Abstract
We investigated how habitat-specific differences in behavioural patterns affected Brent Goose energetics along a feeding continuum from natural aquatic to inland agricultural habitats. Time-budgets showed that geese using salt-marshes and inland habitats spent more time flying, being aggressive and alert than birds feeding in aquatic areas, and also spent much less time roosting. Frequency of disturbance was found to be higher in terrestrial habitats compared to aquatic habitats. These stress-related behavioural differences between habitats highlight the vulnerability of the species associated with adapting to different food sources. Combining time-budgets with activity-specific BMR-multiplicators showed that activity-based metabolic rates ranged from 1.7 to 2.7 × BMR within habitats exploited by Brent Geese, and emphasized that aquatic areas represent the energetically least expensive foraging habitat for these birds. This is largely the result of habitat-specific variation in time spent flying. These findings underline the importance of measuring habitat-specific behaviour and disturbance when studying avian energetics, and demonstrate the risk of uncritically using allometric relationships between body mass and energy expenditure in energetic studies and impact assessments across different habitats.
Zusammenfassung
Unterschiede in den energetischen Kosten von Ringelgänsen Branta bernicla entlang eines Gradienten von aquatischen zu landwirtschaftlich genutzten Lebensräumen: die Bedeutung des habitatspezifischen Energieaufwandes
Wir untersuchten, auf welche Weise habitatbedingte Unterschiede im Verhaltensmuster den Energiehaushalt von Ringelgänsen Branta bernicla beeinflussten, die entlang eines Gradienten vom natürlichen aquatischen Lebensraum bis hin zu landwirtschaftlich genutztem Binnenland nach Nahrung suchten. Die Zeitbudgets zeigten, dass Gänse, die Salzwiesen und Binnenlandhabitate nutzten, mehr Zeit mit Fliegen verbrachten sowie aggressiver und wachsamer waren als Vögel, die in aquatischen Gebieten nach Futter suchten, und außerdem weniger Zeit mit Rasten zubrachten. In den terrestrischen Habitaten war die Störungshäufigkeit im Vergleich höher als in den aquatischen Lebensräumen. Diese stressbedingten Verhaltensunterschiede zwischen den Lebensräumen betonen die mit der Anpassung an verschiedene Nahrungsquellen einhergehende Angreifbarkeit dieser Vogelart. Die Kombination der Zeitbudgets mit aktivitätsabhängigen Leistungsumsatzfaktoren zeigte, dass innerhalb der von den Ringelgänsen genutzten Habitate die aktivitätsbedingten Stoffwechselraten zwischen dem 1,7- und 2,7-fachen Grundumsatz lagen und veranschaulichte, dass aquatische Lebensräume für diese Vögel die Nahrungsgebiete mit den geringsten energetischen Kosten darstellen. Dies ist zum Großteil auf habitatspezifische Unterschiede im Zeitanteil zurückzuführen, der mit Fliegen verbracht wurde. Die Befunde unterstreichen die Bedeutung der Messung von habitatspezifischen Verhaltensmustern und Störungsfaktoren für energetische Untersuchungen an Vögeln und zeigen die Gefahr der unkritischen Verwendung allometrischer Verhältnisse zwischen Körpermasse und Energieaufwand für energetische Studien und Folgenabschätzungen in verschiedenen Habitaten auf.
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References
Ackerman JT, Takekawa JY, Orthmeyer DL, Fleskes JP, Yee JL, Kruse KL (2006) Spatial use by wintering greater white-fronted geese relative to a decade of habitat change in California’s Central Valley. J Wildl Manage 70:965–976
Altmann J (1974) Observational study of behaviour: sampling methods. Behaviour 49:227–267
Amano T, Ushiyama K, Fujita G, Higuchi H (2006) Foraging patch selection and departure by non-omniscient foragers: a field example in white-fronted geese. Ethology 112:544–553
Bédard J, Gauthier G (1989) Comparative energy budgets of greater snow geese Chen caerulescens atlantica staging in two habitats in spring. Ardea 77:3–20
Bos D, Drent RH, Rubinigg M, Stahl J (2005) The relative importance of food biomass and quality for patch and habitat choice in Brent Geese Branta bernicla. Ardea 93:5–16
Boyd H (2005) Brent Goose (Brant) Branta bernicla. In: Kear J (ed) Ducks, geese and swans, vol 1. Oxford University Press, Oxford, pp 321–329
Bruinzeel LW, van Eerden MR, Drent RH, Vulink JT (1997) Scaling metabolisable energy intake and daily energy expenditure in relation to the size of herbivorous waterfowl: limits set by available foraging time and digestive performance. Van Zee tot Land 65:111–132
Brunckhorst H (1996) Ökologie und Energetik der Pfeifente (Anas Penelope L. 1758) im Schleswig-holsteinischen Wattenmeer. Kovač, Hamburg
Burkholder J, Tomasko D, Touchette B (2007) Seagrasses and eutrophication. J Exp Mar Biol Ecol 350:46–72
Clausen P (1998) Choosing between feeding on Zostera and salt marsh: factors affecting habitat use by Brent Geese in spring. Norsk Polarinst Skr 200:277–294
Clausen P (2000) Modelling water level influence on habitat choice and food availability for Zostera feeding Brent Geese Branta bernicla in non-tidal areas. Wildl Biol 6:75–87
Clausen P, Percival SM (1998) Changes in distribution and habitat use of Svalbard Light-bellied Brent Geese Branta bernicla hrota, 1980–1995: driven by Zostera availability? Norsk Polarinst Skr 200:253–276
Cottam C, Munro DA (1954) Eelgrass status and environmental relations. J Wildl Manage 18:449–460
Drent R, Ebbinge B, Weijand B (1978/1979) Balancing the energy budgets of arctic-breeding geese throughout the annual cycle: a progress report. Verh Orn Ges Bayern 23:239–264
Ebbinge BS (1992) Regulation of numbers of dark-bellied Brent Geese Branta bernicla bernicla on spring staging sites. Ardea 80:203–228
Einarsen AS (1965) Black brant, sea Goose of the Pacific coast. University of Washington Press, Seattle
Fox AD, Madsen J, Boyd H, Kuijken E, Norriss DW, Tombre IM, Stroud DA (2005) Effects of agricultural change on abundance, fitness components and distribution of two arctic-nesting Goose populations. Glob Change Biol 11:881–893
Fretwell SD, Lucas HL (1970) On territorial behavior and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheor 19:16–36
Ganter B (2000) Seagrass (Zostera spp.) as food for Brent Geese (Branta bernicla): an overview. Helgoland Mar Res 54:63–70
Gauthier G, Bédard J, Bédard Y (1984) Comparison of daily energy expenditure of greater snow geese between two habitats. Can J Zool 62:1304–1307
Hughes RG (2004) Climate change and loss of salt-marshes: consequences for birds. Ibis 146:21–28
Krause-Jensen D, Sagert S, Schubert H, Bostrom C (2008) Empirical relationships linking distribution and abundance of marine vegetation to eutrophication. Ecol Indic 8:515–529
Ladin ZS, Castelli PM, McWilliams SR, Williams CK (2011) Time energy budgets and food use of Atlantic brant across their wintering range. J Wildl Manage 75:273–282
Lasiewski RC, Dawson WR (1967) A re-examination of the relation between standard metabolic rate and body weight in birds. Condor 69:13–23
Lovvorn JR, Baldwin JR (1996) Intertidal and farmland habitats of ducks in the Puget Sound region: a landscape perspective. Biol Conserv 77:97–114
Madsen J (1985) Relations between change in spring habitat selection and daily energetics of pink-footed geese Anser brachyrhynchus. Ornis Scand 16:222–228
Madsen J (1988) Autumn feeding ecology of herbivorous wildfowl in the Danish Wadden Sea, and impact of food supplies and shooting on movements. Dan Rev Game Biol 13:1–32
Madsen J, Cracknell G, Fox T (eds) (1999) Goose populations of the Western Palearctic. A review of status and distribution. Wetlands International Publ. No. 48, Wetlands International, Wageningen. National Environmental Research Institute, Rönde
McKay HV, Bishop JD, Feare CJ, Stevens MC (1993) Feeding by Brent Geese can reduce yield of oilseed rape. Crop Prot 12:101–105
McKinney RA, McWilliams SR (2005) A new model to estimate daily energy expenditure for wintering waterfowl. Wilson Bull 117:44–55
Merne OJ, Boertmann D, Boyd H, Mitchell C, ÓBrian M, Reed A, Sigfusson A (1999) Light-bellied Brent Goose Branta bernicla hrota: Canada. In: Madsen J, Cracknell G, Fox T (eds) Goose Populations of the Western Palearctic. A Review of Status and Distribution. National Environmental Research Institute, Rönde, Denmark and Wetlands International, Wageningen, The Netherlands. Wetlands International Publication 48, pp 298–311
Miller MR, Eadie JM (2006) The allometric relationship between resting metabolic rate and body mass in wild waterfowl (Anatidae) and an application to estimation of winter habitat requirements. Condor 108:166–177
Nagy KA (1987) Field metabolic rate and food requirement scaling in mammals and birds. Ecol Monogr 57:112–128
Nagy KA (2005) Field metabolic rate and body size. J Exp Biol 208:1621–1625
Nielsen SL, Sand-Jensen K, Borum J, Geertz-Hansen O (2002) Depth colonization of eelgrass (Zostera marina) and macroalgae as determined by water transparency in Danish coastal waters. Estuaries 25:1025–1032
Nolet BA, Bevan RM, Klaassen M, Langevoord O, Van der Heijden YGJT (2002) Habitat switching by Bewick’s swans: maximization of average long-term energy gain? J Anim Ecol 71:979–993
Owen M, Wells RL, Black JM (1992) Energy budgets of wintering barnacle geese: the effects of declining food resources. Ornis Scand 23:451–458
Pease ML, Rose RK, Butler MJ (2005) Effects of human disturbances on the behavior of wintering ducks. Wildl Soc Bull 33:103–112
Persson H (1989) Food selection, movements and energy budgets of staging and wintering geese on South Swedish farmland. PhD thesis, Lund University
Ricklefs RE, Konarzewski M, Daan S (1996) The relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147:1047–1071
Riddington R, Hassall M, Lane SJ, Turner PA, Walters R (1996) The impact of disturbance on the behaviour and energy budgets of Brent Geese Branta b. bernicla. Bird Study 43:269–279
Short FT, Burdick DM (1996) Quantifying eelgrass habitat loss in relation to housing development and nitrogen loading in Waquoit Bay, Massachusetts. Estuaries 19:730–739
Short FT, Neckles HA (1999) The effects of global climate change on seagrasses. Aquat Bot 63:169–196
Smith LM, Vangilder LD, Kennamer RA (1985) Foods of wintering brant in eastern North America. J Field Ornithol 56:286–289
Spaans B, Postma P (2001) Inland pastures are an appropriate alternative for salt-marshes as a feeding area for spring-fattening dark-bellied Brent Geese Branta bernicla. Ardea 89:427–440
Speakman JR (2005) Body size, energy metabolism and lifespan. J Exp Biol 208:1717–1730
Stahl J (2001) Limits to the co-occurrence of avian herbivores. PhD dissertation, University of Groningen, Groningen, The Netherlands
Stock M, Hofeditz F (1996) Zeit-Aktivitäts-Budgets von Ringelgänsen (Branta bernicla bernicla) in unterschiedlich stark von Menschen beeinfluβten Salzwiesen des Wattenmeeres. Vogelwarte 38:121–145
Stock M, Hofeditz F (1997) Grenzen der Kompensation: energiebudgets von Ringelgänsen (Branta b. bernicla)—die Wirkung von Störreizen. J Ornithol 138:387–411
Summers RW (1990) The Effect on winter wheat of grazing by Brent Geese Branta bernicla. J Appl Ecol 27:821–833
Summers RW, Critchley NR (1990) Use of grassland and field selection by Brent Geese Branta bernicla. J Appl Ecol 27:834–846
Therkildsen O, Madsen J (2000) Energetics of feeding on winter wheat versus pasture grasses: a window of opportunity for winter range expansion in the pink-footed Goose Anser brachyrhynchus. Wildl Biol 6:65–74
Tinkler E, Montgomery WI, Elwood RW (2009) Foraging ecology, fluctuating food availability and energetics of wintering Brent Geese. J Zool 278:313–323
Tubbs CR, Tubbs JM (1982) Brent Geese Branta bernicla bernicla and their food in the solent, Southern England. Biol Conserv 23:33–54
van Eerden MR, Zijlstra M, van Roomen M, Timmerman A (1996) The response of Anatidae to changes in agricultural practice: long-term shifts in the carrying capacity of wintering waterfowl. Gibier Faune Sauvage 13:681–706
van Eerden MR, Drent RH, Stahl J, Bakker JP (2005) Connecting seas: western Palaearctic continental flyway for water birds in the perspective of changing land use and climate. Glob Change Biol 11:894–908
Walsberg GE (1983) Avian ecological energetics. In: Farner DS, King JR (eds) Avian biology 7. Academic Press, New York, pp 161–220
Ward DH, Reed A, Sedinger JS, Black JM, Derksen DV, Castelli PM (2005) North American Brant: effects of changes in habitat and climate on population dynamics. Glob Change Biol 11:869–880
Waycott M, Duarte CM, Carruthers TJB, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Short FT, Williams SL (2009) Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci USA 106:12377–12381
Wooley JB, Owen RB (1978) Energy costs of activity and daily energy expenditure in the black duck. J Wildl Manage 42:739–745
Acknowledgments
The Mariager Fjord data were collected in conjunction with two MSc studies (KKC and CCF) supervised by PC, where Kim Nørgaard Mouritsen acted as co-supervisor. He is thanked for his help during these studies. We also want to thank Stuart Bearhop and two anonymous reviewers for very constructive comments on an earlier draft.
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Communicated by F. Bairlein.
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Clausen, K.K., Clausen, P., Fox, A.D. et al. Varying energetic costs of Brent Geese along a continuum from aquatic to agricultural habitats: the importance of habitat-specific energy expenditure. J Ornithol 154, 155–162 (2013). https://doi.org/10.1007/s10336-012-0881-8
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DOI: https://doi.org/10.1007/s10336-012-0881-8