Annual Migratory Patterns of Far East Greylag Geese

Integrative Zoology 2020; 15: 213–223 doi: 10.1111/1749-4877.12414

1 ORIGINAL ARTICLE 1 2 2 3 3 4 4 5 5 6 Annual migratory patterns of Far East Greylag Geese (Anser 6 7 7 8 8 9 anser rubrirostris) revealed by GPS tracking 9 10 10 11 11 1,2 1 3 4 12 Xianghuang LI, Xin WANG, Lei FANG, Nyambayar BATBAYAR, Tseveenmyadag 12 13 NATSAGDORJ,4 Batmunkh DAVAASUREN,4 Iderbat DAMBA,1,2 Zhenggang XU,5 Lei CAO1,2 13 14 14 6 15 and Anthony David FOX 15 16 16 1State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of 17 17 Sciences, Beijing, China, 2University of Chinese Academy of Sciences, Beijing, China, 3School of Life Science, University of 18 18 4 19 Science and Technology of China, Hefei, Anhui, China, Wildlife Science and Conservation Center of Mongolia, Ulaanbaatar, 19 5 20 Mongolia, Key Laboratory of Forestry Remote Sensing Based Big Data & Ecological Security for Hunan Province, Central South 20 6 21 University of Forestry and Technology, Changsha, China and Department of Bioscience, Aarhus University, Rønde, Denmark 21 22 22 23 23 24 24 25 Abstract 25 26 Twenty Far East Greylag Geese, Anser anser rubrirostris, were captured and fitted with Global Positioning Sys- 26 27 tem/Global System for Mobile Communications (GPS/GSM) loggers to identify breeding and wintering areas, 27 28 migration routes and stopover sites. Telemetry data for the first time showed linkages between their Yangtze 28 29 River wintering areas, stopover sites in northeastern China, and breeding/molting grounds in eastern Mongolia 29 30 and northeast China. 10 of the 20 tagged individuals provided sufficient data. They stopped on migration at the 30 31 Yellow River Estuary, Beidagang Reservoir and Xar Moron River, confirming these areas as being important 31 32 stopover sites for this population. The median spring migration duration was 33.7 days (individuals started mi- 32 33 grating between 25 February and 16 March and completed migrating from 1 to 9 April) compared to 52.7 days 33 34 in autumn (26 September–13 October until 4 November–11 December). The median stopover duration was 31.1 34 35 and 51.3 days and the median speed of travel was 62.6 and 47.9 km/day for spring and autumn migration, re- 35 36 spectively. The significant differences between spring and autumn migration on the migration duration, the stop- 36 37 over duration and the migration speed confirmed that tagged adult Greylag Geese traveled faster in spring than 37 38 autumn, supporting the hypothesis that they should be more time-limited during spring migration. 38 39 39 40 Key words: Anser anser, autumn migration, greylag goose, GPS/GSM loggers, spring migration 40 41 41 42 42 43 43 44 INTRODUCTION 44 45 45 46 The Greylag Goose is widely distributed in Eurasia, 46 Correspondence: Lei Cao, State Key Laboratory of Urban and 47 divided between 2 recognized subspecies. The western 47 48 Regional Ecology, Research Center for Eco-Environmental form, Anser anser anser Linnaeus, 1758, breeds from 48 49 Sciences, Chinese Academy of Sciences, Beijing 100085, Iceland to north and central Europe into Russia and win- 49 50 China. ters from Scotland south to North Africa and east to 50 51 Email: [email protected] Iran; the eastern Greylag Goose, Anser anser rubriros- 51

1 tris Swinhoe, 1871, breeds from Romania and Turkey duration of spring migration of birds in this flyway pop- 1 2 to the Russian Far East and northeast China and winters ulation should be shorter than that in autumn. Migration 2 3 from Asia Minor to eastern China (Kear 2005). As a re- theory predicts that long-distance migrants should mini- 3 4 sult of its abundance and distribution, the species as a mize the duration of spring migration to ensure early ar- 4 5 whole is assessed as being of Least Concern (BirdLife rival in breeding areas, in an attempt to enhance fitness 5 6 International 2018). The population of Greylag Geese by occupation of better quality territories (Kokko 1999) 6 7 in western Europe is increasing (BirdLife Internation- and earlier nesting (Moore et al. 2005). Earlier nesting 7 8 al 2018), supplemented by an estimated 300 000 feral contributes to increased clutch size (Rowe et al. 1994) 8 9 escaped/released individuals (Kampe-Persson 2010). and fledging of better quality offspring with higher sur- 9 10 The discrete “Far East” population of rubrirostris (see vival rates during their first migration (Perrins 1970; 10 11 Rozenfeld & Cao 2018), which winters mainly in the McNamara et al. 1998), and enables females to ad- 11 12 Yangtze River Floodplain and along Chinese coasts and just reproductive investment to maximize fitness (Van- 12 13 is thought to breed in Inner Mongolia (China), Mongo- noordwijk et al. 1995). Most migration studies show 13 14 lia and adjacent areas of Russia (Kear 2005), remains that spring migration is faster than autumn migration 14 15 poorly known. The population was formerly estimated (Nilsson et al. 2013). Like these Greylag Geese, Swan 15 16 at 50 000–100 000 (Wetlands International 2012), but Geese, Anser cygnoides, breed in Mongolian-Manchu- 16 17 counts from the wintering areas in the mid-2000s esti- rian steppe wetlands and winter in China; recent studies 17 18 mated a population of 13 000 (Cao et al. 2008), suggest- show that Swan Geese follow the same paradigm, un- 18 19 ing numbers were at that time far lower than this. This dertaking spring migration faster than autumn migration 19 20 population is thought to have undergone major contrac- (Batbayar et al. 2011), so we also use telemetry data to 20 21 tions in breeding range and abundance in the Russian test whether Greylag Geese sharing breeding and win- 21 22 Far East boreal regions but also to the south in steppe tering areas exhibit similar patterns. 22 23 biotopes in Russia, Mongolia and China (Rozenfeld & 23 24 Cao 2018), where the species has declined as this re- MATERIALS AND METHODS 24 25 gion has moved into the driest phase of the drought cy- 25 26 cle (Pederson et al. 2001). Capture of individuals and transmitter 26 27 27 As well as concern about their conservation status, attachment 28 we still lack knowledge about the precise breeding and 28 29 wintering distributions of Far East Greylag Geese, their In December 2014, 5 Greylag Geese were captured at 29 30 migration routes, and their critical stopover sites in be- Poyang Lake (29°0′N, 116°24′E, Jiangxi Province, Chi- 30 31 tween routes. For this reason, we deployed Global Posi- na) and fitted with neck collar-mounted GPS/GSM log- 31 32 tioning System/Global System for Mobile Communica- gers (weight 26 g, Hunan Global Messenger Technolo- 32 33 tions (GPS/GSM) loggers on Greylag Geese in eastern gy, China). One bird died that winter, while signals were 33 34 Mongolia (breeding area) and in the Yangtze River lost from 2 other individuals before migration. In Oc- 34 35 (winter quarters) to confirm the connectivity between tober/November 2016, 10 individuals were captured at 35 36 the 2 areas and to locate potentially important migra- Anhui Lake (30°53′N, 117°42′E, Anhui Province, Chi- 36 37 tion stopover sites. Two other Greylag Geese recently na) and fitted with neck collar-mounted loggers (weight 37 38 caught and fitted with telemetry devices in the Yangtze 35/45 g, Druid Technology, China). Before spring mi- 38 39 River Valley traveled to breeding areas further west in gration, 2 of these birds died on the wintering area and 39 40 Mongolia following a different flyway and the results of another summered on the Yellow River Estuary (Shan- 40 41 these and other studies will be used in a future analysis dong Province, China). Two tagged birds migrated to 41 42 of the movements of eastern Greylag Geese in a wider western Mongolia, which we consider to be outside of 42 43 perspective. However, for the purposes of this analysis, the flyway, the data from which will form the subject of 43 44 we selected data from only those Yangtze marked indi- future analysis. Hence, 5 of these birds were followed to 44 45 viduals that returned to summer in the Mongolian-Man- their ultimate breeding areas. In July 2017, 5 individuals 45 46 churian Grassland Steppe Ecoregion (Olsen et al. 2001) were captured at Buir Lake (47°42′N, 117°35′E, eastern 46 47 of Inner Mongolia (China), Mongolia and adjacent areas Mongolia), and fitted with neck collar-mounted GPS/ 47 48 of Russia as a discrete breeding flyway. GSM loggers (weight 35g, Druid Technology, China). 48 49 49 As a secondary objective, we also used data from Two of these failed before autumn migration. All fit- 50 50 tagged geese to seek support for the hypothesis that the ted devices constituted much less than 3% of individu- 51 51

1 al total body mass (Millspaugh & Marzluff 2001) (Table start and end points of the migration leg. We calculated 1 2 S1). Both logger types included a solar panel with re- the straightness index as the path tortuosity of the move- 2 3 chargeable batteries, transmitting data via the GSM net- ment between breeding and wintering areas in both di- 3 4 work. We preselected the devices to record positions at rections. The straightness index is primarily a measure 4 5 hourly intervals. of the discrepancy between the path actually followed 5 6 by the animal and a perfectly oriented straight segment 6 Identifying stopover sites 7 linking the ultimate goal to the starting point (Benhamou 7 8 For each individual, we defined spring migration as 2004). We calculated migration speed as migration dis- 8 9 starting from the last position received from the over- tance divided by migration duration, and the daily travel 9 10 wintering area and terminating with the first position speed was calculated by dividing migration distance by 10 11 of a series of positions received from the summering total travel days. Travel days were defined as the total 11 12 grounds; autumn migration was defined as the last po- duration of migration (days) minus stopover days (Nils- 12 13 sition received from the breeding/molting grounds be- son et al. 2013). 13 14 14 fore departure until the first point reached on the win- Statistical analysis 15 tering grounds. We applied the method of Wang et al. 15 16 (2018) to segment movement tracks into “fly” and “non- We assessed the seasonal differences on the 7 migra- 16 17 fly,” then we plotted locations in Google Earth to visu- tion parameters (migration duration, number of stop- 17 18 alize movements, to pinpoint arrival and departure dates over sites, stopover duration, migration distance, mi- 18 19 at sites, and to evaluate where birds were wintering, gration speed, daily travel speed and straightness index) 19 20 breeding, molting or stopping (Page et al. 2014). We de- using the Wilcoxon rank-sum test (Wilcoxon 1945). 20 21 fined stopover sites as locations where individual birds We excluded subadults or individuals of unknown age 21 22 remained within a predefined area during migration for from this analysis, as the hypothesized seasonal migra- 22 23 at least 2 days (Koelzsch et al. 2016). tion differences would only be associated with the time 23 24 We attempted to assess the effectiveness of the cur- constraints imposed by the breeding behavior of adults. 24 25 rent extent of designated Important Bird and Biodiver- We identified adult and juvenile individuals based on 25 26 sity Areas (IBAs; BirdLife International 2018), and the morphology characteristics in the field; some individu- 26 27 national special protected areas for the protection of als were not identified. All statistical analyses were con- 27 28 stopover sites used by these tagged Greylag Geese. We ducted in R 3.5.1 (R Development Core Team 2018). 28 29 29 downloaded Asian IBA and national special protected Results 30 area site boundary information with permission (Min- 30 31 istry of Environmental Protection 2014). We then over- Overall, we obtained complete spring and autumn mi- 31 32 laid all stopover sites used by tagged Greylag Geese us- gration tracks from the 10 individuals (Table S1), with 32 33 ing Google Earth to identify which stopover sites were some individuals providing multi-year tracking data 33 34 located within IBA and special protected areas boundar- (Table 1). In all, we obtained 9 autumn migration tracks 34 35 ies. from 8 different individuals (2015: n = 2, 2016: n = 1, 35 36 2017: n = 6) and 14 spring migration tracks from 8 in- 36 37 Defining migration parameters dividuals (2015: n = 2, 2016: n = 2, 2017: n = 6, 2018: 37 38 Migration duration was defined as the total duration n = 4) (Table 1). 38 39 39 of spring and autumn migrations, including the peri- Spring migration routes 40 ods spent at stopover sites. The number of stopover sites 40 41 throughout each migration episode was calculated us- All 10 birds wintered along the Yangtze River 41 42 ing the criteria above to define how many times Grey- (Figs 1b and 2a). Spring migration commenced from 42 43 lag Geese used separate stopover sites, and stopover du- mid-February to mid-March. After leaving the Yang- 43 44 ration was derived as the cumulative sum of all days tze River, most tagged geese flew non-stop for approxi- 44 45 spent at all these stopover sites during each migration mately 1000 km to the first stopover sites. One individ- 45 46 episode. We calculated migration distance by summing ual (ID#159) flew 300 km to stop at Sangjian Reservoir 46 47 the distance of all migration legs of spring/autumn mi- during the 2018 spring migration; otherwise, the first 47 48 gration. The distance of each migration leg was calcu- main spring migration stopover sites of other birds were 48 49 lated by summing the distance of consecutive locations located on the Yellow River Estuary, Yangcheng Res- 49 50 of the migration leg, rather than simply connecting the ervoir, the Nandagang wetlands and Beidagang Reser- 50 51 51

1 - 1 2 2 1 0.7 0.9 0.9 0.8 0.9 0.9 0.7 0.9 0.8 0.7 0.9 0.6 0.9 0.8 0.9 0.9 0.9 0.1 0.1 0.8 0.7 0.9 0.9 0.1 0.1 3 0.9 3 index 4 4 Straightness 5 5 6 6 7 7 1374 1046 798.6 973.7 843.2 543.9 307.8 672.4 641.6 973.7 457.2 684.7 530.7 296.6 634.4 483.1 376.6 577.8 419.7 619.9 speed 1111.5 1139.8 1496.6 1398.1 1445.5 1367.2 8 1273.9 8

9 Daily travel 9 10 10 11 11 0 2 2 3 1 1 2 2 2 1 1 2 2 2 1 2 1 1 1 1 2 2 2 2 1 1 12 1 12 stopovers

13 Number of 13 14 14 15 15 83 85 36 9.7 30.2 78.1 67.1 65.6 39.1 58.8 47.9 69.9 66.5 53.8 66.3 54.9 44.1 87.7 57.4 57.9 48.4 25.6 24.6 16 53.4 16 798.6 148.5 166.9 speed

17 Migration 17 18 18 19 19 20 20 328.6 259.1 314.1 257.3 2562.3 2190.9 2233.6 2531.1 2058.3 1961.3 2855.5 2383.9 2268.4 2406.2 2353.3 2856.4 2330.3 2612.4 2253.8 1992.1 2409.1 1877.5 2721.8 2495.8 2070.6 2134.6 2324.1 distance

21 Migration 21 22 22 23 23 0 9.9 8.1 23.9 25.8 31.7 35.6 51.3 31.5 54.4 26.4 30.8 12.5 41.3 36.8 40.8 56.9 22.4 32.9 27.4 13.1 42.8 24.2 55.8 38.5 14.7 24 39.8 24 duration 25 Stopover 25 26 26 28 29 47 3.2 27 6.9 27 11.2 23.6 33.3 38.6 52.7 33.4 59.6 34.1 34.1 16.2 43.7 43.1 42.4 59.2 25.7 34.7 15.5 29.4 57.5 44.1 13.0 43.5 duration

28 Migration 28 29 29 30 30 31 31 Arrival 2018/4/1 2018/4/1 2017/4/2 2018/4/9 2017/4/1 2017/4/1 2018/4/1 2017/4/9 32 2016/4/1 32 2017/11/4 2017/12/5 2015/4/15 2017/4/28 2016/4/17 2017/4/15 2015/4/15 2017/11/11 2016/11/13 2015/11/25 2017/11/26 2017/11/15 2017/12/11 2015/10/30 33 33 IQR 34 IQR 34 35 35 IQR (only adult) 36 IQR (only adult) 36 2017/3/6 2015/3/1 Departure 2015/3/11 2017/2/11 2017/9/26 2018/2/26 2018/2/25 2017/9/27 2017/3/16 2017/3/16 2018/2/25 2017/10/2 2017/2/25 2016/2/29 2018/3/20 2017/3/16 2016/2/17 2015/10/27 2016/10/16 2015/10/23 2017/10/13 2017/10/13 37 2017/10/13 37 38 38 39 39 40 40 NA NA NA NA NA Age 2015 2016 2015 2017 2017 2017 2017 2017 2017 Adult Adult Adult Adult Adult Adult Juvenile Juvenile 41 Juvenile 41 42 42 43 43 Year 2015 2016 2015 2017 2017 2015 2018 2016 2018 2017 2017 2017 2018 2017 2017 2017 2017 2017 2018 2017 2017 2015 44 2016 44 45 45 46 46 31 15 15 15 159 159 150 149 159 149 149 2347 2342 2342 2042 cas004 cas003 cas003 cas003 cas003 cas003 cas004 cas004

47 Bird ID 47 48 48 49 49 50 50 Spring Season Autumn Table 1 Migration parameters for tracked Greylag Geese, reported by season (autumn/spring) Table 51 The interquartile range (IQR) of each migration parameter is presented with means and the without individuals non-adults. with NA unknown age. Each migration param eter is defined in the Materials and Methods. 51

1 voir (Table 2). Following departure from their first stop- tween early April and the end of that month. The 10 in- 1 2 over sites, the marked Greylag Geese flew 600 km to dividuals summered at the Wulagai Gaobi wetlands and 2 3 their second stopover sites along the Xar Moron Riv- the Huihe National Nature Reserve (both in Inner Mon- 3 4 er. One bird (ID#2342) made no second stopover, fly- golia, China) and Buir Lake in Mongolia. 4 5 ing directly to the ultimate summering area after depar- 5 Autumn migration routes 6 ture from the Nandagang wetlands. Most of individuals 6 7 used the Xar Moron River as their final stopover site be- Most of the tagged Greylag Geese summered with- 7 8 fore arrival at summering areas. The two birds marked in the Mongol-Manchurian Grassland Steppe Ecore- 8 9 in their first winters (ID#15 and ID#150) both used the gion (Fig. 1a). Autumn migration for these birds began 9 10 East Ujimqin wetlands as their last stopover site (Table in late September and extended to late October, using 10 10 11 2). Tagged birds completed their spring migration be- dispersed stopover sites in the course of autumn migra- 11 12 12 13 13 14 14 15 15 16 16 17 17 18 18 19 19 20 Figure 1 Migration routes and main stop- 20 21 over sites used by individual Greylag 21 22 Geese are linked by solid lines. Green cir- 22 23 cles indicate the stopover sites. (a) Autumn 23 24 migration. (b) Spring migration. The shad- 24 25 ed pale red region shows the Mongol-Man- 25 26 churian Grassland Steppe Ecoregion. 1. 26 27 Sangjian Reservoir, 2. Yellow River Estu- 27 28 ary, 3. Yangcheng Reservoir, 4. Nandagang 28 29 wetlands, 5. Beidagang Reservoir, 6. Xar 29 Moron River, 7. Wetland of East Ujimqin, 30 30 8. Huihe NNR, 9. Buir Lake, 10. Wetland 31 31 of Wulagai Gaobi, 11. Wulagai Reservoir, 32 32 12. Farmland of Derina Lingao Legacha, 33 33 13. Yancheng National Nature Reserve. 34 34 35 35 36 36 37 37 38 38 39 39 40 40 Figure 2 Wintering sites and summer- 41 41 ing sites for the tagged Greylag Geese. (a) 42 42 Wintering sites. (b) Summering sites. The 43 shaded pale red region shows the Mon- 43 44 gol-Manchurian Grassland Steppe Ecore- 44 45 gion. 1. Hubei Lake, 2. Longgan Lake, 3. 45 46 Poyang Lake, 4. Qingcao Lake, 5. Caizi 46 47 Lake, 6. Khukh Lake, Mongolia, 7. Hu- 47 48 lun Lake, 8. Wulan Nuo’er wetland, 9. 48 49 Buir Lake, 10. Huihe National Nature Re- 49 50 serve, 11. Wetland of Wulagai Gaobi, 12. 50 51 Zun-Torey Lake, Russia. 51

1 Table 2 Stopover sites of Greylag Geese tracked using satellite transmitters 1 2 Estimated 2 Times of Arrival date Departure Protection IBA sites 3 Number Stopover sites and coordinates Migration duration of 3 stopping range date range status (Y/N) 4 stay (day) + CI 4 5 5 Farmland of Shou County, 6 13 6 1 Anhui Province, China. Autumn n = 1 9 November 4 None N 7 November 7 (32°08′60″N,116°46′48″E) 8 8 Dongfanghong Reservoir, 9 18 25 9 2 Anhui Province, China. Autumn n = 1 7 None N 10 November November 10 (32°19′48″N, 117°10′48″E) 11 11 Sangjian Reservoir, 12 12 3 Anhui province, China Spring n = 1 26 February 4 March 6 None N 13 13 (32°31′48″N, 117°46′12″E) 14 14 Yancheng National Nature National 15 24 15 4 Reserve, Jiangsu Province, China Autumn n = 1 4 November 20 Nature Y 16 November 16 (33°36′00″N,120°31′48″E) Reserve 17 17 12 18 23 March– 18 Spring n = 9 February–17 11–49 19 Yellow River Estuary, Shandong 6 April National 19 March 20 5 Province, China Nature Y 20 18 21 (37°44′24″N, 119°04′12″E) 5–24 Reserve 21 Autumn n = 4 October–4 5–51 22 October 22 23 December 23 24 Yangcheng Reservoir, 24 25 6 Hebei Province, China Spring n = 1 26 February 27 March 29 None N 25 26 (38°08′24″N, 117°41′24″E) 26 27 Nandagang wetland, Spring n = 1 28 February 30 March 30 Provincial 27 28 7 Hebei Province, China 10 Nature Y 28 Autumn n = 1 14 October 27 29 (38°30′36″N, 117°29′24″E) November Reserve 29 30 Beidagang Reservoir, Spring n = 1 13 March 3 April 20 National 30 31 8 Tianjin, China 10 Nature Y 31 Autumn n = 1 19 October 52 32 (38°45′36″N, 117°24′00″E) December Reserve 32 33 Farmland of Derina Lingao Spring n = 1 2 April 8 April 7 33 34 Legacha, 34 9 None N 35 Inner Mongolia, China. Autumn n = 1 15 October 2 November 18 35 36 (42°52′48″N, 119°42′36″E) 36 37 Xar Moron River, 37 19 March–3 31 March 38 10 Inner Mongolia, China. Spring n = 5 4–18 None Y 38 April –14 April 39 (43°15′36″N, 119°24′36″E) 39 40 40 Wetland of Wulagai Gaobi, 41 41 11 Inner Mongolia, China. Autumn n = 1 October 6 13 October 7 None N 42 (45°37′12″N, 118°00′00″E) 42 43 43 Wulagai reservoir, 44 27 44 12 Inner Mongolia, China. Autumn n = 1 1 November 34 None N 45 September 45 (45°52′48″N, 119°30′36″E) 46 46 47 Wetland of East Ujimqin, Inner Spring n = 2 5–10 April 15–26 April 10–17 47 48 13 Mongolia, China 26 None N 48 Autumn n = 1 6 October 10 49 (46°27′36″N, 118°28′12″E) September 49 50 Only sites where the estimated duration of stay was at least 2 days are shown. IBA, Important Bird and Biodiversity Areas. CI, Con- 50 51 fidence interval. 51

1 tion. Two birds (ID#2347 and ID#2042) stopped close es. During spring migration, the tagged Greylag Geese 1 2 to the summering areas, while most flew to the Bohai used the IBA sites for a mean of 20.6 ± 12.2 days, com- 2 3 Bay (Beidagang Reservoir, Nandagang wetlands and pared to 30.0 ± 16.0 days during autumn migration. 3 4 Yellow River Estuary) for their first stopover. One bird Three national nature reserves and one provincial nature 4 5 (ID#cas004) flew non-stop for almost 2500 km directly reserve were used by tagged geese as stopover sites: (i) 5 6 to the wintering sites in 2015. In 2015 and 2016, anoth- Yancheng National Nature Reserve; (ii) Yellow Riv- 6 7 er bird (ID#cas003) used farmland in Anhui Province in er Estuary; (iii) Beidagang Reservoir; and (iv) Nanda- 7 8 China as the stopover site for final refueling. ID#2042 gang wetland (Table 2). During spring migration, the 8 9 undertook a change in migratory direction, moving east tagged Greylag Geese used these nature reserves for a 9 10 from its previous track line to stop on the coast at the mean of 27.3 ± 10.7 days compared to 31.4 ± 17.1 days 10 11 Yancheng National Nature Reserve for 20 days before during autumn migration. During spring migration, the 11 12 flying directly to its ultimate wintering area. Autumn tagged Greylag Geese spent 84% of their stopover dura- 12 13 migration was completed between the end of October tion within IBA sites and 68% of their stopover duration 13 14 and mid-December, with all tagged Greylag Geese win- in the protected areas. During autumn migration, the 14 15 tering along the Yangtze River (Figs 1a and 2a). tagged Greylag Geese spent 69% of their stopover dura- 15 16 tion within IBA sites, same in protected areas. 16 17 Wintering area, summering area and stopover 17 18 sites Migration parameters 18 19 19 All of the tagged Greylag Geese in this study win- During spring migration, tagged Greylag Geese took 20 20 tered in several lakes along the Yangtze River (Fig. 2a). 34.4 days (median value, interquartile range, henceforth 21 21 Most of the tagged Greylag Geese visited Poyang Lake, [IQR] = 6.9) to fly 2296.2 km (IQR = 257.3) between 22 22 while others used Hubei, Longgan, Qingcao and Caizi wintering and summering areas. They spent on average 23 23 Lakes. Several of the tagged individuals shifted between 32.2 days (IQR = 14.7) at a median of 2 (IQR = 1) stop- 24 24 sites on multiple occasions within winters (Fig. 2a). The over sites during spring migration. The spring migra- 25 25 mean duration of the wintering period for the tagged in- tion speed was 62.5 km/day (IQR = 25.6) and the daily 26 26 dividuals was 106.3 ± 26.6 days. In summer, the tagged travel speed was 657 km/day (IQR = 577.8), with a me- 27 27 Greylag Geese used Khukh Lake in Mongolia, Hulun dian straightness index of 0.9 (IQR = 0.1). During au- 28 28 Lake in China, the Wulan Nuo’er wetlands in China, tumn migration, the same birds took 38.6 days (IQR = 29 29 Buir Lake in Mongolia, Huihe National Nature Reserve 23.6) to fly 2409.1 km (IQR = 314.1) from summer- 30 30 in China and the Wulagai Gaobi wetlands in China as ing areas to wintering areas, stopping 2 (IQR = 1) times 31 31 the main summering and molting sites (Fig. 2b). Tagged and spending 35.6 days (IQR = 23.9) on autumn stop- 32 32 birds remained on the summering areas for a mean of over sites. The autumn migration speed was 65.6 km/ 33 33 152.5 ± 45.1 days. During spring migration, Greylag day (IQR = 30.2) and the daily travel speed was 973.7 34 34 Geese used 8 major stopover sites for refueling (Table 2). km/day (IQR = 530.7), with a median straightness index 35 35 The median stopover duration at those sites was 32.2 of 0.9 (IQR = 0.1), identical to spring. The autumn mi- 36 36 days during spring migration, with most using stopover gration duration and stopover duration were significant- 37 37 sites in the Yellow River Estuary and Xar Moron Riv- ly longer than for spring (W = 1, P = 0.009 and W = 1, 38 38 er. The tagged Greylag Geese stopped over in the Yel- P = 0.009, respectively). The autumn migration speed 39 39 low River Estuary (mean 27.8 days) and the individu- was significantly lower than in spring (W = 27, P = 0.03, 40 40 als using the Xar Moron River stopped over for a mean Table 3 and Fig. S1). The number of stopover sites, mi- 41 41 of 10.9 days. During autumn migration, the same birds gration distance, daily travel speed and straightness in- 42 42 used 10 dispersed stopover sites (Table 1) for a median dex did not differ significantly between spring and au- 43 43 of 35.6 days; 4 individuals used the Yellow River Estu- tumn migrations. 44 44 ary for a mean of 28.2 days. 45 Discussion 45 Along the Mongolian-Manchurian/Chinese migra- 46 This is the first study of the migratory routes and pat- 46 tory greylag goose flyway, the movements of tagged 47 terns used by Far East Greylag Geese breeding in wet- 47 birds identified important stopover sites at Beidagang 48 lands within the Mongolian-Manchurian Grassland 48 Reservoir, Nandagang wetland, Yellow River Estuary 49 Steppe Ecoregion (Olson et al. 2001). Migration routes 49 and the Xar Moron River (all are IBAs) as being im- 50 used by 10 individuals over multiple years identified 50 51 portant stopover sites during spring and autumn passag- 51

1 Table 3 Median and Wilcoxon rank-sum test of migration parameters of tagged adult Greylag Geese. Full migration parameters for 1 2 individual birds are reported in Table 1 2 3 Median values Wilcoxon test 3 4 Parameters 4 Spring Autumn W P-value 5 5 6 Migration duration 33.7 52.7 1 0.009 6 7 Number of stopover sites 1.5 2 12 0.614 7 8 Stopover duration 31.1 51.3 1 0.009 8 9 9 Migration distance 2261.1 2531.1 5 0.082 10 10 11 Migration speed 62.6 47.9 27 0.030 11 12 Daily travel speed 865.3 973.7 13 0.792 12 13 Straightness index 0.9 0.8 18 0.662 13 14 14 15 15 16 16 17 17 18 the relationships between their stopover sites, breed- in IBAs/protected areas but especially in unprotected ar- 18 19 ing, molting and wintering grounds, and highlighted the eas elsewhere, to ensure the extent and quality of stag- 19 20 conservation needs of this species along their migration ing habitats is maintained for these birds during their 20 21 routes, especially during prolonged periods at stopover critical stopover periods. We recommend attention be 21 22 sites. During spring and autumn migration, these birds paid to sites along the Xar Moron River based on use by 22 23 used 13 stopover sites, among which most individu- tagged geese in this study. Compared to the Yancheng 23 24 als used Xar Moron River, Beidagang Reservoir and the National Nature Reserve (used by only one bird for 20 24 25 Yellow River Estuary. Although we should be prudent days in autumn migration), the currently unprotected 25 26 about interpreting patterns from just 10 marked indi- Xar Moron River was used by 5 individuals for 4–18 26 27 viduals, it seems likely, based on the frequency and du- days during spring migration. 27 28 ration of use, that these sites are important for this fly- Our results confirmed that the migration duration and 28 29 way population of Greylag Geese. The marked Greylag stopover duration in autumn migration were statistical- 29 30 Geese used IBAs, non-IBAs, protected and non-protect- ly significantly longer than in spring for adult birds and 30 31 ed areas as stopover sites for refueling. During spring migration speed in autumn migration was lower than in 31 32 migration, the tagged Greylag Geese spent 84% of the spring for adult birds. In contrast, numbers of stopover 32 33 stopover duration on the IBA sites and 68% of the stop- sites, migration distance, daily travel speed and straight- 33 34 over duration in other protected areas. During autumn ness indices showed no relation to season. It was re- 34 35 migration, the tagged Greylag Geese spent 69% of the markable that one individual, ID#cas004, flew almost 35 36 stopover duration on both IBA sites and other protect- 2500 km non-stop from its summering area to the win- 36 37 ed areas. The fact that so many of the sites used by Far tering grounds during the 2015 autumn migration. This 37 38 East Greylag Geese are either IBAs or enjoy some lev- shows that Greylag Geese can complete this entire mi- 38 39 el of site safeguard gives cause for satisfaction in the ef- gration in one leg, implying the ability to accumulate all 39 40 fectiveness of current migratory waterbird protected the necessary energy stores before undertaking the jour- 40 41 area networks to protect this species. However, there re- ney without stopovers (Smith et al. 1986). These find- 41 42 main a multitude of threats to the integrity of these ar- ings corresponded to empirical findings that most mi- 42 43 eas, including those from habitat destruction and dete- gratory birds travel faster in spring than autumn because 43 44 rioration, pollution, declining water quality and illegal long-distance migrants are more time-limited during 44 45 hunting pressure. For this reason, we recommend fol- spring migration (Shimada et al. 2016). Theory pre- 45 46 low-up ground surveys in spring and autumn at all these dicts that competition for best breeding sites might be 46 47 sites to establish the numerical importance and precise the dominant driver for arrival earliest at limited breed- 47 48 habitat utilization by Greylag Geese in these areas with ing sites, which suggests that migrants should adopt the 48 49 a view to improved site protection of roost sites and time minimization strategy during spring migration to 49 50 feeding areas and better management of habitats for the arrive as early as possible in the best possible condition 50 51 staging geese. Such information is essential both with- at breeding sites (Kokko 1999). 51

1 Notwithstanding the results above, marked Greylag Yalu River could also be due to the weather and climate 1 2 Geese stopover duration and migration duration during patterns during their migration (Batbayar et al. 2011). 2 3 autumn migration were both longer than spring. Avail- This research has highlighted the precise nature of the 3 4 ability of stopover sites and duration of stay are import- migration patterns of the Mongol-Manchurian Grass- 4 5 ant parts of the annual cycle and influence birds’ migra- land Steppe Ecoregion breeding Greylag Geese and pro- 5 6 tion strategies, implying a physiological need to acquire vided insights into the relative speed and duration of 6 7 stores for the next phase of the annual cycle (Berthold spring versus autumn migratory episodes, but despite 7 8 et al. 2003; Newton 2010). Hence, the prolonged nature the new knowledge, we remain cautious of inferring 8 9 of the autumn migration for some birds may be the re- too much from just 10 individuals. It remains far from 9 10 sult of the need to restore severely depleted body stores clear how much of the Yangtze River Floodplain winter- 10 11 in the prelude to autumn staging (i.e. in preparation for ing stock of Greylag Geese derive from this area and to 11 12 the next phase of migration) or the need to acquire extra what extent its breeding numbers have been affected by 12 13 body stores as a hedge against potential food shortag- recent periods of cyclical drought, which have been ex- 13 14 es on arrival to the winter quarters. Studies suggest that acerbated by climate forcing in the Mongol-Manchuri- 14 15 in East Asia, tail winds were more favorable to support an Grassland Steppe Ecoregion since 1950s (Bao et al. 15 16 migration in autumn compared to spring (Bozó et al. 2015). For this reason, we recommend further ground 16 17 2018), which might explain the more rapid daily trav- fieldwork and telemetry studies to confirm these pat- 17 18 el speed of our tagged Greylag Geese in autumn com- terns and to enhance our understanding of the contribu- 18 19 pared to spring. Although daily travel speed in autumn tions of different breeding flyways of Chinese wintering 19 20 was faster than in spring, tagged Greylag Geese spent Greylag Geese, as well as improved monitoring of their 20 21 more time at stopover sites in autumn, so total migra- abundance and the demographic parameters that con- 21 22 tion duration was still longer than in spring. There were tribute to the annual rate of population change in this 22 23 no major differences in the routes taken by the geese be- poorly known flyway. 23 24 tween spring and autumn, which were remarkably con- 24 25 25 fined (there being no differences in straightness indices ACKNOWLEDGMENTS 26 between seasons) to relatively well-defined corridors. 26 27 The Greylag Goose and the Swan Goose are close- We gratefully acknowledge the contribution of the 27 28 ly related species (Ottenburghs et al. 2016), wintering at fieldwork teams in China and Mongolia and the catch- 28 29 Poyang Lake (Yu et al. 2017) and breeding in the Mon- ing teams for their contributions. We acknowledge the 29 30 gol-Manchurian Grassland Steppe Ecoregion. Despite constructive suggestions of 2 referees and the editor, 30 31 this, they use different migratory routes and stopover which improved an earlier manuscript. Our study was 31 32 sites. Swan Geese exploit the Yalu River Estuary on the supported by the National Key Research and Develop- 32 33 borders of China and North Korea for refueling forag- ment Program of China (Grant No. 2017YFC0505800), 33 34 ing, mostly on mudflats (Batbayar et al. 2011), where- the National Natural Science Foundation of China (Grant 34 35 as the tagged Greylag Geese in our study stopped over No. 31870369), the Chinese Academy of Sciences Key 35 36 at the Beidagang Reservoir and the Yellow River Estu- Strategic Program, Water Ecological Security Assess- 36 37 ary, foraging mostly on farmland. These patterns may ment, the Major Research Strategy for Middle and Low- 37 38 reflect contrasting diet and habitat selection by both spe- er Yangtze River (Grant No. ZDRW-ZS-2017-3-3), In- 38 39 cies at other times of the annual cycle. Greylag Geese ternational Cooperation and Exchange project NSFC 39 40 tend to feed largely on agricultural habitats throughout (Grant No. 31661143027), the National Natural Science 40 41 their European range (Kear 2005) and to a greater extent Foundation of China (Grant No. 31670424) and Chi- 41 42 than most species in China (Yu et al. 2017). Such flexi- na Biodiversity Observation Networks (Sino BON). The 42 43 bility may enable the Greylag Geese to exploit a broad- funders had no role in the study design, data collection 43 44 er range of natural, semi-natural and farmland foods ac- and analysis, decision to publish, or preparation of the 44 45 cording to local resource abundance, availability and manuscript. The Animal Ethics Committee, Research 45 46 the risk of predation/disturbance by predators and hu- for Eco-Environmental Sciences, Chinese Academy of 46 47 mans. In contrast, Swan Geese usually use natural wet- Sciences fully approved this study. The wild bird cap- 47 48 lands as stopover sites during migration (Batbayar et al. ture and sampling permit for Mongolia was granted to 48 49 2011), restricting their possibilities to stop over for re- the Wildlife Science and Conservation Center of Mon- 49 50 fueling elsewhere. Their conspicuous reliance upon the golia from the Ministry of Environment and Tourism of 50 51 51

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