Wintering Swan Geese maximize energy intake through substrate foraging depth when feeding on buried Vallisneria natans tubers
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摘要
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.
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.
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.
引文
Alerstam T,Lindstr?m?.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.
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.