Wintering Swan Geese maximize energy intake through substrate foraging depth when feeding on buried <i>Vallisneria natans</i> tubers

Yan Chen; Yong Zhang; Lei Cao; Willem F. de Boer; Anthony D. Fox

doi:10.1186/s40657-019-0145-x

Volume 10 Issue 1

Nov. 2019

Turn off MathJax

Article Contents

Abstract

References

Avian Research > 2019 > 10(1): 6. > DOI: 10.1186/s40657-019-0145-x

Yan Chen, Yong Zhang, Lei Cao, Willem F. de Boer, Anthony D. Fox. 2019: Wintering Swan Geese maximize energy intake through substrate foraging depth when feeding on buried Vallisneria natans tubers. Avian Research, 10(1): 6. DOI: 10.1186/s40657-019-0145-x

Citation:

PDF (656 KB)

Wintering Swan Geese maximize energy intake through substrate foraging depth when feeding on buried Vallisneria natans tubers

1.
School of Life Sciences, University of Science and Technology of China, Hefei 230027, China
2.
Co-Innovation Center for Sustainable Forestry in Southern China, College of Biology and the Environment, Nanjing Forestry University, Nanjing 210037, China
3.
Research Center for Eco-Environmental Science, Chinese Academic of Sciences, 18 Shuangqing Road, Beijing 100085, China
4.
University of Chinese Academy of Sciences, 19 Yuquan Road, Shijingshan District, Beijing 100049, China
5.
Resource Ecology Group, Wageningen University, Droevendaalsesteeg3a, 6708 PB Wageningen, The Netherlands
6.
Department of Bioscience, Aarhus University, Kalø, Grenåvej 14, 8410 Rønde, Denmark

Funds:

the Natural Science Foundation of Jiangsu Province BK20170922

the Key Strategic Program of the Chinese Academy of Sciences, Water Ecological Security Assessment and Great Strategy Research of Middle and Lower Yangtze River ZDRW-ZS-2017-3

More Information

Corresponding author:
Yong Zhang, yong.zhang@njfu.edu.cn

Lei Cao, leicao@rcees.ac.cn
Received Date: 24 Oct 2018
Accepted Date: 17 Feb 2019
Available Online: 24 Apr 2022
Publish Date: 24 Feb 2019

Graphical Abstract

Abstract

Abstract

Background
Foraging theory predicts that animals select patches that offer the highest net rate of energy gain. Hence, prey distribution patterns and spatiotemporal heterogeneity play important roles in determining animal feeding patch selection. For waterfowl foraging on buried aquatic plant tubers, the distribution and biomass of these plant organs vary with depth in the substrate. Since excavation costs also increase with depth, the energy intake of the animals foraging on these plants is highly sediment depth dependent.
Methods
Here, using observations of Swan Geese (Anser cygnoides) foraging on Vallisneria natans tubers, we test our hypothesis that geese feeding on tubers buried at intermediate sediment depth maximize their daily energy intake because of the interaction between tuber size and abundance with depth. To do this, we measured the distribution patterns of buried Vallisneria tubers under both undisturbed conditions and post-exploitation by geese (i.e. giving-up conditions). We investigated the relationship between tuber size and burial depth, and total tuber biomass within each sediment layer in undisturbed and exploited plots. Finally, we compared modelled Swan Goose daily energy intake feeding on Vallisneria tubers buried at different sediment layers (1-10, 11-20 and 21-30 cm below the surface).
Results
Dry weight of Vallisneria tubers linearly increased with burial depth, while average total dry weight density of tubers showed a unimodal relationship, peaking at intermediate levels. Not surprisingly, Swan Geese foraged most intensively on tubers buried at intermediate sediment depths, where they maximize their daily energy intake. Our results support our hypothesis that Swan Geese feeding on tubers at intermediate depths maximize their daily energy intake.
Conclusions
Our study is the first to quantify foraging strategies of Swan Geese during the wintering period, emphasizing the importance of plant traits on foraging selection of belowground foragers.
- Energetic trade-off,
- Optimal foraging,
- Shengjin Lake,
- Substrate,
- Tuber burial depth,
- Yangtze River

FullText(HTML)

The authors regret that Fig. 1 and its caption should be replaced as below.

Figure 1. The 35 national nature reserves, 16 wetlands of international importance, and 1 UNESCO world heritage site along China's coastal wetlands (till the end of 2022). Some national nature reserves are also wetlands of international importance. E, M, and L represent the national nature reserves that were designated in the 1980s, 1990s, and after 2000, respectively.

DownLoad: Full-Size Img PowerPoint

In addition, the last sentence of the third paragraph of section "3.1. Policy and administration" should be:

To improve the conservation of key waterbird habitats in the Yellow Sea region, which have high conservation priority for migratory birds in the EAAF, coastal wetlands in Yancheng, Jiangsu Province have been inscribed as UNESCO World Heritage Site, "Migratory bird sanctuaries along the coast of the Yellow Sea‒Bohai Gulf of China (Phase Ⅰ)", in 2019 (Fig. 1; World Heritage Committee, 2019), and 11 sites have been included in the list of Phase Ⅱ applications.

The authors would like to apologise for any inconvenience caused.

References (40)

References

Alerstam T, Lindström Å. Optimal bird migration: the relative importance of time, energy, and safety. In: Gwinner E, editor. Bird migration. Berlin: Springer; 1990. p. 331-51.

Amano T, Ushiyama K, Fujita G, Higuchi H. Alleviating grazing damage by white-fronted geese: an optimal foraging approach. J Appl Ecol. 2004;41:675-88.

Bergman CM, Fryxell JM, Gates CC, Fortin D. Ungulate foraging strategies: energy maximizing or time minimizing? J Anim Ecol. 2001;70: 289-300.

Cao L, Barter M, Lei G. New Anatidae population estimates for eastern China: implications for current flyway estimates. Biol Conserv. 2008;141:2301-9.

Caraco T. Time budgeting and group-size—test of theory. Ecology. 1979;60:618-27.

Charnov EL. Optimal foraging, the marginal value theorem. Theor Popul Biol. 1976;9:129-36.

Chudzinska ME, van Beest FM, Madsen J, Nabe-Nielsen J. Using habitat selection theories to predict the spatiotemporal distribution of migratory birds during stopover—a case study of pink-footed geese Anser brachyrhynchus. Oikos. 2015;124:851-60.

Emlen JM. The role of time and energy in food preference. Am Nat. 1966;100:611-7.

Fox AD, Cao L, Zhang Y, Barter M, Zhao MJ, Meng FJ, Wang SL. Declines in the tuber-feeding waterbird guild at Shengjin Lake National Nature Reserve, China—a barometer of submerged macrophyte collapse. Aquat Conserv. 2011;21:82-91.

Fox AD, Glahder CM, Walsh AJ. Spring migration routes and timing of Greenland white-fronted geese—results from satellite telemetry. Oikos. 2003;103:415-25.

Fox AD, Hearn RD, Cao L, Cong PH, Wang X, Zhang Y, Dou ST, Shao XF, Barter M, Rees EC. Preliminary observations of diurnal feeding patterns of Swan Geese Anser cygnoides using two different habitats at Shengjin Lake, Anhui Province, China. Wildfowl. 2008;58:20-30.

Hamberg J, Findlay SEG, Limburg KE, Diemont SAW. Post-storm sediment burial and herbivory of Vallisneria americana in the Hudson River estuary: mechanisms of loss and implications for restoration. Restor Ecol. 2017;25:629-39.

Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM. Plant structural traits and their role in anti-herbivore defence. Perspect Plant Ecol. 2007;8:157-78.

Hidding B, Klaassen M, de Boer T, de Vries PP, Nolet BA. Aquatic plant shows flexible avoidance by escape from tuber predation by swans. Basic Appl Ecol. 2012;13:50-8.

Hidding B, Nolet BA, van Eerden MR, Guillemain M, Klaassen M. Burial depth distribution of fennel pondweed tubers (Potamogeton pectinatus) in relation to foraging by Bewick's swans. Aquat Bot. 2009;90:321-7.

Jeschke JM, Kopp M, Tollrian R. Predator functional responses: discriminating between handling and digesting prey. Ecol Monogr. 2002;72:95-112.

Jokela J, Schmid-Hempel P, Rigby MC. Dr. Pangloss restrained by the Red Queen—steps towards a unified defence theory. Oikos. 2000;89:267-74.

Kear J. Ducks, geese and swans. Oxford: Oxford University Press; 2005.

Kersten M, Visser W. The rate of food processing in the Oystercatcher: food intake and energy expenditure constrained by a digestive bottleneck. Funct Ecol. 1996;10:440-8.

Kim GY, Ji YK, Ganf GG, Lee CW, Joo GJ. Impact of over-wintering waterfowl on tuberous bulrush (Bolboschoenus planiculmis) in tidal flats. Aquat Bot. 2013;107(9):17-22.

Klaassen M, Nolet BA. The role of herbivorous water birds in aquatic systems through interactions with aquatic macrophytes, with special reference to the Bewick's Swan—Fennel Pondweed system. Hydrobiologia. 2007;584:205-13.

Langvatn R, Hanley TA. Feeding-patch choice by Red Deer in relation to foraging efficiency—an experiment. Oecologia. 1993;95:164-70.

Macarthur RH, Pianka ER. On optimal use of a patchy environment. Am Nat. 1966;100:603-9.

Murakami M. Foraging habitat shift in the narcissus flycatcher, Ficedula narcissina, due to the response of herbivorous insects to the strengthening defenses of canopy trees. Ecol Res. 1998;13:73-82.

Nolet BA, Gyimesi A. Underuse of stopover site by migratory swans. J Ornithol. 2013;154:695-703.

Nolet BA, Gyimesi A, Klaassen RHG. Prediction of bird-day carrying capacity on a staging site: a test of depletion models. J Anim Ecol. 2006;75:1285-92.

Oudman T, Onrust J, de Fouw J, Spaans B, Piersma T, van Gils JA. Digestive capacity and toxicity cause mixed diets in Red Knots that maximize energy intake rate. Am Nat. 2014;183:650-9.

Owen M. An assessment of fecal analysis technique in waterfowl feeding studies. J Wildl Manag. 1975;39:271-9.

Pyke GH. Optimal foraging theory—a critical review. Annu Rev Ecol Syst. 1984;15:523-75.

Richman SE, Lovvorn JR. Predator size, prey size and threshold food densities of diving ducks: does a common prey base support fewer large animals? J Anim Ecol. 2009;78:1033-42.

Rowcliffe JM, Sutherland WJ, Watkinson AR. The functional and aggregative responses of a herbivore: underlying mechanisms and the spatial implications for plant depletion. J Anim Ecol. 1999;68:853-68.

Rybicki NB, Carter V. Effect of sediment depth and sediment type on the survival of Vallisneria Americana Michx grown from tubers. Aquat Bot. 1986;24:233-40.

Santamaria L, Rodriguez-Girones MA. Hiding from swans: optimal burial depth of sago pondweed tubers foraged by Bewick's swans. J Ecol. 2002;90:303-15.

Sponberg AF, Lodge DM. Seasonal belowground herbivory and a density refuge from waterfowl herbivory for Vallisneria americana. Ecology. 2005;86:2127-34.

Wang X, Fox AD, Cong PH, Cao L. Food constraints explain the restricted distribution of wintering Lesser White-fronted Geese Anser erythropus in China. Ibis. 2013;155:576-92.

Ward D, Shrestha MK, Golan-Goldhirsh A. Evolution and ecology meet molecular genetics: adaptive phenotypic plasticity in two isolated Negev desert populations of Acacia raddiana at either end of a rainfall gradient. Ann Bot. 2012;109:247-55.

Weiner J. Physiological limits to sustainable energy budgets in birds and mammals—ecological implications. Trends Ecol Evol. 1992;7:384-8.

Wilmshurst JF, Fryxell JM, Colucci PE. What constrains daily intake in Thomson's gazelles? Ecology. 1999;80: 2338-47.

Ydenberg RC. Behavioral decisions about foraging and predator avoidance. In: Dukas R, editor. Cognitive ecology: the evolutionary ecology of information processing and decision making. Chicago: University of Chicago Press; 1998. p. 343-78.

Zhang Y, Cao L, Barter M, Fox AD, Zhao MJ, Meng FJ, Shi HQ, Jiang Y, Zhu WZ. Changing distribution and abundance of Swan Goose Anser cygnoides in the Yangtze River floodplain: the likely loss of a very important wintering site. Bird Conserv Int. 2011;21:36-48.

Cited By

Cited by

Periodical cited type(8)

1.	Fei Xu, Wei Wu, Jie Wei, et al. Migratory herbivorous waterfowl track multiple resource waves during spring migration. Proceedings of the Royal Society B: Biological Sciences, 2024, 291(2030) DOI:10.1098/rspb.2024.1448
2.	Sungbae Joo, Yu-Seong Choi, Sang-Yeon Lee. Home Range and Habitat Use of the Swan Goose (Anser cygnoides L. 1758) during Wintering in the Seocheon Tidal Flat, South Korea, Using GPS-Based Telemetry. Animals, 2022, 12(21): 3048. DOI:10.3390/ani12213048
3.	Li Liu, Xiaoguang Liu, Chao Du, et al. Spring diet and energy intake of whooper swans (Cygnus cygnus) at the Yellow River National Wetland in Baotou, China. PLOS ONE, 2022, 17(2): e0264528. DOI:10.1371/journal.pone.0264528
4.	Li Liu, Chao Du, Yan Sun, et al. Spring diet and energy intake of tundra swan (Cygnus columbianus) at the Yellow River National Wetland in Baotou, China. PeerJ, 2022, 10: e13113. DOI:10.7717/peerj.13113
5.	Nyambayar Batbayar, Kunpeng Yi, Junjian Zhang, et al. Combining Tracking and Remote Sensing to Identify Critical Year-Round Site, Habitat Use and Migratory Connectivity of a Threatened Waterbird Species. Remote Sensing, 2021, 13(20): 4049. DOI:10.3390/rs13204049
6.	Iderbat Damba, Junjian Zhang, Kunpeng Yi, et al. Seasonal and regional differences in migration patterns and conservation status of Swan Geese (Anser cygnoides) in the East Asian Flyway. Avian Research, 2021, 12(1) DOI:10.1186/s40657-021-00308-y
7.	Qin Zhu, Keith A. Hobson, Qingshan Zhao, et al. Migratory connectivity of Swan Geese based on species' distribution models, feather stable isotope assignment and satellite tracking. Diversity and Distributions, 2020, 26(8): 944. DOI:10.1111/ddi.13077
8.	Kevin A. Wood, Geoff M. Hilton, Julia L. Newth, et al. Seasonal variation in energy gain explains patterns of resource use by avian herbivores in an agricultural landscape: Insights from a mechanistic model. Ecological Modelling, 2019, 409: 108762. DOI:10.1016/j.ecolmodel.2019.108762

Other cited types(0)

Figures(5) / Tables(1)

Get Citation

PDF

XML

Article Metrics

Article views (230) PDF downloads (6) Cited by(8)

	Chao Yu, Xuying Lu, Deli Sun, Mengnan Chu, Xueyun Li, Qun Li. 2024: River width and depth as key factors of diurnal activity energy expenditure allocation for wintering Spot-billed Ducks in the Xin’an River Basin. Avian Research, 15(1): 100159. DOI: 10.1016/j.avrs.2024.100159
	Peizhong Liu, Meihan Liu, Dongyang Xiao, Ying He, Rong Fan, Cai Lu, Li Wen, Qing Zeng, Guangchun Lei. 2023: Scaly-sided Merganser (Mergus squamatus) equalizes foraging costs with depth by switching foraging tactics. Avian Research, 14(1): 100129. DOI: 10.1016/j.avrs.2023.100129
	Zhenhua Wei, Lizhi Zhou. 2023: The impact of earlier flood recession on metacommunity diversity of wintering waterbirds at shallow lakes in the middle and lower Yangtze River floodplain. Avian Research, 14(1): 100102. DOI: 10.1016/j.avrs.2023.100102
	Yuxi Wang, Iderbat Damba, Qingshan Zhao, Yanbo Xie, Xueqing Deng, Rdi Ga, Guanhua Liu, Zhiwen Xu, Yue Li, Dali Gao, Wenbin Xu, Guoxun Chen, Lei Cao. 2021: Organising a juvenile ratio monitoring programme for 10 key waterbird species in the Yangtze River floodplain: analysis and proposals. Avian Research, 12(1): 72. DOI: 10.1186/s40657-021-00309-x
	Yanguang Fan, Lizhi Zhou, Lei Cheng, Yunwei Song, Wenbin Xu. 2020: Foraging behavior of the Greater White-fronted Goose (Anser albifrons) wintering at Shengjin Lake: diet shifts and habitat use. Avian Research, 11(1): 3. DOI: 10.1186/s40657-020-0189-y
	An An, Yong Zhang, Lei Cao, Qiang Jia, Xin Wang. 2018: A potential distribution map of wintering Swan Goose (Anser cygnoides) in the middle and lower Yangtze River ﬂoodplain, China. Avian Research, 9(1): 43. DOI: 10.1186/s40657-018-0134-5
	Wenjing Wan, LizhiZhou, Yunwei Song. 2016: Shifts in foraging behavior of wintering Hooded Cranes (Grus monacha) in three different habitats at Shengjin Lake, China. Avian Research, 7(1): 13. DOI: 10.1186/s40657-016-0047-0
	Wei Huang, Lizhi Zhou, Niannian Zhao. 2014: Temporal-spatial patterns of intestinal parasites of the Hooded Crane (Grus monacha) wintering in lakes of the middle and lower Yangtze River floodplain. Avian Research, 5(1): 6. DOI: 10.1186/s40657-014-0006-6
	Fengting ZHAO, Lizhi ZHOU, Wenbin XU. 2013: Habitat utilization and resource partitioning of wintering Hooded Cranes and three goose species at Shengjin Lake. Avian Research, 4(4): 281-290. DOI: 10.5122/cbirds.2013.0032
	Lei CAO, Mark BARTER, Meijuan ZHAO, Haoxian MENG, Yong ZHANG. 2011: A systematic scheme for monitoring waterbird populations at Shengjin Lake, China: methodology and preliminary results. Avian Research, 2(1): 1-17. DOI: 10.5122/cbirds.2011.0001

Wintering Swan Geese maximize energy intake through substrate foraging depth when feeding on buried Vallisneria natans tubers