: Dr. Danny Rogers

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Disclaimer

This thesis contains no material which has been accepted for the award of any other degree or diploma in any university or other tertiary institution and, to the best of my knowledge and belief, contains no material previously published or written by another person, except where due reference has been made in the text. I give consent to this copy of my thesis, when deposited in the University Library, being made available for loan and photocopying subject to the provisions of the Copyright Act 1968.

I hereby also certify that, with the exceptions listed below, I conducted the fieldwork, conceived the chapters and the story of the thesis, analysed the data, helped define aims for statistical analysis that was conducted with colleagues, and wrote all of the text – with the guidance of my supervisors. Initial submission was made in August 2011, and final submission in March 2012, following incorporation of revisions in the text as proposed by supervisors and external examiners. Chapters with extensive collaboration include:

1. Chapter 3. Most of the measurements of tidal-flat grids were conducted by two Birds Korea colleagues. Tyler Hicks (a PhD candidate at Washington State University) also created Figure 3.3 of tidal-flat area.

2. Chapter 4. This chapter documents the Saemangeum Shorebird Monitoring Program. The Program itself involved >80 people. Dr. Danny Rogers was a co-manager of the Program, along with myself and three others. Dr. Rogers conducted much of the initial data analysis and survey design. The migration turnover model (with figures) used in Chapter 4 was constructed by Ken Rogers in collaboration with Dr. Danny Rogers. Figure 4.2 was created by Matthew Irvin of Massey University for use in Moores et al. (2008)

3. Chapter 5. Survey work was conducted in collaboration with shorebird experts from the Australasian Wader Studies Group, the Miranda Naturalist‘s Trust and the Global Flyways Network, as well as with Birds Koreans and local researchers. However, I was fully responsible for the analysis and write-up.

4. Chapter 6. Both the figure on Yellow-billed Loon distribution (using ArcGIS) and analysis of seabird communities was conducted with Tyler Hicks from GPS points and data gathered during my own survey work.

5. In Chapter 9, Stepwise Discriminant analysis of Decrease Susceptibility Index Scores was conducted by Ken Rogers.

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Acknowledgements

Sincere thanks to the University of Newcastle and especially to my Principal Supervisor Professor Phil Hansbro (University of Newcastle) and Associate Supervisor Dr. Danny Rogers (Arthur Rylah Institute, Department of Sustainability and Environment, Victoria, Australia). Prof. Phil Hansbro was the first person to suggest the PhD and has facilitated the process – both logistically and through guiding me over many months through several of the drafts. Dr. Danny Rogers was a co-manager of the Saemangeum Shorebird Monitoring Program (SSMP), and over the years and throughout the thesis-writing process, has consistently contributed much insight and support, despite other pressing work. Thank you both. Further valuable improvements were also made to the original submission in August 2011 due to the expert input of three external examiners, warmly and sincerely thanked here.

Thanks too to all former and present colleagues in Birds Korea, most especially our National Coordinator Ms. Park Meena, Mr. Andreas Kim, Mr. Tyler Hicks, Ms. Tonni Knox-Hiitola and all other Birds Koreans who directly or indirectly contributed in a number of ways to this work. Several of the concepts that run through the thesis were developed during Birds Korea projects, including the Birds Korea 2010 Blueprint.

For Chapters 2, 7 and 8, warmest thanks are given to Dr. Will Duckworth – as always an excellent source of information, support and insight. Mr. Park Jong-Gil of the Korea National Parks, Mr. Chai Seung-Hoon and Mr. Tim Edelsten are also sincerely and warmly thanked. Chapters 3 and 6 also benefited greatly from input from Birds Koreans – most especially Mr. Tyler Hicks and Mr. Geoff Styles. Thank you both. Chapters 4 and 5, on the SSMP and a national shorebird survey in 2008, were made possible only through the massive efforts of a large number of people from within Birds Korea and from the Australasian Wader Studies Group (AWSG): all are thanked sincerely. I hope that the chapters can be used to help tell the story that we so wanted and still need to tell. To that end, I would especially like to give thanks to Mr. Ken Rogers who deciphered numerous of my emails and worked on the shorebird migration models, strengthening our confidence in the results: thank you. Thanks too to all participants of the SSMP. A few persons are perhaps most representative of the hard work and dedication to conservation that came through those difficult surveys on a dying tidal-flat: once more our National Coordinator, Ms. Park Meena; the Styles Family; Dr. Danny Rogers and Mr. Ken Gosbell of the AWSG who co-managed and made the SSMP possible; Dr. Phil Battley and Mr. Adrian Riegen from New Zealand; the Global Flyways Network; and all others who work for shorebirds and intertidal wetlands on this and other Flyways. Of course, special thanks also to all who funded the SSMP – especially the David and Lucile Packard Foundation.

Professor Steven Feldstein and Mr. Magnus Robb are also thanked sincerely for their support and advice on weather systems and on bird vocalisations respectively (I only regret that was not enough opportunity to use the data and sonagrams on Black Woodpigeon and Styan‘s Grasshopper Warbler: next time).

And finally, for her endless support and boundless tolerance: thanks to my life-time partner and soul-mate, and to all in our family.

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Contents Page Acronyms & Nomenclature 13 Synopsis 14

Chapter 1 Background: Conservation, Geography, Avian Biodiversity and the Aims 15 of the Research 1.1 Background and Aims 15 1.1.1 Introduction 15 1.1.2 Conservation framework 16 1.1.3 Research and conservation challenges 17 1.2 The Yellow Sea 22 1.2.1 Physical geography 22 1.2.2 Human geography 24 1.2.3 Climate 24 1.2.4 The East Asian-Australasian Flyway (EAAF) 24 1.3 The Yellow Sea Blueprint Region (YSBR) 25 1.3.1 Physical geography 25 1.3.2 Main research sites 26 1.3.3 Main habitats 27 1.3.4 Human geography 28 1.3.5 Climate 29 1.4 Research on the Avian Biodiversity of the YSBR 30 1.4.1 Introduction 30 1.4.2 Intertidal wetlands 31 1.4.3 Open sea 31 1.4.4 Offshore islands 32 1.5 Information Gaps and the Five Principal Pressures 33 1.5.1 Habitat change 33 1.5.2 Overexploitation and hunting 35 1.5.3 Pollution 36 1.5.4 Invasive alien species 38 1.5.5 Climate change 38 1.6 The Research Chapters 40

Chapter 2 Bias in the Korean Ornithological Literature & the Identification of 42 Long-term Bird Population Trends between 1910 and the Present 2.1 Background 43 2.1.1 Introduction and aims 43 2.1.2 Sources used 44 2.1.3 Change in number of recorded species 45 2.1.4 Changes in abundance and policy response 46 2.2 Literature and Bias 48 2.2.1 Austin (1948) 48 2.2.2 Gore & Won (1971) 53 2.2.3 Won (2000) 56 2.2.4 Moores & Park (2009) 59 2.2.5 The MOE Census (1999-2010) 62 2.3 Interpreting the Four Assessments 64 2.3.1 Geographical scope 65 2.3.2 Taxonomy and identification 66 2.3.3 Access 70 2.4 Methods 71 2.4.1 Four Assessments 71 2.4.2 Tomek (1999, 2002) & DPRK literature 74 6

Page Chapter 2 2.5 Results 76 2.5.1 Status of regularly occurring and less regular species 76 2.5.2 Species of global conservation concern 77 2.5.3 DPRK population trends 79 2.5.4 Decreasing species in the ROK 80 2.5.5 Increasing species in the ROK 81 2.5.6 Species of the YSBR 82 2.5.7 Resolution and modification of the results 82 2.6 Discussion 91 2.6.1 Is there evidence of a decline in avian biodiversity in the ROK? 91 2.6.2 Underestimating declines 93 2.6.3 Use of the results 94

Chapter 3 Intertidal Wetland: Reclamation and Estimates of Remaining Area in the 98 ROK 3.1 Background and Aims 99 3.1.1 International importance of intertidal areas to avian biodiversity 99 3.1.2 Reclamation process 99 3.1.3 History of reclamation 101 3.1.4 Aims of the present study 103 3.2 Methods 103 3.3 Results 105 3.4 Discussion 107 3.4.1 Interpretation of the results 107 3.4.2 Impacts on shorebirds 108 3.4.3 Conservation obligations 110

Chapter 4 Measuring the Impacts of Large-scale Reclamation: The Saemangeum 111 Shorebird Monitoring Program (2006-2008) 4.1 Background and Aims 112 4.1.1 The Saemangeum reclamation 112 4.1.2 International importance of the Saemangeum Estuarine 113 System (SES) 4.1.3 Origin of the Saemangeum Shorebird Monitoring Program (SSMP) 113 4.1.4 Research aims and main species 116 4.2 Methods 118 4.2.1 The Study Region 118 4.2.2 SSMP survey design 121 4.2.3 Changes to the SES and SSMP count method due to seawall 123 closure 4.2.4 Analysis 124 4.3 Results 125 4.3.1 Numbers and international importance of the Study Region 125 4.3.2 Marked birds 127 4.3.3 Phenology and potential bias 130 4.3.4 Models and estimates 132 4.3.5 Changes in numbers of shorebirds between 2006 and 2008 136 4.3.6 Habitat change and declines in the Study Region 142 4.4 Discussion 149 4.4.1 Reclamation and shorebird declines 149 4.4.2 Longer-term declines 151 4.4.3 Displacement to adjacent wetlands 152 4.4.4 Declines during southward migration 152 4.4.5 Concluding remarks 153 7

Page Chapter 5 An Assessment of Changes in Shorebird Numbers in the ROK between 154 Decades: National Shorebird Survey, May 2008 5.1 Background and Aims 155 5.1.1 Introduction 155 5.1.2 Previous shorebird survey (1988 & 1998) 155 5.1.3 Internationally important shorebird sites in the ROK 157 5.1.4 Research aims 158 5.2 Methods 158 5.3 Results 160 5.3.1 Total numbers 160 5.3.2 Changes between 1998 and 2008 outside of the SSMP Study 162 Region 5.3.3 Counts in 2008 and estimates by Yi (2004) 164 5.3.4 Four North-western Sites: 1988, 1998, 2008 166 5.4 Discussion 168

Chapter 6 Survey of Seabirds at Sea in the YSBR from High-speed Ferries and 171 Land-based Counts 6.1 Background and Aims 172 6.2 Methods 174 6.2.1 Counts from ferries 174 6.2.2 Counts from land 176 6.2.3 Analysis 177 6.3 Results 178 6.3.1 Species‘ richness 178 6.3.2 Differences between transects 178 6.3.3 Number of individuals 180 6.3.4 Distribution in open sea and inshore areas 180 6.3.5 Most numerous species 181 6.3.6 Seasonal distribution 184 6.3.7 Distance and detectability 186 6.4 Discussion 188

Chapter 7 Landbird Migration Corridors across the Yellow Sea: 191 Northward Migration through Socheong Island (2010) 7.1 Background and Research Aims 192 7.1.1 Introduction 192 7.1.2 Migration across the Yellow Sea 193 7.1.3 Socheong Island 197 7.1.4 Previous research 197 7.1.5 Research aims 198 7.2 Methods 199 7.2.1 Count method 199 7.2.2 Weather 201 7.2.3 Data collation 202 7.3 Results 202 7.3.1 Species, families and orders 202 7.3.2 Species‘ abundance and richness 203 7.3.3 Species of global conservation concern 204 7.3.4 Timing of migration, peak counts and bird-days 204 7.3.5 Visible migration 216 7.3.6 Most numerous species during Whole Island Counts 221 7.3.7 Most numerous species by Peak Count 222 species 223 8

Page Chapter 7 7.3.8 Whole Island Estimates of the ten most numerous landbird species 223 7.3.9 Comparisons between Socheong and Hong & Heuksan 225 7.4 Discussion 228 7.4.1 Channelled northward migration 228 7.4.2 Channelled southward migration 229 7.4.3 Regional migration strategies 230 7.4.4 Use of the research 232

Chapter 8 Landbird Migration through an ―Intermediate Island‖ and the Influence 235 of Weather 8.1 Background and Aims 236 8.1.1 Introduction 236 8.1.2 Eocheong Island 238 8.1.3 Previous research 239 8.1.4 Research aims 240 8.2 Methods 240 8.2.1 Bird-counts 240 8.2.2 Weather 241 8.3 Results 242 8.3.1 Species, families and orders 242 8.3.2 Difference in total numbers between years 243 8.3.3 Species of global conservation concern 243 8.3.4 Most numerous species 244 8.3.5 Comparison of most numerous landbird species between islands 245 8.3.6 Comparison of migration timing between islands 247 8.3.7 Influence of weather 249 8.4. Discussion 258 8.4.1 Weather and migration 258 8.4.2 Weather-based bias and the detection of underlying population 260 trends

Chapter 9 General Discussion: Towards Meeting Target 19 of the CBD Strategic 264 Plan for Conservation of Biodiversity 2011-2020 9.1 Background 264 9.1.1 Aims 264 9.1.2 Improved knowledge 264 9.1.3 Information sharing 265 9.1.4 Advocacy and policy 265 9.2 Strengths and Weaknesses of the Present Research 270 9.2.1 Historical and contemporary declines 270 9.2.2 The three main habitats of the YSBR 271 9.3 Recommendations on Information Gathering and Sharing 283 9.4 The Decrease Susceptibility Index 285 9.4.1 Rationale 285 9.4.2 Construction of a DSI for bird species in the Republic of Korea 287 9.4.3 Examples of DSI Scores 291 9.4.4 Analysis 293 9.4.5 Summary 298 References 300 Appendix 316

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List of Tables

Page Chapter 1 1.1 Location and habitat type of selected YSBR sites 27 1.2 Monthly mean temperatures in 2009 at selected weather stations in the YSBR 29 and the wider region 1.3 Forest by area and volume in the ROK between 1978 and 2007 34

Chapter 2 2.1 Number of adequately documented species recorded in the ROK in the Four 45 Assessments since 1910, divided into regularly occurring and less regular species 2.2 Gull species adequately documented in the ROK by year of their first record 67 2.3 Conventions used to assign a consistent Index of Abundance (―Abundance 72 Number‖) to the Four Assessments 2.4 Three main and seven subdivisions of population trends in species in the ROK 73 between 1910 and 2009 2.5 Six categories of suggested population trend in the DPRK 75 2.6 National population trend with seven subdivisions between 1910 and 2009 of all 76 511 species in the ROK based on the Four Assessments 2.7 The global conservation status of species by category of ROK national trend 78 between 1910 and 2009 2.8 List of Decreasing species in the ROK between 1910 and 2009 80 2.9 List of Increasing species in the ROK between 1910 and 2009 81 2.10 The number of species recorded annually (2000-2009) within the YSBR 82

Chapter 4 4.1 Shorebird species found in internationally important concentrations of >1% of 117 population in the SSMP Study Region between 1999 and 2003 4.2 Dates and duration of SSMP count cycles and time and height of spring high 122 tides at Gunsan 4.3 Peak counts of the 35 most numerous shorebird species recorded in each of the 126 three wetlands 4.4 Origin of colour-banded and leg-flagged shorebirds observed during SSMP 128 fieldwork 4.5 The 20 main shorebird species in order of earliest peak date 132 4.6 Model of migration timing and transiting numbers of Bar-tailed Godwit 134 4.7 Model of migration timing and transiting numbers of Great Knot 135 4.8 Changes in number in 20 main shorebird species in the SSMP Study Region 137 (2006-2008) 4.9 Changes in peak counts of the 20 main shorebird species within the 138 Saemangeum Estuarine System between 2006 and 2008 4.10 Changes in peak counts within the Geum Estuary between 2006 and 2008 139 4.11 Peak counts of the main shorebird species and the highest count cycle counts of 141 all shorebirds in Gomso Bay by year between 2006 and 2008 4.12 Total number of shorebirds per wetland per year based on peak counts of all 142 shorebird species 4.13 Maximum counts each year of 15 waterbird species found in internationally 146 important concentrations within the Saemangeum Estuarine System, April- November 2003-2005

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List of Tables (cont.) Page

Chapter 5 5.1 Wetlands, survey dates and changes between 1998 and 2008 160 5.2 Numbers of shorebirds that occur in internationally important concentrations in 161 the ROK that were recorded in May 2008 5.3 Change in number of the ten most numerous shorebird species counted at eleven 163 internationally important shorebirds sites outside of the SSMP Study Region between 1998 and 2008 5.4 Fourteen most important shorebird sites in May 2008, their reclamation status 165 and estimates of shorebirds at the same sites during northward migration (1997- 2001) 5.5 Comparison of numbers of internationally important shorebird at four main 166 north-western sites, in May between 1988 and 2008

Chapter 6 6.1 Number of counts of seabirds by month along the Northern and Southern 174 Transects in 2009 and 2010 6.2 Indicator values for the top five indicator species of seabird communities in open 179 sea areas in the Northern versus the Southern Transects 6.3 Number of individual seabirds recorded by month 180 6.4 Numbers of the 16 most numerous seabird species recorded along Northern and 182 Southern Transects 6.5 Peak Counts in open sea of the 26 most numerous seabird species 183 6.6 Monthly counts of selected seabird species in and close to inshore waters 184 6.7 Seasonal status of complete migrant seabirds in open sea in the YSBR 185 6.8 Number of individuals of species and one selected family counted along the 187 Northern and Southern Transects and from Socheong divided into distance bands and behaviours

Chapter 7 7.1 The number of regularly occurring orders and species in the ROK adequately 203 documented on Socheong Island between 2003 and 2009, and that were recorded during the survey period (2010) 7.2 Species with First-dates before Mid-April and Last-dates in June 206 7.3 Species with Last-Dates before the Whole Island Count of May 8th 207 7.4 Species with First-dates between March 30th and April 25th and Last-dates before 209 May 21st 7.5 Species present in April, with Last-dates between May 21st and May 31st 211 7.6 Species with First-dates between April 15th and 30th which were still present into 213 June 7.7 Species with First-dates between May 1st and May 11th 214 7.8 Species only recorded after May 15th 216 7.9 Total numbers, peak counts and main migration dates of the 20 most numerous 217 landbird species counted departing from North Point 7.10 The three most numerous species on each of the 13 Whole Island Counts 221 7.11 Whole Island Estimates and Estimated Bird-days of the 10 Species with the 224 highest peak counts on Socheong 7.12 Comparison of Estimated Bird-days of 10 selected species on Socheong and 227 actual bird-days on Hong Island, April-May 2010

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List of Tables (cont.) Page

Chapter 8 8.1 Number of regularly occurring orders and species in the ROK and on Eocheong 242 Island between April 14th and May 16th, 2003 & 2011 8.2 Species abundance by bird-days of the twelve most numerous landbird species 245 on Eocheong in 2003 and 2011, and their rank by bird-day on Socheong, Hong and Heuksan in 2010 8.3 Local and regional weather the day before and during Large Arrivals of 251 landbirds in 2003 & 2011 8.4 Strength of 850-mb vector winds in 2003 and 2011 on the Peak Count Date of 255 five landbird species that breed on the Northeast Asian Mainland, and of five landbird species which breed mostly in the Far West Pacific Region

Chapter 9 9.1 National and regional population trends of shorebirds 273 9.2 Peak counts and bird-days of 10 species of landbird on Eocheong and Socheong 281 with the strongest evidence of decrease since 2002 9.3 Habitat types used to assess habitat change, level of specialisation and 288 dependence on natural or artificial habitats 9.4 Weight category and migratory status of the 365 regularly occurring species in 289 the ROK 9.5 Decrease Susceptibility Index: additional variables, rationale & process, and the 290 Score attributed to each category for all species 9.6 Decrease Index Susceptibility: additional variables, rationale & process, and the 291 score attributed to each category for migratory species 9.7 Examples of Status Assessments and DSI Scores for four species in the ROK 292 (1910-2009) 9.8 DSI Scores of 37 regularly occurring species of global conservation concern 294 according to weight, habitat change, tendency to concentrate, and susceptibility to climate change 9.9 DSI Scores of ROK species of global conservation concern and their families 295 9.10 Migratory status and DSI Scores of Decreasing species in the past century in the 297 ROK and their families 9.11 Classification functions 298

List of Figures Page Chapter 1 1.1 Map of the Yellow Sea 23 1.2 Map of the Yellow Sea Blueprint Region (YSBR) 26

Chapter 3 3.1 Low resolution scan of Daum.net image of the inner Geum Estuary divided 104 into four areas 3.2 Area 1 at low-tide, looking towards the Geum Estuary barrage (2006) 105 3.3 Area of tidal-flat remaining in the ROK (mid-late 2000s) 106

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List of Figures (cont.) Page

Chapter 4 4.1 The SSMP Study Region in May 1989 before construction started on the 119 Saemangeum seawall, and in late 2005/early 2006 (NASA images) 4.2 Origins of leg-flagged and colour-banded birds resighted by the SSMP 130 4.3 Migration timing of 21 shorebird species in the Study Region 131 4.4 Bar-tailed Godwit in the Geum Estuary and the Saemangeum Estuarine System 134 on northward migration (2006-2008) 4.5 Great Knot in the Geum Estuary and the Saemangeum Estuarine System on 135 northward migration (2006-2008)

Chapter 5 5.1 Location of wetlands surveyed in May 2008 158

Chapter 6 6.1 One of the high-speed vessels used in the surveys 175 6.2 Land-based points on Socheong Island used for seabird counts 176 6.3 Number of species recorded by month 178 6.4 Distribution of Yellow-billed Loon 181

Chapter 7 7.1 Southward migration routes across the Yellow Sea proposed by Gore & Won 194 (1971) and migration route connecting the Korean Peninsula to Japan (Brazil 1991) 7.2 Hypothesised migration routes and breeding areas reached by the Northern and 195 Southern Crossings 7.3 Socheong Island and survey circuits 200 7.4 Numbers of Brown-eared Bulbul and Olive-backed Pipit recorded during 12 201 Whole Island Counts in April and May 7.5 Number of Landbirds recorded during each of the 13 Whole Island Counts 204 7.6 Numbers of Grey Wagtail and Little Bunting recorded by ten-day period 206 7.7 Numbers of Naumann‘s Thrush and Dusky Thrush recorded during the 13 208 Whole Island Counts 7.8 Numbers of Asian Stubtail and Red-flanked Bluetail recorded during the 12 210 Whole Island Counts in April and May 7.9 Numbers of Yellow-browed Warbler, Eyebrowed Thrush and Chestnut Bunting 212 recorded during Whole Island Counts 7.10 Comparison of estimated landbird bird-days on Socheong and landbird bird- 226 days on Hong Island during northward migration

Chapter 8 8.1 Location of Eocheong 236 8.2 Numbers of Little Bunting and Dusky Thrush in 2003 244 8.3 Number of Dusky Thrush, Brambling and Black-tailed Gull recorded in 2011 245 8.4 Daily changes in number of birds (all species) recorded each day of survey in 250 2003 and 2011 8.5 Composite of 1000-mb precipitation rates for the day before eight large 252 Inclement Weather Arrivals 8.6 Composite of 850-mb vector winds on eight dates with Inclement Weather 253 Arrivals 8.7 Composite of 850-mb vector winds during five large Fair Weather Arrivals 254 8.8 Numbers of Chestnut Bunting, Eyebrowed Thrush and Yellow-browed Warbler 256 between May 8th and May 16th 2011 13

Acronyms and Nomenclature

Main Acronyms Used

AWSG Australasian Wader Studies Group CBD Convention on Biological Diversity DPRK Democratic Peoples‘ Republic of Korea DSI Decrease Susceptibility Index EAAF East Asian-Australasian Flyway IBA Important Bird Area IOP International Organisation Partner IUCN International Union for the Conservation of Nature KARICO Korea Agriculture and Rural Infrastructure Corporation KNP Korea National Parks service MAFF Ministry of Agriculture, Forestry and Fisheries MDG Millennium Development Goals MOE National Ministry of Environment NCEP-NCAR National Centers for Environmental Prediction-National Center for Atmospheric Research NGO Non-government Organisation NIBR National Institute of Biological Resources (within the national Ministry of Environment) NIER National Institute of Environmental Research (within the national Ministry of Environment) NPMBC National Parks Migratory Bird Research Centre (within the Korea National Parks service) ROK Republic of Korea SES Saemangeum Estuarine System SSMP Saemangeum Shorebird Monitoring Program UNDP-GEF United Nations Development Programme-Global Environment Facility YSBR Yellow Sea Blueprint Region

Nomenclature Throughout, the taxonomy and nomenclature of bird species follow Moores & Park (2009). Scientific names are included only for the first reference to the species in the text; and are also provided for all regularly occurring ROK species in the Appendix (pp. 316-322).

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SYNOPSIS

The Yellow Sea is at the heart of the East Asian-Australasian Flyway (EAAF). It supports huge numbers of migratory shorebirds and a diverse assemblage of globally threatened species. At the same time, all three of the Yellow Sea‘s main habitats (intertidal wetland, open sea and islands) are under enormous anthropogenic pressure. There has, however, been little research within the region that aims to determine distribution and to identify population trends in bird species. Improvements are also needed in methods of gathering, organising and sharing of information and data in ways that can increase their usefulness for conservation. The primary aim of this thesis is the improvement of conservation opportunities for avian biodiversity in the Republic of Korea (ROK) part of the Yellow Sea, through improving the knowledge base on birds and their habitats. This aim was fulfilled through a diverse range of research approaches. In Chapter 2, ornithological literature is reviewed, sources of bias are assessed and a method is developed through which substantial long-term declines can be identified in a third of the nation‘s regularly occurring bird species. In Chapter 3, measurements are made of remaining intertidal wetland using statellite imagery and ImageJ and Arcview. We estimate that probably 75% of the ROK‘s historical intertidal wetland has already been destroyed. In Chapters 4 and 5, we document declines in shorebird numbers caused by reclamation. Through survey immediately prior to and following seawall closure, we demonstrated that the majority of affected shorebirds could not relocate to adjacent wetlands following loss of a major staging site. Through a national shorebird survey, we were able to confirm that the same shorebirds were unable to relocate to other of the ROK‘s internationally important wetlands. In Chapter 6, high-speed commercial ferries were used to conduct surveys of seabirds at sea, closing several information gaps on seasonal distribution and abundance, and identifying sources of bias in the count method. In Chapters 7 and 8, landbird counts were used to improve understanding of migration phenology and migration strategies. Two main migration corridors were identified, and the influence of weather systems on migration was also assessed. In Chapter 9, recommendations are made towards improving information gathering and sharing, and an index for identifying species most susceptible to decline is presented. It is intended that these methods and results will be of value and can be built on further - not only here in the ROK, but also in other regions where there are also multiple threats to biodiversity and few resources available for research and conservation 15

Chapter One

BACKGROUND: CONSERVATION, GEOGRAPHY, AVIAN BIODIVERSITY AND THE AIMS OF THE RESEARCH

1.1 BACKGROUND AND AIMS 1.1.1 Introduction The primary aim of this research is the improvement of conservation opportunities for the avian biodiversity of the Republic of Korea (ROK), most especially within the ROK part of the Yellow Sea. In combination, the thesis provides a framework for the improved collection, interpretation and sharing of data and for understanding the influences of large-scale ecological and anthropological effects on bird species in the ROK part of the Yellow Sea. The Yellow Sea Blueprint Region (YSBR) is a subregion of the Yellow Sea that lies within the territory of the ROK. It includes extensive intertidal wetland, marine waters and numerous islands. This subregion was first delineated by the author on behalf of the conservation organisation Birds Korea in 2008. The name YSBR was coined to focus conservation attention on a subregion of shared ecological character and governance by a single nation that is of high importance to the conservation of national and regional avian biodiversity (Birds Korea 2010a). The YSBR contains many of the ROK‘s internationally important wetlands (as defined by Ramsar 2005) and 19 Important Bird Areas (IBAs) (BirdLife International 2003). Each year, it regularly supports >30 migratory bird species of global conservation concern as defined by BirdLife International (on behalf of the IUCN), as globally Near Threatened, Vulnerable, Endangered or Critically Endangered. The YSBR is also a subregion in which there is much habitat loss (historical and ongoing), degradation and unsustainable use (UNDP-GEF 2007). Large-scale challenges to conservation within the subregion, as in much of the ROK and the Yellow Sea (shared by China and the DPR Korea), include: high human pressures on natural resources; a very high percentage of migrant bird species potentially threatened by human activities; inadequate research effort; poor information sharing; and inappropriate policies and weak conservation legislation. Within the YSBR, further large-scale infrastructure 16

proposals include more reclamation, tidal power-plants and offshore wind farms (Birds Korea 2010a). There are as yet no long-term (>20 year) monitoring programs focused on the avian biodiversity of the YSBR or the ROK. There are major information gaps on almost all bird species and only limited count data available for identifying declines in a few species. There are, however, clear targets and deadlines for assessing and reducing national and global biodiversity loss by 2020 as set out by the Aichi Biodiversity Targets (CBD 2010). There is therefore an urgent need to improve the knowledge and science base on avian biodiversity status and trends in the ROK and the YSBR. The following sections explain the aims, rationale and background to the research.

1.1.2 Conservation Framework The ROK is a member state of the United Nations (UN), and a signatory to the Convention on Biological Diversity (CBD) and the Ramsar Convention (―Ramsar‖). The UN-led Millennium Development Goals (MDG) and Principles for Sustainable Development (UN 1992), CBD and Ramsar together provide clear, objective and agreed strategies, targets and time-lines to achieve the conservation of biodiversity. The research was therefore designed in response to key texts including: 1. The UN-led MDG Environmental Sustainability Targets that demanded a significant reduction in the rate of biodiversity loss by 2010; and that call for an integration of ―the principles of sustainable development into country policies and programmes‖ by 2015. Principles of sustainable development include the ―Precuationary Principle‖, Principle 15: ―In order to protect the environment, the precautionary approach shall be widely applied by States …Where there are threats of serious or irreversible damage lack of full scientific certainty shall not be used as a reason for postponing cost-effective measures to prevent environmental degradation‖ (UN 1992). 2. CBD‘s Strategic Plan for Biodiversity 2011-2020 which calls by 2020 for ―the rate of loss of all natural habitats (to be) at least halved and where feasible brought close to zero‖ (Target 5); ―the conservation status (of threatened species), particularly of those most in decline, (to be) improved and sustained‖ (Target 12); and ―knowledge, the science base and technologies relating to biodiversity, its values, functioning, status and trends, and the consequences of 17

its loss… improved, widely shared …and applied‖ (Target 19) (―the Aichi Biodiversity Targets‖, CBD 2010); 3. Ramsar Articles and guidance provided through Resolutions, including Resolution VII.21 (requiring contracting parties to modify policies relating to intertidal wetlands); Resolution IX.15, which requested details on the impacts of the Saemangeum reclamation on populations of migratory waterbirds (see Chapter 4); and Resolution X.I, the Ramsar Strategic Plan 2009-2015, including Goal 2 which calls for appropriate management and wise use of those internationally important wetlands that are not yet formally designated as Ramsar sites.

1.1.3 Research and Conservation Challenges The MDG Target of reducing the rate of biodiversity loss and the Aichi Biodiversity Targets make the assumption that species and the ecosystems they are part of are in decline, and demand an appropriate and timely conservation response. This requires an understanding of the present status of biodiversity (defined by Glowka et al. 1994). Birds are better-known and easier to research than any other comparable group of organisms. At a range of geographical scales, indicators based on bird data have proven to be useful for tracking progress in addressing the biodiversity crisis. Research and strategies developed to conserve avian biodiversity in other regions often have value for the conservation of other biodiversity too (BirdLife International 2010). Butchart et al. (2004) were able to confirm a deteriorating threat status for the world's birds, especially for those species known to be of global conservation concern. Moreover, in many of the world‘s developed nations long-term bird monitoring programs with standardised methods (in some cases conducted over several decades) have identified a large number of species showing declines. These include some species that are still widespread and relatively abundant like Eurasian Tree Sparrow Passer montanus (Vorisek et al. 2008), and others that are concentrated at rather few sites like the rufa subspecies of Red Knot Calidris canutus (Niles et al. 2008). Some long-term monitoring programs, by building on previous research and by accounting for sources of variability, have reduced much of the noise inherent in field-studies. They have thus also been able to identify probable causes of these species‘ decline at the site level (Burton et al. 2003, 2006); at the national level (Donald et al. 2000); and 18

at the range and population level (Both et al. 2004, Baker et al. 2004, Niles et al. 2008). In general, declines tend to have been greater for species of some habitat types than others, e.g. in agricultural areas in Europe and in wetlands in Asia (Brickle et al. 2000, Donald et al. 2001, Wetlands International 2010), with habitat loss likely most dangerous to species that are ecologically specialized (Owens & Bennett 2000). Some research also suggests that migratory species might be more susceptible to decline than resident species, potentially due to the exposure of migrant birds to human activities in breeding, staging and non-breeding areas and the link between their non-breeding and breeding fitness (Newton 2004). Migrants are also considered to be susceptible to the effects of rapid climate change, as climate change can lead to an increasing mismatch between migration phenology and seasonally optimal conditions (Both et al. 2006). For both sedentary and migratory species, the causes of decline are often highly complex and difficult to discern with confidence. Nonetheless, they are likely to be the direct or indirect result of one or more of the often interrelated ―five principal pressures directly driving biodiversity loss (habitat change, overexploitation, pollution, invasive alien species and climate change)‖ (CBD Secretariat 2010). In combination these ―Principal Pressures‖ can act to form a deadly anthropogenic cocktail (Travis 2003), driving declines while making interpretation of the causes and the development of appropriate conservation responses highly challenging. Identification of declines and of their causes is essential if appropriate and timely conservation responses are to be developed. In the ROK, in contrast to most developed nations, there are no large-scale, long- term bird- or habitat-monitoring programs; there is no recognised committee to organise species‘ records at the national level; no universally accepted up-to-date national bird checklist; no national population estimates or population trend assessments available for the majority of bird species; and there is no national partner to BirdLife International (or other leading international conservation organisation), with which to try to coordinate research on a species throughout its range. There has also been very limited research within the ROK on the habitat requirements of any bird species, with the exception perhaps of the nationally extirpated and globally Endangered Oriental Stork Ciconia boyciana (Kim 2009). The near-absence of any reliable baseline understanding of distribution, habitat use or population trend for the majority of species is considered by the author be a major hindrance to the 19

development of appropriate research projects and to the conservation of avian biodiversity. While there has been a recent growth in the ROK in the number of eco-centres and government bodies working on environmental issues (MOE 2012), most of these do not yet conduct or coordinate field research, nor do they make relevant data publicly available. There are therefore still only three main sources of easily accessible data on birds from regular government-led survey programmes with which to try to develop a baseline understanding of species‘ status and population trend. Data in these are often presented in ways that limit their value. The first is the 2010 report of the Survey and Resource Management of Wildlife programme (NIBR 2010). This was published online in 2011 by the National Institute of Biological Resources (NIBR), within the national Ministry of Environment (MOE). This NIBR research has since the mid- 1990s been designed to evaluate the ecological characteristics of wildlife in the ROK, with the main focus on ―game species‖, a few indicator species of five main habitats (mountains, hilly areas, farmland, built-up areas and the coastal zone) and species listed under the Convention on Trade in Endangered Species of Fauna and Flora. Calculations of density per 100ha each year are now made for >20 widespread bird species based on their density in 406 randomly-selected quadrats throughout the country. However, while possible causes of decline are suggested for a few species, there is no review of habitat change within or close to the quadrats or description of possible changes in survey method or observer experience. There has also been no investigation of regional effects on populations. Considering the small number of sites being surveyed, and the rapid change in much of the national landscape (see Section 1.5), caution is required in interpreting these data. A second source is the annual winter bird census coordinated by the MOE. The ―MOE Census‖ was initiated in 1999 and now covers >170 sites in the mid-winter period (MOE 2010). However, the MOE Census reports also provide few details on count methods, observer experience or changes to sites. There are also numerous errors in identification (Chapter 2, Section 2.2.5). The third is research conducted by the National Parks Migratory Bird Research Centre (NPMBC). The NPMBC was formally opened in 2007 (Chae 2007). Research effort is focused on the distribution and abundance of birds on two islands towards the south of the YSBR, though it also includes field-based studies on other taxa at other sites. The NPMBC banding program has improved knowledge on the use by migrant birds of these two islands, and also confirmed the movement of some species between 20

them and Japan (KNP 2007, 2010). However, banding areas have been greatly modified since 2007, monitoring effort is inconsistent, and most count data in NPMBC annual reports (KNP 2005-2010) are presented without details of dates or mean or peak counts. Moreover, NPMBC research has yet to address larger ecological effects on migratory birds, including the influence of geography on migration routes and the day- to-day influence of weather on natural variability in the timing of migration, orientation, use of stopover sites or population trends (cf. Shamoun-Baranes et al. 2010a). An improvement in understanding of bias and of ecological effects at a range of scales is required before data from any of these three survey efforts can be used to identify possible underlying population trends in a more robust way. Furthermore, there is still apparently no clear structure for various government and research bodies to assess the merits of data; data appear to be poorly shared between ministries; and in many cases government data are more or less closed to public review (or are at least extremely difficult to access). National assessments of biodiversity including ROK (2009) and MOE (2012) therefore appear flawed. Figures within ROK (2009) for example not only appear to exaggerate the area of intertidal wetland that remains but also suggest that reclamation by drainage has led to an increase in national wetland area of 8% (Chapter 3). Moreover, the estimate of intertidal wetland area in ROK (2009) does not match the estimate in MOE (2012), even when based on government data published the same year. For the present research too, datasets on e.g. shorebirds, weather and vegetation were requested from specialist government bodies but were not received – so that unpublished data or alternative sources of some of the same information from outside of the ROK needed to be utilised. Information gaps and poor sharing of information of this kind likely contribute to the lack of robust science underlying both conservation policy and many major development projects. Perhaps as a result too, MOE (2012) provides neither data nor information on any bird species suspected to be in decline; large-scale reclamation (i.e. the conversion of natural wetland to dry land and artificial wetland by mechanical means) of Ramsar- defined internationally important wetland is still described as ―environmentally- friendly‖ (Ministry of Agriculture, Forestry and Fisheries [MAFF] in Moores 2003a, Kim 2010); and the ongoing deep-dredging and damming of rivers, including internationally important wetlands and IBAs (Moores et al. 2010) has even recently been promoted by the highest levels of government as ―an exemplary model of environment-friendly endeavours‖ (in Korea Herald 2010). 21

At the same time, there is evidence contained within the specialist literature that large-scale infrastructural development of this kind (in some cases combined with other Principal Pressures) is indeed causing a decline in avian and other biodiversity in the ROK, as it is in other developed regions. The ROK is one of the most densely- populated countries in the world, with between 487 and 505 people/km2 (United Nations 2009; World Atlas 2011). Human pressures on land and natural resources are extremely high, and many bird species are likely to be in decline. Several bird species have become nationally-extirpated during the past century (Chapter 2). Analysis by the author of data in NIBR (2010) suggests declines in widespread bird species, including of 49% in Eurasian Tree Sparrow and of 57% in Black-naped Oriole Oriolus chinensis over the past 15 and 16 years respectively. Even the Yellow Sea as a whole has suffered extensive environmental degradation, attributed largely to pollution and unsustainable use (UNDP-GEF 2007), to the extent that it is now in a phase of ecological regime shift, with giant jellyfish and green algae blooms (Sun 2010). Although there are few details available, it is apparent that many of the terrestrial, freshwater and marine habitats of the YSBR (and of the ROK as a whole) have been greatly modified and degraded during the past century especially. While analysis of bird population trends has generally not been forthcoming from the ROK, large-scale population declines have already been described for several regularly occurring migratory bird species of the YSBR and ROK in other parts of their ranges. These include some shorebird species in Australia (Gosbell & Clemens 2006, Rogers et al. 2009, Garnett et al. 2011, Wilson et al. 2011) and some shorebirds and landbirds in Japan (Komeda & Ueki 2002, Ozaki 2008, Amano et al. 2010). Because part of many such species‘ population is found seasonally within the YSBR, declines in their regional or flyway population should in many cases also be apparent within the YSBR subregion too. Furthermore, it seems reasonable to assume that declines in those species that are most-dependent upon the YSBR will likely have been caused to a lesser or greater degree by the Principal Pressures within the YSBR itself, as suggested by Rogers et al. (2006a), van de Kam et al. (2008), Amano et al. (2010) and Birds Korea (2010a). In order to improve conservation opportunities within the present decade, this thesis therefore provides a pragmatic overview of the avian biodiversity of the ROK in general and of the YSBR in particular. The research refines knowledge of the temporal and geographical distribution of a large number of bird species. Ornithological 22

literature is used to identify suspected population trends since 1910, and fieldwork and recent publications are used to identify suspected contemporary trends in selected species dependent upon intertidal wetlands, marine waters and offshore islands - the three main habitats of the YSBR. Detailed explanations of methods are provided, as are peak counts, mean counts (where available), and dates of records for a large number of species recorded during fieldwork. Although such basic field data are often too thin for detailed analysis, summaries are included in most chapters. They help to improve the knowledge base and can help, subsequently, to influence research methods, data organisation and presentation, and conservation policy. In common with much other recent research on poorly known avifauna in East Asia, many of the data sets are not yet long-term enough or suitably designed for advanced statistical analysis (cf eight out of 11 papers published in the refereed journal Forktail in August 2011 contained no statistical analysis). Moreover, the scope of the present research is by necessity wide. Many of the variables affecting data that were gathered in fieldwork, over a short time period, remain poorly-known. Estimated indices that might have been developed through the present research were thus considered in several cases to be either unconvincing or potentially prone to extreme values, which could then have resulted in biased conclusions, as discussed by Fowler & Cohen (1999) and Amano et al. (2010). Throughout, the primary research aim is therefore to determine whether there are indications of declines in species‘ richness and abundance within the past century and whether these declines appear to be continuing. As most of the bird species of the YSBR are migratory, all chapters also investigate the hypothesis that migratory bird species are more susceptible to decline than sedentary species

1.2 THE YELLOW SEA 1.2.1 Physical Geography The Yellow Sea (Figure 1.1) is a shallow semi-enclosed sea lying between China in the west, and the Korean Peninsula to the east, between latitudes 41°00' N and 31°40' N and longitudes 117°35' E and 126°50' E, covering an area of approximately 458,000 km2 (Barter 2002). Historical sea-level rise within the past 10,000 years led to the formation of the present geography of the Yellow Sea. The Yellow Sea proper has an average depth of 44-55m (Hong et al. 1998, Koh 1999), at its deepest reaching only c. 100m near Gageo Island and c. 120m near the volcanic Jeju Island (see Figure 1.2). Within 30km of 23

much of the west coast of the ROK the sea-floor has a gentle slope, and the sea is less than 20m deep, while 50km offshore the sea averages >60m (Feng 1998). Tidal currents are strong within coastal areas, and there is a steadily increasing tidal-range northwards along the west coast of the ROK, with a tidal-range of 4m in the southwest and 9.3m (occasionally more than 10m) in the northwest (Koh 1997). This combination of shallow sloping sea bottom and large tidal-range in the Yellow Sea led to the development of some of the world‘s most extensive tidal-flats, covering an area of approximately 20,000 km2 in 2000 (Barter 2002).

Figure 1.1 Map of the Yellow Sea, showing tidal-range and area of intertidal wetland. (from Barter 2002). Smaller numbers denote the tidal-range in meters, and larger numbers the area of intertidal wetland in km2.

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1.2.2 Human Geography The Yellow Sea is one of the most heavily-exploited and disturbed marine regions in the world (Yellow Sea Ecoregion Planning Programme 2008). It is located in one of the world‘s most densely populated regions and the catchments of its major rivers, including the Yellow and Yangtze Rivers in China and the Han River in the ROK, support more than 10% of the global human population (BirdLife International 2003). Major cities lying close to the Yellow Sea include Shanghai (population >18 million: China Digital Times 2008) and Seoul/Incheon (population >24.5 million: Korea National Statistical Office 2008).

1.2.3 Climate The Yellow Sea lies at the eastern edge of the Asian landmass, with air and sea- water temperatures warmer southwards, and strong seasonal differences. Sea-surface temperatures at their extremes range from <-1°C in February in the coldest areas to >27°C in August in the warmest areas (Moores et al. 2001). Sea-surface temperatures are not evenly graduated north-south, however. There is a large Yellow Sea Cold Water Mass and Cold Surface Water Patches are regular phenomena in parts of the Yellow Sea (most especially off major peninsulas: Lu et al. 2009).

1.2.4 The East Asian-Australasian Flyway (EAAF) A ―flyway‖ is a descriptor for an assemblage of bird migration routes, in the Northern Hemisphere generally oriented on a north-south axis between northern breeding and southern non-breeding areas. The Yellow Sea is situated approximately at the mid-way and narrowest section of the East Asian-Australasian Flyway (EAAF). The hourglass-shaped EAAF extends north from the Yellow Sea to the Siberian and Alaskan tundra (where many of the EAAF‘s shorebird species breed), and south to include both Australia and New Zealand (where many shorebird species spend the boreal winter). Due to the combination of its location on the EAAF, its climate (remaining largely unfrozen in winter) and the vast extent of its intertidal and sub-tidal wetlands, the Yellow Sea is an extremely important region for migratory waterbirds throughout the year. It provides essential habitat and refuelling opportunities for staging shorebirds during southward and northward migration, enabling some species to make spectacular non-stop flights between Australasia and East Asia and North America (Gill et al. 2008, Conklin & Battley 2011). The Yellow Sea also forms the 25

core of the breeding range for several specialised species, including the globally Endangered Black-faced Spoonbill Platelea minor and globally Vulnerable Saunders‘s Gull Chroicocephalus saundersi (BirdLife International 2011). During migration and in the boreal winter intertidal wetlands also support a substantial number of freshwater- or brackish zone-dependent species, e.g. Anseriformes and Gruiformes (MOE Census 1999-2010, Cao et al. 2008, BirdLife International 2011). The Yellow Sea thus supports huge numbers of waterbirds, serving a similar ecological role and function as the Wadden Sea of northern Europe. It is also, along with the East China Sea, an ecological barrier on the route of migratory landbirds. Many such species of landbird spend the boreal winter in Southeast Asia and southern China and breed in the temperate mixed forests of the Amur-Heilong River basin. This latter region has been described as containing the most biologically diverse temperate forests in Asia and possibly the world (Simonov & Dahmer 2008).

1.3 THE YELLOW SEA BLUEPRINT REGION (YSBR) 1.3.1 Physical Geography The YSBR (Figure 1.2) is one part of the Yellow Sea delineated by the author based on its ecological connectivity and distinctiveness; its accessibility; its nationally and internationally important avian biodiversity; and its governance by one national state alone, the ROK. The YSBR is contained within an irregular rectangle north- south between 37°50' N and 33°20' N, and west-east between 124°30' E and 126°55' E. The northern edge of the YSBR lies approximately 40km south of the Hwanghaenam Province coast (DPRK), and the southern edge lies within 10km of the coastline of Jeju Island. The western edge is open sea, on a line from the west of Socheong Island in the north, Gageo Island in the southwest, and Jeju‘s Mara Island in the south. Much of the YSBR can therefore be accessed by commercial ferries. The eastern edge follows the deeply indented western coast of the ROK. The YSBR thus includes all inshore and marine areas; all islands <2000ha in area (and habitats within c. 100m of the sea on islands >2000ha in area); and all intertidal wetlands (including natural, near-natural and semi-natural wetland and other hinterland habitats within c. 100m of areas with tidal influence). Semi-natural intertidal wetlands are here defined as recently impounded (in 2006 or subsequently) and pre-2010 able to support many typical intertidal species (e.g. Saemangeum and Namyang Bay: Table 1.1). This 26

definition excludes older reclamations (e.g. Seosan, impounded in the late 1980s) which support bird species more typical of freshwater and floodplain habitats.

Figure 1.2 Map of the Yellow Sea Blueprint Region (YSBR), outlined in yellow, and highlighting main locations surveyed in the thesis (see also Table 1.3.2), including the Saemangeum Estuarine System (―SES‖) (Chapter 4); the Northern, Central and Southern Transects used for seabird at sea research (Chapter 6) and Socheong, Eocheong, Gageo, Hong and Heuksan Islands (Chapters 7 & 8). Note that the YSBR includes the whole of small islands <2000ha in area, and only those parts of larger islands that are within 100m of the sea.

1.3.2 Main Research Sites Fieldwork for the present research included shorebird counts in intertidal wetlands (Chapters 4 and 5); counts of seabirds along two main seabird transects (Chapter 6); and counts of landbirds on several offshore islands, from hereon defined as islands >10km from the mainland (Chapters 7 & 8). Main sites are listed in Table 1.1.

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Table 1.1 Location and habitat type of selected YSBR Sites. Site Latitude Longitude Habitat Type Chapter Socheong Island 37°45' N 124°44' E Island/Northern Transect 7 Ganghwa Island 37°35' N 126º25' E Intertidal wetland 5 Yeongjong 37°27' N 126º32' E Intertidal wetland 5 Incheon Port 37°48' N 126°62' E Northern Transect 6 Song Do, Incheon 37°25' N 126º39' E Intertidal wetland 3,5 Namyang Bay 37°10' N 126°48' E Intertidal wetland & rice-fields 3,5 Asan Bay 36°54' N 126°54' E Intertidal wetland & rice-fields 3,5 Cheonsu Bay 36°37' N 126°25' E Intertidal wetland & rice-fields 5 Weiyeon Island 36°13' N 126°05' E Island 8 Eocheong Island 36°07' N 125°58' E Island 8 Yubu Island 35°59' N 126°36' E Intertidal wetland & island 4 Geum Estuary 36°01' N 126°35' E Intertidal wetland 3,4,5 Saemangeum Estuarine System 35°50' N 126°45' E Intertidal wetland 3,4,5 Gomso Bay 35°35' N 126°36' E Intertidal wetland 4 Mokpo Wetland 34°47' N 126°25' E Intertidal wetland 5 Chilbal Island 34°47′ N 125°48' E Seabird breeding colony 2,6 Bigeum Island 34°42' N 125°54' E Southern Transect 6 Heuksan Island 34°41' N 125°28' E Island/Southern Transect 6,7,8 Hong Island 34°40' N 125°10' E Island 7,8 Hatei Island 34°23' N 125°18' E Southern Transect 6,9 Gageo Island 34°03' N 125°09' E Southern Transect 6, 8, 9

1.3.3 Main Habitats 1.3.3.1 Intertidal wetlands Intertidal wetlands include the outer part of the Han-Imjin Estuary (free-flowing, and forming part of the border with the DPRK), the Geum and the Yeongsan Estuaries (both of which have estuarine barrages), and extensive tidal flats found along both the mainland coast and also in bays and along the coast of some islands. Reclamation has affected much of the coastline (Koh 1997, Moores 2006; Chapters 3-5). Most of the remaining natural and near-natural areas of intertidal wetland are largely unvegetated, with extensive Suaeda saltmarsh more or less restricted to the upperparts of mud-rich tidal-flats in Gyeonggi Bay (in the northeast). Almost bare sand and sand-mud mix tidal-flats become prevalent southward.

1.3.3.2 Marine waters Most of the YSBR is sea, from hereon categorised as ―open sea‖ (defined as marine waters >2km from shore) and ―inshore waters‖ (defined as marine waters within 2km of islands and the mainland, greater than 6m depth at low tide). Most open sea in the YSBR ranges in depth from between 10m and 50m. However, there is a sea-trench of 100-120m depth that extends towards the southwest of the YSBR, near to Heuksan and Gageo Islands.

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1.3.3.3 Islands and islets As elsewhere within the Yellow Sea, sea-level rise approximately 10,000 years ago part-submerged many hills and hill ridges to form islands, while the much older Jeju Island and associated islets to the south were created by volcanic activity. Islands range greatly in size and ecological character. Within the ROK as a whole, there are 494 inhabited islands with a mean area of 790ha and 2,721 uninhabited islands with a mean area of 3ha. The largest concentration of islands is within Jeollanam Province in the southwest of the ROK, where there are 1,966 islands, with a total area of 183,600ha (Kim et al. 2009). Although some of the Jeollanam Province coast lies outside of the YSBR, most of the YSBR‘s estimated 2000 islands and islets still lie within this one province (Birds Korea 2010a). Although many islands are clustered close to the mainland and/or are linked to other islands by intertidal wetland, a small number are more isolated, and are able to support seabird colonies. The vegetation of most of the larger islands in the YSBR has been heavily modified by forest-clearance, replanting and grazing by feral goats (Moores et al. 2001). Where natural vegetation remains, sedges (e.g. Carex spp) and warm temperate broadleaved evergreen forest (including Camellia japonica, Cyclobalanopsis glauca, and Schima superba: Choi et al. 2010) tend to occur north to 36º N. Middle temperate zone deciduous and coniferous woodland (after Choi et al. 2010) is increasingly dominant north of 37º N. The brief geological history of most islands, their lack of isolation, and perhaps their high human use has likely limited their level of avian endemism, and only Jeju Island is known to support endemic subspecies of birds. At least one of these (the bedfordi subspecies of Eurasian Nuthatch Sitta europaea) has already been extirpated (Moores & Park 2009, Kang et al. 2010). However, YSBR islands still support a large proportion of the world‘s breeding population of at least three migrant species (Black- faced Spoonbill, Swinhoe‘s Storm Petrel Oceanodroma monorhis and Styan‘s Grasshopper Warbler Locustella pleskei: Birds Korea 2010a).

1.3.4 Human Geography There is a large human population within the YSBR and most of the mainland coast and almost all islands larger than 5ha have been substantially modified by people. Remaining intertidal areas and most inshore waters are used intensively for fishing and 29

in many areas for mariculture, while some open sea areas are also heavily fished and cultivated and crossed by commercial shipping lanes (Moores et al. 2001).

1.3.5 Climate Regional climate is a major influence on the distribution and migration strategies of many of the bird species of the YSBR. Within the YSBR, mean annual air temperatures on land range from 14°C in the southwest to 10°C in the northwest. The lowest average monthly mean temperatures are –2°C in January in the northwest and 2°C in the southwest. The highest average monthly mean temperatures in August are 25°C (or below) in the northwest and >26°C in the southwest. Air temperatures across the region, and as a result vegetation distribution, growing seasons, and landbird migration strategies (Chapters 7 & 8) are strongly influenced by proximity to or distance from the Yellow Sea. For example, Beijing, which is c. 140km north of the Yellow Sea coast, is several degrees warmer in both April and May than either Baekryeong Island or even Jeju Island, both within the YSBR, lying 760km and 1150km respectively to the southeast (Table 1.2). Temperatures in April and May are also generally higher in Japan than at similar latitudes in the YSBR and elsewhere on the Korean Peninsula. Mean April and May temperatures in 2010 were 3°C and 2.3°C cooler respectively in Gunsan than in Tokyo (www.TuTiempo.net).

Table 1.2 Monthly mean temperatures (°C) in 2009 at selected weather stations in the YSBR and the wider region. YSBR/ROK Lat. Long. Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Baekryeong 37.96 124.63 -0.4 1.6 3.9 10.2 15.6 18.9 21.7 23.9 20.3 15.9 7.1 0.6 471020 Incheon 37.46 126.63 -1.2 2.9 6.0 11.6 17.3 20.8 23.3 25 21.3 16.3 7.5 -0.1 471120 Seoul 37.36 126.96 -1.9 2.9 6.1 12.8 19.1 22.5 24.3 25.7 21.7 15.9 6.8 -1.1 471080 Gunsan 35.98 126.7 0 3.5 6.5 11.2 17.4 21.7 23.9 25.0 21.2 16.2 8.3 1.1 471400 Jeju 33.28 126.16 6.0 8.5 9.4 13.1 17.3 20.7 24.2 25.8 23.1 19.5 12.8 7.9 471850

Outside YSBR Beijing 39.93 116.28 -3.5 0.5 6.5 15.7 22.5 25.7 26.3 24.8 20.4 13.8 1.4 -3.3 545110 Tianjin 39.10 117.16 -3.0 1.0 7.2 15.5 23 26.1 27.3 25.8 21.3 15.2 1.7 -2.6 545270 Dalian 38.9 121.63 -2.9 -0.2 4.2 12.0 18.9 22.6 24.1 25.3 20.8 15.2 2.5 -2.9 546620 Qingdao 36.06 120.33 -0.8 3.6 6.6 12.9 19.3 23.3 24.5 25.2 21.8 17.4 5.9 0.7 548570 Shanghai 31.40 121.46 3.9 9.0 10.1 16.3 21.9 26.2 28.8 27.8 25 21.2 12 6.4 583620

Note: All data fromTuTiempo.net, including the identification code of each weather station (in italics), their decimalised latitude and longitude, and the mean monthly temperatures. 30

Sea surface temperatures in February range from 3-4°C in the north of the YSBR to 11°C in the south. In colder than average winters (e.g. 2001 and 2011), sections of the intertidal zone and inshore waters close to the mainland can be covered by ice, especially within Gyeonggi Bay (offshore from Incheon Port). However, open sea areas remain ice-free. In August, the warmest month, sea surface temperatures are 23°C in the north and 27°C in the south (Moores et al. 2001).

1.4 RESEARCH ON THE AVIAN BIODIVERSITY OF THE YSBR 1.4.1 Introduction To date there has been no ornithological review of the YSBR, though the assessment of Birds Korea (2010a) was that approximately 480 species of bird have been documented in the YSBR since 2000; that between 335 and 340 of these species are recorded annually; and that 80% or more of regularly occurring species are typically absent from the YSBR on a seasonal basis. In the absence of robust and long-term monitoring programs, the identification of long-term population trends in any of these species needs to be interpreted from the relatively soft data contained within one or more of five major ornithological reviews that cover parts of the YSBR or mainland habitats adjacent to it. These are Austin (1948), covering the whole Korean Peninsula (though intentionally excluding Jeju); Gore & Won (1971) and Park (2002) covering the ROK, though both with a strong bias to mainland areas (Chapter 2); and Won Hong-Koo (1963-1965) and Tomek (1999-2002) covering the DPRK. Collectively, these reviews describe the distribution and abundance of bird species during more than a century in which ornithological activity was much influenced by formal Japanese occupation (1910-1945); by war (1950-1953), which consolidated the division of the Korean Peninsula into two nations; and by access restrictions to much of the coastal zone which in the ROK have only been eased in recent years (Long et al. 1988, Moores 2006, Duckworth & Moores 2008). From the late 1980s and especially in the past decade there has been a substantial increase in ornithological activity in the YSBR, leading to a greatly improved understanding of some species‘ status and a rapid growth in the number of species recorded (Park 2002, KNP 2005-2010, Moores 2007, Choi et al. 2011). However, numerous information gaps remain and there are inconsistencies between existing checklists and accounts, requiring clarification and an improvement in documentation. 31

1.4.2 Intertidal Wetlands The first major surveys to identify internationally important intertidal wetlands for shorebirds within the YSBR were conducted in 1988 (Long et al. 1988), and by 2003 at least 19 internationally important shorebird sites had been identified nationwide (15 in or immediately adjacent to the YSBR: Chapter 5). In total, the 19 sites supported 12.7% and 8.7% of the shorebirds of the EAAF on northward and southward migration respectively. The vast majority were concentrated at relatively few sites, all within the YSBR (Yi 2004). Generally, shorebirds are considered to be especially vulnerable to habitat loss and degradation (Piersma & Baker 2000, Stroud 2006), and many of the most important sites in the ROK are either undergoing (Saemangeum, Namyang Bay, Asan Bay) or are threatened by reclamation (Ganghwa Island) (Chapters 3-5). Although research was being conducted in several sites that were being reclaimed, data from most government research in such areas remain largely inaccessible to the conservation community. There has also been no study aiming to determine the impact of reclamation on shorebird numbers at the site-, national- or Flyway-level, or to determine whether shorebird numbers in the ROK have declined in recent decades.

1.4.3 Open Sea Despite the suspected diversity and the proven local abundance of some seabird species in the YSBR at breeding colonies, major information gaps remain. Although some colonies are well-researched (Lee 1989, Park & Won 1993, Lee et al. 2009), almost no information is available on the distribution of seabirds at sea or their conservation status in the YBSR or the Yellow Sea as a whole. For example, Park (2002) and Tomek (1999, 2002) in their respective ornithological reviews do not include any records of several seabird species now known to be regular in the YSBR; the national Ministry of Maritime Affairs and Fisheries review of marine biodiversity (MOMAF 2006) and the Yellow Sea review by UNDP-GEF (2007) contain no reference to seabirds; and Kim & Pae (2008) refer to seabirds only in the section on information gaps. In the Chinese part of the Yellow Sea too, Ma (2008) highlights the ―very limited data available‖ for seabirds. Most of the limited research on seabirds at sea within the YSBR prior to this research was conducted by the present author. Counts were made opportunistically from commercial ferries along three transects (Figure 1.2) in all months except January and February on a total of 103 journeys (Chapter 6, Section 6.1). These counts proved 32

that large numbers of seabirds were present at sea within the YSBR, and clarified the need to conduct counts with a more robust method in order to improve understanding of seabird seasonal and geographical distribution.

1.4.4 Offshore Islands Offshore islands in the YSBR support specialised breeding species; they are used by large numbers of transitory migrant birds; and they offer the best opportunity for gathering data that might be used to identify population trends in a diverse range of migratory landbird species. Hashimoto in the 1930s made the first detailed observations of breeding seabirds and migrant landbirds on an offshore island in the YSBR (reported by Austin 1948). Several decades later, landbird and seabird breeding surveys were first conducted on Gageo Island (Won & Yoon 1970, Hahm et al. 1994), and subsequently on the Gugeul Islets, 3 km offshore from Gageo Island in the 1980s (Lee 1989). This research found large concentrations of breeding seabirds. As a result of this survey effort, the YSBR is believed to support >90% of the world‘s breeding population of Swinhoe‘s Storm Petrel (Lee 2009, Birds Korea 2010a). The same research also identified some threats to seabird colonies, including predation by rats and invasive alien plant species (Lee et al. 2009, Lee 2010a). An unknown number of small islands also support breeding Styan‘s Grasshopper Warbler, a poorly-known globally Vulnerable species, the majority of which migrate to offshore islands in the Yellow Sea and Japan to breed (BirdLife 2011). For landbirds, open sea is an ecological barrier that needs to be crossed without food or rest. Outlying islands in the YSBR are the first land that such birds reach after crossing the Yellow Sea on northward migration, and the last land before they undertake a sea-crossing on southward migration. As a result, especially in inclement weather in April and May, some offshore islands support a high number of species and occasionally large concentrations of migrant birds (Moores & Kim 2001, Moores 2007, Birds Korea 2010a). Partly in recognition of this, the NPMBC was established on two adjacent islands (Hong and Heuksan) to conduct regular bird counting programs in order to determine species‘ abundance and seasonality (Chae 2007). Nonetheless, major information gaps remain on the migration strategies of most species. No research had been conducted to understand the causes of the large variability shown year-to- year and between islands in count data. 33

In summary, a recent increase in ornithological activity in intertidal wetlands, at sea and on offshore islands has led to an improvement in the understanding of the distribution of several species. However, many information gaps remain. Moreover, data have not yet been analysed in relation to large-scale ecological effects (including geography and weather), and most recent research has not begun to address the impacts of human activities on species at the population level. There has been no research aiming to describe major influences on the population trends of the majority of species. An improved understanding of large-scale effects is needed if research is to contribute substantially to the improvement of conservation strategies aimed at reducing the rate of biodiversity loss in the YSBR and the ROK.

1.5 INFORMATION GAPS AND THE FIVE PRINCIPAL PRESSURES 1.5.1 Habitat Change Species entries on the IUCN Red List for which threats are classified reveal that at the global level habitat destruction is the overwhelming threat (Baillie et al. 2004). Habitat change (including habitat loss, degradation, disturbance and fragmentation) is likely to be causing a loss of avian biodiversity in the YSBR. However, there have been remarkably few studies on the effects of habitat change on bird species in the YSBR or in the ROK, including by reclamation and changes in forest and agricultural areas. Reclamation has been proven to cause massive changes to the ecology of intertidal areas and mass mortality of benthos (Rogers et al. 2006a, Sato 2006, Hong et al. 2007), including benthic animals which are fed on by shorebirds (Zwarts 1996, van de Kam et al. 2004). Generally, suboptimal feeding conditions that are then left available to shorebirds are believed to lead to increased mortality and decreased fecundity, and subsequent population decline (Battley 2002). However, there have been, before the present research, no studies in the Yellow Sea aimed at measuring the impacts of large- scale reclamation of a major staging site on shorebirds at the population level. Most of the landbird species in the ROK breed in wooded habitats. More than 70% of Korea is mountainous and it has been estimated that 8000 years before present 89% of the ROK (including most of the YSBR‘s islands) would have been naturally forested (Worldwatch Institute 2010). In the nineteenth century, most of the historical forest was likely made up of pine (especially Pinus densiflora) and deciduous oak species (based on Youn undated and Choi et al. 2010a). By the early twentieth century, 34

however, Anderson (1907) described the landscape he encountered near to Seoul as ―small cultivated valleys, and barren, dry, and much eroded hills‖ while by mid- century, ―The axes and rakes of the woodchoppers had swept clean one after another of the country‘s mountain ranges and ridges, leaving barren sandy paths and deeply eroded canyons in their wake‖ (Fennell 1952). This forest loss was assessed by Austin (1948) and others to have already contributed to the decline of White-bellied Woodpecker Dryocopus javensis richardsi (listed as nationally extirpated by Moores & Park 2009). During the period from the Korean War (1950-1953) to the end of the twentieth century, the total area of forest in the ROK continued to decline. Many remaining areas of ―open woods, checkered with small areas of wet grass which supported an abundant frog population‖ (Wolfe 1950) were lost, with most of the reduction in area of forest due to land conversion for agricultural and urban use (Youn undated). Due to national reforestation efforts since the 1970s, forest volume (though not area) has increased greatly in the ROK (Table 1.3), from a low point of 4.765 m3/ha in 1952 to 50.21m3/ha in 1996 (Youn undated). At present, 64% of the national territory is covered in forest (ROK 2009), with approximately two million hectares of 20-40 year old plantation forest (Youn undated).

Table 1.3 Forest by area and volume in the ROK between 1978 and 2007. Year Forest area Forest Stand Volume Volume per ha (ha) (㎥) (㎥) 1978 6,578,000 114,000,000 17.33 1980 6,568,000 145,694,000 22.18 1990 6,476,000 248,426,000 38.36 2000 6,422,000 407,575,000 63.46 2007 6,382,000 624,398,000 97.83

Note: From p.8, ROK (2009).

Gore & Won (1971: 53) predicted that these national reforestation efforts would lead to ―an increase in the numbers of many woodland species in the next twenty years‖. However, there are very few data for the 1970s or 1980s with which to assess population trends. More recently, analysis of data in NIBR (2010) instead suggests declines in some woodland species since the 1990s at least, including of 47% since 1996 in Common Pheasant Phasanius colchius (a species of woodland edge). Other species, including the Eastern Great Tit Parus minor, which is more tolerant of closed canopy forest, has in contrast increased 7% in NIBR quadrats since 1995. There has, 35

however, been no research in the ROK that has tried to identify long-term population changes in forest species, or to assess their susceptibility to decline. A large number of bird species in the ROK are ecologically-dependent upon floodplain wetlands. With the loss of natural wetland, many of these are now largely confined to rice-field areas (Moores 2002). Rice cultivation has been practised on the Korean Peninsula for several thousand years. By 1950, almost all natural floodplain wetland had been converted for rice agriculture or for housing and industrial use. By contemporary standards such areas were apparently bird-rich in the summer months, with Watercock Gallicrex cinerea, Striated Heron Butorides striata, Common Kingfisher Alcedo atthis, Grey Heron Ardea cinerea, Eastern Great Egret Ardea modesta, Japanese Quail Coturnix japonica, Far Eastern Skylark Alauda japonica, Grey Wagtail Motacilla cinerea and Eurasian Magpie Pica pica all listed as ―representative of the species to be found in the flat open wheat and rice fields surrounding the small country villages‖ (Fennell 1952). As of 2007, almost all of the nation‘s ―plains‖ (covering 17.9% of the national territory) that were not occupied by cities or industry were used for agriculture, with 60% given over to rice (an area of approximately 1,070,000ha), and the remaining 40% to other ―farms‖ (ROK 2009). No research has yet been conducted in the ROK to identify changes in the avian biodiversity of rice-growing and arable areas between 1950 and the present. However, the Watercock is now nationally scarce (Moores & Park 2009), and the Japanese Quail is classified as globally Near Threatened. Analysis of data in NIBR (2010) also suggests that several widespread and locally abundant species found mostly in agricultural areas have declined steeply since 2000 (when monitoring began). These include Barn Swallow Hirundo rustica (decline of 27% since 2000) and Rook Corvus frugilegus (decline of 39% since 2005).

1.5.2 Overexploitation and Hunting The overexploitation of birds through hunting likely caused declines in a broad range of species, both in the nineteenth and twentieth centuries. Some species that migrated through Korea to winter in Japan were presumably affected by the relaxation of Japanese gun laws during the Meiji Restoration (1868-1912), which resulted in large declines in Japan and East Asia of several geese and large waterbird species (Brazil 1991). Within Korea itself, trapping of large species like Red-crowned Crane Grus japonensis was also widespread in the late nineteenth century, increasing during 36

Japanese occupation (1906-1945) to the point that the species was ―almost at the point of extermination‖ by the late 1930s (Kuroda 1937 in Austin 1948). Other species that were hunted intensively for food appear to include the now globally Vulnerable Great Bustard Otis tarda and the Near Threatened Japanese Quail. An insight into the level of hunting pressure is provided by Wolfe (1950) who stated that the Common Pheasant was “Formerly abundant, but during the three years of [USA] army occupation (1945- 1948) it was greatly reduced in numbers. Not only did the thousands of soldier hunters take a heavy toll during the hunting season, but the ‗liberated‘ Koreans recognized no restrictions. They resorted to both trapping and poisoning for the market. By the fall of 1948 the pheasant had become a comparatively rare bird except in isolated localities.‖ Through until at least the 1970s, trapping of small birds for food was widespread, and by the time of Gore & Won (1971) ―the indiscriminate shooting of all species‖ for recreation was considered ―probably the main cause of concern‖ for bird conservation. The authors warned that ―it is not only rare birds which may be endangered to the point of extinction by uncontrolled shooting‖ (p. 53). While illegal hunting appeared to decline rapidly between the late 1990s and late 2000s, there are still apparently 20,000 hunters using shotguns and half a million hunters using air rifles in Korea (Anon 2010). The Crested Lark Galerida cristata, which was a formerly numerous species targeted by recreational hunters (Gore & Won 1971), is now almost lost to the ROK.

1.5.3 Pollution The twentieth century saw a massive increase in pollution in the ROK, in both agricultural and industrial areas, which likely led to a substantial decline of avian biodiversity. However, in the ROK almost no research has been conducted to suggest which species might have been most susceptible to the effects of pollution. According to Kim & Smith (2001) organochlorine pesticides were used extensively over the period 1946-1980, including hexachlorocyclohexanes, DDT, heptachlor, aldrin, dieldrin and endrin. Fry (1995) reviewed some of the effects of similar pesticides on birds, especially in the USA. His review identified organochlorine pesticides as causing reproductive impacts in birds; cited Carson (1962) as identifying the urban use of pesticides (primarily DDT) as a cause of mass songbird mortalities, with eggshell thinning by DDT metabolites a primary cause of reproductive impairment in birds; and listed other persistent organochlorine pesticides including dieldrin, endrin and aldrin as causing documented negative effects on birds and other biota. A further study found 37

that even small concentrations of dieldrin could prove fatal to thrushes (Jeffreys & Davies 1968). According to the Pesticide Action Network (1996), between 1980 and 1995, pesticide use in the ROK increased approximately 63% (from 16,132 tonnes to 25,834 tonnes), with 25,999 metric tonnes of pesticide-active ingredients used in 1993. Much of this growth was due to insecticide use on fruits, vegetables, ornamentals and greenhouse crops. Primary insecticides used in rice-fields included carbofuran and diazinon. Carbofuran has been described as highly toxic to birds and many species of fish (Extonet 1996). Fish and birds are also quite susceptible to diazinon poisoning, and bird kills associated with diazinon use have been reported in every area of the USA and at all times of the year (Extonet 1993). Both carbofuran and diazinon have also been detected in bird kills in the ROK (Kwon et al. 2004). Moreover, although the use of organochlorine pesticides has been (formally) discontinued in the ROK since 1980, persistent organochlorines were later detected in several waterbird species in the Nakdong Estuary (Busan), including a concentration of 6,119 ng/g fat weight of DDTs in three Little Tern Sternula albifrons collected between 1992 and 1994 (Choi et al. 2001). In addition, substantial concentrations of residues (particularly the oxidized form of heptachlor) remain in the soil, most especially in rice-fields (Kim & Smith 2001). Heptachlor-treated cereal grains in the USA have been identified as causing mortality in Common Pheasant and several other species of bird, also leading to reduced reproductive success in Canada Geese Branta canadensis. In addition, Heptachlor in earthworms was shown to be more toxic to one species of shorebird than DDT (Blus et al. 1984). It seems likely that many of the species typical of agricultural landscapes in the ROK will have been negatively affected by agricultural pesticide use in the ROK – both directly and through reduced food availability. However, there has been no research comparing historical and contemporary abundance or suspected population trends in species of agricultural landscapes with species in less-disturbed habitats. Other forms of pollution could also be affecting bird populations. Pollution and reduced water flow due to dams and water extraction can lead to the degradation of the quality of tidal-flats (Day et al. 1987, Paton et al. 2000). Moreover, coastal regions in East Asia are thought to be one of the highest acid input regions in the world (Doney et al., 2007). Increased acidification is linked to a decrease in calcification and strong negative impacts during early development on some species of bivalve molluscs 38

(Ishimatsu & Dissanayake 2010). Increasing acidification could therefore negatively impact the potential prey of shorebird species like Great Knot Calidris tenuirostris and Red Knot. Industrial pollutants have also been detected in several species found in intertidal wetlands. For example, lead and cadmium in concentrations that exceeded toxic levels were detected in Red-necked Stint Calidris ruficollis (Kim et al. 2009); butyltin residues were detected in three species of gull collected in the Nakdong Estuary (Guruge et al. 1997); and high concentrations of polychlorinated biphenyls (PCBs) were detected in Black-tailed Gull Larus crassirostris, attributed to effluents from two large industrial complexes in the Nakdong River Estuary (Choi et al. 2001). As reported by Schmutz (Birds Korea 2010a), PCB toxicity in eggs of Red- throated Loon Gavia stellata that breed in northern Alaska and winter in Asia were also two orders of magnitude higher than in eggs collected in areas where loons migrate within North America. This suggests that Red-throated Loon accumulate PCBs on their wintering areas. The magnitude of these PCBs is high enough to impact breeding success. Whether due to such toxicity or other causes, the Alaskan-breeding Red-throated Loon population declined 53% between 1997 and 2003 (Schmutz et al. 2009). Oil pollution, both chronic and from major oil spills, also causes mortality in seabirds, including loons and Black-tailed Gull. However, there is no agreed protocol or central database for recording such observations, and no distributional data with which to predict impacts of pollution on seabirds (Birds Korea 2010a)

1.5.4 Invasive Alien Species There is little information on the impacts of invasive alien species on the avian biodiversity of the ROK, beyond studies conducted on seabird colonies, mostly within the YSBR. Researchers have found that introduced Brown Rat Rattus norvegicus were responsible for 84% of recorded breeding failure (in 23 nests) in a Streaked Shearwater Calonectris leucomelas colony during one study (Lee & Yoo 2002). Some introduced plant species (especially Achyrahthes japonica) have been identified as causing loss of burrow access and also increased mortality in Swinhoe‘s Storm Petrel on Chilbal Island (Lee et al. 2009, Lee 2010).

1.5.5 Climate Change During the past 100 years there has been a 2-4°C temperature increase in eastern and north-eastern temperate Asia and a 1-2°C temperature decrease in the eastern half 39

of China except for the coastal area (Watson et al. 1997). There has also been an increase in the frequency of winter-time drastic short-term temperature decreases caused by winter monsoon cold surges manifested over northern China, entailing a drop in mean daily temperature of 10°C or more within one or two days (Gong & Ho 2003). As part of this changing trend, the ROK has become both wetter and warmer during the twentieth century, with an increase of 259mm in annual precipitation in Seoul over the past 97 years (Chung et al. 2004). The annual mean temperature has increased by 0.23°C per decade over the past 40-50 years. During the same period, especially since the 1980s, there has been an increase in the number of extreme maximum temperatures, and a decreasing frequency of extreme minimum temperature events. The increase in annual mean temperature was 1.5°C for Seoul and 0.6°C (closer to the global mean) for rural and coastal weather stations between 1975 and 2004. Winters especially are becoming milder. The January mean temperature increased by between 0.8-2.4°C at ten weather stations during this period, with this increase greater in industrial and urban than rural areas (Jung et al. 2002). According to Chae (2003), the annual mean temperature in the DPRK also increased by about 1.9°C in the twentieth century, with monthly mean temperatures in winter and spring increasing by 4.9°C and 2.4°C respectively. Apparently as a result of the warming climate, the northern distribution limit of many broadleaved evergreen tree species in the YSBR has moved north by 14-74 km since 1941 (Yu & Lee 2009). It therefore seems probable that bird species that depend on broadleaved evergreen forest (such as Black Woodpigeon Columba janthina and Japanese White-eye Zosterops japonica) or that breed regularly in such forest (e.g. Pale Thrush Turdus pallidus) will have been able to extend their breeding distribution northwards as a result. Analysis of data in NIBR (2010) suggests that out of 20 monitored widespread species in the ROK, two appear to be stable (one of which is Pale Thrush) and only three are increasing. All three, like Pale Thrush, are species of woodland and woody habitats. Two of these (Japanese Pygmy Woodpecker Dendrocopos kizuki and Brown-eared Bulbul Microscelis amaurotis) are near-endemic to Japan and the Korean Peninsula as breeding species, and in Japan are numerous in the warm temperate zone which supports broadleaved evergreen forest (Brazil 1991). As such these species can be predicted to benefit from reforestation efforts in the ROK and from a warming climate. Moreover, some species presently distributed largely to the southwest of the ROK (e.g. in eastern China) have recently expanded their range 40

northwards to start to colonise the Korean Peninsula. Such species, all of which were first recorded in the ROK during the present century, include Red-billed Starling Spodiopsar sericeus and Light-vented Bulbul Pycnonotus sinensis (which have both been confirmed as breeding species in the ROK) and Yellow-bellied Tit Periparus venustulus (Choi et al. 2011). Other species (especially insect-eaters) might also be able to over-winter more regularly. At the same time, the warming climate is likely contributing to declines in avian biodiversity in the ROK. Climate change is predicted to lead to further loss of intertidal wetland in the Yellow Sea due to rising sea-levels, and is also linked to reduced annual rainfall in the breeding ranges of some of the wintering waterbirds of the ROK (e.g. the globally Vulnerable Swan Goose Anser cygnoides: Gombobaatar et al. 2003). It is also possible that some species that are presently largely distributed to the north (e.g. Common Redpoll Carduelis flammea) might become less regular and numerous in the ROK. No research has yet compared historical assessments of a large number of species to determine whether there is evidence of changes in distribution of the majority of species, and whether a warming climate might be linked to these changes. For many migrant landbirds in particular there is also an increasing possibility of a mismatch between phenology and climate. In response to a warming regional climate, many species will need to migrate northward earlier to reach breeding areas earlier, as migrants that reach breeding areas late may fail to breed that year (Newton 2004). However, earlier northward migration requires landbird species to either go around or to cross the Yellow Sea earlier. Due to the time-lag between warming air and warming sea temperatures in spring, temperatures are substantially lower on YSBR islands through April and May than on the mainland. This results in suppressed vegetation growth and insect abundance on such islands. Research is required to identify migration timing on different islands within the YSBR, in order to establish a baseline understanding of species‘ migration phenology and to understand better the use of stopover sites at a range of ecological scales (Moore et al. 2005).

1.6 THE RESEARCH CHAPTERS There are two chapters focued on literature review and six chapters focused on field work. The first, Chapter 2, uses two ornithological reviews (Austin 1948, Gore & Won 1971) and two checklists (Won 2000, Moores & Park 2009) to identify for the first time suspected changes in abundance and distribution of all bird species in the 41

ROK during the past century. Bias is discussed, and a framework (a ―Decrease Susceptibility Index‖) is proposed for organising information that can be used to help identify species most susceptible to decline, in order to increase opportunities to influence conservation policy within the present decade. Chapters 3, 4 and 5 are focused on intertidal wetland. Chapter 3 provides an estimate of the remaining area of natural and near-natural intertidal wetland in the ROK, and explains the process of reclamation and the predicted impacts of reclamation on specialised bird species. Chapter 4 includes analysis of shorebird count data from three northward migration periods (2006-2008) within the Saemangeum Estuarine System and two adjacent intertidal wetlands, immediately prior to and following the closure of a seawall. The chapter documents for the first time the impacts of large-scale reclamation on shorebird numbers at an optimal shorebird staging site in the Yellow Sea and in the EAAF. Chapter 5 investigates changes in the numbers of shorebirds staging in other internationally-important intertidal wetlands in the ROK between 1988 and the present. In Chapter 6, the seasonal distribution of seabirds at sea in the Yellow Sea is assessed for the first time through counts conducted along two transects from high-speed commercial ferries and from land. The influence of geography and of weather on landbird migration across the YSBR is the focus of Chapters 7 and 8. Counts of landbirds on Socheong and Eocheong Islands are compared with published and unpublished count data to identify migration strategies and species of landbird suspected to be most in decline. In the absence of robust long-term monitoring of species and habitats it is difficult to identify declines in species and their causes. There is, however, an urgent need to develop an appropriate conservation response. Chapter 9 brings together the results from the previous chapters. It further develops the ―Decrease Susceptibility Index‖ and identifies key research and conservation priorities for meeting existing conservation obligations, including CBD‘s Target 19.

42

Chapter 2

BIAS IN THE KOREAN ORNITHOLOGICAL LITERATURE & THE IDENTIFICATION OF LONG-TERM BIRD POPULATION TRENDS BETWEEN 1910 AND THE PRESENT

ABSTRACT The United Nations-led Millennium Development Goal‘s Environmental Sustainability Target of reducing the rate of biodiversity loss and the Aichi Biodiversity Targets assume that biodiversity is already in decline, and demands a conservation response within the present decade. In the ROK since 1910 more bird species in general and more species of global conservation concern in particular are hypothesized to have shown a negative than a positive population trend due to the combined effects of five ―Principal Pressures‖ identified as driving biodiversity loss at the global level. In the absence of long-term robust monitoring programs, the present research tests both assumptions by comparing status assessments in the ornithological literature for 511 adequately documented bird species recorded in the ROK between 1910 and 2009. Based on the assessments of Austin (1948), Gore & Won (1971), Won (2000) and Moores & Park (2009), 365 out of a total of 511 species are assessed as regularly occurring in the ROK and 146 are assessed as less regular in occurrence. After mitigation for bias, conservative estimates were made that 128 regularly occurring species show evidence of a (substantial) negative trend and 98 evidence of a positive trend during the past 100 years. In total, 25 out of 50 species of global conservation concern show evidence of decline, three show weak evidence of increase, and the remainder show no clear trend. No clear trend was detected in 139 regularly occurring species and in the majority of less regular species. More of these 285 species with unclear or unknown trend in the ROK are also suspected of decreasing than increasing: several species assessed as stable by the present research have declined during the past decade (NIBR 2010), and an even larger number are assessed as decreasing in regional assessments by Wetlands International (2006) and BirdLife International (2011). To further test the validity of the results, a major ornithological review covering the DPRK (Tomek 1999, 2002) was also analysed. In total, after mitigation for bias, 43

evidence of a population trend in the DPRK was apparent in 112 of those regularly occurring bird species that are also regularly occurring in the ROK. Seventy-five of these showed a negative population trend in the DPRK. The results indicate that there has been long-term avian biodiversity loss and decline in the ROK including within the Yellow Sea Blueprint Region (YSBR) and in the DPRK. The results are consistent with hypothesised declines and the predicted negative impacts of the five Principal Pressures. Although causes of decline remain unproven in most cases, there is a need to organise the evidence of decline and on potential drivers of decline in ways that can influence conservation policy within the present decade.

2.1 BACKGROUND 2.1.1 Introduction and Aims The Millennium Development Goals Environmental Sustainability Targets (United Nations 2006) and the Aichi Biodiversity Targets (CBD 2010) assume that species and the ecosystems they are part of are in decline. Both demand an appropriate and timely conservation response, including improving, sharing and applying the knowledge-base on status and trends of biodiversity by 2020 (Target 19, CBD 2010). This requires achieving first, and within the near-future, an improved understanding of population trends and changes in distribution over time. As described in Chapter One, most declines at the global level are the result of one or more of what the CBD Secretariat (2010) described as the ―five principal pressures directly driving biodiversity loss (habitat change, overexploitation, pollution, invasive alien species and climate change)‖ (―Principal Pressures‖). Collectively these interrelated Principal Pressures can form a deadly anthropogenic cocktail (Travis 2003). This chapter aims to help identify CBD Target 19-relevant research and conservation priorities for the present decade by providing an overview of the perceived status of avian biodiversity and of long-term population trends during the past century. It compares assessments of abundance of all bird species recorded in the ROK and the YSBR between 1910 and 2009. In the absence of robust large-scale monitoring programs, preliminary identification of trends in regularly occurring species (defined below) is based on major ornithological reviews, checklists and more contemporary specialist literature, in addition to fieldwork. In order to use the ornithological literature in this way, it is first necessary to identify and then to mitigate 44

for bias. A framework is also presented which organises the information on species and assists in the identification of population trends and likely drivers of decline. Chapter Two tests two main assumptions that support the overarching hypothesis of the thesis. The first is that due to the combined effects of the Principal Pressures a larger number of regularly occurring species in general will have shown a decreasing than an increasing trend during the past century in the ROK. The second is that an even greater proportion of species with a poor global conservation status (as defined in Chapter One) will also have shown a decreasing than an increasing trend in the ROK during the same period.

2.1.2 Sources Used In the absence of hard data generated through robust, large-scale and long-term count programs, only shorter-term research projects and soft data from the ornithological literature are available for assessing national status and long-term population trends. Four assessments have therefore been selected as the main source of historical information. These are (1) the ornithological review by Austin (1948), which covered all of Korea apart from Jeju Island and Ulleung Island (latter in the East Sea, at 37°30' N 130°52' E), before the division of the Korean Peninsula into the ROK and the DPRK; (2) the ornithological review by Gore & Won (1971), which covered only the ROK, including Jeju and Ulleung; (3) the annotated species checklist of Won (2000), and (4) the annotated checklist of Moores & Park (2009). These assessments (from hereon the ―Four Assessments‖) have been selected as they provide details on the status and abundance in the ROK (expressed descriptively or through status codes) of all species recorded to that time; all are well-spaced in time and inclusive, providing records of species from the late nineteenth century, and especially from the 1910s to the present; and all are based both on a substantial review of published literature (including conscious knowledge of those of the Four Assessments that had already been published), as well as on the authors‘ own fieldwork. In order to refine understanding of species within the YSBR, further published and unpublished literature has been reviewed. This includes ornithological reviews by Park (2002) and Tomek (1999, 20002); annual bird reviews collated on behalf of the conservation organisation Birds Korea (Moores & Moores 2002-2005, Moores & Edelesten 2008, Edelesten & Moores 2008, and Birds Korea unpublished data); annual reports produced by the National Parks Migratory Bird Research Centre (NPMBC: KNP 2005- 45

2010) and by the Ministry of Environment (MOE 1999-2010); and also Birds Korea (2010a) and Kang et al. (2010). Throughout this and subsequent chapters, the nomenclature and taxonomy used follows Moores & Park (2009) (also see page 13).

2.1.3 Change in Number of Recorded Species A preliminary review of the Four Assessments reveals that a few species in the ROK that were formerly recorded regularly have not been recorded during recent decades. However, the total number of bird species that are now ―adequately documented‖ (i.e. which are supported by a specimen, photograph or sound recording) has increased at an accelerating pace. This is especially so in the past few decades (Table 2.1). Many of these newly-recorded species are probably regular in occurrence in the ROK even though they are described within the Four Assessments as ―Straggler‖, ―Vagrant‖, ―Wanderer‖, ―Accidental‖, ―Scarcely Recorded‖, ―Rarely Recorded‖ or equivalent. They are, however, referred to from hereon as ―less regular‖ in the ROK. The remainder are categorised as ―regularly occurring‖, as they appear to be, or to have been, widespread and predictable in occurrence. This division is used in the understanding that all species are incompletely recorded; that some species will likely have been misallocated; and that a species‘ status can change over time.

Table 2.1 Number of adequately documented species recorded in the ROK in the Four Assessments since 1910, divided into regularly occurring and less regular species. Name and Number of Number of Total year of Four regularly-occurring less regular number Assessments species species of species

Austin (1948) 286 45 331 Gore & Won (1971) 330 41 371 Won (2000) 345 72 417 Moores & Park (2009) 365 146 511 Note: Number of adequately documented species within present-day ROK since 1910 by each Assessment is based on the taxonomy used in Moores & Park (2009). Totals have also been modified to include or exclude species based on the literature review conducted for the present research.

Based on the taxonomy in Moores & Park (2009), 355 species had been recorded on the Korean Peninsula by 1946. Approximately 331 adequately documented species were recorded in the present-day ROK between 1910 and 1946, with 73 of these believed to breed (Austin 1948, though see Duckworth & Moores 2008). By 1971, probably 374 species had been adequately documented in the ROK alone, 371 of these since 1910, with 110 of these known to breed and ten more suspected of doing so (Gore & Won 1971). By 2009, 513 species had been recorded, 511 since 1910, with 46

153 known to have bred in recent years (Moores & Park 2009). Of this total, >400 species are now recorded annually (Moores & Edelsten 2008), and already 480 species have probably been recorded within the YSBR alone (Birds Korea 2010a). This long-term trend of increase in the number of adequately documented species and breeding species appears to contradict our prediction that more species will have shown a decreasing rather than an increasing trend since 1910. However, the Korean Peninsula received only superficial ornithological exploration until relatively recently (Duckworth 2006). Much of this increase in recorded species is due to increased ornithological activity, better access to offshore islands and open sea areas (especially within the YSBR), and an improvement in identification capacity during recent decades. All of these have led to a greatly-increased number of less regular species being recorded, and also to some species considered as vagrants or stragglers by Austin (1948) and Gore & Won (1971) to be reassessed as regularly occurring by Moores & Park (2009). Some of the increase in records of regularly occurring species and of newly-recorded breeding species is also due to a better understanding of bias. For example, Duckworth & Moores (2008) highlighted sources of bias in the work of Austin (1948). Several species considered to have colonised Korea in the 1950s (as they were rejected as breeding species by Austin) were in fact already breeding on the Korean Peninsula, some since at least the late nineteenth century.

2.1.4 Changes in Abundance and Policy Response Although the number of species recorded in the ROK has increased, the abundance of many is suspected of having decreased during the past century. In better-researched regions coordinated monitoring programs have been able to identify and measure declines in species and the data have then been used to inform policy. In Europe, a program covering 18 nations found regional declines in Barn Swallow of 24.5%, and in Eurasian Tree Sparrow of 82.1% between 1966 and 2002 (Vorisek et al. 2008). Proven and suspected declines in species then help to shape research priorities and to trigger policy responses, e.g. through the European Birds Directive (79/409/EEC) (BirdLife International 2004). In the spirit of the United Nation‘s Precautionary Principle (see Chapter 1, Section 1.1.2), this is even though initial results might sometimes be contradicted by later research. A steep decline in Barn Swallow in the United Kingdom was thus later rejected by Robinson et al. (2003), who identified bias in the survey methods. 47

In the ROK, any initial detection of declines at the national level is only likely if declines are substantial and if they take place either in widespread and familiar species or in species concentrated at only a few well-researched sites. Declines are likely to be especially difficult to detect if gradual, and/or if they occur in poorly-known species or seldom-visited habitats. In contrast, increases might be suggested by increased recording of previously seldom-seen species. Increased ornithological activity and improvements in identification capacity during recent decades will therefore have tended to cause bias towards perceived increase rather than decrease. Several examples suggest, however, that with due caution historical literature might be useful for detecting underlying population trends. Both Barn Swallow and Eurasian Tree Sparrow remain locally numerous in the ROK. However, in recent years there has been no 100,000-strong roost of the former species as reported by Gore & Won (1971), and the description of the latter as ―easily the commonest bird in Korea‖ in Austin (1948) is also no longer appropriate. Although Eurasian Tree Sparrow was the commonest small landbird recorded by the Ministry of Environment midwinter bird census (―MOE Census‖) in 2010 it still ranked only 20th in abundance when all bird species were included (MOE 2010). The MOE Census is conducted largely in habitats not dissimilar to those most-visited by Austin in 1945 and 1946, so some decline in the Eurasian Tree Sparrow is suggested, at least compared with other species. Analysis of data in NIBR (2010) by the author also suggests declines in both species, perhaps more rapid than measured in the same species in Europe since the 1960s. In 406 randomly-selected quadrats there was a decline of 80% in Eurasian Tree Sparrow since 1988, and of 27% in Barn Swallow since 2000. The same analysis further suggests that substantially more species that are widespread in the ROK have declined during the 2000s (15 out of 20) than are stable (two) or are increasing (three). For some species, historical literature provides clearer statements on population trends and also opinion on the causes. The now globally Endangered Crested Ibis Nipponia nippon was formerly a common visitor to the west coast of the ROK. By the time of Gore & Won (1971: 121) it had already become a ―very rare passage migrant and winter visitor‖. Its decline was attributed to its susceptibility to hunting, as it had earlier been described as ―stupid and unsuspicious, falling easy prey to the gun‖. The White-bellied Woodpecker, a species probably never recorded within the YSBR, was earlier ―collected so immoderately…that it decreased very much‖, before facing ―extinction with the needless and ruthless wasting of the little tree cover still remaining 48

in that over-populated land‖ (Austin 1948). That there are no published records in the ROK for more than two decades of either species despite the great increase in ornithological activity supports the declining trend earlier identified by these authors. These four examples suggest that historical literature can in some cases be used to help increase confidence in the identification of long-term trends from short-term or local research projects, and vice versa. In some species trends are instead concealed by biases within the historical literature. Great Knot was considered by Austin (1948) to be a rare transient in the ROK. Its true status as probably the nation‘s most numerous shorebird was only discovered in the late 1990s (Yi 2003) because of increased access to the coastal zone and increased survey effort (Moores 2006). A recent rapid decline in the species has been proven (see Chapters 4 & 5). The decline has been attributed primarily to habitat loss caused by the ongoing reclamation of intertidal wetland in the ROK (Chapters 3- 5). As a result, the Great Knot has now been assessed as globally Vulnerable (BirdLife International 2011). However, this has not yet triggered a national policy response. Instead, earlier statements that large-scale reclamation at Saemangeum ―invites more migratory birds to the area‖ (national Ministry of Agriculture, Forestry and Fisheries in Birds Korea 2003) have been followed by recent promotion of the proposed ―habitats for migratory birds‖ (Kim 2010a) that will be created by the same reclamation project.

2.2 LITERATURE AND BIAS

To improve confidence in the Four Assessments, it is first necessary to examine their historical context and some of their major biases. An introduction to each of the Four Assessments is therefore provided below. These are followed by an overview of the MOE Census, included because of its potential importance to the understanding of contemporary mid-winter bird abundance and distribution.

2.2.1 Austin (1948) O. L. Austin Jr. (―Austin‖) took his doctorate in ornithology at Harvard University, co-founded an ornithological research station with his father in the USA in 1929 (New York Times 1989), and wrote the first English-language ornithological review of Korea (Austin 1948). This review covered all of the Korean Peninsula ―and its contiguous minor islands southward from the Manchurian border‖. It thus excluded Ulleung and Jeju Islands (p.3), the latter island on which Momiyama (1927) had 49

already recorded Slaty-backed Gull Larus schistisagus and Far Eastern Cisticola Cisticola jundicis brunniceps. A well-respected ornithologist, Austin‘s work was ―unashamedly incorporated‖ into the subsequent review of the birds of the ROK by Gore & Won (1971) and was used as the main source of pre-1950 material by Park (2002), who otherwise referenced only four other pre-1950 papers. However, despite the value and great influence of Austin‘s work, a subsequent review by Duckworth & Moores (2008) identified several major sources of bias within it. These included excessive interpolation of Korean status from very limited field experience, imperfect review of material (which itself was limited in scope), and cultural bias. Austin (1948: 3) asserted that his review was based on his ―own collecting and field experiences there between November, 1945 and May, 1946, on a review of all the literature available, and on specimens and other data, much of it unpublished, in museums and private collections in Korea, Japan and the United States‖. While Austin was in Korea between November and May, his species accounts suggest he was able to conduct fieldwork for an even shorter time as he first visited Suwon Lake (close to his place of work) only on December 7th (p.30), and left Suwon for Japan on May 3rd (p.26). Austin was also in Korea and then in Japan (where he finished writing his text) during an especially tumultuous period, both for the region and for himself personally. Japan had declared Korea a protectorate in 1906, and formally annexed the whole peninsula in 1910. With Japan‘s surrender in 1945, Russia took control of Korea‘s northern provinces and the USA military took control of the southern provinces, requiring massive restructuring of social and political structures (Booth 2007). Austin arrived in Korea as part of a newly-formed USA Military Government, after a sudden reassignment requiring him to learn ―about Koreans, and about Korean culture, customs and geography, ‗the hard way‘‖ (p.24). He had little time to acquaint himself with Korea before his arrival. His main work once in-country entailed sharing ―various assorted responsibilities and headaches‖ in the rehabilitation of the Korean agricultural Experiment Station in Suwon. What time he could dedicate to research on birds was therefore conducted between other essential duties. His departure to Japan in May 1947 was as sudden and unexpected as his arrival (p.25). Once in Korea, there is no evidence within Austin‘s work that he travelled widely or had the possibility of being able to do so, beyond almost fortnightly visits to Incheon (p.67), less than 60km to the northwest. The northern provinces of Korea, less than 100km to the north of Suwon, were already under Russian influence. Other 50

western ornithologists writing of their experiences soon after, in 1947 and 1948, describe ―bad roads‖ (Wolfe 1950), and a ban on using ―all types of Korean transportation‖ while ―Army vehicles were extremely difficult to procure for other than strictly official purposes‖ (Fennell 1952). Austin‘s fieldwork was therefore largely confined to the area around Suwon. This was ―one of the poorest collecting grounds in Korea, miserably over-populated and with but scant cover‖ (p.25), though it included ―coastal marshes and extensive cultivated paddies in the lowlands‖, ―occasional patches of woodland on the hillsides‖, and ―barren rocky mountain tops‖. Despite the limitations of time and location, Austin still managed to record one apparently new species for Korea (Little Egret Egretta garzetta), perhaps an indication of the incompleteness of the ornithological record at that time. While his accounts demonstrate a high-level of self-confidence they also contain numerous errors and a different standard applied to his own records than to those of others. His opinions were expressed with an authority that has likely influenced many of the ornithologists that have followed after him. For example, without providing any description of structural or plumage differences, Austin confidently identified cormorants he saw on the freshwater Suwon Lake between April 6th and 15th as Temminck‘s Cormorant Phalacrocorax capillatus. This was despite knowing that Temminck‘s and Great Cormorants Phalacrocorax carbo are ―easily confused‖, and that the specimen record indicated that Temminck‘s Cormorant was a coastal species, believed to nest in seabird colonies (p.35). Indeed, Temminck‘s Cormorant is much more typical of marine inshore waters and rocky coasts than Great Cormorant (Lethaby & Moores 1999), and there appear to be no confirmed ROK records, at least in recent years, of the former species in freshwater habitat (Birds Korea unpublished data). Moreover, Great Cormorant are now known to breed not far from Suwon (pers. obs.), and the dates of Austin‘s observation are a better match for Great Cormorant, as most depart their main wintering area in the southern ROK between mid-March and mid- April (WBK 2005). The timing of their main migration period therefore coincides with the timing of Austin‘s observations. Although there are few data, migration of Temminck‘s Cormorant apparently takes place at sea, and many return to nesting colonies in March (Chapter 6, Table 6.5). Confident in his identification of the Suwon birds, however, Austin even felt able then to describe the Great Cormorant as being of ―uncertain status‖ in Korea. He thus dismissed the description by Won Hong Koo (Korea‘s pre-eminent ornithologist) of it as ―common‖ (p.35), a description that fits 51

well with accounts in Tomek (1999) when describing its earlier status in the DPRK and adjacent regions. Austin‘s account of Baikal Teal Anas formosa (a species he considered to be ―common‖) is also instructive. In it Austin wrote, ―I watched one line go over on 14 March that I hesitated to estimate‖. His hesitation did not prevent him, however, from continuing that the flock ―was at least two miles in length and must have contained well over ten thousand birds‖ (p.61). Based on contemporary counts and flock behaviour of Baikal Teal, it is probable that Austin massively underestimated this flock‘s size. Flocks of approximately similar length observed between 1999 and 2009 have contained from between 174,000 and c. 600,000 individuals (Moores 2005, unpublished data). Based on this understanding, it appears likely that numbers of Baikal Teal in the ROK in the time of Austin were not so dissimilar to the numbers present in the 2000s. The species, after declining catastrophically to reach its lowest population level in the 1980s (resulting in its assessment as globally Vulnerable), has apparently now recovered, in the ROK at least, to its pre-Korean War level of abundance. It has apparently benefited in recent decades from the creation of large reclamation lakes (Moores 2005). Considering that there is no evidence that the Baikal Teal presently over-wintering in the ROK move regularly to Japan, the large concentrations of the species that Austin saw near Suwon suggests that it was not hunting in Japan in the late 1940s that led to the species‘ massive decline as has sometimes been suggested, directly or otherwise. Rather, the main decline in the Baikal Teal instead apparently took place after Austin‘s time – perhaps like the Common Pheasant that Wolfe (1950) described as declining rapidly as a result of mass hunting in Korea following Korea‘s liberation from Japan. Based on present understanding of ROK species‘ distribution and phenology too, and borne out by the species accounts, Austin was also not able to make direct observations on most species of intertidal wetland or on species found at sea; nor was he able to observe a substantial part of the northward migration period, most of the breeding season, or the southward migration of almost any species. The assertions in many of his species accounts on Korea-wide distribution and status were therefore based only on limited field experience, personal interpretation of the specimen record, and the limited literature available to him. While Austin‘s review of the literature and specimen record was remarkable (particularly considering the many constraints that he experienced) it was still 52

incomplete, as too was the ornithological coverage of much of the Korean Peninsula up to that time. In his ‗Historical Sketch‘ (pp.6-27), he remarked that most of Korea remained ―terra incognita to occidental naturalists‖ until the 1880s, and even the next couple of decades hosted few surveys. The formal Japanese annexation of Korea in 1910 brought Japanese ornithologists to the country, though many of the specimens they collected were lost or damaged by earthquakes and war, including those of Mori and Momiyama (pp.16-17; p.52), so were unavailable to him. Austin also did not meet Won Hong Koo, who had started collecting in 1920 and written successive Korean checklists, or even see his collection. Few ornithologists from outside Korea or Japan had been active in Korea, though these too include some that Austin cites (e.g. Cumming 1933); others that he knew incompletely (Bergman 1935a, 1935b, 1938); and others he apparently did not know of at all (including Yankovskii in Tomek 1999, 2002). Even his review of Korean specimens collected by others pre-1910 from the USA was not complete. As he himself stated (pp.10–11), he covered only part of the large late-spring Hall collection from 1903. Austin‘s lack of experience in Korea and the many information gaps that must have been apparent to him did not, however, prevent him from making numerous strong assertions on status. Remarkably, he rejected many of Won Hong Koo‘s status assessments and records. These included easily-identifiable species in appropriate habitat (two of the more notable being Gadwall Anas strepera [p.64] and breeding Fork-tailed Swift Apus pacificus [p.153]), as well as more challenging species like Great Cormorant detailed above. Indeed, throughout the species‘ accounts Austin was often dismissive of Japanese and especially Korean sources. He ―found the Korean scientists not only lacking in knowledge and ability, but regrettably ignorant of any conception of the meaning of truth. To the oriental mind truth is the convenient thing, the polite thing, the honorable thing, not the accurate fact… that is the only explanation of the, shall we say, inconsistencies, in Won (Hong Koo)‘s writings‖ (p.23). This cultural prejudice encouraged Austin to reject, often mistakenly, many assertions on status in the literature that he was able to access. Duckworth & Moores (2008) calculated that Austin underestimated the species richness of the Korean breeding avifauna by at least 30–50%. The result is that subsequent confirmation of breeding has led to the false impression that many such species have colonised Korea since Austin‘s time. 53

Austin completed his research and writing in April 1947 while stationed in Japan – less than 18 months after he had first arrived in Korea. While some recent ornithological literature has apparently overlooked many of the flaws and biases inherent in the work, some of his contemporaries recognized both its importance and its limitations. Wolfe (1950) for example introduced his own paper on Korean birds by stating that ―The presently known ornithology of Korea has been admirably summed up in Dr. Austin's recent publication … which shows many gaps still remain in our knowledge of the bird life of this area.‖

2.2.2 Gore & Won (1971) Won Pyong-Oh, the son of the DPRK‘s pre-eminent ornithologist Won Hong-Koo, was born in 1929. He studied agriculture in Wonsan (within present-day DPRK) and moved to the southern provinces in 1950. After the devastating Korean War (1950- 1953), he started to publish on birds (and other biota), completing an ―Avifauna of Korea‖ in 1961, which was published by the Institute for Agriculture in Suwon. During the 1960s, Won Pyong-Oh then ―added many new species to the Korean list…produced new breeding records…(undertook) several research projects, including a major ringing scheme, and published a number of papers on the birds of Korea‖ (p.63). He also collaborated with M. E. J. Gore (―Gore‖), a self-described ―amateur ornithologist from his schooldays‖ and Consul at the British Embassy in Seoul from 1967. Both travelled ―extensively‖ throughout the ROK (p.65), with Gore even gaining access to parts of the Demilitarized Zone to survey cranes (Gore in lit. 2008). After publishing a national checklist together (Won et al. 1968), they wrote ―The Birds of Korea‖ (Gore & Won 1971): a detailed and well-illustrated review. Its aim was to provide a ―permanent record of the known status in Korea of each species at the time of publication‖, covering all ―366 species of birds (that) occur or have occurred in the Republic of Korea‖. In this review, Gore & Won (1971) made three major departures from Austin (1948). The first was in the geographical scope. Austin (1948) covered the whole of the Korean Peninsula, excluding Jeju and Ulleung Islands. Gore & Won (1971) instead covered only the ROK, so they included species recorded from the offshore Jeju and Ulleung Islands, but they excluded those species that they believed had only been recorded in the DPRK. However, as the boundary between the ROK and the DPRK cuts across the central two provinces of Gyeonggi and Gangwon, and because some of 54

Austin‘s specimen locations are given only at the province level, it is possible that some species were either excluded or included incorrectly, and that some status descriptions, if based on Austin, might also have been misapplied. Second, they did not provide full details of many of the species records. Ruddy-breasted Crake Porzana fusca, for example, which was considered by Austin (1948: 103) as a ―straggler‖ with only two records, was simply reassessed as a ―Summer visitor in small numbers throughout the lowlands‖ (Gore & Won 1971: 191). Coupled with the lack of indication of survey effort within suitable habitat for the species, this lack of detail is unhelpful in assessing whether the species had previously been overlooked; whether it had expanded its range and abundance in the ROK; or whether it was so assessed based on extrapolation of a very few records. Third, while the emphasis remained on documenting new species through collection (e.g. Two-barred Crossbill Loxia leucoptera: Won 1970) the species listed by Gore & Won (1971) do include at least one sight-only record (Sabine‘s Gull Xemus sabini seen at Pohang in 1970 [p.249]). Austin (1948) required a specimen for confirmation and documentation. In the introductory section (pp.21-65) Gore & Won (1971) provided valuable background information on the development of their book (which included further review of specimens held in collections in the USA, Europe and Japan, including by Austin), and background information including sections on ―Habitats and Bird Population‖, ―Migration Through Korea‖, ―The Problem of Conservation‖ and ―The History of Ornithology‖. These introductory sections revealed the greatly improved understanding of the avifauna of the southern provinces when compared to the period reviewed by Austin (1948), with ―much new information…obtained in recent years.‖ Gore & Won (1971) introduced eight main habitat types (including ―rocky cliffs‖, ―offshore‖ water and ―offshore islands and islets‖). However, the species accounts themselves suggest that many such habitats were at that time still seldom visited. In common with Austin, most of their observations appear instead to have been made in and around towns (especially near temples and tombs where woodland remained), in agricultural areas and along streams and rivers. Moreover, the weight of observations appears to have been made in and close to Seoul where both lived and worked, as suggested by the accounts on Brown Shrike Lanius cristatus (p.389) and Black-naped Oriole (p.303) which state that both species occur ―in gardens even in the centre of Seoul‖, and on Long-tailed Rosefinch Uragus sibiricus, with abundance measured by years with ―flocks…present in the Seoul area‖ (p.389). 55

This geographical bias would likely have been unsurprising to the small number of Korean ornithologists at the time. In 1967, there were fewer than 100,000 cars in the country and by 1969 only 6% of the nation‘s roads had been paved (Lankov 2010). Travel from Seoul to other cities, to the mountains or to the coast was time-consuming, and strict military access restrictions were in place in many areas, both close to the DMZ and also along much of the nation‘s coastline. Largely as a result, perhaps, many of the status assessments appear to have been inferred from very limited data rather than based on more complete datasets. For example, a reading of Gore & Won (1971) suggests that most seaducks, loons, saltwater grebes and gulls – species groups more or less ecologically dependent on inshore waters in winter (see Chapter 6) - were, like the Common Gull Larus canus ―most numerous on the south coast‖. This is in contrast to a more contemporary assessment of their present distribution. Between 1999 and 2010 the same species were both more widespread and more numerous along the east coast (e.g. MOE 1999- 2010; unpublished data). While it is possible that there has been a major northward shift in distribution of many species during the past four decades, these species‘ status along the east and south coasts (and their perceived rarity along the west coast) in Gore & Won (1971) appears to be based largely on very limited coverage. That is, presence of these species was assessed mostly on Austin (1948), Fennell (1952), Fennell & King (1963a,b), subsequent visits in March and August to Pohang on the East coast by Gore, and several visits by both authors between December and April to the southeast between Geoje (―Koje‖), Jinhae (―Chinhae‖) and the Nakdong Estuary. Absence, on the other hand, appears largely to have been inferred rather than proven, and unsupported by fieldwork. While the authors made explicit their limited knowledge of the avifauna of Jeju and Ulleung Islands (based largely on single visits) the lack of coverage along most of the coastline on the mainland is left unwritten. Such inference and extrapolation from a few records or local occurrence to a national assessment is, perhaps unsurprisingly, also suggested in the accounts of several other species and habitat types. There is little detail on birds in high mountainous areas, and most of the status assessments of intertidal shorebirds appear to be based largely on Austin (1948), limited survey work especially near Seoul and Incheon in Fennell & King (1964), and still-limited survey work at the Nakdong Estuary near Busan, especially by Won Pyong-Oh (only in September 1970?). The description of Sanderling Calidris alba as ―particularly common on the sandy beaches along the east coast on migration in 56

August-September‖ (p.233) also coincides again with several observations made by Gore at Pohang (on the east coast) in late August/early September 1969 and again in 1970, but apparently in no other autumn or winter month. With this apparent unevenness of coverage, especially intriguing is the observation that ―millions of buntings occur in the millet fields on autumn migration‖ (p.35). The text accounts unfortunately leave unclear how this statement was arrived at. Was it based entirely on the banding of almost 65,000 Chestnut Bunting Emberia rutila (between 1964 and 1969) and almost 60,000 Rustic Bunting Emberiza rustica (between 1964 and 1968) (Gore & Won 1971), in a ―small area‖ of fields near Seoul (Won Pyong-Oh pers. com. 1999), extrapolated out to a national estimate? Or was the assessment instead based on an apparent abundance of buntings in all suitable habitat nationwide during southward migration? Either way, it appears very unlikely that millions of buntings are presently supported by agricultural areas on the mainland during autumn migration. Rather, both the number of millet fields and the number of buntings appear to be much reduced.

2.2.3 Won (2000) Both as a professor and as the Director of the Institute of Ornithology at Kyung- Hee University in Seoul, Won Pyong-Oh (―Won‖) maintained his status as the pre- eminent ornithologist in the ROK through to the end of the twentieth century. Building on earlier research, Won organised greatly-expanded survey effort of the west coast‘s intertidal wetlands (Long et al. 1988) and in inland wetlands (Kim et al. 1996); he taught several doctoral students, many of whom added new species to the national list and helped to close major information gaps on distribution and abundance (including Park Jin-Young: Park 2002); and he published further papers and several checklists (including Won 1993, 1996). Won‘s 2000 Checklist is based on this greatly-expanded ornithological effort by himself and by the growing number of active ornithologists, many of whom had been his students. The introduction to Won (2000) stated that it includes ―every species recorded in Korea and comprises 13 orders, 55 families and 444 species‖ (all but about 10 of which had been recorded in the ROK), and also all subspecies which can be ―separated in the field‖. All taxa were then annotated with abbreviated status notes that cover their relative abundance, seasonal presence, and some geographical weighting (i.e. selected species are marked to indicate that records were confined to the DPRK, or in 57

the north, south, east, west or central areas of Korea). However, despite containing several additions and improvements compared with earlier checklists, Won (2000) also contained several errors in nomenclature; included, without indication, approximately eight species for which there appears to be no specimen, photograph or sound recording; included possibly as many as five species supported by a specimen or photograph in which the identification (by others) seems questionable; omitted at least two species listed for the DPRK by Tomek (1999); omitted many identifiable subspecies; and provided numerous status conclusions contradicted by other research. Some errors, like the listing of the unrecorded Western Crowned Warbler Phylloscopus occipitalis and North American Pine Siskin Carduelis pinus in error for the regularly occurring Eastern Crowned Warbler Phylloscopus coronatus and Eurasian Siskin Carduelis spinus are obvious to detect, and in some cases are possible to attribute to a slow response to changes in taxonomic treatment. Others are rather more difficult to determine. For example, Won (2000) listed American Black Duck Anas rubripes and several other North American species of Anatidae, including Canvasback Aythya valisineria, Redhead Aythya americana and Barrow‘s Goldeneye Bucephala islandica. Amongst these four species, only the record of American Black Duck is supported by anything other than a sight record. According to the account of this record (which was published as a short note eight years after the event), two USA servicemen found a dead duck inland in Gwangju in a rice-field, near to their airbase in mid-June 1977. They noticed that the bird had a USA Fish and Wildlife Service band on it, so they sent in the band (but not the bird). The Fish and Wildlife Service then identified the band as one put on an American Black Duck seven years earlier in Virginia (Banks 1985). In the absence of any accepted records committee, this was accepted by Won as the first national record for the ROK (and Asia), though he apparently believed that the bird was recorded in Gunsan not Gwangju (Won 2003 fide Park 2002). While not impossible, this record still seems highly implausible for a number of reasons, including: 1. The extremely fortuitous circumstances of the discovery of the band (and the absence of images or other evidence of the bird in situ); 2. The peculiar mid-summer date, as most duck species (including the closely- related Mallard Anas platyrhynchos) have largely departed the ROK as early as April and the American Black Duck in its natural range tends to be one of the 58

earlier migrating ducks in spring (Chaulk & Turner 2007), breeding typically far to the north in the boreal forest zone (Jarrett 2005); 3. The improbability of its vagrancy to the Korean Peninsula. The species largely

breeds east of Longitude 85° W (Jarrett 2005), is considered a rare vagrant even in Alaska (Banks 1985), and there are no properly documented records of the species anywhere else in Asia, including in Japan where several North American duck species are well-documented (Brazil 2009). The inclusion of this species by Won (2000), however, and its inclusion in field-guides (including Lee et al. 2000) has apparently encouraged further undocumented claims of American Black Duck in the ROK. These claims have been made so frequently that that the species could be assessed in error as regularly occurring. No less than 80 American Black Duck were ―recorded‖ during the MOE Census in 2008 and published without comment (MOE 2008). Moreover, the apparent presence of (so many) American Black Duck has made the occurrence of other North American duck species appear more plausible. Park (2002) provided details of several records of Canvasback, with a peak count of 14 on January 10th 1994, and the species has also often been reported during the MOE Census (with one in 1999, one in 2002 and 36 in 2003: MOE 1999-2004). However, none of these records, or those of the much more rarely- claimed Redhead or Barrow‘s Goldeneye, had by the end of 2011 been supported by a photograph, despite the rapid growth in digital bird photography. While most species unsupported by the specimen or photographic record were classified by Won (2000) as vagrant, the White-breasted Woodswallow Artamus leucoryhchus was listed enigmatically as a local and scarce summer visitor to Jeju Island. This species is considered to be essentially resident in the Philippines, the Malay Peninsula, Borneo, Indonesia and Australia (Brazil 2009), and had only been proven to wander once as far north as Iriomote in Japan (Brazil 1991), more than 1000km to the south. Again, the absence of adequate documentation for such an out- of-range species that is typically quite visible and should be easy to photograph (pers. obs.) undermines confidence in the veracity both of the species‘ occurrence in the ROK and of the checklist itself. Yet Park (2002) was able to find a further 2001 record from Jeju of the species, and Kang et al. (2010) included an unsupported sight record of six together on Jeju in 2002. Also troubling are numerous misleading status assessments on regularly occurring species that have likely confused understanding. Two examples are included here. Far 59

Eastern Cisticola was listed by Won (2000) as an uncommon resident on Jeju, implying a highly restricted distribution. However, the species is much more widespread. It was first recorded as far north as Gyeonggi Province, to the north of Seoul, as early as October 1954 (Macfarlane 1963). By the late 1990s, the species was known to be widespread along both the west and south coasts, at least in summer (unpublished data; Park 2002). The Willow Tit Poecile montanus was assessed by Won (2000) as an uncommon resident, although there were only two documented records for the ROK by 2001 (Park 2002), and there have been no subsequent adequately documented records. As a result, Tomek (2002) was misled when she stated that the Willow Tit ―On the Korean Peninsula till the seventies… was known only as breeding in the north…Today it occurs also in the southern part of the peninsula because Won Pyong-Oh (1996, 2000) includes the Willow Tit as an uncommon resident on the entire Korean peninsula‖ (Tomek 2002: 113).

2.2.4 Moores & Park (2009) N. Moores (the present author, ―Moores‖ in all text and references) moved from the UK to Japan in 1990 and after annual visits moved to the ROK in 1998, initially to conduct a year-long survey of the ROK‘s coastal wetlands and waterbirds (Moores 1999a, Moores 1999b). From 2000, Moores started research on migrants on offshore islands (Moores & Kim 2001) and increased opportunistic counting of seabirds at sea from commercial ferries. On behalf of bird conservation organisations, he then produced annual reviews (first in 2002). These built upon Won (2000) and Park (2002) by organising contemporary records of ornithological significance, including both his own records and those of others that had been submitted to the organisations, posted on websites or contained in published reports. The number of records and observers cited in these annual reviews (Moores & Moores 2002-2005, Moores & Edelsten 2008; Edelsten & Moores 2008) increased from over 260 notable records (including nine national first records, and multiple presumed new maxima and over-wintering records) made by 38 observers in 2002, to records in 2007 of over 160 species ―of especial note‖ made by over 140 observers. In 2007, records included six fully-documented national first records, one ―new‖ species added by specimen review, one inadequately documented new species, and at least three species found breeding in the ROK for the first time (Edelsten & Moores 2008). 60

In 2009, Moores collaborated with Park Jong-Gil to revise Birds Korea (2007), an existing online checklist developed by the conservation organisation Birds Korea. During the late 1990s and 2000s, Park Jong-Gil conducted research for the Korea National Parks service. This included ornithological survey in the Sorak Mountain National Park (Park & Chai 2001); review of collections in museums; contribution to the establishment of the nation‘s first Migratory Bird Research centre on Hong and Heuksan Islands (KNP 2003); regular bird monitoring on offshore islands and discovery of several national first records (KNP 2005, 2006, 2007); and the development of a national checklist for use by the Korea National Parks (in KNP 2006). Moores & Park (2009), like Birds Korea (2007), was sub-divided into four main categories: (1) species with records that were adequately documented by specimen, photograph or sound-recording since 1980; (2) species that were adequately documented before 1980, but not subsequently (mostly based on the literature, rather than on the specimens themselves); (3) species that lack full documentation (i.e. sight records only and records that were documented but whose identification now seems questionable, e.g. Wilson‘s Phalarope Phalaropus tricolor); and (4) established non- native species. With three exceptions introduced below, it followed the scientific nomenclature and order of Gill & Wright (2006, and subsequent revisions), which is a global species-level checklist that does not include subspecies. English names also followed Gill & Wright (2006), though like Birds Korea (2007) alternative names for some species were also provided. Based on this taxonomic and category arrangement Moores & Park (2009) recognised 521 species and an additional 68 subspecies as adequately documented and naturally occurring on the Korean Peninsula, contained with 79 families and 22 orders. Among these, 513 species were adequately documented in the ROK, two of these only before 1910. A further 25 species were considered to be inadequately documented (with several more listed in a pending file), and there was one additional established non-native species (feral Rock Dove Columba livia). This total of 549 listed species included three adequately documented species not recognised by Gill & Wright (2009): Mongolian Gull Larus mongolicus, Korean Bush Warbler Cettia (canturians) borealis (as distinct from Japanese Bush Warbler Cettia diphone), and Far Eastern Skylark Alauda japonica (as distinct from Eurasian Skylark Alauda arvensis). Reason for the inclusion of Mongolian Gull is covered in Section 2.3.2. Recognition of borealis as specifically distinct from C. diphone was based on differences in songs, habitat, 61

morphology and migration strategies (unpublished data), supported by detailed comparative research (Park 2009) and later followed by the specialist review of Kennerley & Pearson (2010). The separation of the two skylark species is in accordance with BirdLife International (2011), and appears to be supported by genetic analysis (Kerr et al. 2009). In Moores & Park (2009) separation was based largely on: characters outlined by Moores (2003b); on the inclusion of both subspecies intermedia and quelpartae (if not synonyms) in Far Eastern Skylark rather than in Eurasian Skylark; and on sympatric (or near-sympatric) breeding by intermedia and lonnbergi, as noted by the present author in 1998 and 1999 (unpublished data), and earlier by others. Yamashina (1932) stated that quelpartae was identical to birds in Japan and that intermedia was the only skylark sensu lato breeding on the Korean mainland. However, sympatric breeding of different skylark taxa reported by other authors was known to Austin, who wrote in exasperation that ―some even claim two distinct subspecies breeding in the same area!‖ (Austin 1948: 171). Additional information for Moores & Park (2009) from the DPRK, after Won (2000), came through recent survey effort, including counts of shorebirds and other waterbirds (A. Jensen in lit. 2005, Riegen et al. 2009); a very few recreational birdwatching reports (including J. Hammar 2005); and several important publications. Publications included the 217-page second volume review of the DPRK‘s avifauna by Tomek published in 2002 (covering Passeriformes), and papers by Duckworth (2004, 2006). For the ROK a combination of improvements included (but were not limited to) a still-growing number of recreational and professional ornithologists; the annual MOE winter bird Census (MOE 1999-2009); shorebird counts (Yi 2003, 2004; Moores 2006; Moores et al. 2008); greatly improved travel infrastructure and access to especially coastal areas and offshore islands; further museum research (as contained within Park 2002); new field-guides (including Lee et al. 2000, Park & Seo 2008 and Brazil 2009); improved identification criteria for numerous difficult species and species groups, including gulls (Laridae), leaf warblers (Phylloscopidae) and reed warblers (Acrocephalidae), shrikes (Laniidae) and larks (Alaudidae); and some improvement in information-sharing. The 2009 Checklist was therefore also able to include assessments of relative abundance and geographical weighting (similar to the system used by Won 2000), and an indication of whether breeding had been confirmed or suspected. As an online and bilingual (Korean and English) checklist, Moores & Park (2009) was open to public review and comment, and also benefited from being 62

hosted by bilingual websites that enabled discussion both on listed species and on pending records. While Moores & Park (2009) did contain many improvements on previous checklists, it was also, like Birds Korea (2007) and other contemporary checklists, weakened by remaining information gaps (including on some historical records; on the relative abundance of even widespread species; and on the presence or absence of some suspected breeding species); by its lack of authority (in that it was but one of several different checklists used by different organisations); and because there was no formal system in place to assess records and to share data – either between the ROK and the DPRK, or even within the ROK itself. With an increasing number of birdwatchers making observations each year there has been an increasing but unknown number of records lost to the ornithological record. Furthermore, while general identification levels are improving, numerous misidentifications still remain largely unchallenged, as with the Black Duck records discussed above. While Black Duck was omitted from Moores & Park (2009) it was included in other checklists and the regional field-guide by Brazil (2009) (though latter with caveats). Greater documentation and scrutiny of records is required in order to improve understanding of population trends and in some cases even species‘ presence or absence.

2.2.5 The MOE Census (1999-2010) Since 1999 the MOE has coordinated an annual winter bird census with a more or less standard methodology, covering more or less fixed sites. The initial focus of the MOE Census was on waterbirds. Although the range of habitats covered has increased all count sites still contain some wetland habitat or inshore waters. Between 1999 and 2010, the number of count sites covered by the MOE Census (typically conducted over a single weekend in January or February) increased from 56-69 (dependent upon delineation) to 172; the number of observers increased from less than 100 to 173; and the number of species recorded per MOE Census increased from about 175 to 204. The results of the MOE Census are published annually (MOE 1999-2010), and MOE Census records are also incorporated into the Asian Waterbird Census. As such they are the only multi-species ROK bird data used regularly (as opposed to on ad hoc basis) by any international bird monitoring program. The MOE Census therefore provides the most accessible and high-profile data with which to determine national patterns of seasonal distribution, including increased tendency of overwintering and 63

population trends of selected species over the past decade. The MOE Census data were therefore used (with caveats) to assess abundance of some Anatidae and other wintering birds by Moores & Park (2009). Despite their high-profile status, the MOE Census reports annually contain numerous misidentifications that have been published without comment. While a full analysis of these (and of other biases and problems with methodology) is beyond the scope of this chapter, probably at least 14 species listed by MOE (1999) were apparently in error. These included claims of single Jankowski‘s Bunting Emberiza jankowskii (never adequately recorded in the ROK, and no records in the DPRK since either 1929 or ―at best‖ sometime before 1980: Tomek 2002) and single Chinese Hill Warbler Rhopophilus pekinensis (also not reliably documented in the ROK since 1962: Fennell & King 1963, Park 2002). As recently as 2009, probably at least six species were implausibly reported by the MOE Census, including Blyth‘s Pipit Anthus godlewski (35) and Tiger Shrike Lanius tigrinus (two). While both species are regular in the ROK on migration and Tiger Shrike is a localised breeding species, there are no adequately documented records of either in the mid-winter period. Several other species that might be present in small numbers are also very probably over-counted. While one or two Richard‘s Pipits Anthus richardi have been recorded in mid-winter on Jeju in recent years (pers. obs.), a national count of 76 (MOE 2009) seems very unlikely based on present understanding both of the species and of the sites where they were reported. Even more extraordinary was the inclusion in 2000 of a presumed misidentification (and/or typing error?) of 47,471 Asian Short-toed Lark Calandrella cheleensis at one site - especially as there appeared at that time to be less than ten adequately-documented records of this species in the ROK (Moores & Park 2009). Some of the suspected errors have likely been influenced by incorrect status assessments provided by Won (2000), and without appropriate caution these could lead to major errors in assessment of trends. Examples include Garganey Anas querquedula (―scarce winter visitor‖: Won 2000) which was recorded in three out of the first five years of the MOE Census (with 250 reported in 1999: MOE 1999-2004) and Eastern Cattle Egret Bubulcus coromandus (―common resident‖: Won 2000), which increased from two in 2007 to eight in 2009 (MOE 2007-2009). Neither is yet known to be adequately documented in the ROK in mid-winter (Moores & Park 2009) and by 2010 apparently no images of either species in the mid-winter period had been posted on any of the nation‘s numerous websites on birds, even though both species are frequently 64

depicted during migration and in the boreal summer respectively. Little Ringed Plover Charadrius dubius is another species increasingly reported by the MOE Census (e.g. four in 1999 and 90 in 2009). It was, however, apparently adequately documented overwintering for the first time only as recently as January 2009 (unpublished data, supported by photographs). It is but one of several shorebird species that appears to be repeatedly misidentified by the MOE Census. Based on Birds Korea survey effort at several of the same sites, Little Ringed Plover is presumably being claimed in error for Long-billed Plover Charadrius placidus, thus also resulting in under-reporting by the MOE Census of the latter species. Such misidentification is also perhaps influenced by Won (2000), which described Little Ringed Plover as common in winter and Long- billed Plover as scarce in winter. Several other shorebird species that are genuinely very scarce in the mid-winter period seem to be regularly misidentified based on a comparison with MOE Census reports and shorebird survey of many of the same sites in the mid-winter period (Moores 2006). These include frequent misidentification of Red-necked Stint Calidris ruficollis presumably for Dunlin Calidris alpina, and of Far Eastern Curlew Numenius madagascariensis presumably for Eurasian Curlew Numenius arquata. A few other species appear instead to have been overlooked. For example, several Eastern Yellow Wagtail Motacilla tschutschensis taivana were present at sites covered by the MOE Census in early January 2009 (unpublished data, supported by photographs) but the species was not listed in MOE (2009). In short, interpretation of MOE Census to develop an understanding of species‘ abundance and seasonal distribution in the ROK is hampered by a poorly described and apparently inconsistent count methodology and coverage of sites, and an inadequate structure for checking data and removing incorrect identifications. Caution is essential when considering both published and anecdotal records of some species (including both numerous and scarce species), especially those which appear, based on the MOE Census, to be especially difficult for some observers to identify. These still include some ducks, egrets (Ardeidae) and many Charadriiformes, several shrikes and species of pipit (Motacillidae).

2.3 INTERPRETING THE FOUR ASSESSMENTS There are large differences between earlier and more recent decades in the number of active observers; the improved access to certain habitats; improved identification capacity; and changes to positions on taxonomy and status. All of these have 65

influenced the number of species being recorded within the ROK, and very probably the perceptions of some species‘ status and abundance during the past century. Three of these factors are examined further below.

2.3.1 Geographical Scope Difficulties remain in determining the exact number of species recorded in the ROK in Austin (1948) due to the intentional exclusion of species recorded only on Jeju or Ulleung Islands and the lack of clarity over the exact location of some species recorded in Gangwon and Gyeonggi Provinces (now divided between the present-day ROK and DPRK). Based on Gore & Won (1971) and Park (2002) at least four species excluded by Austin (1948) are known to have been recorded on Jeju by his time, namely Greylag Goose Anser anser, Pacific Reef Heron Egretta sacra, Fairy Pitta Pitta nympha and Far Eastern Cisticola. Slaty-backed Gull was also listed by Momiyama (1927) but was not included by these other authors. According to Duckworth (2006) at least one Gangwon Province record (that of Yellow-billed Loon Gavia adamsii) was incorrectly assessed as an ROK record by Gore & Won (1971). In addition, the ROK‘s only record of Swift Tern Thalasseus bergii (included by Park [2002] without comment) seems more likely to be both in error for the now Critically Endangered Chinese Crested Tern Thalasseus bernsteini, and also rather more likely from present-day DPRK than ROK. The specimen was reported by Austin (1948) based on Kuroda (1918) and is believed to be no longer extant (Park 2002). It was one of several species reported in ―random notes‖ made by Kuroda that included several ―questionable‖ records. It was ―said to be‖ collected in July 1917, 72 miles from Incheon, on ―probably one of the outer islands off south-eastern Hwanghae Do (Province)‖ (Austin 1948: 135, 285). The closest corresponding islands in distance from Incheon are those close to the DPRK mainland in Ongjin County – only c. 250km east from islets off the coast of the Shandong Peninsula where in June-July 1937 a total of 21 Chinese Crested Tern specimens were collected. It has also been recorded in more recent years in the north of the Yellow Sea (BirdLife International 2011). Swift Tern, in contrast, was described as an accidental straggler north only to the main islands of Japan (Brazil 1991). Until 2011 (when it was apparently recorded on Jeju: Kim 2011a), the closest recent record to the ROK was one in Japan in October 1991 c. 135km south of Busan (unpublished data). Considering its historical breeding range, more recent records, and the relatively paucity of bird records from the coastal zone 66

before 2000 in the ROK, it seems plausible that the Chinese Crested Tern formerly occurred, at least occasionally, in the YSBR.

2.3.2 Taxonomy and Identification Further difficulties in comparing the Four Assessments directly also arise from taxonomic changes, though almost all of the species elevated to species rank by Moores & Park (2009) (including. Western Great Egret Ardea alba and Eastern Great Egret Ardea modesta; Naumann‘s Thrush Turdus naumanni and Dusky Thrush Turdus eunomus) were included as subspecies by Austin (1948), allowing easy confirmation of their presence during the first half of the twentieth century. The presence or absence, however, of several other taxa during Austin‘s time through to the 1990s remains much more difficult to determine. This is due not only to changes in taxonomic positions but also to recent improvements in identification capacity. Based on present knowledge of phenology and distribution of certain taxa, it seems likely for example that at least Mongolian Gull was regular during Austin‘s time in Korea. It also seems probable that most other gull species now known to be regular in the ROK and the YSBR were also present in earlier decades. Large gulls are challenging taxa to identify, especially those belonging to the Larus argentatus-cachinnans-fuscus complex (after Liebers et al. 2001). From among this group of taxa, Austin only recognised ―Larus argentatus vegae” (―Vega Herring Gull‖) as having been recorded in Korea. He described this species as a common winter visitor and migrant, being common at Incheon ―in November and December, noticeably scarcer in January and February, and again plentiful in March and April‖ (Austin 1948: 133). However, mtDNA sequencing (Liebers et al. 2001) and especially in-field research on breeding ecology, vocalisations, and moult indicates that several large herring-gull type taxa from this complex occur in East Asia, and in the ROK (Moores 2003c, 2003d; Olsen & Larsson 2003). Based on improved identification criteria most individuals can be identified to taxon by experienced observers, at least in juvenile, immature and non-breeding adult plumage (Moores 2003b). Despite continuing discussion and lack of consensus on taxonomy (Yésou 2001, 2002; Moores 2003c; Olsen & Larsson 2003) three taxa from this complex are now considered to be widespread and even locally numerous in the ROK and YSBR (Moores 2003d; Moores & Park 2009). These are Vega Gull Larus vegae (which was included by Austin), Mongolian Gull (confirmed in the ROK through records of wing-tagged birds: van 67

Dijk et al. 2011), and Heuglin‘s Gull Larus heuglini, of subspecies taimyrensis (increasingly referred to as Taimyr Gull, here and by van Dijk et al. 2011). Identification criteria for several of these and other large gull taxa were only developed recently. In the region‘s leading field-guide of the early 1980s, immature Slaty-backed Gull was described as ―indistinguishable‖ from Vega Gull – the only ―Herring Gull‖ recorded at that time in Japan (WBSJ 1982: 88). Following Grant (1982) and Grant (1986), which presented much new information on gull identification, a series of papers looking at the identification and taxonomy of large gulls in East Asia were published (Ujihara & Ujihara 1992, Kennerley et al. 1995, Hoogendoorn et al. 1996). These helped to provide the first detailed identification criteria for many of the region‘s gull species, resulting in numerous gull taxa being identified for the first time in Japan (where there were many more birdwatchers than in Korea) and then in the ROK (Table 2.2).

Table 2.2 Gull species adequately documented with photographs in the ROK, by year of their first record in the ROK and Japan. Species Name Scientific Name First Record First Record ROK Japan Black-tailed Gull Larus crassirostris 1880 1845-1850 Saunders's Gull Chroicocephalus saundersi 1888 1908 Vega Gull Larus vegae 1888 Pre-1953 Common Gull Larus canus 1910 1864 Slaty-backed Gull Larus schistisagus (1915) 1965 Pre-1953 Black-headed Gull Chroicocephalus ridibundus 1916 1856 Black-legged Kittiwake Rissa tridactyla 1966 1882 Relict Gull Ichthyaetus relictus (1988) 1990 1984 Glaucous Gull Larus hyperboreus 1993 1874 Mongolian Gull Larus mongolicus (1994) 1997 1982 Taimyr Gull Larus heuglini 1996 c. 1987 Glaucous-winged Gull Larus glaucescens 1997 Pre-1890 Iceland Gull Larus glaucoides 1997 1984 Thayer‘s Gull Larus thayeri 1999 1987 American Herring Gull Larus smithsonianus 2001 1990s? Slender-billed Gull Chroicocephalus genei 2002 1984 Pallas's Gull Ichthyaetus ichthyaetus 2002 1982 Caspian Gull Larus cachinnans 2006 c. 2003 Lesser Black-backed Gull Larus fuscus 2009 No record Note: Dates of First Records in the ROK are derived from the Four Assessments, Park (2002), and from Birds Korea online accounts, with earlier dates in brackets (omitted by Park 2002) for Relict Gull from BirdLife International (2003); for Mongolian Gull from personal unpublished data; and for Slaty-backed Gull from Momiyama (1927). First records in Japan are based on Brazil (1991), Ujihara & Ujihara (1993) and Ujihara & Ujihara at: www23.tok2.com/home/jgull/gullidentifi_.htm#KamomeHB.

The available evidence suggests that many large gull taxa have been largely overlooked and/or assigned differently until recently. Mongolian Gull, only ten years after its ―discovery‖ in the ROK, is now known to be widespread and regular. Its present-day distribution is helpful when considering the distribution of historical records of large gull taxa. Vega Gull typically breeds on ―islands and sea-cliffs in high Arctic‖ (Olsen & Larsson 2003) and is very seldom-recorded in the YSBR in the 68

summer (unpublished data). Mongolian Gull breeds much further south including in ―NE Mongolia and Hulan Nor, China‖ (Olsen & Larsson 2003) as well as in the ROK. Based on mapped ranges and on the identification of immatures (which are regular in mid-summer), mid-summer records of ―Herring Gull‖ in the ROK are presently much more likely to be of Mongolian Gull than of Vega Gull. Mid-summer records of large gulls are not all recent, however, and out of a total of 11 specimens listed under ―Vega Herring Gull‖ by Austin (1948) (none traced by the present research) four are from the period late May-July: one in late May and two in early June 1917 in Pyongan Buk Province, and one on 25 July 1932 in Pyongan Nam Province (all western DPRK). ―Herring Gulls‖ (presumed to be Mongolian Gull on range) were recently found to be one of the most numerous species nesting within a Black-faced Spoonbill colony in the latter DPRK province (Chong et al. 2000). Between 1995 and 1997, 250 were present at this colony (MAB 2002). It therefore seems probable that Mongolian Gull has been present and widespread in summer in parts of the Yellow Sea from at least the 1910s (and likely earlier too). Many or all of the earlier mid-summer records of Vega Gull listed in Austin (1948) therefore probably refer to Mongolian Gull. Mongolian Gull is also widespread in winter in the YSBR, with small numbers remaining in Incheon through the mid-winter, becoming locally abundant in Incheon between February and early April. In contrast, large numbers of Vega Gull start to arrive back in the ROK and YSBR on southward migration in October, peaking in early to mid-November, with most in the southern YSBR (Chapter 6). Numbers in the southern YSBR peak again between mid-March and late March (Chapter 6, KNP 2008). Northward migration is concentrated in early April, and appears to be mostly through the Korean Strait and north into the East Sea (unpublished data). Most Taimyr Gull apparently remain in open sea during northward migration (unpublished data, Chapter 6). The dates of increase of large gulls in Incheon harbour noted by Austin (1948) therefore also better matches the present migration timing and strategy of Mongolian Gull than of Vega Gull or Taimyr Gull. It is apparent that gulls were an especially challenging group of taxa to identify before the 2000s. Moroever several gull taxa were also more or less confined to the kinds of habitats (coastal zone, intertidal wetlands, open sea areas and offshore islands) that few ornithologists visited. However, misidentification was (and remains) frequent in other hard-to-identify taxa too. This includes many of the warblers. Gore & Won (1971) made explicit that several species of warbler were ―very difficult to separate in 69

the field‖. They described Radde‘s Warbler Phylloscopus schwarzi as ―so difficult to separate in the field from other leaf warblers (that) it may occur regularly on migration but be overlooked.‖ Recent survey (see Chapters 7 & 8) has confirmed that the species is indeed a regular and occasionally numerous migrant on offshore islands in the YSBR. Gore & Won (1971) also cited only one national record of the rather similar Dusky Warbler Phylloscopus fuscatus, and again made explicit that ―it may well occur more often but is overlooked‖. Dusky Warbler was confirmed breeding in the ROK first in the early 2000s, in the subalpine zone on Sorak Mountain, Gangwon Province (Park & Chae 2001). The same decade it was also found overwintering in small numbers, especially on offshore islands and in coastal reedbeds (unpublished data) and it is now known to be common on migration, with a one-day count of 96 on Socheong Island in May 2010 (Chapter 7). Both Radde‘s and Dusky Warbler tend to be numerous mostly in areas that were largely inaccessible to writers of earlier assessments. It is therefore unclear whether there has been a substantial increase in both species in recent decades, or whether they were instead formerly rarely encountered or identified. However, more familiar species of leaf warbler that were regular and numerous in easily-accessible areas were also sometimes misidentified. Arctic Warbler Phylloscopus borealis was described as an ―abundant passage migrant‖ by Gore & Won (1971), ―the most common leaf warbler on migration‖, and ―probably a summer visitor in the highlands‖. It was therefore considered as a familiar and widespread species. Duckworth (2007), confirmed its status as a migrant, but refuted the Arctic Warbler‘s status as a summer visitor and previous assumptions of Korean breeding. He (correctly) attributed both to misidentification (presumably with other species of leaf warbler) and to incorrect interpretation of migration timing. As noted by the same author, misleading statements on its status (including by Austin 1948) have confused recent works. MacKinnon & Phillips (2000) mapped much of Korea in the breeding range, and Tomek (2002) also suggested that it was probably a rare breeding species in the DPRK. It is clear therefore that caution is required when considering historical and even some recent assessments of hard-to-identify species. Improvements in optics and recording equipment, identification capacity and observer experience have all resulted in a substantial increase in credible records of some species of gull, leaf warbler, pipits and other challenging taxa. However, major information gaps still remain and without 70

a system to screen records, misidentification is perhaps sufficiently chronic to lead to incorrect mapping of distribution and incorrect assessment of population trends.

2.3.3 Access Following survey effort in intertidal areas of the west coast that started only in the late 1980s, it became apparent that not only some gull species but several shorebird species staged regularly in large numbers in the ROK‘s estuaries and intertidal wetlands, along both the west and south coasts (Piersma 1985, Long et al. 1988, Kim et al. 1997, Moores 1999a, Barter 2002). The presence and to a greater extent the relative abundance of such species was poorly-known and under-represented in the ornithological literature until very recently, in part due to the inaccessibility of their preferred habitat. Austin makes this explicit in his account of the Red Knot, a ―rare transient visitor, though perhaps more plentiful on the unexplored outer beaches than the record indicates‖ (Austin 1948: 126). Presumably due to the challenges of access and of observing (or shooting) birds in the ―unexplored‖ outer beaches of vast intertidal wetlands, swept by occasionally huge tides (regularly over 9m near Suwon) and the dates he was present in the ROK, Austin also referred to rice-fields three times (but not at all to intertidal areas) in his account of Common Greenshank Tringa nebularia (Austin 1948: 119). This species has been, and remains, more numerous in recent decades in intertidal rather than in agricultural areas (see Chapter 5, Table 5.2). Even more than species of intertidal areas, species typical of open sea areas and offshore islands were poorly known until recently. Increased access to such habitat- types through the 1990s and especially in the 2000s has resulted in much of the increase in the number of newly-recorded species in the ROK. While the number of newly-recorded species averaged 2.1 per year between the time of Austin (1948) and that of Gore & Won (1971), it increased more rapidly to an average of 3.5 newly- recorded species per year in the subsequent 39 years. Two groups make up most of this increase: (1) Laridae and species of marine waters; and (2) species recorded almost only on offshore islands, most of which are landbirds. If these two groups are removed from the comparison, then the annual rate of species increase is much smaller. There were only 1.7 additional species per year between the time of Austin (1948) and Gore & Won (1971), and 1.3 additional species per year between Gore & Won (1971) and Moores & Park (2009). In summary and considering all of the above: 71

1. Much of the increase in the number of species recorded in the ROK since Austin‘s time can be attributed to a range of biases; 2. The decline or loss of most species from previously poorly-covered habitats will not be well-reflected by the ornithological literature: 3. The perceived increased abundance of some species will likely be due to improved identification capacity and increased coverage in recent decades; 4. Few species will likely appear to have declined as a result of increased coverage and identification capacity, and these will be cases where an obvious confusion species has shown strong compensatory increases. 5. It remains necessary to develop clear baselines on species‘ distribution and abundance – both historical and contemporary. Aware of the influence of bias, can large-scale changes in abundance or changes in seasonal presence or absence still be detected in any of the bird species of the ROK between the time of Austin and the present?

2.4 METHODS 2.4.1 Four Assessments Each of the Four Assessments provides a description of perceived abundance for each listed species. In Austin (1948) and Gore & Won (1971) this description is given within the text, through use of broad terms such as ―Abundant‖ and ―Common‖; in Won (2000) each species is annotated (e.g. ―u‖ denotes ―Uncommon‖); and in Moores & Park (2009), there are five bands of estimated abundance (number of individuals or records per year estimated from survey work and collation of data) and three further categories covering ―Rarely-recorded‖ and ―Seldom-recorded‖ species. In combination, these bands of abundance cover the range of least abundant species (recorded less than ten times in total in the ROK to date) to the most abundant (>100,000 individuals counted or estimated to be present annually). A series of steps needed to be taken to convert these different descriptors into a single currency that can both describe changes in abundance between 1910 and 2009, and also enable comparison of the results with assessments by Tomek (1999, 2002), Wetlands International (2006) and BirdLife International (2011). Therefore: 1. Only species considered adequately documented by Moores & Park (2009) were analysed. 72

2. For each of these species, the description of highest abundance in each of the Four Assessments was selected (so if a species was assessed as uncommon in winter and common in summer, then the summer status was selected). 3. Each description of highest abundance in each of the Four Assessments was then converted into an ―Abundance Number‖ (0, 1, 2, 3, 4, 5 or 6) (Table 2.3).

Table 2.3 Conventions used to assign a consistent Index of Abundance (―Abundance Number‖) to the Four Assessments of bird abundance in the ROK. Abundance Term used in Austin (1948), Gore & Equivalent Number used in Number Won (1971) and Won (2000) Moores & Park (2009)

1 ―Abundant‖ or equivalent 1 2 ―common‖, ―not uncommon‖, ―fairly 2 common‖ or equivalent 3 ―locally common‖, ―uncommon‖ or 3 & 4 equivalent 4 ―rare‖ or equivalent 5

5 ―Vagrant‖, ―Straggler‖ or equivalent V1, V2, V3

6 Not Applicable Nationally-extinct; no records since 1980 0 Not recorded Not Applicable

In order to prevent potentially excessive reinterpretation by the present author, Abundance Numbers of earlier authors were then modified to reduce bias, but in only a few cases. Modification was based either on comments provided within the Four Assessments, or on recent information that was known to Moores & Park (2009). This included an improved understanding of first-breeding records (following Duckworth & Moores 2008). For species, however, where first-breeding was recorded by one of the Four Assessments without reasonable evidence of bias, this resulted in either an upward change in Abundance Number (e.g. from 2 to 1) or a change in abundance category (as described below) during the relevant period. Similarly, in a few cases where cessation of breeding was recorded by one of the Four Assessments without reasonable evidence of bias, this resulted in a downward change in Abundance Number (e.g. from 2 to 3). The same process was used in a very few species in which there was clear evidence of a change in seasonal presence or absence (e.g. if a species was assessed as having started to overwinter in substantial numbers, but not to have 73

decreased in another season, then this was also considered as evidence of an increasing trend). In a few cases, recent evidence either suggested substantial errors in the perceptions of earlier authors due to bias, or changes in trend that were not shown by the series of Abundance Numbers. These species are discussed in Section 2.5.7. All 511 bird species adequately documented in the ROK since 1910 were then divided into two main categories, the first of species that are or that were regularly occurring (with Abundance Numbers of 1-4 and 6 respectively); and the second of species that are less regular in occurrence (Abundance Number 5). Although a few taxa might be incorrectly categorised by this coarse division, separation into these categories was considered an essential early step in the refinement of research and conservation priorities. Through this process, the abundance and population trend of every species could be represented by a series of four Abundance Numbers (each more focused on a different time-period of ornithological activity). The resultant sequence could then be assigned to one of three main categories of National Population Trend (Positive, Negative or Unknown) further subdivided into seven categories (Table 2.4).

Table 2.4 Three main and seven subdivisions of population trends in regularly-occuring species in the ROK between 1910 and 2009 based on Abundance Numbers and/or on commentaries in the Four Assessments of Austin (1948), Gore & Won (1971), Won (2000) and Moores & Park (2009). Main Change between Assessments Example of Sub-divided Trend Category of in Abundance Numbers Abundance in ROK Population or in commentary Number Trend Series

Positive 1. Upward change of two or more in 3,2,2,1 Increasing Population Abundance Numbers. Trend 2. Increase of one in upward direction in series 3,3,2,2 Probably Increasing of Abundance Numbers, or suggestion of increase in commentary. 3. Strong evidence of first breeding or rapid 0,0,0,4 Recent Colonist increase in records since 2000.

Negative 4. Downward change of two or more in 2,2,3,4 Decreasing Population Abundance Numbers. Trend 5. Evidence of cessation of breeding; 1,1,2,2 Probably downward change of one in series of Decreasing Abundance Numbers; commentary suggesting decrease. 6. No record since 1980 or earlier in a 0,0,0,6 Nationally Extinct previously regularly-occurring species.

Stable or 7. All four numbers the same; or difference of one 1,1,1,1 Stable or Unknown Unknown or more in Abundance Numbers, but trend or Population unclear; or assessment contradicted by near- 4,3,2,4 Trend contemporaries. 74

2.4.2 Tomek (1999, 2002) & DPRK Literature ROK results were then compared against ornithological literature from the DPRK, especially Tomek (1999, 2002). Tomek built on Austin (1948) and Won Hong Koo (1963-1965) through extensive review of DPRK literature (>30 publications cited) and regional literature, unpublished data, and her own museum-based research and fieldwork. She thus provided the only detailed review of all species recorded up to the end of the twentieth century in the DPRK. All of Tomek‘s species entries were divided into two sections. The first section (―Data‖) contained records of collection or observation organised by location and date with an accompanying map, and the second consisted of a commentary in which she occasionally provided an explicit opinion on population trend, sometimes apparently contradicting the Data. As there was a ―state of ignorance‖ (Tomek 2002: 186) about many species in the DPRK selected texts from Duckworth (2004, 2006), Duckworth & Moores (2008), MAB (2002) and Riegen et al. (2009) were also used to try to confirm or modify Tomek‘s conclusions where appropriate. For the present analysis, ―Data‖ were considered superior to commentary. Data in Tomek (1999, 2002) were first sorted into two main time periods: Pre-1978 and 1978- present, from when, in addition to DPRK nationals, ―non-Korean ornithologists‖ (Tomek 1999: 5) also conducted surveys. Many of the sources used by Tomek were checklists, many covering either single sites in the DPRK or the whole Korean Peninsula. Therefore a data-based record was taken as one record for each exact date or month listed for that species, and also for each year when precise dates were not included (e.g. 1986-1988 is taken as three records). Two sets of ratios were selected to assess large-scale changes in abundance. Ratios of records of 3:1 and 5:1 before and after a given year (pre-1946, 1966, and especially 1978) were selected. The main year used was 1978 because in some easy to identify and widespread species with no commentary indicating decline there were approximately similar numbers of records between the period before 1978 and after 1978 (e.g. Tomek listed c. 65 Eurasian Magpie Pica pica records before and 57 after 1978). This was perhaps because the shorter time period was compensated for by expanded survey effort from that year and/or by a greater proportion of recent records that were made known to her. A reduction in the selected ratio rates (e.g. to twice the number of records before than after 1978) would have increased the number of species that appear to have decreased. The ratios that have been selected are therefore conservative, and biased towards 75

revealing increase rather than decrease. Only those species recorded three or more times between 1910 and 1965, or only since 1966, were assessed. This was to reduce the number of less regular species under consideration and to prevent unnecessary distortion in status arising from too few data, while also retaining species that might be in the early stage of becoming regular in the DPRK (e.g. Chinese Blackbird Turdus [merula] mandarinus). Thus excluded species include Marsh Sandpiper Tringa stagnatilis as the status of this species in the DPRK remains inadequately known. It seems reasonable too, considering the poor knowledge of shorebirds in intertidal wetlands in the ROK until the 1980s and Riegen et al. (2009) that many other shorebird species will at present be under-represented in the DPRK ornithological literature. Data and Commentary were then used in combination to sort species into main categories of trend (Table 2.5). When data indicating decrease were supported by the commentary, a species was considered to be Decreasing; when data of decrease were contradicted by the commentary, a species was considered to be Probably Decreasing. The suspected trends in the DPRK could then be compared to ROK trends, though with species marked as ―*Increasing‖ recorded only once or twice in total, and only since 1966.

Table 2.5 Six categories of suggested population trend in the DPRK based on Data and Commentary in Tomek (1999, 2002). DPRK Data and/or Commentary Used Suspected Trend Trend

Positive 1. All records (>2 in total) between 1966 & present. Increasing Population 2. All records (1 or 2 in total) between 1966 & present. *Increasing Trend 3. Comment on increase or range expansion/new breeding, Probably Increasing contradicted or not by Data; ratio of 1:3 records from pre- 1946: 1946-present.

Negative 4. Three or more records before 1966, but no records between Decreasing Population 1966 & present; ratio of 5:1 records from pre-1978: 1978- Trend present. 5. Comment on decrease, range contraction/cessation of Probably Decreasing breeding, contradicted or not by Data; ratio of >3:1 records from pre-1978: 1978- present.

Stable or 6. No clear statement and no clear trend discernible in data. Unknown Unknown Population Trend

Each species account was then rechecked for apparent contradictions. Comments on new breeders were checked against Duckworth & Moores (2008); other records were checked against Duckworth (2004), which included first-records of eight species, and 76

Duckworth (2006), which provided details of 49 species hitherto largely unrecorded by Tomek (1999, 2002). For these species, if it was recorded more than five times before 1978 but once or not at all subsequently by Tomek (1999, 2002) then: 1. If there was a maximum of only two additional records provided by Duckworth (2006), it was still assessed as ―Decreasing‖; 2. If a species was recorded more than twice by Duckworth (2004, 2006), but rather fewer times than in Tomek (1999, 2002), then the species was assessed as ―Probably Decreasing‖; 3. If a species was recorded multiple times by Duckworth, as well as by earlier observers before (but not after) 1966, then the species was omitted, as it is assumed that the species was overlooked and considered to have an ―Unknown‖ trend; 4. If a species was recorded only once or twice before 1978, but several times by Duckworth (2004, 2006), then the species was re-evaluated as ―Increasing‖.

2.5 RESULTS 2.5.1 Status of Regularly Occurring and Less Regular Species Based on the Methods above, 365 out of the 511 species recorded between 1910 and 2009 in the ROK can be described as regularly occurring. Over one-third of these (128) showed a Negative National Trend, and approximately one-quarter (98) appeared to show a Positive National Trend (Table 2.6). The remainder showed no clear trend. All species are listed in the Appendix (pp. 316-322), with their National Population Trend.

Table 2.6 National Population Trend in seven subdivisions between 1910 and 2009 of all 511 species in the ROK based on the Four Assessments, further divided into regularly occurring and less regular species. National Subdivision of Number of Number of Total Population population trend regularly less regular trend occurring species species

Positive Recent Colonist 5 0 5 Positive Increasing 31 1 32 Positive Probably Increasing 62 1 63 Negative Decreasing 34 0 34 Negative Probably Decreasing 89 11 100 Negative Nationally Extinct 5 0 5 Unknown Stable or Unknown 139 133 272 Total 365 146 511

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Among species showing a Negative National Trend, five were formerly regularly occurring but are now nationally extinct (with no published records since 1980) and among those showing a Positive National Trend five are ―recent colonists‖. Based on Brazil (2009), BirdLife International (2011) and on personal observations, none of the recent colonists are species of global conservation concern; none are yet widespread or numerous in the ROK; and all are small or medium-sized and appear to be tolerant of disturbed or artificial habitats, both in and outside of the ROK. In contrast, two of the nationally extinct species (Crested Ibis and Great Bustard) are of global conservation concern. Both are large-bodied, and both were formerly locally numerous in the boreal winter in the ROK (Austin 1948). Among the remaining three nationally extirpated species, one (Crested Kingfisher Megaceryle lugubris) was probably a very scarce winter visitor, one (Chinese Hill Warbler) was scarce though enigmatic in distribution, and one (White-bellied Woodpecker) was widespread, probably at low density, in lowland forest. The population trend in 133 out of the 146 species that occur less regularly in the ROK is unknown. Two showed a Positive and 11 a Negative National Tend. This category of less regular species likely includes some which will prove to be regularly occurring, either through increased coverage of certain habitats (such as of open sea, where South Polar Skua Stercorarius maccormicki and Red Phalarope Phalaropus fulicarius both probably do occur regularly: Chapter 6) or through colonisation. At least 15 of these less regular species are presently recorded annually (based on Birds Korea Annual Reviews: e.g. Moores & Moores 2002-2005). The less regularly occurring group of species also contains Swift Tern and eleven species of global conservation concern, including the Critically Endangered (and probably globally Extinct) Crested Shelduck Tadorna cristata. This species, along with the globally Vulnerable Short-tailed Albatross Phoebastria albatrus might once have been part of the regularly occurring avifauna of the Korean Peninsula (Austin 1948).

2.5.2 Species of Global Conservation Concern In total, 50 of the 511 species adequately documented between 1910 and 2009 in the ROK are of global conservation concern (i.e. they are assessed by BirdLife International on behalf of the IUCN as Critically Endangered, Endangered, Vulnerable or Near-threatened). Thirty-seven of these are regularly occurring in the ROK and 13 are less regular (Table 2.7). Only three of these showed a Positive National Trend 78

based on the Abundance Numbers (all ―Probably Increasing‖): Near-threatened Cinereous Vulture Aegypius monachus, Vulnerable Greater Spotted Eagle Aquila clanga and Vulnerable Saunders‘s Gull.

Table 2.7 The global conservation status of species by category of ROK National Population Trend between 1910 and 2009, divided into regularly occurring and less regular species. ROK National Trend Global Conservation Status Global Conservation Total regularly occurring species Status less regular species CR EN VU NT CR EN VU NT Recent Colonist Positive National Trend 2 1 3 Nationally Extinct 1 1 1 3 Negative National Trend 1 2 11 5 1 2 22 Stable or Unknown 3 5 5 1 2 2 4 22 Total 1 6 19 11 2 3 4 4 50

According to Birds Korea unpublished data and other sources, the recent increase in Cinereous Vulture is likely genuine (Lee et al. 2004) and due to a combination of factors, including reduced persecution and increased artificial feeding programs. The Positive National Trend in the other two species might instead be attributable to bias. The Greater Spotted Eagle remains a rare migrant (most regular in late October and early November) and winter visitor. There are probably 10-20 records most years although there were only three records in 2008 (Birds Korea unpublished data). The large fluctuation in the number of records each year appears to be a result of inconsistent survey effort during the main migration period and also in part to the different interpretation of counts of migrant birds (Moores 2007). The increase in ROK records in recent years is likely, in part or largely, due to increased observer effort and competence. Saunders‘s Gull is locally numerous, especially in mid-winter, with breeding also increasingly reported. As described above, Laridae are among the most poorly-known group of taxa in the ROK and Saunders‘s Gull has been overlooked until recently. High counts of the species during recent winters are difficult to compare with earlier survey results, even from within the 2000s. The MOE Census (2001) recorded only 519 Saunders‘s Gull nationwide in early 2001 while the present author counted 2,158 in January 2001 at only some of the same sites (unpublished data). It seems possible 79

that with the completion of ongoing reclamation projects in several of the Saunders‘s Gull‘s most important sites (including Song Do, Namyang Bay, Asan Bay and Saemangeum: Chapters 3-5) that the overwintering population is already declining or will soon be in decline. However, survey effort remains inadequate and other variables (including weather-related movements and response to habitat degradation and loss) help obscure any underlying trend in the overwintering population. According to Kwon (2009) the breeding population in the ROK has ―rapidly increased‖. This is even as the species is assessed as decreasing globally (BirdLife International 2011). This perception of increase might be due to improved knowledge of the species since it was first found breeding (Moores 1999c), or to the creation of new habitat through reclamation of intertidal wetland leading to temporarily suitable breeding habitat (but a loss of foraging area used in both the breeding and non-breeding season). Nonetheless, in total, three species of global conservation concern have become nationally extinct, and a much greater number of species of global conservation concern showed a Negative National Trend (22) than Positive National Trend (three). One additional species of global conservation concern (Short-tailed Albatross) had already become nationally extinct before 1910.

2.5.3 DPRK Population Trends Based on the methods outlined in Section 2.4.2, evidence of a population trend was suggested for 112 species in the DPRK which are regularly occurring in the ROK. This total excludes 13 species with only one or two records in Tomek (1999, 2002) which were not recorded in Duckworth (2004, 2006) (including eight considered to be regularly occurring in the ROK). Three of these are species of global conservation concern (Swinhoe‘s Rail Coturnicops exquisitus, Nordmann‘s Greenshank Tringa guttifer, and Styan‘s Grasshopper Warbler). Seventy-five out of the 112 showed a Negative National Trend in the DPRK; and 43 of these 75 also showed a Negative National Trend in the ROK; 27 a Stable or Unknown Trend; and only five a Positive National Trend (none ―Increasing‖ and all ―Probably Increasing‖). Thirty-seven species showed a Positive National Trend. Twenty-five of these also showed a Positive and only three a Negative National Trend in the ROK. Among species that showed a Positive National Trend in the DPRK and ROK are Red-billed 80

Starling and Chinese Blackbird. Both of these are recent colonists in the ROK, and both were first recorded in the DPRK in either 2000 or 2001 by Duckworth (2004).

2.5.4. Decreasing Species in the ROK As outlined above, there is greater confidence in the trend shown by ―Decreasing‖ and nationally extinct species than in the trend shown by species assessed as ―Probably Decreasing‖. Out of the 128 regularly occurring species showing a Negative National Trend, 34 are assessed as Decreasing (Table 2.8). These Decreasing species come from 21 families and 13 orders.

Table 2.8 List of Decreasing species in the ROK between 1910 and 2009, including their global conservation status, Abundance Numbers (from the Four Assessments) and National Population Trend during the same period in the DPRK. English Name Scientific Name Global Abundance DPRK Status Numbers Trend

Japanese Quail** Coturnix japonica NT 2 ,2, 2, 3 Decreasing American Scoter Melanitta americana 2, 1, 2, 3 Long-tailed Duck Clangula hyemalis 2, 2, 3, 5 Common Goldeneye Bucephala clangula 2, 1, 2, 3 Black-necked Grebe Podiceps nigricollis 3, 1, 2, 3 Oriental Stork* Ciconia boyciana EN 3, 4, 4, 4 Grey Heron Ardea cinerea 1, 2, 2, 3 Probably Decreasing Purple Heron Ardea purpurea 4, 3, 3, 5 Decreasing Eastern Great Egret Ardea modesta 2, 1, 2, 3 Black Kite** Milvus migrans 2, 2, 3, 3 Decreasing Steller‘s Sea Eagle* Haliaeetus pelagicus VU 3, 3, 4, 4 Decreasing Golden Eagle* Aquila chrysaetos 3, 3, 4, 4 Probably Decreasing Swinhoe‘s Rail Coturnicops exquisitus VU 3, 3, 4, 5 Decreasing Band-bellied Crake Porzana paykullii NT 2, 3, 4, 5 Decreasing Watercock Gallicrex cinerea 2, 2, 2, 4 Decreasing Yellow-legged Buttonquail Turnix tanki 3, 4, 3, 5 Decreasing Spoon-billed Sandpiper** Eurynorhynchus pygmeus CR 3, 3, 3, 4 Decreasing Hill Pigeon Columba rupestris 2, 2, 3, 4 Eurasian Collared Dove Streptopelia decaocto 3, 3, 4, 5 Common Cuckoo Cuculus canorus 2, 1, 2, 3 Long-eared Owl Asio otus 2, ?, 2, 4 Decreasing Grey-capped Pygmy Woodpecker Dendrocopos canicapillus 2, 3, 3, 4 Decreasing Brown Shrike Lanius cristatus 2, 1, 3, 3 Daurian Jackdaw Coloeus dauuricus 2, 1, 3, 3 Crested Lark Galerida cristata 2, 2, 3, 4 Decreasing Eurasian Skylark Alauda arvensis 2, 1, 1, 3 (Decreasing) Far Eastern Skylark Alauda japonica 2, 2, 1, 3 (Decreasing) Eurasian Treecreeper Certhia familiaris 2, 3, 3, 4 Naumann‘s Thrush Turdus naumanni 2, 1, 2, 3 Decreasing Yellow-rumped Flycatcher Ficedula zanthopygia 1, 1, 2, 3 Common Redpoll Carduelis flammea 4, 3, 3, 5 Probably Decreasing Chinese Grosbeak Eophona migratoria 3, 1, 3, 3 Meadow Bunting Emberiza cioides 2, 1, 2, 3 Probably Decreasing Yellow-breasted Bunting Emberiza aureola VU 3, 1, 2, 3 Decreasing Note: Use of single asterisk denotes the species was lost as breeding species in the ROK during the past century; and a double asterisk denotes that the species was reassessed during the present analysis and is covered in Section 2.5.7.

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Seven of the Decreasing species are species of global conservation concern. All Decreasing species in the ROK that have a detectable trend in the DPRK (19 in total) showed a Negative National Trend in the DPRK (i.e. they were either Decreasing or Probably Decreasing).

2.5.5 Increasing Species in the ROK Out of the 98 regularly occurring species that showed a Positive National Trend in the ROK, 31 were assessed as Increasing (Table 2.9). These Increasing species were from 19 families and five orders.

Table 2.9 List of Increasing species in the ROK between 1910 and 2009, their Abundance Numbers (based on the Four Assessments) and their National Population Trend during the same period in the DPRK. English Name Scientific Name Abundance DPRK Numbers Trend

Tundra Bean Goose Anser serrirostris 2, 2, 3, 1 Greater White-fronted Goose Anser albifrons 2, 2, 3, 1 Common Pochard Aythya ferina 4, 4 ,1, 2 Eurasian Spoonbill Platalea leucorodia 5, 4, 4, 3 Black-crowned Night Heron Nycticorax nycticorax 5, 5, 2, 3 Increasing Chinese Pond Heron Ardeola bacchus 0, 0, 4, 4 Eastern Cattle Egret Bubulcus coromandus 5, 4, 2, 3 Increasing Little Egret Egretta garzetta 5, 3, 2, 3 Increasing White-breasted Waterhen Amaurornis phoenicurus 0, 0, 3, 4 Increasing Common Moorhen Gallinula chloropus 5, 3, 3, 3 Probably Increasing Black-winged Stilt* Himantopus himantopus 5, 5, 3, 4 Increasing Greater Painted Snipe* Rostratula benghalensis 5, 5, 5, 4 Common Redshank* Tringa totanus 4, 3, 3, 3 Marsh Sandpiper Tringa stagnatilis 5, 4, 3, 3 Oriental Pratincole* Glareola maldivarum 0, 5, 5, 4 Black-headed Gull Chroicocephalus ridibundus 3, 2, 1, 2 Increasing Azure-winged Magpie Cyanopica cyanus 3, 2, 2, 1 Varied Tit Poecile varius 3, 2, 2, 1 Coal Tit Periparus ater 3, 2, 2, 1 Chinese Penduline Tit Remiz consobrinus 5, 4, 4, 3 Brown-eared Bulbul** Microscelis amaurotis 2, 2, 2, 1 Probably Increasing Red-rumped Swallow Cecropis daurica 3, 2, 2, 1 Far Eastern Cisticola Cisticola juncidis 0, 4, 4, 3 Chestnut-flanked White-eye Zosterops erythropleurus 0, 5, 3, 2 Japanese White-eye Zosterops japonicus 4, 2, 2, 2 Chestnut-cheeked Starling Agropsar philippensis 0, 5, 4, 3 Citrine Wagtail Motacilla citreola 0, 0, 5, 4 Japanese Wagtail Motacilla grandis 5, 4, 3, 2 Increasing Olive-backed Pipit* Anthus hodgsoni 2, 2, 3, 1 Common Rosefinch Carpodacus erythrinus 0, 4, 3, 3 Common Reed Bunting Emberiza schoeniclus 5, 4, 3, 2 Note: Use of an asterisk denotes that the species was first recorded breeding since the late 1990s; and of a double asterisk that the species was reassessed and is discussed in Section 2.5.7.9.

82

None of the Increasing species had a poor global conservation status. All species that were assessed as Increasing in the ROK that had a detectable trend in the DPRK (nine in total) also showed a Positive National Trend in the DPRK (i.e. they were Increasing or Probably Increasing). None with known trends, however, were considered to be Increasing at the Flyway or Global level by either Wetlands International (2006) or BirdLife International (2011).

2.5.6 Species of the YSBR There is no official species checklist maintained for the YSBR. However, approximately 480 species have been documented in this sub-region since 2000, including probably 352 out of the 365 regularly occurring species in the ROK (Birds Korea data). Probably 329 species were recorded every year in 2006-2009 in the more narrowly-defined three main habitats of the YSBR (i.e. intertidal wetlands, excluding hinterland; inshore and offshore waters; and offshore islands, as defined in Chapter One). Their trends are shown in Table 2.10.

Table 2.10 The number of species recorded annually (2000-2009) within the YSBR, their National Population Trend and their global conservation status. Population Trend National Population Recorded Annually Number of Global Trend Conservation Concern Recent Colonist Positive 4 0 Increasing Positive 29 0 Probably Increasing Positive 52 2 Decreasing Negative 24 5 Probably Decreasing Negative 81 11 Stable or Unknown Unknown 139 13 Total 329 31

2.5.7 Resolution and Modification of the Results The very low precision of the data requires that the bands of estimated abundance (represented by the Abundance Numbers) be very broad. Even if authors were all equally accurate in their assessments (and there is much evidence as outlined above to suggest otherwise), it would still require a massive change in population to trigger a change in Abundance Number. The Abundance Numbers ―2‖ and ―3‖ represent ―common‖ and ―uncommon‖ in three of the Four Assessments, and have an upper limit respectively of 100,000 and 10,000 individuals counted or estimated per year in 83

Moores & Park (2009). Therefore, if a species was accurately assessed as common by Gore & Won (1971) and as uncommon by Won (2000) and Moores & Park (2009), this would indicate, in the most extreme case, a decline in abundance of 90% within 40 years. Such a massive decline would in turn still only result in an assessment as ―Probably Decreasing‖, unless the decline continued. Both Eurasian Magpie and Common Pheasant appeared to be Stable or have an Unknown Population Trend in the ROK during the past century. However, analysis of data in NIBR (2010) reveals there have been rapid declines in both species (of 33% in Eurasian Magpie in 11 years and of 47% in Common Pheasant in 15 years). These declines were not detected by the present research, and also would have been insufficient to trigger a status change even if they had been detected, as both remain ―abundant‖. It therefore seems probable that many more species will have changed in abundance during the past century than can be revealed by the present approach. However, it is also not appropriate to try to increase substantially the sensitivity of the analysis. The species accounts are too sketchy and data-poor, and there are too many potential sources of bias. In recognition of this, the Abundance Number-based population trend was revised for only a small number of species, even though every species trend was assessed for bias. The method was designed so that evidence of new breeding could trigger a change in Abundance Number or category to indicate an increase in population (e.g. from Unknown to Probably Increasing). Since 2000, at least 15 species have been claimed as breeding in the ROK for the first time. A few of these are recent colonists for which evidence of first-breeding is strong (Choi et al. 2011). In contrast, newly discovered breeding in six species including Dusky Warbler and Siberian Rubythroat Luscinia calliope did not trigger a change in Abundance Number or category. This is because their earlier breeding was probably overlooked. According to Park (2002) the first record of Dusky Warbler in the ROK was a specimen collected in 1932; the second and third records were sight-records made on one offshore island in April 1993; the fourth and fifth records were only in 1998; and then 50 Dusky Warbler were recorded on offshore islands in one province alone in 2000 as research effort on offshore islands increased. The next year, Dusky Warbler was recorded breeding in the ROK for the first time, in mountains in Gangwon Province (Park & Chae 2001). Male Siberian Rubythroat are distinctive and easy to identify and therefore might be considered difficult to overlook. However, the species is rather secretive on migration (Brazil 2009); it is most frequent during migration on offshore islands (Moores 2007); and in 84

the ROK, it has only been found in the breeding season in mountainous and previously difficult to access areas. It was first found in June and July, also in Gangwon Province by Park Jong-Gil, during the same research in 2001 that first found breeding Dusky Warbler (Park 2002). Earlier, Austin (1948) listed eight records of Siberian Rubythroat in central and southern provinces of Korea, one of which was in Gangwon Province on June 30th 1914 (location unknown). Gore & Won (1971) did not include many records of any species from high mountains. Such areas were largely unsurveyed until recent decades. The pattern of increased recording in the past decade especially suggests that both species were largely overlooked in the ROK, including as breeding species. There was therefore sufficient reason not to accept first confirmation of breeding as evidence of a major change in distribution or status in these and four other species. There was, by contrast, sufficient reason to modify the assessments of the 12 species in Sections 2.5.7.1-2.5.7.12.

2.5.7.1 Japanese Quail Coturnix japonica Japanese Quail (2, 2, 2, 3) was reassessed as Decreasing (rather than Probably Decreasing), based on a suspected massive decline during the twentieth century. Before the period of review, it was described as ―very abundant‖ between Seoul and Wonsan (latter in the DPRK) in the late 1880s (Taczanowski per Austin 1948). It was reported that on Geomun Island, Jeollanam Province in 1885-1887 ―in the month of October there is an annual invasion of quail; and with a smart dog, it is quite possible to make exceedingly good bags of these little birds; as many as five hundred have been shot by one gun, in part of a season‖ (Neff 2010). It seems probable, based on the dates and location, that many of these Japanese Quail were migrants that would have continued on to overwinter in either Japan or southern China. In the 1930s, the species still peaked in abundance in the ROK in October and early November (Kuroda in Austin 1948), and there was ―an average of more than 500,000 taken per year in the 1930s‖ in Japan (Brazil 1991: 108). Although an unknown number of these Japanese Quail likely came from the breeding population in Hokkaido and Honshu that existed at that time, its present status as migrant and winter visitor to Japan, ―occurring from late October to early November in the Tokyo area‖ (Brazil 1991) supports the belief that the mainland Asian population was still at that time abundant, and also responsible for many of the birds seen (and hunted) in both Japan and Korea. In recent decades the 85

Japanese Quail by contrast appears to be uncommon, local and probably still in decline in the ROK.

2.5.7.2 Mallard Anas platyrhynchos Mallard (2, 1, 1, 1) was reassessed as Probably Decreasing. There is no evidence of a rapid increase between the time of Austin (1948) and Gore & Won (1971) as suggested by the Abundance Numbers, and as with Baikal Teal, Austin probably understated the species‘ abundance. The Negative Population Trend is based largely on a recent rapid decrease in numbers recorded by the MOE Census of more than 50% between 2000 and 2009 (MOE 1999-2008; Moores et al. 2010: 14). It seems unlikely that this perceived decline is due to observer bias within the ROK. This is especially so as analysis of NIBR data indicates a decline of 81% in the ROK between 1996 and 2010; and analysis of waterbird counts recorded by the Asian Waterbird Census between 1987 and 2007 also suggests a substantial decline in Mallard in Asia during the same period (Li et al. 2009: 268).

2.5.7.3 Baikal Teal Anas formosa Baikal Teal ([2], 2, 3, 1) was reassessed as of Unknown Trend. It is a species in which the vast majority of the global population winters in the ROK. It is described as ―Increasing‖ by Wetlands International (2006) largely on the basis of MOE Census data, but as ―Decreasing‖ by BirdLife International (2011). Although described only as ―common‖ by Austin (1948), his own fortuitous sighting of a Baikal Teal flock more than two-miles long suggests that he greatly underestimated the species‘ abundance. This assumption is supported by Wolfe (1950) who did describe the species as ―Abundant‖. The present re-assessment is therefore based on the understanding that the species was formerly abundant; underwent a massive decline in the mid-twentieth century (both within the ROK and globally); and has now likely recovered much of its historical population in the ROK at least (Moores 2005; MOE Census 1999-2010).

2.5.7.4 Black Kite Milvus migrans Black Kite (2, 2, 3, 3) was reassessed as Decreasing (rather than Probably Decreasing) on the basis of its range contraction within the ROK, and the loss of its status as a locally common but probably widespread breeding species at least in the first half of the twentieth century. Austin (1948) saw the species commonly in Incheon (where it is now absent); quoted Won Hong-Koo‘s statement that the species ―is 86

common and breeds‖ (presumably largely in the northern provinces); but ignored much evidence of former abundance and breeding in several parts of Korea. His near- contemporary, Wolfe (1950) found twelve nests (five in and around Seoul, and seven within a 25-mile radius of the city), despite being limited by the challenges of travel at that time. This understandably led Wolfe to describe Black Kite as ―a comparatively common breeder in all of the central area...equally at home either in the city streets or on the uninhabited hills‖. Other near-contemporaries of Austin also described it as a ―common permanent resident‖ around Seoul, although ―strangely‖ absent from the parts of Busan that he visited (Fennell 1952), and ―very common‖, occurring ―right in the [city centres] of Seoul and Inchon‖ in 1951–1952 (Prentice 1952). By the time of Gore and Won (1971: 83, 161) it still bred ―commonly‖ on Jeju Island but was rare on the mainland in summer, with ―scattered pairs‖ breeding throughout the southern provinces. By the time of Moores & Park (2009), the species was no longer present in Incheon or Seoul, or anywhere in the central part of Korea, and it had been lost as a breeder from Jeju. Instead it was a very local breeding resident only in the far southeast of the ROK, and a fairly uncommon migrant through YSBR islands.

2.5.7.5 Great Knot Calidris tenuirostris Great Knot (4, 3, 2, 2) was reassessed as Probably Decreasing. The species was almost entirely overlooked by survey effort before the 1980s due to habitat preference (typically shared in the ROK with Red Knot: Long et al. 1988; own data). Both knot species were considered as ―rare‖ by Austin (1948), and uncommon by Gore & Won (1971) with likely only ten or so records of either species to that time. Following survey work of estuarine areas in the 1980s (Piersma 1985; Long et al. 1988) and subsequently (Kim et al. 1997; Moores 1999; Yi 2003, 2004), Great Knot was assessed as probably the most numerous shorebird in the ROK with an estimated 150,000-248,000 staging during northward migration and 101,000-160,000 staging during southward migration (Yi 2003, 2004; Moores 2006). At the beginning of the twenty-first century, Great Knot therefore met criteria for assessment as abundant (―1‖, or >100,000 individuals counted or estimated each year: Moores & Park 2009). However, it was described only as ―common‖ by Won (2000). This was despite its‘ being equally common as or more numerous during both northward and southward migration than Dunlin Calidris alpina – a species Won (2000) did describe as ―Abundant‖. During the 2000s, Great Knot declined massively within the ROK as a 87

result of reclamation (Chapters 4 & 5). There is no evidence that the species increased during the 1990s before declining catastrophically in recent years. Rather, what little evidence there is suggests that the species has probably been decreasing for several decades. Piersma (1985) counted 1,200 Great Knot in the Nakdong Estuary in mid- September 1984; 388 were recorded in the same area in September 1998 (Moores 1999b); and only eight were counted there in September 2005 (WBK 2005). Great Knot has clearly decreased in the period between Won (2000) and Moores & Park (2009). However, the method of number-interpretation used in this analysis requires a two-number downward change (e.g. from 1 to 3) during the past century to trigger an assessment as ―Decreasing‖ over the long-term.

2.5.7.6 Red Knot Calidris canutus Red Knot (4, 3, 3, 3) was reassessed as Probably Decreasing. This species was, like Great Knot, greatly overlooked before recent survey effort. It is, however, much less numerous than Great Knot in the ROK, and apparently more or less confined to a few west coast sites (Long et al. 1988, Moores 2006). The first intensive shorebird count effort, focused on four main northwest sites (though covering several other intertidal areas along the west and south coasts) found only between 576 and 666 Red Knot in total, most within Great Knot flocks (Long et al. 1988). The only counts of more than 1,000 in the ROK listed by Park (2002) were 2,000 at Namyang Bay in May 1993 and 1,400 in April 1998 at the Dongjin Estuary. During the 2000s, both of these sites and all other sites known to have supported concentrations of more than 100 Red Knot (i.e. Yeongjong Island, Asan Bay and the Mangyeung Estuary) have either been completely or largely reclaimed (Chapters 3-5). In consideration of the Great Knot‘s trend, and both species‘ dependence on the same areas, the Red Knot has also been reassessed as having a Negative Population Trend.

2.5.7.7 Spoon-billed Sandpiper Eurynorhynchus pygmeus The Critically Endangered Spoon-billed Sandpiper (3, 3, 3, 4) was reassessed as Decreasing rather than Probably Decreasing. Austin (1948) described the species as ―uncommon‖. He nonetheless cited 14 ROK specimens - one more than the combined total of Great Knot and Sanderling specimens at that time. He also overlooked at least two more specimens (Y10-11092) now housed in the Yamashina Institute in Japan, collected in 1925. Like Spoon-billed Sandpiper, the largest concentrations of both Great Knot and Sanderling in the ROK have been recorded within extensive and 88

dynamic estuarine systems which remained very poorly explored by ornithologists until more recently. Earliest survey effort of suitable habitat resulted in a count of ―several hundred (Spoon-billed Sandpiper) on the mudflats in the Naktong Delta on 18-20 September, 1970‖ (Gore & Won, 1971: 233). While this 1970 count was re- presented more conservatively as 200 in Long et al. (1988) and 215 in Park (2002), it still remains the highest count of the species in the ROK, and as high (or higher) than a count of 202 in Bangladesh, claimed as the highest-ever single-site count globally by Bird et al. (2010). In contrast, there has been no peak count of >10 in the Nakdong Estuary in the past two decades (Birds Korea 2010a). In the late 1990s, peak counts of 180 (on September 6th 1998) and 150 (on September 28th 1999) were claimed at the Mangyeung Estuary; 100 (on September 29th 1999) were also claimed at the adjacent Dongjin Estuary (Park 2002, Barter 2002). Both estuaries are within the now- reclaimed Saemangeum. With seawall closure in 2006, the number of Spoon-billed Sandpipers there, and globally, has continued to decline (Chapters 4-5).

2.5.7.8 Ancient Murrelet Synthliboramphus antiquus Ancient Murrelet (2, 1, 1, 1) was reassessed as Probably Decreasing. There is no evidence of increase to support a status assessment of Probably Increasing as suggested by the series of Abundance Numbers. The species has instead been very poorly covered by survey effort until recently and there is evidence both of recent decline in the Yellow Sea breeding and non-breeding population (Chapter 6) and of an increase in winter mortality in the East Sea. Earlier, Austin (1948) cited lighthouse keepers‘ accounts that in the 1930s ―several hundred eggs may be collected in a day‖ on Chilbal Island (close to the Seabird Southern Transect in Chapter 6). Similarly, Ancient Murrelet used to breed in the 1930s in large numbers on islands in Qingdao off Shandong Province (China), with ―thousands of murrelet eggs…collected and salted each year‖ (Qiao et al. 2006). The present status of Ancient Murrelet off Qingdao was left unresolved by Qiao, who did not find the species in survey of 14 islands in July (see Chapter 6, Section 6.3.5.2 for commentary on its seasonal distribution in the Yellow Sea). However, Park (2002) only found ten Ancient Murrelet in a two-day survey of Chilbal Island in May 1999, and seven during a five-day survey in 2000. By 2008, a survey of breeding birds on Chilbal Island reportedly failed to find any breeding Ancient Murrelet at all (Lee et al. 2008). The species is often found oiled in the YSBR (Birds Korea 2010a) and along the east coast in the boreal winter (pers. 89

obs.), and a recently-introduced double-net system of gill fishing is believed responsible for mass kills of many hundreds or even thousands of Ancient Murrelet in the East Sea in the late 2000s (Kim Jin-Han, Ministry of Environment, pers. com. 2010).

2.5.7.9 Brown-eared Bulbul Microscelis amaurotis Brown-eared Bulbul (2, 2, 2, 1) was reassessed as Increasing (rather than Probably Increasing), based on its northward range expansion and its change from a species described by Austin (1948: 199) as a ―not uncommon winter visitor to the southern half of Korea‖ to one that is both abundant and resident in the ROK, and widespread as a breeding species in the DPRK everywhere except the north-eastern provinces (Tomek 2002: 32). As summarised by Duckworth & Moores (2008), the ―Brown- eared Bulbul was summering at least locally in the mainland southern provinces in the 1930s, becoming more widespread in the 1950s–1960s, and is now common all year in Korea south of c. 40° N, including the cities of Pyongyang and Seoul … Its urban occurrence, conspicuousness to eye and ear, and the evident familiarity of some historical observers with the species, suggest a genuine major range expansion on the Korean mainland‖. The increasing trend suggested by historical literature appears to be continuing in the ROK. Analysis of data in NIBR (2010) indicates that the species has increased 31% in the past 16 years in 406 randomly-selected quadrats.

2.5.7.10 Barn Swallow Hirundo rustica Barn Swallow (2, 1, 1, 1) was reassessed as Probably Decreasing, rather than Probably Increasing. Austin considered the species to be only a common summer resident, perhaps in part a reflection of his not being present in Korea during most of the breeding season. His near-contemporary Wolfe, who spent from February 1946 to July 1947 in Korea, described the Barn Swallow as an ―Abundant summer resident. The swallows top the list of the few common birds in Korea...They are abundant around all of the villages‖ (Wolfe 1950). The species remained abundant through to the beginning of the 1970s at least. Gore & Won (1971: 299) described the species as an ―Abundant summer visitor and passage migrant‖, with ―Huge numbers‖ gathering at roosts, including one roost in Seoul ―estimated to hold up to 100,000 birds each night from July-October‖. In recent decades, there have been no reports of roosts of comparable size. Rather, there has been a growing body of evidence, some anecdotal 90

and some based on count data, suggesting a rapid decline. Analysis of data in NIBR (2010) by the author reveals a decline of 27% between 2000 and 2010 in the 406 quadrats.

2.5.7.11 Eurasian Tree Sparrow Passer montanus Eurasian Tree Sparrow (1, 1, 1, 1) although still widespread and numerous was reassessed as Probably Decreasing rather than Stable or of Unknown Trend. Austin (1948) described the species as ―the common, door-yard bird of Korea, an abundant permanent resident everywhere‖, and cited ―Cumming (1933, 19) who wrote: ‗…easily the commonest bird in Korea. It may be found around the villages all the way from seaside to the remotest mountain valleys, ubiquitous and assured‘‖. At present, the species remains one of the most numerous small landbird species in urban areas and in agricultural landscapes. However, anecdotal evidence of recent decline and loss as a breeding species from some localities is supported by analysis of data in NIBR (2010). This shows a decline in Eurasian Tree Sparrow of 49% in the past 15 years and of 80% since 1988 in 406 randomly-selected quadrats.

2.5.7.12 Rustic Bunting Emberiza rustica Rustic Bunting (1, 1, 1, 1) was reassessed (conservatively) as Probably Decreasing. While it remains one of the more numerous landbirds in agricultural landscapes in the boreal winter, it is apparently much less numerous at present than in previous decades. Austin (1948: 267) described it as a ―common spring and autumn transient in the northern provinces, and an abundant winter visitor from Kyonggi Do southward‖ and ―found it by far the commonest of the wintering small birds in the Suwon area. When you encountered Fringillids at all, you found Rustic Buntings. From December through March flocks numbering upwards of 500 birds lived among the weeds‖. Gore & Won (1971: 411) provided evidence of its continuing abundance at that time, stating that it was ―Present in the lowlands in very large numbers‖ with a total of 59,705 ringed between 1964 and 1968. In comparison the winter MOE Census, which covers habitats likely to support Rustic Bunting, recorded a nationwide mean of only 1,422 during the years 1999-2004. The largest flock in 2001 was of 350 (MOE 1999-2004). While the species is at present typically more numerous northward in the ROK (pers. obs.; MOE Census 1999-2009), it also appears to have undergone a steep decline in the DPRK, with eight times more ―records‖ before 1978 than between 1978 and 2000 (in Tomek 91

2002: 134-135). The majority of older and more recent records in the DPRK were made during migration. Between 2001 and 2004 Duckworth (in lit. 2011) recorded peak counts of 250 at Hyangsan (40°02‘ N, 126°10‘ E) and of 30 at Munsu (39°01‘ N, 125°47‘ E), both in late October-early November. He found much reduced numbers in the mid-winter period (peak of 46 at Hyangsan in December and of 16 in Munsu). There is at present therefore a lack of evidence to indicate increasing abundance in mid-winter in the DPRK due for example to a northward shift in abundance because of milder winters. Rather, decline in the species is also strongly suggested in Japan. Ozaki (2008) highlighted the decline of Rustic Bunting recorded at Fukushimagata and Otayama, two of Japan‘s ten primary banding stations. At Fukushimagata, more than 7,000 Rustic Bunting were banded each year in the early 1980s; by the early 1990s the number banded each year had fallen below 2,000; and by the early 2000s the number had fallen further, to probably only a few hundred each year. At Otayama, Komeda & Ueki (2002) reported that a total of >20,000 Rustic Bunting were banded during annual banding over a 17-day period in October and November between 1973 and 1996. However, the vast majority of these birds were banded in the 1970s and 1980s, and the annual number of Rustic Bunting banded there had fallen by c. 90% by the 1990s.

2.6 DISCUSSION 2.6.1 Is there Evidence of a Decline in Avian Biodiversity in the ROK? There is a growing urgency in the ROK, as elsewhere, to assess the status of avian biodiversity and to conserve species and habitats as set out by clear targets and exisiting obligations of international conservation conventions (including Ramsar and the Aichi Biodiversity Targets). Despite ratification of such conventions by the ROK, and an acceptance that there is a national biodiversity crisis (MOE 2012), there is still no large-scale long-term effort to monitor bird populations. Data generated by the few monitoring programs which are ongoing remain prone to bias or misinterpretation, due to inconsistencies in methodology or data presentation. As a result, there are very limited data with which to begin to assess the present distribution and population trend of many of the bird species in the ROK and the YSBR. In regions where there has been long-term scientifically-rigorous monitoring, population estimates and trend analysis can be complicated by a range of factors, sometimes requiring the rejection of earlier evidence. Despite a lack of scientific certainty, however, such assessments are often still used to help shape conservation priorities and to influence policies. 92

Conscious of Principle 15 of the United Nation‘s Earth Charter (UN 1992) the Four Assessments have therefore been analysed to provide defendable assessments of population trends in the ROK‘s bird species during the past century. The analysis aims to provide a necessarily-coarse baseline of historical status and long-term population trend, and for the present circumstances propose the best available assessments of ongoing change in the ROK avifauna. More recent research initiatives have also been used to test and to improve some of the species-level assessments. In some cases, the long-term trends identified in the historical literature are well-supported by recent research findings. However, as with the example of Barn Swallow in the UK, it is necessary to continue to test the assessments further with more robust monitoring within the ROK and through improvements in regional collaboration that can help to identify and measure trends at the population and flyway level. In total, the present analysis has revealed population trends during the past century in 239 out of 511 species. It confirms that a larger number of species have shown a Negative than a Positive Population Trend during the past century, in both regularly occurring and less regular species, and also in species of global conservation concern. This is despite biases that are considered likely to help accentuate perceived increase and to help conceal long-term decrease. Several species have also become nationally extinct, including three of global conservation concern (one before and two since 1910). More families and orders are represented by species showing a Decreasing than an Increasing Population Trend. In sum, the analysis confirms a decline in avian biodiversity and loss of some of its components in the ROK. With further interpretation, the results can also be used to start to identify some of the likely causes of this loss and decline. The results from the ROK are supported by the analysis of the more limited DPRK literature. The DPRK is a contiguous area supporting the vast majority of the same regularly occurring species. A very large percentage of species are migratory (therefore likely including many individuals moving between both nations) and the five Principal Pressures driving declines would have been largely similar in both the ROK and the DPRK until at least the late 1940s (when the Korean Peninsula became politically- divided). Long-term trends suggested by the results should therefore be similar in both nations if the methods of interpretation are appropriate. Based on a conservative interpretation of Tomek (1999, 2000) and Duckworth (2004, 2006) the results show that of the 112 species that show an obvious trend in the DPRK that are also regularly 93

occurring in the ROK, the majority do indeed show similar trends in both nations. In addition, in the DPRK there are twice as many species with a Negative than a Positive Population Trend. The greater proportion of species with a Negative Population Trend in the DPRK than the ROK might be an artefact of the different methods used to detect trends; or it might be the result of even greater pressures on some habitats in the DPRK, including on agricultural areas and lowland forests.

2.6.2 Underestimating Declines Analysis of data in NIBR (2010) and comparison with regional or global status species assessments provided by Wetlands International (2006) and BirdLife International (2011) suggest that the present analysis underestimates species‘ decrease, and overestimates species‘ increase. Fifteen widespread species monitored by the NIBR during the 2000s showed a population trend: 12 declined and only three increased. Wetlands International (2006) included population trend assessments at the global or flyway level for 69 waterbird taxa found in the ROK listed by Moores & Park (2009). Of these, 53 are regularly occurring and 16 are less regular species. Among this total, 40 were classified by Wetlands International (2006) as ―Decreasing‖, eight as ―Stable‖ and only nine as ―Increasing‖. Almost half of the ―Decreasing‖ species (19) are considered by the present analysis to be Stable/Unknown in the ROK. In both the NIBR research and the Wetlands International estimates, some of the difference can be attributed to the difference in time baselines, much shorter in NIBR (2010) compared with the present analysis, and in some cases unknown for Wetlands International (2006), as it was not ―possible to standardise the time base for the trend‖ in the latter source. Further differences are also likely to be caused by different trends in different parts of the range shown by the same or different populations. BirdLife International assessments are based on long-term monitoring programs, specialist literature and expert opinion. BirdLife International (2011) provides contemporary global-level trend assessments of 226 of the 365 regularly-occurring species covered by the present analysis (with the remainder comprised largely of poorly-known Passeriformes ―suspected to be stable in the absence of evidence for any declines or substantial threats‖). Of these 226 species, approximately two-thirds (149) are assessed as showing a decreasing trend and only 26 an increasing trend, with the remainder stable: i.e. many more of these species are showing a decreasing trend at the global level than appear to have decreased based on the Four Assessments. In total, 27 94

species show a contradictory trend between the Four Assessments and BirdLife International (2011). Twenty-five of these appear to be showing a Positive Population Trend in the ROK while decreasing globally. It seems likely that a few of these species have indeed shown genuine long-term population trends in the ROK that are at odds with their more recent global trend. These include species that have experienced northward range expansion into the ROK during the past century (e.g. Black-crowned Night Heron Nycticorax nycticorax and Intermediate Egret Egretta intermedia), and two sedentary species (Marsh Tit Poecile palustris and Varied Tit Poecile varius). The brevirostris subspecies of Marsh Tit (sometimes split as Asian Marsh Tit: Brazil 2009) and Varied Tit are both confined to East Asia; and both have likely increased within the ROK due to improvements in forest habitat. This is also plausible for at least two migrant species that are also ecologically-dependent on forest and are tolerant of plantations (Goldcrest Regulus regulus and Eurasian Siskin). Several migratory species assessed as Stable or of Unknown Trend, however, have likely had declines concealed by an increase in observer activity in their preferred habitats. Such species include some that are confined to inshore and open sea areas (e.g. Harlequin Duck Histrionicus histrionicus, Horned Grebe Podiceps auritus, Short-tailed Shearwater Puffinus tenuirostris, Black-legged Kittiwake Rissa tridactyla and Rhinoceros Auklet Cerorhinca monocerata); coastal areas (Marsh Sandpiper and Common Reed Bunting Emberiza schoeniclus); or offshore islands (e.g. Short-toed Lark Calandrella brachydactyla and Thick-billed Warbler Acrocephalus aedon). An improvement in research effort in appropriate habitats is therefore required to establish a baseline through which trends of these species, if any, can be identified.

2.6.3 Use of the Results 2.6.3.1 In Present Form The results in their present form have value for identifying some of the large-scale population changes that have taken place in a large number of species over the past century. They therefore contribute to the improvement in the knowledge base on biodiversity status and trend called for by Target 19 (CBD 2010). Population trends in many species remain poorly-understood, however, and it also remains difficult to determine causes of trend within the ROK for most species. Processes leading to changes in population are often complex and dynamic. However, the results in some cases make it easier to start to suggest probable causes. For 95

example, Black-crowned Night Heron and Eastern Cattle Egret showed an Increasing Population Trend in the ROK during the past century. Both are largely-distributed to the south and southwest of the Korean Peninsula, as are many other of the Increasing species. It therefore seems likely that they were able to expand their range northwards into the ROK in the twentieth century due to a warming climate. However, reduced counts of these species on offshore islands during migration in the 2000s and other anecdotal evidence suggest that both might now be decreasing in the ROK. As they both depend largely on agricultural areas it is possible that the intensification of agriculture (including the excessive use of chemicals) might now be reversing their climate-driven gains. The same agricultural intensification has also likely contributed to declines in a large number of species, including some of global conservation concern (e.g. Japanese Quail, Oriental Stork) and other formerly more numerous species (including Watercock, three lark species, Barn Swallow, Tree Sparrow and Rustic Bunting). At least 13 of the Decreasing species (and many more species showing a Negative National Trend) are strongly associated in the ROK with rice- fields or scrubby grassland, and several more with ―open woods, checkered with small areas of wet grass which supported an abundant frog population‖ as described by Wolfe (1950). Such areas in the ROK have now been largely lost to agricultural intensification and urban sprawl. Abundance Numbers within the Four Assessments therefore can be, with care, used to suggest groups of species which might have been most susceptible to decrease during the past century. The drivers of decline of a small number of species can also be suggested, though for many there is sill a need to improve understanding of both historical and contemporary Principal Pressures and for more focused and robust long- term research.

2.6.3.2 Decrease Susceptibility Index The development of population trend assessments is labour-intensive and time- consuming. In order to assist decision-makers in the ROK in developing appropriate conservation responses within the present decade, a more rapid method for gathering and organising information on species in decline needs to be developed. At present, BirdLife International has responsibility for developing species-level factsheets on all bird species globally, for use by the IUCN and for conservation conventions. As part of the assessment process, they maintain publicly-accessible online fora on globally- 96

threatened bird species (BirdLife International 2012). These English-language fora present contemporary best knowledge on species and invite expert opinion to assist in the process of evaluation of those species considered most likely to be undergoing a substantial change in status. For example, for the period 2010-2011, information on 26 bird species found in Asia was requested in the fora. This resulted in 11 provisional changes in status, and left five status assessments unchanged and ten species assessments left pending. Between February 2011 and February 2012, the fora requested information on 37 bird species found in Asia. Only nine of these species have been recorded in the ROK, with six of these regularly occurring complete migrants, three of which (White-winged Scoter Melanitta deglandi, American Scoter Melanitta americana and Long-tailed Duck Clangula hyemalis) were identified by this research as having a Negative National Trend, and three (Greater Scaup Aythya marila, Streaked Shearwater and Swinhoe‘s Storm Petrel) an Unknown Trend. There was a mean of seven references (range 3-11) from the scientific literature for each of these six species cited in the fora accounts. However, in several cases the published evidence and submitted expert comments were contradictory to some extent, and thus likely to require much further subsequent interpretation by the fora managers. In contrast to the small number of species covered by these fora, the present research conservatively estimated that 128 regularly occurring species show evidence of a substantial negative trend during the past 100 years, including 25 out of 50 species of global conservation concern. More of the 285 species with unclear or unknown trend in the ROK are also suspected of decreasing rather than increasing. In order to influence conservation policy within the present decade, a framework additional to that presently provided by BirdLife International fora is required, to help better organise existing information on these species and on likely drivers of their decline. This framework might best include information on the five Principal Pressures both within the ROK (Chapter Section 1.5) and also within species‘ breeding, staging and non- breeding areas. To be a valuable planning tool, it would also need to anticipate other variables that are considered likely to make certain species more susceptible to decrease than others. In 1995, Gaston & Blackburn advocated the development of simple rules to ensure recognition of species potentially at most risk of global extinction. Research has also helped to identify variables that are associated with extinction risk (Owen & Bennett 2000). Furthermore, better-researched regions (including Europe and Australia) can 97

also help to provide insights into likely causes of decline or loss of some of the ROK‘s bird species. Approximately 170 of the ROK‘s regularly occurring species also breed in the western Palearctic (BirdLife International 2011, Svensson et al. 1999) and 52 of the 59 species included in the original 2007 annex of the ROK-Australia Migratory Bird Agreement also occur regularly in Australia. For many of these species, population trends and/or causes for such trends at the regional or global level have already been identified. However, much of this research remains difficult to access in the ROK and elsewhere in East Asia (in part due to language difficulties), and it has not been modified to allow wider extrapolation in ways that can help to influence policy and decision-making. Potentially, a ―Decrease-Susceptibility Index‖ could contain a range of information on threats and other variables scored on a categorical scale. Such an index (developed further in Chapter 9) could then be used to supplement existing initiatives and help in the short-term to interpret the susceptibility of a large number of species to threats and their decline relative to other species. In summary, the results of the research presented in Chapter 2 are useful for identifying major information gaps, by clarifying which species are poorly-known in the ROK literature. At present, there are many poorly-known species especially in intertidal wetlands, inshore and offshore waters, and on offshore islands. For at least some such species (including many shorebird species, gulls, pelagic species and migrant landbirds) focused survey work and a reduction in the time base for identifying a population trend (e.g. to a decade only) will likely help to reveal otherwise-hidden population trends. This is especially if a more sensitive method of measuring change in abundance for such species can be developed. While this initial analysis is helpful in establishing that avian biodiversity has declined in the ROK during the past century, further survey effort, analysis and organisation of information is required to close some of the more important information gaps, both on species and their habitats. This is the focus of subsequent chapters.

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Chapter 3

INTERTIDAL WETLAND: RECLAMATION, AND ESTIMATES OF REMAINING AREA IN THE ROK

ABSTRACT Intertidal wetland in the ROK supports internationally important concentrations of several globally-threatened bird species and a substantial number of the migratory shorebirds of the East Asian-Australasian Flyway (EAAF). Reclamation of intertidal wetland in the ROK has a long history, but accelerated greatly during the twentieth and into the present century. In 2006, a research body within the former Ministry of Maritime Affairs and Fisheries (MOMAF) predicted that less than 112,000ha of intertidal wetland would remain nationwide by 2011. Based on this assessment, an estimated 75-80% of historical intertidal wetland area would have been lost to reclamation by 2011. However, in 2009 the Fourth National Report to CBD stated that 255,020ha of coastal wetland ―currently‖ remained (ROK 2009). Subsequently too, MOE (2012) stated there were 248,940ha of tidal-flat in the ROK. In 2010, in consideration of the importance of intertidal wetland to avian and other biodiversity and of the range of estimates provided in government reports, we measured the remaining area of natural and near-natural tidal-flat using ImageJ and ArcView. Almost all remaining areas of tidal-flat could be assessed. We estimated that during the late 2000s there were 105,000-112,000ha of natural and near-natural tidal-flat at low tide remaining in the ROK. This estimate is in accordance with earlier predictions. It suggests that by 2010 there had been a loss of approximately 75% of historical tidal- flat area in the ROK, including two-thirds of that which remained in 1987. The recent and rapid loss of intertidal wetland in the ROK, including sites known to be internationally important for waterbirds, is considered likely to have resulted in the decline of several species of shorebird and other waterbird species ecologically- dependent on the same habitat. Despite obligations to conserve intertidal wetland and the biodiversity that is dependent on it made explicit through conservation conventions, large-scale reclamation and conversion of intertidal wetland in the ROK still continues.

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3.1 BACKGROUND AND AIMS 3.1.1 International Importance of Intertidal Areas to Avian Biodiversity The Yellow Sea coast is extremely important for threatened waterbirds (BirdLife International 2003). In the ROK, the combination of shallow coastal slope and high tidal-range has contributed to the formation of very wide intertidal wetlands. These are mostly comprised of unvegetated tidal-flat, in some areas with creek systems, salt- marsh and small islands of sand or shingle. Several globally-threatened bird species are ecologically-dependent on intertidal wetland, and three of these breed in the ROK: the Vulnerable Saunders‘s Gull (which is endemic as a breeder to the Yellow Sea), and the Endangered Black-faced Spoonbill and Vulnerable Chinese Egret (which are both near-endemic breeders to the Yellow Sea) (BirdLife International 2011). The vast majority of the Yellow Sea‘s shorebirds (from hereon defined as Charadriiformes excluding Turnicidae, Laridae, Stercoraririidae and Alcidae) are also ecologically dependent on intertidal wetland during migration and the non-breeding season. Barter (2002) listed 36 shorebird species in the Yellow Sea in concentrations during migration that were ―internationally important‖ (defined throughout in accordance with Ramsar 2005). All 36 species use intertidal wetland habitats and at least 27 are ecologically dependent on them during migration. Such species are not distributed randomly. Most form internationally important concentrations in preferred wetlands. Dependent upon delineation, approximately 20 internationally important wetlands for shorebirds were identified in the ROK (Moores 1999; Yi 2003, 2004). The eight most important shorebird sites in terms of peak counts (Dongjin Estuary, Mangyeung Estuary, Namyang Bay, Yubu Island, Yeongjong Island, Asan Bay, Ganghwa Island and Cheonsu Bay: see Table 1.3.2 in Chapter One) are all in the Yellow Sea Blueprint Region (YSBR). In the late 1990s/early 2000s these eight wetlands supported an estimated 84% and 87% of the ROK‘s shorebirds on northward and southward migration respectively (Yi 2003, 2004).

3.1.2 Reclamation Process The ROK is a signatory to Ramsar and CBD and therefore is formally committed to conserving internationally important wetlands and the biodiversity that depends upon them. However, many internationally important wetlands in the ROK have been degraded and lost to development, and many other areas remain threatened directly and 100

indirectly by human activities. These areas include all eight of the nation‘s most important shorebird sites listed above (see: Chapter 5, Table 5.2.1). The leading cause of loss of intertidal wetland is reclamation (i.e. the conversion of natural wetland into dry land and artificial wetland by mechanical means). Many recent reclamation projects in the ROK have entailed the construction of outer seawalls across the mouths of bays and estuaries, and landward construction of inner dikes. In several projects (as at Saemangeum: Chapter 4), outer seawalls have been built into deeper water, restricting further seaward formation of tidal-flats. The lowest-lying areas behind the outer seawall are then flooded to be used as freshwater reservoirs (―reclamation lakes‖); and the slightly elevated areas, protected by inner dikes and drainage systems, are then changed to land. This reclamation process can convert whole estuarine systems into modified, heavily-managed landscapes. Large reclamation projects can take years or even decades to complete. Nonetheless, the process is far more rapid than natural processes of accretion. Accretion rates in the YSBR are slow and most new sediments in Korean tidal-flats come from Chinese rivers (Lee & Chough 1989). The importance of sediment input from Korean rivers has likely been reduced further by estuarine barrages (Moores et al. 2001), and rivers in China are also undergoing changes that will greatly reduce the input of sediments into the Yellow Sea (Barter 2006). Reclamation therefore causes a substantial loss of intertidal area, and a loss of biodiversity dependent upon intertidal wetlands (Sato 2006, Rogers et al. 2006a, Hong et al. 2007). Reclamation in the ROK has been considered more cost-effective than purchasing land that already existed (Long et al. 1988), in part because intertidal wetlands lack strong legal protection. The administrative process for most large-scale reclamation projects (until the passage of Special Laws and amendments to the Public Waters Reclamation Act in 2007 and 2008) involved several legal procedures and different government bodies at different stages of the project (Kim 2008). For example, the ministry responsible for maritime affairs first identified areas suitable for reclamation; the ministry responsible for infrastructure then led construction of seawalls and drainage systems; and the ministry responsible for agriculture then had primary responsibility for the land being constructed. This administrative chain has likely contributed to confusion over the area of intertidal wetland remaining and of the area that has been reclaimed. The most accessible and perhaps well-informed estimates of change to the area of intertidal wetland are therefore found in specialist literature 101

focused on the impacts of reclamation on avian biodiversity and on benthos. Most of this literature is based on contemporary government data and site visits, and aims to assess habitat change rather than changes in jurisdictional responsibility.

3.1.3 History of Reclamation The ROK has a long history of reclamation of intertidal wetland, dating back to the 13th Century (Long et al. 1988). However, large-scale reclamation started only in the 1920s (Koh 1999). By 1941, 40,000-41,000ha of mostly upper tidal-flat areas including salt-marshes had been reclaimed (Long et al. 1988, Koh 1999). In 1964, there were still an estimated 390,500ha of tidal-flat (Kim 2010b). However, the rate of reclamation then increased further, and 40,000ha were reclaimed in the 1960s and 1970s (Koh 1999). By 1983, 97,000ha had been reclaimed (Long et al. 1988). In the early 1980s, a national masterplan (1984-2001) identified 66.5% of the remaining 630,000ha of ―coastal wetlands along the west and south coasts‖ of the ROK as fit for reclamation by 2001 (NEDECO 1985, in Long et al. 1988). These 420,000ha of ―coastal wetlands‖ were comprised of both intertidal wetlands (approximately 320,000-340,000 ha) and adjacent shallow sea areas. According to MOMAF data published in 1998, 81,050ha of ―mudflat‖ and ―intertidal habitat‖ were reclaimed between 1987 and 1997. This resulted in 239,300ha of intertidal wetland remaining in 1997 (in Yi 2003, 2004; UNDP-GEF 2008; Hong et al. 2010). Between 1996 and 1999, approximately 62,000ha of coastal wetland were newly-diked and 76,000ha (20%) were undergoing development (Koh 1999). Je Jong-Geel in 1999, then working within a research section of MOMAF, estimated that if current plans were executed ―more than 80% of intertidal mud flats‖ would be reclaimed by the end of 2010 (in Choi et al. 2010b). Moores (2006) provided a summary of a MOMAF statement (published in the Hankyoreh, November 6th 2006) which stated that tidal-flat area had by then declined to 225,000ha (a further loss of 14,000ha in seven years). However, there were still 267 reclamation projects ongoing (including the 40,100ha Saemangeum reclamation). The MOMAF statement therefore estimated that with ongoing and future reclamations which had been approved (targeting a further 113,600ha of intertidal wetland) 44.5% of remaining tidal-flat would be lost within the next five years. This would result in less than 112,000ha of tidal-flat remaining by 2011. Moores (2006) calculated that this would represent a decline by 2011 of 75% or more from a pre-reclamation historical 102

area of an estimated 460,000ha of intertidal wetland. This estimate of historical area was calculated from the area published as reclaimed since the 1920s as listed above (a total of 305,000ha). It also included a coarse estimate of lost intertidal wetland area caused by estuarine dam construction (most in the 1980s: KWRC 2004); by historical bund construction along tidal stretches of large rivers; by numerous small local reclamation projects; and some pre-twentieth century reclamation, which was assessed from site visits and the shape of the coastline in maps. This area was estimated to total at least 45,000ha (unpublished data). Almost all intertidal wetland is tidal-flat. The difference (if any) between the estimates of historical intertidal wetland loss of >75% in Moores (2006) and of 80% of tidal-flat in Je (1999) is probably because of the consideration of additional offshore and upstream intertidal areas rather than because of the difference in habitat description. In 2006, previous estimates of tidal-flat loss were contradicted by a report published jointly by MOMAF and the Ministry of Environment (MOMAF/MOE 2006). This report stated that coastal wetlands (―almost tidal mud-flat‖) had decreased only 20% in area by reclamation between 1987 and 2005. The MOE-led ROK Fourth National Report to CBD in May 2009 then stated that 78% of the coast remained natural; that there were ―currently‖ 255,000ha of coastal wetland remaining (210,970ha of which were on the west coast); and that only 20% of intertidal wetland area had been lost since 1987 (ROK 2009). Based on the Report on the Outcome of the Land Use Map of Tidal Flats (MLTM 2008) and the National Biodiversity Strategies and Action Plans (Anon 2009), MOE (2012) further asserted that were still 248,940ha of ―tidal-flat‖ nationwide, with 208,000ha on the west coast. Both ROK (2009) and MOE (2012) thus intentionally excluded the Saemangeum reclamation (impounding almost 30,000ha of intertidal wetlands and 10,000ha of sea-shallows, including two Important Bird Areas totalling 17,042ha) and the Namyang Bay reclamation (impounding 6,675ha of an Important Bird Area) where outer seawalls were completed in 2006, in addition to numerous other ongoing large-scale reclamation projects. Both also excluded newly-approved projects. These included a further 1,600ha of reclamation approved in March 2009, several months after agreement to Ramsar Resolution X.22 which made explicit the ROK‘s formal commitment not to approve any more large-scale reclamation (Birds Korea 2010a).

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3.1.4. Aims of the Present Study We considered the estimate of tidal-flat area in ROK (2009) inappropriate for conservation-planning. There was no clear description of the methodology used to develop the estimate, so that the accuracy of the estimate could not be tested. The estimate also contradicted consistent estimates provided by government bodies in the late 1990s. Our study aimed to provide an assessment of the area of remaining unimpounded (i.e. natural and near-natural) tidal-flat in the ROK in the late 2000s based on analysis of publicly-available imagery. In order to improve conservation opportunities for tidal-flats and shorebirds, we then provided preliminary results of this research in Birds Korea (2010a) to help inform decision-makers at the tenth meeting of the conference of the parties to the Convention on Biological Diversity (CBD COP 10). We then refined our results and commentary further in 2011-2012, in part to help inform larger-scale research initiatives on the conservation status of East Asian intertidal wetlands and shorebirds, including IUCN (2011).

3.2 METHODS Since only 84ha of forested intertidal wetland has been identified in the ROK (and that confined to the Han River: Park et al. 2008), we defined tidal-flat as barren, exposed or evidently exposed mud/silt/sand-flats at low tide with no or little apparent vegetation. This definition in practice included intertidal habitats classified by Park et al. (2008) as ―Sand, Shingle and Pebble Shores‖, estuarine areas, ―Intertidal mud‖ and sandflats, and most intertidal salt-marsh. Our definition excluded all densely-vegetated areas (as they were apparently above the influence of spring high tides), semi-natural intertidal areas that were impounded behind seawalls (even if some level of tidal influence might remain, such as within the Saemangeum reclamation area), coastal brackish/saline lagoons (i.e. reclamation lakes) and beach lying above high-water. We conducted a preliminary review of satellite images. This review, literature (including ROK 2009), and shorebird survey confirmed that there are no substantial intertidal areas remaining on the east coast, and that the west and south coasts possess the vast majority of remaining tidal-flat nationwide. We then divided coastal and island areas of the west and south coasts into 10 minute by 10 minute grids (n=338). We did not measure remaining tidal-flat area on Jeju Island as the amount expected there (based on previous survey work and on satellite images) is minimal compared to that on the mainland (in total <500ha). In addition, tidal-flat area within the Han-Imjin 104

River which forms part of the border with the DPRK was not measured due to lack of imagery at sufficient resolution. Based on coarse estimates made during site visits the area not covered by images was probably between 2,500ha and 4,500ha in total. For all remaining areas (i.e. the vast majority of intertidal wetland nationwide) we imported publicly available, modern, high-resolution imagery from Daum maps (www.daum.net) into the program ImageJ 1.43 (NIH, Bethesda, MD, USA). Based on knowledge of tidal-flats in the images (e.g. in the Incheon area, Geum Estuary, Mokpo area and Nakdong Estuary) and on a comparison with our own images taken of some sites during survey work (2006-2010), the Daum images were assessed as (1) taken in the mid-late 2000s; (2) taken at low tide; and (3) adequate for measuring tidal-flat area. Image resolution was sufficient at a zoom height of between 260m (most images) to a maximum of 520m to identify features typical of areas which either were, or were predicted to be, exposed at low tide (e.g. tidal creeks and rivulets, a reflective sheen on wet mud, and/or a lack of infrastructure) and areas that would not be exposed at lowest tide (e.g. submerged mud lacking rivulets or with mariculture or boats). In most images (as in Figure 3.1 showing the inner Geum Estuary, immediately adjacent to the Geum River Estuarine barrage) the submerged outer edge of tidal-flats was made apparent by a change in colour as water depth increased.

Figure 3.1 Low resolution scan of Daum.net image of the inner Geum Estuary divided into four areas. Area 1 shows tidal-creeks and rivulets to the north of the river. These are different in colour from areas known to be sub-tidal (green-toned), and turbid areas that include small patches of tidal-flat exposed only occasionally (on lowest spring tides) in Area 2. Area 4 is impounded freshwater behind the estuarine barrage. Area 3 (in olive-green) shows the area measured as tidal-flat at lowest tide on the southern side of the river. ―X‖ marks the location where the image in Figure 3.2 (below) was taken.

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. Figure 3.2 Area 1 at low-tide, looking towards the Geum Estuary barrage (2006).

Natural and near-natural tidal-flats (―tidal flats‖) were identified in 88 grids. The area of tidal-flat within each of these grids was then measured from images independently by two different researchers. If there was a >5% difference in measurement, the images (n=20) were then reviewed and reassessed until consistent results were achieved. These tidal-flat areas were then summed within grids and grid values were mapped using a colour scalar in the geographic information systems program ArcView (ESRI, 2009). Tidal-flat values were then summed across all grids to provide a nationwide estimate (± error rate: see below). After completion of tidal- flat measurement in all grids a random sub-sample of twenty grids was selected and tidal-flat re-measured. We compared total tidal-flat estimates from the first estimate with those of the re-sampled estimate to measure observer error rate where: measurement 1 = ∑(tidal flat area from the first estimate in the 20 re-sampled grids) measurement2 = ∑ (tidal flat area from the second estimate in the 20 re-sampled grids)

Using our observer error rate we multiplied this by our nationwide estimate to calculate a ± error rate range for remaining tidal-flat area in km2.

3.3 RESULTS Nationwide we estimate that in the late 2000s there were approximately 103,900ha ± 3,100 ha (1,039 ± 31 km2) of tidal-flat at low tide remaining in the ROK, excluding some parts of the inner Han-Imjin Estuary and Jeju (<5000ha in total, as above). Of the measured total, 90% (or 93,700 ± 2,800ha) was along the west coast/within the YSBR. 106

The total estimated area of 105,000-112,000ha of remaining tidal-flat in the ROK suggests a loss of approximately 75% of historical intertidal wetland. Based on the MOMAF estimate of 320,000ha of tidal-flat area in 1987 (in Yi 2003 and Hong et al. 2010) this suggests a loss of approximately two-thirds of remaining tidal-flat area between 1987 and 2010. The largest remaining areas of tidal-flat found were in the Incheon region in the northwest and in Shinan County, Muan County, Hampyeong County in the southwest, with several grids in those regions containing between 50 and 100 km2 of remaining tidal-flat (Figure 3.3). However, substantial concentrations were also found along the central west coast near Gunsan City in the Geum Estuary and in a few isolated regions of the south coast. Our estimate accords well with predictions made by Je (1999) and Moores (2006), but it is substantially lower than the estimates provided in ROK (2009) and MOE (2012).

Figure 3.3 Area of tidal-flat remaining in the ROK (mid-late 2000s).

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3.4 DISCUSSION 3.4.1 Interpretation of the Results Our analysis shows that there has been a major loss of tidal-flat in the ROK. The results are in accordance with earlier published predictions made by government bodies with responsibility for assessing reclamation projects; and with observations of habitat change made during survey work in Long et al. (1988) and especially since 1998 (Moores unpublished data). There is a huge discrepancy between our analysis and the estimates provided in ROK (2009) and MOE (2012). Some of this is based on the time baseline. Although ROK (2009) stated that ―Currently the area of coastal wetlands has been reduced by around 20%‖, the figures they cited were from 2005. It is less clear why MOMAF/MOE (2006), ROK (2009) and MOE (2012) apparently contradicted earlier assessments provided by MOMAF and used by several subsequent authors including Je (1999) within MOMAF, and Yi (2003, 2004) within MOE. In both MOMAF/MOE (2006) and ROK (2009), the area of c. 255,000ha referred to ―coastal wetlands‖. There is no clear definition of coastal wetland, nor any details on the method used to develop estimates in either report apart from a footnote in MOMAF/MOE (2006). This explains that the ―size of the coastal area was obtained by summing the areas of all coastal municipalities‖. It seems possible that reclamation lakes and semi-natural tidal-flat areas that still had limited tidal influence behind outer sea-walls (as in many of the larger reclamation projects) might have been included by both reports as coastal wetland. This is as Park et al. (2008) found no natural lagoons on the west coast of Korea but instead 42,977ha of reclamation lakes, and ROK (2009:10) included one figure showing that the area of wetland had increased 8% by reclamation. However, MOE (2012) apparently excluded reclamation lakes in their estimate of 248,940ha of ―tidal-flat‖ remaining nationwide in 2008. Some of the difference between MOE (2012) and this study might be due to continued inclusion of impounded tidal-flat and also differences in tide state. This latter difference alone seems unlikely to account for >136,000ha of tidal-flat that we were unable to detect using modern, high-resolution imagery and site visits. Improving access to accurate information is a priority if action plans, conservation policies, and legislation are to be effective in reducing the rate of avian biodiversity loss (Birds Korea 2010a). The need for an independent assessment on the area and conservation status of intertidal wetlands in East Asia, including in the ROK, was therefore formally recognised by the IUCN in 2011 (IUCN 2011). Research on tidal- 108

flat area and on patterns of tidal-flat loss in East Asia is also being undertaken by the University of Queensland. Through use of high resolution imagery and purpose- designed software, this latter research should be able to provide an independent assessment of remaining tidal-flat area and of rate and patterns of loss (R. Clemens, University of Queensland e-newsletter, in lit. 2012; D. Rogers pers. comm. 2012).

3.4.2 Impacts on Shorebirds Migratory shorebirds lead especially energy-demanding lives and require adequate feeding sites along the length of their migrations (Piersma & Baker 2000); many have delayed maturity, and short breeding seasons; and their recruitment rate is limited by having single clutches of four or fewer eggs. Most shorebirds in the ROK depend on tidal-flats for feeding (Chapters 4 & 5), and suboptimal feeding conditions during migration can result in increased mortality and decreased fecundity (Battley 2002). Even a small decrease in the rate of annual adult survival can lead to rapid and substantial declines (Rogers 2006). Research in other regions has already established that loss of feeding opportunity can lead to population declines in migratory shorebirds both at the local (Burton et al. 2006) and population level (Baker et al. 2004; Niles et al. 2008). Within the ROK, reclamation of intertidal wetland has been proven to cause massive changes to the ecology of affected intertidal areas and mass mortality of benthos, including species and genera which are eaten by shorebirds (Rogers et al. 2006a, Sato 2006, Hong et al. 2007, Choi et al. 2010b). Large-scale reclamation can affect patterns of sedimentation and tides in areas that remain (Lee 2010, Lee et al. 2010), and pollution and other anthropogenic changes to remaining areas can also lead to declines in populations of benthos (Choi et al. 2010b). Unsurprisingly, habitat loss and degradation of intertidal wetland is recognised as having contributed to the poor global conservation status of both Black-faced Spoonbill and Saunders‘s Gull (BirdLife International 2011). The East Asian-Australasian Flyway (EAAF) has a disproportionate number of shorebird species that are classified as threatened (IWSG 2003), and >80% of the EAAF‘s shorebird species with known trends are now in decline (Professor N. Davidson, Ramsar Secretariat, in lit. 2011). In total, 13 species of global conservation concern (six of which are shorebird species) and a further 25 species (15 of which are shorebirds) are found regularly in concentrations of >1% of population in intertidal wetland in the YSBR. Twenty-eight of these species are found in internationally important concentrations only in intertidal 109

wetland. The majority of individuals of these species are concentrated in a relatively small number of sites, which are clustered in the northwest (Ganghwa, Yeongjong, Song Do, Namyang and Asan Bays) and along the west coast (Cheonsu Bay and most especially the SES and the Geum Estuary) (Moores 1999a, Moores 1999b, Yi 2003, Yi 2004, Moores 2006). Eight of these species are assessed by Wetlands International (2006) as being in global decline; one as stable and one as increasing (though both of the latter two species are assessed by BirdLife International 2011 as having decreased); and the remainder as having unknown trends. However, more recent assessments by Rogers et al. (2009), Amano et al. (2010), Wilson et al. (2011) and Garnett et al. (2011) based on count data from outside of the ROK have identified declines in at least 14 of the 21 internationally important ROK shorebird species (see Chapter 9, Table 9.1). There has been a paucity of empirical studies directly linking loss of intertidal wetland in the Yellow Sea with declines in avian biodiversity. In the ROK, there is no robust national shorebird monitoring program in place; there has been no detailed research on the quality of intertidal wetland (both of that which remains and that which has been lost) for shorebirds; and no research has been conducted on shorebird energetics (with even the timing of migration of many species being poorly known before the SSMP: Chapter 4). Even formal documentation on timing and size of reclamation projects, and on remaining areas of intertidal wetland, contains numerous contradictions. However, it is now well established that many of the ROK‘s shorebird species are in decline nationally (Chapters 2, 4, 5 & 9) and on the EAAF. Some of these species (including the Critically Endangered Spoon-billed Sandpiper and the now globally Vulnerable Great Knot) are considered to have experienced a recent acceleration in decline (Zöckler et al. 2010, BirdLife International 2011, Murray 2011). It is therefore reasonable to assume that there is some level of connection between the recent and rapid loss of two-thirds of intertidal wetland in the ROK (including several of those sites known to be most important for shorebirds) and the similarly recent and rapid decline of several species of shorebird dependent on the same wetlands.

3.4.3 Conservation Obligations The ROK, by signing bilateral conservation agreements on migratory birds (including the Republic of Korea-Australia Migratory Bird Agreement, 2007) and by being a signatory to several conservation conventions (including Ramsar and CBD) 110

has formally accepted its obligation to conserve intertidal wetlands and the biodiversity that is ecologically-dependent upon them. The ROK was in 1999 one of the lead sponsors of Ramsar Resolution V11.21 (requiring contracting parties to modify policies relating to intertidal wetlands); was later singled out in Ramsar Resolution IX.15, which requested details on the impacts of the Saemangeum reclamation on populations of migratory waterbirds (see Chapter 4); and made a formal commitment through Ramsar Resolution X.22 in 2008 not to approve any more large-scale reclamation. However, large-scale reclamation projects continue to be approved (e.g. a 716ha reclamation project at Song Do was approved in March 2009), and at present include the proposed conversion of intertidal wetlands into reservoirs for tidal-power projects (as at Ganghwa: Jang 2010). More recently, CBD‘s Strategic Plan for Biodiversity 2011-2020 called by 2020 for ― the rate of loss of all natural habitats (to be) at least halved and where feasible brought close to zero‖ (Target 5) and for ―the conservation status (of threatened species), particularly of those most in decline, (to be) improved and sustained‖ (Target 12). Clearly, it is not possible to meet these targets while continuing to reclaim remaining natural intertidal wetland. There is now strong evidence of the impact of reclamation on the area of natural and near-natural intertidal wetland in the ROK. There is a need to improve the accuracy of estimates of remaining tidal-flat area, and to develop methods to measure the ecological health of such areas, including their value to shorebirds and other bird species. In the spirit of the Precautionary Principle, it is also apparent that policies and special laws in the ROK which support the reclamation of intertidal wetland need to be changed in order to conserve biodiversity and ecosystem functions and services.

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CHAPTER 4

MEASURING THE IMPACTS OF LARGE-SCALE RECLAMATION: THE SAEMANGEUM SHOREBIRD MONITORING PROGRAM (2006-2008)

ABSTRACT In the early 2000s, the Saemangeum Estuarine System (SES) was the most important staging site for migratory shorebirds in the ROK and one of the most important shorebird sites on the East Asian-Australasian Flyway (EAAF). Between 1997 and 2001, the SES supported an estimated 316,000 shorebirds during northward migration and c. 257,000 shorebirds during southward migration. This included 30% of the world‘s breeding population of Great Knot and the Yellow Sea‘s largest concentration of Spoon-billed Sandpiper. Construction of a 33-km long seawall to impound the SES started in 1991, and was completed in April 2006. Declines in some shorebird and other waterbird species in the SES were recorded from at least 2003. These declines were predicted to accelerate with seawall closure in 2006. We hypothesised that loss of the SES, a major staging site, to reclamation would cause population-level declines in one or more migratory shorebird species. To measure declines at the site level and regional level following seawall closure, we conducted the Saemangeum Shorebird Monitoring Program (SSMP) during northward migration in 2006-2008. The SSMP was designed in conjunction with a national shorebird survey conducted in 2008 (Chapter 5) and ongoing shorebird monitoring programs in Australia. For the SSMP, we gathered data on the numbers of shorebirds supported by the SES and the two adjacent wetlands of the Geum Estuary and Gomso Bay (combined, the Study Region). We conducted a series of systematic broad-scale surveys centred on spring tides. With data from multiple counts during northward migration it was possible to model migration phenology of most species. These models demonstrated that the more abundant species in the Study Region staged in the area for several weeks: it was therefore the launching point for their final migration north to the breeding grounds. As there was relatively little overlap between latest arrival and earliest departure dates of staging migrants in most species, the peak number of birds counted in each migration season was a reasonably accurate representation of the total numbers of shorebirds that 112

staged in the Study Region each year. Within the SES, based on the sum of peak counts, we recorded almost 180,000 shorebirds in 2006 and 51,560 in 2008. Within the Study Region as a whole, based on the sum of peak counts we recorded almost 264,000 shorebirds in 2006 and 164,261 in 2008. Thus we recorded a decline of almost 130,000 shorebirds within the SES and of 100,000 shorebirds within the Study Region during northward migration between 2006 and 2008. The most-affected species included Great Knot Calidris tenuirostris, with >92,000 lost from the SES and the two adjacent wetlands. The national survey in May 2008 failed to find evidence of displaced Great Knot from the Study Region at other internationally important wetlands nationwide, including all other sites known to be internationally important for the species in the ROK (Chapter 5). Research in Australia (yet to be published in full) also indicated a decline in numbers and adult survival of Great Knot after seawall closure at Saemangeum. We believe that this is the first time that a decline in a shorebird population on the EAAF has been directly linked to the loss of a major staging site by reclamation. While there was some evidence of displacement of a minority of shorebirds to adjacent wetlands following seawall close, there was no evidence to suggest that these two wetlands will support increased numbers of shorebirds long-term. Instead, further construction and conversion of formerly natural intertidal wetland into dry-land and freshwater reservoirs at Saemangeum and other internationally important wetlands in the ROK is predicted to lead to further declines in shorebirds at the site, national and population level.

4.1 BACKGROUND AND AIMS 4.1.1 The Saemangeum Reclamation By 2000, barraging of estuaries and reclamation projects had resulted in the loss of more than half of historical tidal-flat area in the ROK (Chapter 3) and only three main rivers still flowed largely unobstructed into the YSBR (Moores et al. 2001). Two of these were the adjacent Mangyeung and Dongjin Rivers. Together they formed the Saemangeum Estuarine System or ―SES‖ (centred close to 35°50' N, 126°45' E). Since 2006, these two river estuaries have also been impounded, as part of the ROK‘s largest ongoing reclamation project, ―Saemangeum‖. The Saemangeum reclamation aims to convert approximately 29,000ha of tidal-flat and 11,100ha of sea shallows into dry land and freshwater reservoirs through the construction of a 33-km long outer seawall and several hundred km of internal dykes 113

and walls. The reclamation project was first approved in the 1980s and construction of the outer seawall started in 1991. Following delays caused by protests and court cases (Kim 2001) the last gaps in the outer seawall were closed in April 2006 (Rogers et al. 2006a). In 2010, inner dykes were under construction. The stated end-use of Saemangeum has been modified several times since the project‘s inception (see Long et al. 1988, Birds Korea 2010a). Recent plans include the construction of freshwater reservoirs, areas of parkland, industrial zones and a new city. The national Ministry of Environment (MOE) stated that 5,950 hectares of the reclamation area would be reserved as ―Ecological and Environmental Lots‖ (Kim 2010a). However, less than 1000ha of tidal-flat remains seaward of the outer seawall; almost all intertidal wetland landward of the outer seawall will be lost; and there is no conservation plan for the migratory shorebirds supported by the site.

4.1.2 International Importance of the Saemangeum Estuarine System (SES) Surveys by the National Institute of Environmental Research (NIER) within the national Ministry of Environment between 1997 and 2003 led to estimates during northward and southward migration respectively of 138,000 and 145,000 shorebirds supported by the Mangyeung Estuary, and of 178,000 and 112,000 shorebirds supported by the Dongjin Estuary (Yi 2003, 2004). Combined, 330,000-573,000 migratory shorebirds were estimated to be supported by the SES each year. The lower estimate is based on the sum of the seasonal site-maxima in Barter (2002), and the higher estimate on the sum of peak counts of each species at both estuaries in different years between 1997 and 2001 (Yi 2003, 2004). Based on the lower estimate, the SES was the most important known shorebird site in the whole of the Yellow Sea during northward migration (supporting c. 50,000 shorebirds more than the second most important site); and the second most important site in the Yellow Sea during southward migration (Barter 2002). The SES supported c. 30% of the global breeding population of Great Knot on northward migration and the Yellow Sea‘s largest concentration of the now Critically Endangered Spoon-billed Sandpiper on southward migration (Barter 2002).

4.1.3 Origin of the Saemangeum Shorebird Monitoring Program (SSMP) Saemangeum was until recently the largest single coastal reclamation project to date in the world (Barter 2002), resulting in the loss of one of the most important shorebird 114

staging sites on the EAAF. The mechanisms that drive declines in shorebirds due to habitat loss and reduced feeding opportunities are well described in other regions (see Piersma & Baker 2000; Battley 2002; Burton et al. 2003, 2006; Niles et al. 2008). Population decline in several long-distance migrant shorebird species was therefore predicted if the reclamation project continued (Moores 1999b, 2003a). However, there were no studies in the ROK, the EAAF or globally that provided analysis of the impacts of a large-scale reclamation project on shorebirds at the population-level to support or to refute such predictions. Nonetheless, proponents of the Saemangeum reclamation asserted that shorebirds can ―easily move their habitat to the Gomso Bay, Geum River estuary or other tidal flat (239,000ha) which are 5~20km away from Saemangeum‖ (national Ministry of Agriculture, Forestry and Fisheries [MAFF] 2003, in Moores 2003a). There was no evidence that the adjacent Gomso Bay (35°35' N, 126°36' E) was able to support and maintain large concentrations of shorebirds. Moreover, the reclamation of much of the adjacent Geum Estuary (36°01' N, 126°35' E) had (at that time) already been approved. Ramsar Resolution IX.15 (2005) therefore formally requested the ―government of the Republic of Korea to advise the Secretary General of the current situation concerning the seawall construction and reclamation of the Saemangeum coastal wetlands, and the impact of the construction works to date on the internationally important migratory waterbird populations dependent upon these wetlands.‖ No formal response to this request was received by the Ramsar Secretariat in either 2005 or 2006 (Ramsar 2007), despite ongoing waterbird monitoring programs conducted under the auspices of government bodies (Korea Agriculture and Rural Infrastructure Corporation [KARICO] 2003-2005; NIER unpublished data, 2001-2007). The lack of response to Ramsar Resolution IX.15 indicated that there was no adequate (or at least open) monitoring program in place. Moreover, due in part to a lack of domestic research capacity, ongoing shorebird research programs did not cover all sites to which shorebirds might be displaced within the ROK. There was also no shorebird monitoring program in place in the DPRK and limited capacity to cover all major sites along the Chinese coast. Nonetheless, any robust assessment of impact at the population level on migratory shorebirds would require coordinated monitoring in more than one part of the EAAF. Australia is the southern terminus for many of the migratory shorebirds of the EAAF, and most of the world‘s Great Knot spend the boreal winter in Australia (Bamford et al. 2008). Banding effort within the SES since 115

the late 1990s and observations of birds there banded elsewhere has proved that many shorebirds staging in the SES (including Great Knot) spend the boreal winter in Australia (Minton et al. 2006). In addition, Australia has both the greatest number of skilled counters and banders of any country on the EAAF (Barter 2005), and also has robust national monitoring programs that could contribute to the detection during the boreal winter of long-term population trends of some shorebird species that stage in the Yellow Sea (Gosbell & Clemens 2006). Rapid declines at the population level in some shorebird species are difficult to detect with confidence through short-term monitoring in Australia alone (Milton et al. 2005). However, improved monitoring approaches and increased survey effort would be better able to detect such rapid declines (Rogers et al. 2006b). As c. 30% of the breeding population of Great Knot was concentrated in the SES during northward migration, we predicted that the loss of this area would lead to a substantial decline in this species which would be detectable both in the ROK during northwards migration and in Australia during the boreal winter. A coordinated count effort, both in the ROK and Australia, would have the potential to test this prediction and enable an assessment of whether reclamation at Saemangeum (and elsewhere in the Yellow Sea) was driving declines at the population-level in Great Knot (and other shorebird species). The conservation organisation Birds Korea and the Australasian Wader Studies Group (AWSG) therefore established a partnership to develop the Saemangeum Shorebird Monitoring Program (―the SSMP‖) in early 2006. Northward migration (April and May) was selected as the main focus for the SSMP. This was because most previous counts indicated that the largest shorebird concentrations were supported by the SES during northward migration (Moores 1999a; Barter 2002; Yi 2003, 2004), and northward migration is more concentrated in time (thus requiring a shorter field season that can be more fully covered). Moreover, shorebird biology suggests greater susceptibility to, and therefore likely easier detection of, problems caused by habitat loss during northward migration. Shorebirds need to arrive at breeding sites within a narrow time-frame and in appropriate physiological condition if they are to breed successfully (Piersma & Baker 2000, Battley 2002, Conklin & Battley 2011). Pragmatically, three seasons of northward migration were considered adequate (though not optimal) to assess whether birds would be affected by the closing of the seawall itself. The period 2006-2008 was selected for reasons that included a court decision to permit the reclamation to continue (made in early 2006) and the intention to inform the 2008 Ramsar conference of the 116

research results (Moores et al. 2008). The SSMP focused on the SES and the adjacent Gomso Bay (to the south) and the Geum Estuary (to the north). These three wetlands were selected in order to test the claim of project proponents and decision-makers that shorebirds could ―easily move‖ to adjacent sites (an important argument to refute or prove for landuse and conservation planning purposes); because some shorebirds were recorded during previous survey moving between the SES and Geum Estuary; and because we assessed that all three wetlands could be surveyed adequately during periods of high spring tides in all three years. In order to assess where shorebirds had displaced to other sites within the ROK, the SSMP was also designed to mesh-in with a national shorebird survey in 2008, which would cover all internationally important wetlands nationwide, including those known to support internationally important concentrations of Great Knot (Chapter 5). It was also designed in conjuction with count initiatives in Australia, including shorebird survey of North-west Australia (Rogers at al. 2006a, 2009).

4.1.4 Research Aims and Main Species Our primary aim was to gather robust data on the numbers (and if possible the origins) of shorebirds supported by intertidal wetland within the SES and the adjacent Geum Estuary and Gomso Bay (all three areas combined: the ―Study Region‖) during northward migration. This was in order to measure changes between 2006 and 2008 (the ―study period‖) in the number of shorebirds within the SES and the Study Region as a whole. Barter (2002) and Moores (2003e) listed 20 species of shorebird that were supported by the SES and/or the adjacent Geum Estuary in Ramsar-defined internationally important concentrations of >1% of population during northward and/or southward migration. All are ecologically-dependent on intertidal wetland. These were the species predicted to be most affected by the Saemangeum reclamation (Moores 2003a, 2003e), and thus were the main focus of the present research. These species are listed in Table 4.1, with the 1% criterion from Wetlands International (2006) and the minimum estimate represented by the sum of the highest peak count listed for each of the Mangyeung and Dongjin Estuaries (the SES) and the Geum Estuary (irrespective of season) as listed in Barter (2002).

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Table 4.1 Shorebird species found in internationally important concentrations of >1% of flyway population in the SSMP Study Region between 1999 and 2003 (from Barter 2002 and Moores 2003e). English Name Scientific Name Global 1% of % in Status Pop. SSMP Study Region

Far Eastern Oystercatcher Haematopus (ostralegus) osculans 100 57 Great Knot Calidris tenuirostris VU 3,800 22 Kentish Plover Charadrius alexandrinus 1,000 22 Mongolian Plover Charadrius mongolus 600 14 Nordmann‘s Greenshank Tringa guttifer EN 8 14 Eurasian Curlew Numenius arquata NT 350 12 Terek Sandpiper Xenus cinereus 500 12 Spoon-billed Sandpiper Eurynorhynchus pygmeus CR 30 9 Black-tailed Godwit Limosa limosa NT 1,600 8 Grey Plover Pluvialis squatarola 1,300 7 Far Eastern Curlew Numenius madagascariensis VU 380 6 Dunlin Calidris alpina 17,500 5 Bar-tailed Godwit Limosa lapponica 3,300 3 Red-necked Stint Calidris ruficollis 3,200 3 Whimbrel Numenius phaeopus 550 3 Common Greenshank Tringa nebularia 1,000 2 Sanderling Calidris alba 220 1 Broad-billed Sandpiper Limicola falcinellus 1,000 1 Ruddy Turnstone Arenaria interpres 1,000 1* Grey-tailed Tattler Tringa brevipes 400 1 Note: Global conservation status of NT (Near-threatened), VU (Vulnerable), EN (Endangered) and CR (Critically Endangered) is from BirdLife International (2011); 1% of Pop. is the estimate of 1% of Flyway Population from Wetlands International (2006); the % in SSMP Study Region is the sum of peak counts, irrespective of season, for the Mangyeung and Dongjin Estuaries and the Geum Estuary in Barter (2002), expressed as a percentage of that species‘ EAAF population. One of the listed species (*) did not meet the 1% criterion in Wetlands International (2006): Ruddy Turnstone was listed by Barter (2002) using a different Flyway estimate. Estimates for several of these species have also subsequently been recently revised downwards, including that of Spoon-billed Sandpiper (see BirdLife International 2011).

As the SSMP was designed to inform other research initiatives in the ROK and Australia, the results could be used to determine whether: 1. Shorebird species of intertidal wetland were able to remain within the reclamation area after seawall closure in 2006; 2. Shorebirds were displaced by the Saemangeum reclamation to Gomso Bay and the Geum Estuary; 3. Shorebirds were displaced from the SES and the Study Region to other sites in the ROK; 4. Shorebirds suffered a decline at the population level substantial enough to be detected in Australia in the boreal winter. The research could thus be used to investigate our hypothesis that loss of a major staging site through reclamation in the Yellow Sea can cause population-level declines 118

in migratory shorebird species, and to contribute to an assessment of whether avian biodiversity is in decline in the ROK. In addition to fieldwork, the SSMP was designed to advocate responsibly (cf. Noss 1999) for shorebird and wetland conservation through a range of public awareness events; media involvement; and rapid publication of preliminary results in the conservation literature (Rogers et al. 2006a; Moores et al. 2006, 2007, 2008). This chapter provides detailed results and analysis of the SSMP shorebird research. To help determine longer-term population trends caused by the reclamation project, shorebird numbers and habitat change in the Study Region before the survey period are also described (see Section 4.3.7 and the Discussion). As noted in Chapter Three, large-scale reclamation projects can take years or even decades to complete. Declines of shorebirds caused by a large-scale reclamation project might also take place over several years.

4.2 METHODS

4.2.1 The Study Region 4.2.1.1 Saemangeum Estuarine System: SES The first shorebird survey in the SES was conducted in the late 1980s. Increased survey effort between the mid-1990s and early 2000s (see Section 4.3.6) improved knowledge of the distribution and movements of shorebirds within the SES, including the identification of several high-tide roosts. Based on survey by the present author and others, the inner stretches of both the Mangyeung and Dongjin estuaries were known to contain extensive salt-marsh (e.g. at Hwapo) used for roosting, and unvegetated tidal- flats in both inner and outer areas used by feeding shorebirds at low tide (see Figure 4.1). During low tide, tidal-flats extended 3km north–south and up to 10km west-east in some areas. Upstream from Simpo, most tidal-flat areas were steep-sided, muddy or mud-sand mix, while most outer tidal-flats were sandy with a very gentle slope. During spring high-tides (which reached >7m), a tidal bore (+/- 1m) moved up the Mangyeung River, and the whole system was temporarily inundated. Most shorebirds moved into the hinterland, or remained in flight until the tide started to ebb (shorebird behaviour noted in other regions: Hötker 2000). The hinterland of the whole system (through to at least 2010) was separated from the estuaries by inner seawalls and dykes and contained a mix of agriculture (largely rice-fields) and rural villages, with the exception of Okgu 119

(which contained >200ha of saltpans, used by roosting shorebirds during previous survey) and some urban-type development to the north of the Mangyeung.

Figure 4.1 The Study Region in May 1989 (Left) before construction started on the Saemangeum seawall, and in late 2005/early 2006 (Right) (NASA images).

4.2.1.2 Geum Estuary The total area of the estuary is given as 12,000ha in Barter (2002). Survey effort in the late 1990s and early 2000s identified three main areas of shorebird habitat within the Geum Estuary totalling c. 6000ha: 1. Mainland tidal-flats (c. 900ha) within the main river channel below the estuarine barrage (see Chapter 3, Figure 3.1), and near-by rice-fields (especially upstream of the estuarine barrage); 2. Mainland tidal-flats of the Janghang coastline, north from the river-mouth to Janggu Bay (>2,000ha); 3. Complex tidal-flats surrounding Yubu and Daechuk Islands (c. 3,000ha), partially separated from the main river channel to the south by a seawall. Substrates vary from silt-rich within the river channel, to more extensive sand-mud and sand-flats near Yubu Island (Kim et al. 2006, Moores et al. 2007). Tidal-range is often 120

<3m during neap tides, and reaches >7.5 m during the highest spring tides at Gunsan Outer Port and 7.7m at Gunsan (MMAF 2006). Due to differences in relative heights, tidal-flats within the river channel are inundated most regularly and for longest. Shorebird roosts are dispersed throughout the estuary, and appear to be used or avoided based on quite small differences in tide-heights. In earlier surveys (and during the SSMP), large numbers of shorebirds roosted on remaining exposed tidal-flats near to the tide-edge during neap tide, often >1km from shore. On high tides of intermediate height, mainland roosts on tidal-flats north of the river-mouth were used. During high tides of between c. 6.7-7.0m, the majority of shorebirds were concentrated on remaining elevated sandbanks especially on tidal-flats close to Yubu and Daechuk Islands. On spring tides >7m, and especially of the very highest tides of >7.5m, only one remote sand bank (―Sandy Island‖) and some seawalls and islets were left part- uncovered by tides. Large numbers of shorebirds then moved to the SES to roost. During the SSMP we recorded shorebird movements and roost choices during different stages of the high tide cycle. We timed our counts to avoid double-counting of birds using different roosts on different tides. Much of the hinterland of the Geum Estuary is unsuitable for large shorebird roosts, as it includes a heavily altered, industrial and residential landscape along both flanks of the river. However, some species on occasion also roosted upstream of the estuarine barrage or on the barrage walls. There were also several small or medium-sized roosts on elevated banks along the more rural Janghang-Janggu coastline during spring tides.

4.2.1.3 Gomso Bay Gomso Bay is c.15km west-east and 5km north-south towards its mouth. It is fed by one small river and several smaller creeks. Tidal-flats in the inner part of the bay are largely mud-sand mix, and lightly vegetated with salt-marsh. Outer intertidal wetland areas are made up largely of sandy tidal-flats, with the outer third or so of the bay occupied by sea-shallows. Spring high tides reach approximately 7m when the whole bay is inundated. Although the site was first surveyed in 1998 (Moores unpublished data) there was only limited knowledge of potential shorebird feeding areas and roost sites prior to the SSMP. In 2006 and subsequently, shorebirds and some other waterbird species moved into several well-dispersed roosts in the hinterland during spring high tides. Although such roosts can be difficult to locate, elevated count points in clear weather enabled coverage of most feeding shorebirds in the bay at mid-low 121

tide. The hinterland is rural, with saltpans, several areas of fish-ponds and rice-fields in low-lying reclaimed areas, and wooded hills.

4.2.2 SSMP Survey Design In total, >70 people participated in at least one day of fieldwork. The number of shorebirds recorded in a count is typically inexact and we were conscious of previous research by Rappoldt et al. (1985) and Rogers et al. (2006b) that investigated the influence on counts of conditions prevailing during the count, the size of flocks, the experience of observers and the accessibility of roosts. These studies found that much of the variation in shorebird counts made by experienced observers is stochastic (i.e. randomly scattered around the number of shorebirds that were really present), and can be calculated if the number of component counts is known. However, variation caused by birds being overlooked or double-counted (termed ―bias‖ by Rogers et al. 2006b, and ―area error‖ by Rappoldt et al. 1985) defies calculation. We accordingly designed the fieldwork to reduce bias, using the following approach: 1. There were four to >20 counters per tide series, logistics being arranged so that numbers were greatest when shorebird numbers peaked. All counts used in the Results were conducted by experienced counters, usually in teams of two to four, using tripod-mounted telescopes and equipped with GPS units. 2. Shorebirds were only counted at high tide, when they were concentrated into a reasonably small number of roosts (though see Section 4.2.3). At low tide they were scattered over very large areas of exposed tidal-flat, much of which was inaccessible to observers working on foot or from boats. 3. All major roosts within a site complex were surveyed on the same high tide, to eliminate the possibility of overlooking or double-counting birds that moved from one roost to another during the same single count. This made it essential to carry out shorebird counts on spring tide series, as it was only on spring high tides that shorebirds were confined to a small enough number of roosts for simultaneous counts of all sites to be achievable. The site complexes counted concurrently were: (1) all sites in the Geum Estuary, with additional inspection of the northernmost SES to assess if any Geum Estuary birds were forced there on the highest tides; (2) all sites in the Mangyeung Estuary; (3) all sites in the Dongjin Estuary (including teams at Simpo and on boats looking 122

for any indications of movements of birds between the Dongjin and Mangyeung Estuaries); and (4) all sites in Gomso Bay. 4. Extensive explorations were carried out to ensure all major roosts were located and surveyed. All coastal sites identified by previous survey and from satellite imagery as having topography potentially suitable for roosting shorebirds were visited at high tide, and birds detected in flight on rising tides (often detectable from several km range) were followed to find where they settled. In general the formal counts carried out on spring tide series were preceded by several days of initial surveys and preliminary counts. Counts cannot be compared directly between years on the same dates (as tides follow the lunar calendar), but they can be compared between main count periods (―count cycles‖) (Table 4.2). During each count cycle, count teams accessed target roost sites before high tide, and communicated by phone to coordinate count times.

Table 4.2 Dates and duration of SSMP count cycles and time and height of spring high tides at Gunsan (MMAF 2006, 2007, 2008). Count Year Dates Highest Time Highest Time Cycle Spring Tide Spring Tide Height (cm) Height (cm) AM PM First 2006 April 15-17 674 0439 622 1612 Second 2006 April 27-29 736 0405 675 1455 Third 2006 May 13-17 690 0421 600 1517

First 2007 April 2-8 686 0452 655 1558 Second 2007 April 14-19 762 0420 698 1508 Third 2007 April 30-May 6 686 0424 612 1522 Fourth 2007 May 14-22 761 0407 657 1442

First 2008 April 4-8 739 0428 688 1524 Second 2008 April 18-20 673 0318 633 1455 Third 2008 May 6-12 750 0414 649 1535 Fourth 2008 May 20-24 671 0404 583 1530

During every count, the number of each shorebird species was recorded, along with the start and finish time, the weather and the tide-stage. An effort was made to assess the percentage of birds that were feeding or resting. Often counts of selected species were repeated rapidly in order to help reduce potential inaccuracies. Counts were then reviewed, and if considered incomplete or inaccurate, they were repeated within the same count cycle. Fieldwork was also conducted during neap tides between count cycles to improve understanding of shorebird movements, to locate leg-flagged and colour-banded (―marked‖) shorebirds, and to find difficult to locate species, such as Nordmann‘s Greenshank Tringa guttifer and Spoon-billed Sandpiper, which were considered easy 123

to overlook in main counts. The largest concentration of Spoon-billed Sandpiper was found during such a neap tide series on May 26th 2007, two days after the Fourth Count Cycle. This count is included in subsequent tables and discussion as both the Fourth Count Cycle count and the peak count that year for this species. In 2006, the main fieldwork was conducted between March 31st and May 18th, with three count cycles. During each count cycle we counted six high tide roosts in the Geum Estuary, up to 20 roosts within the SES and from five points in Gomso Bay (see Figure 4.1 above). In 2007, with a larger count team, fieldwork was conducted at the Geum Estuary on most dates in March, and then throughout the Study Region between April 2nd and May 27th, with four count cycles. In 2008, fieldwork was conducted between April 1st and May 26th, with four count cycles. In 2007 and 2008, the same roosts and count points in the Geum Estuary and Gomso Bay as in 2006 were recounted, and due to improved knowledge of sites and larger count teams, one or two additional areas were also included (e.g. Sandy Island in the outer Geum Estuary), likely contributing to higher counts of Eurasian Curlew Numenius arquata and Sanderling Calidris alba that year. Although the main emphasis throughout the SSMP was on shorebird counts, all bird species of global conservation concern were also recorded (Section 4.3.6). In addition, basic assessments of habitat change and major ecological events were made, including some mapping of vegetation and recording of shellfish die-offs, fish kills and sudden increases or decreases in tidal range within the SES following closure of the seawall. Informal interviews were also conducted with local fisherfolk as part of the SSMP and of ongoing research by Jeonbuk University to assess the impacts of the reclamation of fishing communities and local culture (SLJU 2008).

4.2.3 Changes to the SES and SSMP Count Method due to Seawall Closure The construction of the 33-km long Saemangeum outer seawall has resulted in massive changes to the ecological status and landform of the SES since at least 2000, and also some changes in sedimentation (Lee 2010b) and tidal currents over a wider area (Lee et al. 2010). These changes necessitated a change in survey method during the SSMP. In 2003 the outer seawall was 80%-90% complete (Moores 2003a) with gaps still >5km wide. By early 2006 the remaining gaps in the seawall had been reduced to only 1km wide, and tidal range had fallen by c. 1m on highest spring tides. On April 1st 2006, the 727 cm high tide in Gunsan (MMAF 2006) inundated most but 124

not all salt-marsh areas, suggesting a high tide within the SES of 6m (pers. obs.). That month the remaining gaps in the seawall were closed, so that by April 21st all tidal movement was channelled through two sluice gates with a total width of 540m. Although the sluice gates remained open throughout the 2006 fieldwork, tidal-range dropped markedly after mid-April and in late April and May it was <1m, even on spring tides. As a result, tides no longer reached higher tidal-flats or upstream areas, and there was a mass die-off of shellfish (see Section 4.3.6). During fieldwork in 2007, the tidal range was only c. 25cm, and on most dates probably 90-95% of the (former) tidal-flats were either permanently flooded or exposed. During fieldwork in 2008, the sluices were left fully open on most days, resulting in a tidal range that we measured as 1.3m, at least in the outer part of the system. However, the sluice-gates were twice kept closed at lowest tide during the spring tide series for 4-5 days, resulting in a loss of tidal movement and several days of exposure of lower tidal-flats. There were further large die-offs of benthos and we suspected a decline in salinity in much of the system. During the three years of the SSMP, the greatly reduced tidal exchange resulted in the prolonged inundation of most former low-lying tidal-flat; and the exposure and drying out of higher areas within the SES. Survey methods needed to be modified in response, with greater effort in 2007 and 2008 invested in active searching of shorebirds feeding in wet mud areas near to the water‘s edge, and of birds feeding and roosting on newly-formed islands which needed to be reached by boat. There were also physical changes to surface sediments in some parts of the Geum Estuary and changes in abundance of some species of benthos that probably affected shorebird distribution. However, these did not necessitate a substantial modification of count method, either at the Geum Estuary or at Gomso Bay.

4.2.4 Analysis To calculate the peak number of shorebirds in the Study Region, we took the highest count cycle count for each species. This was not necessarily the count cycle in which numbers peaked within all three areas. For example, if numbers of Great Knot in the SES peaked in the First Count Cycle, but numbers within the Study Region as a whole peaked in the Third Count Cycle, we would use only the counts from the Third Count Cycle. We then treated this highest count cycle count as the minimum count of that species that northward migration period. This enabled us to compare numbers for each species between the three wetlands and between years. 125

It was necessary to develop an understanding of migratory turnover in the Study Region to assess whether peak counts were representative of the number of shorebirds migrating through it. We modified a shorebird migration and turnover model developed by Thompson (2003). This model was designed for repeated counts carried out at a migratory staging site, and assumes that the arrival date and departure date of each species are normally distributed. Iterative modelling was used to estimate the number of individuals that staged in the Study Region and the arrival and departure dates (and associated standard errors) that best explained the changes in numbers of birds counted through the whole study period. Realistic starting values for the calibrations were obtained by an interactive evaluative procedure, and final parameters were estimated using the NONLIN procedure in SYSTAT 11 (SYSTAT 2005) with a sum of squares loss function. The SSMP data were not perfectly suited to the Thompson model, as it was only possible to carry out complete counts once per spring tide series (i.e. during each of the 3-4 count cycles in each migration season). Sufficient samples for modelling could only attained by pooling date from separate years. Even so, we needed to estimate numbers at three different sites, one much changed between years, during three years of northward migration, using only 11 count cycle counts. In our calculations, each data point was weighted by the size of the counts on which the proportions were based. The consequent estimates were then used in conjunction with the count data to obtain estimates of the number of birds transiting and to assess the level of confidence in the counts. Although the estimates are based on defendable assumptions, the problem remains that they are based on models calculating a number of parameters from a small number of data points. Accordingly we use the estimates as an exploratory tool only, giving us a general understanding of turnover through the region, and of how representative peak counts were of total shorebird passage.

4.3 RESULTS 4.3.1 Numbers and International Importance of the Study Region In total, 45 species of shorebird were recorded in the Study Region by SSMP fieldwork. Based on a sum of the highest count cycle count for each of these 45 species in all three years, a minimum 264,567 shorebirds were recorded. The highest shorebird count during a single count cycle was 244,348 (May 13th-17th, 2006), representing 92% of the sum of maxima of all 45 shorebird species recorded during all three years. The 126

highest shorebird counts per wetland during the 11 count cycles were 176,954 within the SES, 97,670 at the Geum Estuary and 9,457 at Gomso Bay. Nineteen shorebird species were found in internationally important concentrations of 1% or more of Flyway Population (Table 4.3).

Table 4.3 Peak counts of the 35 most numerous shorebird species recorded in each of the three wetlands and the highest single count recorded within a single count cycle in the SSMP Study Region. Saemangeum Geum Gomso SSMP % Estuarine Estuary Bay Study Region of System Flyway Pop.

*Great Knot 86,288 50,000 2,966 116,126 31 *Dunlin 62,508 53,565 3,127 82,718 5 *Bar-tailed Godwit 5,826 13,175 284 18,305 6 *Mongolian Plover 5,914 4,385 226 7,606 13 *Grey Plover 3,488 4,763 213 6,602 5 *Red-necked Stint 5,154 2,127 33 6,242 2 *Terek Sandpiper 3,855 3,301 615 5,633 11 *Far Eastern Curlew 2,261 2,582 315 4,843 13 *Whimbrel 1,028 1,215 1,686 2,682 5 *Common Greenshank 912 1,482 204 2,414 2 *Sharp-tailed Sandpiper 645 1,014 42 1,659 1 *Ruddy Turnstone 744 695 13 1,439 1 *Black-tailed Godwit 613 1,202 49 1,543 1 *Far Eastern Oystercatcher 324 1,225 14 1,453 14 *Eurasian Curlew 213 1,103 6 1,322 4 *Broad-billed Sandpiper 338 1,142 1 1,278 1 Kentish Plover 486 186 7 658 <1 *Grey-tailed Tattler 430 268 97 606 1 *Sanderling 222 572 0 578 2 Spotted Redshank 175 117 8 292 <1 *Nordmann‘s Greenshank 14 70 0 84 10 Red Knot 65 30 10 74 <1 Common Redshank 50 23 2 66 <1 Wood Sandpiper 17 12 37 66 <1 Pacific Golden Plover 33 20 6 53 <1 *Spoon-billed Sandpiper 31 8 0 39 1 Curlew Sandpiper 32 15 0 37 <1 Black-winged Stilt 29 1 0 29 <1 Common Sandpiper 20 9 10 26 <1 Little Ringed Plover 22 10 5 25 <1 Common Snipe 19 5 0 19 <1 Greater Sand Plover 2 2 7 8 <1 Marsh Sandpiper 7 1 2 7 <1 Ruff 5 4 0 6 <1 Green Sandpiper 3 4 5 4 <1 Total 181,773 144,333 9,990 264,542 Note: An asterisk is used to denote each of the 20 main shorebird species, and bold is used to indicate internationally important concentrations. Flyway Population criterion of 1% is from Wetlands International (2006).

There was substantial overlap between the 20 species previously identified as internationally important by Barter (2002) and Moores (2003e) (listed in Table 4.1) 127

and these 19 species. Exceptions were the presence of >1% of Sharp-tailed Sandpiper Calidris acuminata (previously also numerous, but very difficult to count accurately without large count teams: pers. obs.) and only small numbers of Kentish Plover Charadrius alexandrinus (1,500 were listed in the Mangyeung Estuary during northward migration by Barter 2002). Also, the peak count of Black-tailed Godwit Limosa limosa fell fractionally short of 1% (1,543 or 0.96%). However, internationally important concentrations of this species were counted in the hinterland and some turnover seemed likely from our migration model. Because of their clear international importance, these 20 species (marked with an asterisk in Table 4.3) were selected as the main focus for the remainder of this chapter and from hereon are called the ―20 main shorebird species‖. During the SSMP, 15 of these 20 main shorebird species were recorded in internationally important concentrations within the SES, 14 in the Geum Estuary and two in Gomso Bay. The most numerous species (and the only ones with peak counts of >10,000 in the Study Region) were Great Knot, Dunlin Calidris alpina and Bar- tailed Godwit Limosa lapponica. These three species are also among the more numerous shorebird species on the EAAF (Wetlands International 2006), and the same as identified by all previous survey effort as the three most abundant shorebird species in the Study Region during northward migration. In total, the Study Region supported ten shorebird species in concentrations of 5% or more of the 2006 EAAF Population (as shown in parentheses): Great Knot (31%), Far Eastern Oystercatcher Haematopus (ostralegus) osculans (14%), Far Eastern Curlew Numenius madagascariensis (13%), Mongolian Plover Charadrius mongolus (12%), Terek Sandpiper Xenus cinereus (11%), Nordmann‘s Greenshank (8%), Grey Plover Pluvialis squatarola (5%), Bar-tailed Godwit (5%), Whimbrel Numenius phaeopus (5%) and Dunlin (5%).

4.3.2 Marked Birds Marked birds enable the identification of origin and likely destination of individual birds, and in some cases also helped to identify movement and minimum staging times within the SSMP Study Region. Between 2006 and 2008 there were 1,145 records of marked shorebirds of 19 species found during SSMP fieldwork (Table 4.4). The two most numerous species were Bar-tailed Godwit and Great Knot. Most resighted birds were marked in areas where there are intensive shorebird research programs including 128

south-eastern and north-western Australia, New Zealand, Taiwan, and Chongming Island (China). Birds from 12 other colour-flagging regions were seen, however, confirming that shorebirds from a very broad region congregate in the SSMP Study Region and the YSBR during migration (Figure 4.2).

Table 4.4 Origin of colour-banded and leg-flagged shorebirds observed during SSMP fieldwork, 2006-2008. Region Dunlin Great Knot Bar-tailed Terek Other Total Godwit Sandpiper species1 Alaska 14 0 0 0 0 14 Chukotka 1 0 0 0 1 2 Kamchatka 0 1 0 0 0 1 Japan 0 1 1 1 8 11 Republic of Korea 14 6 5 0 9 34 Chongming Island 16 196 21 7 13 253 Taiwan 74 1 3 0 2 80 Hong Kong 0 0 1 0 0 1 Thailand 0 0 1 1 2 4 Sumatra 0 1 0 0 0 1 NW Australia 0 297 123 32 9 461 Queensland 0 4 30 0 0 34 New South Wales 0 0 6 0 0 6 South Australia 0 0 0 0 5 5 Victoria, Australia 0 27 315 0 22 364 King Island 0 0 0 0 2 2 New Zealand 0 0 160 0 12 170 Grand Total 119 534 666 41 85 1445 Other Species1 = Ruddy Turnstone (3 Japan, 1 NW Australia, 5 SE Australia, 7 New Zealand), Sharp- tailed Sandpiper (1 Chongming Island, 1 SE Australia), Red Knot (3 NW Australia, 2 SE Australia, 3 New Zealand), Curlew Sandpiper (1 SE Australia), Red-necked Stint (1 Japan, 1 ROK, 2 Chongming Island, 2 Thailand, 5 SE Australia), Kentish Plover (1 Taiwan), Mongolian Plover (4 Japan, 5 ROK, 4 SE Australia), Spoon-billed Sandpiper (1 Chukotka), Broad-billed Sandpiper (1 NW Australia), Black-tailed Godwit (1 Chongming Island, 2 NW Australia), Far Eastern Curlew (5 SE Australia), Grey Plover (3 ROK, 5 Chongming Island, 1 Taiwan, 3 NW Australia, 1 SE Australia), Grey-tailed Tattler (1 NW Australia), Nordmann‘s Greenshank (2 Chongming Island), Common Greenshank (2 Chongming Island, 1 NW Australia).

Observations of marked birds confirmed that Bar-tailed Godwit of the baueri subspecies (that largely spend the boreal winter in New Zealand and eastern Australia) arrived and peaked earlier than those of the menzbieri subspecies (many of which spend the boreal winter in and had also been marked in north-western Australia). Marked baueri were present in the first week of April (first on April 2nd). However, the first marked menzbieri was not seen until April 14th. The number of Bar-tailed Godwit counted in the Study Region at any one time was therefore likely to have been 129

lower than the total number during the whole period of northward migration. There were also a small number of resightings of individually-marked birds. In 2006, five were seen more than once (within the same area) including one 25 days later. In 2007, there were 28 observations of individually-marked birds, including two (or more likely three) Bar-tailed Godwit that had also been observed at the same location in 2006. These included one bird that was seen on several dates on tidal-flats there (and nowhere else) between March 27th and April 17th. Such resightings suggest fidelity by at least some birds to the same part of the Study Region between years. A large number of observations of marked birds were of Great Knot that had been flagged at Chongming Island at the mouth of the Yangtze River. In 2006 the flag combination for that site was changed and resightings in the SSMP Study Region shortly after confirm that at least some Great Knot arrived on the Chinese coast of the Yellow Sea before then crossing to the YSBR to continue staging. Most marked Great Knot were from north-western Australia, and a smaller number from south-eastern Australia (where relatively few Great Knot had been marked). Numbers of resighted Great Knot from south-eastern Australia appeared quite consistent through April and May. In contrast, the increase in total counts of Great Knot through April coincided with an increase in the numbers of flagged birds seen from both north-western Australia and China. The large number of observations of marked Great Knot during the three years enabled us to estimate the number of Great Knot within the Study Region that came from non-breeding sites in north-western Australia. Data on the number of Great Knot that have been flagged in north-western Australia each year came from AWSG banding records (D. Rogers in lit. 2008). Average annual survival of 81% was calculated based on unpublished Mark-Recapture studies in north-western Australia by A. Ewing, and independently, using different birds, by the Global Flyways Network (D. Rogers, C. Hassell and T. Piersma in prep.). This enabled us to calculate the number of Great Knot leg-flagged in north-western Australia present in the EAAF at the time of the present research. Thus, the peak count of 116,126 Great Knot from the SSMP Study Region in 2006 included 27,270 Great Knot predicted to be from non-breeding grounds in north-western Australia. This improved our understanding of the potential magnitude of decline in Great Knot numbers in north-western Australia to be expected if most of the Great Knot that staged in the SES were to die as a result of the loss of their core staging site. 130

Figure 4.2 Origins of leg-flagged and colour-banded birds resighted by the SSMP. The numbers indicate the number of birds seen from each region of origin.

4.3.3 Phenology and Potential Bias The most numerous species peaked at a similar time each year. However, turnover and differences in migration strategies meant that survey effort needed to be spread over two months. The SSMP, conducted through April and May, likely captured the peaks of most species. Research effort in the Study Region prior to the SSMP, however, suggested that both Far Eastern Oystercatcher and Eurasian Curlew peaked in the boreal mid-winter and in late March respectively (Lee et al. 2002). Early April SSMP counts therefore will probably have missed their annual peaks in number, and might or might not also have included individuals of these and two other species (Grey Plover and Dunlin) from the Study Region‘s regular over-wintering population. In addition, several other species were already present at the beginning of fieldwork in small numbers, including Bar-tailed Godwit, Far Eastern Curlew and Great Knot. Counts conducted in 2007 in the Geum Estuary confirmed that numbers of these species were very much lower in March than in April. It is however possible that SSMP fieldwork might have missed some of their early through-movement. 131

250

200 Total Count ('000)

150 2006 2007 2008 100

50

0 1 Apr 11 Apr 21 Apr 1 May 11 May 21 May 31 May 6 Apr 16 Apr 26 Apr 6 May 16 May 26 May

Figure 4.3 Migration timing of 21 shorebird species in the Study region (2006-2008). The bars are the total numbers of the 20 main shorebird species plus Red Knot during each of the 11 count cycles during the survey period. All counts each count cycle were made over a number of days; component counts are aggregated to the date on which the largest numbers of birds were counted. The trend curves have been added to illustrate the general pattern of the counts. The only count which is markedly different is that for the third count cycle in 2006 on May 15th. It may be relevant that seawall closure between the 2006 and 2007 surveys might have led to a change in the timing of shorebird departures.

In all three years, the numbers of shorebirds and shorebird species within the Study Region increased rapidly from early April, and 17 out of the 20 main shorebird species were already present before April 10th. The exceptions were Whimbrel Numenius phaeopus, Nordmann‘s Greenshank and Spoon-billed Sandpiper. Arrivals of some species were easily detected by their first records for the year and increases in number between dates and count cycles. Departures could also be identified by changing numbers through the migration season, and it was often possible to watch migratory departures in the field, as departure behaviour of shorebirds is distinctive (Piersma et al. 1990, Conklin & Battley 2011). In 2006, most departures were noted only after May 15th (including of Common Greenshank, Mongolian Plover, Bar-tailed Godwit and Dunlin). Near-daily counting of one core area that year that continued beyond main SSMP counts recorded a rapid decline in numbers of shorebirds present, falling from c. 50,000 shorebirds on May 13th to only 233 shorebirds on May 21st. In 2008, departures of several species included single flocks of 245 Great Knot on May 20th, and 190 Terek Sandpiper on May 21st. The intensity of these departures and the lateness of the 132

departure dates support the assumption that most of the shorebirds used the Study Region as a staging area before undertaking an extended flight towards breeding areas. The date of the largest count within each of the three years of fieldwork for each of the 20 main species is listed in Table 4.5, along with the mean date of their peak count for the three years. A very few species (including Far Eastern Oystercatcher) appeared to peak in early April, while the largest number of species peaked in the first half of May. At least four species (Ruddy Turnstone Arenaria interpres, Sharp-tailed Sandpiper, Spoon-billed Sandpiper and Broad-billed Sandpiper Limicola falcinellus) were recorded in small numbers in April, but peaked late in May. It is likely that at least some individuals of these four late-peaking species would have been missed by the SSMP in 2006 because main fieldwork that year was completed in Mid-May. Therefore the SSMP results need to be used with caution for interpreting changes in their numbers between years.

Table 4.5 The 20 main shorebird species in order of earliest peak date, including the dates of their earliest and latest record during fieldwork. Earliest Latest Date of Date of Date of Mean Record Record Peak Peak Peak 2006-2008 2006 2007 2008 Date of Peak Far Eastern Oystercatcher April 1 May 24 April 5 April 15 April 5 April 8 Eurasian Curlew April 1 May 24 April 26 April 5 April 5 April 12 Far Eastern Curlew April 1 May 24 April 17 April 15 April 6 April 13 Grey Plover April 1 May 24 April 6 May 5 April 6 April 16 Sanderling April 13 May 24 April 29 April 15 May 8 Apr 27 Bar-tailed Godwit April 1 May 24 May 8 April 17 May 8 May 1 Great Knot April 1 May 24 May 15 April 17 May 8 May 3 Common Greenshank April 2 May 24 May 17 April 30 May 8 May 8 Dunlin April 1 May 24 May 14 May 6 May 8 May 9 Whimbrel April 12 May 24 May 17 May 3 May 6 May 9 Mongolian Plover April 2 May 24 May 8 May 15 May 8 May 10 Black-tailed Godwit April 4 May 24 May 9 May 15 May 9 May 11 Terek Sandpiper April 3 May 24 May 15 May 17 May 8 May 13 Grey-tailed Tattler April 7 May 24 May 15 May 15 May 8 May 13 Red-necked Stint April 2 May 24 May 14 May 17 May 10 May 14 Nordmann's Greenshank April 17 May 24 May 17 May 20 May 8 May 15 Spoon-billed Sandpiper April 13 May 24 May 15 May 26 May 8 May 16 Ruddy Turnstone April 3 May 24 May 17 May 15 May 24 May 19 Broad-billed Sandpiper April 12 May 24 May 15 May 22 May 24 May 20 Sharp-tailed Sandpiper April 2 May 24 May 17 May 22 May 24 May 21 Note: the earliest day of fieldwork = April 1st, and the latest day of counts in count cycles = May 24th. Presence on April 1st or 2nd therefore suggests presence before the start of fieldwork, and presence on May 24th suggests continued presence after the end of fieldwork.

4.3.4 Models and Estimates Modelling turnover of migrants through the Study Region was problematic as suitable tidal conditions restricted counting to only three or four counts per northwards migration, yet estimates were needed of 30 parameters: the numbers of birds transiting, and means and standard deviations of arrival and departure dates, for two sites (Geum 133

Estuary and the SES) and for each year (2006-2008). We reduced the number of parameters to be estimated by adopting a two stage approach and making judicious assumptions about year to year differences. It was reasonable to assume that the arrival time distribution is the same at the Geum Estuary and SES, given that the sites are adjacent to one another. There was no a priori reason to expect arrival times to differ between years (though in reality there might be small variations from year to year according to variations in weather experienced during migration). However, it was considered likely that departure times would differ from one year to the next, given that the reclamation of the SES likely influenced prey resources and may have forced birds to spend longer fuelling, hence delaying their departures. Alternatively some shorebird species might have abandoned the site earlier in search of better foraging areas. Seawall closure occurred in late April 2006, and we suspect that departures from the SES that year were not substantially influenced as there was still some tidal flow, and because some species of shorebird exploited carrion from mass shellfish die-offs. In 2007, there was more evidence of birds relocating within and perhaps outside of the system, as birds arrived and tried to feed within areas greatly modified since 2006. By 2008, reduced numbers of birds were assumed to contain many displaced individuals that were again expected to depart on a schedule closer to timing of departure recorded in 2006. The calculation was made in two stages: arrival and departure times were estimated before estimation of numbers of birds transiting. In estimating arrival and departure times for a particular year, we transformed each count to the proportion of the annual maximum for each tide cycle. Nonlinear regression methods were then used to calculate maximum likelihood estimate of arrival and departure parameters. The consequent estimates were then used in conjunction with the count data to obtain estimates of the number of birds transiting. Examples of the resulting models are shown for two species, Bar-tailed Godwit (Table 4.6 and Figure 4.5) and Great Knot (Table 4.7 and Figure 4.6). Despite the presence of two subspecies, the model for Bar-tailed Godwit fitted closely with count data: it calculated an average arrival date of April 10th, and departure dates of c. May 17th in 2006 and 2008. In 2007 departures apparently occurred slightly earlier from the Geum Estuary than from the SES; numbers of staging shorebirds in the SES declined from 2006 to 2008, but apparently increased slightly in the Geum Estuary.

134

Table 4.6 Model of migration timing and transiting numbers of Bar-tailed Godwit. Dates presented as days since April 1st, ± Asymptotic Standard Error. R2 (Obs. versus Est.) = 0.965.

BAR-TAILED GODWIT Estimate S.D. ± A.S.E ± A.S.E Arrival times Geum & SES 2006-2008 9.8 ± 1.28 5.9 ± 1.52 Departure times Geum & SES 2006 & 2008 47.0 ± 1.29 4.9 ± 1.91 Geum, 2007 41.6 ± 4.04 11.4 ± 7.96 SES, 2007 45.4 ± 0.76 1.7 ± - Transiting Numbers Geum 2006 10726 ± 600 - Geum 2007 9483 ± 645 - Geum 2008 13553 ± 584 - SES 2006 5244 ± 500 - SES 2007 3493 ± 542 - SES 2008 2835 ± 573 -

Ba r-ta ile d Godwit - Geum 14 12 10 8 Observed 6 Predicted

Count ('000) 4 2 0

6Apr07 4May07 6Apr08 8May08 17Apr0626Apr0616May06 17Apr07 15May07 18Apr08 23May08

Ba r-ta ile d Godwit - Sa ema ngeum 14 12 10 8 Observed 6 Predicted

Count ('000) 4 2 0

6Apr07 4May07 7Apr08 16Apr0626Apr0615May06 17Apr07 15May07 19Apr0810May0821May08

Figure 4.4 Bar-tailed Godwit in the Geum Estuary (upper chart) and the SES (lower chart) on northward migration (2006-2008).

The Great Knot model generated quite different results in the year to year trend in number of transiting birds. Average arrival date was April 12th, and departure dates 135

from the Geum Estuary in all years, and from the SES in 2006 and 2008, were about May 16th-20th. These dates correspond well with the timing in the last third of May of their main northward migration through the Russian Far East to breeding areas (Tomkovich 1997).

Table 4.7 Model of migration timing and transiting numbers of Great Knot. Dates presented as days since April 1st, ± Asymptotic Standard Error. R2 (Obs. versus Est.) = 0.868 GREAT KNOT Estimate S.D. ± A.S.E ± A.S.E Arrival times Geum & SES 2006/07/08 12.9 ± 3.94 16.1 ± 8.37 Departure times Geum & SES 2006 & 2008 50.9 ± 0.00 0.1 ± 0.08 Geum, 2007 46.1 ± 9.15 10.8 ± 17.39 SES, 2007 32.3 ± 30.34 4.7 ± 82.43 Transiting Numbers Geum 2006 23926 ± 7321 - Geum 2007 54516 ± 8846 - Geum 2008 17854 ± 8682 - SES 2006 86940 ± 7387 - SES 2007 40626 ± 13913 - SES 2008 10764 ± 8451 -

Gre at Knot - Geum 90 80 70 60 50 Observed 40 Predicted

30 Count ('000) 20 10 0

6Apr07 4May07 6Apr08 8May08 17Apr0626Apr0616May06 17Apr07 15May07 18Apr08 23May08

Gre at Knot - Sae ma ngeum 90 80 70 60 50 Observed 40 Predicted

30 Count ('000) 20 10 0

6Apr07 7Apr08 16Apr0626Apr06 17Apr074May07 19Apr08 15May06 15May07 10May0821May08

Figure 4.5 Great Knot in the Geum Estuary (upper chart) and the SES (lower chart) on northward migration (2006-2008). 136

Great Knot, however, departed the SES much earlier in 2007 than in 2006. This was consistent with field observations that season; in April large numbers of Great Knot were concentrated on small tidal-flats remaining near the Saemangeum seawall, but they apparently rapidly depleted the prey there and then left the SES. Despite the major differences in their responses to seawall closure, the models for Great Knot and Bar-tailed Godwit had important elements in common. They matched the count data reasonably well (R2 = 0.965 for Bar-tailed Godwit; 0.868 for Great Knot). They calculated a long staging duration of 4-7 weeks, indicating that the Study Region was a major fuelling area rather than a group of wetlands where birds simply stopped briefly before moving on. Finally, for both species the predicted and observed counts corresponded well, and the calculated number of transiting birds was similar to the maximum counts made during the SSMP. This suggests the maximum counts were a reasonable index of the number of birds staging in the study year, and are a suitable basis for the examination of year-to-year differences.

4.3.5 Changes in Numbers of Shorebirds between 2006 and 2008 4.3.5.1 Twenty main shorebird species Following closure of the Saemangeum seawall in 2006, there were declines in 14 of the 20 main shorebird species in the SSMP Study Region by 2008. The largest decline in the Study Region was shown by Great Knot, with the ―loss‖ of >92,000. Because of the Great Knot‘s former abundance and the severity of its decline, this represented a decline of 42% in the summed peak counts of individuals of the 20 main shorebird species, and a decline of 41% of all shorebirds between the highest count cycle counts in 2006 and 2008 (Table 4.8). There were declines of >10% in twelve species in the Study Region between 2006 and 2008. Eleven of these are absent in the boreal winter in the ROK. The largest declines were shown by Great Knot (80%), Black-tailed Godwit (76%), Sharp-tailed Sandpiper (74%) and Spoon-billed Sandpiper (69%). It is likely that the decline in Spoon-billed Sandpiper was substantially greater than that which we recorded. The species is difficult to locate when mixed in with large flocks of other small shorebirds; there were fewer counters in 2006 to find the species than in 2008; and the species peaked in the Study Region late in May, so the actual peak might not have been recorded in 2006 (when the main survey work was completed by May 17th).

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Table 4.8 Changes in number in 20 main shorebird species in the SSMP Study Region (2006- 2008) listed in order of largest decrease to largest increase. Peak Peak Change Peak Change % Change 2006 2007 2006>2007 2008 2006>2008 2006-2008 Great Knot 116,126 83,403 - 32,723 23,748 - 92,378 - 80% Black-tailed Godwit 1,543 1,334 - 209 376 - 1,167 - 76% Sharp-tailed Sandpiper 1,659 654 - 1,005 439 - 1,220 - 74% Spoon-billed Sandpiper 35 39 +4 11 - 24 - 69% Common Greenshank 2,414 780 - 1,634 824 - 1,590 - 66% Ruddy Turnstone 1,439 989 - 450 882 - 557 - 39% Far Eastern Curlew 4,843 2,499 - 2,344 3,089 - 1,754 - 36% Mongolian Plover 7,606 6,273 - 1,333 5,288 - 2,318 - 30% Far Eastern Oystercatcher 1,453 939 -514 1,022 - 431 - 30% Nordmann's Greenshank 84 60 -24 60 - 24 - 29% Red-necked Stint 5,873 6,242 + 369 4,727 - 1,146 - 20% Bar-tailed Godwit 18,305 12,195 - 6,110 16,259 - 2,046 - 11% Dunlin 82,718 69,830 - 12,888 75,577 - 7,141 - 9% Terek Sandpiper 5,633 5,075 - 558 5,539 - 94 - 2% Whimbrel 2682 1,833 - 849 2,676 - 6 0% Grey-tailed Tattler 302 413 + 411 606 + 304 +1% Grey Plover 5,254 6,602 +1,348 6,020 +766 + 15% Sanderling 418 233 - 185 578 + 160 + 38% Eurasian Curlew 515 472 - 43 1,322 + 807 + 57% Broad-billed Sandpiper 349 427 +78 1,278 + 929 + 166% Sum of 20 species 259,251 200,292 - 58,959 150,321 - 108,930 - 42% Highest Count Cycle Count 244,348 148,929 - 95,419 143,990 - 100,358 - 41%

The largest recorded declines were experienced by a diverse range of transitory migrant shorebird species that are dependent upon different parts of estuarine systems and on different prey items, including shellfish-rich mudflats (Great Knot), sand- mudflats (Spoon-billed Sandpiper), and tidal creeks and wetlands in the hinterland (Black-tailed Godwit and Sharp-tailed Sandpiper). We recorded an increased number of five species. The largest increase was suggested by Broad-billed Sandpiper. However, this is probably due at least in part to the later timing of the final count cycle between years as noted above. Three out of the remaining four species with an apparently increasing trend (Grey Plover, Sanderling and Eurasian Curlew) are present in the ROK during the boreal winter (Moores 2006). Most of the decline in the numbers of shorebirds supported by the Study Region was due to declines in numbers within the SES, which far outweighed the increases of shorebirds recorded within the Geum Estuary and Gomso Bay.

4.3.5.2 The SES Based only on the sum of peak counts, 181,755 shorebirds were recorded within the SES. Between 2006 and 2008, 16 out of the 20 main shorebird species showed declines that totalled >126,000 (Table 4.9). The largest declines in number were shown by Great Knot (>74,000), Dunlin (>37,000) and Mongolian Plover (5,327). The largest declines in percentage terms were shown by Sanderling (96%), Sharp-tailed Sandpiper (94%) and Spoon-billed Sandpiper (91%). 138

Table 4.9 Changes in peak counts within the Saemangeum Estuarine System between 2006 and 2008 of the 20 main shorebird species, and of the sum of shorebirds recorded during the highest count cycle in the three years. 2006 2007 2008 Change Change in % 2006-2008 2006-2008 Sanderling 222 3 8 - 214 - 96% Sharp-tailed Sandpiper 654 230 36 - 618 - 94% Spoon-billed Sandpiper 34 31 3 - 31 - 91% Mongolian Plover 5,914 1,888 677 - 5,237 - 89% Black-tailed Godwit 613 425 65 - 548 - 89% Great Knot 86,288 31,739 11,994 - 74,294 - 86% Far Eastern Curlew 2,261 1,470 499 - 1,762 - 78% Common Greenshank 912 558 221 - 691 - 76% Nordmann's Greenshank 14 7 4 - 10 - 71% Ruddy Turnstone 744 417 255 - 489 - 66% Dunlin 62,508 31,074 24,744 - 37,764 - 60% Terek Sandpiper 3,855 2,650 1,623 - 2,232 - 58% Whimbrel 1,028 997 551 - 477 - 46% Bar-tailed Godwit 5,826 4,161 3,190 - 2,636 - 45% Red-necked Stint 5,154 4,115 3,565 - 1589 - 31% Broad-billed Sandpiper 338 155 244 - 94 - 28% Grey Plover 2,179 3,488 2,238 + 59 + 3% Far Eastern Oystercatcher 227 249 324 + 97 +43 % Grey-tailed Tattler 233 176 430 + 197 + 85% Eurasian Curlew 83 216 213 + 130 + 157% Sum of 20 Main Species 179,087 86,056 52,892 - 126,195 - 70% Highest Count Cycle 176,954 68,743 44,044 - 108,211 - 61%

There were increased numbers of four species. The apparent increase in Grey-tailed Tattler Tringa brevipes could be in part a result of the earlier completion of fieldwork in 2006 compared to later years. The increase in Far Eastern Oystercatcher was due in part to the increased number of birds that had established breeding territories in upper (and now permanently dry) areas of tidal-flat which had been regularly inundated before seawall close. The increase in Grey Plover (although very slight) and of Eurasian Curlew (larger than can be accounted for by the increase in identification rate of curlews) appeared to be a continuation of an increasing trend that was already established before seawall closure (KARICO 2003-2005). Counts of 2,780 Grey Plover and >2,000 Eurasian Curlew were made within the SES during the boreal winter between 1999 and 2000 (Moores 1999a, unpublished data). It seems likely that some of the small increase in Grey Plover and of Eurasian Curlew that we recorded might therefore have been due to an increased number of birds delaying northward migration, so that overwintering birds overlapped more obviously in timing with those birds that had overwintered further south. 139

4.3.5.3 The Geum Estuary The number of shorebirds recorded by the SSMP within the Geum Estuary (and thus the site‘s international importance) increased between 2006 and 2008. In 2006, the number recorded was less than the 70,939 shorebirds counted there during northward migration by the NIER in 2004, despite more intensive survey coverage by the SSMP. In 2007, the highest count cycle count increased by >26,000 (with some of this increase likely due to increased coverage), and then in 2008, the number increased again, but more slightly, by a further 4,000. However, the sum of the peak counts of the 20 main shorebird species increased between 2006 and 2007 before falling >14,000 in 2008 (Table 4.10).

Table 4.10 Changes in peak counts within the Geum Estuary between 2006 and 2008 of the 20 main shorebird species, and of shorebirds recorded during the highest Count Cycle. 2006 2007 Change 2008 Change Change 2006 - 2006- 2006-2008 2007 2008 Common Greenshank 1,482 209 - 1,273 399 - 1,083 - 73% Black-tailed Godwit 930 1,202 + 272 311 - 619 - 67% Sharp-tailed Sandpiper 1,014 642 - 372 361 - 653 - 64% Whimbrel 1,215 468 - 747 519 - 696 - 57% Great Knot 29,838 50,000 + 20,162 13,780 - 16,058 - 54% Far Eastern Oystercatcher 1,225 774 - 451 690 - 535 - 44% Nordmann's Greenshank 70 51 - 21 56 - 14 - 20% Far Eastern Curlew 2,582 1,405 - 1,177 2,360 - 222 - 9% Ruddy Turnstone 695 603 - 92 690 - 5 - 1% Bar-tailed Godwit 12,479 9,500 - 2,997 13,175 + 696 + 6% Red-necked Stint 719 2,127 + 1,408 1,144 + 425 + 59% Grey Plover 3,004 3,601 + 597 4,763 + 1,758 + 59% Terek Sandpiper 1,629 2,268 + 6,39 3,301 + 1,672 + 103% Dunlin 23,310 38,664 + 15,354 53,565 + 30,255 + 130% Eurasian Curlew 428 451 + 23 1,103 + 675 + 158% Mongolian Plover 1,691 4,385 + 2,694 4,385 + 2,694 + 159% Sanderling 196 232 + 36 572 + 376 + 192% Grey-tailed Tattler 59 231 + 172 268 + 209 + 354% Spoon-billed Sandpiper 1 8 + 7 8 +7 + 700% Broad-billed Sandpiper 11 272 + 261 1,142 + 1,131 + 10282%

Sum of 20 82,578 117,093 + 34,495 102,592 + 20,014 + 24% Highest Peak Count Cycle 66,627 93,342 + 26,715 97,670 + 31,043 + 47%

Based only on the sum of peak counts, almost 145,000 shorebirds were recorded during the survey period. Fourteen species were recorded in internationally important concentrations. Ranked in terms of percentage of flyway population these were Great Knot (13%), Far Eastern Oystercatcher (12%), Nordmann‘s Greenshank (9%), 140

Mongolian Plover (7%), Far Eastern Curlew (c. 7%), Terek Sandpiper (6%), Bar-tailed Godwit (4%), Grey Plover (3%), Dunlin (3%), Eurasian Curlew (3%), Sanderling (2%), Whimbrel (2%), Common Greenshank (1%) and Broad-billed Sandpiper (1%). There was also a minimum count of eight Spoon-billed Sandpiper (likely >1% of the present global total: BirdLife International 2011). In 2007 there were possibly up to 13 present on Yubu Island (with possibly 11 full adults on May 17th and two presumed Second Calendar-years on May 21st). The pattern of increase or decrease between years was not the same for all species. Between 2006 and 2007, 12 of the Study Region‘s 20 main shorebird species increased and eight showed a decreasing trend. Most of the increase in total numbers in 2007 was the result of a count of 50,000 Great Knot at Yubu Island during the Second Count Cycle only. In 2008, 11 of the Study Region‘s 20 main shorebird species were recorded in the Geum Estuary in larger numbers than in 2006, with Dunlin showing the largest increase (an increase in peaks between 2006 and 2008 of >30,000). It seems likely, based on the decline of >37,000 Dunlin within the SES between 2006 and 2008, that most of this increase was comprised of birds that had been displaced by the Saemangeum reclamation.

4.3.5.5 Gomso Bay Based on the sum of peak counts, the SSMP recorded almost 10,000 shorebirds during northward migration between 2006 and 2008 in Gomso Bay. Survey effort prior to the SSMP found very few shorebirds there, and in 2006 the bay continued to support very few shorebirds, with the lowest count (in mid-April) of only one and the highest count of 901. While it is possible that the First Count Cycle in 2006 failed to find all the shorebirds present on that date, a reconnaissance survey ten days earlier on April 5th recorded only 38 shorebirds. Numbers increased in 2007, and between 2006 and 2008, none of the 20 main shorebird species showed a decline, and 16 increased (Table 4.11). Unlike in the Geum Estuary, the upward trend in most species continued between years. In 2008, based on peak count cycle counts, Gomso Bay supported >8,600 shorebirds, with internationally important concentrations of Whimbrel and Terek Sandpiper (both species that tend to feed on crabs). There was also a large increase in the number of Great Knot: a mollusc specialist. Based on interviews with local fisherfolk and observations of fishing practices, Gomso Bay supports large concentrations of crabs but rather few shellfish. The peak of Great Knot in 2008 was <1% of estimated population, and the species was recorded only in the Second and 141

Third Count Cycles, even though Great Knot were present in the SES and the Geum Estuary during all four count cycles. It is therefore unclear whether large numbers of displaced Great Knot can be supported by Gomso Bay throughout a whole northward migration period.

Table 4.11 Peak counts of the main shorebird species and the highest count cycle counts of all shorebirds in Gomso Bay by year between 2006 and 2008. 2006 2007 2008 Change 2006-2008 Black-tailed Godwit 0 49 0 0 Broad-billed Sandpiper 0 0 1 + 1 Eurasian Curlew 4 1 6 + 2 Far Eastern Oystercatcher 3 6 14 + 11 Ruddy Turnstone 0 6 13 + 13 Red-necked Stint 16 0 33 + 17 Sharp-tailed Sandpiper 0 2 42 + 42 Grey-tailed Tattler 10 6 97 + 87 Grey Plover 71 159 213 + 142 Common Greenshank 55 111 204 + 149 Far Eastern Curlew 14 315 230 + 216 Mongolian Plover 1 1 226 + 225 Bar-tailed Godwit 0 34 284 + 284 Terek Sandpiper 149 157 615 + 466 Whimbrel 609 368 1,686 + 1,077 Dunlin 169 1,627 3,127 + 2,958 Great Knot 0 1,876 2,966 + 2,966 Total 1,101 4,718 9,757 + 8,656 Highest Peak Count Cycle 901 2,802 9,457 + 8,556 Note: there were no records in any year of three of the main shorebird species.

4.3.5.6 Changes in numbers of other shorebirds and waterbirds In addition to the 20 main shorebird species, 26 other shorebird species were recorded during the SSMP. Only six species had peak counts of >50. Three of these (Kentish Plover, Common Redshank and Red Knot) showed declines and three showed increases (Pacific Golden Plover Pluvialis fulva, Spotted Redshank Tringa erythropus and Wood Sandpiper Tringa glareola). The three species that declined are all strongly dependent on intertidal wetland. Kentish Plover decreased in both the Geum Estuary and the SES (despite increased breeding within the SES); Red Knot decreased in the SES, but remained similarly scarce in the Geum Estuary; and Common Redshank declined in the SES but increased in the Geum Estuary and Gomso Bay. The three increasing species are either ecologically dependent on intertidal wetland and the 142

adjacent hinterland (Pacific Golden Plover and Spotted Redshank), or almost exclusively on freshwater habitats (Wood Sandpiper). Additional waterbirds of global conservation concern in intertidal areas during SSMP fieldwork included Vulnerable Swan Goose (20 on April 1st 2008 in the Geum Estuary, remaining from the estuary‘s over-wintering population); Endangered Black- faced Spoonbill (all three wetlands, with 3-10 on several dates); Vulnerable Chinese Egret (all three wetlands, with <5 on several dates); Vulnerable Hooded Crane Grus monacha (including 15 in the SES on April 6th 2006 and 60 in Gomso Bay on April 4th 2008); Near-threatened Asian Dowitcher Limnodromus semipalmatus (one in 2006, none in 2007 and at least two in the Study Region in 2008); and Vulnerable Saunders‘s Gull (all three wetlands, with a high count of 81 at Yubu Island in April 2008, and observations of several pairs nesting in 2007 on reclaimed land between the Geum Estuary and Saemangeum). The population trends between 2006 and 2008 of these species are harder to determine than for the main shorebird species, because their anticipated peaks (except for Asian Dowitcher) lie outside the main period of fieldwork.

4.3.6 Habitat Change and Declines in the Study Region 4.3.6.1 2006-2008 The sum of maximum counts of all shorebird species per wetland per year in the Study Region fell 38%, from almost 264,000 in 2006 to 164,000 in 2008 (Table 4.12).

Table 4.12 Total number of shorebirds per wetland per year based on peak counts of all shorebird species. 2006 2007 2008 Saemangeum Estuarine System 179,930 82,692 51,560 Geum Estuary 82,725 117,440 102,853 Gomso Bay 1,139 4,753 9,848 Total 263,794 204,885 164,261

Fieldwork confirmed that there was a very substantial decline in the number of birds supported by the SES, especially following sea-wall closure. In 2006, there was a strong decline in numbers of some species within inner areas of the SES between mid- April and early May. In a few species including Black-tailed Godwit this could have been a continuation of a protracted decline in the same species earlier recorded by KARICO (2003-2005), perhaps caused by gradually reduced tidal-exchange and 143

worsening water quality as gaps in the sea-wall became narrower, or due more to the sudden reduction of tidal movement in April 2006. Between mid-April and April 21st, the last gaps in the seawall were closed, and by the end of the month high tides no longer reached upper tidal-flats or the inner parts of the estuaries. Within one week of seawall closure, huge numbers of shellfish in many elevated areas of tidal-flat came to the surface and died. Gaping open, they provided an easily accessible and abundant food source for some species of shorebird. In particular, large numbers of Great Knot and Dunlin were seen picking the flesh out of freshly-dead shellfish in the Simpo area, and while both species appeared to show a decreasing trend between 2003 and 2005 (KARICO 2003-2005) there was little (if any) evidence of either species being displaced in large numbers to adjacent wetlands in 2006. Instead, the number of shorebirds within the SES in 2006 continued to increase between late April and mid- May (as in previous years), when the peak of almost 177,000 shorebirds was recorded. While some species (including Great Knot) were able to gain mass (based on coarse assessment of abdomen profiles) and depart more or less on anticipated schedule, other species were likely negatively affected in 2006. The latter group includes Black-tailed Godwit. Although this species frequently feeds in rice-fields at high-tide (both within the Study Region and at other sites in the YSBR), the largest concentrations in the SES were in upstream river-channels (pers. obs.). In late April 2006, it was initially more numerous in the SES than in the Geum Estuary. However, as the river-channel tidal- flats dried out, numbers in the SES increased only slightly. During the same period, numbers in the Geum Estuary increased much more rapidly, in line with their anticipated migration timing. Numbers of shorebirds in the early part of northward migration 2007 were more or less similar to numbers at the same time of year in 2006. In mid-April 2007, 68,743 shorebirds were counted within the SES, compared to 73,711 in mid-April 2006. This included increased numbers of all three of the larger shorebirds that also regularly overwintered in the SES (Far Eastern Oystercatcher, Grey Plover and Eurasian Curlew). However, unlike in 2006 and previous years the total number of shorebirds, and especially of Great Knot, then started to decrease. Less than 55,000 shorebirds were counted within the SES at the end of April/beginning of May 2007. It is probable that large numbers of shorebirds at this time moved to the Geum Estuary. During the Second Count Cycle, 50,000 Great Knot were counted at Yubu Island. These birds cannot be considered to have successfully relocated to stage within the Geum Estuary, 144

however. Frequent aggressive interactions between normally highly gregarious and tolerant Great Knot were observed, including pecking and wing-tugging, suggesting that densities in the Geum had become unsustainably high. Large numbers of birds apparently disappeared from the Geum Estuary shortly after this peak count; the number of Great Knot both at the Geum Estuary and within the Study Region declined between the Second and Third Count Cycles (instead of peaking in number in mid- May as in previous years); and the peak counts of Great Knot within the Geum Estuary and the Study Region were both much lower in 2008 than in 2007. By 2008, the number of shorebirds supported by the SES had fallen markedly in all count cycles, and based on the sum of peak counts of all species there was also a decline at the Geum Estuary between 2007 and 2008. The increase in numbers recorded in Gomso Bay represented only a small proportion of the total numbers of birds lost to the Study Region. The majority of shorebirds were therefore no longer able to be supported by the SES 1-2 years after seawall closure; and the majority of shorebirds were not able to successfully relocate to the two adjacent wetlands. The results also suggest that further declines might be anticipated in the Study Region. These are predicted (1) if remaining areas within the SES that had tidal influence in 2008 continue to be converted to freshwater or land; (2) if displaced birds fail to find optimal feeding conditions within Gomso Bay and the Geum Estuary (see below); and (3) if degradation of the Geum Estuary continues through changes in sedimentation and water quality caused by Saemangeum reclamation activities and other infrastructural development.

4.3.6.2 Previous Research and Evidence of Declines before Seawall Closure Prior to a series of twentieth century reclamation projects, the SES was the indented inner part of a more or less unbroken system of intertidal wetland that extended approximately 160km north-south. It was fed by eight or more rivers, including the Geum. By the late 1990s, the SES was confined to two free-flowing estuaries divided by a triangular headland (Simpo), and separated from the Geum Estuary to the north by a reclamation project started in the mid-late 1980s (Long et al. 1988). Construction of the Geum barrage and other reclamation projects within the SES will likely have caused declines in shorebirds, but numbers of shorebirds supported by this system in its historical condition are unknown. The first shorebird survey in the SES was conducted in 1988. Only small numbers of birds were recorded 145

at that time, likely due to a combination of access restrictions, unsuitable tides and the dates of survey (Long et al. 1988). Survey effort increased gradually during the 1990s. Between 1993 and 1996, the Mangyeung and Dongjin Estuaries were surveyed on a total of eight dates, in mid-May and again between September 7th and October 21st. Peak counts included 52 Nordmann‘s Greenshank (Kim et al. 1997). Kim et al. (1997) also included count summaries of other researchers to identify a total of 13 species of shorebird that had by that time been recorded in the SES in internationally important concentrations (based on estimates in Wetlands International 2006). Moores (1999a, 1999b) conducted counts on 12 dates in 1998 and 1999, supported by a scribe who recorded counts (see Methods in Chapter 5). Additional counts (ten days in total) were also made during the boreal winter in 1999/2000 and January 2001 (unpublished data). No counts were conducted in the boreal summer (June-July). All counts were incomplete, and during both migration periods several species were recorded in lower numbers than by NIER teams conducting simultaneous counts at several high-tide roosts on similar dates. The vastness of the tidal-flats meant that most shorebirds could only be observed at spring high tide roosts (which were largest in salt- pans at Okgu and in salt-marsh near Hwapo). Species‘ abundance and diversity was assessed as highest during northward migration, lower during southward migration, and lowest during the boreal winter. The survey identified the SES as the most important natural wetland in the ROK for shorebirds and other waterbirds (Moores 1999b). In total, internationally important concentrations of 12 species of shorebird and four other waterbird species were recorded by this limited survey effort. Substantial differences in species‘ composition and relative abundance were evident in different parts of the SES (e.g. in inner and outer areas) and between and within seasons suggesting that greater survey effort would find much larger numbers of birds. The NIER estimated that 316,000 shorebirds staged during northward migration in the SES annually between 1997 and 2001 (Yi 2003, 2004). Between 1998 and 2003, due to a continued increase in survey-effort and improved site-knowledge, a total of 53 shorebird species were recorded in intertidal areas and the adjacent hinterland of the SES. A minimum 18 shorebird and nine other waterbird species were recorded in internationally important concentrations (Moores 2003e). These included peak counts of 180 Spoon-billed Sandpiper in the Mangyeung Estuary and of 100 in the adjacent Dongjin Estuary (Barter 2002). 146

Between 2003 and 2005 there was a gradual increase in the time lag between predicted and actual high-tide times within the SES; disappearance of the Mangyeung tidal bore; and a decrease in high tide heights. At least until 2005, highest spring high tides within the SES were only c. 50 cm smaller than those experienced in Gunsan. Highest tides therefore still reached >7m and inundated all intertidal areas (pers. obs.). During the same period, survey by NIER and KARICO suggested that declines took place in many bird species within the SES. The NIER recorded 207,000-240,000 shorebirds during northward migration in the SES between 2001 and 2003; 167,000 shorebirds in 2004; and 141,000 shorebirds in 2005 (NIER unpublished data). Bird survey once a month between April and November (2003-2005) also found a rapid decline in waterbirds, with 29% fewer birds counted in 2005 than in 2003 (KARICO 2003, 2004, 2005). Nonetheless, at least 20 waterbird species were recorded in internationally important concentrations during this period. Maximum counts of 15 of these species (including 12 species of shorebird), are shown in Table 4.13. It is likely that some of the year-to-year differences in peak counts published by KARICO (2003, 2004, 2005) might be due to differences in counting conditions which were not fully documented. However, several species (including Common Greenshank) showed only small differences in number between years, suggesting either a reasonably consistent count method and/or little change in numbers of that species between years. Some species, by contrast, showed rapid declines.

Table 4.13 Maximum counts each year of 15 waterbird species found in internationally important concentrations within the Saemangeum Estuarine System, April-November 2003- 2005 (from KARICO 2003, 2004, 2005). Species 2003 2004 2005 Change Change 2003-2005 2003-2005

Kentish Plover 10,810 5,300 1,410 - 9,400 -87% Black-tailed Godwit 12,230 1,951 4,970 - 7,260 - 59% Mallard 80,084 66,480 45,282 34,802 -43% Black-faced Spoonbill 48 30 29 19 -40% Red-necked Stint 1,590 4,300 1,160 - 430 - 27% Dunlin 41,300 36,000 32,420 - 8,880 - 22% Great Knot 94,500 123,745 79,950 - 14,550 - 15% Common Greenshank 2,087 1,901 1,984 - 103 - 5% Mongolian Plover 5,470 4,800 5,937 + 467 +9% Bar-tailed Godwit 3,180 5,501 4,586 + 1,406 + 44% Grey Plover 4,535 9,790 6,532 + 1,997 +44% Eurasian Curlew 1,386 1,505 2,013 + 627 + 45% Far Eastern Curlew 1,315 1,150 3,559 + 2,244 + 171% Terek Sandpiper 905 3,472 3,134 + 2,229 +246% Saunders‘s Gull 35 76 195 + 160 + 457% Sum of maxima of all 316,628 302,859 226,332 - 90,296 - 29% species / year

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At least one of the declines within the SES recorded by KARICO survey appeared similar to national trends recorded by other survey effort, including the MOE winter bird Census (MOE Census) (i.e. the steep decline in Mallard: see Chapter 2, Section 2.5.7.2). Some declines apparently exceeded recorded declines during the same period elsewhere in the ROK (e.g. Kentish Plover), or were opposite to the national or global trend (e.g. Black-faced Spoonbill). Declines in such species therefore appeared to suggest a more local cause, as did the fall in total numbers recorded. A diverse range of species associated with a broad range of habitat types showed declines. The exact causes of decline therefore remain unknown. For example, Mongolian Plover (which was often found in the same areas of the SES as Kentish Plover before seawall closure) was recorded in approximately similar numbers each year of the survey, while Kentish Plover declined 87% in the SES between 2003 and 2005. In the ROK and within the SES, Kentish Plover often feeds on crabs and declined, while other species that also often feed on crabs (including Terek Sandpiper, Far Eastern Curlew and Saunders‘s Gull) were all recorded in greatly increased numbers between years. The decline in Kentish Plover might have been in part a result of Principal Pressures in other parts of the Flyway (and a decline in the species was also recorded in Japan by Amano et al. 2010). However, the increase within the SES of Far Eastern Curlew and Saunders‘s Gull (both globally Vulnerable) contrasted with the declining trend in both species detected elsewhere in the EAAF (BirdLife International 2011). During northward migration in 2006, NIER researchers recorded 140,630 shorebirds in the SES: a decline of only 600 shorebirds compared with 2005. By 2007, the number they recorded had fallen to only 32,350 (NIER unpublished data). However, their survey effort in 2007 did not include counts on tidal-flat islands that needed to be reached by boat (Yi Jeong-Yeon pers. comm., May 2007). Thus, while NIER counts were lower than those recorded by the SSMP (perhaps due to the smaller count teams and less comprehensive coverage), they also identified a similar decline to the SSMP in shorebird numbers following seawall closure between 2006 and 2008, and they also identified a longer-term decline between 2003 and 2005. Moreover, shorebird declines were not confined to northward migration periods. During southward migration, the NIER recorded 151,000-192,000 shorebirds within the SES between 2002 and 2004, but only 68,139 shorebirds in 2005 and <39,000 shorebirds in 2006 (NIER unpublished data).

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4.3.6.3 Previous survey, displacement and declines at the Geum Estuary Large areas of intertidal wetland at the mouth of the Geum River were reclaimed during the twentieth century. In addition, an estuarine barrage was constructed in the 1980s resulting in strict regulation of discharge into the estuary. A total of 137 large dams had been completed within the Geum River basin by 2004 (KWRC 2004), and more dams are now under construction (Moores et al. 2010). Before the construction of the estuarine barrage, saltwater used to penetrate a further 55km upstream (Kim et al 2006). The historically extensive brackish and upstream tidal zone, stretching for several kms, has been replaced by a freshwater reservoir above the barrage and largely marine conditions below it, apart from after heavy rain events when sluices are opened (Moores 1999b). Such changes have likely had pronounced effects on the estuary and perhaps also on populations of shorebirds. Sediment loads and deposition patterns have also changed (Kim et al. 2006). There is almost no information on shorebirds or other waterbirds supported by the Geum Estuary before the mid-1980s. However the largest known concentrations globally of Crested Ibis were apparently recorded in the river‘s floodplain in 1911, and a pair of Crested Shelduck (now probably globally Extinct) was collected in the estuary in 1913 or 1914 (Austin 1948). Seventy years later, Ham & Lee (1985) conducted the first published waterbird survey in the Geum Estuary, and recorded 850 Far Eastern Oystercatcher during the mid-winter period. The first shorebird-specific surveys were conducted on three dates during northward migration in 1988, including the first research visit to Yubu Island. However, access throughout much of the estuary was restricted, and only low numbers of shorebirds (<3,000 in total) were observed (Long et al. 1988). In 1998, Moores (1999a) conducted shorebird counts along the river channel and along the Janghang-Janggu coastline on three dates in April-May, once in August and September, and on two dates in February 1999. Six Nordmann‘s Greenshank and internationally important concentrations of at least seven species of shorebird were recorded, including 18,850 Great Knot, 2,049 Black-tailed Godwit and 2,896 Far Eastern Oystercatcher. Shorebird diversity and abundance were highest during northward migration, lower during southward migration and lowest during the boreal winter. Based on the sum of peak counts, >37,700 shorebirds were counted from mainland sites alone. Between August 1999 and July 2000, Lee et al. (2002) conducted counts at one high-tide roost at Yubu Island on one date per month, timed to coincide with highest tides. Great Knot was the commonest shorebird (with a peak count of 149

24,800), and 30 breeding pairs and a peak count in mid-winter of 3,200 Far Eastern Oystercatcher were also recorded. In total, seven shorebird species were found in internationally important concentrations. There were also peak counts of seven Spoon- billed Sandpiper and four Nordmann‘s Greenshank. Between 2001 and 2003, annual NIER survey effort during northward migration found 24,500-44,900 shorebirds within the whole Geum Estuary. In 2004, the number recorded increased by 42,000 to reach 71,000. The same northward migration period, numbers of shorebirds counted by the NIER within the SES fell by >58,000. It appears likely that at least some of this increase in the Geum Estuary in 2004 was therefore caused by displacement of birds from the SES. Between 2004 and 2005, numbers within the SES and also in the Geum Estuary fell (at the latter site to only 21,320), suggesting that previously displaced shorebirds from the SES had not been able to stage successfully within the Geum Estuary. In 2006 and 2007, the NIER recorded 65,967 and 51,573 shorebirds respectively during northward migration (NIER unpublished data), compared with 82,578 and 117,093 shorebirds recorded during the same period by the SSMP. It is unclear why numbers recorded by the NIER increased at the Geum Estuary but remained almost unchanged within the SES during northward migration in 2006. However, perhaps due to smaller team sizes the NIER recorded 20- 56% fewer shorebirds than the SSMP teams during 2006 and 2007 within the Geum Estuary. Although there is a paucity of robust data, previous count data suggest that the Geum Estuary was unable to sustain large numbers of shorebirds displaced by the Saemangeum reclamation before seawall closure. Small count teams recorded several species, including large numbers of Great Knot, and small numbers of Spoon-billed Sandpiper and Nordmann‘s Greenshank, in the Geum Estuary even before the large- scale declines of shorebirds and other waterbirds within the SES between 2003 and 2005 and before Saemangeum seawall closure in 2006.

4.4 DISCUSSION

4.4.1 Reclamation and Shorebird Declines The present study found a minimum 179,930 shorebirds within the SES during northward migration in 2006, and measured a decline of 60%-70% in this number within the SES by 2008. A minimum 128,000 shorebirds were lost to the SES during northward migration in only three years. This is a more rapid rate of decline than 150

would be predicted by already-ongoing declines in many of the same species on the EAAF (as for example estimated in Japan by Amano et al. 2010). However, the total number of shorebirds directly affected by the Saemangeum reclamation is likely to be much higher than the number of birds we recorded. First, our estimates are based on peak counts and do not include any allowance for turnover, which would increase the numbers of affected birds further. Second, the SSMP was focused only on northward migration over a three-year period. The conversion of >40,000ha of tidal-flat and sea-shallows to freshwater habitats and to dry land at Saemangeum is a long process that has already taken two decades, and will eventually lead to the loss of the SES to almost all shorebirds and other waterbirds that are ecologically-dependent on intertidal wetland. There are no earlier studies we are aware of that document changes to the numbers of birds caused by large-scale reclamation in the ROK or in the Yellow Sea. However, a series of smaller reclamations in Hakata Bay, Japan (described in Moores 1997) resulted in a series of declines in migratory waterbirds that took place over >10 years which suggest several similarities. Between 1984 and 1991, >200,000 over-wintering waterbirds (mostly Anatidae) were supported by the whole of Hakata Bay annually. This number had fallen to 80,000 waterbirds by 1996 following the completion of one reclamation project (<150ha) and the start of a second (400ha), both in the eastern part of the bay. In the eastern part of the bay, the number of waterbirds counted during annual one-day counts in January showed almost no variation between 1989 and 1992 (range 29,049- 29,288). Following the completion of a seawall in mid-1992, tidal movement to the largest tidal-flat (80ha) was reduced and there was an immediate 64-65% decline (1993-1994). Start of the second reclamation project in mid-1994 then coincided with a further rapid fall of 30% in waterbird numbers. Numbers then apparently reached a revised, reduced state of dynamic equilibrium for the next two years (1995-1996). Declines in waterbirds were attributed to reduced tidal exchange and increased disturbance caused by each new construction phase, which resulted (each time) in worsening water quality in the whole wetland and changes to potential roosting and feeding areas within and close to reclamation sites. Habitat change affected different species differently. Between 1991 and 1996, some shorebird species increased before decreasing again as they used newly-reclaimed areas, either for feeding (Dunlin) or for nesting (Kentish Plover). Other species, including small numbers of Great Knot and Sanderling (maximum 155 and 550 respectively during southward migration in 1991) 151

were restricted to feeding on natural tidal-flats adjacent to the reclamation sites. Even though these tidal-flats remained intact, Great Knot using them declined 85% during weekly autumn counts between 1991 and 1992, and in total by 95% by 1996. Similarly, Sanderling declined 55% between 1991 and 1992 and in total by 87% by 1996. As in Hakata Bay, the SSMP data suggest different rates of decline in some species than others, caused by complex variations in response (at the species-level and perhaps at the level of population or individuals) to habitat change. There were steeper declines recorded in some species between 2006 and 2007 (e.g. Sharp-tailed Sandpiper) than in others (e.g. Great Knot). However, declines in almost all species were recorded between 2006 and 2008 in addition to declines in species that included Kentish Plover and Black-tailed Godwit already ongoing since at least 2003 (KARICO 2003, 2004, 2005).

4.4.2 Longer-term Declines There are too few data to estimate the number of shorebirds supported historically by the SES. It is known, however, that construction of the outer seawall started in 1991 and that survey effort resulted in an NIER estimate of 316,000 shorebirds during northward migration in the SES between 1997 and 2001 (Yi 2003, 2004). The NIER then identified large declines in many shorebird species, especially between 2003 and 2005 (NIER unpublished data), a period in which tides became increasingly restricted by construction of the outer seawall. During northward migration in 2006 (using the same count methods as in previous years) the NIER counted only 140,630 shorebirds within the SES: a decline of >40% in shorebird numbers over five years. These declines are similar to those recorded of all waterbirds by KARICO (2003-2005). Data therefore suggest that there was a decline of c. 175,000 shorebirds during northward migration between 1997 and 2006 (based on NIER estimates and counts), and a further fall of 128,000 between 2006 and 2008 (based on SSMP data). By 2008, there were only 51,560 shorebirds counted within the SES (by the SSMP), with most of these birds restricted to the outermost parts of the system where there was still some limited tidal exchange. We predict that almost all of these remaining shorebirds will also be lost to the SES as reclamation work continues and the presently-inundated brackish sea-shallows are converted to a freshwater reservoir.

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4.4.3 Displacement to Adjacent Wetlands Reclamation proponents asserted that shorebirds would easily relocate from the SES to adjacent wetlands. The present survey found evidence that there was some relocation of shorebirds to adjacent wetlands in 2007 and 2008. However, this accounted for only 30,000-40,000 shorebirds. More than 100,000 shorebirds were lost to the SSMP Study Region as a whole between 2006 and 2008. Furthermore, there is no evidence to support the assumption that these shorebirds will be sustained at the two adjacent sites in coming years. The Geum Estuary and Gomso Bay together supported 107,000 shorebirds during northward migration in 2008. This is only approximately one-third of the estimated number of shorebirds lost to the SES since 1997-2001, and less than the number lost to the SES since 2006. The increase of c. 30,000 shorebirds supported by the Geum Estuary between NIER counts in 2004 and SSMP counts in 2006 and 2008 similarly represents less than a fifth of the shorebirds lost to the SES since 2004. Gomso Bay supported very few shorebirds in both 1998 (during southward migration and in winter) and 2006 (during northward migration). There is therefore no evidence that a substantial proportion of birds lost to the SES between 1997 and 2006 were able to stage there annually. Numbers did increase in Gomso Bay in both 2007 and 2008. Even in 2008, however, Great Knot were only recorded in two of the four count cycles, suggesting that Gomso Bay remains a suboptimal site for this species.

4.4.4 Declines during Southward Migration A very large number of shorebirds were also formerly supported by the SES during the boreal winter and especially during southward migration. MOE survey between 1997 and 2001 led to an estimate of 257,000 shorebirds supported by the SES during southward migration (Yi 2003, 2004). There is no evidence that the majority of these shorebirds were able to relocate to the adjacent Gomso Bay or Geum Estuary. Yi (2003, 2004) estimated that 36,300 shorebirds were supported by the Geum Estuary between 1997 and 2001. Between 2001 and 2006 the NIER recorded a mean of c. 23,000 shorebirds per year during southward migration, with a maximum of 52,327 in 2001 and a minimum of 15,611 in 2005. In 2007, the same survey effort recorded 19,046 shorebirds there (NIER unpublished data). This latter count compares with 47,430 shorebirds (based on simple addition of peak counts) recorded during the same period by an SSMP team. Even with more intensive survey effort, we still therefore recorded 153

fewer shorebirds in the Geum Estuary in 2007 than were recorded there by the NIER in 2001.

4.4.5 Concluding Remarks The present research proves that most shorebirds were unable to remain within the impounded areas of the SES 1-2 years after seawall closure. The majority of displaced shorebirds were also unable to relocate successfully to either the Geum Estuary or Gomso Bay. Related research programs have also confirmed that the majority of shorebirds displaced from the SSMP Study Region did not successfully relocate to other internationally-important shorebird sites in the ROK (Chapter 5). Moreover, several of the species that showed large declines before and following seawall closure at Saemangeum have also shown rapid and substantial declines large enough to be detected in the EAAF outside of the ROK in the boreal winter during the same period. Preliminary analysis of count data for five species predicted to decline in Australia as a result of the Saemangeum reclamation by Rogers et al. (2009) suggested that all five showed an abrupt decline in at least some study areas in north-western Australia in the two years that followed seawall closure. These included Great Knot, which declined 23.9% at Eighty Mile Beach from levels recorded in 1999 and 2001. This decline corresponded closely with the 23.9% decline in overall non-breeding populations predicted as a result of the loss the SES. The recent global decline in the population of Great Knot has therefore been attributed to recent reclamation projects including Saemangeum (Moores et al. 2008, BirdLife International 2011). Spoon-billed Sandpiper has also declined very rapidly in the 2000s. This has also been attributed largely (Moores et al. 2008, Birds Korea 2010) or in part to habitat loss, including the Saemangeum reclamation (Pain et al. 2011). The SSMP data therefore provide no support for the assumption that shorebirds can easily move their habitat to adjacent or other intertidal wetlands once a major staging site is reclaimed. Rather, our data and earlier government surveys prove that there have been massive and in some cases prolonged declines in many species of shorebird caused by the Saemangeum reclamation. In combination with other surveys the SSMP data therefore support our hypothesis that loss of a major staging site through reclamation in the Yellow Sea can, and already has, caused population-level declines in some migratory shorebird species.

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CHAPTER 5

AN ASSESSMENT OF CHANGES IN SHOREBIRD NUMBERS IN THE ROK BETWEEN DECADES: NATIONAL SHOREBIRD SURVEY, MAY 2008

ABSTRACT There is only a short history of shorebird research in the ROK. Most sites of international importance for shorebirds were identified between 1988 and 1999. In the late 1990s and early 2000s, at least 21 species of shorebird were found regularly in internationally important concentrations in intertidal wetlands in the ROK during northward migration. However, three-quarters of historical tidal-flat area, including two-thirds of that which remained in 1987, have been lost to reclamation. Several of the most important shorebird sites have been partially or completely reclaimed. We therefore surveyed the ROK‘s most important remaining shorebird sites in May 2008 in order to determine whether there was evidence of population declines or of shorebirds maintaining their numbers by relocating from reclaimed areas to remaining intertidal wetland. Despite the limitations of the data gathered in 1988, 1998 and 2008 through northward migration and differences in count methods between years, we found strong evidence of decline between decades, including in the globally Vulnerable Great Knot and the Near-threatened Black-tailed Godwit. The same populations of these species that stage in the Yellow Sea have also suffered sharp declines in recent decades in well-surveyed non-breeding areas in Australia. We found no strong evidence that any shorebird species was able to relocate without decline to new areas once optimal staging sites like the Saemangeum Estuarine System (SES) were lost. Instead, it is almost certain that further declines in many species will take place as recently-reclaimed areas lose their capacity to support shorebirds remaining within them, and as new reclamation projects proceed. The survey provides further support for our hypothesis (presented in Chapter 4) that loss of a major staging site through reclamation in the Yellow Sea causes population-level declines in migratory shorebird species

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5.1 BACKGROUND AND AIMS 5.1.1 Introduction Twenty-one species of shorebird (as defined in Chapter 3) are found regularly in Ramsar-defined internationally important concentrations in the ROK during northward migration. All of these species are ecologically dependent upon intertidal wetland during migration, although four also regularly use rice-fields for feeding. However, two-thirds of intertidal wetland in the ROK that existed in 1987 has since been lost to reclamation (Chapter 3). Many remaining areas have been affected by the damming of estuaries and suffer from over-use, pollution and the reduced health and flow of rivers (Barter 2002, UNDP-GEF 2007). There have also been many changes to agricultural areas since the 1950s, with increased use of agricultural chemicals (see Chapter 1, Section 1.5.3) along with increased infrastructure and intensification of use (Moores 2006). It is therefore anticipated that many species of migratory shorebird in the ROK will be in decline, as suggested by recent research on the same populations of these species in other regions (Rogers et al. 2009, Amano et al. 2010, Garnett et al. 2011, Wilson et al. 2011). However, there is a short history of shorebird research in the ROK, and there has been no assessment of shorebird population trends at the national level.

5.1.2 Previous Shorebird Survey (1988 & 1998) The first shorebird surveys in the ROK covering more than a few sites were conducted by Long et al. (1988). These counts followed an initial study of topographical maps to identify potential research sites. Between April 10th and June 6th, >30 areas were visited, most around high tide, and likely shorebird roosts were located. Nearby rice-fields were visited at other times. In all areas, all birds were counted using binoculars and tripod-mounted telescopes. In total, 14 people were involved in the count-effort. However, due to access restrictions and the size of tidal-flats, coverage was described as complete at only one site (South Ganghwa, counted on eight dates). The remainder of sites had partial or incomplete coverage. Some of these were counted six or seven times (including Namyang Bay and Asan Bay), and others were counted only once or twice at high tide (Yeongjong) or during neap tides (including the Mangyeung and Dongjin Estuaries: i.e. the Saemangeum Estuarine System or SES). This pioneering survey work found four previously unrecognized internationally important shorebird sites, and improved greatly on the knowledge base of the distribution and numbers of shorebirds in the ROK. The survey also raised concerns 156

about the impacts on shorebird populations of the numerous ongoing and planned reclamation projects. Most other internationally important shorebird sites, including the SES and the Geum Estuary were not surveyed adequately until the late 1990s (Kim et al. 1997; Moores 1999a; Yi 2003, 2004). In 1998, the present author conducted counts of shorebirds at >20 wetlands between April 13th and May 27th (Moores 1999a, 1999b). Wetlands were selected based on Long et al. (1988) and Kim et al. (1997), on satellite images, and on information from local environmental organisations. Reclamation had apparently changed potential counting conditions at a few of the wetlands, with some still difficult to access (e.g. Namyang Bay) and others (e.g. the Geum Estuary) easier to access than earlier reported by Long et al. (1988). In the latter areas, this enabled roost sites to be reached more easily and for better observation of exposed tidal-flats used by feeding shorebirds. Sites were visited during three ―circuits‖ of the south and west coasts, with each circuit taking between 12 and 13 days, and each site counted on only one or two dates per circuit. All sites with internationally important concentrations of shorebirds in the first circuit were counted again in the second and third circuits. Counts were made through a tripod-mounted telescope by one counter (the author) at high-tide roosts, though a few supplementary counts of selected species were also made at low tide and in extensive rice-field areas (the latter especially between Namyang and Asan Bay and between Seosan City and Cheonsu Bay). A boat was used to access roosts on islands in the Nakdong Estuary. Most of the counts were considered to be incomplete or partial, and only eight counts were assessed, perhaps optimistically, as likely to have recorded 80% or more of birds present (Moores 1999a). Such coarse assessments were based on the level of visibility; the size of the wetland; the state of the tide cycle (with spring high tides required for all west coast intertidal sites); the number of potential roost sites visited; and the ratio of roosting birds counted at high-tide to the number of feeding and flying birds seen on the falling tide. Comparison of counts made by this survey with those made by count teams from the National Institute of Environmental Research (NIER, within the Ministry of Environment) in 1998 and subsequently (on occasion at the same wetlands and on the same dates), suggests that many roost sites were missed and that the survey therefore substantially underestimated the number of birds present.

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5.1.3 Internationally Important Shorebird Sites in the ROK Although regular survey was continued at some of these sites through the 2000s, many of the data have not been made publicly available. Moreover, counts made with different survey methods can lead to large differences in count estimates, especially when survey methods are not documented sufficiently to enable subsequent workers to assess whether all key roosts were located and visited in suitable tide conditions (Rogers et al 2006b). Nationwide counts made in the late 1990s/early 2000s, especially those of the author (Moores 1999a) and by Yi (2003, 2004) provide probably the most accessible and easy to interpret baseline for identifying internationally important sites and also recent trends in shorebird numbers at these sites. This is because most of the same sites and roost-sites were counted by both Moores and Yi, and because many of the resultant count data were published together in Barter (2002). Between 1999 and 2001, approximately 20 sites (dependent upon delineation) were identified as internationally important for shorebirds in the ROK (Moores 1999a, Yi 2004). According to Yi (2003, 2004) who conducted shorebird research for the NIER, the ROK at that time supported an estimated 12.7% of the East Asian-Australasian Flyway‘s (EAAF) migratory shorebirds on northward migration, and 8.7% on southward migration. The two most numerous species during northward migration were Great Knot (~248,000) and Dunlin (~213,000). The eight most important shorebird sites were the Dongjin and Mangyeung Estuaries, both within the SES (Chapter 4), Namyang Bay, Yubu Island in the Geum Estuary, Yeongjong Island, Asan Bay, Ganghwa Island and Cheonsu Bay. Together, they supported 535,000 shorebirds during northward migration, and 388,000 shorebirds during southward migration. The next twelve most important sites combined supported only 100,000 and 55,000 shorebirds on northward and southward migration respectively. Thus, the eight most important sites supported 84% and 87% of the ROK‘s shorebirds on northward and southward migration respectively (Yi 2004). By the mid-2000s, shorebirds at many of these sites had been affected directly or indirectly by reclamation. For example, following seawall closure at Saemangeum in 2006, there was a large decline of shorebirds within the SES not compensated for by smaller increases in the number of shorebirds in the adjacent Geum Estuary and Gomso Bay, combined, the ―Saemangeum Shorebird Monitoring Program (SSMP) Study Region‖ (Chapter 4). At Ganghwa, research on benthos identified large declines in diversity between surveys conducted in 2003 and 2008. These were considered 158

likely to have been caused by increased pollution loads and physical changes in adjacent areas. Such changes included the construction of artificial structures and reclamation activities (Choi et al. 2010b).

5.1.4 Research Aims The present research had two inter-related aims. The first was to compare counts of shorebirds made with similar methods at many of the same sites in 1998 and in some cases in 1988. This would enable, for the first time, a comparison of shorebird numbers at the same sites made one or two decades apart. The second aim was to determine whether large numbers of shorebirds had been displaced by the Saemangeum reclamation following seawall closure in 2006 to other internationally important shorebird sites in the ROK. The survey was used to test the hypothesis that loss of an optimal shorebird staging site in the Yellow Sea to reclamation leads to declines in some species of shorebird at the population level.

5.2 METHODS Between May 2nd and 15th 2008, shorebird surveys were conducted at a total of 17 wetlands (Figure 5.1).

YSBR Sites

1. Ganghwa Island 2. Yeongjong Island 3. Song Do 4. Namyang Bay & Teibu 5. Honwon Ri 6. Asan Bay 7. Cheonsu Bay and Rice-fields 8. Geum Estuary 9. The SES 10. Gomso Bay 11. Baeksu 12. Hampyeong Bay & Meian Muan 13. Aphae Island 14. Mokpo Wetland 15. Haenam Hwangsan

Outside of the YSBR 16. Suncheon Bay 17. Nakdong Estuary

Figure 5.1 Location of wetlands surveyed in May 2008. 159

These wetlands included the SES; the six other most important sites identified by Yi (2004) in the Yellow Sea Blueprint Region (YSBR); and several additional internationally important wetlands earlier surveyed by the present author in 1998 (Moores 1999a). Counts were conducted by a total of 18 counters on one or more dates outside of the SSMP Study Region and 20 within it. The dates of survey were selected to include a week of spring high tides (essential for counting along the west coast, especially in the northwest, where tidal range is regularly >9m); to overlap with the third count cycle of the SSMP (see Chapter 4); and to enable comparisons to be made with counts made between April 29th and May 11th 1998 during the second count cycle of Moores (1999a). Counting was conducted by teams of experienced shorebird specialists (with two to four counters per team) using tripod-mounted telescopes, counting at high tide roost sites, and in some areas, also on falling or rising tides. Boat-based surveys were conducted within the SSMP Study Region (see Methods in Chapter 4) and in the Nakdong Estuary. After reconnaissance counts on May 2nd, simultaneous counts were conducted by four teams of counters on May 3rd (Yeongjong Island and Song Do) and May 4th (Ganghwa Island and Teibu Do); by three teams on May 5th (Namyang Bay and Asan Bay, and in rice-fields between them at Honwon Ri); two teams on May 6th (Seosan rice-fields and Cheonsu Bay); within the SES, Geum Estuary and Gomso Bay between May 6th and 12th as part of the SSMP; by one team on May 9th (Baeksu); two teams on May 10th (Hampyeong Bay, Meian Muan, Aphae Island); three teams on May 11th (Mokpo Wetland); and two teams on May 12th (Haenam Hwangsan and Suncheon Bay) and May 13th (Nakdong Estuary). Although access was improved at many of the wetlands when compared with 1998, many had been substantially changed by reclamation projects and infrastructure development. There was insufficient time and information to quantify changes to wetlands in much detail, even though such changes probably influenced both the accuracy of counts and the number of birds that were supported by each wetland in 2008 (and we predict in future years). However, some of the changes included: 1. At Ganghwa Island, infrastructure development since 1998 included new roads and new resort development. The whole tidal-flat is presently threatened by impoundment (Choi et al. 2010b, Kang 2010); 2. At Yeongjong Island, a new bridge and town development since 1998 has led to increased disturbance of feeding areas and the loss of several roost-sites. The northern tidal-flat is now threatened by impoundment; 160

3. At Namyang Bay, seawall closure in 2006 led to the loss of the whole inner bay, and six out of seven roost sites counted by Long et al. (1988) and Moores (1999a). Further reclamation is planned for an outer part of the estuary; 4. At Asan Bay, large-scale reclamation since 1998 has impounded the main tidal-flat used by feeding and roosting shorebirds. Infill and drainage of areas behind seawalls constructed since the early 2000s will lead to loss of the site to most shorebirds. 5. The Saemangeum Estuarine System was impounded by an outer seawall in 2006 (Chapter 4). A summary of changes to sites and access is provided in Table 5.1.

Table 5.1 Wetlands, survey dates and changes to sites between 1998 and 2008. Wetland Survey Survey Main Access Change Dates Dates Habitat 1998-2008 1998-2008 1998 2008

Ganghwa Island May 10 May 4 IW Same 4, 5, 6 Yeongjong Island May 10-11 May 2-3 IW Improved 3, 4, 5 Song Do - May 2-3 IW Improved 1,4, 5 Teibu Island May 9 May 4 IW Same 5 Namyang Bay May 8-9 May 5 IW Improved 1, 5 Honwon Ri May 8 May 5 RF Same 5 Asan Bay May 8 May 5 IW Same 1, 5 Cheonsu Bay May 6-7 May 6 IW, RF Improved 5, 6 Geum Estuary May 6 May 6-12 IW Improved 5, 6 SES May 5 May 6-12 IW, RF Improved 1 Gomso Bay - May 6-12 IW Improved 5 Baeksu - May 9 IW, RF Same 3 Hampyeong Bay May 3 May 10 IW Same 5 Aphae Island May 4 May 10 IW Improved 5 Mokpo Wetland - May 11 IW - - Haenam Hwangsan May 2 May 12 IW Same None Suncheon Bay April 30 May 12 IW, RF Improved 5, 6 Nakdong Estuary April 29 May 13 IW Same 3, 5, 6 Locations indicated in Figure 5.1, and coordinates are provided for the most important YSBR wetlands in Chapter 1, Table 1.1. Several of the sites were not surveyed in May 1998. IW=Intertidal Wetland, RF=Rice-fields. In ―Change‖, 1= Reclamation of >80% of site; 2= Reclamation of 30%-80% of site; 3 = Reclamation of 5%-30% of site; 4= Urbanisation; 5= Increased infrastructure (roads, harbours etc); 6= Increased disturbance.

5.3 RESULTS 5.3.1 Total Numbers In 2008, shorebird counts were carried out at all of the most important shorebird sites nationwide identified by Yi between 1997 and 2003 (Yi 2003, 2004) and by Moores (1999a), through the period of maximum annual shorebird abundance. The high level of experience within the counting teams, the favourable tides and weather, and the knowledge of the sites from previous survey work led to a high level of 161

confidence in the counts in all areas, with the exception of Meian Muan, an area suggested by previous shorebird survey work to hold more shorebirds during southward migration. In total, we recorded ~291,000 shorebirds. This was less than half of the 635,000 shorebirds estimated to be in the ROK during northward migration between 1997 and 2003 (Yi, 2004). This total was comprised of 147,577 shorebirds outside of the SSMP Study Region and 143,990 shorebirds within it. The counts of the 21 species regularly recorded in internationally important concentrations in the ROK are listed in Table 5.2.

Table 5.2 Numbers of shorebirds that occur in internationally important concentrations in the ROK that were recorded during the present survey, May 2008. 1% Intertidal Rice-field Inside Total Criterion Wetland Areas SSMP Outside Outside Study SSMP SSMP Region Study Region Study Region Far Eastern Oystercatcher 100 99 5 545 649 Grey Plover 1,300 5,122 0 5,912 11,034 Kentish Plover 1,000 212 3 427 642 Mongolian Plover 600 2,720 0 5,288 8,008 Black-tailed Godwit 1,600 92 1,974 278 2,344 Bar-tailed Godwit 3,300 11,510 0 16,259 27,769 Whimbrel 550 3,672 113 2,676 6,461 Eurasian Curlew 350 149 0 107 256 Far Eastern Curlew 380 2,206 0 1,616 3,822 Common Greenshank 1,000 1,968 50 824 2,842 Nordmann’s Greenshank 8 51 0 60 111 Terek Sandpiper 500 4,054 4 5,539 9,597 Grey-tailed Tattler 400 938 0 407 1,345 Ruddy Turnstone 1,000 672 0 715 1,387 Great Knot 3,800 26,385 0 21,593 47,978 Sanderling 220 113 0 578 691 Red-necked Stint 3,200 2,927 12 4,727 7,666 Sharp-tailed Sandpiper 1,600 33 511 106 650 Dunlin 17,500 75,421 0 75,577 150,998 Spoon-billed Sandpiper 30 0 0 11 11 Broad-billed Sandpiper 1,000 7 0 448 455 Others 239 1,063 197 1,499 Unidentified 5,202 50 100 5,352 Total 143,792 3,785 143,990 291,567 Note: 1% criteria are from Wetlands international (2006). These 1% estimates have recently been revised downward for several species by subsequent authors. Species marked in bold were recorded in highest numbers in SSMP fieldwork in 2008 during this survey period.

Twelve of the species, including Black-tailed Godwit, were recorded in their highest numbers in SSMP fieldwork in 2008 during this same time-period. These species are marked in bold in Table 5.2. Of the remainder, Far Eastern Oystercatcher, Eurasian Curlew and Far Eastern Curlew tend to peak in March or April, and Grey-tailed Tattler, Ruddy Turnstone and Broad-billed Sandpiper tend to peak after mid-May (Chapter 4, Table 4.5). Other species, including Great Knot, peaked in early-mid May during 162

previous survey periods and in the SSMP in 2006. A higher number of shorebirds were recorded during this early-mid May SSMP count cycle than during the other three SSMP count cycles in 2008. Although we missed the expected peak of migration of a few species, the timing of the survey was therefore confirmed as the period in which most species of shorebird peaked in number during northward migration in 2008. The results confirmed the importance of the SSMP Study Region to shorebirds. The three adjacent wetlands of the SSMP Study Region supported a similar number of shorebirds to the number recorded at all other internationally-important shorebird sites combined. As described in Chapter Four, however, the numbers of birds supported by the SSMP Study Region are predicted to continue to fall as areas within the Saemangeum reclamation are converted into dry-land.

5.3.2 Changes between 1998 and 2008 outside of the SSMP Study Region We recorded a total of 107,547 shorebirds in 2008 at eleven internationally important sites outside of the SSMP Study Region (Yeongjong Island, Ganghwa Island, Namyang Bay, Asan Bay, Cheonsu Bay, Hampyeong Bay, Aphae Island, Meian Muan, Haenam Hwangsan, Suncheon Bay and the Nakdong Estuary). This compares with 130,868 counted at the same sites between April 29th and May 11th in 1998 (Moores 1999a). There was therefore a decrease of >23,000 shorebirds recorded, despite improved access to some sites and the substantially improved capacity of counting teams in 2008 compared to 1998. Most of the decrease in total numbers was due to very large declines in two species, Great Knot and Black-tailed Godwit. Of the 21 internationally important shorebird species, 13 were recorded in increased numbers and six in lower numbers in 2008 than in 1998, and two species were recorded in the same numbers both years (with zero Spoon-billed Sandpiper and two Broad-billed Sandpiper both years). More than 1,000 individuals of ten species were recorded in both years. Six of these were recorded in increased numbers and four in decreased numbers in 2008 compared with 1998. There was no robust method with which to measure bias and likely stochastic error within and between the counts. However, it is reasonable to assume that some increase in Whimbrel and especially Far Eastern Curlew and some decrease in Black-tailed Godwit and Great Knot numbers were genuine. All four species are medium to large-sized (so easy to detect, even during the more rapid counting effort required in 1998); all were very familiar to all counters; and all were recorded in numbers with >45% difference between years (Table 5.3). 163

Table 5.3 Change in the number of the ten most numerous shorebird species counted at eleven internationally important shorebirds sites outside of the SSMP Study Region between 1998 and 2008. 1998 2008 Change

Grey Plover 3,293 3,978 +685 +17% Mongolian Plover 2,780 2,183 -597 -21% Black-tailed Godwit 22,656 2,055 -20,601 -91% Bar-tailed Godwit 7,855 9,747 +1,892 +24% Whimbrel 1,983 2,900 +917 +46% Far Eastern Curlew 1,365 2,032 +667 +49% Terek Sandpiper 2,915 3,571 +656 +23% Great Knot 33,881 18,135 -15,746 -46% Red-necked Stint 2,609 1,662 -947 -36% Dunlin 49,537 57,439 +7,902 +16% Total 128,874 103,702 -25,172 -20% Note: The eleven sites were surveyed between April 29th and May 11th, 1998 (Moores 1999a) and May 3rd to May 13th, 2008.

Some of the increase in Whimbrel, however, could have been influenced by the slightly later dates of survey, as this species tended to increase rapidly from late April during the SSMP 2006-2008 (with a mean peak date of May 9th: Chapter 4, Table 4.5). The species is also generally difficult to count well at high-tide because of its roost choices, which include sea-walls, fishing poles, or areas of rather dense vegetation, as opposed to the more open roost choices of many other shorebird species of intertidal wetland. Several count teams (as in 2008) would therefore have been more likely to find a larger number of roost-sites than a single counter (as in 1998). Far Eastern Curlew are early-departing migrants, though large numbers of pre- breeders or non-breeders are regular in June on tidal-flats in Gyeonggi Bay, with 500- 1000 recorded most years between Ganghwa and Yeongjong (unpublished data). The increased number recorded in 2008 compared with 1998 is difficult to interpret. The number of pre-breeding birds might be related to recent breeding success. Alternatively, it could be due to a genuine increase between years or instead due to delayed northward migration as a result of reduced fitness (as suggested for several larger shorebirds within Saemangeum). Some of the increase might also have been due to displacement of some birds from the SES following seawall closure. If so, the increase of 667 Far Eastern Curlew at these 11 other internationally important wetlands sites would represent approximately only one-third of the 1,754 Far Eastern Curlew lost from the SSMP Study Region between 2006 and 2008 (Chapter 4, Table 4.8). The reduced number of Great Knot recorded provides strong evidence that this species was unable to relocate from the SES following sea-wall close in 2006. Based 164

on peak counts, >92,000 Great Knot were ―lost‖ from the SSMP Study Region between 2006 and 2008 (Chapter 4) In 1998 (as in 2008) the Great Knot was concentrated at only a few sites (most especially the adjacent Namyang and Asan Bays, and the adjacent SES and Geum Estuary). Most of Namyang and Asan Bays have been reclaimed since 1998, and rather than increasing there due to displacement from the SES, the number of Great Knot at Namyang and Asan also fell almost 60% from 30,500 on May 8th and 9th 1998 to 12,405 on May 5th 2008. There was a substantial decline in Black-tailed Godwit outside of the SSMP Study Region which exceeded the rate of decline within it. Numbers at the 11 sites declined by >20,000 (91%) compared to a fall in peak count within the SSMP Study Region of 1,543 in 2006 to 376 in 2008 (a decline of 76%). This was despite greater survey effort in 2008 focused in rice-fields where the species was numerous in 1998. In 1998, the highest count was made in Asan Bay (with a peak count of 18,282 on May 8th). There were also 1,701 counted near-by in rice-fields at Honwon Ri and 1,635 in Namyang Bay (Moores 1999a). In 2008, the number counted in rice-fields at Honwon Ri remained similar (1,799), but numbers at Asan Bay (43) and at Namyang Bay (38) were both massively reduced in 2008 compared with 1998. The counts therefore do not provide evidence of substantial numbers of birds relocating from the SES to other internationally important sites following seawall close in 2006. Rather the data suggest a decrease in the number of some species supported by sites that are also undergoing or are affected by reclamation.

5.3.3 Counts in 2008 and Estimates by Yi (2004) Further suggestion of declines in some shorebird species during the past decade is provided by a comparison of counts within the SES, the Geum Estuary and the same 11 most important shorebird sites in May 2008 with estimates for many of the same sites between 1997 and 2001 (in Yi 2004). Yi‘s estimates were based on counts made by teams of experienced counters during northward migration over several years. The estimates were therefore likely to be higher than the number of birds recorded by a single observer in 1998 (Moores 1999a). Dunlin and Great Knot were the two most abundant shorebird species, together representing 73% of the estimated total number of shorebirds during northward migration (Yi 2004). Both species peak in number in early-mid May. Largely as a result, 92% of the sum of maxima of all 45 shorebird species recorded during three years of the SSMP was recorded during one count cycle 165

in mid-May (Chapter 4, Section 4.3.1). It can be assumed therefore that (1) the counts in early-mid May 2008 recorded the vast majority of shorebirds earlier estimated by Yi (2004) to be present during northward migration at the same sites; and (2) if there had been a large displacement of shorebirds from the SES to these other sites, then numbers would have increased there between years. This is because the SES supported more shorebirds than all of the other most important shorebird sites combined. Yi (2004) provided estimates of shorebird numbers between 1997 and 2003 at eight of the wetlands we surveyed in 2008. Only one of these wetlands supported more shorebirds in 2008 than Yi‘s estimate. This higher count (at the Geum Estuary) is perhaps due in part to undercounting during the earlier NIER survey because of their smaller team size, time-constraints and the omission of some roost sites which were reached by boat during the SSMP. It is also because the Geum Estuary temporarily supported large numbers of some shorebird species displaced by the Saemangeum reclamation (Chapter 4, Section 4.4.4). Numbers at the seven other wetlands were lower (Table 5.4).

Table 5.4 Fourteen most important shorebird sites in May 2008, their reclamation status and estimates of shorebirds at the same sites during northward migration from1997-2001(Yi 2004). Shorebird Site 2008 Estimate 1997-2001 Geum Estuary 97,670 66,700 Saemangeum Estuarine System 39,557 316,000 Namyang Bay 33,389 74,000 Song Do 28,028 N/A Yeongjong Is. 24,169 46,000 Ganghwa Is. 11,894 29,700 Asan Bay 9,570 45,000 Aphae Island 8,835 N/A Hampyeong & Muan 7,279 N/A Suncheon Bay 6,201 9,300 Cheonsu Bay 5,089 N/A Teibu 2,798 7,000 Nakdong Estuary 2,525 N/A Baeksu 2,249 N/A Note: N/A denotes that estimates are not available for these sites. Sites in bold have been directly affected by large-scale reclamation between 1998 and 2008.

The difference between numbers recorded in 2008 and the numbers estimated by Yi (2004) were greatest at sites that have been largely-reclaimed during the past decade (the SES, Asan Bay and Namyang Bay); substantial at sites close to reclamation areas (Ganghwa, Yeongjong and Teibu); and smallest at the only site to have been only weakly influenced by reclamation activities in the past decade (Suncheon Bay). Yi (2004) also provided national estimates of several of the most numerous shorebird 166

species during the period 1997-2001. Notably, our study nationwide in 2008 found 90% fewer Black-tailed Godwit and 80% fewer Great Knot than estimated to be present in the ROK during northward migration by Yi (2004).

5.3.4 Four North-western Sites (1988-2008) The survey by Long et al. (1988) identified the four north-western sites of Ganghwa and Yeongjong Islands, and Namyang and Asan Bays as internationally important for shorebirds. Subsequent surveys by the NIER identified the same four sites as the most important shorebird sites nationwide after the Mangyeung and Dongjin Estuaries (i.e. the SES). Between 1988 and 1996, an estimated 181,000 shorebirds were supported by these four sites during northward migration, with 27,100 at Ganghwa Island, 30,000 at Yeongjong Island, 58,000 at Namyang Bay and 65,900 at Asan Bay (Yi 2004). Table 5.5 contains a comparison of counts of the 21 internationally important shorebird species at these four sites between 1988 and 2008.

Table 5.5 Comparison of numbers of internationally important shorebird counts at four north-western sites, in May between 1988 and 2008 Species 1988 1998 2008 Far Eastern Oystercatcher 3 0 14 Grey Plover 2,751 1,786 2,880 Kentish Plover 146 1 13 Mongolian Plover 3,749 389 1,408 Black-tailed Godwit 15,170 19,922 1,880 Bar-tailed Godwit 10,240 3,442 6,722 Whimbrel 1,033 583 1,489 Eurasian Curlew 67 3 119 Far Eastern Curlew 965 1,405 1,965 Common Greenshank 900 131 487 Nordmann‘s Greenshank 108 6 37 Terek Sandpiper 937 1,804 1,545 Grey-tailed Tattler 265 2 27 Ruddy Turnstone 174 52 114 Great Knot 18,846 34,846 16,777 Sanderling 0 0 20 Red-necked Stint 2,931 15 301 Sharp-tailed Sandpiper 75 502 452 Dunlin 55,344 25,179 42,127 Spoon-billed Sandpiper 5 0 0 Broad-billed Sandpiper 32 0 0 Total 113,741 90,068 78,377 Numbers in Table 5.5 are from Long et al. (1988) in 1988 at Ganghwa (May 1st-6th), at Yeongjong north and south (May 11th-12th), at Namyang Bay (minimum estimate from several main roosts between May 2nd and 7th) and Asan Bay (minimum estimate from six visits between April 12th and May 29th); between May 8th and 11th 1998 (in Moores 1999a); and between May 2nd and 5th 2008 (this survey). 167

The differences in site accessibility and count-capacity between decades probably increased the proportion of birds that could be found in 2008. Nonetheless, the present research found 100,000 shorebirds fewer in 2008 than were estimated at these four sites between 1988 and 1996 by Yi (2004); >35,000 (31%) fewer shorebirds than the minimum estimate recorded by the survey of Long et al. (1988); and c. 12,000 fewer (13%) shorebirds than recorded by Moores (1999a). Knowledge of the sites and experience of several of the species was much higher in 2008 than in 1998 (and presumably than in 1988) and most of the shorebirds were concentrated into rather fewer roosts (due to loss of alternative roosts sites through reclamation and infrastructure development). The declines are therefore likely to be genuine. One of the most striking of these declines at the species-level is again that of Black-tailed Godwit. The number of Great Knot in 2008 was also substantially lower than in 1998, but only slightly lower than the minimum number recorded by Long et al. (1988) that is listed in Table 5.5. Long et al. (1988), however, also provided a maximum estimate of 32,050 Great Knot at these four sites. Count data from the Nakdong Estuary suggest that the species has likely been in a protracted decline in the ROK (see Chapter 2, Section 2.5.7.5). It therefore seems probable that the higher numbers recorded in 1998 than in 1988 were either of birds displaced from elsewhere (perhaps due to other reclamation projects in the Incheon area), or that birds were overlooked in 1988 – as much of the area was then incompletely surveyed and difficult to access. The decline in the number of the globally Endangered Nordmann‘s Greenshank between 1998 and 2008 is also of great concern. The concentrations of this poorly-known species (and of Great Knot) were the highest known in Asia when recorded by Long et al. (1988). The low number found in 1998 was due to limited experience with the species, as Nordmann‘s Greenshank is surprisingly difficult to detect at long-range, apparently mimicking the postures of the species it flocks with when roosting (especially Grey Plover). The teams of observers in 2008 were familiar with the species; and the species was also likely concentrated into easily-viewable areas due to reclamation and loss of roost-sites in formerly extensive habitat (including salt-pans and salt-marsh edge). In combination, this suggests that there has been a major decline of Nordmann‘s Greenshank at these four sites between decades, as earlier cautioned by Long et al. (1988).

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5.4 DISCUSSION The study aimed to identify whether shorebirds were able to relocate to other wetlands following the closure of the Saemangeum seawall in 2006, and whether there were changes in the number of shorebirds supported by other internationally important shorebird sites in the ROK between decades. Our count data indicate that there has been no large-scale relocation of most of the shorebirds from the SES to other internationally important shorebird sites in the ROK following closure of the Saemangeum seawall. On the contrary, they indicate that there have been substantial declines in some species, in some cases exceeding declines estimated in other parts of the EAAF. Species of global conservation concern recorded in decreased numbers include the Endangered Nordmann‘s Greenshank, the Vulnerable Great Knot and the Near Threatened Black-tailed Godwit. Although there are inadequate data to determine the rate of global decline in Nordmann‘s Greenshank (BirdLife International 2011), both Great Knot and Black-tailed Godwit have also shown marked declines in well- surveyed areas in Australia in recent decades, estimated respectively at 30-49% over 22 years and 20-29% over 26 years (Garnett el al. 2011). We therefore recorded rates of decline in these two species in the ROK that are substantially more rapid than so far detected in their boreal winter range in Australia. Moreover, despite the high capacity of the counters in 2008 and the good knowledge of sites, no Critically Endangered Spoon-billed Sandpiper were recorded. This species has in previous years been recorded in small numbers at Ganghwa, Asan Bay, Namyang Bay (see: distribution map in Zöckler & Bunting 2010), and five were recorded at Namyang Bay by Long et al. (1988). Although the survey in 2008 was conducted earlier than the peak numbers recorded of this species in the SSMP Study Region in 2006 and 2007, we found no evidence that Spoon-billed Sandpiper have been able to relocate to other ROK wetlands following the loss of the SES, their former optimal staging site. As observed in the SES, it appears likely that declines in some species will have occurred more rapidly than in others. In consideration of the further conversion into land of areas within Namyang Bay and Asan Bay, it appears likely that a large proportion of shorebirds presently using these sites will also be lost in the near future. It seems likely therefore that the rapid decline of the Great Knot, caused primarily by the Saemangeum reclamation, will continue. The Great Knot was concentrated at only a few sites in the 1990s and early 2000s (Moores 1999a, Yi 2003, Moores 2006). In 2008, our survey covered all of these sites. Only 26,000 Great Knot were recorded 169

outside of the SSMP Study Region, with >8,000 of these at Song Do. Song Do is another internationally important wetland presently undergoing large-scale reclamation. Our study did not attempt to plot changes in shorebird numbers against habitat change between decades. Such research (in part, presently being undertaken by the University of Queensland: R. Clemens, University of Queensland e-newsletter, in lit. 2012) will be useful in strengthening confidence in the detection of declines and especially in the identification of their causes. This major undertaking is beyond the scope of the present study. Our study was constrained by the paucity of shorebird data and, as noted in previous chapters, by a lack of access to high-quality information on the rate of habitat change in intertidal and agricultural areas used by migratory shorebirds. As outlined in Chapter 3, there are substantial inconsistencies in government estimates of remaining intertidal area. Moreover, some reclamation projects take >10 years to complete, and include periods of gradually declining tidal range, followed by greatly restricted tidal exchange and eventual conversion of affected impounded wetland into land and freshwater reservoirs (Chapters 3 & 4). This series of physical changes in affected areas probably contributes substantially to differences in the rate of decline shown by shorebird species in response to reclamation. Moreover, large-scale reclamation also causes physical changes to adjacent sites (Kim & Choi 2006, Choi et al. 2010b, Lee 2010b). In addition to potentially exacerbating problems for feeding shorebirds, this further complicates efforts to determine the mechanisms of shorebird decline, as some species might benefit from changes in substrates and tidal patterns, while others might decline. In addition, there has also been no detailed study in the ROK investigating use by shorebirds of rice-fields and small rivers in the hinterland of major shorebird staging sites, or research on the impacts of agricultural intensification on shorebirds (at either the individual or the population level). Such research is required to enable the better interpretation of changes in the numbers we recorded of some species, such as Black-tailed Godwit. In combination, however, the SSMP and the national shorebird survey, successfully refute for the first time the claims of reclamation proponents that shorebirds can relocate to other areas in the ROK without a loss of population. Surveys or demography studies on the non-breeding grounds remain necessary to determine whether the Saemangeum reclamation has caused declines in some shorebird species at the population-level as our data suggest. And already, research in Australia has indeed detected declines in many shorebird species that stage in intertidal wetlands of the 170

ROK (Rogers et al. 2009, Wilson et al. 2011, Garnett el al. 2011, BirdLife International 2011). We estimate that two-thirds of remaining intertidal wetland in the ROK has been reclaimed in less than 25 years (Chapter 3); all major rivers have dams (KWRC. 2004); and the Han-Imjin remains the only major estuary in the ROK without an estuarine barrage (Moores et al. 2001). Even in the outer part of this estuary, at Ganghwa, there have been substantial declines – both in the diversity of benthos (Choi et al. 2010b) and in the numbers of shorebirds supported by the wetland. We therefore consider that loss and degradation of habitat in the SES and at several other internationally important wetlands has already resulted in substantial and measurable declines in some shorebird species within the ROK and at the population level. The extent and rate of decline in several species, including Great Knot and Black-tailed Godwit, exceed those so far detected by research outside of the ROK. The loss of the nation‘s optimal shorebird sites is therefore implicated in the declines of several shorebird species of the EAAF.

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CHAPTER 6

SURVEY OF SEABIRDS AT SEA IN THE YSBR FROM HIGH-SPEED FERRIES AND LAND-BASED COUNTS

ABSTRACT There are no published surveys of seabirds at sea in the YSBR or in the Yellow Sea. Opportunistic counts during 103 journeys on ferries along three routes within the YSBR between 2000 and 2008 improved baseline understanding of the seasonal distribution and abundance of some species. In the present surveys, a further 47 journeys on 45 dates were made along two transects between March 2009 and May 2010. Count methods had to be substantially modified from those recommended by specialist literature due to the high speed of the vessels used in surveys. Monthly counts were also made from an offshore island. Counts were subdivided into inshore waters (<2km from shore) and open sea (>2km from shore). In total, 91,646 seabirds of 34 species (29 regularly occurring species and five of less regular occurrence in the ROK) were recorded. Of these, approximately one-third were counted in open sea and two-thirds in inshore waters. Only six species were seen on both transects in open sea but not in inshore waters, and there were total counts in open sea of >1000 in only four species. Black-tailed Gull was the most numerous species along both transects through open sea, representing 62.5% of all seabirds recorded. Only three species (including Black-tailed Gull) were recorded in all months in either open sea or inshore waters, and all other species are therefore considered to be complete migrants. The survey methods used have limitations. Nonetheless, for the first time the research provides insights into seasonal distribution and possible migration strategies of several species in the YSBR. They therefore can be used as a first-step towards improving the knowledge base on seabirds at sea in the Yellow Sea and for identifying further conservation-driven research priorities.

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6.1 BACKGROUND AND AIMS The ROK has a long coastline adjacent to three different seas: the Yellow Sea, the Korean Strait, and the East Sea (or Sea of Japan). Although there has been some research on seabird colonies (Lee 1989, Park & Won 1993, Lee et al. 2009) and the annual Ministry of Environment winter bird census includes some inshore waters (here defined as marine waters within 2km of shore), there has been almost no research on birds at sea (Birds Korea 2010a). The national Marine Ecosystem Management Strategy Study Final Report (MOMAF 2006) does not refer to birds, and we know of no published surveys of seabird at sea distribution in the Yellow Sea. We consider that the paucity of research and of formal structures to share information (Chapter 1, Section 1.3.1) contribute to the exclusion of all 33 regularly occurring species of seabird in the ROK from recent assessments of Yellow Sea biodiversity, including UNDP-GEF (2007) and Kim & Pae (2008). At the same time, the Yellow Sea is undergoing an ecological regime shift (Sun 2010), attributed largely to unsustainable use and pollution (UNDP-GEF 2007). Within the Yellow Sea, there are likely to be numerous direct and indirect threats to seabirds at the population level. Many nesting islands have invasive alien species (Lee 2010a) and seabirds at sea are wholly dependent upon marine systems for food (Balance 2007). Evidence from breeding colonies suggests declines in some species (Chapter 2, Section 2.5.7.8) and Alaskan- breeding Red-throated Loon that winter in seas around the ROK declined 53% in breeding areas between 1997 and 2003, perhaps due to pollution in wintering areas (Schmutz et al. 2009; Chapter 1, Section 1.5.3). In other regions, seabirds at sea have been researched from ships (Tasker et al. 1984, Woehler et al 1996, Camphuysen et al. 2004). Conducting such research is generally expensive and these resources have been largely unavailable to ornithologists in the ROK. Almost all research on seabirds at sea in the YSBR has therefore been undertaken by necessity from ―vessels of opportunity‖ (cf. Hyrenbach et al. 2007). The only such vessels to cross large areas of open sea (defined as >2km from land) in the YSBR regularly during daylight hours are high-speed commercial passenger ferries. Between 2000 and 2008, the present author (sometimes with other observers) counted seabirds at sea during 103 high-speed ferry journeys in the YSBR. Most journeys were in March-May and again in September-November, with only two in December and none in January or February. These comprised 46 journeys, each of c. 150km, from between the west of Incheon Port (37°20' N, 126°19' E) and Socheong Island (37°45' N, 173

124°44' E) (―The Northern Transect‖); 15 journeys, each of between 93km and c. 160km in length, between Bigeum Island (34°42' N, 125°54' E) and Heuksan (34°41' N, 125°28' E) and Gageo Islands (34°03' N, 125°09' E) (combined, ―The Southern Transect‖); and 42 journeys, each of c. 40km, between Yeon Island (36°04' N, 126°27' E) and Eocheong Island (36°07' N, 126°00' E) (―The Central Transect‖). All three transects are shown in Chapter 1, Figure 1.2. Each journey, all birds were counted irrespective of range and where possible on both sides of the vessel. The counts confirmed the presence of several species in the YSBR which were omitted from or under-represented in the ROK ornithological literature. However, mid-summer and winter months were poorly covered by these counts. It was also difficult to interpret the data for some species because of the high speed of the vessels (29-33km/hr on the Central Transect and 45-55km/hr in calm conditions on the Northern and Southern Transects). These speeds are two to five times faster than recommended for boat-based seabird at sea research in Camphuysen et al. (2004), and up to twice that of the high- speed survey platform described by Hyrenbach et al. (2007). The present research therefore had two aims. The first was to refine understanding of seabird seasonal presence and abundance within the YSBR, and the potential influence of large-scale effects including geography and human use (including fishing activities and mariculture). We predicted that by comparing counts along two transects and from one island each month it would be possible to identify seabird species more typical of open sea than of inshore waters. Differences in numbers of seabird species seasonally and between transects might also be used to support our hypothesis that several species migrate overland to reach the YSBR from the north or east including Yellow-billed Loon and Black-legged Kittiwake (Schmutz 2004, 2010; Moores 2007), rather than arriving by sea from the south through the Korean Strait or South China Sea as proven in satellite-tracked Streaked Shearwater Calonectris leucomelas (Choi 2008). The second aim was to identify challenges and biases in different survey approaches in order to inform future research initiatives. Based on previous survey, in addition to differences in distance-from-land distribution, we predicted that: 1. Most species would avoid oncoming fast-moving ferries and would be detected in flight, while a larger proportion of birds detected from land would be sitting on water or feeding by swimming; 2. Identification of some species (including all Gaviidae loons) would be more difficult from a fast-moving vessel than from a stationary count point on land; 174

3. Smaller species (including Alcidae, Red-necked Phalarope Phalaropus lobatus, Red Phalarope and Swinhoe‘s Storm Petrel) would be easiest to detect in flight and difficult to detect at ranges >1km from vessels. Biases caused by differences in survey approaches need to be understood if data are to be used in the detection of population trends and to develop appropriate conservation strategies. For the present research, counts were therefore conducted on a total of 47 journeys on 45 dates in 2009 and 2010 along the Northern and Southern Transects (including along sections in inshore areas), and once a month from Socheong Island.

6.2 METHODS 6.2.1 Counts from Ferries Counts of seabirds at sea were conducted in all months between March 2009 and February 2010 with the exception of December. Additional counts were made along the Northern Transect in March, April and May 2010. In total, there were 26 counts along the Northern Transect and 21 counts along the Southern Transect (Table 6.1).

Table 6.1 Number of counts of seabirds at sea by month along the Northern and Southern Transects in 2009 and 2010. Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Northern Transect 2 2 3 3 2 2 2 4 4 1 1 Southern Transect 4 2 1 2 2 1 3 2 1 1 2 Note: Northern Transect counts were conducted in 2009 on: March 17th & 20th; April 11th; May 9th; June 23rd & 24th; July 22nd & 23rd; August 19th, 22nd & 31st (outward and return legs); September 13th, 18th, 21st & 22nd; October 16th; and November 9th. In 2010 on: January 2nd & 19th; February 17th & 19th; March 30th; April 8th & 12th; and May 16th. Southern Transect counts were conducted in 2009 on: March 24th; April 4th & 17th; May 20th & 28th; June 25th; July 5th/6th, July 24th & 31st; August 13th & 18th; September 24th; October 12th; and November 16th & 19th. In 2010 on: January 3rd (outward and return legs), January 9th & 15th; and February 20th (outward and return legs).

On the Northern Transect, counts were started close to an offshore buoy in Gyeonggi Bay, and continued until the boat reached two small islets of the southwest of Socheong Island (a total length of 150km in a straight line, and a total of 161-167km as travelled). On the Southern Transect, main counts started 500m from each of several islands (Bigeum, Heuksan, Hatei, Manjay, Hong and Gageo). On the outward leg, the total length through open sea was c. 93km (37.8km between Bigeum and Heuksan; 17.4.km between Heuksan and Hatei; and 37.7km from Hatei to Gageo). The return leg included an additional two sections totalling 65km, from Gageo to Manjay, and 175

from Manjay to Hatei. On a few journeys, the ferry also visited Hong. The total return journey was therefore c. 158-180km dependent on the route taken. Counts in open sea were changed to counts of ―Southern Inshore Waters‖ when the boat was within 500m- 1km of land. This included two extensive areas of mariculture platform and several harbours. All birds within view of the vessel (up to 2km range) were counted. It was essential to modify methods recommended by Tasker et al. (1984) and Camphuysen et al. (2004) for a lone counter on a very high-speed vessel. Based on previous experience and on preliminary work (counting from inside and towards the front of high-speed ferries, and using a range-finder), it was not possible to count well the 300m-forward quadrant. Instead, all counts were conducted from outside and towards the rear third of the vessel, at c. 6-7m above sea-level (Figure 6.1). All birds were recorded through constant scanning with 10x42 binoculars of one rear quadrant for the whole journey (approximately 3-4 hours), divided into ten-minute sections.

Figure 6.1 One of the high-speed vessels used in the surveys. Counting was conducted from the second floor, from the rear third of the vessel (often while holding onto a safety rail descending from the bridge).

In order to assess detectability and response (if any) of seabirds to the vessel, estimated distance for each bird or flock was recorded. Distances were difficult to estimate accurately from such large and fast-moving vessels. Moreover, rather few birds in open sea areas were recorded within 300m of the vessels. Instead birds appeared to avoid the vessels on approach. Therefore, all records were instead divided into five coarsely estimated bands of 1-150m, 150-300m, 300m-1km, 1-2km and >2km. Where possible, for each 10-minute section notes were also taken on sea state, cloud cover and visibility, in addition to GPS coordinates. All birds were identified to species or family and categorised as flying, sitting on water or perched. Association with mariculture, 176

active fishing boats, and other physical features were also recorded including suspected upwellings and tidal-fronts, indicated by a rapid transition between clear and turbid sea.

6.2.2 Counts from Land Counts were made once a month from fixed points on Socheong Island (Figure 6.2), and were conducted close in time to Northern Transect counts, either over one or two days (on March 19th & 20th; April 12th; May 13th & 14th; June 23rd & 24th; July 22nd & 23rd; August 19th & 20th; September 13th & 14th; October 22nd & 23rd; and November 8th 2009; and on January 29th & 30th and February 18th 2010). Count points were all >55m above sea level and selected so that all sea areas could be surveyed.

Figure 6.2 Land-based points (in red) on Socheong Island used for seabird counts (also see Figure 6.4 and Chapter 7, Figure 7.3).

All land-based counts were made on days with good visibility, and timed to avoid glare from the sun, so that counts from near the lighthouse looking west were made in the morning and counts looking east from Northeast Point were made in the late afternoon. Efforts were made to avoid double-counting and to record only once similar-sized flocks seen from different points. The extent of double-counting (or undercounting) is unknown. As with boat-based counts land-based counts recorded all seabirds identified to species or family; divided each record into the same five distance bands and three types of behaviour; and noted weather conditions, sea-state and GPS coordinates. Two main differences were use of a tripod-mounted telescope and restricting counting at each observation point to 20 minutes.

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Thus, most of both Northern and Southern Transect records were made in open sea, and most of Southern Inshore and Socheong counts were of birds in inshore areas. However, there was no method to measure distances precisely (apart from through use of a GPS when departing land) and as in previous survey many birds were concentrated at an estimated distance 1-5km from land.

6.2.3 Analysis In order to help test our hypothesis on different migration strategies, it was necessary to identify differences between seabird at sea communities recorded on the Northern and Southern Transects. To do this, we used a multi-response permutation procedure (MRPP). MRPP is a nonparametric procedure used to compare differences in two or more groups of entities, in this case avian communities (Mielke & Berry 2001, McCune & Grace 2002). Data from all months January-November (see Table 6.1 above) was used, as replication was insufficient to test seasonal differences between dates of journeys along Northern (n=25) and Southern (n =20) Transects. We justify inclusion of all seabird community data across seasons as surveys were balanced in replication across time. MRPP procedures used Euclidian distances in measuring seabird community assemblage differences. Next, we used Indicator Species Analysis (ISA) to determine which species were most indicative of Northern and of Southern Transect seabird communities. ISA generates indicator values for each species using presence/absence, abundance, and frequency with which each was species was recorded (Dufrêne & Legendre 1997) in each grouping (i.e. on Northern Transect versus Southern Transect). Indicator values range from 0-100, where a species with a 100 indicator value is perfectly faithful to that group (recorded exclusively in that group on every survey and not elsewhere) and an indicator of 0 is perfectly non- faithful (McCune & Grace 2002). Additionally, ISA uses a Monte Carlo randomization test (randomizations = 1000) to evaluate the indicator values for each species. We excluded seabird indicator values that did not pass the Monte Carlo randomization test. We then ranked seabirds by the indicator value by transect (Northern versus Southern) and selected the five species that contrasted most between the two transects. MRPP and ISA analysis were all completed using PC-ORD software (Gleneden Beach, OR, USA) and in all cases we set α = 0.05.

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6.3 RESULTS 6.3.1 Species‘ Richness During the present survey, in line with definitions in Chapter 2 (Section 2.1.3), 29 species of regularly occurring and five less regular seabird species were recorded out of a total of 33 regularly occurring and 19 less regular seabird species recorded in the ROK (Moores & Park 2009). In addition, single Little Auks Alle alle were also recorded on January 2nd and January 9th 2010 in open sea. These 35 species are from 11 families (Anatidae, Gaviidae, Procellariidae, Hydrobatidae, Podicipedidae, Sulidae, Phalacrocoracidae, Scolopacidae, Laridae, Stercorariidae and Alcidae) in six orders (Anseriformes Gaviiformes, Procellariiformes, Podicipediformes, Pelecaniformes and Charadriiformes). In total, 27 species were recorded in open sea along both the Northern and Southern Transects (with 19 shared between transects). Twenty-one species were recorded in inshore waters from Socheong Island and 14 during counts in Southern Inshore Waters (13 shared). Seasonally, species richness was highest in the winter months and lowest in mid-summer (Figure 6.3).

15

10

Transect 5 No. species of Northern Socheong Southern 0 S Inshore Waters 0 2 4 6 8 10 12 Month

Figure 6.3 Number of species recorded by month (when single count) or as the mean that month of counts along the Northern Transect, from Socheong, along the Southern Transect and in Southern Inshore Waters. In all count areas, species‘ richness was lowest in June-July.

6.3.2 Differences between Transects There was a significant difference in the community composition of seabird at sea communities along the Northern and Southern Transects (A = 0.04, P = 0.007). The mean indicator value for Northern Transect seabirds using ISA was 9.1 ± 2.3 (SE) and for Southern Transect seabirds was 13.8 ± 2.7. The top five indicator species for the Northern Transect ranked from greatest to least were: Streaked Shearwater, Common 179

Tern Sterna hirundo, Taimyr Gull, Pomarine Skua Stercorarius pomarinus, Skua/Jaeger spp. The top five indicator species for the Southern Transect ranked from greatest to least were: Loon spp., large white-headed gulls (including Mongolian, Vega and Taimyr gull, unidentified to taxon), Red-throated Loon, Ancient Murrelet, and Vega Gull (Table 6.2).

Table 6.2. Indicator values for the top five indicator species of seabird communities in open sea areas in the Northern versus the Southern Transects. Northern Southern Species Transect Transect Loon spp. - 38 Large white-headed gull - 35 Red-throated Loon - 32 Ancient Murrelet - 29 Vega Gull - 27 Streaked Shearwater 37 - Common Tern 32 - Taimyr Gull 25 - Pomarine Skua 17 - Skua/Jaeger spp. 13 -

During monthly land-based survey on Socheong Island, four species of seabird were found breeding (Pelagic Cormorant Phalacrocorax pelagicus, Temmick‘s Cormorant, Streaked Shearwater and Black-tailed Gull), and all were seen both along the Northern Transect and from the island itself in all months between April and October. No seabirds were found breeding on Gageo Island. However, Streaked Shearwater is known to breed on the nearby Gugeul Islets, and small numbers of immature Temminck‘s Cormorant remained on Gageo through the year and several adults and immatures were also recorded near Hatei Island. Although the Southern Transect passed within 10km of islands supporting most of the world‘s breeding Swinhoe‘s Storm Petrel none were seen from Gageo Island or in Southern Inshore Waters; records on the Southern Transect were confined to June-August; and only small numbers of Swinhoe‘s Storm Petrel were observed on four out of six Southern Transect ferry journeys in those months.

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6.3.3 Number of Individuals In total 91,646 individuals seabirds were counted during the surveys. Of these, approximately one-third were counted in open sea areas (with 22,239 seabirds along the Northern Transect and 7,983 along the Southern Transect) and two-thirds in inshore waters (with 19,757 recorded from Socheong and 41,667 recorded within Southern Inshore Waters). Daily counts in open sea areas are likely to be underestimates. Detection rates were probably low for some species (see Section 6.3.5), and there was likely little double-counting as the high speed of the vessels meant that while ship-following was actively searched for, it seldom occurred until the vessels slowed down to <30km/hr. However, many of the same individuals in inshore waters were likely recorded in more than one month. The actual number (if only one count made that month) and the mean number of individuals recorded per month for each of the four count areas is given in Table 6.3.

Table 6.3 Number of individual seabirds recorded by month (when single count) or as monthly mean in the four count areas (2009-2010). Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Northern YSBR Northern 295 247 491 292 3,630 402 200 913 973 2,033 970 Transect Socheong 189 274 210 345 7,014 464 4,565 788 1,081 3,237 1,590 Island Southern YSBR Southern 754 134 36 248 63 32 146 373 28 1,684 557 Transect Southern 1,881 1,154 814 916 63 32 146 426 1,451 4,212 13,377 Inshore

6.3.4 Distribution in Open Sea and Inshore Areas Only six species were seen on both transects in open sea but not in inshore waters: Swinhoe‘s Storm Petrel, Red-necked Phalarope, Red Phalarope, Common Tern, South Polar Skua and Little Auk. Of species recorded in inshore waters, only Black-necked Grebe Podiceps nigricollis was recorded in both Southern Inshore counts and from Socheong (at the western end of the Northern Transect) but not in open sea. However, there were only three records of Pelagic Cormorant >4km from land (with the maximum recorded distance of 5.5km). Also, with the exception of one group in flight, no Temminck‘s Cormorant were recorded >4km from land. Several other species 181

(including all other Podicipedidae and both White-winged and American Scoter) were recorded almost only within 5km of land. Other species were recorded near to land and also in open sea areas, including Streaked Shearwater and all Gaviidae. Yellow- billed Loon showed a bimodal distribution (Figure 6.4), with several records within 1- 5km of shore (including one seen from Socheong, not in figure) and others in open sea areas. The mean distance from land was 12.5 km (n=19). All Yellow-billed Loons recorded along the Northern Transect were in waters c. 30m-55m deep, apart from one close to a subtidal ridge where the water was 10m-25m deep (based on NORI 2008a). Along the Southern Transect, birds were recorded in water between 34m and 104m deep at lowest low tide (based on NORI 2008b).

Figure 6.4 Distribution of Yellow-billed Loon recorded along the Northern and Southern Transects, with hatching indicating route of transect (based on GPS readings) and size of dot indicating number of individual Yellow-billed Loon that were recorded (smallest= 1, largest=4).

6.3.5 Most Numerous Species 6.3.5.1 Open sea In open sea areas, only four species had total counts of >1000, with Black-tailed Gull the most numerous species along both transects, representing 62.5% of all 182

seabirds recorded. On the Northern Transect, the largest counts of this species were made around fishing boats at the entrance to Gyeonggi Bay, c. 10-20km from land, in May and October. Common Tern and Black-legged Kittiwake were much more numerous along the Northern Transect and Pacific Loon Gavia pacifica along the Southern Transect (Table 6.4). The records of all three species were concentrated in time and space. On the Northern Transect all Common Tern were recorded on journeys between August 19th and September 21st with the exception of one outlier on October 16th. A count of 1,644 on August 31st represented 74% of all records. Almost half of these were recorded in one ten-minute section along a suspected tidal-front or tidal upwelling, perhaps marking the edge of a Surface Cold Water Mass (Lu et al. 2009). None were recorded during survey on any date within 15km of land. Similar concentrations were recorded on similar dates in previous survey. Counts of Black-legged Kittiwake were all on either October 16th or November 9th, a period during which large movements of the species were noted on Socheong in 2009.

Table 6.4 Numbers of the 16 most numerous seabird species recorded along the Northern and Southern Transects. Results are presented as the largest concentrations of each species within ten minute count sections, and the total expressed as a percentage of all seabirds recorded. Northern Transect Southern Transect Combined Total Species Total Largest Total Largest Number % number number number number of All 10 min. 10 min. Seabirds

Black-tailed Gull 15,627 1,205 3,323 294 18,950 62.5 Streaked Shearwater 3,136 800 1,858 492 4,994 16.5 Common Tern 2,211 697 20 7 2,231 7.4 Pacific Loon 3 3 1,077 970 1080 2.8 Ancient Murrelet 220 109 331 32 551 1.8 Black-legged Kittiwake 380 132 23 8 403 1.3 Swinhoe‘s Storm Petrel 96 10 85 35 181 0.6 Arctic Loon 13 3 160 120 173 0.6 Vega Gull 13 3 108 42 121 0.4 Red-necked Phalarope 13 9 50 35 63 0.2 Pomarine Skua 56 11 7 2 63 0.2 Taimyr Gull 29 3 17 6 46 0.1 Red-throated Loon 4 1 36 9 40 0.1 Common Gull 11 5 21 14 32 0.1 Great Crested Grebe 0 0 23 9 23 <0.1 Yellow-billed Loon 7 2 12 3 19 <0.1

A comparison of peak counts in open sea of the 26 most numerous species along the Northern, Central and Southern Transects shows that Black-tailed Gull was either the most or the second most numerous seabird recorded along all three transects (Table 6.5). Black-legged Kittiwake, Common Tern and Pomarine Skua have all been 183

recorded in substantially higher numbers along the Northern Transect. The highest number of Red-necked Phalarope was recorded along the Central Transect (perhaps due to higher rates of detection as the boat is slower than along the other two transects). On the Southern Transect during the present research, most Pacific Loon (>1000) were concentrated in one area 2-8km from Heuksan Island on January 9th 2010. There was only one Pacific Loon in the same area on January 3rd and none on January 15th. There are too few data from other winters to assess whether large numbers of this species are regular or not in the southern YSBR. Large flocks were regular in mid-winter in southern Japan in the 1990s and are regular along the east coast of the ROK (unpublished data), but the highest peak count along the Southern Transect during previous research was only four.

Table 6.5 Peak counts in open sea of the 26 most numerous seabird species along the Northern, Central and Southern Transects during previous (2000-2008) and present research (2009-2010). Species are ranked in order of highest to lowest peak count. Previous Research (2000-2008) Present Research (2009-2010) Species Northern Central Southern Northern Southern Transect Transect Transect Transect Transect

Black-legged Kittiwake 5,900 5 25 242 13 Black-tailed Gull 5,500 620 1,000 5,236 664 Common Tern 921 62 79 1,644 17 Streaked Shearwater 1,177 625 879 1,036 995 Pacific Loon 110 0 4 3 1,039 Ancient Murrelet 292 21 126 114 58 Swinhoe‘s Storm Petrel 178 30 11 54 46 Arctic Loon 4 2 4 8 124 Red-necked Phalarope 0 92 25 9 49 Pomarine Skua 82 1 4 34 3 Taimyr Gull 75 40 1 6 6 Vega Gull 10 10 5 8 68 Common Gull 50 8 0 5 15 White-winged Scoter 20 0 0 1 0 American Scoter 16 0 0 0 12 Red-throated Loon 4 2 2 2 17 Slender-billed Shearwater 3 2 6 1 1 Yellow-billed Loon 1 0 0 3 6 Parasitic Jaeger 6 1 1 0 0 Flesh-footed Shearwater 4 3 0 3 2 Crested Murrelet 0 4 1 0 3 Red Phalarope 3 1 1 1 3 South Polar Skua 2 0 2 3 2 Slaty-backed Gull 1 3 1 1 0 Rhinoceros Auklet 3 0 0 0 1 Long-billed Murrelet 1 1 0 0 2

6.3.5.2 Inshore waters From Socheong Island, the most numerous species recorded was Streaked Shearwater, with the count of 6,400 1-2km offshore on May 14th 2009 higher than any count in the Korean ornithological literature before the present century (Park 2002). 184

Numbers of seabirds were highest in the summer months. In contrast, there were very few birds in the summer months within Southern Inshore Waters (Table 6.6). Instead, most seabirds were observed in winter when Laridae were most numerous, including Black-tailed Gull (32,386), Vega Gull (4,254) and Common Gull (1,165). All three species were most numerous between November and February, and were concentrated around extensive mariculture platforms near Heuksan Island, with the former two species also present in large concentrations on Hatei and attending active fishing vessels in Gageo harbour (for locations of these islands, see Figure 6.4 above).

Table 6.6 Monthly counts of selected seabird species in and close to inshore waters recorded by land-based counts from Socheong and by commercial ferry in Southern Inshore Waters.

JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV White-winged Scoter Socheong 53 22 32 34 0 0 0 0 0 0 1 Southern Inshore 0 0 0 0 0 0 0 0 0 0 0 Arctic Loon Socheong 4 5 1 31 0 0 0 0 0 0 0 Southern Inshore 3 3 0 0 0 0 0 0 0 0 0 Great Crested Grebe Socheong 12 4 17 8 0 0 0 0 0 8 37 Southern Inshore 10 32 12 4 0 0 0 0 0 0 1 Pelagic Cormorant Socheong 64 128 112 44 185 172 342 68 184 161 131 Southern Inshore 15 8 0 1 0 0 0 0 0 0 1 Temminck‘s Cormorant Socheong 19 1 24 41 28 16 36 36 25 172 125 Southern Inshore 149 206 4 8 5 8 7 12 13 37 52 Black-legged Kittiwake Socheong 0 0 0 0 0 0 0 0 0 2,439 849 Southern Inshore 4 0 1 1 0 0 0 0 0 0 1 Black-tailed Gull Socheong 19 5 4 183 367 262 879 374 189 206 443 Southern Inshore 1,085 749 610 288 7 0 3 491 1,438 4,121 11,640 Common Gull Socheong 0 0 0 0 0 0 0 0 0 0 0 Southern Inshore 520 284 0 0 0 0 0 0 0 0 1 Vega Gull Socheong 1 1 2 0 0 0 0 0 0 3 0 Southern Inshore 181 100 639 90 0 0 0 0 0 6 3,050 Ancient Murrelet Socheong 1 0 5 0 0 0 0 0 0 0 0 Southern Inshore 2 0 0 2 0 0 0 0 0 0 0 Note: For Southern Inshore Waters the highest day count was selected for months with more than one count.

6.3.6 Seasonal Distribution 6.3.6.1 Partial migrants Only three species (Pelagic Cormorant, Temminck‘s Cormorant and Black-tailed Gull) were recorded in the YSBR throughout the year by the present survey. All three species appear to be widespread breeders in the north of the YSBR (including on Socheong) and both Temminck‘s Cormorant and Black-tailed Gull also breed more 185

locally further south in the YSBR (unpublished data). Many individuals of both cormorant species apparently disperse southward in winter as the monthly pattern of count maxima on Socheong were inverse to those in Southern Inshore Waters. Similarly, Black-tailed Gull was most abundant April-October northward (with a peak count recorded on May 16th) and most abundant November-March southward in the YSBR. All three species are therefore best-considered as partial migrants, presumably migrating north-south in the YSBR seasonally.

6.3.6.2 Complete migrants The dates of presence and absence suggest that with the exception of the two cormorant species and Black-tailed Gull all seabird species are complete migrants to the YSBR (Table 6.7).

Table 6.7 Seasonal status of complete migrant seabirds in open sea in the YSBR identified from the date of the peak count in the present survey (2009-2010) and from first and last dates recorded during 150 ferry journeys along the Northern, Central and Southern Transects in these and previous surveys (2000-2010). Seasonal Status Species Date of Peak First and Last Dates 2009-2010 2000-2010 Winter Visitors White-winged Scoter Jan 2 Jan 2-Mar 26 American Scoter Nov 16 Nov 13-Mar 22 Red-throated Loon Jan 3 Nov 19-May 30 Arctic Loon Jan 9 Nov 13-May 30 Pacific Loon Jan 9 Nov 3-May 30 Yellow-billed Loon Jan 3 Dec 16-May 18 Common Gull Jan 9 Nov 9-Apr 27 Vega Gull Nov 19 Oct 1-Apr 27 Taimyr Gull Mid-Apr Sep 9-May 9 Slaty-backed Gull Mar 30 Oct 24-May 2

Summer Visitors Streaked Shearwater Sep 21 Mar 14-Nov 10 Swinhoe‘s Storm Petrel Aug 19 May 30-Oct 19

Regular Transitory Slender-billed Shearwater Multiple Dates May 16-Nov 2 Migrants Flesh-footed Shearwater Aug 31 Jul 23-Oct 31 Red-necked Phalarope Jul 31 May 2-Sep 15 Black-legged Kittiwake Oct 16 Oct 1-Apr 21 Common Tern Aug 31 Apr 9-Oct 4 Pomarine Skua Oct 16 Mar 14-Nov 16 Parasitic Jaeger No record Apr 12-Oct 31

Less Regular Transitory Red-footed Booby Jul 24 Jul 24 Migrants Brown Booby No record Oct 20 Red Phalarope Nov 19 Sep 22-Mar 14 Aleutian Tern Aug 31 Aug 23-Sep 4 Sooty Tern Sep 18 Sep 18 South Polar Skua Oct 16 Jul 31-Nov 3 Long-tailed Jaeger No record May 14-May 19 Little Auk Jan 2 & Jan 9 Jan 2-Jan 9 Brunnich‘s Murre Sep 21 Sep 21

Poorly Known Long-billed Murrelet Feb 20 Aug 20-Apr 21 Crested Murrelet Apr 4 Apr 1-May 23 Ancient Murrelet Apr 11 Oct 1-Jun 13 Rhinoceros Auklet Jan 15 Jan 15 186

The seasonal status of several of these species, including of four species of Alcidae, remains poorly-known. Ancient Murrelet might be a complete or partial migrant within the YSBR. The species formerly bred on several islands close to the Southern Transect (see Chapter 2, Section 2.5.7.8). Two young were seen at sea with adults on the Southern Transect near to Chilbal Island on May 30th 2001; three were in inshore waters off Socheong on June 4th 2004 and 2005; and birds were seen on five out of six journeys in June on the Central Transect between 2002 and 2007. However, there were no records during any of 32 journeys (these and previous surveys) between June 13th and October 1st. This absence of late summer records is apparently paralleled in waters off North America (BC Ministry 2006). The globally Vulnerable Crested Murrelet Synthliboramphus wumizusume is either a less regular species or more likely a scarce local summer visitor to the south of the YSBR (breeding was first confirmed in the 1980s near Gageo and in 2011 on Jeju: Yeonhap 2011).

6.3.7 Detectability & Distance The distance from the counter and behaviour of all birds when first observed were recorded. If all species were distributed evenly at sea, and if all birds were detected, then numbers would be equal between the three closest bands (0-150m; 150-300m; 300m-1km) and the fourth band (1km-2km); and there would be 2-3 times as many birds in the third band (300m-1km) than in the first two bands (0-300m). Predictably, no species showed this exact pattern. Instead distance, size, detection and identification were related. The majority of observations of small species were made in the distance band of 150m-300m with few at >1km. Thus all 15 records of phalaropes were at ranges of <1km, and 11 were at ranges of <300m; 69 out of 71 records of Swinhoe‘s Storm Petrel were at ranges of <1km; and only three out of 105 records of Ancient Murrelet (total 551 individuals) were detected at a range of >1km, with 84 of these records at <300m (Table 6.8). Smaller species are thus likely under- counted from these vessels compared to larger species. As with smaller species the majority of larger species between 0-300m were also recorded in flight. In open sea, Streaked Shearwater were 2-3 times more numerous between 300m-1km than between 0-300m, suggesting limited avoidance behaviour. However, loons were seldom recorded within 300m of vessels. Between 1km and 2km, some larger distinctive species remained visible in flight and straightforward to identify (e.g. Streaked Shearwater), but were recorded in lower numbers than between 0m-1km, suggesting 187

reduced rates of detection. A much smaller proportion of loons were also found sitting on the sea at a range of>1km compared with <1km, but were not possible to identify to species from a moving vessel.

Table 6.8 Number of individuals of species and one selected family counted along the Northern and Southern Transects and from Socheong divided into distance bands and behaviours (Fly= Flying; Swim=Sitting on water). DISTANCE 0-150m 150-300m 300m-1km 1-2km >2km Fly Swim Fly Swim Fly Swim Fly Swim Fly Swim Ancient Murrelet Northern Transect 7 38 90 27 39 19 0 0 0 0 Southern Transect 16 12 60 79 104 43 17 0 0 0 Socheong 0 0 0 0 0 5 0 1 0 0 Streaked Shearwater Northern Transect 111 1 546 138 1,397 303 485 119 36 0 Southern Transect 38 1 177 71 549 323 202 467 30 0 Socheong 0 0 0 0 88 0 273 6,508 160 3,504 Loon sp. Northern Transect 0 0 4 0 18 0 10 1 3 0 Southern Transect 4 0 8 0 164 121 119 11 65 0 Socheong 0 0 0 0 0 0 2 0 0 99 Arctic Loon Northern Transect 0 0 4 1 7 0 1 0 0 0 Southern Transect 1 0 4 4 106 40 5 0 0 0 Socheong 1 0 0 0 1 0 1 34 0 4

From land, a higher proportion of birds could be identified with confidence at a greater range, and as predicted a larger number of most species were observed sitting on the sea. There were 20 records of loons involving four species and 148 individuals: these included only four records (five individuals) of birds in flight. It is likely that the larger proportion of birds seen in flight from ferries than from land was due to their active avoidance of such vessels. Several ferries travel the whole length (Northern Transect) or most of the length (Southern Transect) of these transects each day, and other vessels also travel along part of the same routes or cross the transects with an unknown frequency. It is therefore likely that numbers of several seabird species along these transects will be lower than in ecologically similar though less-disturbed sea areas, at >2km range from the main ferry and shipping routes. Such an assumption is supported by observations of seabirds from smaller fishing boats close to the Southern Transect (personal observations, Park Jong-Gil in lit. 2011).

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6.4 DISCUSSION In order to develop appropriate conservation strategies for seabird species within the time constraints imposed by the Aichi Biodiversity Targets (CBD 2010) it will be necessary to interpolate seasonal and geographical distribution across the YSBR and Yellow Sea from short-term data sets and incomplete survey effort. The present study for the first time confirms the importance of the YSBR for seabirds and seabird conservation away from breeding colonies. Three species of global conservation concern were recorded (Near Threatened Yellow-billed Loon, Vulnerable Crested Murrelet and Near Threatened Long-billed Murrelet Brachyramphus perdix), as were large concentrations of several other species (including an internationally important concentration of Black-tailed Gull). However, only small numbers of White-winged Scoter were found, contradicting the assessment of its wintering ―extremely commonly‖ along the west coast of Korea (Pihl & Fox 2005). The research confirmed that seabirds are not distributed evenly within the YSBR, and that all species are probably either partial or complete migrants to the subregion (at least along the three transects). We also recorded substantial differences between species composition and abundance in inshore and marine waters, which would likely become more apparent if the definitions used by this study were refined (e.g. by extending out inshore waters to include all marine waters <4km from land). Furthermore, we found significant differences between seabird communities of the Northern and Southern Transects, in addition to substantial differences in peak counts, mean counts and timing of peak between some species along all three transects. These data, however, are not yet adequate for larger-scale extrapolation of seabird density across the YSBR. We confirmed that many species avoided the vessels that were used for counting – presumably as such vessels are large, noisy and fast-moving. As the transects ran along or close to main commercial shipping lanes in some areas it was not possible to determine whether other vessels had already disturbed birds along or close to the transects which we surveyed. Therefore, although Distance Sampling was attempted, analysis suggested that our results would likely lead to biased conclusions. Although more research is required, the substantial differences in abundance of some species between Northern and Southern Transects which were suggested by our count data appear to be supported by literature review and to be consistent with our hypothesis on differences in migration strategies. Understanding such species-level differences in migration strategy is important for conservation. Such differences might, 189

for example, be responsible for higher levels of polychlorinated biphenyls detected in Alaskan breeding Red-throated than in Yellow-billed Loons. The Red-throated Loon was described by Gore & Won (1971) as fairly common along the south coast while Park (2002) listed only one specimen and two sight records from Gyeonggi Province (both from 1932). During the present research Red-throated Loon was uncommon along the Northern Transect but was identified as one of the five top indicator species of the Southern Transect. It appears therefore that most Red-throated Loon probably enter the Yellow Sea from the south, after migrating first along the east and south coasts of the ROK. Its migration therefore takes it through marine waters that are much affected by commercial shipping and coastal industries. By contrast, many Yellow-billed Loon migrate overland to the Yellow Sea from the East Sea, as proven by studies using satellite transmitters (Schmutz 2004). These Yellow-billed Loon thus avoid the most polluted areas. Based on the substantially higher counts of Pomarine Skua, Common Tern, Taimyr Gull and Black-legged Kittiwake on the Northern than the Southern Transect it appears likely that these species also migrate overland to reach the YSBR. Although the source population of these species has not yet been proven, Moores (2007) speculated that Black-legged Kittiwake probably reached the YSBR after a short overland crossing from the East Sea. However, it is notable that Taimyr Gull breed on the Taimyr Peninsula and winter in coastal East Asia (Djik et al. 2011); that they are one of the top five indicator species of the Northern Transect, and are more numerous northward in the YSBR earlier in autumn and later in spring; that two first-year Black-legged Kittiwake ringed on Novaya Zemlya (to the west of the Taimyr) were recovered on Kamchatka (in Malling Olsen 2003); and that >99% of all Black-legged Kittiwake recorded in the Northern Transect and off Socheong have been adults. If both Taimyr Gull and adult Black-legged Kittiwake reach the Yellow Sea by a lengthy overland migration (while younger birds take a longer coastal route), the most direct route would be 3,650km from the Laptev Sea via the Lena River into the Yellow Sea to the north of Socheong. Based on estimated flight speeds of c. 60km/hr (Olden & Peterz 1985), Black-legged Kittiwake would be able to complete this flight non-stop within three days. Counts of Black-legged Kittiwake were made daily from Socheong at the end of October/beginning of November 2009. Reanalysis data on 850-mb vector winds (from the National Centres for Environmental Prediction and for Atmospheric Research) during the period of most rapid increase showed that birds crossing from the 190

East Sea at that time would have confronted very strong headwinds. These conditions would not have been energy-efficient for undertaking a potentially hazardous overland flight for a largely pelagic species. However, birds migrating south to the Yellow Sea through mainland north-east Asia (e.g. from the Laptev Sea) would by contrast have experienced almost calm and stable conditions, at least as far south as northern China. There are limitations in the survey methods used in the present study. The results need to be considered as a necessary first-step towards improving the baseline understanding of the distribution and abundance of seabirds at sea in the YSBR. There remains an urgent need to identify migratory bird and habitat relations in the Yellow Sea at a range of scales (Moore et al. 2005), and to improve data collection, analysis and sharing - both nationally and internationally. Already, at the largest scale the migration routes of two tracked and one banded species (Yellow-billed Loon, Streaked Shearwater and Taimyr Gull) make clear the ecological connections between the Arctic, Pacific and southern oceans and between North America, the Yellow Sea and Australia. The United Nations Law of the Seas and the establishment of Exclusive Economic Zones give coastal states extensive rights but also obligations for the appropriate management of marine areas (Camphuysen et al. 2004). The Convention on Biological Diversity further provides clear targets and time-frames for improving the knowledge- base and the conservation status of the seabirds of the Yellow Sea.

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CHAPTER 7

LANDBIRD MIGRATION CORRIDORS ACROSS THE YELLOW SEA: NORTHWARD MIGRATION THROUGH SOCHEONG ISLAND (2010)

ABSTRACT The Yellow Sea is an ecological barrier on the route of migratory landbirds moving between non-breeding and breeding areas. In the absence of radar studies, it is not known whether most landbirds cross this barrier on a broad front or if they are instead concentrated by geography. There are substantial differences in seasonal distribution and abundance of migrant birds observed on offshore islands in the Yellow Sea Blueprint Region (YSBR). We hypothesise that during northward migration landbirds are concentrated by three or more geographical features on the Chinese coast. Birds are then channelled into two main migration corridors, the Northern Crossing and the Southern Crossing. We propose that most birds on the Northern Crossing breed in the DPRK and on the Northeast Asian Mainland, while most birds on the Southern Crossing breed in the southern provinces of the ROK, Japan, Sakhalin and Kamchatka. We predicted that this channelled migration would result in substantial differences in abundance, species composition and timing of migration on different islands north- south in the YSBR, even though such islands are only 400km apart. To test these hypotheses, counts of grounded migrants and visible migration were conducted on Socheong Island, on the Northern Crossing. During the main period of northward migration in spring 2010 a minimum 11,671 landbirds of 167 species were recorded, and >30,000 landbirds were estimated to have passed through the island. These results were compared with published count data from two islands (Hong and Heuksan) on the Southern Crossing. As predicted, abundance was greater and migration timing was later on the Northern Crossing. There were also differences in species composition that support the existence of channelled landbird migration across the YSBR. The concentration of migrant landbirds through geography along two main crossings has enormous implications for research and conservation of species and stopover sites.

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7.1 BACKGROUND AND RESEARCH AIMS 7.1.1 Introduction There are 185 regularly occurring migratory landbird species in the Republic of Korea (ROK) (from hereon defined as all species belonging to the orders Galliformes, Accipitriformes, Falconiformes, Otidiformes, Columbiformes, Cuculiformes, Strigiformes, Caprimulgiformes, Apodiformes, Coraciiformes, Bucerotiformes, Piciformes and Passeriformes). Together they encompass a diverse range of migrant- habitat relations, migration strategies and breeding and non-breeding areas. The development of comprehensive conservation strategies for migratory species depends on understanding migrant-habitat relations at different ecological scales (Moore et al. 2005). Presently, major information gaps remain on migration timing and strategies of almost all these landbird species on a large scale (within East Asia and across the Yellow Sea) and on a small scale (at a stopover site). We are unaware of any research that has investigated whether most landbirds cross the Yellow Sea on a broad front or if they are concentrated during migration by geography. Concentrated migration has enormous implications for research and conservation of species and stopover sites. Bird abundance will not be evenly distributed, and habitat loss and degradation in key staging sites has the potential to affect adversely much larger numbers of birds than in areas where they are not concentrated. In many regions, radar studies have been used in combination with ground-based studies to assess the scale of migration, and reduce the challenge of interpolating observations (Riddiford 1984, Bruderer 1997, Sun 2007). This is not yet possible in the YSBR, due in large part to military concerns. Research to close some of the information gaps on migration is therefore limited to ground-based observations at ―migration hotspots‖ (Åkesson & Hedenström 2004). This chapter presents data from the migration hotspot of Socheong (37°46′ N, 124°45′ E) towards the north of the YSBR. These data are then compared with count data from Eocheong (36°07′ N, 125°58′ E) towards its centre, and Gageo (34°03′ N, 125°09′ E), Hong (34°40′ N, 125°10′ E) and Heuksan (34°41′ N, 125°28′ E) towards the south. Survey on these islands commenced in the early 2000s, and to date there has been only patchy and irregular survey effort on Gageo (Moores & Kim 2001) and Eocheong (see Chapter 8). On Hong and the adjacent Heuksan, regular monitoring of migrants began in 2003, and has increased in frequency since the opening of the Korea National Park Migratory Birds Center (NPMBC) in 2007 (Chae 2007). In 2010, the NPMBC surveyed birds on 193

Hong on 332 days of the year, including throughout the whole of northward migration (March-June). Researchers on both of these islands counted birds that were heard or seen each day, along established count transects, and through the use of mist-nets. The survey area on Hong is c. 20ha, with 8.9ha of land and 11ha of inshore waters (Park Jong-Gil in lit., 2011). On Heuksan, in 2010 there was coverage almost daily in March, daily in April, but for only 17 days in May, with data gathered through the same survey method as on Hong. The survey area is about 113ha (57ha of habitats on land including 14.3ha of freshwater wetland, and the remainder inshore waters) (Park Jong-Gil in lit., 2011, KNP 2010). On neither island was there complete coverage of the much more protracted southward migration (from July to November) (KNP 2010). While incomplete, research on YSBR islands has already led to a substantial improvement in the knowledge base. National status assessments for many species have been modified as a result (see Chapter 2). In order to use data from migrant hotspots to describe the status of populations or to identify underlying population trends, it is first necessary to improve understanding of large-scale influences on the migration of these species across the YSBR.

7.1.2 Migration Across the Yellow Sea The Yellow Sea is an ecological barrier on the route of migratory landbirds that spend the boreal winter in southern China southwards to Southeast Asia and spend the boreal summer in regions east of longitude 125° E: the Korean Peninsula, parts of northeast China and Far East Russia, and Japan. To cross the Yellow Sea, there is a minimum sea-crossing of 450km from the Chinese coast to Hong, and a minimum of 180km from the Shandong Peninsula to Socheong. Based on research in other regions, this barrier can either be crossed by birds maintaining a pre-existing bearing more or less on a broad front, as earlier suggested for birds crossing the Mediterranean Sea (Bruderer 2001), or it will result in concentrated departures from peninsulas and abrupt bends of the coast, as shown by some species in Europe (Bruderer 1997). Earlier, Gore and Won (1971) proposed that there were three main routes used to cross the Yellow Sea during southward migration, all shaped by geographical features (Figure 7.1): 1. Dalian-Shandong Peninsula (both in China), as also taken during northward migration by a Crested Honey Buzzard Pernis ptilorhynchus satellite-tracked by Higuchi et al. (2005); 194

2. Hwanghaenam Province (DPRK)-Shandong Peninsula; 3. Along the west coast of the ROK (exiting the Korean Peninsula in autumn in the southwest, across Jeju and presumably on to Taiwan). Brazil (1991) extended the latter route, depicting a ―Siberia and Manchuria-Korean Peninsula-southern Japan‖ route as a curving arc taken by birds migrating from Taiwan and islands of the Nansei Shoto (Japan) through to the west coast of the ROK. More recently, Chae (2007) implied a broad front Yellow Sea crossing during northward migration at least, from China through Yellow Sea islands and on to the Korean Peninsula. We propose that although broad front homogenous migration remains possible in some species (though as yet unproven) many species are concentrated during northward migration by geographical features. In the absence of radar studies it is not possible to identify the geographical features at the point of departure with certainty. However, there are three well-separated areas on the Chinese coast that appear especially suitable: (1) the Shandong Peninsula; (2) Haizhou Bay (Jiangsu Province); and (3) the coast near Shanghai.

Figure 7.1 Southward migration routes across the Yellow Sea proposed by Gore & Won (1971) and migration route used during southward and northward migration connecting the Korean Peninsula to Japan (Brazil 1991) marked with arrows. Hypothesised departure points during northward migration from Chinese coast for birds migrating to/through the ROK and key YSBR islands marked by yellow dots. Satellite Image from Google Earth. 195

As in other regions, migrant landbirds need to balance the demands of energy, time and safety (Alerstam and Lindström 1990). This includes balancing the potential costs of a long sea-crossing against adding additional distance to the total length of migration required to avoid it. We hypothesise that following concentration by geographical features on the Chinese coast, birds are then channelled into migration corridors During northward migration, populations and species that breed in the DPRK, Amurland and regions to the north and east are channelled into a bearing towards the north of the YSBR on a ―Northern Crossing‖. The Northern Crossing runs southwest- northeast off the east coast of China from Shangai and Haizhou Bay, before turning west-east between 38° N and 37° N for the 180km sea-crossing between Shandong and Hwanghaenam (Figure 7.2). This route takes many of these landbirds across or close to Socheong. Landbirds that breed in southernmost provinces of the ROK and Japan are instead channelled west-east across the south of the YSBR on a ―Southern Crossing‖. This Southern Crossing is concentrated between latitudes 34° N and 31° N and takes many of these landbirds across or close to Hong and Heuksan.

Figure 7.2 Hypothesised migration routes and breeding areas of (1) the Northern Crossing and Northeast Asian Mainland (green); (2) intermediate Areas (unshaded or green-brown); and (3) the Southern Crossing and Far West Pacific Region (yellow). Map outline from NASA Outline.

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A broad front migration strategy across the YSBR should result in a more or less equal number of birds and similar species composition on Socheong, Hong and Heuksan as these islands are only 400km apart. Our hypothesis, focused on northward migration, instead predicts that due to concentration and channelling through the geography of departure points: 1. The largest numbers of birds and the highest species richness will occur on the Northern Crossing. The Northern Crossing is narrow, and use of the Northern Crossing and of Socheong is likely to be efficient for species that breed in a huge region including the DPRK, east Jilin and Heilongjiang, Ussuriland, east Amurland, Khabarovsk and Yakutia (combined, ―Northeast Asian Mainland‖), and progressively less efficient for populations that breed westward and eastward. The Southern Crossing is wider and less concentrated. Migrants have more choices of departure points and routes from China (e.g. across Taiwan and along the Nansei Shoto, or across open sea). Use of Hong and Heuksan will likely be most efficient for landbirds that over-winter in eastern China and breed in the southern provinces of the ROK, and also in Japan, southern Sakhalin and Kamchatka (combined, the ―Far West Pacific Region‖). It will be progressively less efficient northward and westward. 2. There will be a substantial difference in species-composition that use northern (Socheong) and southern (Hong and Heuksan) islands in the YSBR. Socheong will be used by a larger proportion of species that breed on the Northeast Asian Mainland and not in southern ROK provinces and Japan (e.g. Chestnut-flanked White-eye Zosterops erythropleurus). Taxa that breed only in the Far West Pacific Region (―Far West Pacific‖ taxa) will be proportionately more numerous in the south. These include: Sakhalin Leaf Warbler Phylloscopus borealoides, Chestnut-cheeked Starling Agropsar philippensis, Grey Thrush Turdus cardis, Brown-headed Thrush Turdus chrysolaus, Japanese Robin Erithacus akahige, Yellow Bunting Emberiza sulphurata and the personata subspecies of Black-faced Bunting Emberiza spodocephala. 3. There will be differences in the timing of migration shown by the same species north-south, with species migrating earlier along the Southern Crossing. The intensity of migration will thus also peak and decline earlier in the south than in the north. This is because mean temperatures tend to be higher at similar latitudes in Japan than on the Korean Peninsula during April and May (Chapter 197

1, Section 1.3.5). Therefore, populations of species will arrive at breeding grounds in Japan earlier than populations of the same species that breed on the Asian mainland. 4. ―Intermediate Islands‖, lying between Northern and Southern Crossings (e.g. Eocheong), will be intermediate in species richness, species composition and migration timing. Moreover, as Intermediate Islands are outside of the main corridors of migration, most arrivals will be influenced by wind-drift from either the Southern or Northern Crossing (see Chapter 8). This chapter tests these hypotheses by presenting count data from Socheong gathered through northward migration in 2010, including research on Passeriform visible migration. This is the first such account from the ROK. These results are then compared with published data from the southern islands of Hong and Heuksan (KNP 2010) and from unpublished observations made by the author on Gageo and the intermediate Eocheong Island.

7.1.3 Socheong Island Socheong is the smallest (291ha) and southernmost of three closely adjacent inhabited islands. It is separated by a 4.1km channel from the neighbouring island of Daecheong (rising to 343m), and lies 26km to the west and 36km south of the mainland coast of DPRK. The island is heavily vegetated (mostly secondary pine and mixed woodland with some more open grassy areas) and hilly with several low peaks (reaching 174m at highest) and a largely rocky coastline. Much of the western half of the island is <1km wide, and oriented on a southwest-northeast axis. From a lighthouse in the southwest it is 2.2km north-east to a north-facing headland, ―North Point‖. The eastern half of the island is triangular in shape. The longest side is formed by the northern coastline that runs 2.6km east from North Point to ―Northeast Point‖. Socheong thus has several vantage points which allow wide views of birds in flight across the island; known heights and distances that can be used in estimating flight altitude and distance; and geographical features that concentrate migrants once they reach the island.

7.1.4 Previous Research The first systematic counts of birds on Socheong were conducted in 2002 and focused on the migration of diurnal birds of prey. Subsequent research conducted by 198

the author on 130 dates between May 2003 and October 2005 then found almost 300 species, the vast majority of which are either complete or partial migrants to the ROK. During this period seasonal peaks in number of >30 species of landbird were tentatively identified, and 16 species of global conservation concern, eight of which are landbird species, were recorded (Moores 2007). Further counts were then made annually, including counts in 2009 from March 17th-20th; April 11th-16th; May 9th-18th; June 23rd-24th; July 23rd-24th; August 19th-22nd; September 13th-22nd; and October 16th- November 8th. These counts provided further insight into the northward and southward migration periods. By early 2010, 334 adequately documented species had been recorded on the island. However, survey coverage of migration periods remained incomplete. It was thus not possible to estimate, even coarsely, the number of birds present during a whole migration period. All accessible parts of the island are too large to cover every day throughout a whole migration period by a single observer, and there is often much visible migration (Moores 2007). Research in 2009 therefore included an assessment of potential survey circuits, a clearer delineation of count areas, and the identification of the most suitable location and timing during the day for survey of visible landbird migration.

7.1.5 Research Aims Counts of birds were conducted on Socheong during northward migration in 2010. There were three inter-related research aims. The first was to improve understanding of species composition on Socheong. The second was to refine understanding of migration timing of regularly occurring landbird species. Knudsen et al. (2007) describe many of the challenges inherent in characterising the migration phenology of species, even in areas with constant survey effort and many years of data. There are presently too few data and too many differences between count methods on YSBR islands to be able to develop robust models of migration timing and intensity. We therefore focused on the identification of the earliest records (―First-dates‖), the date of the highest count (―Peak Count Dates‖), and the date of the latest record (―Last-dates‖). These dates help to reveal similarities and dissimilarities in migration strategies between species on Socheong, and between Socheong and other islands. The third aim was to estimate the abundance of the more numerous landbird species on Socheong throughout one period of northward migration. This required sub-dividing the island into countable units (see Methods) and also conducting research on visible diurnal 199

migration. Much published literature on passerine migration appears to accept, implicitly or explicitly, the existence of different migration strategies between nocturnal and diurnal passerine migrants (Åkesson et al. 1996, Bruderer 1997, Åkesson et al. 2004, Chernetsov 2006, Delingat et al. 2006, Fischer et al. 2012). Assumptions on such differences can affect survey methods and analysis of count data. However, prior research on several YSBR islands suggested that rather few Passeriform species had exclusively nocturnal or diurnal migration strategies.

7.2 METHODS 7.2.1 Count Method Counts of all birds (heard and seen, irrespective of range from the observer) were made through binoculars and a tripod-mounted telescope on all dates between March 30th and June 2nd 2010 (―the survey period‖) with the exception of April 9th-11th, May 11th-14th and May 23rd. Counts were made each day by active search along one or more of four transect ―circuits‖ (Figure 7.3): (1) The central part of the island near to the main village, each day for between one and three hours; (2) North Point on 39 dates, for between one and six hours; (3) all easily-accessible parts of the western half of the island (―West‖), on 11 dates for between four and ten hours; and (4) all easily- accessible parts of the eastern half of the island (―East‖), on 11 dates for between four and nine hours. ―Whole Island Counts‖, covering all the above areas (i.e. all easily- accessible areas on the island, an area of c. 200ha), were also conducted on 13 additional dates, each taking between 11 and 14 hours. To facilitate estimates of seasonal abundance, Whole Island Counts were conducted twice within each ten- or eleven-day period in April and May, in early- (1st-10th), mid- (11th-20th) and late- (21st- month end) month, on April 3rd & 7th, 16th & 20th and 23rd & 29th; and on May 7th & 10th, 16th & 20th, and 25th & 29th. A Whole Island Count was also conducted once in June, on June 1st. Thus birds were counted in total in all of the West and East on 24 dates and on North Point on 52 dates. Twelve of the 13 Whole Island Counts were conducted on days of good visibility, and ten of the Whole Island counts were preceded and followed by a fuller day of survey in the West and East. This was in order to count more difficult to identify species and to determine whether some individuals or species were demonstrating high rates of through-movement or if they appeared to be staging for more than one day.

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Fig. 7.3 Socheong Island and survey circuits: ―West‖ outlined in yellow, with dotted lines indicating transect routes; ―Central‖ outlined in pink; and ―East‖ outlined in red with orange dotted lines indicating transect routes.

These circuits, along both paved and unpaved surfaces, covered all the main habitats and aimed to maximise raw counts and to identify all bird species. On some days more time was spent in one habitat or searching for shy species than on others. Throughout, there is likely to have been bias towards the discovery of vocal species and species of open and edge habitats and away from especially cryptic or silent species, especially those that prefer closed canopy woodland. Counts along transects were supplemented by further fixed-point counts of arriving and departing migrants, most especially from North Point (with the focus on the movement of Passeriformes near to sun-rise, for a total of 40 hours spread across 32 dates), and at Northeast Point (due to access restrictions, more opportunistically, only for 145 minutes on a total of four dates). At such times, the direction of birds‘ movements at departure were assessed through the use of a GPS unit and through landmarks identified by maps. Counting large numbers of birds is typically inexact (Rappoldt et al. 1985, Rogers et al. 2006b). There was no robust method with which to assess the completeness or accuracy of these counts. However, a comparison of counts of two species with widely-differing migration strategies shown in Figure 7.4 suggests that coverage was sufficient to detect differences in migration strategies and substantial changes in number. For example, no Brown-eared Bulbul was seen to depart the island in either 201

April or May during visible migration counts (although there was an arrival of 55 on June 2nd). Whole Island Counts of Brown-eared Bulbul in April remained almost constant, and showed some reduction in May as several previously vocal birds started nesting. There was some variation between East and West components within these counts (not shown) that reflected an observed movement of birds across the centre of the island from West to East and vice-versa. In contrast, there was a marked change in the number of Olive-backed Pipit Anthus hodgsoni recorded during each of the Whole Island Counts, and this was also one of the more numerous species recorded during diurnal migration counts (Section 7.3.8).

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150 BROWN-EARED BULBUL OLIVE-BACKED PIPIT 100

50

0 03 April 07 April 16 April 20 April 23 April 29 April 07 May 10 May 16 May 20 May 25 May 29 May 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010

Figure 7.4 Numbers of Brown-eared Bulbul and Olive-backed Pipit recorded during 12 Whole Island Counts in April and May.

On each day, count data were reviewed for double-counting. Movement of birds from the southwest towards the centre of the island was observed on most dates, and distinctive individuals and similar-sized flocks were on some days located first in the southwest of the island and then in the centre or northeast the same day. Such distinctive birds were counted only once for that day. It was not possible to determine the scale of potential double-counting of birds that were not distinctive. However, based on repeat counts of the same areas on multiple dates, we consider that more birds were likely missed than double-counted.

7.2.2 Weather Weather was assessed daily (and at 30-minute intervals during counts of visible migrants), including visibility in kilometres (based on the invisibility or otherwise of other islands and landmarks), wind speed and direction. Reanalysis data from the National Center for Environmental Prediction–National Center for Atmospheric Research (NCEP-NCAR) were also accessed (at: www.esrl.noaa.gov/psd/data/histdata). 202

Composites of 850-mb vector winds from NCEP-NCAR data were examined for selected dates, as they can reveal many of the weather processes relevant to birds in flight (S. Feldstein in lit. 2011).

7.2.3 Data Collation The data were then collated in three main ways, ranging in scale from a minimum to a possible maximum number of counted birds: 1. The ―peak count‖ is the highest count of a species on any one date during the survey period (not confined to Whole Island Counts). Due to asynchronous migration strategies (with e.g. some individuals departing before others of the same species have arrived) and incomplete coverage, the peak count is likely to be an underestimate of the total number present during a migration season of almost all species – more so than for shorebirds (Chapter 4) because many of the landbirds in the present research likely stopped over for hours or days rather than for weeks. 2. A ―Whole Island Estimate‖ is provided for ten species (see Section 7.3.7). 3. ―Bird-days‖ are presented for all species individually and collectively; and ―Estimated Bird-days‖ are provided for ten species and collectively. Bird-days treat counts of e.g. 100 individuals on one day and one bird on 100 days equally. They do not distinguish between survey frequency, the number of days a bird stays within a given recording area and the actual number of birds present. Bird-days therefore overestimate the number of individuals that are recorded if those same individuals are recorded on more than one date. However, the NPMBC uses bird-days for Hong and Heuksan and does not include peak counts or specific dates for most species (KNP 2005-2010). Bird-days are therefore used here and in Chapter 8 to help define the upper ceiling for the number of birds recorded during the survey period, and to enable comparison with counts on Hong and Heuksan in 2010 (Section 7.3.9) and with Eocheong in 2011 (Chapter 8, Table 8.2).

7.3 RESULTS 7.3.1 Species, Families and Orders A total of 229 species from 56 families and 18 orders including 167 species of landbird were recorded on Socheong during the survey period (Table 7.1). 203

Table 7.1 Number of regularly occurring orders and species in the ROK (from Moores & Park, 2009), that were adequately documented on Socheong Island between 2003 and 2009, and that were recorded during the survey period (2010). Order Number of Adequately Number of species regularly documented recorded during the occurring species recorded present survey period species in ROK on Socheong on Socheong (2003-2009) (2010) Galliformes 3 1 1 Anseriformes 34 18 7 Gaviiformes 4 4 3 Procellariiformes 4 3 1 Podicipediformes 5 4 2 Ciconiiformes 2 1 0 Pelecaniformes 21 22 14 Accipitriformes 19 20 10 Falconiformes 5 6 4 Otidiformes 1 0 0 Gruiformes 12 6 2 Charadriiformes 74 52 33 Columbiformes 4 5 2 Cuculiformes 5 7 7 Strigiformes 8 8 2 Caprimulgiformes 1 1 1 Apodiformes 2 3 2 Coraciiformes 5 3 3 Bucerotiformes 1 1 1 Piciformes 8 3 2 Passeriformes 147 166 132 Total 365 334 229

In total, 207 of the species recorded by the survey are regularly occurring in the ROK and 22 occur less regularly. The majority of species (58%) were Passeriformes, with the remainder comprised of 34 landbird Non-Passeriform species (from 12 families and 10 orders) and 62 species of waterbird and seabird (from 15 families and 7 orders). Six out of nine seabird species (here defined as Procellaridae, Phalacrocoracidae, Laridae and Alcidae) were present on most dates, with up to a maximum of 3,300 individuals. As the research focus was on landbirds, seabirds are included in Table 7.1 and in Chapter 6 but are excluded from the rest of the analysis in this chapter.

7.3.2 Species‘ Abundance and Richness Based on the sum of peak counts, and excluding seabirds, a minimum of 11,907 birds identified to species were recorded. Of these, 236 were waterbirds and 11,671 were landbirds. During each of the 13 Whole Island Counts, a mean of 77 species and 1,207 birds (landbirds and waterbirds combined) were recorded. A minimum 47 species were recorded on April 7th and a maximum 98 species were recorded on April 204

29th. The minimum number of individuals recorded was 497 (on June 1st) and the maximum was 3,208 individuals, comprised of 3,176 landbirds and 32 waterbirds (on April 29th) (Figure 7.5).

Landbirds During Whole Island Counts

3500 3000 2500 2000 Total 1500 1000 500 Number Landbirds of 0 03 07 16 20 23 29 07 10 16 20 25 29 01 April April April April April April May May May May May May June 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 Date of Whole Island Count

Figure 7.5 Number of landbirds recorded during each of the 13 Whole Island Counts.

7.3.3 Species of Global Conservation Concern Ten species of global conservation concern were recorded during the survey period, all of which had also been previously recorded on Socheong. In addition to globally Vulnerable Yellow-breasted Bunting Emberiza aureola there were single Near- threatened Japanese Quail (on May 9th), Endangered Japanese Night Heron Gorsachius goisagi (from May 18th to at least until June 2nd), Vulnerable Chinese Egret (on May 25th), Near-threatened Japanese Waxwing Bombycilla japonica (on May 8th), Vulnerable Manchurian Reed Warbler Acrocephalus tangorum (on May 8th) and Vulnerable Yellow Bunting (one on April 19th); between one and three Vulnerable Fairy Pitta Pitta nympha (on three dates between May 29th and June 3rd); two Near- threatened Black Paradise Flycatcher Terpsiphone atrocaudata (on May 31st); and two Near-threatened Ochre-rumped Bunting Emberiza yessoensis (on April 17th, with single birds recorded on five further dates).

7.3.4 Timing of Migration, Peak Counts and Bird-days 7.3.4.1 Species selection Analysis of migration timing was conducted on landbird species that were: transitory, complete migrants to Socheong and which were recorded on five or more dates in the present research. In total, 57 landbird species were thus excluded. This 205

group comprised one (irruptive) sedentary species (Eurasian Jay Garrulus glandarius); seven breeding partial migrants (Peregrine Falcon Falco peregrinus, Oriental Turtle Dove Streptopelia orientalis, Large-billed Crow Corvus macrorhynchos, Eastern Great Tit, Brown-eared Bulbul, Grey-capped Greenfinch Carduelis sinica and Meadow Bunting Emberiza cioides); one breeding summer visitor (Blue Rock Thrush Monticola solitarius), which was recorded daily from April 2nd; and 48 species recorded on only 1-4 dates.

7.3.4.2 Data presentation The remaining 120 species have been divided into seven main groups (documented in Subsections 7.3.4.3-7.3.4.9). These groups range from ―Early Migrants‖ (none of which had Last-dates after May 7th) to ―Very Late Migrants‖ (all with First-dates after May 15th). For each of these groups, a table is presented in which species are divided into partial migrants and complete migrants to the ROK (where appropriate), and listed in order of their First-date, Last-date and then Peak Count Date. Breeding status in the ROK (No, Scarce and Yes) is based on Moores & Park (2009) and Birds Korea unpublished data. ―No. of Dates‖ indicates the number of dates on which each species was recorded during the 57 dates of the present survey. Each species‘ unadjusted peak counts and the number of bird-days are also provided. Further details are included on selected species in the main text as representative examples of species‘ migration strategies, thus including sexually dimorphic species and distinctive subspecies with different migration timing, and species that breed on and those that breed far from the Korean Peninsula. These examples are therefore considered useful for further interpretation of the data, and to inform the discussion in this and the subsequent chapter.

7.3.4.3 Extended presence Eleven species had First-dates before mid-April and were also recorded into June (Table 7.2). Therefore First-dates or Last-dates might have occurred outside of the survey period. Of these, only Light-vented Bulbul Pycnonotus sinensis migrates through and is also known to breed on Socheong. Little Bunting Emberiza pusilla showed evidence of three phases of migration, including departing over-wintering birds, followed by northward movement of the main population, and then by late outliers (Figure 7.6). With the exception of Hawfinch Coccothraustes coccothraustes 206

(which in most years was not recorded after mid-May but was atypically still present into June in 2010), the remaining eight species are absent from Socheong in the mid- winter period, and all have also occurred very late during northward migration in other years.

900 800 700 600 500 GREY WAGTAIL

400 LITTLE BUNTING Number 300 200 100 0 1 2 3 4 5 6 Ten-day Period

Figure 7.6 Numbers of Grey Wagtail and Little Bunting recorded by 10-day period between April 1st (decade 1) and the end of survey on June 2nd. Most Little Bunting were recorded in late April, with a long ―tail‖ of records after the Peak Count Date. Small numbers of Grey Wagtail were recorded almost daily, including during visible migration counts.

Some of the species have breeding ranges that extend far to the north and west of the ROK (e.g. Barn Swallow, Grey Wagtail Motacilla cinerea and Red-throated Pipit Anthus cervinus); others might breed some years on Socheong (Pale Thrush and Grey- backed Thrush Turdus hortulorum); and some breed in the DPRK, either rarely (Chinese Blackbird), regularly (Black-faced Bunting) (Tomek 1999, 2002) or commonly in some areas (Olive-backed Pipit: J.W. Duckworth in lit. 2011).

Table 7.2 Species with First-dates before Mid-April and Last-dates in June. Species Breeds No. of First- Peak Count Last- Peak Bird- ROK? dates date Date date Count days Partial Migrant Pale Thrush Yes 39 Apr 3 Apr 29 Jun 2 97 804 Light-vented Bulbul Scarce 32 Apr 3 May 29 Jun 2 15 136 Complete Migrant Black-faced Bunting No 51 Mar 30 Apr 29 Jun 2 283 2,408 Chinese Blackbird Scarce 18 Mar 31 Apr 4, May 3 Jun 1 4 25 Barn Swallow Yes 45 Mar 31 May 25 Jun 2 122 809 Hawfinch No 34 Mar 31 May 16 Jun 2 11 107 Olive-backed Pipit Scarce 52 Apr 2 Apr 30 Jun 2 609 2,973 Little Bunting No 43 Apr 2 Apr 28 Jun 1 370 1,267 Grey Wagtail Yes 47 Apr 3 Apr 23, May 26 Jun 1 10 163 Grey-backed Thrush Yes 47 Apr 3 Apr 29 Jun 2 652 1,439 Red-throated Pipit No 26 Apr 12 Apr 23 Jun 1 10 69

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7.3.4.4 Early Migrants Twelve species were present in April and had Last-dates before May 8th (Table 7. 3). Three of these (Bull-headed Shrike Lanius bucephalus, White-cheeked Starling Spodiopsar cineraceus and Eastern Buzzard Buteo japonicus) had slightly later single outliers in 2009, between May 9th and May 11th. Eleven of the 12 occur regularly in the ROK in the boreal winter and half also breed in the ROK. Based on previous survey, it is likely that at least some individuals of these species migrated through Socheong before the study period. Several of the non-breeding winter-visitors to the ROK might also have peaked before the start of the survey period in March, as all were present on Socheong during survey between March 17th and 20th, 2009.

Table 7.3 Species with Last-Dates before the Whole Island Count of May 8th. Species Breeds No. First- Peak Count Last- Peak Bird- ROK? of Date Date Date Count days Dates Partial Migrant Far Eastern Skylark Yes 6 Mar 30 Apr 2 Apr 3 3 9 Bull-headed Shrike Yes 15 Mar 30 Apr 3 Apr 17 27 76 White-cheeked Starling Yes 16 Mar 31 Apr 3 May 6 90 158 Common Kestrel Yes 5 Apr 6 Apr 6, Apr 29 Apr 29 2 7 Complete Migrant Long-tailed Rosefinch No 11 Mar 30 Apr 2 Apr 15 14 43 Rustic Bunting No 13 Mar 31 Apr 1 Apr 24 60 126 Naumann‘s Thrush No 27 Mar 31 Apr 3 May 3 117 332 Siberian Accentor No 9 Apr 1 Apr 3 Apr 20 3 15 Buff-bellied Pipit No 24 Apr 1 Apr 17 Apr 30 19 131 Eurasian Skylark Scarce 13 Apr 2 All Dates May 2 1 13 Black Redstart* No 9 Apr 4 Apr 17 May 7 2 11 Eastern Buzzard No 9 Apr 21 All dates May 7 1 9 Note: Black Redstart is presently considered not to be a regularly occurring species in the ROK.

The peak of White-cheeked Starling might also have occurred in March. More than 200 were counted in the West of Socheong in late March 2004. In 2010, the species was also recorded on June 1st. This was considered likely due to post-breeding dispersal, as 506 were present on Socheong in late June 2009, including many juveniles. Such post-breeding dispersal by White-cheeked Starling and other starling species to YSBR islands appears to be widespread and regular (unpublished data). The June 1st record is therefore excluded from Table 7.3.

7.3.4.5 Early-Mid Season Migrants Seven species were present at the beginning of the survey which (in addition to ten other species with First-dates between April 1st and April 24th) also had Last-dates between May 8th and May 21st (Table 7.4). This group of 17 species includes six that 208

are most widespread in the ROK as winter visitors or as migrants during April; and six that have been recorded breeding in the ROK but not on Socheong. Among the former group, Dusky Thrush Turdus eunomus peaked two weeks later than the closely-related Early Migrant Naumann‘s Thrush (Figure 7.7). Dusky Thrush has a breeding range that is generally to the west, north and east of Naumann‘s Thrush (Brazil 2009).

140 120 100 80 DUSKY THRUSH

60 NAUMANN'S THRUSH Number 40 20 0 03 07 16 20 23 29 07 10 16 20 April April April April April April May May May May 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 Whole Island Count

Figure 7.7 Numbers of Naumann‘s Thrush and Dusky Thrush during the 13 Whole Island Counts.

As in previous years, early migrating White Wagtail Motacilla alba included some of the subspecies lugens (which over-winters in the ROK) with the majority leucopsis (which is mostly a summer visitor to the ROK and adjacent regions: Alström and Mild 2003). The more northerly-breeding ocularis had a First-date of April 14th, and was the most numerous White Wagtail subspecies between April 25th and May 7th (a similar pattern to that shown on other YSBR islands: unpublished data). It is possible that the peak of leucopsis White Wagtail and of Yellow-throated Bunting Emberiza elegans occurred in late March before the survey period. The highest counts of leucopsis on Eocheong have been recorded in late March (unpublished data), and 200 Yellow-throated Bunting were counted in the West of Socheong on March 24th 2004. Both species reached their peak in late March on Hong in 2010 (KNP 2010). Two of the Early-Mid Season Migrants are Far West Pacific taxa: Brown-headed Thrush and Grey Thrush. Most of the Brown-headed Thrush were of the nominate Japan-breeding subspecies, though on April 19th included one of subspecies orii (which breeds in the Kuril Islands: Brazil 2009). In both species (and in the majority of Passeriformes which were straightforward to sex and age in the field) early individuals 209

were adult-type males, followed by females and then by second calendar-year birds. In both species, second calendar-year birds were responsible for the late outlying dates.

Table 7.4 Species with First-dates between March 30th and April 25th and Last-dates before May 21st. Species Breeds No. of First- Peak Last- Peak Bird- ROK? Dates Date Count Date Count days Date Partial Migrants Yellow-throated Bunting Yes 35 Mar 30 Apr 3 May 9 130 899 White Wagtail Yes 37 Mar 31 Apr 3 May 10 37 337 Coal Tit Yes 30 Mar 31 Apr 4 May 8 30 189 Winter Wren Scarce 24 Apr 1 Apr 20 May 9 11 79 Complete Migrants Eurasian Hoopoe Yes 28 Mar 30 Apr 29 May 8 6 52 Goldcrest No 30 Mar 30 Apr 16 May 10 23 186 Dusky Thrush No 43 Mar 31 Apr 17 May 20 233 1,016 Pallas‘s Reed Bunting No 15 Mar 31 Apr 1 May 16 4 24 Eurasian Siskin No 11 Apr 1 May 2 May 10 11 43 Greater Short-toed Lark No 23 Apr 3 Apr 16 May 9 13 69 White‘s Thrush Yes 38 Apr 15 Apr 27 May 18 80 374 Grey Thrush No 14 Apr 15 Apr 27 May 18 3 19 Eurasian Wryneck No 21 Apr 16 Apr 29 May 10 22 108 Ochre-rumped Bunting No 6 Apr 17 Apr 17 May 19 2 7 Brown-headed Thrush No 17 Apr 19 Apr 23 May 19 5 36 Yellow-bellied Tit No 5 Apr 24 Apr 25 May 8 7 13 Hume‘s Leaf Warbler* No 13 Apr 24 May 2, 16 May 20 2 15 Note: survey started on March 30th; Hume‘s Leaf Warbler is presently considered not to be a regularly- occurring species in the ROK.

7.3.4.6 Mid-Season Migrants Twenty-three species were present in April, most from mid-month, and had Last- dates between May 21st and May 31st (Table 7.5). These include seven widespread breeders in the ROK and only two species that are widespread in mid-winter and absent in summer (Eurasian Sparrowhawk Accipiter nisus and Brambling Fringilla montifringilla). Although many within this group were present throughout the survey period, the timing of the Peak Count Date for 10 out of 11 of the species with a peak of >15 was before mid-May. The exception was Yellow-breasted Bunting, which peaked during a substantial inclement weather movement on May 18th. In 2009, the peak of Yellow-breasted Bunting was recorded on May 15th, in a similar movement. In 2009 and 2010, based on male-plumages, subspecies aureola made-up the majority of the small number of early records and continued migration through to at least Mid-May. Subspecies ornata (which breeds only in parts of East Asia east to Sakhalin and now only very locally in Hokkaido: BirdLife International 2011) was recorded only in May, with the earliest in 2010 on May 7th. This pattern is similar to that recorded on Eocheong, where the earliest ornata was confirmed on May 8th 2003 and on May 14th 210

2011. The difference in timing of First-dates between subspecies might be the result of the remaining distance to breeding grounds: much shorter for ornata than more westerly-breeding aureola. Many species with earlier Peak Count Dates showed large differences in turnover rates, including Asian Stubtail Urosphena squameiceps and Red-flanked Bluetail Tarsiger cyanurus (Figure 7.8).

500 450 400 350 300 ASIAN STUBTAIL 250 RED-FLANKED BLUETAIL

Number 200 150 100 50 0 03 07 16 20 23 29 07 10 16 29 April April April April April April May May May May 2010 2010 2010 2010 2010 2010 2010 2010 2010 2010 Whole Island Count

Figure 7.8 Numbers of Asian Stubtail and Red-flanked Bluetail recorded during the 12 Whole Island Counts in April and May, showing a contrast in the length of their migration timing.

Asian Stubtail showed a series of small peaks (on April 17th, 20th and 24th), with most birds departing the following day. This was followed by a very substantial arrival from mid-morning to the afternoon of April 29th which resulted in a Whole Island Count of 464. On April 30th, the number in the West had fallen approximately 80%, with one moribund and two dead individuals also found. There was no evidence of a further peak, rather a gradual reduction from 12 on May 4th to only two during the Whole Island Count on May 10th (the last record until a single outlier on May 29th). The compactness of the main migration period, with 65% of the total recorded on only two days, resembled the pattern on Eocheong in 2011, when 50% of Asian Stubtail bird-days were recorded between April 26th and April 29th. It seems plausible that this concentrated peak might be a result of the species‘ rather narrow breeding range (confined to the Korean Peninsula, Ussuriland, Sakhalin and Japan: Brazil 2009). By contrast, Red-flanked Bluetail is present locally in the boreal winter in the ROK. It initially showed a similar pattern to Asian Stubtail and several other species. There was a series of small peaks and troughs, followed by a large arrival between April 16th 211

and 17th. However, the subsequent post-peak tail was much longer than in Asian Stubtail and contained several further small peaks. The five-day period with the highest peak (April 16th-20th) contained 32% of the total of Red-flanked Bluetail bird- days. This was followed by two five-day periods containing 14% and 8% of bird-days respectively. During the same period there was evidence of some birds (including adult males) arriving and establishing temporary territories for several days, coincident with the number of Red-flanked Bluetail in the West remaining almost steady. The last count of >10 Red-flanked Bluetail was on May 2nd; the species was recorded daily until May 10th; and the last outliers were recorded on May 18th and May 27th. The early Peak Count Date and extended tail are likely a result of the species‘ over-wintering within East Asia and its very wide breeding range (extending from the DPRK northwest to Finland and east to Japan: Brazil 2009). The majority of adult males passed through early in the main migration period, in mid-April. The presence of both early and later migrating adult males suggests that different populations, with different non-breeding and breeding areas, might move through the YSBR.

Table 7.5 Species present in April with Last-dates between May 21st and May 31st. Species Breeds No. of First- Peak Count Last- Peak Bird- ROK? Dates Date Date Date Count days Partial Migrant Daurian Redstart Yes 40 Mar 30 Apr 3 May 24 69 366 Japanese Sparrowhawk Yes 21 Apr 23 May 25 May 28 5 38 Complete Migrant Red-flanked Bluetail No 42 Mar 30 Apr 17 May 27 247 1,574 Siberian Stonechat Yes 57 Mar 30 Apr 29 May 30 135 1,048 Red-billed Starling Scarce 12 Mar 31 Many Dates May 26 2 17 Brambling No 39 Mar 31 Apr 6 May 27 402 2,434 Grey-faced Buzzard Scarce 41 Apr 1 May 8 May 29 114 425 Siberian Rubythroat Scarce 32 Apr 7 Apr 29 May 29 25 382 Pallas‘s Leaf Warbler Scarce 39 Apr 12 May 7 May 29 31 224 Asian Stubtail Yes 24 Apr 15 Apr 29 May 29 464 849 Eurasian Sparrowhawk No 11 Apr 16 All Dates May 24 1 11 Yellow-browed Bunting No 25 Apr 17 May 8 May 27 175 930 Common House Martin* No 5 Apr 20 May 25 May 26 12 21 Blue-and-white Flycatcher Yes 6 Apr 20 Apr 29 May 26 16 104 Citrine Wagtail No 6 Apr 25 All Dates May 25 1 6 Common Rosefinch No 23 Apr 26 May 25 May 29 10 75 Asian House Martin No 14 Apr 27 May 26 May 27 9 52 Yellow-breasted Bunting No 15 Apr 28 May 18 May 28 28 59 Oriental Cuckoo Yes 13 Apr 29 May 1, 24 May 28 2 17 Bluethroat No 7 Apr 29 May 1 May 21 2 9 Grey Nightjar Yes 10 Apr 29 Three Dates May 31 2 13 Rufous-tailed Robin No 18 Apr 29 May 20 May 31 10 62 Eastern Yellow Wagtail No 32 Apr 30 Apr 30 May 29 79 407 Note: Common House Martin is presently considered not to be regularly occurring in the ROK.

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7.3.4.7 Main Period Twenty-five species had First-dates between April 15th and 30th, and were still present into June, 17 of which have been recorded breeding in the ROK (Table 7.6). Five of these were present in late June 2009, and therefore might breed on or near Socheong: Korean Bush Warbler, Oriental Scops Owl Otus sunia, Eurasian Hobby Falco subbuteo, Red-rumped Swallow Cecropis daurica and Black-naped Oriole. While the majority of species showed a series of small peaks and troughs, three species (Yellow-browed Warbler Phylloscopus inornatus, Chestnut Bunting and Eyebrowed Thrush Turdus obscurus) showed extremely sharp peaks (Figure 7.9), indicating rapid through-movement, mostly associated with weather-related arrivals (see Chapter 8). On April 27th, only five Yellow-browed Warbler were counted on North Point and in the West. On April 28th, 2,586 were recorded (68% of all bird-days) in the East, including c. 2,500 seen arriving and trying to depart (Section 7.3.8.2). On April 29th, the Whole Island Count recorded 144: a 94% decline between days, despite the larger area surveyed. Based on previous research, the size of this movement was exceptional. This very sharp peak was then followed by a further smaller peak in Mid-May. This latter peak was similar in timing to that observed during northward migration on Eocheong in 2011.

160 140 120 100 CHESTNUT BUNTING 80 EYE-BROWED THRUSH

Number 60 YELLOW-BROWED WARBLER 40 20 0 23 29 07 10 16 20 25 29 01 April April May May May May May May June 2010 2010 2010 2010 2010 2010 2010 2010 2010 Whole Island Count

Figure 7.9 Numbers of Yellow-browed Warbler, Eye-browed Thrush and Chestnut Bunting during Whole Island Counts. The largest Yellow-browed Warbler peak occurred during a major weather event at the end of April (missed by the Whole Island Count), and was followed by several peaks and troughs into late May. Numbers of both Eyebrowed Thrush and Chestnut Bunting were more concentrated, with almost all records in two weeks in May.

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The migration of Chestnut Bunting migration was highly-concentrated, with 76% of bird-days recorded on three dates: May 8th (49%), May 18th (20%) and May 20th (7%). Eyebrowed Thrush migration showed a similar pattern. This species was recorded on 36 dates during the survey period, but 72% of bird-days were recorded on only three well-spaced dates, with peaks steadily decreasing in size: May 8th (45%), May 18th (21%) and May 27th (6%).

Table 7.6 Species with First-dates between April 15th and 30th which were still present into June. Species Breeds No. of First- Peak Last- Peak Bird- ROK? Dates Date Count Date Count days Date Partial Migrant Common Kingfisher Yes 24 Apr 17 May 2 Jun 1 9 53 Complete Migrant Ashy Minivet No 28 Apr 15 Apr 26 Jun 2 38 153 Korean Bush Warbler Yes 35 Apr 15 May 30 Jun 2 19 181 Oriental Scops Owl Yes 20 Apr 16 Apr 29 Jun 1 6 37 Eastern Crowned Warbler Yes 26 Apr 16 Apr 29 Jun 2 12 73 Yellow-browed Warbler No 41 Apr 17 Apr 28 Jun 1 2,586 3,825 Siberian Blue Robin Yes 33 Apr 17 May 20 Jun 1 74 382 Tristram‘s Bunting Scarce 38 Apr 17 Apr 29 Jun 2 159 739 Eurasian Hobby Scarce 27 Apr 17 May 8 Jun 2 10 73 Chestnut-eared Bunting Yes 25 Apr 17 May 26,29 Jun 2 8 76 Richard‘s Pipit No 38 Apr 19 May 19 Jun 1 26 248 Red-rumped Swallow Yes 30 Apr 20 May 24 Jun 1 291 938 Fork-tailed Swift Yes 19 Apr 20 May 21 Jun 2 210 381 Yellow-rumped Flycatcher Yes 26 Apr 20 May 20 Jun 2 36 296 Pale-legged Leaf Warbler No 30 Apr 20 May 29 Jun 2 54 334 Asian Brown Flycatcher Scarce 30 Apr 21 May 29 Jun 1 45 389 Eyebrowed Thrush No 36 Apr 21 May 8 Jun 2 785 1,744 Chinese Grosbeak Yes 29 Apr 25 May 21 Jun 2 22 166 White-throated Needletail Scarce 13 Apr 28 May 27 Jun 1 22 74 Brown Shrike Scarce 30 Apr 28 May 25 Jun 2 95 443 Black-naped Oriole Yes 23 Apr 28 May 30 Jun 2 26 178 Pechora Pipit No 21 Apr 30 May 18 Jun 2 8 68 Crested Honey Buzzard Scarce 15 Apr 30 May 6 Jun 1 21 81 Blyth‘s Pipit No 19 Apr 30 May 19 Jun 1 7 29 Chestnut Bunting No 23 Apr 30 May 8 Jun 1 750 1,520

Count data from Socheong in 2009 and Eocheong in 2011 suggest that such concentrated passage in Mid-May is regular in both Chestnut Bunting and Eyebrowed Thrush, and that both species are often involved in the same movements. Based on Brazil (2009) the breeding ranges of both species overlap in Khabarovsk and westward, although Eyebrowed Thrush additionally breeds further east in Sakhalin and Kamchatka. The First-date of Eyebrowed Thrush on Socheong in 2010 was nine days earlier than that of Chestnut Bunting. Brazil (1991) described Chestnut Bunting as a rare spring migrant to Japan, and Eyebrowed Thrush as an uncommon or even reasonably common migrant to Japanese islands in the East Sea in late April and May. 214

In consideration of the substantial overlap during their peak migration periods, and of the earlier migration timing shown by some more eastern-breeding taxa, it is probable that the small number of early migrating Eyebrowed Thrush belong to the more eastern population, and the main movements involve birds migrating towards their mainland Asia breeding range.

7.3.4.8 Late Migrants Nineteen species had First-dates between May 1st and May 11th (Table 7.7). All of these apart from Japanese White-eye are complete migrants to the ROK. However, all Japanese White-eye recorded during the survey period were of the subspecies simplex, which is a complete migrant at the national level. None of the 19 taxa have been recorded during the boreal winter in the ROK; nine have been recorded breeding in the ROK; and while two of the species (Oriental Dollarbird Eurystomus orientalis and Oriental Reed Warbler Acrocephalus orientalis) were recorded on the island in late June 2009, none of the nine species are considered to breed on Socheong.

Table 7.7 Species with First-dates between May 1st and May 11th. Species Breeds No. of First- Peak Last- Peak Bird- ROK? Dates Date Count Date Count days Date *Japanese White-eye No 11 May 1 May 8 May 20 50 168 Oriental Dollarbird Yes 17 May 2 May 20 Jun 2 10 56 Black-capped Kingfisher Yes 9 May 3 May 24, 28 May 28 2 11 Forest Wagtail Yes 13 May 6 May 18 May 27 21 57 Taiga Flycatcher No 17 May 6 May 25 May 30 14 78 Radde‘s Warbler Scarce 21 May 6 May 7 Jun 2 32 151 Common Cuckoo Yes 20 May 7 May 25 Jun 1 9 53 Grey-streaked Flycatcher No 19 May 7 May 16 Jun 2 24 148 Two-barred Warbler No 15 May 7 May 26 Jun 1 17 83 Chestnut-flanked White-eye No 17 May 7 May 25 Jun 2 335 1,475 Daurian Starling Scarce 8 May 8 May 24, 26 May 29 2 10 White-throated Rockthrush No 14 May 8 May 19 May 29 15 71 Chinese Sparrowhawk Yes 18 May 8 May 20 Jun 2 18 83 Mugimaki Flycatcher No 21 May 8 May 20 Jun 2 26 189 Siberian Thrush No 17 May 8 May 25 May 31 19 90 Northern Hawk-cuckoo Yes 15 May 8 May 25 Jun 2 10 44 Pallas‘s Grasshopper Warbler No 10 May 10 May 29 May 31 5 22 Oriental Reed Warbler Yes 13 May 10 May 27 Jun 2 11 39 Black Drongo No 10 May 10 Jun 1 Jun 2 5 21 Note: All taxa are complete migrants to the ROK. Japanese White-eye records refer to subspecies simplex.

Among this group, Chestnut-flanked White-eye was the only species with a peak count of >100. The species typically forms compact and fast-moving flocks. Flocks were often observed arriving in the southwest of the island, and moving rapidly eastward. Although some flocks appeared to stage for one or more days in the East of the island, 215

other birds probably crossed the island in under an hour. On Eocheong in 2011, the species was also a late migrant, with the first birds recorded on May 10th, and a larger wave of birds arriving on May 12th. The majority of individuals in this second wave were considered to have staged for three days as numbers remained constant between May 12th and 14th (Chapter 8). It seems reasonable to assume that in the absence of strong headwinds, individuals of the same species that have undertaken longer flights will need to stage for longer than those that have undertaken a shorter flight. Thus, many of the Chestnut-flanked White-eye on Socheong probably arrive there after undertaking a short sea-crossing (i.e. from the Shandong Peninsula), while those on Eocheong in 2011 arrived there after a longer sea-crossing (e.g. either through wind- drift from near the Shandong Peninsula, or from further south along the Chinese coast).

7.3.4.9 Very Late Migrants Eleven species had First-dates between May 15th and May 21st, all of which had Peak Count Dates between May 25th and June 1st (Table 7.8). None have been reliably recorded in the ROK in the mid-winter period, and only four have been recorded breeding. It is possible that some of these species first arrived during May 11th-15th when there was no survey. Survey between May 8th and 18th in 2009 recorded eight of these species: Sand Martin Riparia riparia (first on May 12th, with four bird-days by May 15th), Dark-sided Flycatcher Muscicapa sibirica (first on May 15th), Arctic Warbler (first on May 10th, with 57 bird-days by May 15th), Lanceolated Warbler Locustella lanceolata (first on May 13th, with five bird-days by May 15th), Black- browed Reed Warbler Acrocephalus bistrigiceps (first on May 10th, with 19 bird-days by May 15th), Gray‘s Grasshopper Warbler Locustella fasciolata (one on May 17th), Tiger Shrike (one on May 17th) and Thick-billed Warbler (one on May 17th). It is also probable that several of these species were present or peaked in number after the survey period. This is based on evidence of ongoing migration in 2010 and later counts of several of these species in earlier years recorded in Moores (2007). As in previous years the Arctic Warbler was absent in early May, but became the most numerous warbler species in late May. Differences in songs indicate that two taxa were present: nominate borealis and Far West Pacific xanthodryas (c. 3 individuals). In 2009, Arctic Warbler (nominate), Sand Martin and Dark-sided Flycatcher were also present on June 23rd (but absent on June 24th and in July, with no evidence of oversummering). The numbers of Locustella warblers were rather lower than recorded 216

during previous survey effort, though the Peak Count Dates were very similar. Previous peak counts of Gray‘s Grasshopper Warbler included >20 on May 31st 2003 and nine on June 1st 2004 (Moores 2007), compared to seven on May 30th in 2010. In 2010, both subspecies of Gray‘s Grasshopper Warbler were tentatively identified. Most were nominate fasciolata (based on the greyish wash to the underparts) and there were two suspected Far West Pacific amnicola (on May 30th and 31st). However, the nominate subspecies shows increasing colour saturation from west to east (Kennerley & Pearson 2010) increasing their resemblance to amnicola. Birds might therefore have been both from the west and the far east of the nominate subspecies‘ breeding range.

Table 7.8 Species only recorded after May 15th. Species Breeds No. First- Peak Last- Peak Bird- ROK? of Date Count Date Count days Dates Date Sand Martin No 8 May 16 May 26 May 29 10 25 Dark-sided Flycatcher No 13 May 16 May 20 Jun 2 17 100 Lesser Cuckoo Yes 10 May 16 May 26,29 Jun 2 3 16 Arctic Warbler No 16 May 16 May 27 Jun 2 197 861 Lanceolated Warbler No 11 May 18 May 25 May 29 8 41 Black-browed Reed Warbler Scarce 14 May 18 May 29 Jun 2 42 308 Gray‘s Grasshopper Warbler No 9 May 18 May 30 Jun 2 7 37 Tiger Shrike Yes 11 May 19 May 29 Jun 2 25 80 Indian Cuckoo Yes 5 May 20 All Dates May 28 1 5 Thick-billed Warbler No 11 May 20 May 30 Jun 2 24 101 Middendorff‘s Grasshopper Warbler No 9 May 21 May 29 Jun 1 3 14 Note: All species are Complete Migrants to the ROK.

7.3.5 Visible Migration There is no detailed published research on counts of visible migration of landbirds in the ROK with the exception of some counts of diurnal raptors. However, large numbers of birds move across and sometimes depart from Socheong (and other YSBR islands) during daylight, complicating the interpretation of count data (Moores 2007). During the survey period, counts over 41 hours on 34 dates from two fixed points (North Point and Northeast Point) recorded a total of 6,615 departing birds of 94 species.

7.3.5.1 Migration at North Point 1) Most Numerous Species Counts from a fixed-point at 59m above sea-level on North Point (37°46.638‘ N, 124°44.465‘ E) were made from close to first light (earliest start 05:45; latest start 06:25) for 35.5 hours and in the afternoon for 4.5 hours, spread across 32 dates 217

between April 2nd and June 1st. This fixed count point allowed an unobstructed view along most of the northern flank of the island, as well as of the shortest sea-crossing to the adjacent Daecheong Island. However, it does not permit views of the very northern tip of the headland. A large number of birds circled the count point, or returned a short time after initiating a sea-crossing. These were recorded as non-departing. Those that passed the count point which were then not seen or heard to return were assumed to have departed. This assumption was supported by high numbers of departing birds being followed by an obvious reduction in number of the same species on North Point on several dates. For example, on April 29th, there were an estimated 500 Grey-backed Thrush on North Point, 301 of which were then seen to depart North Point during 90 minutes of visible migration counts. Subsequently, 144 were counted on North Point itself, including several groups in flight attempting departure. In the remainder of the West and in East, 129 and 78 were then recorded. On the 30th, there were only nine Grey-backed Thrush counted on North Point and 55 in the remainder of the West. A total of 69 waterbirds of 18 species, 449 Passeriformes unidentified to species, and 2,584 departing landbirds of 68 species were recorded. While there was some movement before sunrise, this total includes only birds counted after it was light enough to see clearly the outline of adjacent islands. The total numbers and peak counts of the 20 most numerous identified species are shown in Table 7.9.

Table 7.9 Total numbers, peak counts and main migration dates of the 20 most numerous landbird species counted departing from North Point between April 2nd and June 1st 2010. Total Peak First-Date Date of Peak Last-Date Count Count Grey-backed Thrush 308 301 April 26 April 29 April 30 Dusky Thrush 235 191 April 17 April 17 April 29 Brambling 202 106 April 3 April 24 April 30 Olive-backed Pipit 178 69 April 7 April 30 May 25 Eyebrowed Thrush 105 60 April 29 May 27 May 27 Red-rumped Swallow 104 61 April 25 May 25 May 28 White Wagtail 99 26 April 2 April 30 May 6 Eastern Yellow Wagtail 79 24 April 24 April 30 May 27 Black-faced Bunting 74 27 April 17 May 6 May 15 Arctic Warbler 63 59 May 17 May 27 May 28 Little Bunting 61 22 April 17 May 9 May 28 Yellow-browed Bunting 61 26 April 24 April 29 May 9 Barn Swallow 55 8 April 18 May 25 May 28 Chestnut-flanked White-eye 52 31 May 19 May 24 May 24 Chestnut Bunting 51 17 April 30 May 9 May 28 Yellow-browed Warbler 43 31 April 29 April 29 May 27 Pale Thrush 38 21 April 25 April 26 April 29 Richard‘s Pipit 37 6 April 20 May 27 May 28 Grey Wagtail 34 5 April 5 May 27 May 28 Buff-bellied Pipit 33 9 April 2 April 18 April 26 Note: Species marked in bold are also among the 22 most numerous species during the survey period based on peak counts (section 7.3.7). 218

2) Size of groups at departure The largest number of departures were of single birds (n=490), with 78% of these (n=380) remaining on their own, and the rest assessed as having formed loose or tight duos or larger groups with other species. Of the 130 departures of two birds of the same species, 48 joined with other species; and 16 out of the 48 groups of three birds also joined with other species. The largest departing flocks observed were of 60 (Eyebrowed Thrush on May 27th), 75 (a mixed flock of passerines on April 27th), 80 (Dusky Thrush on April 27th) and 100 (a mixed flock of passerines on April 17th).

3) Direction The direction of flight (at a range of 250-500m from the count point for small and medium-sized birds, and of c. 1km from the count point for larger species such as Grey-faced Buzzard Butastur indicus) was recorded for 2,186 landbirds of 63 species: 1. 461 birds of 22 species flew to the east (with some remaining close to shore). These are presumed to have then undertaken a 20km long sea-crossing to the next island to the east; 2. 576 birds of 37 species flew between east and north, i.e. they headed out over open sea, to undertake a sea-crossing of at least 26km to the DPRK mainland; 3. 959 birds of 46 species flew between north and northwest, i.e. on a line to the east of or across Daecheong and Baekryeong islands. They were presumed to have either stopped over on these islands or more likely to have continued on towards the DPRK mainland (36km to the north). While birds tended to take a northerly line across the sea, a reduction in visibility increased the number of birds taking a line to the northwest and the mountain peak on Daecheong; 4. 150 birds of 25 species flew between northwest and southwest. Such birds could have altered direction once over open sea or might instead have continued towards the Shandong Peninsula; 5. 40 birds of six species appeared to fly towards the southeast. This direction crossed the main hill ridge so that the birds were not seen to depart the island. It is possible that these birds remained on Socheong or reoriented once they reached the island‘s south or east shoreline. For the vast majority of individuals, the final direction taken when departing North Point would lead towards mapped breeding ranges.

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4) Altitude and ascent Based on the known height of the count point and of island hill peaks, the majority of birds were estimated as flying between 50m and 200m above sea level (m.a.s.l) during departure. Most maintained altitude (at least for the first 500m to 1km) though some species (especially Hirundinidae) tended to lose altitude over the sea, especially when ground-level winds were above Beaufort Force 3 or 4. A minority of birds were observed at much greater height (e.g. small passerines on two dates estimated at >2000 m.a.s.l), and at least 18 Passeriform species were seen to ascend to >300 and some individuals to >1000m.a.s.l. These latter heights were estimated based on observations of other passerines flying over points of known distance from the count point. Ascent was achieved in one of two main ways: through upward circling (spiralling with flapping flight), and through flying upwards and forward at a steep angle. Circling was often accompanied by vocalisations (including by Siberian Accentor, most bunting and pipit species), and forward flapping was undertaken more often by species that did not call in flight, like Arctic Warbler. On May 27th, there was much daytime movement of Arctic Warbler across the island. Forty-three out of 59 Arctic Warbler departing North Point ascended from near ground-level, many from vegetation within 10-50m of the count point. Approximately 40 of these ascended at a steep angle, rather closer to the vertical than the horizontal plane. During the same 90-minute period, several flocks of passerines (believed also to include Arctic Warbler based on their similar structure in flight) were seen moving towards the north and northeast, with the highest groups estimated at between 1500 and 2000m.a.s.l. It seems reasonable to assume that the departing warblers were climbing steeply in order to join either these high-flying flocks or flocks that were migrating unseen at even greater altitude. The flight-path of such high-flying birds appeared very direct, and above the usual height of local Peregrine Falcon. NCEP-NCAR reanalysis data for May 27th indicate that vector winds at 1000-mb were moderate and from the south-east, while vector winds at 850- mb were lighter and apparently from the southwest. Plausibly, the energy costs of steep ascent were therefore offset both by the benefits of a smoother tailwind (or reduced side-wind) and a reduced threat of predation.

7.3.5.2 Northeast Point During previous research visits, large numbers of birds (including Phylloscopidae, Turdidae and Muscicapidae) were observed departing from Northeast Point during the 220

morning and afternoon. It is assumed that the majority of birds departing from Socheong to the east do so from this part of the island (and not from North Point). Due to increasingly strict access restrictions, however, counts could only be made opportunistically near Northeast Point on April 23rd, April 25th and April 28th, each time in the late afternoon. On April 23rd and 24th, only one bird was seen to depart towards the east during 30 minutes of observation. On April 28th, heavy rain was followed by fogbanks and heavy overcast conditions. Between 16:35 and 17:05, 3,511 birds of 27 species were counted departing or attempting to depart the island to the northeast and east. This number is considered to be conservative as many birds were believed missed due to poor viewing conditions (including a limited horizon, heavy precipitation and the large numbers of birds that were seen moving into the very low cloud base). Most numerous were Yellow-browed Warbler (c. 2500), Olive-backed Pipit (c. 250), Brambling (83) and Little Bunting (81). The most intense departures coincided with the rain restarting and a brief ten-minute interval when visibility near sea-level increased from <5km to >30km, so that the DPRK coastline became visible. Departures then decreased in intensity again as visibility declined, the wind increased, temperatures fell, and the rain turned to snow. At this time, large numbers of birds (including several hundred Yellow-browed Warbler) started to drop to the ground to start feeding while others tried to roost in roadside vegetation. The numbers of some species near and at Northeast Point between 15:00 and 17:30 (i.e. shortly before and during this movement) greatly exceeded the numbers of the same species counted the previous day, earlier the same afternoon on the island, and the following day during a Whole Island Count. The movement also produced the First-date of White-throated Needletail Hirundapus caudacutus and the only Pied Harrier Circus melanoleucos of the survey period on the island. Thus most of the birds were assessed as moving in daytime across the Yellow Sea, within a low pressure system. In short, the research on visible migration found no evidence of a strict division between nocturnal and diurnal migration in e.g. Phylloscopidae, Turdidae and Muscicapidae. Acrocephalidae and Megaluridae were recorded arriving during the day in inclement weather, but were not confirmed during departure (perhaps due to the difficulty of identification once in sustained flight). On several dates, daytime departures of Passeriformes involved large numbers of individuals, including birds assumed to have arrived on the island the same day. For at least Yellow-browed Warbler, the number of individuals seen departing exceeded numbers recorded during 221

Whole Island Counts. Counts of visible migration therefore appear to be essential if species‘ abundance is to be estimated, and a site‘s importance is to be properly assessed. Most visible migrants during northward migration departed towards the north and east. This is consistent with the prediction that the majority of regularly occurring species recorded on Socheong breed on the Northeast Asian Mainland.

7.3.6 Most Numerous Species during Whole Island Counts There was a marked shift in species‘ composition and relative abundance during the survey period (Table 7.10).

Table 7.10 The three most numerous species on each of the 13 Whole Island Counts Date Number of Total Number of Three most numerous Species Number species Individuals Per Count Cycle April 3 52 1,000 Yellow-throated Bunting 130 Naumann‘s Thrush 117 Red-flanked Bluetail 100 April 7 47 810 Brambling 164 Red-flanked Bluetail 137 Grey-faced Buzzard 71 April 16 54 780 Red-flanked Bluetail 119 Black-faced Bunting 85 Brambling 65 April 20 79 1,052 Siberian Stonechat 100 Red-flanked Bluetail 85 Dusky Thrush 84 April 23 72 1,137 Brambling 285 Olive-backed Pipit 102 Red-flanked Bluetail 83 April 29 98 3,410 Grey-backed Thrush 652 Asian Stubtail 464 Black-faced Bunting 283 May 7 91 1,208 Yellow-browed Warbler 153 Black-faced Bunting 131 Olive-backed Pipit 74 May 10 89 882 Yellow-browed Warbler 86 Black-faced Bunting 78 Olive-backed Pipit 57 May 16 83 846 Chestnut Bunting 79 Yellow-browed Warbler 61 Black-faced Bunting 46 May 20 93 1,590 Chestnut-flanked White-eye 260 Yellow-browed Warbler 114 Chestnut Bunting 112 May 25 95 1,524 Chestnut-flanked White-eye 300 Red-rumped Swallow 165 Barn Swallow 120 May 29 83 930 Arctic Warbler 131 Pale-legged Leaf Warbler 54 Asian Brown Flycatcher 45 June 1 69 524 Chestnut-flanked White-eye 54 Arctic Warbler 49 Black-browed Warbler 39 222

The three most numerous species recorded during each of the 13 Whole Island Counts differed between surveys but accounted for a mean of 32% (minimum 22%, maximum 46%) of the total numbers of birds recorded that day. Throughout, there was a change in the most numerous species from Early Migrants that often over-winter in the ROK, to Mid-Season species (many of which breed in the ROK), to Late and Very Late Migrants, which neither spend the boreal winter nor in most cases breed on the Korean Peninsula. Diversity among the most numerous species was rather limited, however, and families containing one or more of the three most numerous species during the 13 Whole Island counts included Emberizidae seven times, Phylloscopidae six times, Muscicapidae five times, and Turdidae three times.

7.3.7 Most Numerous Species by Peak Count There were 126 landbird species with peak counts of <10, and 22 species with peak counts of >100 individuals. These 22 species include 14 of the most numerous landbird species recorded during visible migration at North Point (Table 7.9 above). In order of highest to lowest (with peak count numbers in parentheses) these were: Yellow-browed Warbler (2,586), Eyebrowed Thrush (785), Chestnut Bunting (750), Grey-backed Thrush (652), Olive-backed Pipit (609), Asian Stubtail (464), Brambling (402), Little Bunting (370), Chestnut-flanked White-eye (335), Red-rumped Swallow (291), Black- faced Bunting (283), Red-flanked Bluetail (247), Dusky Thrush (233), Fork-tailed Swift Apus pacificus (210), Arctic Warbler (197), Yellow-browed Bunting Emberiza chrysophrys (175), Tristram‘s Bunting Emberiza tristrami (159), Siberian Stonechat (135), Yellow-throated Bunting (130), Barn Swallow (122), Naumann‘s Thrush (117) and Grey-faced Buzzard Butastur indicus (114). These 22 species comprised 78% of the sum of peak counts of all landbird species, and 66% of the 45,590 actual bird-days of identified species during counts. Only seven of the 22 are regular breeders in the ROK (Grey-backed Thrush, Asian Stubtail, Red-rumped Swallow, Fork-tailed Swift, Siberian Stonechat, Yellow-throated Bunting and Barn Swallow). The remainder is comprised of species which are both widespread passage migrants and winter visitors (Brambling, Dusky Thrush and Naumann‘s Thrush) or which are primarily passage migrants. None of the 22 are Far West Pacific Taxa and seven (Yellow-browed Warbler, Chestnut Bunting, Grey-backed Thrush, Chestnut-flanked White-eye, Yellow-browed Bunting, Tristram‘s Bunting and Naumann‘s Thrush) are rare in Japan (Brazil 1991). Based on maps in Brazil (2009), at 223

least 19 out of the 22 breed in either Ussuriland and/or the Khabarovsk Region, with four largely confined globally as breeding species to the Northeast Asian Mainland, between the Korean Peninsula and the Sea of Okhotsk: Grey-backed Thrush, Chestnut- flanked White-eye, Tristram‘s Bunting, and Yellow-throated Bunting. While banding data and other research approaches have not yet proven the destination of migrants staging on Socheong, the relative abundance and mapped breeding ranges of these 22 species suggests that many will be migrating towards the Northeast Asian Mainland to breed.

7.3.8 Whole Island Estimates of the Ten Most Numerous Landbird Species The development of Whole Island Estimates for species through an entire migration season is complicated by a range of factors, including incomplete coverage, the lack of knowledge on turnover rates, and the large fluctuations caused by the passage of weather systems that might (or might not) result in large numbers of grounded migrants or migrants in sustained flight. The variation in the pattern of peaks and troughs in number means that existing models to estimate turnover, including those developed for shorebirds by Thompson (1993), are inappropriate. Instead, Whole Island Estimates were generated for the ten species with the highest peak counts through a series of steps that aimed to reduce potential bias by interpolating counts from a range of count areas: 1. Whole Island Counts were used unaltered for the 13 dates; 2. For days when survey was in either the West or East, the mean of the ratio between West and East during all Whole Island Counts throughout the survey period was taken, and used for the area that was not surveyed (in several species, this ratio tended to be similar during Whole Island Counts); 3. For the three days with counts only in the Central part of the island, the number of birds recorded was multiplied by three; 4. For days with counts on North Point but not in the West or East, numbers in the West and East were calculated from the ratio of counts of grounded individuals on North Point to West and East on all other relevant dates though the study period; 5. For the two dates without adequate survey effort due to heavy rain (May 5th and May 23rd), the mean of the day before and the day after were used 224

(based on the rapid through-movement of birds associated with weather systems, these counts were likely to be conservative); 6. For the gap between April 9th and 11th, the mean of the estimates for the preceding three days was used for the first day; the mean of the estimates for the following three days was used for the third day; and the median of the April 9th and 11th estimate was used for April 10th. 7. For the four-day gap between May 11th and 14th, the mean of the estimates of the preceding four days were used for May 11th and 12th; and the mean of the estimates of the following four days was used for May 13th and 14th; 8. And finally, the incremental differences between each estimated peak (i.e the difference between the estimated peaks and troughs in abundance) throughout the survey period were then summed.

Estimated Bird-days were calculated by taking the mean of the two Whole Island Counts of a species each ten (or eleven) day period and using this resultant number as the estimate for all days within that period; and then summing each of the ten day period estimates together. Both estimates are listed in Table 7.11. As turnover is treated conservatively through both methods of calculation, and as some large departures might have occurred unrecorded, it is likely that both underestimate the numbers of each species that would have been recorded had coverage been complete. Nonetheless, the two methods provide estimates that can be used for comparison both between years and between islands.

Table 7.11 Whole Island Estimates and Estimated Bird-days of the ten species with the highest peak counts on Socheong (by peak count) during April and May 2010. Species Whole Island Estimated Estimate Bird-days Yellow-browed Warbler 3,626 5,295 Eyebrowed Thrush 2,148 3,747 Chestnut Bunting 1,463 2,628 Grey-backed Thrush 1,246 2,476 Olive-backed Pipit 1,875 4,591 Asian Stubtail 649 1,191 Brambling 1,424 4,203 Little Bunting 945 1,939 Chestnut-flanked White-eye 591 2,670 Red-rumped Swallow 657 1,444 Total 14,624 30,184

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7.3.9 Comparisons between Socheong and Hong and Heuksan In making comparisons between islands, differences in survey effort, method (see Sections 7.1.1 and 7.2.1) and observer experience need to be considered. Based on personal observations, the largest discrepancies between counts are likely to be in the identification of Passeriformes in sustained flight (with a higher rate of identification on Socheong by the present survey and a lower rate of identification on Hong and Heuksan).

7.3.9.1 Species richness, abundance and migration intensity As predicted, species‘ richness and the number of birds (both grounded and in diurnal movements) on Socheong were much higher than recorded on the adjacent Hong and Heuksan. In April and May 2010, 167 landbird species of 12 orders were recorded on Socheong. This compares with 117 species of landbird from 11 orders recorded on Hong and 99 landbird species from 10 orders recorded on Heuksan (though with 14 fewer days of coverage on the latter island) (KNP 2010). Based on the mean of the two Whole Island Counts for each of the 10 or 11 day periods there were almost 77,000 estimated landbird bird-days on Socheong compared with 10,327 landbird bird-days on Hong and 8,723 on Heuksan during the same period. If the number of bird-days on Heuksan during the two-week gap in survey was equivalent to one-third of the six weeks that were surveyed, this would produce an estimate of c. 11,000 landbird bird-days for April and May on Heuksan and of <23,000 landbird bird-days on Hong and Heuksan combined. The area of landbird habitat that was surveyed on Socheong (<200ha) was approximately three times the combined area of that surveyed on Hong and Heuksan (c. 65 ha in total). There were approximately 389 landbird bird-days/ha recorded on Socheong and 354 landbird bird-days/ha recorded on the two other islands combined. Hence, the density of birds/ha was similar between the islands. However, survey effort on Hong and Heuksan was conducted mostly in open areas and in wetlands where birds are more concentrated and easier to see than in areas of closed forest, which is the main habitat on all three islands. On Gageo Island, survey by the author in late April 2009 found that the density of landbirds was 3-10 times higher in open areas with arable plots and forest-edge (similar to the habitats surveyed on Hong and Heuksan) than in more heavily vegetated forest-edge and closed canopy forest (most of the habitat on Socheong). 226

As predicted, there was a substantial difference in the recorded intensity of migration between Socheong and Hong. Throughout April and May, there were on average seven times more birds estimated per 10 or 11 day period recorded on Socheong than on Hong (Figure 7.10).

30000

20000

Bird-days 10000

SOCHEONG 0 HONG 0 1 2 3 4 5 6 7 Decades after 1st April

Figure 7.10 Comparison of estimated landbird bird-days on Socheong and actual landbird bird-days on Hong Island during northward migration in 10 or 11 day periods in April and May.

This ratio was not stable throughout the migration period. The difference between these two islands was lowest in early and mid-April (with a ratio of 5 to1) and greatest in mid- and late-May (reaching a ratio of 12 to1). Migration was thus most intense early during northward migration on Hong, falling between early- and mid-May. On Socheong, the intensity of migration peaked in late April, but was maintained at a high-level throughout May. This difference in migration intensity is also apparent at the species-level. It is not possible to compare the migration intensity on Heuksan with these other islands because of the missing dates of survey (dates unknown) in May.

7.3.9.2 Far West Pacific Taxa Despite the greater species richness and the larger numbers of birds recorded, only four Far West Pacific taxa were recorded on Socheong (with bird-days in parentheses): Grey Thrush (19), Brown-headed Thrush (36), Japanese Robin (3) and Yellow Bunting (1). All seven Far West Pacific taxa were recorded on Hong, and five of the seven were recorded on Heuksan. Substantial differences between islands were evident in the comparative abundance of some of these Far West Pacific taxa within families. On Hong, Brown-headed Thrush was the second commonest Turdus thrush (with 113 bird- days in Late April and 164 bird-days in total, accounting for 18% all of Turdidae). 227

Grey Thrush bird-days represented 2% of all Turdus bird-days. Although the differences were less marked on Heuksan, the 16 Brown-headed Thrush bird-days represented 2% of all Turdus bird-days and the 28 Grey Thrush bird-days represented 3%. On Socheong, Brown-headed Thrush and Grey Thrush accounted for only 0.7% and 0.4% of Turdus bird-days respectively during the same period. These differences are consistent with concentrated migration across Northern and Southern Crossings and not with broad front migration.

7.3.9.3 Most numerous species On Hong and Heuksan combined, there was a total of 24 landbird species with >100 bird-days on either island in April and May. There was overlap between Hong and Heuksan in 15 of the 24 most numerous species, including in all ten of the most recorded species on Hong: Black-faced Bunting, Brown-eared Bulbul, Red-flanked Bluetail, Barn Swallow, Brambling, Olive-backed Pipit, Yellow-throated Bunting, Pale Thrush, Japanese Bush Warbler and Little Bunting. Only three of these species (Olive- backed Pipit, Brambling and Little Bunting) were among the ten most numerous species on Socheong (Table 7.12).

Table 7.12 Comparison of Estimated Bird-days of ten selected species on Socheong and actual bird-days on Hong Island, April-May 2010. Early Mid- Late Early Mid- Late Total April April April May May May Yellow-browed Socheong 0 6 3,002 869 922 497 5,296 Warbler Hong 0 0 31 79 37 1 148 Olive-backed Pipit Socheong 54 171 1,790 1,198 1,136 233 4,582 Hong 17 103 202 133 39 1 495 Brambling Socheong 1,513 855 1,506 238 23 0 4,135 Hong 227 148 151 66 15 0 607 Eyebrowed Thrush Socheong 0 0 55 1,142 2,091 453 3,741 Hong 0 0 2 9 46 2 59 Chestnut Bunting Socheong 0 0 2 811 1,477 328 2,618 Hong 0 0 2 7 7 0 16 Chestnut-flanked Socheong 0 0 0 65 501 1,925 2,491 White-eye Hong 0 0 0 0 0 0 0 Grey-backed Thrush Socheong 2 440 1,312 555 134 21 2,464 Hong 1 8 11 8 5 0 33 Little Bunting Socheong 8 30 984 565 253 98 1,938 Hong 11 2 93 98 46 0 250 Red-rumped Socheong 0 1 126 202 143 967 1,439 Swallow Hong 0 0 7 19 0 46 72 Asian Stubtail Socheong 0 165 868 153 3 2 1,191 Hong 0 10 38 15 1 0 64 Total Socheong 1,577 1,622 9,645 5,798 6,683 4,720 29,905 Hong 256 271 537 434 196 50 1,744

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In contrast, three out of the ten most numerous species recorded on Socheong (Eyebrowed Thrush, Chestnut Bunting and Chestnut-flanked White-eye) were not among the 24 most numerous species on either Hong or Heuksan. Two of these (Chestnut Bunting and Chestnut-flanked White-eye) breed only on the Northeast Asian Mainland, and Chestnut Bunting is an easy-to-identify species often found in open habitats. The difference in numbers between islands of this species is thus the result of a difference in migration strategy rather than in survey effort or observer experience between islands.

7.4 DISCUSSION 7.4.1 Channelled Northward Migration A channelled rather than a broad front migration strategy across the YSBR has several important implications. Certain sites (islands, headlands and areas of coast) will have disproportionate importance for migrant landbirds compared with other sites, and research in only one small part of the YSBR will be insufficient to describe landbird migration through the YSBR as a whole. Moreover, differences in numbers of species between islands (if identified by constant survey effort and properly interpreted) could over time be used to identify differences in underlying population trends between the Northeast Asian Mainland and the Far West Pacific Region. Although more research is required to test our hypotheses further, the results demonstrate that there were major differences in the abundance and species composition of migrant landbirds on Socheong and the two southern islands of Hong and Heuksan during northward migration in 2010. Despite substantial day-to-day and annual variations between the numbers of some species, comparison with datasets in other years since 2003 also suggests that there are regular underlying differences between these same islands in the number and relative abundance of groups of species with different breeding areas (Moores 2007, KNP 2005-2010). Moreover, many of these differences are to some extent predictable, and are shared with other islands at similar latitudes. Data from Gageo to the south and Mungap (37° 10′ N, 126° 06′ E) to the north of the YSBR are much less complete. However, during northward migration on Gageo there are, as on Hong and Heuksan, proportionately larger numbers of Far West Pacific taxa than on islands further north, and fewer records of Chestnut-flanked White-eye. Similarly, on Mungap large numbers of Chestnut-flanked White-eye but few Far West Pacific taxa have been recorded (unpublished data, T. Edelsten in lit. 229

2011). These differences are consistent with the channelling of migrant landbirds by geographical features at the time of departure from the Chinese coast. They are inconsistent with homogenous broad front migration across the YSBR.

7.4.2 Channelled Southward Migration During southward migration there is also evidence of channelling, as first suggested by Gore & Won (1971). Counts made of birds departing from North Point on Socheong during southward migration on 16 dates in 2009 recorded a total of 8,458 birds. Only c. 5% (418) flew eastward (on any heading between north and south); 73% (6,188) flew between west and northwest (over open sea or initially towards the western end of Daecheong); and 22% (1,852) flew to the southwest. If birds continued on this bearing between northwest and southwest as taken at departure by 95% of birds, this would take them towards the Shandong Peninsula. There are less data for southward than northward migration. However, it is already evident that not all species depend on the same islands for stopover equally in both seasons. Some of the more numerous species recorded on Socheong during northward migration (including Eyebrowed Thrush) have not yet been recorded in comparable numbers during southward migration on any island. This could be because they are able to fly the comparatively short distance from the Korean mainland over YSBR islands without stopping, and/or because they take a different route. The numbers of Grey-faced Buzzard recorded on Socheong appear to be more or less the same during both northward and southward migration (unpublished data). However, much larger numbers of Grey-faced Buzzard have been recorded on Gageo during southward than northward migration, concentrated each year into a two-week period. A total of 7,518 Grey-faced Buzzard were counted arriving (from the south and east) and departing Gageo (to the west) between October 3rd and 11th 2009. On Socheong only 81 were counted between October 4th and 14th 2004 (unpublished data). Although recorded in much smaller numbers than on Gageo, Grey-faced Buzzard were also recorded on Hong and Heuksan in higher numbers during southward than northward migration in both 2009 and 2010 (KNP 2009-2010). These differences in migration strategy are likely to be result from seasonal differences in regional weather systems, as also surmised by Higuchi (2010). There is a prevalent westerly airflow, stronger northward in the YSBR, in April and May. This favours migration from the Shandong Peninsula towards the Korean Peninsula. In 230

September and October, however, large and stable high pressure systems regularly form over Far East Russia. These result in clear skies and a moderate to strong north- easterly airflow over the Korean Peninsula. Such systems provide energy-saving tail- winds for Grey-faced Buzzard and other species migrating out from breeding areas in Ussuriland and Amurland, down the Korean Peninsula and on towards the Chinese coast, and also for species from Japan migrating across the East China Sea (including Oriental Honey Buzzard: Higuchi 2010). In some species, however, the southward migration strategy remains enigmatic. Between 2003 and 2005, there were more records of Asian House Martin Delichon dasypus on Socheong during southward than northward migration. While most records involved small numbers, a single flock of 3,000 (more than seventy times larger than any previous count of the species nationwide) was recorded during a rain shower (Moores 2007). It is probable that these birds would not have been seen if the weather had remained dry (F. Crystal in lit. 2005). However, it is not known whether the strong easterly airflow at that time resulted in an exceptional movement of the species near Socheong, or if the species instead typically migrates across this part of the Yellow Sea undetected and in large numbers (either at high altitude or only a few kilometres to the north of the island). Nonetheless, the southward migration strategies of species such as Grey-faced Buzzard and Asian House Martin also appear to be consistent with the channelling of migrant landbirds to the north and the south of the YSBR. They too highlight the need to interpret count data in relation to the large-scale effects of geography, and also weather. It is clear much more research is required. There has only been a decade of research on migratory landbirds on YSBR islands and a single rain shower on a single island still has the potential to alter perceptions of a species‘ national status and population trend.

7.4.3 Regional Migration Strategies In other regions, decades of research have shown that population-specific migration routes are most evident in species with a migratory divide separating adjacent populations with different migratory directions (Bairlein 2003). While such a divide across the Yellow Sea remains hypothetical, it is already well described for the Mediterranean Sea. The Mediterranean Sea is an ecological barrier for birds migrating north-south between Europe and Africa, with a length of sea-crossing ranging from <20km to 660km at widest. These distances compare with a minimum sea-crossing of 231

180km from the Shandong Peninsula to Socheong, of 450km from the Chinese coast to Hong, and of almost 700km from Shanghai to the Goto Islands off western Kyushu (Japan). Birds crossing the Mediterranean Sea can reduce the length of unbroken sea- crossings by migrating through Italy, or by using large islands (including Sicily and Cyprus) for stopover. Nonetheless, the Mediterranean Sea has been shown by radar studies to contribute to ―guided broad-front migration‖ across much of southern Europe (Bruderer 2001). Many species do not migrate north-south across the sea. Instead, migratory routes toward southwest and southeast prevail (Erni et al. 2005). Passerines that migrate between Portugal and Morocco tend to migrate towards the southwest, thus avoiding both the widest parts of the Mediterranean and a direct crossing of the Sahara Desert (Finlayson 1998). It has even been suggested that today‘s migratory routes around the Mediterranean reflect the ancient route of colonisation of their breeding ranges, with several ―sister‖ taxa evolving separately to the west and the east of the Mediterranean (Bruderer & Liechti 1999). In the absence of evidence to the contrary, it seems reasonable to assume that the Yellow Sea and the East China Sea are also influential on present-day migration strategies and perhaps the distribution of some bird species in Far East Asia. The ecological barrier formed by the seas around Japan has apparently contributed to the divergent evolution of several sedentary bird species, and to higher levels of avian endemism in Japan than in the ROK. Several Japan-breeding endemics and near- endemics, both sedentary and migratory, have close ecological counterparts on the Asian mainland (e.g. Narcissus Ficedula narcissina and Yellow-rumped Flycatchers Ficedula zanthopygia, Sakhalin and Pale-legged Leaf Warblers, xanthodryas and borealis Arctic Warblers; and perhaps even Brown-headed, Pale and Eyebrowed Thrushes). Several migratory Far West Pacific taxa and their East Asian Mainland counterparts are either known to or are suspected of overlapping in range during the boreal winter (Brazil 2009). In the YSBR, many of the same taxa are now known to share stopover sites, though in different proportions to the north and to the south. Soon after stopover during northward migration these same taxa then arrive separately in their geographically discrete breeding grounds. These different breeding areas must be reached by taking different migration routes while crossing the Yellow Sea and East

China Sea, and when departing from YSBR islands used for staging. In consideration of each migrant bird‘s need to balance the demands of energy, time and safety, it seems reasonable to assume that populations of monotypic 232

migratory species which have extensive breeding ranges (e.g. Eyebrowed Thrush, Dusky Thrush and Little Bunting) will also have developed different migratory routes and strategies to reach their western and their eastern breeding areas. It would not be energy-efficient for a bird over-wintering in southern China to migrate north through mainland Asia and then to turn east to cross the much wider Sea of Okhostk in order to reach Kamchatka. Nor would it be energy-efficient for an individual of the same species to migrate on a southwest-northeast axis through Japan and Kamchatka if its intended migration was to Amurland. It can therefore be assumed that many of the birds recorded on Hong and Heuksan and other islands in the Southern Crossing (whether Far West Pacific taxa or not), are migrating to and from breeding areas different from those used by many of the birds recorded on Socheong. Banding recoveries of several species have confirmed the connection between Hong and Heuksan and Japan (KNP 2007). Differences in migration timing between islands also suggest that different populations migrating to different breeding areas are involved.

7.4.4 Use of the Research The results suggest that research on Socheong is likely to provide valuable insights on species and populations that are breeding in the DPRK and on the Northeast Asian Mainland. Hong and Heuksan are better placed to provide insights on migration strategies and underlying population trends of species that breed in the southern provinces of the ROK and in the Far West Pacific Region. Differences in population trends shown by the same species on Socheong versus Hong and Heuksan (if consistent over time and correctly interpreted) might therefore be helpful in the identification of differences of population trends in the same species in different regions. In order to improve the resolution of data, research effort needs to increase greatly, to include Intermediate Islands and analysis of weather systems (see Chapter 8). Consistency between different areas in survey methods, and data analysis and presentation also need to be improved. In other regions, much effort has been made to standardise count methodologies and to ensure daily coverage of many geographically separated migrant hotspots during whole migration seasons. Some bird observatories in the United Kingdom (UK) have collected daily observational data on birds and weather through both northward and southward migration periods, supported by regular 233

banding programs, over several decades. Even so, there is still a general reluctance to depend on the data that have been generated by such research to try to identify underlying population trends. This is in part because of the large numbers of birds that are shown by radar-studies to be passing overhead (Bruderer 1997), and the poor correlation found by some research between daily changes in the number of grounded migrants and the number of overhead migrants detected by radar (Fischer et al. 2012). In addition, weather events affect both the numbers of migrants undertaking migration and also the number and visibility of ―grounded‖ birds, while other sources of bias can also make the characterisation of bird migration phenology challenging (Knudsen et al. 2007). Furthermore, there are also already large-scale, long-term and well-coordinated monitoring programs of breeding birds both in the UK and in adjacent regions (BirdLife International 2004, Vorisek et al. 2008). This simultaneous gathering of data through a range of well-coordinated research methods, however, enables some assessment of the potential value of ground-based observations at migration hotspots. Preliminary analysis by the British Bird Observatory Council of visual migration data over a decade on eight species (selected because of their strong trend shown by breeding studies) showed a strong correlation between population trends in observations from bird observatories and in trends revealed by the national Common Bird Census and Constant Effort Sites during the same period. In a second study, longer-term datasets on four nationally-scarce and declining species also matched well for two species; were too data-poor for one species; and showed an unexpected pattern in the fourth that nonetheless could be explained by differences in trend shown by populations breeding in different areas (British Bird Observatory Council, online 2011). In the ROK, there are still no large-scale, long-term breeding bird research programs, and as recently as 2010, no migration hotspot for landbirds was surveyed daily. At the same time, the nation is formally committed through the Aichi Biodiversity Targets (CBD 2010) and other conservation agreements to improving the knowledge base on species‘ populations and trends, and to reducing the rate of biodiversity loss within the present decade. There is therefore an urgent need to increase data collection (at migrant hotspots and in breeding areas), to refine survey methodologies and to improve understanding of large-scale effects on migration, including the importance of geography. In the near-term, sites that are known to hold large concentrations of migrant birds (including Socheong, Eocheong, Gageo, Hong and Heuksan) need to be managed as 234

priority areas for conservation and research. On Hong, research has already included use by migrant birds of water and fruiting plants (Choi 2007) and on-island mortality caused by cats and collision with man-made structures (Bing 2007). Such research needs to be expanded and solutions applied on these and other islands. On a larger- scale, concentration of migrants necessitates a reassessment of the suitability of some areas for offshore wind-plants, as presently proposed for several areas of the YSBR. If a wind-farm was to be constructed near Socheong the combination of channelled migration across the island and the large numbers of birds migrating in inclement weather could potentially put many tens of thousands of landbirds each year at increased risk. In the spirit of the United Nation‘s Precautionary Principle, development proposals that might result in declines in migratory birds need immediate modification or cancellation.

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CHAPTER 8

LANDBIRD MIGRATION THROUGH AN ―INTERMEDIATE‖ ISLAND AND THE INFLUENCE OF WEATHER

ABSTRACT Most landbirds migrating across the YSBR intend migration along the Northern and Southern Crossings (Chapter 7). However, large numbers of birds sometimes occur on Eocheong and other islands that lie between these crossings (―Intermediate Islands‖). We hypothesise that most large arrivals of landbirds on Intermediate Islands are caused by wind-drift from the Northern and Southern Crossings, and predict that species composition and migration timing will therefore be intermediate on Eocheong compared to islands in the Northern and Southern Crossings. Results from survey work during northward migration in 2003 and 2011 support our hypotheses. Most large arrivals of birds in both years on Eocheong were associated with two main weather systems. Inclement Weather Arrivals tended to be the result of rain-bearing low pressure systems moving across the southern part of the Yellow Sea, which were followed by northwesterly winds. Fair Weather Arrivals tended to be the result of low pressure systems moving to the north of the Yellow Sea, which were then followed by a strong westerly airflow. Large weather-related arrivals of birds tended to share several additional elements, including high species richness and rapid departure of some species. Species composition within large arrivals was influenced by the timing and track taken by weather systems. These differences resulted in large variations in count data (both day to day and between years), and therefore have the potential to distort the interpretation of count data gathered by ground-based observers. Despite the influence of differences in weather systems between years, several species were recorded in greatly reduced numbers in 2011 compared with 2003 – both within and outside of large arrivals. Declines in such species, several of which breed in the forests of the Northeast Asian Mainland, are therefore suspected.

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8.1 BACKGROUND AND AIMS 8.1.1 Introduction The distribution of transitory migrant landbirds on islands within the Northern and Southern Crossings (Chapter 7) can be explained by their need to balance the demands of energy, time and safety (Alerstam and Lindström 1990). However, the large numbers of birds that are recorded during northward migration on an island like Eocheong (36°07′ N, 125°58′ E) which lies between these two crossings do not appear to fit this explanation well. To reach Eocheong from near Shanghai, Haizhou Bay or the eastern Shandong Peninsula either requires landbirds to undertake a longer flight over open sea than required to reach parts of the Korean mainland itself, or for some migration to occur towards the southeast (rather than the east or northeast). Costs of stopover are also likely to be high. YSBR islands typically experience temperatures several degrees lower than the mainland at similar latitudes in April and May (Chapter 1, Table 1.3.5) and thus experience delayed plant growth and reduced insect abundance. YSBR islands also often support a high density of raptors.

Fig. 8.1 Location of Eocheong (in red), other main YSBR islands (in orange), and distance from proposed main areas on the Chinese coast suspected to concentrate landbird migrants during northward migration. 237

In Chapter 7, we made two inter-related predictions concerning northward migration through Intermediate Islands that lie outside and between the Northern and the Southern Crossings. The first is that species richness, composition and migration timing will be intermediate between them and islands in the Northern and Southern Crossings. Second, because Intermediate Islands are outside of the main corridors of migration most arrivals of migrants will be influenced by wind-drift from either the Southern or Northern Crossing. The influence of weather systems on the migration of most landbird species across the Yellow Sea has been poorly addressed by research. However, in other regions it has been shown that rain influences departure decisions (Erni et al. 2002), and flight altitude (Bruderer 2001). Wind also has important implications for departure decisions (Åkesson et al. 2000, 2002), flight-orientation and flight energetics (Shamoun-Baranes et al. 2007), and even for the viability of migration routes (Erni et al. 2005). In Scandinavia, most night-migrating passerines flying overland were recorded in light or moderate winds, and not during strong winds, perhaps to avoid the risks of extensive drift by wind from their intended direction (Karlsson et al. 2011). Other radar studies confirm that migrant birds flying below 4000m adjust flight levels to prevailing winds; that headwinds help make finches more visible to observers on the ground, as they do not stop migration under adverse conditions (Bruderer 1997); and that birds compensate for weak lateral winds but drift increasingly with stronger winds (Bruderer 2001). Strong winds even have the capacity to drift landbirds huge distances off course, including out from the Asian landmass far into the Pacific Ocean (Hameed et al. 2009). Both rain and wind are therefore likely to influence birds migrating across the Yellow Sea, and also the ability of researchers to observe them. Wind and rain therefore have the potential either to distort or to reveal underlying migration strategies and population trends. Survey since 2000 suggests that wind and rain often result in arrivals on offshore islands in the YSBR (Moores 2007, unpublished data). On Socheong, in the Northern Crossing, reduced visibility by fog and heavy overcast can also result in substantial arrivals, probably because of the greater numbers of birds involved and the relative narrowness of the migration corridor. Many such arrivals on Socheong are likely due to the loss of altitude of birds that otherwise would migrate too high to be observed.

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Eocheong, by contrast, is an Intermediate Island and we therefore predict that on Eocheong: 1. Species richness, composition and migration timing will be intermediate between Socheong and Hong and Heuksan; 2. Much of the daily and annual variation in numbers of species and individuals will be attributable to variations in weather conditions, especially wind and rain. ―Large arrivals‖ (from hereon defined as days on which 800 or more birds are recorded) will usually take place on days with rain or on days following rain, and/or on days with strong winds. There will be only small arrivals of landbirds on most other dates; 3. Large arrivals will not take place on days with very poor visibility; 4. More Far West Pacific taxa (as defined in Chapter 7, Section 7.1.2) will be recorded when winds are between southeast and southwest, as they will be drifted northward from the Southern Crossing. Conversely, higher numbers of species intending migration to the Northeast Asian Mainland (including Chestnut-flanked White-eye and Eyebrowed Thrush) will be recorded when winds are between west and north, as they will be drifted southeastwards to Eocheong. Evidence to test these predictions was gathered through counts of migrant birds on Eocheong from Mid-April to Mid-May in 2003 and 2011. Data from this fieldwork were compared to published and unpublished count data collected during northward migration from the northern island of Socheong in 2010 (Chapter 7), and the southern islands of Gageo, Hong and Heuksan (unpublished data; KNP 2005-2010, Park Jong- Gil in lit. 2010).

8.1.2 Eocheong Island Eocheong is the westernmost of a chain of islands lying c. 200km southeast of Socheong and c. 235 km northeast of Hong and Heuksan, 11km southwest of the Weiyeon island group (36°13′ N, 126°05′ E), and 45km west of the mainland. It is the potential first landfall for birds migrating from a wide arc of sea from the west towards the central ROK. The island is approximately 230ha in area, and shaped like an upper case ―A‖ (widest in the south), with its outline defined by a forested hill ridge that rises to 162m in the west, and 100m in the east. The open space in the south is occupied by a bay. The main village lies close to sea-level in the centre of the ―A‖, which also 239

holds the most diverse habitats on the island, including areas of open ground, small arable plots, a freshwater reservoir and stream, and a beach with intertidal area (approximately 10ha at lowest spring tide). There is also an area of open ground with a small stream near a lighthouse in the northwest of the island, reached by a road running north from the reservoir. Most of the remainder of the island is covered in planted coniferous woodland with broadleaved evergreen undergrowth.

8.1.3 Previous Research The first counts of migrant birds on Eocheong were made on 19 dates between April 18th and May 22nd 2002 by the author, joined by other observers on six dates. These counts found 181 species, eight species of which are of global conservation concern. Higher counts of several landbird species than had been previously recorded either in the YSBR or in the ROK as a whole were also made. Although this initial survey was limited in time and scope, a strong relationship was suggested between the largest daily increases in the number of birds and two main types of weather system, one anti-cyclonic (―Fair Weather‖) and one cyclonic (―Inclement Weather‖). A similar pattern had already been noted during research on Gageo in 2000 and 2001 (Moores & Kim 2001). The ―Fair Weather Arrivals‖ observed in 2002 on Eocheong were small to medium-sized in scale and short in length. They involved, on several dates with locally clear conditions, afternoon arrivals of up to several hundred birds, especially Phylloscopidae and Muscicapidae. These included more than 150 Eastern Crowned Warbler Phylloscopus coronatus on April 22nd. ―Inclement Weather Arrivals‖ instead involved much larger arrivals that coincided with the passage of low pressure systems. Several mixed flocks (especially from families Turdidae, Motacillidae and Emberizidae) occasionally of more than 100 individuals, arrived from the southwest, often coincident with or soon after the first rainfall. The largest such arrival took place between April 28th and 30th, with 5,600 birds of 122 species recorded on the latter date. This included a conservative estimate of 3,000 Olive-backed Pipit and 300 Ashy Minivet Pericrocotus divaricatus. These counts were three and seven times higher respectively than the highest counts nationwide listed for either species by Park (2002). In 2002, much higher numbers of birds were recorded in or near open areas and only small numbers of birds were recorded in more heavily-wooded areas in the southeast of the island or from tracks off the main road north of the lighthouse. Survey 240

between 2003 and the present was therefore concentrated in two areas: ―the main survey area‖ (consisting of all accessible areas to the south and west of the reservoir, including the bay and inshore waters off the south of the island), and ―the supplementary count area‖ (all wooded areas along the road to the lighthouse, the lighthouse environs, and sea visible from near the road).

8.1.4 Research Aims Counts were made daily of all birds on Eocheong by the author between April 14th and May 16th 2003 and 2011, intentionally over the same dates and with the same method and similar survey effort in both years. Dates were selected initially as they covered the period of most intense northward migration recorded in 2000 and 2001 on Gageo (Moores & Kim 2001), and several large arrivals on Eocheong in 2002. The present research had two inter-related aims. The first was to improve understanding of species composition and migration timing, in order to test our prediction that these will be ―intermediate‖ on Eocheong. The second aim was to assess the influence of weather on arrivals and departures during two different seasons of northward migration. Improved understanding of the influence of the large-scale effects on geography and weather can then be used to inform comparisons of data between years on Eocheong, and between Eocheong and other YSBR islands.

8.2 METHODS 8.2.1 Bird-counts Birds were counted within the main survey area on all 33 dates in both 2003 and 2011, and within the supplementary survey area on 19 dates in 2003 and 17 dates in 2011. All individual birds and species (either heard or seen, irrespective of distance) were counted with the use of binoculars and a tripod-mounted telescope through active search. On most dates, counts started between 06:00 and 06:30. Survey each day varied from four hours (adequate to cover all of the main survey area, and to re-count one area to assess whether movement was taking place) up to a maximum of 14 hours (on dates with much movement, when the supplementary count area was also surveyed). In both years, there was bias towards the discovery of vocal species and species of open and edge habitats and away from especially cryptic or silent species in woodland. An unknown proportion of birds over-flying the island were missed. Counts focused on visible migration on several dates from one of two fixed points in 2003, and 241

on five dates for >1hour in the southwest in 2011, suggest that the numbers of missed birds were probably not substantial on days without overcast conditions or precipitation. The location, time, sex and age of individuals or any unusual plumages that could help to identify individual birds were recorded, in order to refine understanding of species-level turnover and to reduce the probability of double- counting. Each day, records were reviewed and individuals or flocks suspected of moving around the island were counted only once for that day. All species were familiar to the author before 2003. However, the increase in field-experience and an improvement in understanding of intra-island movements meant that there was less rounding-off of count data (e.g. to the nearest ten) in 2011. Moreover, a smaller proportion of birds were left unidentified in 2011 than in 2003 (c. 500 in 2011, and <1000 in 2003), almost all on days of substantial movements. Unidentified birds cannot be properly assessed or included in the analysis as there is no method with which to determine whether such birds were earlier or subsequently included in counts. The data were then collated in two main ways. The peak count of a species on a single date is presented as the minimum number of that species recorded on the island during the survey period. Bird-days (defined in Chapter 7, Section 7.2) are also presented. Differences in the timing of peak counts and the number of bird-days are then compared between Socheong (in 2010), and Hong and Heuksan (see Chapter 7, Section 7.1.1).

8.2.2 Weather Details on weather were collected in two main ways. Each day, estimates of cloud cover, wind direction and Beaufort Wind Force, precipitation, and visibility (based on the visibility or invisibility of adjacent islands) were made. Subsequently, custom analysis for the region between 28° & 45° N, and 110° & 140° E for each date between April 13th and May 16th 2003 and 2011 was conducted, using reanalysis data from the National Centres for Environmental Prediction and for Atmospheric Research (NCEP- NCAR) (at: www.esrl.noaa.gov/psd/data/histdata/). Daily composites were generated for 850-mb vector winds and 1000-mb precipitation rates. These two variables reveal many of the weather processes relevant to birds in flight (S. Feldstein in lit. 2011). Through this combination of sources, local and regional weather conditions could be reconstructed on all 66 dates of survey-work and linked to counts (Section 8.3.7).

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8.3 RESULTS 8.3.1 Species, Families and Orders In total, 211 species from 19 orders were recorded (Table 8.1), with 179 species from 17 orders in 2003 and 189 species from 17 orders in 2011. Fifty-four species were recorded in only one of the years. Of the species recorded in 2011, all but one (Watercock) had been recorded on Eocheong at least once between 2002 and 2009. During the surveys, 135 and 138 landbird species were recorded in 2003 and 2011 respectively. Species richness in landbirds on Eocheong thus was intermediate between Socheong (167 landbird species recorded during 57 dates of survey in 2010), and Hong (117 during all dates in April and May 2010) and Heuksan (99 on 46 dates in April and May 2010) (KNP 2010). On Eocheong, 56% of the 211 species were Passeriformes from 27 families. In total, 197 of the recorded 211 species occur regularly in the ROK, and the remaining 14 are less regular. All of the less regular and 160 of the regularly occurring species are complete migrants and 37 are partial migrants to the ROK. No species sedentary at the national level was recorded.

Table 8.1 Number of regularly occurring orders and species in the ROK recorded on Eocheong Island between April 14th and May 16th, 2003 & 2011. ROK Eocheong Order Number of Number of Number of Total regularly- species species occurring 2003 2011 species Galliformes 3 1 0 1 Anseriformes 34 4 3 4 Gaviiformes 4 0 2 2 Procellariiformes 4 0 0 0 Podicipediformes 5 1 3 3 Ciconiiformes 2 0 0 0 Pelecaniformes 21 12 11 13 Accipitriformes 19 9 9 11 Falconiformes 5 4 4 4 Otidiformes 1 0 0 0 Gruiformes 12 3 3 4 Charadriiformes 74 25 29 32 Columbiformes 4 2 1 2 Cuculiformes 5 3 4 4 Strigiformes 8 1 2 2 Caprimulgiformes 1 1 1 1 Apodiformes 2 4 2 4 Coraciiformes 5 3 3 3 Bucerotiformes 1 1 1 1 Piciformes 8 1 1 1 Passeriformes 147 104 110 119 Total 365 179 189 211

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8.3.2 Difference in Total Numbers between Years Based on the sum of peak counts, a minimum 5,075 birds were recorded during the survey period in 2003 and a minimum 7,417 birds in 2011, an increase between years of 2,342 (46%). Due to asynchronous migration strategies, the actual number of birds in both years is assumed to have been substantially higher. This assumption is supported by daily changes in number of several species with distinct plumages (including Laridae and Muscicapidae), and by several species showing a series of small peaks and troughs in number during the survey period in addition to their peak count. Excluding unidentified birds, the difference in bird-days between years was much smaller than in peak-counts, increasing 7% from 20,285 bird-days in 2003 (a mean of 615 birds/day) to 21,773 in 2011 (a mean of 660 birds/day) There was a mean of 72 species recorded per day throughout the combined survey periods. Species‘ richness was lowest during the first third of the period (between April 14th and April 25th) in both 2003 and 2011; and highest in the second third in 2003 and the final third in 2011. Thus, in April the timing of highest species‘ richness was similar to that found on Socheong and the adjacent Hong and Heuksan. In May 2003 it was closer to Hong & Heuksan and in May 2011 it was closer to Socheong.

8.3.3 Species of Global Conservation Concern Eight species of global conservation concern were recorded, with all eight recorded in 2003 but only four in 2011. Four were recorded only once, all as singles, in 2003 (Near-threatened Japanese Quail, on April 30th; Near Threatened Falcated Duck Anas falcata on April 16th; Vulnerable Far Eastern Curlew on April 22nd; and Near Threatened Black Woodpigeon on April 14th). Species recorded in both years were Vulnerable Chinese Egret (seven on May 8th 2003 and singles on five dates in 2011); Near Threatened Japanese Waxwing (single bird on six consecutive dates in 2003, and two in 2011); Vulnerable Yellow-breasted Bunting (peak count of 20 in 2003 with 128 bird-days, and a peak count of eight in 2011 with 28 bird-days); and Vulnerable Yellow Bunting (peak count of three with 32 bird-days in 2003, and peak count of four in 2011 with 11 bird-days). Yellow Bunting is a Far West Pacific taxon, recorded in higher numbers southward in the YSBR. There was a peak count of 26 on Gageo on April 25th 2009 (own data), and 44 bird-days in 2009 on Heuksan (KNP 2009). On Socheong there was a total of only four bird-days between 2003 and 2005 (Moores 2007) and only one in 2010 (Chapter Seven). Thus the number of Yellow Bunting on 244

Eocheong in 2003 and 2011 was intermediate between islands on the Southern Crossing and Socheong on the Northern Crossing

8.3.4 Most Numerous Species Two-thirds of all 211 species were recorded with peak-counts of <10 individuals. Seventy-two species had peak counts of >10; 13 of these had peak counts of >100 in either 2003 or 2011; and five of these species had peak counts of >100 in both years. In 2003, the seven species with peak counts of >100 comprised 20% of the sum of all peak counts, compared to ten species comprising 48% in 2011. This increase was in part due to the strong visible migration recorded on several dates in 2011, and the comparative paucity of similarly large movements in 2003 (rather than to increased identification confidence). Based on peak counts, the two most numerous species in 2003 were Dusky Thrush (200) and Little Bunting (250), with the latter peak count part of a large arrival. Although the timing of the Peak Count Dates (and Last-dates) of both species were well-separated, there was some correlation in their numbers between April 19th and 29th, suggesting a common effect on both species during this period (Figure 8.2). This common effect was weather (see Table 8.4 below).

300

250

200 DUSKY THRUSH - 2003 150

LITTLE BUNTING - 2003 Number 100

50

0 14-15-16-17-18-19-20-21-22-23-24-25-26-27-28-29-30- 1- 2- 3- 4- 5- 6- 7- 8- 9- 10-11-12-13-14-15-16- AprAprAprAprAprAprAprAprAprAprAprAprAprAprAprAprAprMayMayMayMayMayMayMayMayMayMayMayMayMayMayMayMay Date

Figure 8.2 Numbers of Little Bunting (in pink) and Dusky Thrush (in black) in 2003.

The two most numerous species in 2011 were Black-tailed Gull and Dusky Thrush. Both species showed two peaks in 2011 (Figure 8.3), with one of these peaks falling on the same date (April 26th). There was stronger correlation, however, between daily changes in number of Dusky Thrush and some other landbird species, and the two highest peaks in Dusky Thrush and Brambling were both on the same dates. Both 245

species were observed in large numbers on days with moderate or strong winds, as part of inclement weather arrivals.

900 800 700 600 DUSKY THRUSH - 2011 500 BLACK-TAILED GULL - 2011 400 Number BRAMBLING - 2011 300 200 100 0 14-15-16-17-18-19-20-21-22-23-24-25-26-27-28-29-30- 1- 2- 3- 4- 5- 6- 7- 8- 9- 10-11-12-13-14-15-16- AprAprAprAprAprAprAprAprAprAprAprAprAprAprAprAprAprMayMayMayMayMayMayMayMayMayMayMayMayMayMayMayMay Date

Fig. 8.3 Numbers of Dusky Thrush, Brambling and Black-tailed Gull recorded in 2011.

8.3.5 Comparison of Most Numerous Landbird Species between Islands A total of 12 landbird species had peak counts of >100 in either 2003 or 2011 (Table 8.2). Based on the mean of bird-days in 2003 and 2011, Black-faced Bunting was the most numerous (and is therefore ranked ―1st‖) and Chestnut-flanked White-eye the least numerous (and is therefore ranked ―12th‖). Ranking in this way allows direct comparison of their abundance on Eocheong, Socheong (based on 2010 count data) and the adjacent Hong and Heuksan during April and May 2010 (KNP 2010).

Table 8.2 Species abundance by bird-days of the twelve most numerous landbird species on Eocheong in 2003 and 2011, and their rank by bird-day on Socheong, Hong and Heuksan in 2010. Species Eocheong Socheong Hong Heuksan Bird- Rank Rank Rank Rank days

Black-faced Bunting 1,486 1st 4th 1st 10th Dusky Thrush 1,474 2nd 13th 20th 7th Brambling 951 3rd 3rd 5th 2nd Eurasian Siskin 942 4th 104th No record No record Pale Thrush 940 5th 20th 8th 8th Olive-backed Pipit 933 6th 2nd 6th 12th Little Bunting 849 7th 12th 11th 5th Red-rumped Swallow 500 8th 14th 28th 7th Eyebrowed Thrush 498 9th 5th 31st 74th Grey-backed Thrush 395 10th 9th 50th 34th Chestnut Bunting 330 11th 7th 64th 27th Chestnut-flanked White-eye 315 12th 8th No record No record Note: On Heuksan, there were only 16 days of survey in May 2010.

Ten of the twelve most numerous species have been recorded in substantial numbers annually on Eocheong (unpublished data), the two exceptions being Eurasian 246

Siskin and Chestnut-flanked White-eye. The Eurasian Siskin is an irruptive species (Newton 2006), which was present in very low numbers on YSBR islands in 2010 but in high numbers in both 2003 and 2011. The Chestnut-flanked White-eye appears to be increasing in the ROK (Chapter 2); is regular in substantial numbers on Socheong (Chapter 7); and is seldom-recorded on islands in the Southern Crossing, including Gageo (unpublished data) and Hong and Heuksan (KNP 2005-2010). On Eocheong, its numbers tend to fluctuate year to year. Only 15 were recorded in 2003 (and on a single date), while there was a peak count of 170 in 2011 and a total of 605 bird-days. If most species migrated across the YSBR on a homogenous broad front then most of the regular, numerous species on Eocheong would also be the most numerous species on Socheong and on Hong and Heuksan. However, as we predicted there were differences between islands. Overlap in the most numerous species was stronger between Eocheong and Socheong than with Hong or Heuksan. Eleven of the 12 most numerous species on Eocheong were among the 20 most numerous species on Socheong. Notably, three species confined as breeding species to the Northeast Asian Mainland were numerous on both Eocheong and Socheong (Grey-backed Thrush, Chestnut-flanked White-eye and Chestnut Bunting), but were much less numerous on Hong and Heuksan. All of the same eleven overlapping species were also among the most numerous 20 species recorded during counts of visible migration on North Point on Socheong (see Chapter 7, Table 7.9). It can therefore be concluded that the same species tended to migrate during the day and as part of weather-related movements both on Socheong in 2010 and on Eocheong in 2011. Several of the more numerous species on Socheong were by contrast less numerous on Eocheong. These included Yellow-browed Warbler, Yellow-browed Bunting and Asian Stubtail (on Socheong, ranked 1st, 15th and 18th respectively). Yellow-browed Warbler and Yellow-browed Bunting are both rare in Japan (Brazil 1991), suggesting most migrate on the Northern Crossing. All three species still had more bird-days on Eocheong than on either Hong or Heuksan, despite the shorter survey period on Eocheong. Six and seven respectively of the eleven most numerous species on Eocheong were among the most numerous 20 species on Hong and Heuksan. Among these, Pale Thrush breeds on Eocheong, Hong and Heuksan, as well as throughout much of the ROK and was comparatively more numerous on these islands than on Socheong. The other five most numerous species that overlapped (Black-faced Bunting, Dusky Thrush, Brambling, Olive-backed Pipit and Little Bunting) all have 247

wide breeding ranges that include both the Far West Pacific Region and the Northeast Asian Mainland. All five species are also frequently involved in substantial weather related movements of birds across YSBR islands, including on Gageo (unpublished data), Eocheong and Socheong.

8.3.6 Comparison of Migration Timing between Islands 8.3.6.1 Survey-dates and species If landbirds migrated on a broad front across the YSBR then the timing of migration would be similar on Socheong, Eocheong and Hong and Heuksan Islands. This is because the three islands are within 400km of each other: i.e. <1 day‘s flying distance for migratory Passeriformes We predicted that due to channeled migration there will instead be substantial differences in migration timing between these three islands, with most populations migrating earlier on the Southern Crossing. To test this prediction the migration timing of 38 landbird species are compared. These species were selected as they met three conditions: (1) they are more or less absent from the ROK in winter; (2) all were recorded on at least three dates on Eocheong in both years; and (3) all showed single or near-consecutive peak counts in both 2003 and 2011. The First-dates, Peak Count Dates and Last-dates used are: 1. For Eocheong, the median of those dates in 2003 and 2011; 2. For Heuksan, on 22 dates in March (including all dates from 15th, with the exception of 21st-22nd); 23 dates in April (all except 14th-15th, 19th-20th, 26th- 27th); 28 dates in May (all expect 19th, 24th and 31st); and daily from June 1st-4th (Park Jong-Gil for the NPMBC). 3. For Socheong, from 57 days of survey between March 31st and June 2nd 2010 (Chapter 7). All 38 of these species were recorded on Socheong, but five were not recorded on Heuksan (including four which do not breed in Japan). Due to the short duration of the research period, many species were already present on Eocheong at the beginning and/or the end of surveys.

8.3.6.2 First-dates Twenty-three species had First-dates that (1) can be compared between all three islands and (2) were not shared with another island. Heuksan had the highest number of earliest First-dates not shared with another island (n=13); Eocheong and Socheong 248

both had five. The pattern was somewhat reversed with latest First-dates. Socheong had the highest number of latest First-dates (n=11) and Eocheong the least (n=4). There were 21 species with earlier First-dates on Heuksan than Socheong (mean of 4 days earlier), and nine with earlier First-dates on Socheong than Heuksan (mean of 6 days earlier). In most species, their First-date was within ten days between islands. However, the First-date of Black-browed Reed Warbler Acrocephalus bistrigiceps was 20 days earlier on Heuksan than Eocheong and 31 days earlier on Heuksan than Socheong. This species is a Very Late Migrant on Socheong (Chapter 7, Section 7.3.4.8), and was the third most numerous landbird in the Whole Island Count on June 1st (Chapter 7, Table 7.10). The early Black-browed Reed Warbler on Heuksan were therefore probably migrating towards breeding-grounds in Japan. Banding recoveries prove at least occasional migration of the species between Hong and Honshu, Japan (KNP 2007), and the species arrives in April in Honshu (Brazil 1991).

8.3.6.3 Peak Count Dates Peak Count Dates can be compared directly for 33 species between the three islands. Only Eyebrowed Thrush had similar Peak Count Dates on all three islands. This species showed a very concentrated migration through Socheong in 2010 (Chapter 7), and also through Eocheong in both 2003 and 2011. There were seven species with Peak Count Dates within one day of each other on Heuksan and Eocheong. Of the remainder, 17 out of 25 had earlier Peak Count Dates on Heuksan than on Eocheong. The difference was even greater between Heuksan and Socheong. Only one species had the same Peak Count Date. Twenty-five species had earlier Peak Count Dates on Heuksan than on Socheong, with a mean of 18 days difference (ranging from a minimum six days difference in Asian Stubtail and Siberian Rubythroat, to a maximum 35 and 38 days in Barn Swallow and Korean Bush Warbler respectively). There were seven species with later Peak Count Dates on Heuksan (mean of 7 days difference). These included Eastern Yellow Wagtail Motacilla tschutschensis. This species has a very extensive breeding range, reaching into Alaska to the northeast (Brazil 2009). For birds migrating from southern China to such remote north-eastern breeding areas, their most direct route would be by the Southern Crossing, through Japan and then Kamchatka. Later migration on the Southern Crossing might therefore be anticipated.

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8.3.6.4 Last-dates Only three species had Last-dates which could be clearly detected on all three islands (as the other species were still present on Eocheong at the end of fieldwork). These include Pallas‘s Leaf Warbler Phylloscopus proregulus which had a Last-date 20 days earlier on Eocheong than on Socheong. This species was not recorded at all on Heuksan. There were 28 species with earlier Last-dates on Heuksan than on Socheong, with a mean of 9 days difference, rising to >23 days difference in Eastern Crowned Warbler and of at least 29 days difference in Siberian Thrush. Both of the latter species breed in Japan as well as on the Northeast Asian Mainland. Eastern Crowned Warbler is monotypic and Siberian Thrush has two subspecies. The pattern of records of different subspecies of Siberian Thrush suggests channeled migration. The Far West Pacific davisoni subspecies of Siberian Thrush has been recorded on Gageo and on Eocheong, but not on Socheong. Subspecies davisoni arrives in Honshu at breeding grounds in late April or early May (Brazil 1991), and would be expected to complete migration early. The Last-date of Siberian Thrush on Heuksan was May 2nd. By contrast, nominate sibirica breeds on the Asian mainland west to 85° E in Siberia, with some only reaching northernmost breeding areas in mid-June (Clement & Hathway 2000). Nominate Siberian Thrush were still present on both Eocheong and Socheong at the end of survey.

In summary, migration dates are consistent with the hypothesis of channeled migration, and with Eocheong‘s status as an Intermediate Island. Among the 38 species which can be compared, there is evidence of: 1. Earlier First-dates southward of most species and of some populations that breed in the Far West Pacific Region (e.g. Black-browed Reed Warbler); 2. Concentrated migration (e.g. Eyebrowed Thrush); 3. Later Peak Counts northward (most species); 4. Later Last-dates northward (most species) including of taxa with a more westerly distribution.

8.3.7 Influence of Weather

8.3.7.1. Large Arrivals and weather We predicted that large arrivals on the Intermediate Island of Eocheong will be strongly influenced by drift by wind from the Northern and Southern Crossings. Thus, 250

in addition to observation of weather at ground-level, 850-mb vector wind was also assessed from NCEP-NCAR reanalysis data for the area close to Eocheong; for the area approximately halfway between Shanghai and Hong (to represent the Southern Crossing); and for an area halfway between the Shandong Peninsula and Socheong (to represent the Northern Crossing, even though we propose that this crossing also extends on a southwest-northeast axis from Shanghai to the Shandong Peninsula). Estimates of vector wind strength were based each day on the number used for shading of reanalysis composites. Absence of colour was interpreted as ―calm‖, the values 2-5 as ―light winds‖, 6-9 as ―moderate winds‖, 10-13 as ―strong winds‖, and 14+ as ―very strong winds.‖ In 2003 and 2011 there were a total of twelve large arrivals, including one where more than half the birds were Black-tailed Gull, and the remainder comprised largely of landbirds (see Figure 8.4).

3500 3000 2500

2000 2003

1500 2011 Number 1000 500 0 14- 15- 16- 17- 18- 19- 20- 21- 22- 23- 24- 25- 26- 27- 28- 29- 30- 1- 2- 3- 4- 5- 6- 7- 8- 9- 10- 11- 12- 13- 14- 15- 16- Apr Apr Apr Apr Apr Apr Apr Apr Apr Apr Apr Apr Apr Apr Apr Apr AprMayMayMayMayMayMayMayMayMayMayMayMayMayMayMayMay Date

Figure 8.4 Daily changes in number of birds (all species) recorded each day of survey in 2003 and 2011.

Analysis of weather conditions at ground-level for the 11 large landbird arrivals (averaging one large arrival for every six days of survey) revealed that: 1. None were on the 13 days when visibility remained less than 5km; 2. Eight were on one of the 25 days (32%) with some precipitation; 3. Two were on one of the 13 days (15%) with local winds of Beaufort Force 0-2; 4. Eight were on one of the 41 days (20%) with locally moderate winds (Beaufort Force 3-5); 5. Three were on one of the nine days (33%) with locally strong (Beaufort Force 6-7) or very strong (Beaufort Force 8+) winds. There was therefore a negative correlation with large arrivals and locally poor visibility, and a positive correlation with large arrivals and locally strong wind and/or 251

precipitation. There was also a positive correlation with strong or very strong winds in the Southern and Northern Crossings and substantial arrivals either the same or the following day (Table 8.3).

Table 8.3 Local and regional weather the day before and during Large Arrivals of landbirds in 2003 and 2011 Date Number Local Vector Vis. Local Vector Vector of Wind Wind (Km) Precipitation Wind Wind Birds Eocheong Southern Northern Crossing Crossing 2003 Apr 21 374 NW3 N,L 30 None NW, L E,L Apr 22 1,315 W2-3 SW, M 20-30 Rain Showers SW, M SW, L Apr 23 939 NW2-3 SW,M 20-30 Rain Trace SW, ST NW, L Apr 24 667 NW2-3 E,L <10 Rain Evening SW, ST E, L Apr 25 826 NE 5>3 NE, L 10-15 Rain A.M. SW, M NE,L Apr 30 664 NW3>2 NW, ST 10 None N, M NW, M May 1 914 S2 W, L 10-15 None Calm W, M May 7 586 SE>NW6 SW, M 0.2 Rain>Drizzle SW,VS NE, M May 8 1,255 NW>NE3 NE, M 5>30 Rain A.M. NW, M NE, M 2011 Apr 17 260 SW3 NW, L 10 None NW, L W, M Apr 18 1,030 NW3-4 N, M 10-15 Rain Showers NW, VS N, ST Apr 25 567 SW4 W, M 10 Rain Trace W, VS W, M Apr 26 3,025 W4 W, M 10>5 Rain>Drizzle W, ST W, L May 10 360 W3 W, M 0.5 Rain Showers SW, VS Calm May 11 1,085 W2 Calm 0.5>100 Rain Showers W, M Calm May 12 1,071 NW 2-6 NW, M 0.5>15 Drizzle NW, M NW, M May 13 881 NW1-6 NW, VS 15 None NW, ST NW, VS May 14 1,662 NW1-4 W, M 20 None NW, M NW, ST Figures in bold indicate large arrivals. In all other columns, ―>‖ denotes ―became‖, and < denotes less than. NW =Northwest, SW=Southwest etc. In the three columns with Vector Winds, strength: ―L‖=Light, ―M‖=Moderate, ―ST‖=Strong and ―VS‖=Very Strong. In column ―Vis‖, visibility was estimated in km at ground-level.

Ten of the eleven large landbird arrivals in 2003 and 2011 can be explained, at least in part, by a combination of visibility of >5km, and/or local precipitation and/or strong winds across the Northern and/or Southern Crossing. The only apparent exception is the Fair Weather Arrival of May 1st 2003. At that time, it seems plausible that large numbers of migrant landbirds departed the Chinese coast the previous evening and then encountered moderate northerly headwinds which became northwesterly close to the Shandong Peninsula. Northwest winds would then have drifted these birds southeastward towards Eocheong. In contrast, there were only four dates with some precipitation and visibility of >5km without a large arrival. One of these was accompanied by a loss of visibility (to <1km), and another was accompanied by very strong winds in the Southern Crossing and was followed the next day (April 26th 2011) by the largest arrival in either year.

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8.3.7.2 Inclement weather arrivals The composites of precipitation rates and 850-mb vector winds tend are used here in the understanding that the weather conditions of many more large arrivals need to be researched in order to improve levels of confidence in the results. Supported by observations in the field, the composites suggest that low pressure systems can carry substantial numbers of birds (as on Socheong: see Chapter 7, Section 7.3.5.2). The eastward passage of low pressure systems results in northwest winds that can also cause wind-drift of large numbers of birds from the Northern Crossing. Figure 8.5 is a composite of eight dates of 1000-mb precipitation rates (near to sea- level) one day before large arrivals were recorded on Eocheong. The composite therefore shows precipitation rates close to the time of presumed departure for birds from the Chinese coast. Height at 1000-mb has been selected as birds adjust altitude downwards in relation to precipitation, and birds observed arriving on Eocheong during arrivals have done so at low altitude.

Figure 8.5 Composite of 1000-mb Precipitation Rates for the day before eight large Inclement Weather Arrivals (i.e. April 1st, 22nd, 24th and May 7th 2003; and April 17th, 25th, May 10th and 11th 2011). Reanalysis data are from NCEP-NCAR. Eocheong is represented by the small black dot, immediately to the west of the most intense area of precipitation (in purple).

In the large arrivals of 2003 and 2011, birds tended to depart the Chinese coast soon after the passage of inclement weather, and tended to arrive as the precipitation moved eastward across the ROK mainland. Several days with Inclement Weather Arrivals on Eocheong had heavier rain in the first half of the day, followed by a rapid increase in 253

visibility in the second half (see Table 8.3 above). On such days, 850-mb vector winds (Figure 8.6) tended to be moderate and from the northwest.

Figure 8.6 Composite of 850-mb vector winds on eight dates with Inclement Weather Arrivals (April 22nd, 23rd, 25th and May 8th 2003; and April 18th, 26th, May 11th and 12th 2011). Reanalysis data are from NCEP-NCAR. Black Dot marks the location of Eocheong.

8.3.7.3 Fair Weather Arrivals A composite of 850-mb vector winds on the same day as five large Fair Weather Arrivals (Figure 8.7) shows that the strongest winds were centred to the northeast of the Korean Peninsula (rather than off southern Japan, as in Inclement Weather Arrivals). It therefore seems likely that birds tended to depart the Chinese coast (perhaps from near to Shanghai) in calm conditions or with a light south-westerly tail wind. For those birds that intended migration towards the northeast, they then presumably encountered rapidly strengthening westerly and north-westerly winds over open sea as they approached the Shandong Peninsula. Winds were strongest to the east of the Shandong. Birds were then drifted towards the southeast, to arrive on Eocheong. On May 8th 2005, simultaneous research on Weiyeon and Eocheong found that a large Fair Weather Arrival (included in the composite) started on Weiyeon c. 30 minutes earlier than on Eocheong 15km to the southeast (Kim Hyun-tae and Moores, unpublished data). Such timing is consistent with wind-drift from the northwest

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. Fig. 8.7 Composite of 850-mb vector winds during five large Fair Weather Arrivals, on April 22nd 2002, May 1st 2003, May 8th 2005, and May 13th & 14th 2011. Reanalysis data are from NCEP-NCAR. Black dot marks the location of Eocheong.

8.3.7.4 Species-based evidence of drift by wind To identify whether there was any relationship between Peak Count Dates on Eocheong and wind direction, records of ten landbird species were compared (Table 8.4). Four of the ten are Far West Pacific taxa (and one is a near-endemic to Japan); the remaining five breed mostly on the Korean Peninsula and on the Northeast Asian Mainland. Eight of the ten form pairs of taxa with similar mass and ecological niche which might be considered relevant to species-level decision-making on migration and weather. There are too few data to conduct a robust analysis. However, Peak Count Dates in these species and 850-mb vector winds near to Eocheong and across the Southern and Northern Crossing at the time of these Peak Count Dates suggest a positive relationship. Only two of the 10 species had peak counts during southerly or south-easterly winds. Both of these (Chestnut-cheeked Starling in 2003 and Yellow Bunting in 2003 and 2011) are Far West Pacific taxa that thus intended migration to Japan, presumably across the Southern Crossing. Both species were apparently wind-drifted northward to Eocheong. Seven of the remaining eight species had peak counts during strong or very strong winds in either one or both years including all four Turdus species. The peaks of Eyebrowed Thrush numbers were recorded during very strong winds across the Southern Crossing in 2003 and in calm to moderate winds in 2011. In 2011, there were rain showers and the peak count followed one day after very strong winds on the 255

Southern Crossing. The southernmost entry point into the Northern Crossing is presumed to lie close to Shanghai. It therefore seems likely that birds recorded on Eocheong departed the Chinese coast near Shanghai and then used these strong winds to cross the Yellow Sea in both years.

Table 8.4 Strength of 850-mb vector winds in 2003 and 2011 on the Peak Count Date of five landbird species that breed on the Northeast Asian Mainland, and of five landbird species which breed mostly in the Far West Pacific Region. Species 2003 2011 Local Vector Vector Local Vector Vector Vector Wind Wind Vector Wind Wind Wind Southern Northern Wind Southern Northern Crossing Crossing Crossing Crossing

Eyebrowed Thrush SW,M SW, VS NE, M Calm W, M Calm Brown-headed Thrush W, M SW, ST Calm SW, VS SW, VS W, ST Grey-backed Thrush SW, M SW, ST NW, L W, M W, ST W, L Grey Thrush E,L SW, ST E, L E, M NE, L NW, M Yellow-rumped Flycatcher Calm Calm Calm NW, M NW, M NW, M Narcissus Flycatcher N, L NW, ST NW, M SW, VS SW, VS W, M Chestnut Bunting NE, M NW, M NE, M W, M NW, M NW, ST Yellow Bunting SW, M S, M SW, M S, M SE, L SW, M Chestnut-flanked White-eye SW, M SW, M Calm NW, VS NW, ST NW, VS Chestnut-cheeked Starling SW, M S, M SW, M NW, M SW, M SW, M Note: Species in italics are Far West Pacific Taxa. Local 850-mb Vector Wind = near to Eocheong. Wind direction and strength are as in Table 8.3, e.g. L = Light winds, M = Moderate winds, ST= Strong winds, VS = Very strong winds; and SW= southwest, NW = Northwest, SW=Southwest etc.

The two flycatcher species (Yellow-rumped and Narcissus) peaked in different weather conditions. Yellow-rumped Flycatcher breed in the ROK and the similarity of peak date between years (May 11th 2003 and May 12th 2011) suggests that birds from the same population might have been involved both years. By contrast, the Peak Count Dates in 2003 (April 21st) and 2011 (May 9th) for Narcissus Flycatcher were very different between years and coincided with strong or very strong winds. As the species does not breed in the ROK and most breed in Japan, birds that reach Eocheong are likely wind-drifted northwards from the Southern Crossing.

8.3.7.3 Other characteristics of large arrivals A comparison of counts between May 8th and May 15th in 2003 and 2011 suggests that large arrivals of landbirds on Eocheong shared a number of characteristics. These included a rapid increase in species‘ richness and the number of individual birds that were numerically dominated by a few species, which in most cases staged on the island for only a short period of time. In 2003, there was an increase from 586 individuals of 73 species on May 7th to 1,225 individuals of 98 species on May 8th. The six most numerous species on May 8th 256

together comprised 51% of the total number of recorded individuals. On May 9th, as a ridge of high pressure became established, the number of species and individuals fell rapidly, to only 505 individuals of 81 species, and all six of the most numerous species decreased in number by >50%. On subsequent dates, when the weather remained dry and visibility high to moderate, the day-to-day changes in number were much less marked. Either most of the same individuals remained on the island, or within-species turnover was concealed by similar numbers of the same species arriving and departing each day. In May 2011, the six most numerous species involved in the large arrival on May 8th 2003 were all present on the 8th but in comparatively lower numbers. The first large arrivals took place in inclement weather on the 11th and 12th. The number of individuals and species increased rapidly between May 10th and May 11th, and continued to increase until the 12th. Although the total number of birds recorded on both the 11th and 12th were similar, this included very rapid turnover, with 447 Eyebrowed Thrush present on the 11th but only 20 on the 12th. The three most numerous species on May 12th (Chestnut-flanked White-eye, Chestnut Bunting and Yellow-browed Warbler) all showed large increases from the 11th, and two of these (Chestnut Bunting and Yellow-browed Warbler) then also showed a rapid fall in number on 13th, before increasing again markedly during the Fair Weather Arrival on May 14th (Figure 8.8).

500 450 400 350 300 CHESTNUT BUNTING 250 EYEBROWED THRUSH

Number 200 YELLOW-BROWED WARBLER 150 100 50 0 2011 2011 2011 2011 2011 2011 2011 2011 2011

8-May 9-May 10-May 11-May 12-May 13-May 14-May 15-May 16-May Date

Figure 8.8 Numbers of Chestnut Bunting, Eyebrowed Thrush and Yellow-browed Warbler on Eocheong between May 8th and May 16th 2011.

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On May 14th, a large fair-weather arrival of passerines took place between 13:00 and 15:00, a period in which winds eased from northwesterly Beaufort Force 3-4, to become light and variable. During these two hours, several hundred birds per hour arrived. Tens of passerines were observed in low flight across open water of the main harbour, and feeding flocks of several species became widespread in all suitable habitats. Some birds were seen to depart the island between 16:00 and 18:00, and a substantial departure took place between 19:50 and 20:30 (within one hour of sunset), involving at least three shorebird species, two species of thrush and two species of bunting.

In summary, the large arrivals on Eocheong Island in 2003 and 2011: 1. Contained the largest number of individual birds and a disproportionate number of peak counts. For example, there were season peak counts of 19 species on May 8th 2003 and of 25 species on May 14th 2011. 2. Included a high number of species: the six dates with large arrivals in 2011 had a mean of 85 species, compared to a mean of 66 species on the other 27 dates. 3. Contained a few dominant species that were in their main period of migration, with species that over-winter but which do not breed in the ROK (e.g. Dusky Thrush and Brambling) more frequent and numerous before April 25th; species that breed in the ROK or adjacent regions (e.g. Pale Thrush and Black- faced Bunting) more numerous in late April and early May; and species that neither over-winter nor breed in the ROK (e.g. Eyebrowed Thrush and Chestnut Bunting) more numerous in large arrivals later in May. 4. Contained mostly species that are regular diurnal migrants and smaller numbers of species (e.g. Asian Stubtail) which apparently depart mostly over- night. 5. Were followed by a rapid fall or change in the number of birds and individuals.

These large arrivals on Eocheong therefore shared several of the same characteristics with the large arrivals observed on Socheong Island (Chapter 7), and with arrivals observed on other YSBR islands (unpublished data).

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8.4. DISCUSSION 8.4.1 Weather and Migration The results support our hypotheses on geography and weather. They suggest that the abundance and composition of species observed on Eocheong in 2003 and 2011 were strongly influenced by the island‘s intermediate location between the Northern and Southern Crossings, and by weather systems. Most large arrivals recorded on Eocheong in 2003 and 2011, on Gageo (2000-2002), and on Socheong (2003-2010) were weather-related. It therefore seems likely that most large arrivals on other islands will also be weather-related. With the exception of species that might select to migrate in strong winds (e.g. Turdus thrushes), it also seems probable that large numbers of birds over-fly islands in the Northern and Southern Crossings undetected during periods of light winds and high visibility. In contrast, although further research is required, it seems probable that in clear and calm weather few migrants over-fly Eocheong. On days with clear weather, usually 5-60 birds/hour were seen either circling (raptors and Hirundinidae) or departing the island. No birds were recorded flying at altitudes of >1km and a large proportion of departing birds were suspected of having earlier staged on the island, as they were seen to gain altitude rapidly on departure. The necessary balance of energy, time and safety and the species composition during settled weather suggest that many of the landbird migrants that do reach Eocheong in such conditions can be divided into two groups. The first is comprised of raptors and other species (some of which might be arriving on the island from the south) that use Eocheong for orientation and for gaining altitude; and the second, of species and individuals that intend migration across that part of the Yellow Sea. That is presumably because, like Yellow-rumped Flycatcher, they breed in the central provinces of the ROK (a much smaller area than reached by the two main migration corridors). The peak count of Yellow-rumped Flycatcher on Eocheong in 2003 took place when there were calm conditions near to Shanghai and across the YSBR, and in 2011 when there were moderate winds. Such conditions might be considered suitable for nocturnal passerine migration (Karlsson et al. 2011), with less probability of drift by wind. In contrast to species regularly involved in large arrivals, species such as Yellow-rumped Flycatcher and Asian Stubtail also tend to be rather poorly represented in diurnal departures (at least from Socheong: Chapter 7, Section 7.3.5). This is perhaps because both species tend to select for optimal conditions to cross the Yellow Sea to reach Korean breeding grounds, so that there is no need for 259

them to re-orientate or to mitigate for time lost following wind-drift. In contrast, large arrivals of the majority of species were dominated by species that do not breed in the ROK. These arrivals took place on relatively few dates, most clearly associated with two types of weather systems. Although some birds probably migrate northward along the west coast of the ROK to reach Eocheong, most appear to have completed a direct sea-crossing from China. This assumption is supported by reanalysis data on vector winds (as above), on observation of the direction of arriving and departing birds (most of which are moving on a southwest- or west-northeast axis), and by the ranking of more numerous species between islands north-south in the YSBR. Chestnut-flanked White-eye was numerous on Eocheong in May 2011. It is also regularly one of the most numerous species further north on Socheong in mid-late May, and was common and seasonally abundant on passage in south-central DPRK during 1999–2004 (J. W. Duckworth in lit. 2006). However, Chestnut-flanked White-eye does not breed in the southern part of the Korean Peninsula, remains very scarcely recorded in the southwest of the ROK, and is also rare in Japan (Brazil 1991). On southwestern islands, there were only four bird- days in total recorded during daily coverage in May on Hong between 2008 and 2010 (KNP 2008-2010), and none were recorded by the present author during daily coverage of Gageo between May 20th and 28th 2009. It has also yet to be recorded reliably further south on Jeju Island (Kang et al. 2010). If most migrant landbirds were arriving on Eocheong from islands to the south, then it would seem likely that proportionately larger numbers of Chestnut-flanked White-eye and other species that breed on the Northeast Asian Mainland would also be recorded southward. The timing of arrivals of landbirds, which often occur in the afternoon on days with good visibility and light to moderate winds on Eocheong, also suggests a non-stop flight from China. Most nocturnal passerine migrants in other regions depart within one to four hours of sunset (Moore 1987, Åkesson et al. 1996), and birds recorded in European radar studies with a fast intermittent flapping flight, i.e. mainly warblers and flycatchers, travel at a speed of between 11 and 12.5 m/s (Bruderer 1997). If birds departed mainland China in the evening at 2100hrs and flew for 700km at a constant speed of 11m/s they would arrive on Eocheong at about 1500hrs, consistent with the time when many small (and large) arrivals do occur. In large inclement weather arrivals, however, birds sometimes arrived on Eocheong pre-dawn or soon after, most likely achieved through a substantial increase in flight 260

speed. In 2011, on April 26th there were moderate westerly winds at ground level and strong 850-mb vector winds on the Southern Crossing. Birds were heard arriving before dawn, and 2,150 birds (most of which were Dusky Thrush) were seen to arrive between 06:30 and 07:45. Despite the presumed long sea crossing, many of the birds involved still had sufficient energy to continue migration without prolonged staging on Eocheong. Indeed, there was often a rapid departure of birds following large arrivals, ranging from minutes (on April 18th and 26th) to less than one day. Research in other regions indicates that birds select for favourable wind conditions both at departure (Åkesson & Hedenström 2000) and when aloft to save energy. For some long-distance migrants a tail-wind is an indispensable support to cover large barriers (Liecthi 2006). It therefore seems plausible that some species, especially Turdus thrushes, might be intentionally ―surfing‖ certain weather systems as part of their regular migration across the Yellow Sea. The unpredictable conditions of such weather systems, however, would likely lead to large-scale drift by wind on occasion (perhaps the cause of Eyebrowed Thrush flocks on Attu Island in the Northern Pacific reported by Hameed et al. 2009). Birds using such weather systems can become channelled by rain fronts and forced lower by a reduction in visibility. Even in such conditions, however, many birds apparently continued their migration once they reached Eocheong, especially if other islands (only 11km away to the northeast) were visible. Some individuals of the same species and the majority of some other species instead ceased flight when they reached Eocheong. For such birds Eocheong might have been more of an emergency staging site than an optimal staging area, somewhat analogous to that described for shorebirds in the Western Palearctic by Shamoun-Baranes et al. (2010b).

8.4.2 Weather-based bias and the detection of underlying population trends If most individuals of many species are observed on Eocheong due to rain and drift by wind, then it seems likely that the presence of flocks of Chestnut-flanked White-eye in some years and their absence in others on the island will have been influenced more by the track and strength of weather systems than by annual fluctuations in their abundance. The same is likely true of other species, which might also then show First- dates that are earlier (or later) and peak counts which are more elevated (or reduced) between years due to the timing and size of the same kinds of systems. The difference in timing of such systems in 2003 and 2011 might therefore have been responsible for later First-dates of several species in 2011 compared with 2003. 261

There were more large arrivals in 2011 than in 2003. As a result, more species were likely recorded in higher numbers (in terms of peak counts and bird-days) in 2011 than in 2003. In total, 93 species showed an increase between 2003 and 2011 compared with 79 that showed a decrease and 39 that showed an unclear trend (with an increase in peak count but a decrease in bird-days). Weather-related large arrivals, however, also tend to carry with them small numbers of many other species. If all species with a peak count of less than 10 individuals throughout the whole survey period are excluded, then in 2011 there were only 30 species with higher peak counts and more bird-days compared to 33 with lower peak counts and fewer bird-days between 2003 and 2011. Despite the greater incidence of large arrivals in 2011, based on the daily mean there was a lower number of species present on dates without large arrivals in 2011 compared to 2003, and fewer species of global conservation concern were recorded. Moreover, three of the four species of global conservation concern that were recorded showed a decline, at least in bird-days. It is possible that some of the perceived declines in numbers recorded between years in some species might be due to local habitat degradation and disturbance. However, there is presently little evidence for this beyond an apparent decline in the staging time of a few species and the loss of three species (Bull-headed Shrike, Barn Swallow and Tree Sparrow) as breeders between years. However, all three of these species also showed a Negative National Population Trend (Chapter Two). The most substantial difference was instead between the timing and the number of weather systems affecting the island. It is evident that a greater or lesser number of weather- related large arrivals in some years than others might obscure underlying population trends. Nonetheless, consideration of the changed relative bird abundance within similarly-timed large arrivals between years and on the numbers of birds recorded between them in small-sized arrivals suggests that several species might have decreased substantially, at least on Eocheong, between 2003 and 2011. Most or all such species are complete migrants to the ROK and include Barn Swallow, Olive- backed Pipit, Ashy Minivet, Eastern Crowned Warbler, Pale-legged Leaf Warbler and Yellow-breasted Bunting. All were recorded in much reduced numbers, both as peak counts and in bird-days in 2011 compared with 2003. This was despite similar numbers or increases recorded between years in species within the same families or which tended to peak during similar weather systems and dates. 262

As in all species, the apparent decline in Barn Swallow (of 61% bird-days and of >50% in peak counts) on Eocheong between 2003 and 2011 might be a result of variability in weather. However, annual monitoring since 2000 by the National Institute of Biological Resources (NIBR) also suggests a decline in Barn Swallow in the ROK of 27% since 2000 (Chapter 2, Section 2.3.7.10). Moreover, Red-rumped Swallow, which often migrates across the YSBR with Barn Swallow, had a much smaller fall of only 14% in bird-days. There are no monitoring programs to detect changes in the ROK‘s breeding population of Eastern Crowned Warbler. On YSBR islands between 2000 and 2004 Eastern Crowned Warbler was one of the most numerous leaf warblers, often forming large mixed groups with other Phylloscopidae (own data). The peak count of Eastern Crowned Warbler on Eocheong of >150 in 2002 fell to 40 with a total of 293 bird-days in 2003. It remained, however, the second commonest leaf warbler. In 2011, the peak count of Eastern Crowned Warbler on Eocheong was eight, and the total of 61 bird-days meant it ranked fifth in abundance amongst leaf warblers. A similar decline is apparent on Socheong, where there was a peak count of 250 in 2004 but of only 27 in 2010 with a total of 73 bird-days (see Chapter 9, Table 9.2). This was despite much increased coverage in the latter year. While Black-faced Bunting remains numerous, the number of Yellow-breasted Bunting recorded on YSBR islands has also declined greatly in recent years. On Eocheong, there were 80% fewer Yellow-breasted Bunting bird-days in 2003 compared to 2011. The rapid decline in Yellow-breasted Bunting, observed in several parts of its range, has already resulted in its assessment as globally Vulnerable, while the more poorly-known Eastern Crowned Warbler remains as Least Concern. Like many of the passerines of East Asia, its population is ―suspected to be stable in the absence of evidence for any declines or substantial threats‖ (BirdLife International 2011). While the Barn Swallow, Olive-backed Pipit and Yellow-breasted Bunting have a wide breeding distribution, Ashy Minivet, Eastern Crowned Warbler and Pale-legged Leaf Warbler are all forest-specialists, confined as breeding species to a narrow region of northeast Asia. All are complete migrants to the ROK and to the region. Analysis of datasets from other islands and other years, increased monitoring effort, improved sharing of information and regional collaboration are all essential in determining whether declines in such species are genuine and sustained (and more likely affecting complete migrants or species of certain habitats and regions), or whether they too 263

might plausibly be an artifact of different weather systems during migration periods between years. Either way, migrating birds depend on the integrity of multiple stopover sites (Shamoun-Baranes et al., 2010b), and successful migration for passerine birds depends largely on the quality of stopover habitats (Ktitorov et al. 2010). Once they have crossed the Yellow Sea to reach an island in the YSBR, birds need to be able to find correct habitat if they are to survive and to achieve the fuel deposition rate necessary for further successful migration (Chernetsov 2006). On days with certain weather conditions, and each year through northward (and southward) migration, Eocheong regularly supports many thousands of landbird and several species of global conservation concern. Improved management of Eocheong and other migration hotspots is therefore essential if the ROK is to meet agreed targets for the reduction in the rate of biodiversity loss, and the conservation status of those species most in decline is to be improved and sustained.

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CHAPTER 9

GENERAL DISCUSSION: TOWARDS MEETING TARGET 19 OF THE CBD STRATEGIC PLAN FOR CONSERVATION OF BIODIVERSITY 2011-2020

9.1 BACKGROUND 9.1.1 Aims The primary aim of the present study is the improvement of conservation opportunities for the avian biodiversity of the Republic of Korea (ROK), most especially within the ROK part of the Yellow Sea. The research aims of each chapter have been framed within existing national commitments to conservation conventions, and the 2020 deadline provided by the CBD Strategic Plan for Conservation of Biodiversity (2011-2020) (Chapter 1, Section 1.1.2). The main focus of the present chapter is Target 19. Target 19 calls for ―knowledge, the science base and technologies relating to biodiversity, its values, functioning, status and trends, and the consequences of its loss… improved, widely shared …and applied‖. It thus builds on other Targets (including 5 and 12) set out within the same CBD Strategic Plan. Chapter 9 therefore discusses some of the main findings of the previous chapters; identifies further research questions; and recommends several pragmatic steps on information gathering and sharing that can be taken towards meeting Target 19. This includes recommending the development of a species-based Decrease Susceptibility Index (DSI).

9.1.2 Improved Knowledge As described in previous studies (Moores et al. 2001, Barter 2002, BirdLife International 2003) and in the present study, the Yellow Sea is a densely-populated region that is critical for the conservation of a large number of migratory bird species. The present study has provided an improved understanding of the historical and contemporary abundance and distribution of bird species within the ROK and the YSBR. It has identified large-scale effects that influence abundance and distribution, and contributed to the knowledge base on migration strategies and phenology (Chapters 3-8). Throughout, it has been shown how this improved knowledge base can 265

be used to help focus future research effort and to help analyse existing data sets with increased confidence.

9.1.3 Information Sharing To meet Target 19, improvements in the knowledge base also need to be more widely shared. This requires increasing the accessibility of information for stakeholders, including local communities, domestic and international Non- governmental organisations (NGOs), development bodies and decision-makers. To date, there has been a paucity of research on avian biodiversity in the YSBR and in the ROK. Some of the information and data that have been gathered are difficult to access and interpret - either being closed to public review or unsupported by a detailed description of methodology. In addition, much of that which has been made publicly available is written in technical language, and often only in English or only in Korean, thus excluding one or more groups of stakeholder. Regionally too, there are no formal structures in place, either within or outside of the East Asian-Australasian Flyway (EAAF), for translation of key texts on avian biodiversity between the main languages of East Asia. For example, several waterbird species that are largely confined to East Asia are already covered by international species action plans (e.g. Chan et al. 2010, Zöckler et al. 2010c). However, even these action plans have been published in full only in English, and there is no clear protocol or financial support for translation, or for sharing information on these species with a greater range of stakeholders. Although Birds Korea publications cited in the present study (including Moores et al. 2008 and Birds Korea 2010a) are bilingual, much conservation literature remains poorly- understood, even by many of the environmental organisations within the ROK (pers. obs.). There is therefore a need to increase the quantity, quality and accessibility of information in both English and Korean, and where appropriate, also in other main languages of the region (including Russian, Chinese and Japanese). Mechanisms to increase information exchange need to be strengthened (see below).

9.1.4 Advocacy and Policy Target 19 also calls for improvements in the application of knowledge to policy and decision-making. Improvement in the quality of information and its accessibility supports, but does not necessarily result in, improvements in policy. Decision-makers in the ROK already have access to much high-quality information, through the 266

establishment of several dedicated institutions (including the NIER and NIBR) and through hosting of international meetings focused on biodiversity conservation. Such meetings have included the Tenth Conference of the Parties to the Ramsar Convention in 2008, and will include the IUCN World Conservation Congress in September 2012 (MOE 2012). However, the present study (largely conducted between 2006 and 2011) finds little evidence of improvements in the use of the knowledge base by ROK government bodies or in policies for biodiversity conservation during the same period. For example, both ROK (2009) and MOE (2012) underestimate the area of tidal-flat lost to reclamation and exaggerate the area of intertidal wetland that presently remains (Chapter 3). Neither contains any clear reference to the rate of decline in any bird species, either due to reclamation or other causes. This is even though substantial declines in several bird species are indicated by data gathered during the annual MOE Census (1999-2010) and in NIBR (2010), which have both been analysed in the present study. Moreover, while CBD Secretariat (2010) identified habitat change as the leading driver of biodiversity globally, the Act on the Conservation and Use of Biodiversity (newly enacted in January 2012: MOE 2012) does not provide any legal impediment to habitat change (see Birds Korea 2010b). Even the proceedings of an International Symposium on Ecological Site Development of Saemangeum (MOE 2011) did not include any assessment of the current ecological status of tidal-flats within the Saemangeum reclamation area or any clear reference to declines in shorebirds caused by the reclamation project. This is despite earlier MOE data that clarified the national and international importance of the Saemangeum Estuarine System (SES) (Barter 2002; Yi 2003, 2004); the easily-accessible data contained in Saemangeum Shorebird Monitoring Program (SSMP) reports (Moores et al. 2006, 2007, 2008); and ongoing national government support for the Korean Shorebird Network. The Korea Shorebird Network (2011) reported that fewer than 10,000 shorebirds were counted within Saemangeum in September 2010. This compares to NIER research that found 151,000-192,000 shorebirds there during southward migration between 2002 and 2004, >68,000 in 2005 and 39,000 in 2006 (NIER unpublished data). As the national ministers of the Ministry of Environment and of the Ministry of Land, Transport and Maritime Affairs (responsible for modifying much of the wetland) both provided forewords to Korea Shorebird Network (2011), it is apparent that these data (and thus shorebird declines) were known to both ministries. Similarly, there are several institutions and initiatives supported by ROK government 267

bodies that are working towards Yellow Sea conservation. These should be well- placed to generate, share and analyse data and to support improvements in conservation policy. These include the Yellow Sea Large Marine Ecosystem (YSLME) Project and the office of the East Asian-Australasian Flyway Partnership (EAAFP), housed in Incheon. Neither, however, are referred to in the section on ―Plans and Efforts for Biodiversity Conservation‖ in MOE (2012). Improvements in the knowledge base on biodiversity conservation therefore need to be accompanied by an increase in responsible and honest advocacy that strives to minimize biases, as called for by Noss (1999). Within the ROK, advocacy for the environment is largely being undertaken by NGOs. To be effective and to influence policy, NGO advocacy in the ROK requires adequate popular and political support and appropriate structures. Successful NGO advocacy therefore needs to help build consensus among groups of stakeholders and to utilise existing conservation structures (Moores 2004). The size and influence of civil society in the ROK grew from the late 1980s through the 1990s (Lee 2000), and by 2011 there were more than 9,900 registered non-profit NGOs in the ROK (Kim 2011b). However, although NGO influence on national policies increased in some areas, such influence was limited, as elsewhere, due to a lack of capacity when compared with development bodies (Rootes 2004). Moreover, confrontation between liberal civic groups (including most environmental NGOs) and politically-conservative civic groups in the ROK escalated in the mid-late 2000s, as did conflict between many civic organisations and the ruling administration. This has resulted in an increased politicisation of many NGOs (Kim 2011b) and a reduction in many organisations‘ support-base and influence. Moreover, despite the growth in number, there is still only irregular collaboration between domestic NGOs and the International Organisation Partners (IOPs) of conservation conventions. Uniquely among the 34 member nations of the Convention on the Organisation for Economic Cooperation and Development, there is still no partner organisation in the ROK to BirdLife International or the World Wide Fund for Nature, nor any office of Wetlands International. This has hindered the active participation of domestic NGOs in international meetings and flyway-wide initiatives, such as the EAAFP. Confronted by language difficulties and lacking direct IOP support, only Birds Korea (among domestic NGOs) has actively promoted IOP-led initiatives in the ROK, including Birdlife-identified Important Bird Areas (IBAs) and IUCN Key Biodiversity Areas. Few NGOs have used convention texts in their advocacy for site or 268

species-conservation either. It has therefore been especially difficult for environmental NGOs in the ROK to build consensus on conservation priorities (either within the ROK or within the region). In turn, this lack of consensus and the limited use by domestic NGOs of existing conservation structures appears to reduce political opportunity for decision-makers working for conservation. Without NGO support for such initiatives, designation of IBAs as nationally-protected areas, or the cancellation of development projects in order to fulfil existing obligations under Ramsar or the CBD Strategic Plan would, in most cases, be unsupported by local stakeholders. They would therefore be politically costly for decision-makers. Improvements in the capacity of domestic NGOs is therefore required in order to help build consensus, to identify shared conservation priorities and to improve the effectiveness of NGO advocacy (Moores 2004). Although only alluded to in Chapters 1 and 4, the need for scientific research and unbiased data to support honest and responsible advocacy by NGOs and other bodies is a major part of the context and rationale of the present study. Based on some of the preliminary findings of the present research, Birds Korea has already made media releases; met with local stakeholders and with political representatives (including diplomats and ministry officials); provided commentary on laws; and worked towards building scientific consensus around existing conservation initiatives and conventions. There has been no formal analysis performed in the ROK to measure the relative success of each of these advocacy approaches, so that such an analysis remains outside the scope of this study. However, several conservation successes have been achieved when best information has been provided openly in a timely and apolitical manner, and in ways that can increase political opportunity for those decision-makers who are working towards conservation. For example, the SSMP was a scientific program, designed to gather robust data on shorebirds within the Saemangeum Estuarine System, the Geum Estuary and Gomso Bay (Chapter 4). It was also developed as an advocacy tool. It was built on concerns over global shorebird declines (summarised by Stroud 2006), and concerns over the likely impacts of the Saemangeum reclamation on shorebirds of the EAAF (Moores 1999b, Barter 2002, Battley 2002, Barter 2006). The SSMP incorporated research on the impacts of the reclamation on local fishing communities (Moores et al. 2008) and a national shorebird survey (Chapter 5). It was also designed to support the Monitoring Yellow Sea Migrants in Australia program (Moores et al. 2008, Rogers et al. 2009). It was therefore able to inform and support local, national and international 269

advocacy efforts by Birds Korea, the Australasian Wader Studies Group (within BirdLife Australia) and other conservation organisations (both government and NGO). The SSMP also included several symposia, workshops (both in the ROK and in Australia) and media releases. These provided audiences with up-to-date scientific information on the impacts of reclamation on shorebirds and on local communities, both in Korean and English (and on occasion in other languages, including Chinese and Japanese). Research results and preliminary analyses were also published in hard copy and online in bilingual reader-friendly annual reports (Moores et al. 2006, 2007, 2008). The report in 2008 summarised preliminary data from all three years of research, and confirmed that the Saemangeum reclamation had resulted in massive shorebird declines locally, nationally and in the case of Great Knot, in its total population. It contained forewords by a leading academic specialising on Korean tidal-flats and by the Chief Executive of BirdLife International. Moreover, it was published in time to circulate widely to NGO and government organisation participants as well as to media at the Ramsar COP10 (ROK, October 2008). It cited Ramsar texts, explained relevant legal frameworks, and fulfilled the role of a civil society response to Ramsar Resolution IX.15 (which had earlier requested information from the ROK government on the impacts of the Saemangeum reclamation on waterbirds). The SSMP thus made accessible the best information in the most appropriate manner, at the most appropriate time. As a result, it contributed to improved conservation opportunities of two internationally important wetlands, helping to win cancellation of the reclamation of the Geum Estuary and part Ramsar-designation of Gomso Bay. The value of the SSMP as a research and advocacy tool was also honoured by leaders of Korean Civil Society through their recognition of Birds Korea as a national ―Leading Light‖ in late 2008 (Birds Korea 2008). The SSMP therefore provides a potentially useful example of several approaches that (used in tandem) might also work in helping the ROK to meet the Targets of the CBD Strategic Plan by 2020. However, research and advocacy for the SSMP were both highly labour and resource intensive. The SSMP did not succeed in conserving shorebird populations dependent on the SES; it had little government input within the ROK (despite invitations to the NIER and NIBR to participate), and as noted above the SSMP results have not thus far been cited in government publications. Its influence on mid-long term conservation policy has apparently been limited. 270

Thus, this chapter clarifies the need to synthesise existing knowledge and to develop approaches that can help to increase the influence of improved information on policy and on legal frameworks. Towards this end, the following sections discuss some of the strengths and weaknesses of the present research. They also identify some remaining research questions, and among several recommendations, propose the development of the Decrease Susceptibility Index (DSI) as an easily-accessible framework for organising, sharing and updating current knowledge.

9.2 STRENGTHS AND WEAKENESSES OF THE PRESENT RESEARCH 9.2.1 Historical and Contemporary Declines In order to develop appropriate biodiversity conservation policies, it is first necessary to identify if there has been a loss of biodiversity; to determine which species and habitats have been most affected; and then to identify probable drivers of decline. The primary research aim of the present study, therefore, was to determine whether there are indications of declines in bird species‘ richness and abundance within the past century, and whether these declines appear to be continuing. We predicted that more species of bird in general and more species of global conservation concern in particular would show evidence of decrease than increase. Ornithological literature was reviewed and major potential sources of bias and variability within datasets were identified. The present study for the first time is able to confirm that many bird species in the ROK have declined. It provides a baseline on which recent population trends can also start to be measured. Using different methodologies to detect changes against different time baselines we demonstrated that: 1. During the past century, a third of regularly occurring bird species showed evidence of substantial decline in the ROK, and 24 out of 50 species of global conservation concern also declined. Rapid and recent declines in many more species are suspected (Chapter 2), and through our analysis of government research data in NIBR (2010) declines during the present decade have also been confirmed in 15 out of 20 widespread species. 2. In line with our predictions, there have been substantial declines in several species of migratory shorebird dependent on intertidal wetland, both at the national population level and on the EAAF (Chapters 3 & 5). 3. Seabirds at sea in the YSBR and the Yellow Sea remain poorly-known (Chapter 6), and outside of the scope of most ongoing initiatives including the 271

YSLME Project and national government assessments of marine biodiversity (MOMAF 2006). This study provides the first count data of seabirds at sea in the Yellow Sea throughout an annual cycle and helps to identify several parameters influencing distribution. There are numerous threats to seabirds in the YSBR and Yellow Sea (see Chapter 1, Section 1.5) and this study identified at least one breeding and one overwintering species that have declined (Ancient Murrelet and Red-throated Loon, both largely from the ornithological literature). 4. Landbirds migrating across the YSBR are exposed to a range of threats, at the large scale (including climate change) and at the level of stopover site. This study for the first time identifies major migration routes across the YSBR and identifies a relationship between the large-scale influences of geography and weather systems and the numbers of migrant birds counted at migration ―hotspots‖. Based on the patchy datasets and threads of evidence that are available, the study suggests that several species of migratory landbird might be undergoing rapid decline. It is considered plausible that if such declines are taking place that they can be attributed, at least in part, to changes in the breeding range (Chapters 7 & 8).

9.2.2 The Three Main habitats of the YSBR 9.2.2.1 Intertidal wetland and Shorebirds The present study predicted that the loss of the SES (and other internationally important wetlands) to reclamation would lead to a substantial decline in some shorebird species. We predicted that these declines would be detectable both in the ROK during northwards migration and elsewhere on the EAAF during the boreal winter. The research supports these predictions. The present study was not able to build on long-term ROK datasets or on a detailed knowledge of sites or species. Published shorebird population estimates for many migratory shorebird species of the EAAF too are based on an incomplete understanding of actual abundance and distribution. Some areas within the flyway remain poorly surveyed, and numbers of individuals of each species are annually influenced by breeding success and the rate of recruitment. Within the ROK, sites used by large numbers of staging shorebirds have also been undergoing substantial change, in many cases for several decades or more. There are too few data with which to 272

develop even coarse estimates of the numbers of shorebirds that staged in the ROK before the late 1980s. Although there are rather more data for the late 1990s and early 2000s, all counts have been limited in time and scope, and there are undescribed differences in counting methodology and incomplete descriptions of changes to sites. Moreover, there are no baseline studies focused either on the shorebird carrying capacity of sites within the YSBR, or on the energetics of shorebirds staging in the ROK. It was therefore considered inappropriate to base the present study on a theoretical framework that assumed that increased local densities would result in population declines or to try to estimate population change against habitat loss. Instead the present study was focused largely on improving count accuracy; on confirming migration phenology; and on analysing changes in numbers and status that could be identified through a conservative interpretation of the ornithological literature and fieldwork. Despite the limitations of available data, the three-year SSMP documented shorebird declines following closure of the Saemangeum seawall in 2006. Declines were not offset by corresponding increases in shorebird numbers at adjacent sites or elsewhere in the ROK. There was no evidence that the majority of shorebirds were able to relocate once this optimal staging site had been reclaimed (Chapters 4 and 5). Rather, there is a substantial body of evidence (from related studies in Australia and elsewhere on the EAAF) that the "missing" birds have perished and that several species have declined. Moreover, the research suggests that shorebird declines in the ROK have likely been ongoing for several decades at least. One species (Spoon-billed Sandpiper) was therefore assessed as ―Decreasing‖, and a further 21 shorebird species were assessed as having a Negative Population Trend in the ROK during the past century (Chapter 2 and Appendix). In the 2000s almost all remaining internationally important shorebird sites were adversely affected directly or indirectly by reclamation (Chapter 5). Decreases or probable decreases at the national level of at least 12 migratory shorebird species that depend on intertidal wetland were detected (Chapters 4 and 5). These include six species now assessed as being of global conservation concern, out of a total of 21 shorebird species found within the ROK in internationally important concentrations (Table 9.1). Robust monitoring programs and analyses from outside of the ROK (Rogers et al. 2009, Amano et al. 2010, Garnett et al. 2011, BirdLife International 2011) have identified declines in at least seven of the same shorebird species in other 273

parts of the EAAF: Kentish Plover, Mongolian Plover, Black-tailed Godwit, Nordmann‘s Greenshank, Ruddy Turnstone, Great Knot, and Spoon-billed Sandpiper. Declines in additional species (including Common Greenshank) have been identified by others (Wilson et al. 2011, N. Davidson in lit. 2010, and D. Rogers in lit. 2011). Well-established long-term monitoring programs in Australia (and perhaps elsewhere in the EAAF) will likely provide by 2020 the firmest basis for the identification of long-term population trends in many of the shorebird species that stage in the ROK.

Table 9.1 National and regional population trends of shorebirds found in internationally important concentrations in the ROK during northward migration during the past 30 years and 10 years in the ROK and Japan, and in recent decades in the non-breeding season in Australia. Species Global Global Past Past Past Past Trend in Status Status 30 yrs 10 yrs 30 yrs 10 yrs Australia 1990s 2000s ROK ROK Japan Japan 10 Yrs

Far Eastern Oystercatcher Unknown (-) N/A N/A N/A Grey Plover + + - - Decreasing Kentish Plover - - - - N/A Mongolian Plover - - - - Decreasing Black-tailed Godwit NT Unknown - + + Decreasing Bar-tailed Godwit - + - - Decreasing Whimbrel + (+) + - Decreasing Eurasian Curlew NT + + + + N/A Far Eastern Curlew VU + (-) + - Decreasing Common Greenshank - (+) + - Unknown Nordmann‘s Greenshank EN EN - - N/A N/A N/A Terek Sandpiper + + + - (Decreasing) Grey-tailed Tattler - + + - Decreasing Ruddy Turnstone - - - - Decreasing Great Knot VU - - + + Decreasing Sanderling Unknown (+) + + Unknown Red-necked Stint - - + - Unknown Sharp-tailed Sandpiper + - - + Unknown Dunlin - - - - N/A Spoon-billed Sandpiper VU CR - - N/A N/A N/A Broad-billed Sandpiper Unknown + + + Unknown Notes: use of ―+‖ indicates probable increase; use of ―-‖ denotes probable decrease; parentheses ( ) indicate weak agreement between sources; N/A, here and in all subsequent tables indicates ―Not Applicable‖. Sources: Global (Conservation) Status from BirdLife International 2011; ROK 30-year trend based on Tables 4.11, 5.3.2 & 5.3.4, and for Red-necked Stint from Moores 1999(b); ROK 10-year trend based on Tables 4.3.5.1.2 & Tables 5.3.2 & 5.3.4; Japan 30-year and 10-yr trends from Table 1 in Amano et al. (2010); Australia trends from Garnett et al. (2011) & for North-western Australia from Rogers et al. (2009).

Future Research The present study helps to identify several future research priorities for improving knowledge of the impacts of reclamation on populations of migratory shorebirds in the YSBR. In order to meet Target 19: 1. Detailed and robust studies are required to measure the habitat needs, feeding ecology and energy budgets of many of the YSBR‘s shorebird species. These include the Critically Endangered Spoon-billed Sandpiper, the Endangered 274

Nordmann‘s Greenshank and the Far Eastern Oystercatcher (this latter taxon having recently been assessed as specifically distinct from Eurasian Oystercatcher Haematopus ostralegus: Livezey 2010). There has been no detailed feeding or habitat use study conducted on any of these three taxa anywhere within their ranges, and all three have small global populations that depend largely on the Yellow Sea during part of their life-cycle. 2. More research and analysis is required to determine with greater confidence whether some species are more susceptible to rapid decline than others following habitat degradation and loss (so that declines in these species are easier to detect by monitoring programs conducted over a few years). Such differences potentially have major implications for project design, data interpretation and population models. The mechanisms driving shorebird declines have been researched in other regions and are broadly understood (see Chapter 3). Burton et al. (2006) also provided empirical evidence that habitat loss can impact individual fitness in a shorebird population. Their study investigated the impact of the sudden loss of 200ha of intertidal wetland by impoundment on a population of c. 300 Common Redshank Tringa totanus, 49% of which were marked. Their research entailed a decade of regular counting of the affected site and adjacent sites before impoundment, and for >3 years after impoundment. By contrast, the present research aimed to measure within three years the impacts of a progressive loss of tidal-flat >150 times larger than in their study, affecting several hundred thousand shorebirds. Massive declines in shorebirds within the SES, and some displacement to adjacent sites were detected. However, we did not detect a sudden loss to the SES of all species once the seawall was closed. Instead, there were a range of responses, which were not shared by all species. Analysis of our data does not yet provide a method with which to explain with confidence the species-level responses we observed. The SES, in common with many intertidal wetlands, supported a high diversity of shorebird species. Although some species in 2006 (and during prior research) apparently preferred certain parts of the SES for feeding and roosting, there was much overlap in the distribution of the majority of species. A few species (e.g. Kentish Plover) declined rapidly in number in the years before seawall closure; others apparently declined much more rapidly following seawall closure. Great Knot was one of the species that 275

declined rapidly, as predicted earlier (Moores 1999b, 2003a). The species is a mollusc specialist dependent on extensive estuarine systems (Battley 2002, Rogers 2006). The reduction in tidal exchange within the SES caused by seawall closure in 2006 resulted in a loss of tidal-range and a mass die-off of shellfish (Rogers et al. 2006). The rapid degradation of a formerly optimal staging site thus resulted in the loss of the majority of Great Knot. There was also a 46% decline in Great Knot at other internationally important sites in the ROK (including at all those sites that were formerly important for the species) between 1998 and 2008 (Chapter 5). Many of these other sites had also been affected by reclamation within the same decade. As the displaced birds could not successfully relocate to other suitable habitat in the ROK, a rapid decline in the national population of Great Knot took place. A large decline was also detected in north-west Australia coincident with the declines in the ROK (Rogers et al. 2009). Other species, however, declined more slowly or later (e.g. Dunlin) than Great Knot (Chapter 4). Moreover, declines were not detected in a few shorebird species that were dependent on the same sites and habitats, during either the SSMP or the national shorebird count. The data from the ROK which are available to make an assessment over a two decade period are inadequate for robust analysis. However, they suggest that several larger and one medium-sized shorebird species in the ROK (Grey Plover, Whimbrel, Eurasian Curlew, Far Eastern Curlew and Terek Sandpiper) have shown a less rapid decline than most smaller species, or appear to have increased. For example, the count data suggest Grey Plover increased in the ROK between 1988 and 2008 by 4%, even though there have been large declines in the Grey Plover population that spends the boreal winter in Australia, estimated at 30-49% in three generations (Garnett et al. 2011). More than 90% of the EAAF‘s breeding population of Grey Plover is supported by the Yellow Sea during northward migration, and five of the top 12 sites for the species in the Yellow Sea are in the ROK (Barter 2002). All five of these ROK sites have been affected by reclamation. It is likely that reclamation in the ROK has therefore contributed to declines in the population of Grey Plover that spends the austral summer in Australia, while not yet causing apparent declines in the ROK. The decline in Far Eastern Curlew in Australia is also well documented, including within a core non-breeding area (Moreton Bay: 276

Wilson et al. 2011); within a major staging area (north-west Australia: Rogers et al. 2009); and at the population level (Garnett et al. 2011, BirdLife International 2011). Large numbers of Far Eastern Curlew also stage in the ROK (including birds marked in Australia), with internationally important concentrations at many of the same sites that have been affected by reclamation. The increase in Far Eastern Curlew recorded between May 1998 and May 2008 outside of the SSMP Study Region represented a third of the Far Eastern Curlew lost to it, based on peak counts. It is therefore possible that these included some of the birds displaced by the Saemangeum reclamation. However, while overall counts of Far Eastern Curlew within the SSMP Study Region declined, mid-May counts there showed a large increase between 2006 and 2008. One possibility suggested by our data is that larger shorebirds, which tend to be longer-lived, might be more likely to suspend migration than smaller shorebirds if they are unable to find sufficient food during northward migration. Species with shorter life-spans might be more prepared to risk continued northwards migration without a complete load of fuel as they have fewer potential breeding opportunities in their lifetime. Thus, it was suggested in Chapter 4 that the increase in Grey Plover and Eurasian Curlew within the SSMP Study Region might have been at least in part a result of delayed migration, so that overwintering birds overlapped more obviously in migration timing with birds that were arriving from further south. Similarly, it is possible that total numbers of Far Eastern Curlew have declined substantially in the ROK during the past two decades, but that this underlying trend was concealed in our counts by delayed northward migration leading to higher numbers still present in May (as May counts were used for the analysis in Chapter 5). Further research, with counting continued over a longer period, is required to assess whether reclamation tends to cause more migratory shorebirds to delay migration or to remain in the Yellow Sea (and other non-breeding areas) through the boreal summer each year instead of continuing on to the breeding grounds. If this is the main cause of apparent anomalies between the SSMP data and trends detected in Australia in the same species, then declines in these species will likely become increasingly apparent in the ROK in the near-future. 3. Shorebird monitoring of YSBR sites is required during the boreal winter and summer, in addition to during migration periods. First, such monitoring is 277

required to determine whether species suspend migration in response to reclamation (as above), and whether rates of decline are experienced equally by overwintering and staging populations of the same species. Second, it is necessary to determine which species routinely oversummer in the Yellow Sea. A hypothesis on the acceleration in decline of Spoon-billed Sandpiper proposed by Zöckler et al. (2010a, 2010b) depends in part on the assumption that many immature birds remain throughout the boreal summer in areas also used by the species during the boreal winter. This would expose immature birds to a greater risk from hunting pressure than adult birds. However, the SSMP also recorded several Second Calendar-year Spoon-billed Sandpipers. At least part of this non-breeding population therefore reaches the Yellow Sea during migration. Research is required to determine whether some Spoon- billed Sandpiper oversummer in the Yellow Sea, and whether this exposes the species to additional environmental factors that might be contributing to their decline. In summary, large-scale reclamation results in declines in shorebirds. The mechanisms driving declines in some species can be inferred from existing knowledge of shorebird biology. It appears likely, however, that the research presented in Chapters 4 and 5 was too brief to detect the full extent of declines in many shorebird species, between 2006 and 2008 or between decades. This is because it was focused on only five seasons of northward migration (1988, 1998 and 2006-2008) and the fieldwork period did not extend into the boreal summer (June) to assess numbers of shorebirds, especially late-migrating species that failed to migrate on schedule.

9.2.2.3 Seabirds in marine waters There has been insufficient research conducted on the abundance and distribution of seabirds at sea (or at colonies) to identify population trends in most seabird species in the YSBR. The research provided evidence that some Laridae (gulls) populations were previously overlooked (Chapter 2) and are now very numerous within the YSBR (Chapter 6). However, as with shorebirds in intertidal habitats, different species of Laridae have responsed differently to potential drivers of decline. The more abundant gull species (including Black-tailed Gull and Vega Gull) tended to be concentrated in areas of mariculture and around fishing boats in the non-breeding season. As in other regions (see Furness et al. 1992), these gull species were therefore able to exploit 278

fishery practices that have been described as unsustainable in the Yellow Sea by UNDP-GEF (2007). In contrast, the only two gull species that do not exploit fisheries and are dependent on intertidal wetland in the non-breeding season (Saunders‘s Gull and Relict Gull) are both globally Vulnerable (BirdLife International 2011). Over-exploitation of marine waters and pollution are likely to be leading to population declines in some seabird species. A few species in the YSBR appear to be especially susceptible to fouling by oil including Black-tailed Gull, three loon species and Ancient Murrelet (Birds Korea 2010a). Although there is a paucity of data, the present research presented a hypothesis for large declines that have been measured by Schmutz et al. (2009) in Alaska-breeding Red-throated Loon. As the species migrates and winters along the east and south coasts of the ROK, it is likely to be exposed to higher-levels of pollution than Yellow-billed Loon, which also breeds in Alaska but largely avoids the ROK east and south coasts by migrating overland to reach the YSBR (Chapter 6). Fieldwork also appeared to support the Negative National Conservation Status assessment of Ancient Murrelet provided in Chapter 2. In addition to reduced numbers found breeding during the past decade (see Section 2.5.7.8), the peak count of Ancient Murrelet recorded during 150 ferry journeys by the author in the YSBR was only 10% of the count of 3,000 Ancient Murrelet in December 1999 in inner Gyeonggi Bay reported by Park (2002). This is even though the present study included 72 ferry journeys through Gyeonggi Bay between 2003 and 2010.

Future Research Future research on seabirds at sea will depend largely on the availability of sufficient resources. Ideally, experienced counters need to be deployed regularly using appropriate vessels. Pragmatically, most survey effort will likely depend largely or in part on vessels of opportunity. In both cases, in order to meet Target 19: 1. Transect counts need to be repeated along or close to the existing Northern and Southern Transect routes. This is so that sufficient data can be made available for statistical analysis of seasonal distribution and population density. 2. Additional transects need to be counted, so that mapping of seabird distribution and population density across the whole of the YSBR/Yellow Sea can be achieved. 3. Identification of key seabird feeding areas has enormous implications for seabird conservation. The influence on seabird distribution of Surface Cold 279

Water Patches, the Yellow Sea Cold Water Mass, and tidal-fronts therefore needs to be investigated. Research by Lu et al. (2009) showed that strong tidal mixing plays an important role in vertical circulation in the Yellow Sea, and that the Yellow Sea Cold Water Mass is fringed by tidal mixing fronts which separate the cold, stratified water at the offshore side from the warm, well- mixed, shallow water at the other side. Such areas experience active vertical circulation, and have been identified in at least three areas of ROK waters, including close to (and sometimes crossed by) the Northern and Southern Transects described in Chapter 6. Large concentrations of seabirds (including Black-legged Kittiwake and Common Tern) were observed several times during the present research in sea areas where there was a sharp division between turbid and clear water and localised sea-swell, indicating upwelling. In the Irish Sea, Begg & Reid (1997) found that some seabird species (including Manx Shearwater Puffinus puffinus and two species of Alcidae) were distributed along a shallow sea tidal mixing front in relation to sea- surface temperatures and salinity. As the Yellow Sea Cold Water Mass and Surface Cold Water Patches are predictable phenomena it seems possible that they might influence the distribution of feeding seabirds in the Yellow Sea. 4. The potential impacts (both direct and indirect) of fisheries practices on seabird abundance and distribution needs to be investigated and methods to reduce negative impacts need to be developed.

9.2.2.4. Migratory landbirds on offshore islands Before the present study, no research in the ROK had described the influences of geography and weather on migratory landbirds during crossing of the Yellow Sea. The results (presented in Chapters 7 & 8) support our predictions on channelled migration, north-south differences in species‘ composition and abundance, and on wind-drift. The research also confirmed the importance of offshore islands to the research and conservation of migratory landbirds. Between 30,000 and 77,000 landbirds were estimated to have used Socheong Island during northward migration in 2010 (Chapter 7); and based on the sum of peak counts, >7,400 birds were recorded on Eocheong in only 33 days of survey in April and May 2011 (Chapter 8). The location of these islands relative to the two migration corridors influenced the ways in which birds used them: for orientation or for gaining altitude, for short staging or for longer staging. The 280

breeding distribution of a large number of species suggests that these migration corridors have likely existed for a long time (i.e. millennia). It is therefore likely that species‘ migration routes have, at least in part, evolved to take advantage of offshore islands. All islands visited for this study had experienced and were undergoing extensive habitat degradation, including the concreting of streams on Socheong, and the construction of new piers and boardwalks along the narrow strip of intertidal wetland on Eocheong. Feral cats had also been introduced on many islands, to help control the abundant populations of Brown Rat. Thus the threats to staging migrants have increased, and concomitantly the culture, beauty and ecotourism potential of many islands have been rapidly eroded (Birds Korea 2010a). It appears possible that habitat loss and degradation on offshore islands might contribute to population declines in a few species that are most dependent on them during migration, both through increased mortality during stopover and subsequently through reduced fitness on arrival in the breeding areas. Despite substantial differences in survey effort and weather between years, large decreases within a single decade were suggested in ten or more landbird species that were not attributed to habitat changes on the islands themselves and which also seemed, at least in some cases, to be greater than might be expected due to differences in weather patterns. Within the narrow time-frame of the present research, decreases were also suspected in a further 20-30 species. The ten species suggesting the strongest evidence of decrease are listed in Table 9.2. Declines in several of these species have been detected in mainland ROK. Analysis of data in NIBR (2010) suggests that, in 406 randomly-selected quadrats, Black-naped Oriole decreased by 57% in 16 years and Barn Swallow decreased by 27% in 11 years. Barn Swallow, Ashy Minivet, Grey-streaked Flycatcher Muscicapa griseisticta and Yellow-breasted Bunting were also shown to have undergone long-term declines by the Four Assessments. Declines in Yellow-breasted Bunting have also already been detected in other parts of its range (BirdLife International 2011), leading to its assessment as globally Vulnerable. Six of the declining species identified in Table 9.2 were not detected as declining by the Four Assessments, however. It remains unclear whether this is because of the conservative nature of that methodology, or because the declines are comparatively recent, or because the species are not in decline at the national level.

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Table 9.2 Peak counts and bird-days of ten species of landbird on Eocheong and Socheong with the strongest evidence of decrease since 2002. EOCHEONG SOCHEONG Year 2002 2003 2004-2006 2011 2011 2003- 2010 2007 Type of Count Peak Peak Peak Peak % Peak Count % of Count Count Count Count of 2003 2003- 2007 Eastern Crowned Warbler 200 40 120 8 20% 125 10% Chinese Sparrowhawk 75 37 220 17 40% 200 9% Yellow-breasted Bunting 15 20 40 8 31% 70 40% Black-naped Oriole 25 50 75 19 58% 150 17% Ashy Minivet 300 60 30 18 29% 75 51% Asian Brown Flycatcher 25 40 40 17 42% 100 45% Grey-streaked Flycatcher 45 17 6 9 40% 30 80% Pale-legged Leaf Warbler 150 30 100 22 58% 80 68% Barn Swallow 300 75 250 35 43% 150 81% Siberian Blue Robin 15 20 6 18 85% 115 64% Note: In bold under Eocheong 2011, column ―% of 2003‖ is the percentage of that total recorded in 2011 compared with 2003, based on the mean of the peak count and the number of birds-days in both years. In bold under Socheong 2010, ―% 2003-2007‖ is the percentage of the peak count recorded in 2010 compared with peak counts recorded during less intensive survey during 2003-2007.

It is not possible to determine with confidence the drivers of decline that might be affecting the species in Table 9.2. However, Siberian Blue Robin Luscinia cyane is described as one of the few migrants adversely affected by oil palm expansion in Borneo by Phillipps & Phillipps (2009). In contrast, counts in Castelletta et al. (2006), Round & Brockelman (1998) and Maas et al. (2009) provide no strong evidence of decline in the other nine species caused by habitat change in their non-breeding range. However, this might not be unexpected when the difficulties of surveying large areas of habitat during the non-breeding season are considered. As mapped by Brazil (2009), all ten are complete migrants to the ROK and all breed on the Northeast Asian Mainland. Five of them have the centre of their global breeding distribution within eastern Amurland, Khabarovsk and Ussuriland; and all but Barn Swallow and Yellow- breasted Bunting are forest or forest-edge species. The Amur-Heilong basin and Ussuriland appear to form the core of the breeding range of many of the landbird species that migrate through the ROK (Chapters 7 & 8). This is an extensively forested region that largely avoided ice-cover during the Pleistocene glaciation, and as a result supports the most biologically diverse temperate mixed forest in Asia and possibly the world (Simonov & Dahmer 2008). A comparative study of trends in forest species in 282

North America and Europe by Mönkkönen & Welsh (1994) suggests that species dependent on forest in East Asia are likely to be sensitive to disturbance and habitat fragmentation. This is because fragmentation adversely affects birds that have evolved in and only experienced unfragmented conditions. This includes the avifauna of the Amur-Heilong basin. According to Simonov & Dahmer (2008) large areas of primary forest in the Amur-Heilong basin have in recent decades suffered increasing fragmentation caused by a range of human activities. These include extensive land use and change from natural wetland and river valley forest to farmland. There has also been an increased tendency of reduced rainfall and drought in part of the basin. Species that breed in wetlands (e.g. Yellow-breasted Bunting) and in forest in the Amur- Heilong Basin might therefore be in decline due to habitat loss and/or climate change. It is therefore plausible that changes in breeding areas might be contributing to population declines and reduced numbers of the same species recorded at YSBR migration hotspots.

Future Research To determine population trends and causes of those trends in the large number of migratory landbirds which are supported by the YBSR, and in order to meet Target 19: 1. More research, conducted with consistent methodology on a larger number of islands over a longer time-frame, is required in order to develop datasets fit for robust statistical analysis. Such analysis is required to determine with confidence which species are undergoing significant declines, and to test whether there are differences in the rate of decline between some species on islands in the Northern and Southern Crossings. 2. Further research is required to measure if habitat loss and degradation on hotspot islands has a substantial negative affect on individual landbirds and waterbirds. Such research could include mark and recapture studies, and comparative analysis of bird weights and staging times on islands with and without invasive alien predators, and on islands with low and with high levels of disturbance. 3. For the present study, the Yamashina Institute in Japan was contacted and several appeals for information on population trends in landbirds were made (though e-mails and regional English-language listservers, and at international meetings) to researchers in Japan, China and Russia as well as in the ROK. 283

However, there appears to be very little easily-accessible research from within East Asia on migration phenology, or on population trends of almost any landbird species. Further identification of potentially relevant literature is required, as too is analysis of long-term datasets, where they exist, from banding stations (e.g. in Japan) and breeding survey work. 4. Improved analysis of climate change and of other principal drivers of decline is required, both within the YSBR and the wider region.

9.3 RECOMMENDATIONS ON INFORMATION GATHERING AND SHARING The research (and conservation work by the author in East Asia since 1990) suggests that to meet Target 19 by 2020, multiple actions need to be undertaken by relevant stakeholders. Recommendations on information gathering and information sharing are provided below, in response to some of the challenges encountered during the present study. They are therefore likely to be of most relevance to researchers and the NGO community. They are based on three main assumptions: 1. That the most efficient use of resources is to increase the collective impact of existing research programs, conservation initiatives and organisations; 2. That improvements in information gathering and sharing will lead to increased opportunities for honest and responsible advocacy and for consensus and trust to develop among and between NGOs and other stakeholders (including government bodies); 3. Decision-makers intend to fulfill existing obligations under conservation conventions including the Aichi Biodiversity Targets. Especially if provided with increased political opportunity, descision-makers are thus willing to amend national policies and implement support programs in order to do so.

Recommendations on Information Gathering 1. The consistency of survey and monitoring approaches in the YSBR and throughout East Asia needs to be improved, so that datasets can be compared between research projects and between geographical regions. This includes the improved description of observer experience, count conditions, and any changes to count sites and adjacent areas. This process needs to be standardized and based on expert publications, guided by independent entities 284

(including the IUCN and national partners to BirdLife International) and could be supported by e.g. the EAAFP office and by local wetland and nature centres. 2. Survey and monitoring effort needs to be expanded, both temporally and geographically, within the YSBR, throughout East Asia, and along the EAAF. At present, there is little financial support available within the region for such research, despite the size and strength of several of the region‘s national economies. An increased monitoring effort will require an increase in government funding and greater support and coordination to be provided by backbone organizations (e.g. the IOPs) to ensure relevance to conservation aims. 3. Although ideally all bird species and species groups should be monitored, at present representative species groups, habitats and threats need to be selected for focused research, in order to facilitate rapid and robust analysis of trends and to identify causes of declines. Priority should therefore be given to the development of multi-species plans and frameworks, and to those species that are already listed in international agreements (including the Republic of Korea-Australia Migratory Bird Agreement).

Recommendations on Information Sharing 1. Much greater collaboration is required between researchers from different disciplines and from different regions. To help achieve this, relevant institutions and organizations need to be strengthened to facilitate their role as backbone organizations. For example, the YSLME project, or similar, should be established as a permanent project office, and mechanisms then need to be developed through this office to receive, to process and to share information on the YSBR and Yellow Sea biodiversity more widely. The EAAFP, or similar, needs greater support from private financial bodies, BirdLife partner organizations, IUCN members, and specialist organisations in order to become an independent, scientific body, able to coordinate and to help translate information on different species and species groups (and their habitats) throughout the EAAF. Local wetland and eco-centres also need to increase sharing of information generated both by themselves and by regional centres (such as the EAAFP office and YSLME project), with local communities, stakeholder groups, and decision-makers. 285

2. Easy to use, multilingual websites on key bird species and key species groups need to be established. These need to present shared information in all of the main languages used in the region (e.g. Korean, Chinese, Russian, Japanese and English). These dedicated websites need to be maintained and updated by existing organizations, including the EAAFP, partners to BirdLife International and other specialist organisations. To achieve this, funding needs to be provided by governments or private financiers so that national conservation organizations can translate relevant information from English into their national language and from the national language into English, for online sharing. 3. Regional expert committees need to be established and funded in order to review and to advise on records, on analysis approaches and on publications. Their findings and statements then need to be summarized and presented on dedicated multilingual websites (as above). In the short-term, these committees could be regional extensions of existing specialist organizations, including e.g. the AWSG (to review information on shorebirds), the International Crane Foundation (to review information on cranes) and specialist working groups established by the IUCN for other taxa. These committees need to be entrusted with the development of population estimates and conservation status assessments of relevant species groups, in support of work directed towards the same end already being conducted by Wetlands International and BirdLife International. 4. A mechanism needs to be established that better enables the input of information into a shared, easy-to-update online resource, on species and their population trends. This study therefore recommends the development of a Decrease Susceptibility Index (introduced in Section 2.6.4.2 and below) or similar framework.

9.4 THE DECREASE SUSCEPTIBILITY INDEX (DSI) 9.4.1 Rationale Both Amano et al. (2010) and N. Davidson (in lit. 2011) clarify the relationship between loss of intertidal wetland in the Yellow Sea and declines in shorebird populations dependent upon the same habitat. The results presented in Chapters 4 and 286

5 support their conclusions. However, the results also indicate that species of shorebird, even those sharing apparently similar habitat within the same wetlands, tended to decrease at different rates. Species-level declines did not appear to be caused by a single driver (e.g. habitat change) working on all species equally, but instead by a combination of factors that apparently affected each species differently. The evolutionary radiation of shorebirds is to large extent a radiation of the bill-tip organ (Piersma 2011), which has helped to define each species‘ niche and prey choice. Niche and prey choice helps define migration strategies and distribution, which in turn helps to increase or decrease each species‘ exposure to threats, including habitat change and hunting. To improve conservation opportunities for species in decline these complex relationships have thus far required the development of lengthy Single Species Action Plans, information fact-sheets and annotated checklists. However, this work is generally labour-intensive, time-consuming and (ultimately) often rather subjective. Moreover, the length and detail of many single-species assessments increases the difficulty of their translation or interpretation, rendering important research inaccessible to many stakeholders. Much information on species and their habitats in East Asia (written in one or more languages of the region) therefore remains omitted from regional conservation literature that has been written only in English. In order to help build understanding and consensus by 2020 among stakeholders within the ROK and regionally, a more rapid and easily-accessible method for organising and updating information on potential threats to species is required. In Chapter 2 (Section 2.3.6.2), some of the potential advantages of creating a Decrease Susceptibility Index (DSI) were suggested. As envisaged by the present study, the DSI could entail the organisation of information into a single spreadsheet. Each species would have its own row, and each threat to a species would have its own column (requiring translation only of single words or phrases for headings). By assessing each species and each threat through a points system (with a potential DSI Score of +1, zero, or -1 added to each column for each species for each variable), it would then become possible to identify those species most likely to be susceptible to decrease by those causes. The DSI could then, following further refinement, be used to store information on species within different areas and time-frames, enabling comparison between nations, regions and decades. Further, it could easily be updated with new information on factors influencing national or global population trends of either single species or of all species within the index. 287

9.4.2 Construction of a DSI for bird species in the Republic of Korea Information on each species gathered through the present research was used to provide an example of this approach. A DSI was constructed for all 365 regularly occurring species in the Republic of Korea, for the period 1910-2009. The DSI Scores generated through this index are provided for each of these species in the Appendix. The DSI and DSI Scores required extensive literature review; a selection of potential threats and factors (―variables‖); and testing of several of the component parts, through Pearson Chi-Square Tests and stepwise linear discriminant analysis. The CBD Secretariat (2010) identified five Principal Pressures driving global biodiversity loss (i.e. habitat change, over-exploitation, pollution, alien invasive species and climate change). The assumption that the same Principal Pressures have driven declines in many bird species in the ROK is supported by the present research and thus underlies the DSI presented here. Species entries on the IUCN Red List for which threats are classified reveal that at the global level habitat destruction is the overwhelming threat (Baillie et al. 2004). Moreover, habitat loss should be most dangerous to species that are ecologically specialized (Owens & Bennett 2000). A pragmatic definition of specialization can be found from long-term monitoring programs in Europe: bird species with more than 75% of their population occurring in one of eight main habitats were classified as specialists of that habitat (BirdLife International 2004). For the ROK, Chapters 4 and 5 provide the strongest evidence to date of declines in species caused by habitat loss, including in several species that are almost entirely dependent upon intertidal wetland. However, for the majority of species in the ROK, there are as yet inadequate data to assess either habitat use or species‘ level of habitat specialisation with a similar level of confidence. Instead, main habitat types (based on BirdLife International 2004) were first divided into several main categories (Table 9.3). A DSI Score of +1 was then given to main habitat types that were believed to have decreased in area or quality in the ROK during the past century (e.g. grasslands and rivers); and a DSI Score of -1 was given to habitats that had increased in area or quality during the same period (e.g. parklands and plantations).

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Table 9.3 Habitat Types used to assess Habitat Change, Level of Specialisation and Dependence on Natural or Artificial Habitats. Category Biome Habitat Type DSI Score Terrestrial Cool temperate forest 0 Natural and Near- Broad-leaved evergreen -1 natural Light woodland, Scrub, grassland, bare areas 1 Freshwater Heavily-vegetated wetlands 0 Still freshwater -1 Flowing freshwater 1 Brackish and Intertidal wetland 1 Marine Rocky shores, narrow beaches, sea (<2km from 1 shore) Open sea (>2km from shore) 1 Artificial and Heavily- Terrestrial Urban matrix -1 managed Parkland, temple complexes, heavily managed -1 areas Plantations -1 Agricultural (rural villages, pasture, orchards) 1 Freshwater Rice-fields (excluding reclamation lakes) 0 Marine Harbours, Mariculture platforms etc. -1

Use by each of the 365 species of each main habitat was then taken from a neutral source (Brazil 2009), modified where necessary by the present research and unpublished data. For example, main habitats used by Japanese Quail in Brazil (2009) are given as ―Wet and dry meadows, dry grassland and agricultural land‖ and those of Brown-eared Bulbul as ―Wide range of forest types (deciduous, mixed and evergreen broadleaf…In winter also in rural/agricultural areas with scattered trees and in suburban and urban gardens and parks‖. The DSI Scores for each of the habitats used were then totalled up for each species. Those species most dependent on habitats that had, in total, declined in quality or area were given a DSI Score of +1 (e.g. Japanese Quail); those for which habitat use balanced out were given a DSI Score of zero; and those for which habitat had likely improved in area or quality over the past century (e.g. Brown-eared Bulbul) were given a DSI Score of -1. Using the same habitat categories, it was then also possible to define specialist and generalist species. For the present chapter, specialists have been defined as those confined (more or less) as breeding species to two habitats or to a maximum of four habitats during the non-breeding season. Species that used a larger number of habitats (between four and seven) have been defined as near-specialist; and species that used more than eight habitat types as generalist. Specialist species are considered to be more susceptible to decrease by habitat change than generalist species, so were given an additional DSI Score of +1. Near-generalists and generalists were given an additional 289

DSI Score of zero and of -1 respectively. The other Principal Pressures were also scored in a similar way. Mass was also selected as a variable. Gaston & Blackburn (1995) suggested that species with larger body mass have been more prone to extinction than birds with smaller body mass of less than 50gm. Larger species tend to be more susceptible to a range of threats (including hunting and habitat fragmentation). Increased extinction risk (incurred through persecution and introduced predators) is also associated with large body size and long generation time (Bennett & Owen 2000). Median weights for all 365 species were therefore taken from Brazil (2009) and supplemented where appropriate from other sources. Bennett & Owen (2000) separated species above 1000gm as large and those below 1000gm as small. However, for the present study this would have resulted in 299 ―small‖ species and only 66 ―very large‖ species, many of which have only small population sizes in the ROK. Species were therefore divided into three weight categories, of large (>150gm), medium (50-150gm) and small (<50gm). Through this process, 160 species were assessed as large, 76 as medium- sized and 129 as small-sized. Larger species were given a DSI Score of +1; medium- sized species were given a DSI Score of zero; and small species were given a DSI Score of -1. The arrangement of information in this way facilitates the identification of possible relationships, for example between migratory status and mass (Table 9.4).

Table 9.4 Weight category and migratory status of the 365 regularly occurring species in the ROK. Large Medium Small Total Completely Migratory 124 66 96 286 Partially Migratory 23 6 26 55 Sedentary 13 4 7 24 Total 160 76 129 365

Through this process (one of trial and error), a total of 14 variables were selected to generate DSI Scores for each species. Eight of the selected variables were considered to be of relevance to all species (Table 9.5) and six additional variables were considered to be of most relevance to migrants (Table 9.6).

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Table 9.5 Decrease Susceptibility Index: variables, rationale & process, and the score attributed to each category for all species. Variable Rationale & Process Category DSI Score Mass Larger species more prone to extinction (Gaston & a) Species >150gm +1 Blackburn 1995), and more susceptible to some other b) Species 50-150gm 0 threats. Weights from Brazil (2009) and other c) Species <50gm -1 sources.

Habitat 15 habitats selected based on BirdLife International a) Habitats much degraded +1 Change within & IUCN publications, species‘ use from Brazil (e.g. intertidal wetland) the ROK (2009) and Birds Korea unpublished data. Each b) Habitats unchanged 0 habitat scored; and if most habitat used degraded (e.g. cool temperate score =+1. See also Chapter 1, Section 1.5.1. forest) c) Habitats increased (e.g. -1 urban area)

Use of natural 15 habitats divided into two categories: natural or a) Species with higher +1 or artificial artificial. Artificial habitat (e.g. farmland, parkland) dependence on natural habitats increased in area; area of natural habitat (e.g. habitats intertidal wetland) decreased. Species using more b) Species with higher -1 natural than artificial habitat types assessed as dependence on artificial having higher dependence on natural habitats. habitats

Degree of Specialisation described by number of 15 habitat a) Specialised, using few +1 specialisation types used (e.g. breeding in only 2 habitats, non- habitats breeding in 4 or less habitats = specialised). b) Not specialised, using 0 several habitats c) Generalist, using many -1 habitats

Tendency to Large concentrations make species vulnerable to loss a) Form concentrations of +1 concentrate of key sites, disease, hunting, and invasive alien >30% species. Species recorded in concentrations of >30% b) Form concentrations of 0 of population assessed as most susceptible to 1-29% decrease. c) No concentrations >1% -1

Distribution Distribution based on Brazil (2009), modified where a) Distribution centred to +1 & Climate appropriate by Cheng (1987), Brazil (1991) and north and west Change Tomek (1999, 2002). Species with centre of b) Distribution centred on 0 distribution to warmer south and east (e.g. China Korean Peninsula south of Yangtze, southern Japan) might benefit c) Distribution centred to -1 from warming climate and colonise/expand range in south and east Korean Peninsula; species centred to north and west might be climate change losers (due to range contraction and e.g. increased drought). See Chapter 1, Section 1.5.5.

Over- Austin (1948), Gore & Won (1971), Park (2002) and a) Hunted species (e.g. +1 exploitation other sources reviewed for commentary on hunting Japanese Quail) within the in the ROK. Hunted species assessed as more b) Not documented as 0 ROK susceptible to decrease. See Chapter 1, Section 1.5.2. hunted

Susceptibility Information in Chapter 1 and other evidence of a) Susceptible +1 to pollution susceptibility to pollution and invasive alien species b) No evidence 0 and invasive reviewed; a few species assessed as benefiting from c) Benefiting from -1 alien species increased eutrophication of inshore waters (e.g. pollution Greater Scaup Aythya marila). See Chapter 1, Sections 1.5.3 and 1.5.4.

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Table 9.6 Decrease Susceptibility Index: additional variables, rationale & process, and the score attributed to each category for migratory species. Variable Rationale & Process Category DSI Score Persecution, Brazil (1991), Cheng (1987), and BirdLife a) Overexploited (e.g. +1 over- International Factsheets (2011) reviewed for Yellow-breasted Bunting) exploitation evidence of persecution and over-hunting in b) No evidence 0 outside ROK populations of species likely to migrate to/ through ROK (e.g. waterbirds in Japan after Meiji Restoration; Black-naped Oriole in China).

Effective Effective conservation measures can stop and reverse a) No conservation 0 Conservation declines (e.g. crane conservation initiatives: BirdLife measures in place Measures 2011) b) Focus of successful -1 conservation measures

East Asia Milder winters and warmer summers will support a) Species sensitive to +1 Region range extension; prolonged drought e.g. in Amur- drought; winter visitors Climate Heilong reduces reproductive success of Oriental from taiga zone Change Stork and other waterbirds (Simonov & Dahmer b) Species that are likely 0 2008). unaffected c) ―Warm climate‖ species +1

East Asia: Data on habitat changes including forest and wetland a) Species affected by loss +1 Habitat area in East Asia reviewed, as likely affect breeding of required habitats Change and non-breeding ranges of some ROK bird b) Generalists 0 populations. Habitat loss extensive in Amur-Heilong c) Species that favour -1 basin (see main text), and in China c. 90% of plantations and degraded grassland and 40% of major wetlands are degraded habitats or severely degraded; national forest area increased from a historic low of 8.6% in 1949 to 18.21% in 2008, but a substantial percentage is monoculture plantation (China, national Ministry of Environmental Protection 2008).

Southeast Probably >100 of ROK‘s regularly occurring a) Species requiring +1 Asia: complete migrant species spend boreal winter in closed-canopy forest and Habitat Thailand (Robson 2000), and 109 species in Borneo natural wetlands in non- Change (Phillipps & Phillipps 2009). In Thailand many water breeding season. basins and wetlands transformed by dams; national b) Species tolerant of 0 forest area declined from 53.35 % in 1961 to 32.1 % secondary habitats in the late 2000s (Thailand, Office of Natural c) Species favoring -1 Resources 2009). Similar habitat changes affect fragmented and edge much of Southeast Asia. habitats

Additional Species that tend to form large concentrations a) Species especially +1 threats outside outside of ROK or that are susceptible to fisheries susceptible to additional of the ROK practices, pollution or collision with artificial threats structures are assessed as more susceptible to b) No evidence of 0 decline. additional threat.

9.4.3 Examples of DSI Scores All 365 regularly-occuring species were then assessed against each of the 14 variables selected for the present DSI, so that each species could be given a total DSI Score. Four examples are shown in Table 9.7.

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Table 9.7 Examples of Status Assessments and DSI Scores for four species in the ROK (1910- 2009). Japanese Quail Common Crested Lark Brown-eared Pheasant Bulbul Status Four Assessments Numbers 2,2,2,3* 1,1,1,1 2,2,3,4 2,2,2,1 National Population Trend Negative Unknown/ Negative Positive Stable Migratory Status (ROK) Complete Migrant Sedentary Partial Migrant Partial Migrant BirdLife International (2011) Decreasing Decreasing Decreasing Increasing Variables (ROK) Mass 0 +1 -1 -1 Habitat Change +1 +1 +1 -1 Natural/Artificial 0 0 0 -1 Generalist/Specialist +1 -1 +1 -1 Large Concentrations 0 -1 0 0 Climate Change +1 0 0 -1 Over-exploitation/ hunting +1 +1 +1 0 Pollution/ Invasive species +1 +1 +1 +1 Variables Outside ROK Over-exploitation (East Asia) +1 N/A 0 +1 Conservation measures 0 N/A 0 0 Habitat Change East Asia +1 N/A +1 0 Habitat Change SE Asia 0 N/A N/A N/A ―Others‖ 0 N/A 0 0 Total DSI Score +7 +2 +4 -3

Japanese Quail is a complete migrant to the ROK, which is assessed as Decreasing in the ROK (Chapter 2, Section 2.5.7.1) and as Decreasing at the global level (BirdLife International 2011). As a complete migrant it is potentially susceptible to threats inside and outside the ROK. It is typically confined to a few habitats; distributed largely to the north and west of the Korean Peninsula; and has suffered from extensive overexploitation within and outside of the ROK. Habitat change within and outside of the ROK (namely agricultural intensification and conversion/degradation of grasslands) and a likely susceptibility to pesticides (in agricultural landscapes) contributed to its DSI Score of +7 (compared to a DSI Score of only +2 for Common Pheasant). The high DSI Score of Japanese Quail suggests that it has been (and remains) susceptible to decline. In contrast, Brown-eared Bulbul is a partial migrant (Chapter 7), which is assessed as increasing in the ROK (Chapter 2, Section 2.5.7.9). 293

It has a centre of population to the south-east of the ROK (in Japan) and is tolerant of artificial and disturbed habitats (including city parks). Its distribution and habitat preferences suggest that it is likely to benefit from the northward expansion of broad- leaved evergreen forest in response to a warmer climate. It is, however, also likely to be susceptible to the effects of agricultural pollution in orchards. In total, several changes are likely to have benefited the species over the past century. It therefore has a low DSI Score of -3.

9.4.4 Analysis 9.4.4.1 Species of global conservation concern In order to analyse relationships, a reliable baseline is required with which to test each of the 14 variables and to start to assess their relative weighting – for example, to determine if the mass of a species is as likely to lead to its decline as the degradation of some of the habitats that it depends on. This baseline should include strong evidence of species‘ susceptibility to decline and known population trends caused in response to one or more of the variables. In the absence of robust data on national or regional population trends, or on causes of those trends, the assumption was therefore made that species of global conservation concern (i.e. those classified as Near Threatened, Vulnerable, Endangered and Critically Endangered) are more susceptible to decline than those species classified as Least Concern. This is even though the Four Assessments (Chapter 2) failed to detect a negative national population trend in several of the same globally threatened species in the ROK. Pearson‘s Chi-square tests were then conducted on the DSI Scores for several of the variables for all 37 of the ROK‘s regularly occurring species of global conservation concern (Table 9.8). Among the 37 species, none are sedentary, two are partial migrants and 35 are complete migrants. Status as a complete migrant is therefore 2 considered to be statistically highly significant (X 2 = 62.67, P<0.01). Based on their weights in Brazil (2009), 25 of the 37 are large, four are medium-sized and eight are small. There is therefore a statistically highly significant tendency towards larger mass 2 among species of global conservation status (X 2 =20.95, P<0.01). Among the 37 species, 30 have been recorded in concentrations of >30% of total national population since 2000; seven have been recorded in medium-sized concentrations; and none have been reported only in concentrations of <1% in all years since 2000. Species of global conservation concern in the ROK therefore have a statistically highly significant 294

2 tendency to form large concentrations (X 2=39.96, P<0.01). There is also a highly significant tendency for the same species to be susceptible to climate change 2 (X 2=38.98, P<0.01).

Table 9.8 DSI Scores of 37 regularly occurring species of global conservation concern according to mass, habitat change in the ROK, tendency to concentrate, and susceptibility to climate change. Species Migratory status Mass Habitat Tendency to Climate/ Change Concentrate Distribution Japanese Quail Complete migrant 0 +1 0 +1 Swan Goose Complete migrant +1 +1 +1 +1 Lesser White-fronted Goose Complete migrant +1 0 +1 +1 Falcated Duck Complete migrant +1 +1 +1 +1 Baikal Teal Complete migrant +1 0 +1 +1 Scaly-sided Merganser Complete migrant +1 +1 +1 +1 Yellow-billed Loon Complete migrant +1 +1 +1 +1 Oriental Stork Complete migrant +1 0 +1 +1 Crested Ibis Complete migrant +1 0 +1 +1 Black-faced Spoonbill Complete migrant +1 +1 +1 -1 Chinese Egret Complete migrant +1 +1 +1 -1 Steller‘s Sea Eagle Complete migrant +1 +1 +1 +1 Cinereous Vulture Complete migrant +1 +1 +1 +1 Greater Spotted Eagle Complete migrant +1 0 +1 +1 Great Bustard Complete migrant +1 +1 +1 +1 Swinhoe‘s Rail Complete migrant -1 0 0 +1 Band-bellied Crake Complete migrant 0 +1 0 +1 White-naped Crane Complete migrant +1 +1 +1 +1 Hooded Crane Complete migrant +1 +1 +1 +1 Red-crowned Crane Complete migrant +1 +1 +1 +1 Black-tailed Godwit Complete migrant +1 +1 +1 +1 Eurasian Curlew Complete migrant +1 +1 +1 +1 Far Eastern Curlew Complete migrant +1 +1 +1 +1 Nordmann‘s Greenshank Complete migrant 0 +1 +1 +1 Great Knot Complete migrant +1 +1 +1 +1 Spoon-billed Sandpiper Complete migrant -1 +1 +1 +1 Saunders‘s Gull Partial migrant +1 +1 +1 +1 Relict Gull Complete migrant +1 +1 +1 +1 Long-billed Murrelet Complete migrant +1 +1 +1 +1 Black Woodpigeon Partial migrant +1 -1 0 -1 Fairy Pitta Complete migrant 0 -1 0 -1 Black Paradise Flycatcher Complete migrant -1 -1 0 -1 Japanese Waxwing Complete migrant -1 -1 +1 +1 Styan‘s Grasshopper Warbler Complete migrant -1 0 +1 0 Yellow-breasted Bunting Complete migrant -1 +1 +1 +1 Yellow Bunting Complete migrant -1 +1 +1 -1 Ochre-rumped Bunting Complete migrant -1 0 0 +1 295

The DSI Scores themselves are also of potential value in identifying species-level trends against phylogeny (Table 9.9). Omission of single-species families (n=3), and measurement of the difference between the remaining species and other species within the same families (DSI Scores one or more than average=higher; within one= same; and one or more less than average=lower) reveals that there is a highly significant number of species of global conservation concern that have higher DSI Scores than 2 other species within their families (X 2= 9.38, P<0.01).

Table 9.9 DSI Scores of ROK species of global conservation concern and their families. Species Global DSI- Family Average DSI-Score for Status Score taxonomic Family Japanese Quail NT +7 Phasanidae +3.3 (n= 3) Swan Goose VU +10 Anatidae +6.5 (n=34) Lesser White-fronted Goose VU +5 Anatidae +6.5 (n=34) Falcated Duck NT +9 Anatidae +6.5 (n=34) Baikal Teal VU +7 Anatidae +6.5 (n=34) Scaly-sided Merganser EN +7 Anatidae +6.5 (n=34) Yellow-billed Loon NT +7 Gaviidae +7 (n=4) Oriental Stork EN +10 Ciconiidae +8.5 (n=2) Crested Ibis EN +7 Threskiornithidae +6 (n=3) Black-faced Spoonbill EN +5 Threskiornithidae +6 (n=3) Chinese Egret VU +8 Ardeidae +3.9 (n=15) Steller‘s Sea Eagle VU +7 Accipitridae +5.6 (n=19) Cinereous Vulture NT +4 Accipitridae +5.6 (n=19) Greater Spotted Eagle VU +7 Accipitridae +5.6 (n=19) Swinhoe‘s Rail VU +4 Rallidae +3.4 (n=9) Band-bellied Crake NT +6 Rallidae +3.4 (n=9) White-naped Crane VU +10 Gruidae +9.3 (n=3) Hooded Crane VU +9 Gruidae +9.3 (n=3) Red-crowned Crane EN +9 Gruidae +9.3 (n=3) Black-tailed Godwit NT +7 Scolopacidae +5.3 (n=36) Eurasian Curlew NT +6 Scolopacidae +5.3 (n=36) Far Eastern Curlew VU +8 Scolopacidae +5.3 (n=36) Nordmann‘s Greenshank EN +7 Scolopacidae +5.3 (n=36) Great Knot VU +8 Scolopacidae +5.3 (n=36) Spoon-billed Sandpiper CR +9 Scolopacidae +5.3 (n=36) Saunders‘s Gull VU +9 Laridae +3.1 (n=19) Relict Gull VU +9 Laridae +3.1 (n=19) Long-billed Murrelet NT +7 Alcidae +8.3 (n=6) Black Woodpigeon NT +5 Columbidae +2.3 (n=4) Japanese Waxwing NT +5 Bombycillidae +3.5 (n=2) Styan‘s Grasshopper Warbler VU +4 Megaluridae +3.8 (n=5) Yellow-breasted Bunting VU +8 Emberizidae +2.9 (n=16) Yellow Bunting VU +3 Emberizidae +2.9 (n=16) Ochre-rumped Bunting NT +3 Emberizidae +2.9 (n=16) 296

9.4.4.2 Decreasing and Increasing Species Review of the Four Assessments and the discussion in Chapter 2 make clear that the data on the population trends of a large number of species in the ROK are inadequate for robust analysis of differences between species of global conservation concern and species of least concern. The DSI and DSI Scores, however, can be used in their present form to assist in a review of those species assessed as ―Decreasing‖ (including both species of global conservation concern and of least concern) and ―Increasing‖ (all least concern) during the past century (listed in Chapter 2, Tables 2.8 and 2.9) to suggest shared characteristics. For example: 1. By present weightings of variables, the mean DSI Score for all 365 regularly occurring species in the ROK is +3.7. For species identified as ―Nationally- extinct‖ or ―Decreasing‖ in the ROK (n=39) the mean DSI Score is +4.8 (Table 9.10). For ―Recent Colonists and species identified as ―Increasing‖ in the ROK (n=36), the mean DSI Score is +1.5. 2. In total, 74% of Nationally-extinct/Decreasing species are complete migrants; 18% are partial migrants and 8% are sedentary species. Similar percentages were recorded for Recent Colonists and Increasing species, in which 72% were complete migrants, 19% were partial migrants, and 9% were sedentary. However, there was a substantial difference in geographical distribution between them, with a larger proportion of the Increasing species and Recent Colonists having a centre of population to the southwest, south and east of the ROK (thus assessed as being likely to benefit from climate change).. 3. The DSI Score of all sedentary species (mean +0.58, n= 24) was lower than that of partial migrants (mean +2.04, n=53) which was lower than that of complete migrants (mean +4.27, n=288).

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Table 9.10 Migratory status and DSI Scores of Decreasing species in the past century in the ROK and their families. English Name Migratory DSI- Family Average DSI- Status in ROK SCORE Score for taxonomic Family Japanese Quail Complete Migrant +7 Phasanidae +3.3 (n= 3) American Scoter Complete Migrant +7 Anatidae +6.5 (n=34) Long-tailed Duck Complete Migrant +6 Anatidae +6.5 (n=34) Common Goldeneye Complete Migrant +6 Anatidae +6.5 (n=34) Black-necked Grebe Complete Migrant +7 Podicipedidae +6.2 (n=5) Oriental Stork Complete Migrant +10 Ciconiidae +8.5 (n=2) Crested Ibis* Complete Migrant +7 Threskiornithidae +6 (n=3) Grey Heron Partial Migrant +5 Ardeidae +3.9 (n=15) Purple Heron Complete Migrant +4 Ardeidae +3.9 (n=15) Eastern Great Egret Complete Migrant +4 Ardeidae +3.9 (n=15) Black Kite Partial Migrant +6 Accipitridae +5.6 (n=19) Steller‘s Sea Eagle Complete Migrant +7 Accipitridae +5.6 (n=19) Golden Eagle Complete Migrant +4 Accipitridae +5.6 (n=19) Great Bustard* Complete Migrant +11 Otitidae +11 (n=1) Swinhoe‘s Rail Complete Migrant +4 Rallidae +3.4 (n=9) Band-bellied Crake Complete Migrant +6 Rallidae +3.4 (n=9) Watercock Complete Migrant +7 Rallidae +3.4 (n=9) Yellow-legged Buttonquail Complete Migrant +4 Turnicidae +4 (n=1) Spoon-billed Sandpiper Complete Migrant +9 Scolopacidae +5.3 (n=36) Hill Pigeon Sedentary +3 Columbidae +2.3 (n=4) Eurasian Collared Dove Complete Migrant +1 Columbidae +2.3 (n=4) Common Cuckoo Complete Migrant +1 Cuculidae +1.8 (n=5) Long-eared Owl Complete Migrant +6 Strigidae +2.6 (n=8) Crested Kingfisher* Complete Migrant +5 Alcedinidae +1.5 (n=4) Grey-capped Pygmy Woodpecker Sedentary +1 Picidae +0.6 (n=8) White-bellied Woodpecker* Sedentary +5 Picidae +0.6 (n=8) Brown Shrike Complete Migrant +3 Laniidae +3.8 (n=4) Daurian Jackdaw Complete Migrant +3 Corvidae +1.5 (n=8) Crested Lark Partial Migrant +4 Alaudidae +3.3 (n=4) Eurasian Skylark Complete Migrant +4 Alaudidae +3.3 (n=4) Far Eastern Skylark Partial Migrant +2 Alaudidae +3.3 (n=4) Chinese Hill Warbler* Partial Migrant +4 Timaliidae +2 (n=2) Eurasian Treecreeper Partial Migrant +2 Certhiidae +2 (n=1) Naumann‘s Thrush Complete Migrant +4 Turdidae +2.8 (n=11) Yellow-rumped Flycatcher Complete Migrant +4 Muscicapidae +1.8 (n=19) Common Redpoll Complete Migrant +2 Fringillidae +2.5 (n=13) Chinese Grosbeak Complete Migrant +3 Fringillidae +2.5 (n=13) Meadow Bunting Partial Migrant +3 Emberizidae +2.9 (n=16) Yellow-breasted Bunting Complete Migrant +8 Emberizidae +2.9 (n=16)

Note: Species are from Chapter 2, Table 2.8. Asterisk denotes Nationally extinct.

9.4.4.3 Complete Migrants In total, there are 286 regularly occurring complete migrants in the ROK. For the DSI, each of these has been assigned to one of three main groups corresponding to Positive (n=51), Negative (n=90) and Unknown (or stable) national population trend (n=145). The data on species groups with known trends were used in a stepwise discriminant analysis. This technique identifies the subset of the variables and their relative importance, which maximises the correct allocation of species to group. The 298

default values of the SYSTAT 11 software were used in this analysis. The five variables of Table 9.11 were identified.

Table 9.11 Classification functions. Calculated discriminant weight for each variable and each trend. Discriminant score for a species and trend is calculated as the sum of the constant and the product of each variable value and the corresponding coefficient from the table. Species are assigned to the group that gives the higher total.

Variable Negative Positive trend trend Constant -1.789 -1.327 1. Mass -0.029 -0.404 2. Habitat Change (ROK) 1.393 0.732 3. Tendency to Concentrate 0.760 1.530 4. Susceptibility to Climate Change 0.897 -0.133 5. Habitat Change (East Asia) 1.290 0.371

This analysis correctly classified 74% of the 90 decreasing species and 61% of the 51 increasing species. Overall, 70% (SD = 3.9 % points) of these 141 species were estimated to be declining. The classification functions applied to the 145 ―other‖ species estimate 68 to be decreasing and 77 to be increasing. The data therefore are useful in indicating, in general, the relationships between these variables and observed population trends in a large number of species.

9.4.5 Summary As proposed, the DSI facilitates the organisation and management of data. These data in their present form suggest that complete, long-range migrants have been and are more susceptible to decline than sedentary species and partial migrants in the ROK. DSI Scores also identify the majority of ―Decreasing‖ species identified in Chapter 2, both as more susceptible to decline than non-Decreasing species and also more susceptible to decline than other species within the same family. With further refinement (including modification of the variables and the reweighting of their scores following input from other specialists), the DSI is proposed here as an additional tool to help with the rapid identification of conservation priorities, in support of existing and more time-consuming approaches (e.g. Factsheets and Species Action Plans). 299

The DSI and the other recommendations in Chapter 9 are thus intended as steps towards improving the knowledge and science base relating to avian biodiversity, its status and trends, and to sharing this knowledge, as called for by Target 19 (CBD 2010). Of course, much still remains to be done within this decade. There is a need for further research on the distribution and abundance of species so that conservation priorities can be better refined. Advocacy approaches also need to be refined and improved, to help support improvements in policies and legal frameworks. All are essential if the Aichi Biodiversity Targets are to be met, and if the future ecological health of the Yellow Sea Blueprint Region and the Yellow Sea, vital for both birds and for people, are to be conserved.

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Appendix

LIST OF REGULARLY OCCURRING SPECIES

The list follows the English nomenclature of Moores & Park (2009), and includes the scientific name for taxa based on Gill & Wright (2006 and subsequent revisions); the National Population Trend between 1910 and 2009 based on the Four Assessments (Chapter 2); and the DSI Score (Chapter 9) of each species.

English Name Scientific Name National DSI Population Score Trend Hazel Grouse Tetrastes bonasia Unknown +3 Japanese Quail Coturnix japonica Negative +7 Common Pheasant Phasianus colchicus Unknown +2 Swan Goose Anser cygnoides Negative +10 Taiga Bean Goose Anser fabalis Positive +8 Tundra Bean Goose Anser serrirostris Positive +4 Greater White-fronted Goose Anser albifrons Positive +4 Lesser White-fronted Goose Anser erythropus Unknown +5 Brant Goose Branta bernicla Negative +8 Mute Swan Cygnus olor Negative +8 Tundra Swan Cygnus columbianus Negative +7 Whooper Swan Cygnus cygnus Negative +8 Common Shelduck Tadorna tadorna Unknown +7 Ruddy Shelduck Tadorna ferruginea Negative +8 Mandarin Duck Aix galericulata Negative +8 Gadwall Anas strepera Positive +6 Falcated Duck Anas falcata Negative +9 Eurasian Wigeon Anas penelope Negative +6 Mallard Anas platyrhynchos Negative +7 Eastern Spot-billed Duck Anas zonorhyncha Unknown +5 Northern Shoveler Anas clypeata Negative +5 Northern Pintail Anas acuta Unknown +6 Garganey Anas querquedula Unknown +4 Baikal Teal Anas formosa Unknown +7 Eurasian Teal Anas crecca Unknown +6 Common Pochard Aythya ferina Positive +6 Tufted Duck Aythya fuligula Unknown +5 Greater Scaup Aythya marila Unknown +7 Harlequin Duck Histrionicus histrionicus Negative +6 White-winged Scoter Melanitta deglandi Negative +6 American Scoter Melanitta americana Negative +7 Long-tailed Duck Clangula hyemalis Negative +6 Common Goldeneye Bucephala clangula Negative +6 Smew Mergellus albellus Negative +6 Common Merganser Mergus merganser Unknown +5 Red-breasted Merganser Mergus serrator Unknown +7 Scaly-sided Merganser Mergus squamatus Unknown +7 Red-throated Loon Gavia stellata Unknown +7 Arctic Loon Gavia arctica Unknown +7 Pacific Loon Gavia pacifica Positive +7 Yellow-billed Loon Gavia adamsii Unknown +7 Streaked Shearwater Calonectris leucomelas Unknown +7 Short-tailed Shearwater Puffinus tenuirostris Positive +4

317

English Name Scientific Name National DSI Population Score Trend Flesh-footed Shearwater Puffinus carneipes Unknown +4 Swinhoe's Storm Petrel Oceanodroma monorhis Unknown +4 Little Grebe Tachybaptus ruficollis Unknown +3 Red-necked Grebe Podiceps grisegena Unknown +7 Great Crested Grebe Podiceps cristatus Positive +7 Horned Grebe Podiceps auritus Positive +7 Black-necked Grebe Podiceps nigricollis Negative +7 Black Stork Ciconia nigra Negative +7 Oriental Stork Ciconia boyciana Negative +10 Crested Ibis Nipponia nippon Negative +7 Eurasian Spoonbill Platalea leucorodia Positive +6 Black-faced Spoonbill Platalea minor Unknown +5 Eurasian Bittern Botaurus stellaris Unknown +3 Yellow Bittern Ixobrychus sinensis Positive +3 Von Schrenck's Bittern Ixobrychus eurhythmus Negative +4 Black-crowned Night Heron Nycticorax nycticorax Positive +5 Striated Heron Butorides striata Unknown +4 Chinese Pond Heron Ardeola bacchus Positive +2 Eastern Cattle Egret Bubulcus coromandus Positive +2 Grey Heron Ardea cinerea Negative +5 Purple Heron Ardea purpurea Negative +4 Western Great Egret Ardea alba Unknown +6 Eastern Great Egret Ardea modesta Negative +4 Intermediate Egret Egretta intermedia Positive +4 Little Egret Egretta garzetta Positive +3 Pacific Reef Heron Egretta sacra Positive +1 Chinese Egret Egretta eulophotes Negative +8 Pelagic Cormorant Phalacrocorax pelagicus Unknown +4 Great Cormorant Phalacrocorax carbo Unknown +6 Temminck's Cormorant Phalacrocorax capillatus Unknown +5 Western Osprey Pandion haliaetus Positive +2 Crested Honey Buzzard Pernis ptilorhynchus Positive +7 Black Kite Milvus migrans Negative +6 White-tailed Eagle Haliaeetus albicilla Unknown +6 Steller's Sea Eagle Haliaeetus pelagicus Negative +7 Cinereous Vulture Aegypius monachus Positive +4 Eastern Marsh Harrier Circus spilonotus Unknown +8 Hen Harrier Circus cyaneus Negative +4 Pied Harrier Circus melanoleucos Unknown +5 Chinese Sparrowhawk Accipiter soloensis Unknown +9 Japanese Sparrowhawk Accipiter gularis Negative +4 Eurasian Sparrowhawk Accipiter nisus Negative +4 Northern Goshawk Accipiter gentilis Unknown +5 Grey-faced Buzzard Butastur indicus Negative +10 Eastern Buzzard Buteo japonicus Negative +7 Upland Buzzard Buteo hemilasius Negative +5 Rough-legged Buzzard Buteo lagopus Negative +2 Greater Spotted Eagle Aquila clanga Positive +7 Golden Eagle Aquila chrysaetos Negative +4 Common Kestrel Falco tinnunculus Unknown +1 Amur Falcon Falco amurensis Unknown +3 Merlin Falco columbarius Negative +1 Eurasian Hobby Falco subbuteo Unknown +3 Peregrine Falcon Falco peregrinus Unknown +1

318

English Name Scientific Name National DSI Population Score Trend Great Bustard Otis tarda Negative +11 Swinhoe's Rail Coturnicops exquisitus Negative +4 Brown-cheeked Rail Rallus indicus Unknown +3 White-breasted Waterhen Amaurornis phoenicurus Positive -1 Baillon's Crake Porzana pusilla Negative +6 Ruddy-breasted Crake Porzana fusca Positive +2 Band-bellied Crake Porzana paykullii Negative +6 Watercock Gallicrex cinerea Negative +7 Common Moorhen Gallinula chloropus Positive 0 Eurasian Coot Fulica atra Positive +4 White-naped Crane Grus vipio Negative +10 Common Crane Grus grus Negative +10 Hooded Crane Grus monacha Negative +9 Red-crowned Crane Grus japonensis Negative +9 Yellow-legged Buttonquail Turnix tanki Negative +4 Far Eastern Oystercatcher Haematopus (ostralegus) osculans Negative +6 Black-winged Stilt Himantopus himantopus Positive +1 Northern Lapwing Vanellus vanellus Unknown +9 Pacific Golden Plover Pluvialis fulva Negative +6 Grey Plover Pluvialis squatarola Unknown +7 Long-billed Plover Charadrius placidus Negative +3 Little Ringed Plover Charadrius dubius Negative 0 Kentish Plover Charadrius alexandrinus Unknown +5 Mongolian Plover Charadrius mongolus Unknown +6 Greater Sand Plover Charadrius leschenaultii Positive +7 Greater Painted Snipe Rostratula benghalensis Positive +2 Eurasian Woodcock Scolopax rusticola Unknown +4 Solitary Snipe Gallinago solitaria Unknown +7 Latham's Snipe Gallinago hardwickii Unknown +5 Pin-tailed Snipe Gallinago stenura Negative +4 Swinhoe's Snipe Gallinago megala Positive +5 Common Snipe Gallinago gallinago Negative +5 Black-tailed Godwit Limosa limosa Negative +7 Bar-tailed Godwit Limosa lapponica Negative +7 Little Whimbrel Numenius minutus Unknown +5 Whimbrel Numenius phaeopus Negative +7 Eurasian Curlew Numenius arquata Negative +7 Far Eastern Curlew Numenius madagascariensis Negative +7 Spotted Redshank Tringa erythropus Negative +7 Common Redshank Tringa totanus Positive +6 Marsh Sandpiper Tringa stagnatilis Positive +6 Common Greenshank Tringa nebularia Unknown +6 Nordmann's Greenshank Tringa guttifer Unknown +7 Green Sandpiper Tringa ochropus Negative +2 Wood Sandpiper Tringa glareola Negative +3 Grey-tailed Tattler Tringa brevipes Unknown +6 Terek Sandpiper Xenus cinereus Positive +6 Common Sandpiper Actitis hypoleucos Negative +3 Ruddy Turnstone Arenaria interpres Negative +4 Great Knot Calidris tenuirostris Negative +8 Red Knot Calidris canutus Negative +8 Sanderling Calidris alba Negative +5 Red-necked Stint Calidris ruficollis Negative +4 Temminck's Stint Calidris temminckii Negative +2 Long-toed Stint Calidris subminuta Negative +2

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English Name Scientific Name National DSI Population Score Trend Sharp-tailed Sandpiper Calidris acuminata Negative +5 Curlew Sandpiper Calidris ferruginea Unknown +6 Dunlin Calidris alpina Unknown +6 Spoon-billed Sandpiper Eurynorhynchus pygmeus Negative +9 Broad-billed Sandpiper Limicola falcinellus Unknown +5 Ruff Philomachus pugnax Positive +3 Red-necked Phalarope Phalaropus lobatus Unknown +4 Oriental Pratincole Glareola maldivarum Positive +3 Black-legged Kittiwake Rissa tridactyla Positive +6 Black-headed Gull Chroicocephalus ridibundus Positive +5 Saunders's Gull Chroicocephalus saundersi Positive +9 Relict Gull Ichthyaetus relictus Negative +9 Black-tailed Gull Larus crassirostris Unknown +5 Common Gull Larus canus Unknown +4 Glaucous-winged Gull Larus glaucescens Positive +2 Glaucous Gull Larus hyperboreus Positive +2 Vega Gull Larus vegae Unknown +5 Mongolian Gull Larus mongolicus Unknown +4 Taimyr Gull Larus heuglini Unknown +5 Slaty-backed Gull Larus schistisagus Unknown +3 Little Tern Sternula albifrons Negative +7 Common Tern Sterna hirundo Unknown +6 Whiskered Tern Chlidonias hybrida Positive +3 White-winged Tern Chlidonias leucopterus Positive +3 Pomarine Skua Stercorarius pomarinus Unknown +5 Parasitic Jaeger Stercorarius parasiticus Negative +4 Brunnich's Murre Uria lomvia Unknown +8 Common Murre Uria aalge Negative +9 Spectacled Guillemot Cepphus carbo Unknown +8 Long-billed Murrelet Brachyramphus perdix Unknown +8 Ancient Murrelet Synthliboramphus antiquus Negative +10 Rhinoceros Auklet Cerorhinca monocerata Positive +8 Hill Pigeon Columba rupestris Negative +3 Black Wood Pigeon Columba janthina Unknown +5 Oriental Turtle Dove Streptopelia orientalis Unknown 0 Eurasian Collared Dove Streptopelia decaocto Negative +1 Northern Hawk-cuckoo Hierococcyx hyperythrus Positive +2 Lesser Cuckoo Cuculus poliocephalus Positive +3 Indian Cuckoo Cuculus micropterus Unknown +1 Oriental Cuckoo Cuculus optatus Negative +2 Common Cuckoo Cuculus canorus Negative +1 Northern Scops Owl Otus semitorques Negative +3 Oriental Scops Owl Otus sunia Negative +2 Eurasian Eagle-Owl Bubo bubo Negative +2 Chinese Tawny Owl Strix nivicola Unknown +2 Ural Owl Strix uralensis Positive +2 Northern Boobook Ninox scutulata Negative 0 Long-eared Owl Asio otus Negative +6 Short-eared Owl Asio flammeus Negative +4 Grey Nightjar Caprimulgus jotaka Unknown +4 White-throated Needletail Hirundapus caudacutus Unknown +4 Fork-tailed Swift Apus pacificus Positive +2 Oriental Dollarbird Eurystomus orientalis Negative +4

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English Name Scientific Name National DSI Population Score Trend Ruddy Kingfisher Halcyon coromanda Unknown +3 Black-capped Kingfisher Halcyon pileata Unknown +2 Common Kingfisher Alcedo atthis Negative -2 Eurasian Hoopoe Upupa epops Negative +1 Eurasian Wryneck Jynx torquilla Positive +2 Japanese Pygmy Woodpecker Dendrocopos kizuki Positive -4 Grey-capped Pygmy Woodpecker Dendrocopos canicapillus Negative +1 White-backed Woodpecker Dendrocopos leucotos Unknown +1 Great Spotted Woodpecker Dendrocopos major Unknown -2 White-bellied Woodpecker Dryocopus javensis Negative +5 Black Woodpecker Dryocopus martius Positive +2 Grey-headed Woodpecker Picus canus Unknown 0 Fairy Pitta Pitta nympha Unknown +3 Ashy Minivet Pericrocotus divaricatus Negative +3 Tiger Shrike Lanius tigrinus Negative +4 Bull-headed Shrike Lanius bucephalus Negative +3 Brown Shrike Lanius cristatus Negative +3 Chinese Grey Shrike Lanius sphenocercus Negative +5 Black-naped Oriole Oriolus chinensis Unknown +2 Black Drongo Dicrurus macrocercus Positive -1 Black Paradise Flycatcher Terpsiphone atrocaudata Negative +1 Eurasian Jay Garrulus glandarius Negative +3 Azure-winged Magpie Cyanopica cyanus Positive -1 Eurasian Magpie Pica pica Unknown -1 Spotted Nutcracker Nucifraga caryocatactes Unknown +6 Daurian Jackdaw Coloeus dauuricus Negative +3 Rook Corvus frugilegus Unknown +3 Carrion Crow Corvus corone Negative +1 Large-billed Crow Corvus macrorhynchos Positive 0 Bohemian Waxwing Bombycilla garrulus Unknown +2 Japanese Waxwing Bombycilla japonica Unknown +5 Marsh Tit Poecile palustris Positive -3 Varied Tit Poecile varius Positive -2 Coal Tit Periparus ater Positive 0 Yellow-bellied Tit Periparus venustulus Positive -3 Eastern Great Tit Parus minor Positive -3 Chinese Penduline Tit Remiz consobrinus Positive +3 Greater Short-toed Lark Calandrella brachydactyla Positive +3 Crested Lark Galerida cristata Negative +4 Eurasian Skylark Alauda arvensis Negative +4 Far Eastern Skylark Alauda japonica Negative +2 Light-vented Bulbul Pycnonotus sinensis Positive -2 Brown-eared Bulbul Microscelis amaurotis Positive -3 Sand Martin Riparia riparia Negative +3 Barn Swallow Hirundo rustica Negative +1 Asian House Martin Delichon dasypus Negative +3 Red-rumped Swallow Cecropis daurica Positive -1 Asian Stubtail Urosphena squameiceps Unknown +3 Japanese Bush Warbler Cettia diphone Unknown -3 Korean Bush Warbler Cettia canturians Unknown +4 Long-tailed Tit Aegithalos caudatus Positive -1 Dusky Warbler Phylloscopus fuscatus Positive +1 Radde's Warbler Phylloscopus schwarzi Positive +3 Pallas's Leaf Warbler Phylloscopus proregulus Positive +3

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English Name Scientific Name National DSI Population Score Trend Yellow-browed Warbler Phylloscopus inornatus Unknown +1 Arctic Warbler Phylloscopus borealis Unknown +3 Two-barred Warbler Phylloscopus plumbeitarsus Unknown +3 Pale-legged Leaf Warbler Phylloscopus tenellipes Unknown +5 Eastern Crowned Warbler Phylloscopus coronatus Unknown +5 Thick-billed Warbler Acrocephalus aedon Positive +2 Oriental Reed Warbler Acrocephalus orientalis Unknown 0 Black-browed Reed Warbler Acrocephalus bistrigiceps Negative +3 Lanceolated Warbler Locustella lanceolata Unknown +4 Pallas's Grasshopper Warbler Locustella certhiola Unknown +4 Middendorff's Grasshopper Warbler Locustella ochotensis Unknown +2 Styan's Grasshopper Warbler Locustella pleskei Negative +3 Gray's Grasshopper Warbler Locustella fasciolata Unknown +5 Far Eastern Cisticola Cisticola juncidis Positive -1 Vinous-throated Parrotbill Paradoxornis webbianus Positive -3 Chinese Hill Warbler Rhopophilus pekinensis Negative +4 Chestnut-flanked White-eye Zosterops erythropleurus Positive +4 Japanese White-eye Zosterops japonicus Positive -2 Goldcrest Regulus regulus Positive +2 Winter Wren Troglodytes troglodytes Unknown -2 Eurasian Nuthatch Sitta europaea Unknown +1 Chinese Nuthatch Sitta villosa Negative +2 Eurasian Treecreeper Certhia familiaris Negative +2 Red-billed Starling Spodiopsar sericeus Positive 0 White-cheeked Starling Spodiopsar cineraceus Unknown +4 Chestnut-cheeked Starling Agropsar philippensis Positive +3 Daurian Starling Agropsar sturninus Unknown +5 Common Starling Sturnus vulgaris Positive +2 Siberian Thrush Zoothera sibirica Unknown +7 White's Thrush Zoothera aurea Unknown +1 Grey-backed Thrush Turdus hortulorum Positive +2 Grey Thrush Turdus cardis Unknown +5 Chinese Blackbird Turdus merula Positive -2 Eyebrowed Thrush Turdus obscurus Unknown +5 Pale Thrush Turdus pallidus Positive +3 Brown-headed Thrush Turdus chrysolaus Positive +3 Red-throated Thrush Turdus ruficollis Positive +4 Naumann's Thrush Turdus naumanni Negative +4 Dusky Thrush Turdus eunomus Unknown +2 Japanese Robin Erithacus akahige Positive 0 Bluethroat Luscinia svecica Unknown 0 Siberian Rubythroat Luscinia calliope Unknown +2 Siberian Blue Robin Luscinia cyane Unknown +4 Rufous-tailed Robin Luscinia sibilans Negative +4 Red-flanked Bluetail Tarsiger cyanurus Unknown +2 Daurian Redstart Phoenicurus auroreus Unknown 0 Plumbeous Water Redstart Rhyacornis fuliginosa Positive 0 Siberian Stonechat Saxicola maurus Unknown +1 Blue Rock Thrush Monticola solitarius Unknown -1 White-throated Rock Thrush Monticola gularis Positive +4 Grey-streaked Flycatcher Muscicapa griseisticta Negative +2 Dark-sided Flycatcher Muscicapa sibirica Negative +2 Asian Brown Flycatcher Muscicapa dauurica Unknown +2

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English Name Scientific Name National DSI Population Score Trend Yellow-rumped Flycatcher Ficedula zanthopygia Negative +4 Narcissus Flycatcher Ficedula narcissina Unknown +1 Mugimaki Flycatcher Ficedula mugimaki Unknown +3 Taiga Flycatcher Ficedula albicilla Unknown +2 Blue-and-white Flycatcher Cyanoptila cyanomelana Unknown +2 Brown Dipper Cinclus pallasii Unknown +2 Russet Sparrow Passer rutilans Negative +1 Eurasian Tree Sparrow Passer montanus Negative -2 Alpine Accentor Prunella collaris Positive +3 Siberian Accentor Prunella montanella Unknown +2 Forest Wagtail Dendronanthus indicus Negative 0 Eastern Yellow Wagtail Motacilla tschutschensis Unknown +3 Citrine Wagtail Motacilla citreola Positive +2 Grey Wagtail Motacilla cinerea Unknown +1 White Wagtail Motacilla alba Negative +1 Japanese Wagtail Motacilla grandis Positive 0 Richard's Pipit Anthus richardi Unknown -1 Blyth's Pipit Anthus godlewskii Unknown +1 Olive-backed Pipit Anthus hodgsoni Positive +2 Pechora Pipit Anthus gustavi Unknown +2 Red-throated Pipit Anthus cervinus Positive +1 Buff-bellied Pipit Anthus rubescens Unknown +3 Brambling Fringilla montifringilla Unknown +1 Grey-capped Greenfinch Carduelis sinica Positive +1 Eurasian Siskin Carduelis spinus Positive +3 Common Redpoll Carduelis flammea Negative +2 Long-tailed Rosefinch Uragus sibiricus Unknown +3 Common Rosefinch Carpodacus erythrinus Positive +1 Pallas's Rosefinch Carpodacus roseus Unknown +3 Red Crossbill Loxia curvirostra Unknown +2 Eurasian Bullfinch Pyrrhula pyrrhula Positive +2 Hawfinch Coccothraustes coccothraustes Unknown +3 Chinese Grosbeak Eophona migratoria Negative +3 Japanese Grosbeak Eophona personata Positive +5 Pine Bunting Emberiza leucocephalos Unknown +1 Meadow Bunting Emberiza cioides Negative +3 Tristram's Bunting Emberiza tristrami Positive +1 Chestnut-eared Bunting Emberiza fucata Negative +5 Little Bunting Emberiza pusilla Positive +2 Yellow-browed Bunting Emberiza chrysophrys Unknown +3 Rustic Bunting Emberiza rustica Negative +3 Yellow-throated Bunting Emberiza elegans Unknown -1 Yellow-breasted Bunting Emberiza aureola Negative +8 Chestnut Bunting Emberiza rutila Negative +3 Yellow Bunting Emberiza sulphurata Unknown +3 Black-faced Bunting Emberiza spodocephala Unknown +5 Grey Bunting Emberiza variabilis Unknown +2 Pallas's Reed Bunting Emberiza pallasi Unknown +1 Ochre-rumped Bunting Emberiza yessoensis Unknown +3 Common Reed Bunting Emberiza schoeniclus Positive +3 Lapland Longspur Calcarius lapponicus Positive +3