Water level affects availability of optimal feeding habitats for threatened migratory waterbirds

Abstract

Extensive ephemeral wetlands at Poyang Lake, created by dramatic seasonal changes in water level, constitute the main wintering site for migratory Anatidae in China. Reductions in wetland area during the last 15 years have led to proposals to build a Poyang Dam to retain high winter water levels within the lake. Changing the natural hydrological system will affect waterbirds dependent on water level changes for food availability and accessibility. We tracked two goose species with different feeding behaviors (greater white-fronted geese Anser albifrons [grazing species] and swan geese Anser cygnoides [tuber-feeding species]) during two winters with contrasting water levels (continuous recession in 2015; sustained high water in 2016, similar to those predicted post-Poyang Dam), investigating the effects of water level change on their habitat selection based on vegetation and elevation. In 2015, white-fronted geese extensively exploited sequentially created mudflats, feeding on short nutritious graminoid swards, while swan geese excavated substrates along the water edge for tubers. This critical dynamic ecotone successively exposes subaquatic food and supports early-stage graminoid growth during water level recession. During sustained high water levels in 2016, both species selected mudflats, but also to a greater degree of habitats with longer established seasonal graminoid swards because access to tubers and new graminoid growth was restricted under high-water conditions. Longer established graminoid swards offer less energetically profitable forage for both species. Substantial reduction in suitable habitat and confinement to less profitable forage by higher water levels is likely to reduce the ability of geese to accumulate sufficient fat stores for migration, with potential carryover effects on subsequent survival and reproduction. Our results suggest that high water levels in Poyang Lake should be retained during summer, but permitted to gradually recede, exposing new areas throughout winter to provide access for waterbirds from all feeding guilds.

REFERENCES Aharon-Rotman, Y., Bauer, S., & Klaassen, M. (2016). A chain is as strong as its weakest link: Assessing the consequences of habitat loss and degradation in a long-distance migratory shorebird. Emu, 116, 199–207. https://doi.org/10.1071/MU15029 Alerstam, T., & Högstedt, G. (1982). Bird migration and reproduction in relation to habitats for survival and breeding. Ornis Scandinavica, 13, 25–37. https://doi.org/10.2307/3675970 Barzen, J. (2008). Phase 1 report: How development projects may impact wintering waterbirds at Poyang Lake. Unpublished report submitted to Hydro-ecology Institute of the Yangtze Water Resources Commission. International Crane Foundation, Baraboo, Wisconsin, USA Barzen, J., Engels, M., Burnham, J., Harris, J., & Wu, G. (2009). Potential impacts of a water control structure on the abundance and distribution of wintering waterbirds at Poyang Lake. International Crane Foundation, Baraboo, Wisconsin. Cadieux, M.-C., Gauthier, G., Hughes, R. J., & Burger, A. (2005). Feeding ecology of Canada Geese (Branta canadensis interior) in sub-arctic inland tundra during brood-rearing. The Auk, 122, 144–157. https://doi.org/10.1642/0004-8038(2005)122[0144:FEOCGB]2.0.CO;2 Cao, L., Barter, M., & Lei, G. (2008). New Anatidae population estimates for eastern China: Implications for current flyway estimates. Biological Conservation, 141, 2301–2309. https://doi.org/10.1016/j.biocon.2008.06.022 Cao, L., Meng, F., Yang, W., Shan, K., Liu, J., & Fox, A. D. (2011). Effects of length of growing season on biomass accumulation and reproductive investment of Vallisneria natans (Lour.) H. Hara. Fundamental and Applied Limnology, 179, 115–120. https://doi.org/10.1127/1863-9135/2011/0179-0115 Cao, L., Zhang, Y., Barter, M., & Lei, G. (2010). Anatidae in eastern China during the non-breeding season: Geographical distributions and protection status. Biological Conservation, 143, 650–659. https://doi.org/10.1016/j.biocon.2009.12.001 Casanova, M. T. (1999). Plant establishment in Paroo wetlands: The importance of water regime. In R. T. Kingsford (Ed.), A free-flowing river: The ecology of the Paroo river (pp. 138–148). Sydney: New South Wales National Parks and Wildlife Service. Cheng, Y., Cao, L., Barter, M., & Xu, W. (2009). Wintering waterbirds at the Anhui Shengjin Hu National Nature Reserve, China. University of Science and Technology of China Press (In Chinese and English), Hefei, China. de Leeuw, J., Si, Y., Zeng, Y., Lei, G., Li, L., & Liu, Y. (2006). Mapping flood recessional grasslands used by overwintering geese: a multi-temporal remote sensing application ISPRS mid-term symposium 2006 remote sensing: from pixels to processes, vol. 1, Enschede, The Netherlands, p 5. Fang, J., Wang, Z., Zhao, S., Li, Y., Tang, Z., Yu, D., … Da, L. (2006). Biodiversity changes in the lakes of the Central Yangtze. Frontiers in Ecology and the Environment, 4, 369–377. https://doi.org/10.1890/1540-9295(2006)004[0369:BCITLO]2.0.CO;2 Feng, L., Hu, C., Chen, X., Cai, X., Tian, L., & Gan, W. (2012). Assessment of inundation changes of Poyang Lake using MODIS observations between 2000 and 2010. Remote Sensing of Environment, 121, 80–92. https://doi.org/10.1016/j.rse.2012.01.014 Finlayson, M., Harris, J., McCartney, M., Lew, Y., & Zhang, C. (2010). Report on Ramsar visit to Poyang Lake Ramsar site, PR China. Report prepared on behalf of the Secretariat of the Ramsar Convention, April 12–17, pp. 1–34. Fox, A. D., & Abraham, K. F. (2017). Why geese benefit from the transition from natural vegetation to agriculture. Ambio, 46, 188–197. https://doi.org/10.1007/s13280-016-0879-1 Fox, A. D., Cao, L., Zhang, Y., Barter, M., Zhao, M. J., Meng, F. J., & Wang, S. L. (2011). Declines in the tuber-feeding waterbird guild at Shengjin Lake National Nature Reserve, China – a barometer of submerged macrophyte collapse. Aquatic Conservation: Marine and Freshwater Ecosystems, 21, 82–91. https://doi.org/10.1002/aqc.1154 Fox, A. D., Hearn, R. D., Cao, L., Cong, P. H., Wang, X., Zhang, Y., … Rees, E. C. (2008). Preliminary observations of diurnal feeding patterns of Swan Geese Anser cygnoides using two different habitats at Shengjin Lake, Anhui Province, China. Wildfowl, 58, 20–30. Gekara, O., Prigge, E., Bryan, W., Nestor, E., & Seidel, G. (2005). Influence of sward height, daily timing of concentrate supplementation, and restricted time for grazing on forage utilization by lactating beef cows. Journal of Animal Science, 83, 1435–1444. https://doi.org/10.2527/2005.8361435x Guo, H., Hu, Q., Zhang, Q., & Feng, S. (2012). Effects of the three gorges dam on Yangtze river flow and river interaction with Poyang Lake, China: 2003–2008. Journal of Hydrology, 416, 19–27. https://doi.org/10.1016/j.jhydrol.2011.11.027 Harrison, X. A., Blount, J. D., Inger, R., Norris, D. R., & Bearhop, S. (2011). Carry-over effects as drivers of fitness differences in animals. Journal of Animal Ecology, 80, 4–18. https://doi.org/10.1111/j.1365-2656.2010.01740.x Harrison, X. A., Hodgson, D. J., Inger, R., Colhoun, K., Gudmundsson, G. A., McElwaine, G., … Bearhop, S. (2013). Environmental conditions during breeding modify the strength of mass-dependent carry-over effects in a migratory bird. PLoS ONE, 8, e77783. https://doi.org/10.1371/journal.pone.0077783 Hassall, M., Riddington, R., & Helden, A. (2001). Foraging behaviour of brent geese, Branta b. bernicla, on grasslands: Effects of sward length and nitrogen content. Oecologia, 127, 97–104. https://doi.org/10.1007/s004420000563 Heuerman, N. (2007). Tall swards and small grazers: competition, facilitation and coexistence of different-sized grazers. Ph.D. Thesis, Wageningen Inger, R., Harrison, X. A., Ruxton, G. D., Newton, J., Colhoun, K., Gudmundsson, G. A., … Bearhop, S. (2010). Carry-over effects reveal reproductive costs in a long-distance migrant. Journal of Animal Ecology, 79, 974–982. https://doi.org/10.1111/j.1365-2656.2010.01712.x Ji, W., Zeng, N., Wang, Y., Gong, P., Xu, B., & Bao, S. (2007). Analysis on the waterbirds community survey of Poyang Lake in winter. Geographic Information Sciences, 13, 51–64. https://doi.org/10.1080/10824000709480632 Jia, Q., Koyama, K., Choi, C.-Y., Kim, H.-J., Cao, L., Gao, D., … Fox, A. D. (2016). Population estimates and geographical distributions of swans and geese in East Asia based on counts during the non-breeding season. Bird Conservation International, 26, 1–21. https://doi.org/10.1017/S0959270915000386 Jiao, L. (2009). Scientists line up against dam that would alter protected wetlands. Science, 326, 508–509. https://doi.org/10.1126/science.326_508 Kingsford, R. T. (2000). Ecological impacts of dams, water diversions and river management on floodplain wetlands in Australia. Austral Ecology, 25, 109–127. https://doi.org/10.1046/j.1442-9993.2000.01036.x Kingsford, R. T., Bino, G., & Porter, J. L. (2017). Continental impacts of water development on waterbirds, contrasting two Australian river basins: Global implications for sustainable water use. Global Change Biology, 23, 4958–4969. https://doi.org/10.1111/gcb.13743 Kingsford, R., & Thomas, R. (2004). Destruction of wetlands and waterbird populations by dams and irrigation on the Murrumbidgee River in arid Australia. Environmental Management, 34, 383–396. https://doi.org/10.1007/s00267-004-0250-3 Lai, X., Shankman, D., Huber, C., Yesou, H., Huang, Q., & Jiang, J. (2014). Sand mining and increasing Poyang Lake's discharge ability: A reassessment of causes for lake decline in China. Journal of Hydrology, 519, 1698–1706. https://doi.org/10.1016/j.jhydrol.2014.09.058 Lai, G., Wang, P., & Li, L. (2016). Possible impacts of the Poyang Lake (China) hydraulic project on lake hydrology and hydrodynamics. Hydrology Research, 47, 187–205. https://doi.org/10.2166/nh.2016.174 Lane, S. J., & Hassall, M. (1996). Nocturnal feeding by Dark-bellied Brent Geese Branta bernicla bernicla. Ibis, 138, 291–297. https://doi.org/10.1111/j.1474-919X.1996.tb04341.x Li, Y., Zhang, Q., Yao, J., Werner, A. D., & Li, X. (2013). Hydrodynamic and hydrological modeling of the Poyang Lake catchment system in China. Journal of Hydrologic Engineering, 19, 607–616. Lu, J., & Zhang, J. (1996). Feeding ecology of three wintering geese species at lower Yangtze valley, China. In Chinese Ornithological Society, Wild Bird Society of Taipei and China Wildlife Conservation Association (Eds.), Chinese ornithological research (pp. 143–152). Beijing: China Forest Publishing House. McComb, A. J., & Lake, P. S. (1990). Australian Wetlands. Sydney: Angus & Robertson. Morrissette, M., Bêty, J., Gauthier, G., Reed, A., & Lefebvre, J. (2010). Climate, trophic interactions, density dependence and carry-over effects on the population productivity of a migratory Arctic herbivorous bird. Oikos, 119, 1181–1191. https://doi.org/10.1111/j.1600-0706.2009.18079.x Nolet, B., Bevan, R., Klaassen, M., Langevoord, O., & Van der Heijden, Y. (2002). Habitat switching by Bewick's swans: Maximization of average long-term energy gain? Journal of Animal Ecology, 71, 979–993. https://doi.org/10.1046/j.1365-2656.2002.00662.x Owen, M., Wells, R. L., & Black, J. M. (1992). Energy budgets of wintering barnacle geese: The effects of declining food resources. Ornis Scandinavica, 23, 451–458. https://doi.org/10.2307/3676676 Prop, J., & Vulink, T. (1992). Digestion by barnacle geese in the annual cycle: The interplay between retention time and food quality. Functional Ecology, 6, 180–189. https://doi.org/10.2307/2389753 R Core Team (2014). A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Si, Y., Skidmore, A. K., Wang, T., de Boer, W. F., Toxopeus, A. G., Schlerf, M., … Exo, K.-M. (2011). Distribution of Barnacle Geese Branta leucopsis in relation to food resources, distance to roosts, and the location of refuges. Ardea, 99, 217–226. https://doi.org/10.5253/078.099.0212 Studds, C. E., Kendall, B. E., Murray, N. J., Wilson, H. B., Rogers, D. I., Clemens, R. S., … Melville, D. S. (2017). Rapid population decline in migratory shorebirds relying on Yellow Sea tidal mudfiats as stopover sites. Nature, 8, 1. https://doi.org/10.1038/ncomms14895 Tan, G., Guo, S., & Wang, J. (2013). Study on the evolution of hydrology and water resources in Poyang Lake ecological economic zone. Beijing, China: China Water & Power Press. Tinkler, E., Montgomery, W., & Elwood, R. (2009). Foraging ecology, fluctuating food availability and energetics of wintering brent geese. Journal of Zoology, 278, 313–323. https://doi.org/10.1111/j.1469-7998.2009.00578.x Van der Wal, R., Madan, N., Van Lieshout, S., Dormann, C., Langvatn, R., & Albon, S. (2000). Trading forage quality for quantity? Plant phenology and patch choice by Svalbard reindeer. Oecologia, 123, 108–115. https://doi.org/10.1007/s004420050995 Wang, X., Fox, A. D., Cong, P., & Cao, L. (2013). Food constraints explain the restricted distribution of wintering Lesser White-fronted Geese Anser erythropus in China. Ibis, 155, 576–592. https://doi.org/10.1111/ibi.12039 Wang, Z. Y., Lee, J. H., & Cheng, D. (2005). Impacts of the TGP project on the Yangtze River ecology and management strategies. International Journal of River Basin Management, 3, 237–246. https://doi.org/10.1080/15715124.2005.9635264 Warnock, N. (2010). Stopping vs. staging: The difference between a hop and a jump. Journal of Avian Biology, 41, 621–626. https://doi.org/10.1111/j.1600-048X.2010.05155.x Wu, J., Huang, J., Han, X., Gao, X., He, F., Jiang, M., … Shen, Z. (2004). The three gorges dam: An ecological perspective. Frontiers in Ecology and the Environment, 2, 241–248. https://doi.org/10.1890/1540-9295(2004)002[0241:TTGDAE]2.0.CO;2 Wu, G., & Liu, Y. (2015). Capturing variations in inundation with satellite remote sensing in a morphologically complex, large lake. Journal of Hydrology, 523, 14–23. https://doi.org/10.1016/j.jhydrol.2015.01.048 Xie, P. (2003). Three-Gorges Dam: Risk to ancient fish. Science, 302, 1149–1151. https://doi.org/10.1126/science.302.5648.1149b Ydenberg, R., Prins, H. T., & Van Dijk, J. (1984). A lunar rhythm in the nocturnal foraging activities of wintering barnacle geese. Wildfowl, 35, 93–96. Yu, H., Wang, X., Cao, L., Zhang, L., Jia, Q., Lee, H., … Fox, A. D. (2017). Are declining populations of wild geese in China “prisoners” of their natural habitats? Current Biology, 27, 376–377. https://doi.org/10.1016/j.cub.2017.04.037 Zhang, Y., Cao, L., Barter, M., Fox, A. D., Zhao, M., Meng, F., … Zhu, W. (2011). Changing distribution and abundance of Swan Goose Anser cygnoides in the Yangtze River floodplain: The likely loss of a very important wintering site. Bird Conservation International, 21, 36–48. https://doi.org/10.1017/S0959270910000201 Zhang, Y., Jia, Q., Prins, H. H., Cao, L., & de Boer, W. F. (2015). Effect of conservation efforts and ecological variables on waterbird population sizes in wetlands of the Yangtze River. Scientific Reports, 5, 17136. https://doi.org/10.1038/srep17136 Zhang, J.-X., & Lu, J.-J. (1999). Feeding ecology of two wintering geese species at Poyang Lake, China. Journal of Freshwater Ecology, 14, 439–445. https://doi.org/10.1080/02705060.1999.9663702 Zhang, Y., Prins, H. H., Cao, L., Zhao, M., & de Boer, W. F. (2016). Variation in elevation and sward height facilitate coexistence of goose species through allometric responses in wetlands. Waterbirds, 39, 34–44. https://doi.org/10.1675/063.039.0105 Zhang, Q., Ye, X.-C., Werner, A. D., Li, Y.-L., Yao, J., Li, X.-H., & Xu, C.-Y. (2014). An investigation of enhanced recessions in Poyang Lake: Comparison of Yangtze River and local catchment impacts. Journal of Hydrology, 517, 425–434. https://doi.org/10.1016/j.jhydrol.2014.05.051 Zhao, M., Cao, L., Klaassen, M., Zhang, Y., & Fox, A. D. (2015). Avoiding competition? Site use, diet and foraging behaviours in two similarly sized geese wintering in China. Ardea, 103, 27–38. https://doi.org/10.5253/arde.v103i1.a3 Zhao, M., Cong, P., Barter, M., Fox, A. D., & Cao, L. (2012). The changing abundance and distribution of Greater White-fronted Geese Anser albifrons in the Yangtze River floodplain: Impacts of recent hydrological changes. Bird Conservation International, 22, 135–143. https://doi.org/10.1017/S0959270911000542 Zhou, Y., Jeppesen, E., Li, J., Zhang, Y., Zhang, X., & Li, X. (2016). Impacts of Three Gorges Reservoir on the sedimentation regimes in the downstream-linked two largest Chinese freshwater lakes. Scientific Reports, 6, 35396. https://doi.org/10.1038/srep35396 Zhou, B., Zhou, L. Z., Chen, J. Y., Xu, W. B., & Cheng, Y. Q. (2009). The assemblage dynamic and territorial behaviors of wintering Hooded Crane (Grus monacha) in Shengjin Lake. Chinese Journal of Wildlife, 30, 133–136. (in Chinese).