Volume 13 Issue 1
Mar.  2022
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Yang Wu, Weipan Lei, Bingrun Zhu, Jiaqi Xue, Yuanxiang Miao, Zhengwang Zhang. 2022: Identification of annual routines and critical stopover sites of a breeding shorebird in the Yellow Sea, China. Avian Research, 13(1): 100068. doi: 10.1016/j.avrs.2022.100068
Citation: Yang Wu, Weipan Lei, Bingrun Zhu, Jiaqi Xue, Yuanxiang Miao, Zhengwang Zhang. 2022: Identification of annual routines and critical stopover sites of a breeding shorebird in the Yellow Sea, China. Avian Research, 13(1): 100068. doi: 10.1016/j.avrs.2022.100068

Identification of annual routines and critical stopover sites of a breeding shorebird in the Yellow Sea, China

doi: 10.1016/j.avrs.2022.100068
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  • Corresponding author: E-mail address: zzw@bnu.edu.cn (Z. Zhang)
  • Received Date: 08 Oct 2022
  • Accepted Date: 24 Oct 2022
  • Rev Recd Date: 22 Oct 2022
  • Available Online: 12 Jan 2023
  • Publish Date: 31 Oct 2022
  • Pied Avocets (Recurvirostra avosetta) are common migratory shorebirds in the East Asian–Australasian Flyway. From 2019 to 2021, GPS/GSM transmitters were used to track 40 Pied Avocets nesting in northern Bohai Bay to identify annual routines and key stopover sites. On average, southward migration of Pied Avocets started on 23 October and arrived at wintering sites (mainly in the middle and lower reaches of the Yangtze River and coastal wetlands) in southern China on 22 November; northward migration started on 22 March with arrival at breeding sites on 7 April. Most avocets used the same breeding sites and wintering sites between years, with an average migration distance of 1124 ​km. There was no significant difference between sexes on the migration timing or distance in both northward and southward migration, except for the departure time from the wintering sites and winter distribution. The coastal wetland of Lianyungang in Jiangsu Province is a critical stopover site. Most individuals rely on Lianyungang during both northward and southward migration, indicating that species with short migration distances also heavily rely on a few stopover sites. However, Lianyungang lacks adequate protection and is facing many threats, including tidal flat loss. We strongly recommend that the coastal wetland of Lianyungang be designated as a protected area to effectively conserve the critical stopover site.


  • 1 These authors contributed equally to this work.
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  • Abad-Gómez, J.M., Villegas, A., Gutiérrez, J.S., Parejo, M., Navedo, J.G., Sánchez-Guzmán, J.M., et al., 2020. Pro-inflammatory immune response is linked to wintering habitat in a migratory shorebird. Auk 137, ukaa046. https://doi.org/10.1093/auk/ukaa046.
    Allcock, J., Carey, G., Chow, G., Welch, G., 2012. Hong Kong Bird Report 2009–10. HongKong Bird Watching Society. https://www.hkbws.org.hk/cms/resource-tw/bird-report-tw/file/39-2009-2010. (Accessed 15 September 2021).
    Bates, D., Mächler, M., Bolker, B., Walker, S., 2015. Fitting Linear mixed-effects models using lme4. J. Stat. Softw. 67, 1-48. https://doi.org/10.18637/jss.v067.i01.
    Battley, P.F., Warnock, N., Tibbitts, T.L., Gill, R.E., Piersma, T., Hassell, C.J., et al., 2012. Contrasting extreme long-distance migration patterns in bar-tailed godwits Limosa lapponica. J. Avian Biol. 43, 21-32. https://doi.org/10.1111/j.1600-048X.2011.05473.x.
    Bracey, A., Lisovski, S., Moore, M., McKellar, A., Craig, E., Matteson, S., et al., 2018. Migratory routes and wintering locations of declining inland North American Common Terns. Auk 135, 385-399. https://doi.org/10.1642/AUK-17-210.1.
    Bucher, E.H., 1992. The causes of extinction of the passenger pigeon. In: Power, D.M. (Ed.), Current Ornithology. Springer, Boston, pp. 1–36. https://doi.org/10.1007/978-1-4757-9921-7_1.
    Cao, L., Tang, S., Wang, X., Barter, M., 2009. The importance of eastern China for shorebirds during the non-breeding season. Emu 109, 170-178. https://doi.org/10.1071/MU08051.
    Chambon, R., Dugravot, S., Paillisson, J-M., Lemesle, J-C., Ysnel, F., Gélinaud, G., 2018. Partial migration in inexperienced pied avocets Recurvirostra avosetta: distribution pattern and correlates. J. Avian Biol. 49. https://doi.org/10.1111/jav.01549.
    Chan, Y.C., Peng, H.B., Han, Y.X., Chung, S. S-W., Li, J., Zhang, L., et al., 2019. Conserving unprotected important coastal habitats in the Yellow Sea: shorebird occurrence, distribution and food resources at Lianyungang. Glob. Ecol. Conserv. 20, e00724. https://doi.org/10.1016/j.gecco.2019.e00724.
    Choi, C.Y., Li, J., Xue, W.J., 2020. China coastal waterbird census report 2012–2019 (English). Hong Kong Bird Watching Society. https://cms.hkbws.org.hk/cms/en/resource/publication/regional-publication/file/657-ccwc-report-2012-2019-eng. (Accessed 15 September 2021).
    Cresswell, W., 2014. Migratory connectivity of Palaearctic–African migratory birds and their responses to environmental change: the serial residency hypothesis. Ibis 156, 493–510. doi:doi.org/ 10.1111/ibi.12168.
    Duijns, S., van Gils, J.A., Spaans, B., ten Horn, J., Brugge, M., Piersma, T., 2014. Sex-specific winter distribution in a sexually dimorphic shorebird is explained by resource partitioning. Ecol. Evol. 4, 4009-4018. https://doi.org/10.1002/ece3.1213.
    Estrella, S.M., Masero, J.A., 2010. Prey and prey size selection by the Near-Threatened Black-Tailed Godwit foraging in non-tidal Areas during migration. Waterbirds 33, 293-299. https://doi.org/10.1675/063.033.0304.
    Giunchi, D., Baldaccini, N.E., Lenzoni, A., Luschi, P., Sorrenti, M., Cerritelli, G., et al., 2019. Spring migratory routes and stopover duration of satellite-tracked Eurasian Teals Anas crecca wintering in Italy. Ibis 161, 117-130. https://doi.org/10.1111/ibi.12602.
    Hijmans, R.J., Williams, E., Vennes, C., 2017. Geosphere: Spherical Trigonometry, Version 1.5-10. https://CRAN.R-project.org/package=geosphere. (Accessed 12 January 2021)
    Hill, D., 1988. Population dynamics of the Avocet (Recurvirostra avosetta) breeding in Britain. J. Anim. Ecol. 57, 669-683. https://doi.org/10.2307/4932.
    Hotker, H., West, R., 2005. Population size, population development and habitat use by Avocets in Western Europe at the end of the 20th century. Wader Study 107, 57.
    Inger, R., Gregory, R., Duffy, J.P., Stott, I., Voříšek, P., Gaston, K.J., 2015. Common European birds are declining rapidly while less abundant species' numbers are rising. Ecol. Lett. 18, 28-36. https://doi.org/10.1111/ele.12387.
    IUCN, 2020. Recurvirostra avosetta (pied avocet). IUCN red list threat. Species. https://www.iucnredlist.org/species/22693712/155534228. (Accessed 30 November 2020).
    Kirby, J.S., Stattersfield, A.J., Butchart, S.H.M., Evans, M.I., Grimmett, R.F.A., Jones, V.R., et al., 2008. Key conservation issues for migratory land- and waterbird species on the world's major flyways. Bird Conserv. Int. 18, S49-S73. https://doi.org/10.1017/S0959270908000439.
    Kuang, F., Coleman, J.T., Hassell, C.J., Leung, K. K-S., Maglio, G., Ke, W., et al., 2020. Seasonal and population differences in migration of Whimbrels in the East Asian-Australasian Flyway. Avian Res. 11, 24. https://doi.org/10.1186/s40657-020-00210-z.
    Kuznetsova, A., Brockhoff, P.B., Christensen, R.H.B., 2017. lmerTest package: tests in Linear mixed effects models. J. Stat. Softw. 82, 1-26. https://doi.org/10.18637/jss.v082.i13.
    Lei, W., Masero, J.A., Piersma, T., Zhu, B., Yang, H-Y., Zhang, Z., 2018. Alternative habitat: the importance of the Nanpu Saltpans for migratory waterbirds in the Chinese Yellow Sea. Bird Conserv. Int. 28, 549-566. https://doi.org/10.1017/S0959270917000508.
    Lei, W., Wu, Y., Wu, F., Piersma, T., Zhang, Z., Masero, J.A., 2021. Artificial wetlands as breeding habitats for shorebirds: a case study on Pied Avocets in China's largest saltpan complex. Front. Ecol. Evol. 9, 622756. https://doi.org/10.3389/fevo.2021.622756.
    Lisovski, S., Gosbell, K., Hassell, C., Minton, C., 2016. Tracking the full annual-cycle of the Great Knot, Calidris tenuirostris, a long-distance migratory shorebird of the East Asian-Australasian Flyway. Wader Study 123. 177-189. https://doi.org/10.18194/ws.00048.
    Lourenço, P.M., Kentie, R., Schroeder, J., Alves, J.A., Groen, N.M., Hooijmeijer, J.C.E.W., et al., 2010. Phenology, stopover dynamics and population size of migrating Black-Tailed Godwits Limosa limosa limosa in Portuguese Rice Plantations. Ardea 98, 35-42. https://doi.org/10.5253/078.098.0105.
    Ma, Z., Hua, N., Peng, H., Choi, C., Battley, P.F., Zhou, Q., et al., 2013. Differentiating between stopover and staging sites: functions of the southern and northern Yellow Sea for long-distance migratory shorebirds. J. Avian Biol. 44, 504-512. https://doi.org/10.1111/j.1600-048X.2013.00213.x.
    McMahon, B.J., Whelan, J., Bracken, F., Kavanagh, B.P., 2003. The impact of farming on over-wintering bird populations. Tearmann – Irish J. Agri-Environ. Res. 3, 67–76. https://hdl.handle.net/10779/rcsi.10767518.v2. https://hdl.handle.net/10779/rcsi.10767518.v2
    Meissner, W., 2006. Timing and phenology of Curlew Sandpiper Calidris ferruginea on southward migration through Puck Bay, Poland. Int. Wader Stud. 19, 121–124.
    Moreira, F., 1995. The winter feeding ecology of Avocets Recurvirostra avosetta on intertidal areas. I. Feeding strategies. Ibis 137, 92-98. https://doi.org/10.1111/j.1474-919X.1995.tb03224.x.
    Murray, N.J., Clemens, R.S., Phinn, S.R., Possingham, H.P., Fuller, R.A., 2014. Tracking the rapid loss of tidal wetlands in the Yellow Sea. Front. Ecol. Environ. 12, 267-272. https://doi.org/10.1890/130260.
    Nebel, S., 2005. Latitudinal clines in bill length and sex ratio in a migratory shorebird: a case of resource partitioning? Acta Oecologica 28, 33-38. https://doi.org/10.1016/j.actao.2005.02.002.
    Pierce, R.J., Kirwan, G.M., Boesman, P.F.D., 2020. Pied Avocet (Recurvirostra avosetta), Version 1.0. In: del Hoyo, J., Elliott, A., Sargatal, J., Christie, D.A., de Juana, E. (Eds.), Birds of the World. Cornell Lab of Ornithology, New York. https://doi.org/10.2173/bow.pieavo1.01.
    Piersma, T., 2003. "Coastal" versus "inland" shorebird species: interlinked fundamental dichotomies between their life- and demographic histories? Wader Study Group Bull. 100, 5-9.
    Piersma, T., Kok, E.M.A., Hassell, C.J., Peng, H-B., Verkuil, Y.I., Lei, G., et al., 2021. When a typical jumper skips: itineraries and staging habitats used by Red Knots (Calidris canutus piersmai) migrating between Northwest Australia and the New Siberian Islands. Ibis 163, 1235-1251. https://doi.org/10.1111/ibi.12964.
    Piersma, T., Lok, T., Chen, Y., Hassell, C.J., Yang, H-Y., Boyle, A., et al., 2016. Simultaneous declines in summer survival of three shorebird species signals a flyway at risk. J. Appl. Ecol. 53, 479-490. https://doi.org/10.1111/1365-2664.12582.
    R Core Team, 2020. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
    Spoon-billed Sandpiper in China, 2022. Jiangsu Coastal Waterbird Census Report 2019-2020. https://ff.lingxi360.com/f?fid=BDI=dmYCPWcc6&utm_bccid=LXEQrkjjWjUzhyCR. (Accessed 15 September 2022).
    Studds, C.E., Kendall, B.E., Murray, N.J., Wilson, H.B., Rogers, D.I., Clemens, R.S., et al., 2017. Rapid population decline in migratory shorebirds relying on Yellow Sea tidal mudflats as stopover sites. Nat. Commun. 8, 14895. https://doi.org/10.1038/ncomms14895.
    Tao, X.D., Lei, J.Y., Richard, H., Lei, G., 2017. Report on the Coordinated Survey for Wintering Waterbird of the Central and Lower Yangtze in 2015. China Forestry Publishing House, Beijing.
    Van der Velde, M., Haddrath, O., Verkuil, Y.I., Baker, A.J., Piersma, T., 2017. New primers for molecular sex identification of waders. Wader Study 124, 147-151. https://doi.org/10.18194/ws.00069.
    Verhoeven, M.A., Loonstra, A.J., McBride, A.D., Macias, P., Kaspersma, W., Hooijmeijer, J.C., et al., 2020. Geolocators lead to better measures of timing and renesting in black-tailed godwits and reveal the bias of traditional observational methods. J. Avian Biol. 51, e02259. https://doi.org/10.1111/jav.02259.
    Wetlands International, 2020. Waterbird Population Estimates. http://wpe.wetlands.org/. (Accessed 2 December 2020).
    Woodworth, B.K., Wheelwright, N.T., Newman, A.E., Schaub, M., Norris, D.R., 2017. Winter temperatures limit population growth rate of a migratory songbird. Nat. Commun. 8, 14812. https://doi.org/10.1038/ncomms14812.
    Yang, Z., Li, J., Han, Y., Hassell, C.J., Leung, K.K-S., Melville, D.S., et al., 2021. Coastal wetlands in Lianyungang, Jiangsu Province, China: probably the most important site globally for the Asian Dowitcher (Limnodromus semipalmatus). Avian Res. 12, 38. https://doi.org/10.1186/s40657-021-00272-7.
    Zhu, B., Verhoeven, M.A., Loonstra, A.H.J., Sanchez-Aguilar, L., Hassell, C.J., Leung, K.K-S., et al., 2021. Identification of breeding grounds and annual routines of the newly discovered bohaii subspecies of Black-tailed Godwits. Emu - Austral Ornithol. 121, 292-302. https://doi.org/10.1080/01584197.2021.1963287.
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