Zhang et al. Avian Res (2020) 11:49 https://doi.org/10.1186/s40657-020-00230-9 Avian Research

RESEARCH Open Access Assessing site‑safeguard efectiveness and habitat preferences of Bar‑headed Geese (Anser indicus) at their stopover sites within the Qinghai‑Tibet Plateau using GPS/ GSM telemetry Junjian Zhang1,2, Yanbo Xie3, Laixing Li4, Nyambayar Batbayar5, Xueqin Deng1,2, Iderbat Damba1,6, Fanjuan Meng1, Lei Cao1,2* and Anthony David Fox7

Abstract Background: The Bar-headed Goose (Anser indicus) breeds across the high plains and plateau of Central Asia and winters in the Qinghai-Tibet Plateau (QTP), the Yunnan-Guizhou Plateau and the Indian sub-continent. Of the two rec- ognized discrete fyways of the Bar-headed Goose, the Eastern Tibetan Flyway (ETF) is the larger, comprising at least six migration routes. However, we remain ignorant about their migratory connectivity, habitat use and efectiveness of site-safeguard mechanisms set in place for the species. Methods: We tracked 30 ETF Bar-headed Geese from Chinese and Mongolian breeding areas to their wintering grounds using GPS/GSM transmitters, to determine their migration routes and stopover staging patterns within the QTP, overlaying these upon GIS layers of protected area status and habitat type, to model their habitat selection. Results: In total, 14 tagged Bar-headed Geese provided information on their entire autumn migration and 4 geese on their entire spring migration. Qinghai Lake marked birds overwintered in the QTP (n 2), geese tagged in Mongo- lia wintered either in the QTP (n 3) or in India/Bangladesh (n 9), representing three of= the migration routes within the ETF. In total, tagged birds staged= at 79 diferent stopover sites= within QTP in autumn and 23 in spring, of which 65% (autumn) and 59% (spring) of all fxes fell within the boundaries of either National Nature Reserves (NNRs) or Important Birds Areas (IBAs) in the QTP. Bar-headed Geese predominantly occurred on four land-cover types: grass- land (mostly by day), water bodies (at night), wetlands and bare substrates (salt fats, dry lake/river substrates and plough) with little change in proportion. Generalized linear mixed models comparing presence with pseudo-absence data suggested geese strongly selected for wetlands as staging habitat, avoiding bare substrates in spring. Conclusions: Based on our limited observations of these tagged geese, this study is the frst to show that the current designated National Nature Reserves in place in the staging areas within the QTP appear adequate to protect this increasing population. In addition, Hala Lake in Qinghai Province and adjacent areas used as initial QTP staging during

*Correspondence: [email protected] 1 State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China Full list of author information is available at the end of the article

© The Author(s) 2020. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativeco​ ​ mmons.org/licen​ ses/by/4.0/​ . The Creative Commons Public Domain Dedication waiver (http://creativeco​ mmons​ .org/publi​ cdoma​ in/​ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Zhang et al. Avian Res (2020) 11:49 Page 2 of 13

autumn migration (currently outside of designated as NNRs/IBAs) are recommended for protection, based on their use by tagged birds from this study. Habitat modelling confrmed the importance of natural wetlands as feeding areas and safe areas of open water as roosting places. Keywords: Anser indicus, Bar-headed goose, Habitat use, Habitat selection, Important bird area, National nature reserve

Background the potential to rapidly transmit HPAI along its migration Te Bar-headed Goose (Anser indicus) has increased routes (Liu et al. 2010). greatly in abundance since the 1990s, reaching an esti- Te ETF includes more than 70% of the individuals in mated world population of 97,000‒118,000, distrib- the global population, and most previous studies of this uted across a fragmented breeding range throughout fyway have focused on their breeding and wintering the high plains and plateaux of Central Asia (Liu et al. grounds. For instance, breeding habitat use and selec- 2017; Fox and Leafoor 2018). Previous telemetry stud- tion of the Bar-headed Geese has been studied at Qinghai ies have demonstrated the existence of two major fy- Lake in China (Liu et al. 2008; Cui et al. 2011; Zhang et al. ways of this species in Central Asia (Additional fle 1: Fig. 2011b) and Hangcuo Lake (Zhang et al. 2011a), west- S1; Prosser et al. 2009, 2011; Bourouiba et al. 2010; Hao central Mongolia (Batbayar et al. 2014) and Ladakh in et al. 2010; Köppen et al. 2010; Zhang et al. 2011b; New- India (Prins and van Wieren 2004). Similar studies have man et al. 2012). Tese can be summarized as follows. taken place on the wintering grounds, including at Cao- Te frst fyway is the Western Tibetan Flyway, breed- hai Lake (Yang et al. 2012, 2013), Lashihai Lake (Yan et al. ing in SE Kyrgyzstan, Kazakhstan and the NW Xinjiang 2014) and Yamdrok Lake (Zhang et al. 2016) in China, Uygur Autonomous Region in China. Tese birds winter and Keoladeo National Park in India (Middleton 1992). in Pakistan and the Western Indian subcontinent and Tese studies are important, because Bar-headed Geese comprise more than 30,000 birds, based on wintering distribute two-thirds of their year between the breed- counts, including 1800‒5000 in Pakistan (Li et al. 2009; ing and wintering sites (Takekawa et al. 2017). However, Van der Ven et al. 2010), and 19,000‒40,000 at Pong Dam few studies have attempted to identify crucial stopo- (Takekawa et al. 2017), the major site for the species on ver sites used during migration, especially in the ETF the Indian subcontinent. (Hao et al. 2010; Zhang et al. 2011b; Prosser et al. 2011). Birds from the second fyway, the Eastern Tibetan Fly- Although the migration period comprises only one-third way (hereafter ETF), breed from Western Mongolia, the of the annual cycle of the geese, energy acquisition to SE Xinjiang Uygur Autonomous Region, China to the fuel migration can be critical and it is known that migra- Qinghai-Tibet Plateau, China (hereafter QTP). Tese tion mortality can exceed 85% of overall annual deaths in birds are thought to winter mainly in the southern QTP some species (Ydenberg 2017). Hence, an understanding and the Yunnan-Guizhou Plateau in China, through- of stopover sites used by Bar-headed Geese is fundamen- out the Central and Eastern Indian subcontinent, and in tal to our ability to efectively conserve the species and Myanmar. Tis population is estimated to number more understand the potential for disease transmission. than 80,000 birds based on wintering counts, including Te Bar-headed Goose is famous for its trans-Himala- 67,000 along the Yarlung Zangbo River and adjacent area yan migration and studies have demonstrated its physi- (Liu et al. 2017), 5300‒7200 on the Yunnan-Guizhou Pla- ological adaptations for fying at altitudes over 6000 m teau (Yang 2005; Yang and Zhang 2014) and 3500‒5800 where oxygen pressure is very low (Hawkes et al. 2011, in Nepal/Bangladesh/Myanmar (Li et al. 2009; Takekawa 2013, 2017; Bishop et al. 2015). Due to the lower air den- et al. 2009; Van der Ven et al. 2010). Unknown numbers sity, Bar-headed Geese fying at such altitudes, sufer not also winter in East India. only severe hypoxia, but increase wing beat rates com- Movements of the Bar-headed Goose were closely pared to those at sea level to gain the same lift efect, studied after an outbreak of highly pathogenic avian doubling the power requirement (Bishop et al. 2015). infuenza (HPAI) H5N1, which killed more than 3000 Bearing this in mind, however, given the importance of geese in Qinghai Lake (Chen et al. 2006). Tese studies their stopover sites within QTP to provide the necessary identifed the importance of tracking their annual move- energy to cross the QTP, complete their migration and ments, because such an increasing and expanding spe- breed successfully, we know lamentably little about the cies, showing diverse migration routes and which often precise Bar-headed Goose staging areas, habitat prefer- uses agriculture areas during staging and in winter, has ences and their conservation status there. Zhang et al. Avian Res (2020) 11:49 Page 3 of 13

Here, we attempt to defne Bar-headed Goose habi- Devices attached in 2016 and 2018 were set to record tat selection (as distinct from simple habitat use; Jones the GPS locations at 2 h and 10 min intervals through- 2001) to understand how the birds might be showing out the research project, respectively. Some individuals behavioral responses to changes in habitat conditions, were tracked for more than one year and two individuals which potentially afect the survival and adaptability of migrated together. To avoid pseudo-replication, only the individuals (Block and Brennan 1993). Only by reveal- frst spring and autumn migration tracks were selected ing habitat selection patterns, can we fully understand from each individual, and only one bird from the indi- the spatial and temporal distribution of the Bar-headed viduals that accompanied each other on migration were Geese we follow. Based on results from a previous study, selected (Additional fle 2: Table S1). which used geographical information to model habitat selection in ETF breeding areas (Zheng et al. 2018), we Identifying stopover sites identifed six key parameters in modelling habitat selec- We applied the method of Wang et al. (2018) to segment tion, including land cover (each class is treated as a sepa- movement tracks into “fy” and “non-fy”, then we plot- rate variable), elevation, slope, aspect, distance to river/ ted locations in Google Earth to visualize movements, lake and road. pinpoint arrival and departure dates at sites, and evalu- In this investigation, we applied further telemetry ate where birds were wintering, summering or stopping devices to samples of birds on their key breeding areas (Page et al. 2014). We defned stopover sites as locations in China and Mongolia, to extend earlier studies of this where a bird did not move > 30 km over a 48 h period species, with the specifc aim of identifying key staging (Kölzsch et al. 2016). Te staging areas, which include areas throughout the migratory life cycle of these birds. at least two stopover sites with distance less than 30 km Most importantly, we specifcally compare the areas from each other, were identifed and categorized by used by tagged Bar-headed Geese to assess the efective- manual checking on maps and Google Earth according ness of currently designated areas in the QTP to protect to duration and location (Chen et al. 2016). In order to key staging areas during migration for the species and to exclude the moving positional fxes during stopovers, determine their habitat use and selection at these areas. we only retained the GPS locations where the velocity between adjacent points was less than 1 km/h. Methods Capture of individuals and transmitter attachment Conservation status of stopovers within the Qinghai‑Tibet In June 2016, three Bar-headed Geese (of unknown age Plateau and sex) rescued and rehabilitated by the Qinghai Lake We attempted to assess the efectiveness of the current National Nature Reserve Rescue Center were ftted with extent of designated Important Bird and Biodiversity neck collar-mounted GPS/GSM loggers (weight 40 g, Areas (IBAs), and National Nature Reserves of China Hunan Global Messenger Technology Co., China) and (NNRs) for the protection of stopover sites in the QTP released at Qinghai Lake (37.07 °N, 99.82 °E, China). used by these tagged Bar-headed Geese. We downloaded Te signal was lost from one of the birds during autumn China’s IBA (BirdLife International 2020) and NNR migration, but the two other geese completed their boundary information with permissions (https​://www. autumn migrations in 2016. resdc​.cn/data.aspx?DATAI​D=272). We then overlaid In July 2018, 27 individuals (adult, unknown sex) were all stopover sites in the QTP used by tagged Bar-headed rounded up during the fightless moult period and cap- Geese in our study through ArcMap 10.6 to identify tured at Terkhiin Tsagaan Lake (48.15 °N, 99.59 °E, Mon- which GPS fxes were located within IBA and NNR golia) and Bayan Lake (49.94 °N, 93.90 °E, Mongolia), and boundaries. ftted with backpack-mounted GPS/GSM loggers (weight 27.5 g, Ornithology and Telemetry Applications, UAB). Environmental variables Of these marked birds from Mongolia, 13 geese provided To characterize the landcover used by tracked geese, we complete data on the full autumn migration in 2018 used the “FROM-GLC 2017v1” land cover dataset (reso- (among them, two geese accompanied each other on lution 10 m × 10 m) created by the Department of Earth migration), and four geese on the full spring migration in System Science, Tsinghua University (Gong et al. 2019). 2019. Although we cannot eliminate the possibility that Te dataset is based upon 10 land cover classifcation the ftted devices afected the behaviour and ecology of types, namely artifcial surfaces, bare substrate, cropland, these individuals, the loggers constituted much less than forest, grassland, permanent snow/ice, shrubland, tun- 3% to individual total body mass above which it is consid- dra, wetland and water bodies. Wetland includes marsh- ered this may more likely occur (Millspaugh and Marzluf land and mudfats with natural and semi-natural aquatic 2001; Bodey et al. 2018). or regularly fooded vegetation; water bodies include Zhang et al. Avian Res (2020) 11:49 Page 4 of 13

natural and artifcial waterbodies, such as lake, river and AUC values can range between 0 and 1, where 0.5 indi- reservoir/pond (for detailed defnitions of land cover cates predictions no better than chance, 1 indicates per- categories, see Gong et al. 2013). We assigned each GPS fect discrimination, with values above 0.7 being generally location within the stopover sites in the QTP to a specifc accepted as indicating reasonable predictions (Hosmer land-use type defned by the land cover data using R 3.6.0 et al. 2013). Finally, we applied odds ratios to evaluate (R Core Team 2019). GPS fxes were assigned to day or efect size of the variables (Szumilas 2010). night based on local sunrise and sunset times calculated by “solartime” package (v0.0.1; Wutzler 2018). Results We used elevation data measured from SRTM3-DEM Tracking results dataset (resolution 30 m × 30 m) created by NASA and A total of 17 geese in autumn, and 8 geese in spring NIMA, and calculated slope and aspect (defned as a began migration with functioning transmitters, how- parameter value running from 0 to 360, starting from the ever, due to mortalities and transmitter malfunction, we West and increasing clockwise) for each GPS fx using were only able to obtain information on the full migra- ArcMap 10.6. Finally, we calculated the shortest distance tion for 14 and 4 geese during autumn and spring migra- of each GPS fxes in stopovers to roads (downloaded tion, respectively. Based on the complete migration data from https​://www.world​clim.org/) and rivers (down- from 2016 and 2018 combined, the tagged birds fol- loaded from https​://downl​oad.csdn.net/downl​oad/weixi​ lowed three diferent migration routes. Birds marked at n_38779​546/10613​773), respectively. Qinghai Lake overwintered in the Shigatse Prefecture of Tibet Autonomous Region (TAR) (n = 2), whereas geese Resource selection modeling marked in Mongolia either wintered in the Shigatse Pre- We used generalized linear mixed models (GLMMs) with fecture (n = 3) or continued down into India (n = 7) or a binomial error structure to evaluate stopover resource Bangladesh (n = 2) to winter (Fig. 1). In addition, tracked selection during autumn and spring migration respec- geese (another three geese in autumn and another four tively, with use/availability as response variable and envi- in spring that started but did not complete migration) ronment variables as explanatory variables (Meng et al. staged at 79 diferent stopover sites in autumn and 23 in 2020). We diluted GPS fxes to hourly intervals to reduce spring within the QTP (Fig. 1; Additional fle 2: Tables S2, the potential for autocorrelation (Signer et al. 2019). S3). Te cumulative time that all birds spent at stopover Availability data (i.e., pseudo-absence data) at each sites within the QTP totaled 1445 h, which constituted stopover site were generated by creating 100% minimum 86.7% of the entire stopover duration (1667 h). convex polygons (MCPs) based on each set of positions Tagged Bar-headed Geese that summered in Mon- for tagged individuals. We extended these outwards by golia and wintered in India/Bangladesh, arrived in the 11.3 km (the average maximum hourly displacement QTP during autumn migration on average on Septem- for all individuals at all stopover sites) in all directions ber 8 (± 7 days standard deviation; n = 9 individuals) around the MCPs to represent the area potentially avail- and left the QTP on November 19 (± 13 days). In spring, able to each of the staging birds. We then randomly they arrived in the QTP from India or Bangladesh on selected locations from the extended MCP for each stop- average on March 15 (± 6 days; n = 6) and left on April over site as pseudo-absence data, generating 20 pseudo- 25 (± 6 days; n = 3; another three geese started but did absence points for each positional fx to gain stable and not complete migration). Bar-headed Geese spent an unbiased parameter estimates (Northrup et al. 2013). average of 72.3 ± 17.3 days (n = 9) and 44.3 ± 7.1 days Rare land cover types (< 5% of total land use by either (n = 3) in the QTP during autumn and spring migration use or availability data points) were excluded (namely respectively. artifcial surfaces, cropland, forest, shrubland, tundra and snow/ice), to escape model convergence problems likely Conservation status of stopover sites below such levels (Altman et al. 2004). We rescaled vari- Data from the goose-borne loggers generated 123,539 ables using the “scale” function in “base” package in R, non-moving GPS fxes in autumn and 51,282 in spring following the method of Becker and Chambers (1984) to at stopover sites within the QTP. Of these, 59% and estimate the efect size of explanatory variables. 53% of GPS fxes in autumn and spring respectively We used the “dredge” function in “MuMIn” package fell within NNRs, while 27% and 23% of GPS fxes were (v1.43.10; Bartoń 2019) in R to develop our resource from within IBAs. Overall, 65% and 59% of GPS fxes selection model using model weights derived from AICc were from within NNRs/IBAs (Figs. 2, 3; Additional criteria. Te cross-prediction accuracy of our resource fle 2: Table S4). In all, we found 12 important staging selection model was tested by estimating the area under areas with at least two stopover sites (Table 1). Among the receiver operating characteristic (ROC) curve (AUC). Zhang et al. Avian Res (2020) 11:49 Page 5 of 13

Fig. 1 Autumn and spring individual migration routes (black lines) and stopover sites (green circles) of Bar-headed Geese (Anser indicus) derived from GPS/GSM telemetry devices deployed on birds tracked in 2016 and 2018/2019. The shaded red region shows the Qinghai-Tibet Plateau. TtoT: Qinghai Lake Shigatse Prefecture routes; MtoT, Mongolia Shigatse Prefecture routes; MtoA, Mongolia-India/Bangladesh routes. Sample sizes are − − indicated by n (number of individuals fnishing migration)

these, there were three areas containing at least three (3) Duoqingcuo Lake, TAR, Ns = 11 (No. 12; a national stopovers, which fell outside existing NNRs/IBAs des- wetland park and close to the highway). ignation (Fig. 2). Tese were: (1) Shule River, Qinghai Habitat use and selection in stopover sites Province, Ns = 6 (Ns in each case represents the num- ber of stopovers; No. 2 in Table 1; close to Hala Lake); Habitat types used by the Bar-headed Geese were pre- (2) Dangqu River, TAR, Ns = 3 (No. 11; outside of the Se dominantly natural ecosystems: 31% grassland, 29% bare Lin Cuo NNR and near downtown Dangxiong county); substrate (including dry salt fats, bare herbaceous crop- lands and dry lake/river bottoms; Gong et al. 2013), 26% water bodies and 11% wetlands. Habitat types used by Zhang et al. Avian Res (2020) 11:49 Page 6 of 13

Fig. 2 GPS fxes of stopover sites within the QTP for tagged Bar-headed Geese during autumn and spring migration in 2016 and 2018/2019. a stopovers during autumn migration; b stopovers during spring migration. NNRs: National Nature Reserves of China; IBAs: Important Bird and

Biodiversity Areas; QTP, the Qinghai-Tibet Plateau. Sample sizes are indicated by n (number of instrumented individuals generating the data), Ns (number of stopovers within QTP) and Ng (total number of GPS fxes per category). The explanations apply also to Figs. 3, 4 Zhang et al. Avian Res (2020) 11:49 Page 7 of 13

geese difered between day (the majority on grassland, 47% in autumn and 33% in spring) and night (when the majority were using waterbodies, 33% in autumn and 41% in spring), but were similar during autumn and spring migration (Fig. 4). Comparing GLMMs results, the best ft models for predicting spring and autumn Bar-headed Goose stopo- ver sites within the QTP were based on the same nine parameters. Tese included the four habitat types, as well as slope, aspect, elevation, distance to roads and rivers (autumn: weight = 1.000, AUC = 0.80; spring: weight = 1.000, AUC = 0.83; Table 2). All these param- Fig. 3 Conservation status of Bar-headed Geese stopovers within eters are signifcant (p < 0.001; Fig. 5). Among habitat the Qinghai-Tibet Plateau during autumn (totally 63.3%) and spring types, Bar-headed Geese tended to strongly select wet- (58.7%) migration in 2016 and 2018/2019 lands (βautumn = 1.94, βspring = 2.03), slightly select water bodies (βautumn = 0.62, βspring = 0.80), slightly avoided to select grassland (βautumn = ‒0.95, βspring = ‒1.05), and were least likely to select bare substrates in spring (βspring = ‒2.01). Among terrain variables, geese tended to select stopovers facing south (βautumn = 0.30,

Table 1 Important staging areas used by tagged Bar-headed Geese (Anser indicus) migrating in the Eastern Tibetan Flyway in 2016 and 2018/2019 No Stopover sites & coordinates Season No. Date range Length of stay Protection status IBA of stopovers (range in days) sites (Y/N)

1 River of Subei Mongolian Autono- Autumn 3 9/2‒9/21 4‒16 Yan Chi Wan National Nature Reserve N mous County, Gansu Province, Spring 1 4/25 6/4 41 China (95.829 °N, 39.105 °E) ‒ 2 Shule River, Tianjun County, Qinghai Autumn 5 9/2‒9/29 3‒11 None N Province, China (98.321 °N, 38.297 Spring 1 5/13 5/17 5 °E) ‒ 3 Lake of Madoi County, Qinghai Prov- Autumn 5 8/27‒11/9 8‒63 San Jiang Yuan National Nature Y ince, China (97.773 °N, 34.848 °E) Reserve Spring 2 4/12‒5/11 11‒16 4 River of Qumarleb County, Qinghai Autumn 5 9/18‒10/24 4‒23 San Jiang Yuan National Nature N Province, China (96.654 °N, 35.083 Reserve °E) 5 River of Qumarleb County, Qinghai Autumn 2 9/1‒11/1 3‒9 San Jiang Yuan National Nature N Province, China (95.141 °N, 35.265 Reserve °E) 6 River of Qumarleb County, Qinghai Autumn 4 9/11‒10/14 3‒20 San Jiang Yuan National Nature N Province, China (93.707 °N, 34.67 °E) Reserve 7 River of Zhidoi County, Qinghai Prov- Autumn 6 9/2‒11/15 5‒21 San Jiang Yuan National Nature N ince, China (93.581 °N, 33.86 °E) Reserve 8 Lake of Zadoi County, Qinghai Prov- Autumn 7 9/2‒10/22 4‒27 San Jiang Yuan National Nature Y ince, China (93.497 °N, 33.025 °E) Reserve Spring 1 4/17‒4/27 11 9 Lake of Ando County, Tibet, China Autumn 3 10/1‒10/24 2‒8 Se Lin Cuo National Nature Reserve N (91.491 °N, 31.992 °E) Spring 2 4/3‒4/24 2‒22 10 Lake of Naqu County, Tibet, China Autumn 5 10/9‒10/31 2‒20 Se Lin Cuo National Nature Reserve N (91.506 °N, 31.424 °E) Spring 2 4/5‒4/15 3‒5 11 Dangqu River, Damxung County, Autumn 2 10/26‒11/14 4‒13 None N Tibet, China (91.165 °N, 30.525 °E) Spring 1 4/13‒4/21 8 12 Duoqingcuo Lake, Yadong County, Autumn 8 10/21‒11/19 8‒24 None N Tibet, China (89.357 °N, 28.139 °E) Spring 3 3/6‒4/12 20‒26 Only areas with at least two stopovers sites where the estimated duration of stay was at least two days are shown Zhang et al. Avian Res (2020) 11:49 Page 8 of 13

Discussion Te results of this tracking study clearly show that three NRRs: Yan Chi Wan (Gansu Province), San Jiang Yuan (Qinghai Province), and Se Li Cuo (TAR) are of critical importance to Bar-headed Geese in the ETF during both autumn and spring migration. In particular, the impor- tance of rivers in Yan Chi Wan (No. 1 in Table 1) and San Jiang Yuan NNRs (No. 5, 6) were not previously known. Overall, 65% of autumn GPS fxes were from within NNRs/IBAs and 59% in spring. Our studies confrmed the importance of Hala Lake (close to Shule River, No. 2), San Jiang Yuan NNR (No. 3, 4) and Se Lin Cuo NNR (No. 7‒10) indentifed by tagged Bar-headed Geese in previ- ous studies (Hao et al. 2010; Zhang et al. 2011b; Prosser et al. 2011). Nevertheless, our tracking data found addi- Fig. 4 Percentage habitat use of Bar-headed Geese during stopovers within the Qinghai-Tibet Plateau during autumn and spring migration tional areas frequently used by tracked geese, which are in 2016 and 2018/2019 respectively, based on positional fxes from not currently designated as NNRs/IBAs. Of these, the deployed GPS loggers overlaid on land-cover maps of the world (see most important appear to be the Shule River, Qinghai Methods) Province, the Dangqu River, TAR and Duoqingcuo Lake, TAR, all of which are recommended for ground survey during the migration season based on their prolonged Table 2 Model selection results for the top fve stopover use (3‒26 days) by tagged birds from this study. habitat selection analysis models for the Bar-headed We would also recommend surveying the suitability of Geese during autumn and spring migration in 2016 and 2018/2019 respectively adding Hala Lake and adjacent areas (97.60 °N, 38.30 °E; Fig. 2) to the protected area network for this species, as a b Season ID Model structure­ df ΔAIC Weight part of the ecological redline for the region. Tis is part of Autumn 1 LC ROA RIV ELV SLP ASP 12 0.0 1 the NE edge of the QTP which represents the frst stag- + + + + + 2 LC ROA RIV SLP ASP 11 206.6 0 ing area encountered and used by geese during autumn + + + + 3 LC RIV ELV SLP ASP 11 397.4 0 migration, yet very few of our tracked birds used areas + + + + 4 LC ROA ELV SLP ASP 11 567.8 0 inside the current protected area boundaries, despite + + + + 5 LC RIV SLP ASP 10 607.4 0 the importance of the position of this area in the overall + + + Spring 1 LC ROA RIV ELV SLP ASP 12 0.0 1 migration network (Xu et al. 2020). + + + + + 2 LC RIV ELV SLP ASP 11 110.9 0 Te ETF represents the larger of the two fyways of the + + + + 3 LC ROA RIV SLP ASP 11 342.6 0 Bar-headed Goose, supporting more than 80,000 individ- + + + + 4 LC ROA ELV SLP ASP 11 437.8 0 uals. Within this fyway, it is thought that there at least six + + + + 5 LC ELV SLP ASP 10 446.4 0 migration routes (Additional fle 1). Tese are: (1) Mon- + + + golia–Yarlung Zangbo River, China; (2) Mongolia–East a LC, land cover; ROA, distance to roads; RIV, distance to river; ELV, elevation; SLP, slope; ASP, aspect Indian sub-continent; (3) Qinghai Lake–Yarlung Zangbo b ΔAIC, the diference between the current model AIC value and the minimum River, China; (4) Qinghai Lake–Yunnan-Guizhou Plateau, AIC value China (Zhang et al. 2011b); (5) Xinjiang–Yarlung Zangbo River, China (Liu et al. 2010); (6) Yarlung Zangbo River, China–Central Indian sub-continent (Newman et al. βspring = 0.32), with low elevation (βautumn = ‒0.12, 2012). Our study only covered the frst three of these βspring = ‒0.31) and slope (βautumn = ‒2.00, βspring = ‒1.17) migration routes, so there remains three other migration both during autumn and spring migration. Among other routes that are poorly studied, not to mention those used variables, geese tended to select stopover sites, which by geese from the Western Tibetan Flyway (Köppen et al. were away from roads (βautumn = 0.16, βspring = 0.29) and 2010). close to rivers (βautumn = ‒0.22, βspring = ‒ 0.43) both dur- After pooling the data from tracked Bar-headed ing autumn and spring migration (see Additional fle 2: Geese (both from this and other studies) which com- Tables S5, S6 for full model details). pleted autumn migration and were captured in Mongo- lia (n = 24) and Qinghai Lake, China (n = 40), 38 of these individuals wintered in the QTP, 25 in Indian sub-conti- nent, and only one on the Yunnan-Guizhou Plateau (Tian Zhang et al. Avian Res (2020) 11:49 Page 9 of 13

Fig. 5 Odds ratios of fxed efects in highest-ranked generalized mixed-efect model for autumn and spring stopovers in 2016 and 2018/2019. Red symbols depict negative efects, and blue symbols depict positive efects. Signifcant results are marked with asterisks (*** indicates p-value < 0.001)

et al. 2015; Takekawa et al. 2017). Tis diversity of migra- extent of wetlands have increased in the eastern part and tion patterns underlines the need to apply telemetry stud- decreased in the western-central sectors (Xu et al. 2019), ies to more Bar-headed Geese marked throughout their factors which may explain increases in breeding Bar- breeding distribution to enable us to better delineate the headed Geese in this area relative to numbers in Mongo- fyway structure of this species, which remains poorly lia. On the other hand, in TAR, the species is considered known, and to ensure adequate site safeguard for geese to be more vulnerable to power line strikes (Li et al. 2011) of diferent breeding provenance. Such an understanding and avian infuenza (Liu et al. 2010). is essential if we are to be able to appraise the efective- Te results from this analysis of habitat use by Bar- ness of the cohesive site-safeguard network to protect headed Geese refect those of many northern hemisphere all the elements of this complex population throughout goose species, which typically feed out in wetlands and its annual cycle. Tis is especially important because the grassland by day but resort to open water bodies by night species exploits arid and high altitude ecosystems at dif- as protection from potential predators (Zhao 2017). ferent times of its annual cycle, all of which are known Bar-headed Geese mainly used natural ecosystems dur- to be particularly susceptible to the efects of current ing migration and on the summering areas, but cropland on-going climate change. For example, efects of climate during winter. In summer, 35% of positional fxes from change at one of the Bar-headed Goose’s major breeding tagged geese captured at Qinghai Lake were from grass- sites in west Mongolia, which has experienced the most land and 54% from wetlands during the breeding and rapid rise in temperatures in the past decade outside of post-breeding period (Prosser et al. 2011). Zheng et al. the Arctic regions (Batbayar et al. 2014), may have seri- (2018) reported 53% of positional fxes from their telem- ous impacts on their breeding success. In the QTP, the etry tracked Bar-headed Geese were from wetland, 21% Zhang et al. Avian Res (2020) 11:49 Page 10 of 13

forest and 18% bare substrate in Qinghai Lake (n = 8). gain maximum solar insolation to stimulate the growth We found very low forest cover when overlaying the of food plants to support fat accumulation during the home ranges from Zheng et al. (2018) on the ESA Global spring migration and shelter from the north wind dur- Cover 2009 maps and goose use of forest habitats seems ing the autumn migration. Geese avoided bare substrates extremely unlikely. strongly in spring, probably because of the low surface During migration, geese mainly used grassland, water temperatures and frost during spring migration in these bodies, wetlands and bare substrates at their stopover areas. Summering Bar-headed Geese at Qinghai Lake sites in our study. Prosser et al. (2011) reported 75% of preferred wetland, open land with sparse vegetation, sites positions of tagged Bar-headed Geese came from grass- close to rivers/lakes and away from roads, croplands and land and > 12% from wetlands during autumn and spring higher elevations (Zheng et al. 2018) and we contest that migration. Both studies therefore confrmed tagged geese they also avoided forest. Wintering Bar-headed Geese mainly used natural ecosystems during migration. Small at Caohai Lake showed a preference for sites with high diferences between our and Prosser et al.’s (2011) results vegetation cover, low vegetation height, far from human may be the consequence of land-cover changes that have disturbance, close to the water, open habitats and lower afected goose habitat availability in the last two decades elevation as their foraging sites (Yang et al. 2013). Our and improvements in accuracy of the land cover dataset. results closely followed theirs, confrming that all stages Prosser et al. (2011) used the 2003 dataset based on 1 km of the life cycle, Bar-headed Geese tend to select wetland resolution, whereas our study used the 2019 dataset with areas, close to rivers/lakes, away from roads and at lower 10 m accuracy. elevations than would be expected by chance. During winter, geese mainly used winter wheat felds, Te habitat selection patterns of Bar-headed Geese also or fallow croplands, rivers, lakes and marshes along the refect patterns shown by Greylag Geese in their breeding Yarlung Zangbo River. Ground counts of feeding geese and wintering areas in East China (Li 2019). Both spe- (n = 44,657 in January 2009) found 72.1% on fallow crop- cies tend to select water bodies and wetland as habitat, land (Liu et al. 2010). Prosser et al. (2011) also reported although Greylag Geese occur in sites nearer to roads tagged geese used 39% cropland near Lhasa city. In addi- and tend to show greater selection for cropland, suggest- tion, Bar-headed Geese also used grassland and crop- ing they are more tolerant of human disturbance than land as their main diurnal feeding areas at Caohai, China Bar-headed Geese. Cropland was not used as a parameter (Yang et al. 2013), Lashihai Lakes, China (Yan et al. 2014) in our model, because it contributed only 1% to habi- and Keoladeo National Park, India (Middleton and Van tat use among tagged Bar-headed Geese. In conclusion, der Valk 1987). Hence, like many northern hemisphere these results, together with the results of previous stud- goose species, the Bar-headed Goose has shown a plas- ies of the species, continue to indicate that Bar-headed ticity that has enabled it to take advantage of the new Geese rely predominantly on wetland and water bodies farmland feeding opportunities on the wintering areas during migration staging in the QTP in the absence of (Fox and Abraham 2017). We speculate that restricted major human impacts on the landscape in these areas. use of croplands in summer and on migration simply In contrast, increasing numbers of Bar-headed Geese refects the general remoteness of the areas that they use are shifting to croplands during the winter. Tis is espe- at these stages of the life cycle, in regions where the area cially evident along the Yarlung Zangbo River (where the of cropland available for foraging is extremely restricted. area of cropland increased by 15.5% between 1990 and In our original GLMM modelling to compare the habi- 2015; Wu et al. 2017). Numbers of Bar-headed Geese tat types used by geese with pseudo-absence measures in wintering along the Yarlung Zangbo River rose from the immediate vicinity, we also entered water recurrence 15,000 in the 1990s (Bishop et al. 1997) to 30,000 in 2007 (Pekel et al. 2016) as a potential explanatory parameter, (Bishop and Tsamchu 2007) to 67,000 in 2014 (Liu et al. but it was highly correlated with “water body”. Deletion 2017) as increasing numbers resorted to farmland to of water recurrence from the model resulted in an AUC feed. of more than 0.7, indicating reasonable predictions from Te Qinghai-Tibet Plateau is a vast territory with high this simplifed model. In our fnal model, geese tended biodiversity interest and a sparse human population, to select wetland and water bodies as habitat, because which has beneftted from the positive efects of nature the seasonal growth of aquatic plants provides acces- conservation designation, particularly evident through sible digestible biomass which can be exploited to accu- the current large extent of protected areas. Relatively mulate fat stores by day (Cong et al. 2012; Wang et al. high levels of site protection for the Greylag Geese in 2013), and open water ofers a night time roosting ref- East China have resulted in that species spending more uge to avoid predators. Geese also appeared to prefer than 65% of their stopover duration within IBA/pro- south facing stopover sites, probably because these areas tected areas during migration, and their population size Zhang et al. Avian Res (2020) 11:49 Page 11 of 13

is increasing (Li et al. 2020), suggesting that site protec- selection of Bar-headed Geese in stopovers within the Qinghai-Tibet tion can contribute to supporting increasing numbers Plateau during spring migration. of geese over time. It would therefore appear that Bar- headed Geese have beneftted from improved conserva- Acknowledgments tion action (especially protected areas designation) at We gratefully acknowledge the contribution of Xin Wang and Xianghuang Li for their help on data analysis, and Ming Ma for his help on the Bar-headed migration stopovers en route to and from their breeding Goose distribution in the Xinjiang Uygur Autonomous Region, China. We are areas, as well as from the increasing use of energy rich also indebted to the anonymous reviewers for their constructive comments agriculture areas as winter quarters. Nevertheless, as we and suggestions that greatly improve the manuscript. identify above, with climate change imposing spatially Authors’ contributions explicit patterns of change in diferent parts of the annual LC, JZ, YX and ADF conceived the ideas and designed methodology; LL, NB, range of the Bar-headed Goose, it remains essential we ID and FM collected the data; JZ and XD analyzed the data. JZ led the writing of the manuscript, with contributions from LC, YX and ADF. All authors contrib- improve our understanding of their migration routes and uted critically to the drafts and gave fnal approval for publication. All authors fyways through extended telemetry studies and monitor read and approved the fnal manuscript. their population dynamics and abundance to ensure the Funding future of this unique Asian goose species. Our study was supported by the National Natural Science Foundation of China (Grant No. 31870369 & No. 31970433 & No. 31670424) and China Biodiversity Observation Networks (Sino BON). The funders had no role in study design, Conclusions data collection and analysis, decision to publish, or preparation of the manuscript. Tis study is the frst to identify the paramount impor- tance of stopover sites within the QTP to Bar-headed Availability of data and materials The datasets used in the present study are available from the corresponding Geese in their annual cycle, but also to confrm the satis- author on reasonable request. factory level of current site protection given the patterns revealed by our telemetry data, which is consistent with Ethical approval and consent to participate The following information was supplied relating to ethical approvals (i.e., the upward trend in abundance of the ETF Bar-headed approving body and any reference numbers): The Animal Ethics Committee, Goose. We recommend Hala Lake and adjacent areas for Research for Eco-Environmental Sciences, Chinese Academy of Sciences fully protection because of their disproportionate importance approved this study. Approval for bird capture and transmitter deployment in Mongolia was obtained from the Ministry of Nature, Environmental and to the geese during the initial stages of their autumn Tourism of Mongolia (permission number: No 06/2862). Approval for transmit- migration, which are currently outside the present net- ter deployment at Qinghai Lake, China was obtained from the Qinghai Lake work of NNRs/IBAs. Bar-headed Geese mainly used nat- National Nature Reserve authorities. ural ecosystems during migratory stopovers (the majority Consent for publication feeding on grasslands by daytime and roosting on water Not applicable. body at night). Habitat modelling confrmed geese tend Competing interests to select wetland areas, close to rivers/lakes, away from The authors declare that they have no competing interests. roads and at lower elevations. Author details Supplementary information 1 State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, Supplementary information accompanies this paper at https​://doi. China. 2 University of Chinese Academy of Sciences, Beijing 100049, China. org/10.1186/s4065​7-020-00230​-9. 3 Department of Modern Physics, University of Science and Technology of China, Hefei 230026, China. 4 Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810008, China. 5 Wildlife Science and Conserva- Additional fle 1: Figure S1. Map showing the nature and extent of the tion Center, B‑802 Union Building, Sukhbaatar District, Ulaanbaatar 14210, two distinctive fyways of the Bar-headed Goose (Anser indicus) in Central Mongolia. 6 Institute of Biology, Mongolian Academy of Sciences, Ulaan- Asia. baatar 13330, Mongolia. 7 Department of Bioscience, Aarhus University, Kalø, Additional fle 2: Table S1. Summary table of Bar-headed Geese (Anser Grenåvej 14, DK‑8410 Rønde, Denmark. indicus) ftted with solar-powered GPS/GSM telemetry devices in the cur- rent analysis. Table S2. The location and duration of stopover sites in the Received: 22 May 2020 Accepted: 27 October 2020 Qinghai-Tibet Plateau used by tracked Bar-headed Geese (n 17) during autumn migration in 2016 and 2018. Table S3. The location =and duration of stopover sites in the Qinghai-Tibet Plateau used by tracked Bar-headed Geese (n 8) during spring migration in 2019. Table S4. Conservation = status of Bar-headed Geese stopovers in the Qinghai-Tibet Plateau during References autumn and spring migration. Table S5. Parameter estimates (β), standard Altman M, Gill J, McDonald MP. Numerical issues in statistical computing for errors, p values, and 95% confdence limits from the highest-ranked model the social scientist. Hoboken, New Jersey: Wiley; 2004. (Table 2) estimating habitat selection of Bar-headed Geese in stopovers Bartoń K. MuMIn: Multi-model inference. R package version 1.43.15. 2019. within the Qinghai-Tibet Plateau during autumn migration. Table S6. https​://CRAN.R-proje​ct.org/packa​ge MuMIn​. Parameter estimates (β), standard errors, p values, and 95% confdence Batbayar N, Takekawa JY, Natsagdorj T, Spragens= KA, Xiao X. Site selection and limits from the highest-ranked model (Table 2) estimating habitat nest survival of the Bar-headed Goose (Anser indicus) on the Mongolian Plateau. Waterbirds. 2014;37:381–93. Zhang et al. Avian Res (2020) 11:49 Page 12 of 13

Becker RA, Chambers JM. S: An interactive environment for data analysis and Li X. Annual migratory patterns of Greylag Geese (Anser anser rubrirostris) graphics. Boca Raton: CRC Press; 1984. revealed by satellite tracking. Master’s Thesis. Beijing: University of Chi- BirdLife International. Country profle: China (mainland). 2020. https​://www. nese Academy of Sciences; 2019 (In Chinese). birdl​ife.org/dataz​one/count​ry/china​. Accessed 07 Jan 2020. Li X, Wang X, Fang L, Batbayar N, Natsagdorj T, Davaasuren B, et al. Annual Bishop CM, Spivey RJ, Hawkes LA, Batbayar N, Chua B, Frappell PB, et al. The migratory patterns of Mongolian-Manchurian Eastern Greylag Geese roller coaster fight strategy of bar-headed geese conserves energy dur- (Anser anser rubrirostris) revealed by GPS/GSM loggers. Integr Zool. ing Himalayan migrations. Science. 2015;347:250–4. 2020;15:213–23. Bishop MA, Tsamchu D. Tibet Autonomous region january 2007 survey for Li ZWD, Bloem A, Delany S, Martakis G, Quintero JO. Status of waterbirds in Black-necked crane, Common crane, and Bar-headed goose. China Crane Asia—Results of the Asian Waterbird Census: 1987–2007. Kuala Lumpur, News. 2007;11:24–6. Malaysia: Wetlands International; 2009. Bishop MA, Yanling S, Zhouma C, Binyuan G. Bar-headed Geese Anser indicus Liu D, Zhang G, Li F, Ma T, Lu J, Qian F. A revised species population estimate wintering in south-central Tibet. Wildfowl. 1997;48:118–26. for the Bar-headed Goose (Anser indicus). Avian Res. 2017;8:7. Block WM, Brennan LA. The habitat concept in ornithology. In: Power DM, edi- Liu D, Zhang G, Jiang H, Shan K, Hou Y-Q, Dai M, et al. Movement and habitat tor. Current ornithology. Berlin: Springer; 1993. p. 35–91. utilization of breeding Bar-headed Goose and the relationship with Bodey TW, Cleasby IR, Bell F, Parr N, Schultz A, Votier SC, et al. A phylogeneti- humans in Qinghai Lake. Acta Ecol Sin. 2008;28:5201–8 (In Chinese). cally controlled meta-analysis of biologging device efects on birds: Liu D, Zhang G, Qian F, Hou Y, Dai M, Jiang H, et al. Population, distribution deleterious efects and a call for more standardized reporting of study and home range of wintering bar-headed goose along Yarlung Zangbo data. Methods Ecol Evol. 2018;9:946–55. River, Tibet. Acta Ecol Sin. 2010;30:4173–9 (In Chinese). Bourouiba L, Wu J, Newman S, Takekawa J, Natdorj T, Batbayar N, et al. Spatial Meng F, Wang X, Batbayar N, Natsagdorj T, Davaasuren B, Damba I, et al. dynamics of bar-headed geese migration in the context of H5N1. J R Soc Consistent habitat preference underpins the geographically divergent Interface. 2010;7:1627–39. autumn migration of individual Mongolian common shelducks. Curr Chen H, Li Y, Li Z, Shi J, Shinya K, Deng G, et al. Properties and dissemination of Zool. 2020. https​://doi.org/10.1093/cz/zoz05​6. H5N1 viruses isolated during an infuenza outbreak in migratory water- Middleton BA. Habitat and food preferences of Greylag and Barheaded Geese fowl in western China. J Virol. 2006;80:5976–83. wintering in the Keoladeo National Park. India J Trop Ecol. 1992;8:181–93. Chen W, Doko T, Fujita G, Hijikata N, Tokita K-I, Uchida K, et al. Migration of tun- Middleton BA, Van der Valk AG. The food habits of Greylag and Barheaded dra swans (Cygnus columbianus) wintering in Japan using satellite track- Geese in the Keoladeo National Park. India Wildfowl. 1987;38:94–102. ing: identifcation of the Eastern Palearctic fyway. Zool Sci. 2016;33:63–72. Millspaugh JJ, Marzluf JM. Radio-tracking and animal populations: past trends Cong P, Wang X, Cao L, Fox AD. Within-winter shifts in Lesser White-fronted and future needs. In: Millspaugh JJ, Marzluf JM, editors. Radio tracking Goose Anser erythropus distribution at East Dongting Lake, China. Ardea. and animal populations. San Diego: Academic Press; 2001. p. 383–93. 2012;100:5–11. Newman SH, Hill NJ, Spragens KA, Janies D, Voronkin IO, Prosser DJ, et al. Cui P, Hou Y, Tang M, Zhang H, Zhou Y, Yin Z, et al. Movement patterns of Bar- Eco-virological approach for assessing the role of wild birds in the spread headed Geese Anser indicus during breeding and post-breeding periods of avian infuenza H5N1 along the Central Asian Flyway. PLoS ONE. at Qinghai Lake, China. J Ornithol. 2011;152:83–92. 2012;7:e30636. Fox AD, Abraham KF. Why geese beneft from the transition from natural Northrup JM, Hooten MB, Anderson CR Jr, Wittemyer G. Practical guidance on vegetation to agriculture. Ambio. 2017;46:188–97. characterizing availability in resource selection functions under a use- Fox AD, Leafoor JO. A global audit of the status and trends of Arctic and availability design. Ecology. 2013;94:1456–63. Northern Hemisphere goose populations. Akureyri: Conservation of Page GW, Warnock N, Tibbitts TL, Jorgensen D, Hartman CA, Stenzel LE. Annual Arctic Flora and Fauna International Secretariat; 2018. migratory patterns of Long-billed Curlews in the American West. Condor. Gong P, Liu H, Zhang M, Li C, Wang J, Huang H, et al. Stable classifcation with 2014;116:50–61. limited sample: transferring a 30-m resolution sample set collected in Pekel J-F, Cottam A, Gorelick N, Belward AS. High-resolution mapping of global 2015 to mapping 10-m resolution global land cover in 2017. Sci Bull. surface water and its long-term changes. Nature. 2016;540:418–22. 2019;64:370–3. Prins HHT, van Wieren SE. Number, population structure and habitat use of Gong P, Wang J, Yu L, Zhao Y, Zhao Y, Liang L, et al. Finer resolution observation bar-headed geese Anser indicus in Ladakh (India) during the brood- and monitoring of global land cover: frst mapping results with Landsat rearing period. Acta Zool Sin. 2004;50:738–44. TM and ETM data. Int J Remote Sens. 2013;34:2607–54. Prosser DJ, Takekawa JY, Newman SH, Yan B, Douglas DC, Hou Y, et al. Satellite- Hao M, Zhang Y, Lei+ F, Yan B, Xing Z. Potential habitat analysis of Anser indicus marked waterfowl reveal migratory connection between H5N1 outbreak with digital elevation model. Chin J Zool. 2010;45:35–42 (In Chinese). areas in China and Mongolia. Ibis. 2009;151:568–76. Hawkes L, Batbayar N, Bishop C, Butler PJ, Frappell P, Meir JU, et al. Goose Prosser DJ, Cui P, Takekawa JY, Tang M, Hou Y, Collins BM, et al. Wild bird migra- migration over the Himalayas: Physiological adaptations. In: Prins HHT, tion across the Qinghai-Tibetan plateau: a transmission route for highly Namgail T, editors., Bird migration across the Himalayas: Wetland func- pathogenic H5N1. PLoS ONE. 2011;6:e17622. tioning amidst mountains and glaciers. Cambridge: Cambridge University R Core Team. R: A language and environment for statistical computing. Vienna, Press; 2017. p. 241–53. Austria: R Foundation for Statistical Computing; 2019. https​://www.R- Hawkes LA, Balachandran S, Batbayar N, Butler PJ, Frappell PB, Milsom WK, et al. proje​ct.org/. The trans-Himalayan fights of bar-headed geese (Anser indicus). P Natl Signer J, Fieberg J, Avgar T. Animal movement tools (amt): R package for Acad Sci USA. 2011;108:9516–9. managing tracking data and conducting habitat selection analyses. Ecol Hawkes LA, Balachandran S, Batbayar N, Butler PJ, Chua B, Douglas DC, et al. Evol. 2019;9:880–90. The paradox of extreme high-altitude migration in bar-headed geese Szumilas M. Explaining odds ratios. J Can Acad Child Adol Psy. 2010;19:227–9. Anser indicus. P Roy Soc B-Biol Sci. 2013;280:20122114. Takekawa J, Heath SR, Douglas DC, Perry WM, Javed S, Newman SH, et al. Hosmer DW Jr, Lemeshow S, Sturdivant RX. Applied logistic regression. 3rd ed. Geographic variation in Bar-headed Geese Anser indicus: connectivity of Hoboken, New Jersey: John Wiley & Sons; 2013. wintering areas and breeding grounds across a broad front. Wildfowl. Jones J. Habitat selection studies in avian ecology: a critical review. Auk. 2009;59:100–23. 2001;118:557–62. Takekawa JY, Palm EC, Prosser DJ, Hawkes LA, Batbayar N, Balachandran S, et al. Kölzsch A, Müskens GJ, Kruckenberg H, Glazov P, Weinzierl R, Nolet BA, et al. Goose migration across the Himalayas: Migratory routes and movement Towards a new understanding of migration timing: slower spring than patterns of Bar-headed Geese. In: Prins HHT, Namgail T, editors. Bird autumn migration in geese refects diferent decision rules for stopover migration across the Himalayas: Wetland functioning amidst mountains use and departure. Oikos. 2016;125:1496–507. and glaciers. Cambridge: Cambridge University Press; 2017. p. 15–29. Köppen U, Yakovlev AP, Barth R, Kaatz M, Berthold P. Seasonal migrations of Tian H, Zhou S, Dong L, Van Boeckel TP, Cui Y, Wu Y, et al. Avian infuenza four individual bar-headed geese Anser indicus from Kyrgyzstan followed H5N1 viral and bird migration networks in Asia. P Natl Acad Sci USA. by satellite telemetry. J Ornithol. 2010;151:703–12. 2015;112:172–7. Li F, Bishop MA, Drolma T. Power line strikes by black-necked cranes and bar- Van der Ven J, Gole P, Ouweneel G. Bar-headed Geese Anser indicus: Notes from headed geese in Tibet Autonomous Region. Chin Birds. 2011;2:167–73. breeding and wintering areas. Goose Bull. 2010;10:7–17. Zhang et al. Avian Res (2020) 11:49 Page 13 of 13

Wang X, Fox AD, Cong PH, Cao L. Food constraints explain the restricted at Caohai Lake of Guizhou, China. Acta Ecol Sin. 2012;32:7280–8 (In distribution of wintering Lesser White-fronted Geese Anser erythropus in Chinese). China. Ibis. 2013;155:576–92. Yang Y, Zhang G, Lu J, Liu W, Li Z. Foraging habitat selection of Bar-headed Wang X, Cao L, Bysykatova I, Xu Z, Rozenfeld S, Jeong W, et al. The Far East Goose in winter at Caohai National Reserve in Guizhou. Sci Silvae Sin. taiga forest unrecognized inhospitable terrain for migrating Arctic-nest- 2013;49:176–80 (In Chinese). ing waterbirds? PeerJ. 2018;6:e4353. Ydenberg RC. The Himalayas as an ecological barrier for avian migrants: High Wu B, Qian J, Zeng Y, Zhang L, Yan C, Wang Z, et al. Land cover atlas of the and dry, but also dangerous? In: Prins HHT, Namgail T, editors. Bird migra- People’s Republic of China (1: 1,000,000). Beijing: China Map Publishing tion across the Himalayas: Wetland functioning amidst mountains and House; 2017. (In Chinese). glaciers. Cambridge: Cambridge University Press; 2017. p. 283. Wutzler T. Solartime: Utilities dealing with solar time such as sun position and Zhang G, Liu D, Qian F, Jiang H, Hou Y, Dai M. Diversity of waterbirds and time of sunrise. R package version 0.0.1. 2018. https​://CRAN.R-proje​ct.org/ change in home range of bar-headed geese Anser indicus during breed- packa​ge solar​time. ing period at Hangcuo Lake of Tibet, China. Acta Ecol Sin. 2011a;31:395– Xu W, Fan X, Ma= J, Pimm SL, Kong L, Zeng Y, et al. Hidden loss of wetlands in 400 (In Chinese). China. Curr Biol. 2019;29:3065–71. Zhang GG, Liu DP, Hou YQ, Jiang HX, Dai M, Qian FW, et al. Migration routes Xu Y, Si Y, Takekawa J, Liu Q, Prins HHT, Yin S, et al. A network approach and stop-over sites determined with satellite tracking of bar-headed to prioritize conservation eforts for migratory birds. Conserv Biol. geese Anser indicus breeding at Qinghai Lake, China. Waterbirds. 2020;34:416–26. 2011b;34:112–6. Yan L, Hu M, Meng F, Liu N. Foraging habitat selection of Anser indicus Zhang G, Liu D, Qian F, Hou Y, Chen L, Dai Q, et al. The water bird community during winter at Lashihai Lake in Yunnan Province. Mod Agr Sci Tech. and home range of the bar-headed goose at Yamdrok Lake in Tibet, 2014;10:164 (In Chinese). China. Acta Ecol Sin. 2016;36:946–52 (In Chinese). Yang F. Report on a three year survey of Black-necked Crane and large-sized Zhao M. Wintering ecology and population trend of Anseriformes in the mid- waterbirds on the Yunnan and Guizhou Plateau. In: Li F, Yang X, Yang F, dle and lower Yangtze River foodplain. PhD Thesis. Hefei: University of editors. Status and conservation of Black-necked Cranes on the Yunnan Science and Technology of China; 2017 (In Chinese). and Guizhou Plateau, People’s Republic of China. Kunming: Yunnan Zheng R, Smith LM, Prosser DJ, Takekawa JY, Newman SH, Sullivan JD, et al. Nationality Publishing House; 2005. p. 59–64 (In Chinese). Investigating home range, movement pattern, and habitat selection Yang F, Zhang YQ. Quantities and distribution of the Black-necked Crane (Grus of Bar-headed Geese during breeding season at Qinghai Lake, China. nigricollis) and other large waterfowl on the Yunnan and Guizhou Plateau. Animals. 2018;8:182. Zool Res. 2014;35:80–4. Yang Y, Zhang G, Lu J, Liu W, Li Z. Diurnal activity patterns and environmen- tal factors on behaviors of Bar-headed Geese Anser indicus wintering

Ready to submit your research ? Choose BMC and benefit from:

• fast, convenient online submission • thorough peer review by experienced researchers in your field • rapid publication on acceptance • support for research data, including large and complex data types • gold Open Access which fosters wider collaboration and increased citations • maximum visibility for your research: over 100M website views per year

At BMC, research is always in progress.

Learn more biomedcentral.com/submissions