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Persistent use of a shorebird staging site in the Yellow Sea despite severe declines in food resources implies a lack of alternatives

  • SHOU-DONG ZHANG (a1), ZHIJUN MA (a1), CHI-YEUNG CHOI (a2), HE-BO PENG (a1) (a3), QING-QUAN BAI (a4), WEN-LIANG LIU (a5), KUN TAN (a1), DAVID S. MELVILLE (a6), PENG HE (a1), YING-CHI CHAN (a3) (a7), JAN A. VAN GILS (a7) and THEUNIS PIERSMA (a3) (a7)...
Summary

Many shorebird populations are in decline along the East Asian-Australasian Flyway. The rapid loss of coastal wetlands in the Yellow Sea, which provide critical stop-over sites during migration, is believed to be the cause of the alarming trends. The Yalu Jiang coastal wetland, a protected area in the north Yellow Sea, supports the largest known migratory staging populations of Bar-tailed Godwits Limosa lapponica (menzbieri and baueri subspecies) and Great Knots Calidris tenuirostris. Monitoring of the macrozoobenthos food for these shorebirds from 2011 to 2016 showed declines of over 99% in the densities of the bivalve Potamocorbula laevis, the major food here for both Bar-tailed Godwits and Great Knots. The loss of the bivalve might be caused by any combination of, but not limited to: (1) change in hydrological conditions and sediment composition due to nearby port construction, (2) run-off of agrochemicals from the extensive shoreline sea cucumber farms, and (3) parasitic infection. Surprisingly, the numbers of birds using the Yalu Jiang coastal wetland remained stable during the study period, except for the subspecies of Bar-tailed Godwit L. l. menzbieri, which exhibited a 91% decline in peak numbers. The lack of an overall decline in the number of bird days in Great Knots and in the peak numbers of L. l. baueri, also given the published simultaneous decreases in their annual survival, implies a lack of alternative habitats that birds could relocate to. This study highlights that food declines at staging sites could be an overlooked but important factor causing population declines of shorebirds along the Flyway. Maintaining the quality of protected staging sites is as important in shorebird conservation as is the safeguarding of staging sites from land claim. Meanwhile, it calls for immediate action to restore the food base for these beleaguered migrant shorebirds at Yalu Jiang coastal wetland.

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Corresponding author
*Author for correspondence, e-mail: zhijunm@fudan.edu.cn
References
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Amano, T., Székely, T., Koyama, K., Amano, H. and Sutherland, W. J. (2010) A framework for monitoring the status of populations: an example from wader populations in the East Asian-Australasian Flyway. Biol. Conserv. 143: 22382247.
Bai, Q. Q., Chen, J., Chen, Z., Dong, G., Dong, J., Dong, W., Fu, V. W. K., Han, Y., Lu, G., Li, J., Liu, Y., Lin, Z., Meng, D., Martinez, J., Ni, G., Shan, K., Sun, R., Tian, S., Wang, F., Xu, Z., Yu, Y. T., Yang, J., Yang, Z., Zhang, L., Zhang, M. and Zeng, X. (2015) Identification of coastal wetlands of international importance for waterbirds: a review of China Coastal Waterbird Surveys 2005–2013. Avian Res. 6: 12. doi: 10.1186/s40657-015-0021-2.
Bamford, M., Watkins, D., Bancroft, W., Tischler, G. and Wahl, J. (2008) Migratory shorebirds of the East Asian-Australasian Flyway: Population estimates and internationally important sites. Canberra, Australia: Wetlands International-Oceania.
Barter, M. A. (2002) Shorebirds of the Yellow Sea: Importance, threats and conservation status. Canberra, Australia: Wetlands International. (Global Series 9, International Wader Studies 12).
Battley, P. F., Warnock, N., Tibbitts, T. L., Gill, R. E., Piersma, T., Hassell, C. J., Douglas, D. C., Mulcahy, D. M., Gartrell, B. D. and Schuckard, R. (2012) Contrasting extreme long-distance migration patterns in bar-tailed godwits Limosa lapponica. J. Avian Biol. 43: 2132.
Boxall, A. (2004) The environmental side effects of medication. EMBO Rep. 5: 11101116.
Cabello, F. C., Godfrey, H. P., Tomova, A., Ivanova, L., Dölz, H., Millanao, A. and Buschmann, A. H. (2013) Antimicrobial use in aquaculture re-examined: Its relevance to antimicrobial resistance and to animal and human health. Environ. Microbiol. 15: 19171942.
Chen, Y., Dong, J., Xiao, X., Zhang, M., Tian, B., Zhou, Y., Li, B. and Ma, Z. J. (2016) Land claim and loss of tidal flats in the Yangtze Estuary. Sci. Rep. 6: 24018. doi: 10.1038/srep24018.
Chen, Y. B. (2015) Analysis of drainage from mariculture area in Laizhou Bay and estimation of mariculture pollutant loadings in China. Master Thesis. Dalian University of Technology, People’s Republic of China. (In Chinese).
Choi, C. Y. (2015) The Northward migration stopover ecology of Bar-tailed Godwits and Great Knots in the Yalu Jiang Estuary, National Nature Reserve, China. PhD thesis. Massey University, New Zealand.
Choi, C. Y., Battley, P. F., Potter, M. A., Ma, Z. J., Melville, D. S. and Sukkaewmanee, P. (2017) How migratory shorebirds selectively exploit prey at a staging site dominated by a single prey species. Auk 134: 7691.
Choi, C. Y., Battley, P. F., Potter, M. A., Ma, Z. J. and Liu, W. L. (2014) Factors affecting the distribution patterns of benthic invertebrates at a major shorebird staging site in the Yellow Sea, China. Wetlands 34: 10851096.
Choi, C. Y., Battley, P. F., Potter, M. A., Rogers, K. G. and Ma, Z. J. (2015) The importance of Yalu Jiang coastal wetland in the north Yellow Sea to Bar-tailed Godwits Limosa lapponica and Great Knots Calidris tenuirostris during northward migration. Bird Conserv. Internatn. 25: 5370.
Choi, C. Y., Rogers, K. G., Gan, X., Clemens, R. S., Bai, Q. Q., Lilleyman, A., Lindsey, A., Milton, D. A., Straw, P., Yu, Y. T., Battley, P. F., Fuller, R. A. and Rogers, D. I. (2016) Phenology of southward migration of shorebirds in the East Asian-Australasian Flyway and inferences about stop-over strategies. Emu 116: 178189.
Conklin, J. R., Lok, T., Melville, D. S., Riegen, A. C., Schuckard, R., Piersma, T. and Battley, P. F. (2016) Declining adult survival of New Zealand Bar-tailed Godwits during 2005–2012 despite apparent population stability. Emu 116: 147157.
Edelaar, P., Drent, J. and de Goeij, P. (2003) A double test of the parasite manipulation hypothesis in a burrowing bivalve. Oecologia 134: 6671.
Escudero, G., Navedo, J. G., Piersma, T., de Goeij, P. and Edelaar, P. (2012) Foraging conditions ’at the end of the world’ in the context of long-distance migration and population declines in red knots. Austral Ecol. 37: 355364.
Han, M. K. (2002) Human influences on muddy coasts. Pp. 293–318 in Healy, T., Wang, Y. and Healy, J. A., eds. Muddy coasts of the world: Processes, deposits and function. Amsterdam, the Netherlands: Elsevier Science B.Y.
He, P., Melville, D. S., Peng, H. B., Tan, K., Chen, Y. and Ma, Z. J. (2016) Aquaculture pond banks as high tide roosts: What physical characteristics are more attractive to shorebirds? Stilt 69 & 70: 6265.
Hong, J., Yamashita, H. and Sato, S. (2007) The Saemangeum Reclamation Project in South Korea threatens to extinguish a unique mollusk, ectosymbiotic bivalve species attached to the shell of Lingula anatina. Plankton and Benthos Res. 2: 7075.
Hua, N., Åkesson, S., Zhou, Q. Y. and Ma, Z. J. (2017) Springtime migratory restlessness and departure orientation of Great Knots (Calidris tenuirostris) in the south compared to the north Yellow Sea. Avian Res. 8: 20. doi: 10.1186/s40657-017-0078-1.
Hua, N., Tan, K., Chen, Y. and Ma, Z. J. (2015) Key research issues concerning the conservation of migratory shorebirds in the Yellow Sea region. Bird Conserv. Internatn. 25: 3852.
Lee, H. J. and Ryu, S. O. (2008) Changes in topography and surface sediments by the Saemangeum dyke in an estuarine complex, west coastal of Korea. Cont. Shelf Res. 28: 11771189.
Liu, J. M. and She, J. T. (2003) Reproductive behaviour of Potamocorbula laevis (Hinds). Fisheries Sci. 5: 1213. (In Chinese).
Ma, Z. J., Hua, N., Peng, H. B., Choi, C., Battley, P. F., Zhou, Q. Y., Chen, Y., Ma, Q., Jia, N. and Xue, W. (2013) Differentiating between stopover and staging sites: functions of the southern and northern Yellow Sea for long-distance migratory shorebirds. J. Avian Biol. 44: 504512.
Ma, Z. J., Melville, D. S., Liu, J., Chen, Y., Yang, H., Ren, W., Zhang, Z., Piersma, T. and Li, B. (2014) Rethinking China’s new great wall. Science 346: 912914.
Melville, D. S., Chen, Y. and Ma, Z. J. (2016a) Shorebirds along the Yellow Sea coast of China face an uncertain future: a review of threats. Emu 116: 100110.
Melville, D. S., Peng, H. B., Chan, Y. C., Bai, Q. Q., He, P., Tan, K., Chen, Y., Zhang, S. D. and Ma, Z. J. (2016b) Gaizhou, Liaodong Bay, Liaoning Province, China – a site of international importance for Great Knot Calidris tenuirostris and other shorebirds. Stilt 69 &70: 5660.
Moores, N., Rogers, D. I., Kim, R. H., Hassell, C. J., Gosbell, K., Kim, S. A. and Park, M. N. (2008) The 2006–2008 Saemangeum shorebird monitoring program report. Busan, Korea: Birds Korea.
Moores, N., Rogers, D. I., Rogers, K. and Hansbro, P. M. (2016) Reclamation of tidal flats and shorebird declines in Saemangeum and elsewhere in the Republic of Korea. Emu 116: 136146.
Murray, N. J., Clemens, R. S., Phinn, S. R., Possingham, H. P. and Fuller, R. A. (2014) Tracking the rapid loss of tidal wetlands in the Yellow Sea. Front. Ecol. Environ. 12: 267272.
Peng, H. B., Choi, C. Y., Jia, N., Melville, D. S., Tan, K., He, P., Chen, Y. and Ma, Z. J. (2014) A perfect storm? The decrease of Great Knot food in the Yalu Jiang coastal wetland in the Yellow Sea, China. Presentation at the Australasian Shorebird Conference, Charles Darwin University, Darwin, Northern Territory, 20–21 September 2014.
Peng, H. B., Hua, N., Choi, C., Melville, D. S., Gao, Y., Zhou, Q., Chen, Y., Xue, W., Ma, Q., Wu, W. (2015) Adjusting migration schedules at stopping sites: time strategy of a long-distance migratory shorebird during northward migration. J. Ornithol. 156: 191199.
Piersma, T. and Baker, A. J. (2000) Life history characteristics and the conservation of migratory shorebirds. Pp. 105–124 in Gosling, L. M. and Sutherland, W. J., eds. Behaviour and conservation. Cambridge, UK: Cambridge University Press.
Piersma, T., Lok, T., Chen, Y., Hassell, C. J., Yang, H. Y., Boyle, A., Slaymaker, M., Chan, Y. C., Melville, D. S., Zhang, Z. W. and Ma, Z. J. (2016) Simultaneous declines in summer survival of three shorebird species signals a flyway at risk. J. Appl. Ecol. 53: 479490.
Riegen, A. C., Vaughan, G. R. and Rogers, K. D. (2014) Yalu Jiang Estuary shorebird survey report 1999–2010. Yalu Jiang Estuary Nature Reserve, China and Miranda Naturalists’ Trust, New Zealand.
Rogers, D. I., Yang, H., Hassell, C. J., Boyle, A. N., Rogers, K. G., Chen, B., Zhang, Z. and Piersma, T. (2010) Red Knots (Calidris canutus piersmai and C. c. rogersi) depend on a small threatened staging area in Bohai Bay, China. Emu 110: 307315.
Ryu, J., Nam, J., Park, J., Kwon, B., Lee, J., Song, S. J., Hong, S., Chang, W. K. and Khim, J. S. (2014) The Saemangeum tidal flat: long-term environmental and ecological changes in marine benthic flora and fauna in relation to the embankment. Ocean Coast. Manage. 102: 559571.
Stroud, D. A., Baker, A., Blanco, D. E., Davidson, N. C., Delany, S., Ganter, B., Gill, R., González, P., Haanstra, L., Morrison, R. I. G., Piersma, T., Scott, D. A., Thorup, O., West, R., Wilson, J. and Zöckler, C. (on behalf of the International Wader Study Group) (2006) The conservation and population status of the world’s waders at the turn of the millennium. Pp. 643648 in Boere, G. C., Galbraith, C. A. and Stroud, D. A., eds. Waterbirds around the world. Edinburgh, UK: The Stationery Office.
Studds, C. E., Kendall, B. E., Murray, N. J., Wilson, H. B., Rogers, D. I., Clemens, R. S., Gosbell, K., Hassell, C. J., Jessop, R., Melville, D. S., Milton, D. A., Minton, C. D. T., Possingham, H. P., Riegen, A. C., Straw, P., Woehler, E. J. and Fuller, R. A. (2017) Rapid population decline in migratory shorebirds relying on Yellow Sea tidal mudfiats as stopover sites. Nature Commun. 8: 14895.
Thompson, J. J. (1993) Modeling the local abundance of shorebirds staging on migration. Theor. Popul. Biol. 44: 299315.
van Gils, J. A., Kraan, C., Dekinga, A., Koolhaas, A., Drent, J., de Goeij, P. and Piersma, T. (2009) Reversed optimality and predictive ecology: burrowing depth forecasts population change in a bivalve. Biol. Lett.5: 58.
Wang, C. K. (2015) Effects of marine aquaculture on water environment and counter measures for pollution prevention and control: a case study of sea cucumber breeding in Jimo, Qingdao, China. China Agricult. Inform. 7: 148. (In Chinese)
Wang, Y., Ren, M. and Zhu, D. (1986) Sediment supply to the continental shelf by the major rivers of China. J. Geol. Soc. 143: 935944.
Wang, Y. and Aubrey, D. G. (1987) The characteristics of the China coastline. Cont. Shelf Res. 7: 329349.
Wei, L. P. (1984) A preliminary experiment on the artificial rearing of Aloidis laevis (Hinds) and its habits. Mar. Sci. 6: 3235. (In Chinese).
Yang, H. Y., Chen, B., Piersma, T., Zhang, Z. and Ding, C. (2016) Molluscs of an intertidal soft-sediment area in China: Does overfishing explain a high density but low diversity community that benefits staging shorebirds? J. Sea Res. 109: 2028.
Zhang, C. P. and Li, F. X. (2016) Spatial distribution and potential ecological risk assessment of heavy metals in sediments of Yalu River estuary wetland mudflat. Chi. J. Appl. Ecol. 27: 28842890. (In Chinese).
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