Abstract
Current guidelines for instrumenting birds state that external devices should not exceed 3–5% of the birds’ body mass; however, the energetic consequences of carrying any given device mass are likely to vary according to the morphology and ecology of the species concerned. We used a freeware program to estimate the mechanical power requirements of flight at the minimum power speed for 80 species of flying seabird from 8 major groups with payloads of increasing mass. Devices representing 3% of the bird’s body mass resulted in an increase in energy expenditure for flight ranging from 4.67 to 5.71% without accounting for the increase in body drag coefficient associated with external devices. This effect differed within and between seabird lineages with members of the Alcidae and Phalacrocoracidae experiencing the highest energetic costs of any increase in device mass. We propose that device effects on seabirds could be further reduced through consideration of species-specific effects of added payload and drag.
Similar content being viewed by others
References
Afanasyev V, Prince P (1993) A miniature storing activity recorder for seabird species. Ornis Scand 24:243–246
Ballard G, Ainley DG, Ribic CA, Barton KR (2001) Effect of instrument attachment and other factors on foraging trip duration and nesting success of Adélie penguins. Condor 103:481–490
Bannasch R, Wilson RP, Culik B (1994) Hydrodynamic aspects of design and attachment of a back-mounted device in penguins. J Exp Biol 194:83–96
Barron D, Brawn J, Weatherhead P (2010) Meta analysis of transmitter effects on avian behaviour and ecology. Methods Ecol Evo 1:180–187
Benvenuti S, Bonadonna F, Dall’Antonia L, Gudmundsson G (1998) Foraging flights of breeding thick-billed murres (Uria lomvia) as revealed by bird-borne direction recorders. Auk 115:57–66
Birt-Friesen V, Montevecchi W, Cairns D, Macko S (1989) Activity-specific metabolic rates of free-living northern gannets and other seabirds. Ecology 70:357–367
Blanc F, Brelurut A (1997) Short-term behavioral effects of equipping red deer hinds with a tracking collar. Int J Mamm Biol 62:18–26
Bowlin M, Wikelski M (2008) Pointed wings, low wingloading and calm air reduce migratory flight costs in songbirds. PLoS One 3:e2154
Bowman R, Aborn D (2001) Effects of different radiotransmitter harnesses on the behavior of Florida scrub-jays. Fla Field Nat 29:81–86
Brown R (1963) The flight of birds. Biol Rev 38:460–489
Buehler DA, Fraser JD, Fuller MR, McAllister LS, Seegar JKD (1995) Captive and field-tested radio transmitter attachments for bald eagles. J Field Ornithol 66:173–180
Burger A, Shaffer S (2008) Application of tracking and data-logging technology in research and conservation of seabirds. Auk 125:253–264
Burns J, Ydenberg R (2002) The effects of wing loading and gender on the escape flights of least sandpipers (Calidris minutilla) and western sandpipers (Calidris mauri). Behav Ecol Sociobiol 52:128–136
Butler P, Green J, Boyd I, Speakman J (2004) Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods. Funct Ecol 18:168–183
Caccamise D, Hedin R (1985) An aerodynamic basis for selecting transmitter loads in birds. Wilson Bull 97:306–318
Cairns D, Bredin K, Montevecchi W (1987) Activity budgets and foraging ranges of breeding common murres. Auk 104:218–224
Calvo B, Furness R (1992) A review of the use and the effects of marks and devices on birds. Ringing Migr 13:129–151
Chiaradia A, Ropert-Coudert Y, Healy M, Knott N (2005) Finding the balance: the effect of the position of external devices on little penguins. Polar Biosci 18:46–53
Cramp S, Simmons K (1983) The birds of the Western Palearctic. vol. 3: waders to gulls. Oxford University Press, Oxford
Croll D, Gaston A, Burger A, Konnoff D (1992) Foraging behavior and physiological adaptation for diving in thick-billed murres. Ecology 73:344–356
Croxall J (1987) Seabirds: feeding ecology and role in marine ecosystems. Cambridge University Press, Cambridge
Culik B, Wilson RP (1991) Swimming energetics and performance of instrumented Adélie penguins (Pygoscelis adeliae). J Exp Biol 158:355–368
Culik B, Wilson R (1992) Field metabolic rates of instrumented Adélie penguins using double-labelled water. J Comp Physiol B Biochem Syst Environ Physiol 162:567–573
Culik B, Bannasch R, Wilson R (1994) External devices on penguins: how important is shape? Mar Biol 118:353–357
De la Cueva H, Blake R (1993) Mechanics and energetics of ground effect in flapping flight. Contemp Math 141:421–442
Del Hoyo J, Elliott A, Sargatal J, Cabot J, ICfB Preservation (1992) Handbook of the birds of the world. Lynx Edicions, Barcelona
Del Hoyo J, Elliott A, Sargatal J, Cabot J, ICfB Preservation (1996) Handbook of the birds of the world. Lynx Edicions, Barcelona
Dial K, Biewener A, Tobalske B, Warrick D (1997) Mechanical power output of bird flight. Nature 390:67–70
Falk K, Benvenuti S, Dall’Antonia L, Kampp K, Ribolini A (2000) Time allocation and foraging behaviour of chick rearing Brünnich’s Guillemots Uria lomvia in high arctic Greenland. Ibis 142:82–92
Fedak M (2004) Marine animals as platforms for oceanographic sampling: a “win/win” situation for biology and operational oceanography. Mem Natl Inst Polar Res 58:133–147
Fraser WR, Trivelpiece WZ (1996) Factors controlling the distribution of seabirds: winter-summer heterogeneity in the distribution of Adélie penguin populations. Antarct Res Ser 70:257–272
Fraser G, Jones I, Hunter F (2002) Male-female differences in parental care in monogamous crested auklets. Condor 104:413–423
Furness R, Bryant D (1996) Effect of wind on field metabolic rates of breeding northern fulmars. Ecology 77:1181–1188
Furness RW, Camphuysen KCJ (1997) Seabirds as monitors of the marine environment. ICES J Mar Sci J du Conseil 54:726–737
Gales R, Williams C, Ritz D (1990) Foraging behavior of the little penguin, eudyptula-minor—initial results and assessment of instrument effect. J Zool 220:61–85
Garthe S, Montevecchi W, Davoren G (2007) Flight destinations and foraging behaviour of northern gannets (Sula bassana) preying on a small forage fish in a low-Arctic ecosystem. Deep Sea Res. (II Top Stud Oceanogr) 54:311–320
Gauthier-Clerc M, Le Maho Y (2001) Beyond bird marking with rings. Ardea 89:221–230
Gessaman J, Nagy K (1988) Transmitter loads affect the flight speed and metabolism of homing pigeons. Condor 90:662–668
Gessaman J, Workman G, Fuller M (1991) Flight performance, energetics and water turnover of tippler pigeons with a harness and dorsal load. Condor 93:546–554
Gillespie TW (2001) Remote sensing of animals. Prog Phys Geogr 25:355–362
Godfrey JD, Bryant DM (2003) Effects of radio transmitters: review of recent radio-tracking studies. Sci Conserv 214:83–95
Greenwood RJ, Sargeant AB (1973) Influence of radio packs on captive mallards and blue-winged teal. J Wildl Manage 37:3–9
Grémillet D, Dey R, Wanless S, Harris MP, Regel J (1996) Determining food intake by great cormorants and European shags with electronic balances (Determinando las caracteristicas de ingestión de Phalacrocorax carbo y P. aristotelis con balanzas electrónicas). J Field Ornithol 67:637–648
Hambly C, Harper E, Speakman J (2004a) The energy cost of loaded flight is substantially lower than expected due to alterations in flight kinematics. J Exp Biol 207:3969–3976
Hambly C, Pinshow B, Wiersma P, Verhulst S, Piertney S, Harper E, Speakman J (2004b) Comparison of the cost of short flights in a nectarivorous and a non-nectarivorous bird. J Exp Biol 207:3959–3968
Harper P, Croxall J, Cooper J (1985) A guide to foraging methods used by marine birds in Antarctic and Subantarctic seas. BIOMASS Handbk 24:1–24
Harrison P (1983) Seabirds. An identification guide. Breckenham: Croom Helm. Houghton Mifflin, Boston
Hazekamp AAH, Mayer R, Osinga N (2010) Flow simulation along a seal: the impact of an external device. Eur J Wildl Res 56:131–140
Hedenström A (1993) Migration by soaring or flapping flight in birds: the relative importance of energy cost and speed. Philos Trans R Soc Lond Ser B Biol Sci 342:353–361
Hodum P, Sydeman W, Visser G, Weathers W (1998) Energy expenditure and food requirement of Cassin’s auklets provisioning nestlings. Condor 100:546–550
Hooge PN (1991) The effects of radio weight and harnesses on time budgets and movements of acorn woodpeckers. J Field Ornithol 62:230–238
Huettmann F, Diamond A (2001) Seabird colony locations and environmental determination of seabird distribution: a spatially explicit breeding seabird model for the Northwest Atlantic. Ecol Model 141:261–298
Hull C, Kaiser G, Lougheed C, Lougheed L, Boyd S, Cooke F (2001) Intraspecific variation in commuting distance of marbled murrelets (Brachyramphus marmoratus): ecological and energetic consequences of nesting further inland. Auk 118:1036–1046
Jenni L, Jenni-Eiermann S (1998) Fuel supply and metabolic constraints in migrating birds. J Avian Biol 29:521–528
Kenward RE (2001) A manual for wildlife radio tagging. Academic Press, London
Klaassen M (1996) Metabolic constraints on long-distance migration in birds. J Exp Biol 199:57–64
Kvist A, Lindström Å, Green M, Piersma T, Visser G (2001) Carrying large fuel loads during sustained bird flight is cheaper than expected. Nature 413:730–732
Lovvorn J, Jones D (1994) Biomechanical conflicts between adaptations for diving and aerial flight in estuarine birds. Estuar Coasts 17:62–75
Mahoney S (1984) Plumage wettability of aquatic birds. Auk 101:181–185
Massey B, Keane K, Boardman C (1988) Adverse effects of radio transmitters on the behaviour of nesting least terns. Condor 90:945–947
Mehlum F, Gabrielsen G (1993) The diet of high arctic seabirds in coastal and ice covered, pelagic areas near the Svalbard archipelago. Polar Res 12:1–20
Murray DL, Fuller MR (2000) A critical review of the effects of marking on the biology of vertebrates. In: Boitani L, Fuller TK (eds) Research techniques in animal ecology: controversies and consequences. Columbia University Press, New York, pp 15–64
Naef-Daenzer B, Widmer F, Nuber M (2001) A test for effects of radio-tagging on survival and movements of small birds. Avian Sci 1:15–23
Nagy K (1980) CO2 production in animals: analysis of potential errors in the doubly labeled water method. Am J Physiol Regul Integr Comp Physiol 238:466–473
Navarro J, González-Solís J, Viscor G, Chastel O (2008) Ecophysiological response to an experimental increase of wing loading in a pelagic seabird. J Exp Mar Biol Ecol 358:14–19
Norberg U (1990) Vertebrate flight: mechanics, physiology, morphology, ecology and evolution. Springer, Berlin
Norberg U, Winter Y (2006) Wing beat kinematics of a nectar-feeding bat, Glossophaga soricina, flying at different flight speeds and Strouhal numbers. J Exp Biol 209:3887–3897
Nudds R, Bryant D (2002) Consequences of load carrying by birds during short flights are found to be behavioral and not energetic. Am J Physiol Regul Integr Comp Physiol 283:249–256
Obrecht H, Pennycuick C, Fuller M (1988) Wind tunnel experiments to assess the effect of back-mounted radio transmitters on bird body drag. J Exp Biol 135:265–273
Ortega-Jiménez V, Álvarez-Borrego S, Arriaga-Ramírez S, Renner M, Bridge E (2010) Takeoff flight performance and plumage wettability in Cassin’s auklet Ptychoramphus aleuticus, Xantus’s murrelet Synthliboramphus hypoleucus and Leach’s storm-petrel Oceanodroma leucorhoa. J Ornithol 151:169–177
Paquette GA, Devries JH, Emery RB, Howerter DW, Joynt BL, Sankowski TP (1997) Effects of transmitters on reproduction and survival of wild Mallards. J Wildl Manage 61:953–961
Paredes R, Jones IL, Boness DJ (2005) Reduced parental care, compensatory behaviour and reproductive costs of thick-billed murres equipped with data loggers. Anim Behav 69:197–208
Passos C, Navarro J, Giudici A, González-Solís J (2010) Effects of extra mass on the pelagic behavior of a seabird. Auk 127:100–107
Pelletier D, Guillemette M, Grandbois J, Butler P (2008) To fly or not to fly: high flight costs in a large sea duck do not imply an expensive lifestyle. Proc R Soc Lond Ser B Biol Sci 275:2117–2124
Pennycuick C (1972) Animal flight. Edward Arnold, London
Pennycuick C (1987) Flight of seabirds. In: Croxall JP (ed) Seabirds: feeding ecology and role in marine ecosystems. Cambridge University Press, Cambridge, pp 43–62
Pennycuick C (1989) Bird flight performance. Oxford University Press Oxford, Oxford
Pennycuick C (2002) Gust soaring as a basis for the flight of petrels and albatrosses (Procellariiformes). Avian Sci 2:1–12
Pennycuick C (2008) Modelling the flying bird. Academic Press/Elsevier, Boston
Perry MC (1981) Abnormal behaviour of canvasbacks equipped with radio transmitters. J Wildl Manage 45:786–789
Phillips RA, Xavier JC, Croxall JP, Burger AE (2003) Effects of satellite transmitters on albatrosses and petrels. Auk 120:1082–1090
Piatt J, Sydeman W, Browman H (2007) Seabirds as indicators of marine ecosystems. Mar Ecol Prog Ser 352:199–204
Pietz PJ, Krapu GL, Greenwood RJ, Lokemoen JT (1993) Effects of harness transmitters on behaviour and reproduction of wild mallards. J Wildl Manage 57:696–703
Prince P, Francis M (1984) Activity budgets of foraging gray-headed albatrosses. Condor 86:297–300
Rayner J (1988) Form and function in avian flight. Curr Ornithol 5:1–66
Rayner J (1993) On aerodynamics and the energetics of vertebrate flapping flight. Contemp Math 141:351–400
Rayner J (1999) Estimating power curves of flying vertebrates. J Exp Biol 202:3449–3461
Reynolds RT, White GC, Joy SM, Mannan RW (2004) Effects of radiotransmitters on northern goshawks: do tailmounts lower survival of breeding males? J Wildl Manage 68:25–32
Ribak G, Weihs D, Arad Z (2005) Water retention in the plumage of diving great cormorants Phalacrocorax carbo sinensis. J Avian Biol 36:89–95
Ricklefs R, White S (1981) Growth and energetics of chicks of the sooty tern (Sterna fuscata) and common tern (S. hirundo). Auk 98:361–378
Ropert Coudert Y, Kato A, Poulin N, Grémillet D (2009) Leg attached data loggers do not modify the diving performances of a foot propelled seabird. J Zool 279:294–297
Ropert-Coudert Y, Wilson RP (2005) Trends and perspectives in animal-attached remote sensing. Front Ecol Environ 3:437–444
Ropert-Coudert Y, Knott N, Chiaradia A, Kato A (2007) How do different data logger sizes and attachment positions affect the diving behaviour of little penguins? Deep Sea Res (II Top Stud Oceanogr) 54:415–423
Rosén M, Hedenström A (2001) Testing predictions from flight mechanical theory: a case study of Cory’s shearwater and Audouin’s gull. Acta Ethol 3:135–140
Rutz C, Hays GC (2009) New frontiers in biologging science. Biol Lett 5:289–292
Ryan P, Pichegru L, Ropert-Coudert Y, Grémillet D, Kato A (2010) On a wing and a prayer: the foraging ecology of breeding cape cormorants. J Zool 280:25–32
Saraux C, Le Bohec C, Durant JM, Viblanc VA, Gauthier-Clerc M, Beaune D, Park YH, Yoccoz NG, Stenseth NC, Le Maho Y (2011) Reliability of flipper-banded penguins as indicators of climate change. Nature 469:203–206
Schmid D, Grémillet D, Culik B (1995) Energetics of underwater swimming in the great cormorant (Phalacrocorax carbo sinensis). Mar Biol 123:875–881
Schmidt-Wellenburg C, Biebach H, Daan S, Visser G (2007) Energy expenditure and wing beat frequency in relation to body mass in free flying barn swallows (Hirundo rustica). J Comp Physiol B Biochem Syst Environ Physiol 177:327–337
Schmidt-Wellenburg C, Engel S, Visser G (2008) Energy expenditure during flight in relation to body mass: effects of natural increases in mass and artificial load in rose coloured starlings. J Comp Physiol B 178:767–777
Schultner J, Welcker J, Speakman J, Nordøy E, Gabrielsen G (2010) Application of the two-sample doubly labelled water method alters behaviour and affects estimates of energy expenditure in black-legged kittiwakes. J Exp Biol 213:2958–2966
Shaffer S (2010) A review of seabird energetics using the doubly labeled water method. Comp Biochem Physiol A: Mol Integr Physiol. Published online doi:10.1016/j.cbpa.2010.07.012
Snow D, Perrins C, Gillmor R (1998) The birds of the Western Palearctic. Oxford University Press, Oxford
Spear L, Ainley D (1997) Flight behaviour of seabirds in relation to wind direction and wing morphology. Ibis 139:221–233
Storer R (1960) Adaptive radiation in birds. Biol Comp Physiol birds 1:15–55
Sydeman W, Hobson K, Pyle P, McLaren E (1997) Trophic relationships among seabirds in central California: combined stable isotope and conventional dietary approach. Condor 99:327–336
Thaxter C, Wanless S, Daunt F, Harris M, Benvenuti S, Watanuki Y, Grémillet D, Hamer K (2010) Influence of wing loading on the trade-off between pursuit-diving and flight in common guillemots and razorbills. J Exp Biol 213:1018–1025
Tieleman BI, Dijkstra TH, Klasing KC, Visser GH, Williams JB (2008) Effects of experimentally increased costs of activity during reproduction on parental investment and self-maintenance in tropical house wrens. Behav Ecol 19:949–959
Tobalske B, Hedrick T, Dial K, Biewener A (2003) Comparative power curves in bird flight. Nature 421:363–366
Tucker V (1977) Scaling and avian flight. In: Pedley T (ed) Scale effects in animal locomotion. Academic Press, New York, pp 497–510
Tuyttens F, Macdonald D, Roddam A (2002) Effects of radio-collars on European badgers (Meles meles). J Zool 257:37–42
Vermeer K (1981) The importance of plankton to Cassin’s auklets during breeding. J Plankton Res 3:315–329
Videler J, Groenewegen A, Gnodde M, Vossebelt G (1988) Indoor flight experiments with trained kestrels. II: The effect of added weight on flapping flight kinematics. J Exp Biol 134:185–199
Watanabe Y, Takahashi A, Sato K, Viviant M, Bost C (2011) Poor flight performance in deep-diving cormorants. J Exp Biol 214:412–421
Watanuki Y, Daunt F, Takahashi A, Newell M, Wanless S, Sato K, Miyazaki N (2008) Microhabitat use and prey capture of a bottom-feeding top predator, the European shag, shown by camera loggers. Mar Ecol Prog Ser 356:283–293
Watson KP, Granger RA (1998) Hydrodynamic effect of a satellite transmitter on a juvenile green turtle (Chelonia mydas). J Exp Biol 201:2497–2505
Weimerskirch H, Mougey T, Hindermeyer X (1997) Foraging and provisioning strategies of black-browed albatrosses in relation to the requirements of the chick: natural variation and experimental study. Behav Ecol 8:635–643
Weimerskirch H, Guionnet T, Martin J, Shaffer S, Costa D (2000) Fast and fuel efficient? Optimal use of wind by flying albatrosses. Proc R Soc Lond Ser B Biol Sci 267:1869–1874
Wikelski M, Kays R, Kasdin N, Thorup K, Smith J, Swenson G (2007) Going wild: what a global small-animal tracking system could do for experimental biologists. J Exp Biol 210:181–186
Wilson RP, McMahon CR (2006) Measuring devices on wild animals: what constitutes acceptable practice? Front Ecol Environ 4:147–154
Wilson RP, Wilson MPT (1989) A peck activity record for birds fitted with devices. J Field Ornithol 60:104–108
Wilson RP, Grant WS, Duffy DC (1986) Recording devices on free-ranging marine animals: does measurement affect foraging performance? Ecology 67:1091–1093
Wilson R, Spairani H, Coria N, Culik B, Adelung D (1990) Packages for attachment to seabirds: what color do adelie penguins dislike least? J Wildl Manage 54:447–451
Wilson R, Hustler K, Ryan P, Burger A, Nöldeke E (1992) Diving birds in cold water: do Archimedes and Boyle determine energetic costs? Am Nat 140:179–200
Wilson R, Kreye J, Lucke K, Urquhart H (2004) Antennae on transmitters on penguins: balancing energy budgets on the high wire. J Exp Biol 207:2649–2662
Xirouchakis SM, Andreou G (2009) Foraging behaviour and flight characteristics of Eurasian griffons Gyps fulvus in the island of Crete, Greece. Wildl Biol 15:37–52
Yen P, Huettmann F, Cooke F (2004) Modelling abundance and distribution of marbled murrelets (Brachyramphus marmoratus) using GIS, marine data and advanced multivariate statistics. Ecol Model 171:395–413
Zschille J, Stier N, Roth M (2008) Radio tagging American mink (Mustela vison)—experience with collar and intraperitoneal-implanted transmitters. Eur J Wildl Res 54:263–268
Acknowledgments
We are grateful to Colin Pennycuick for his help at various stages from the use of his Flight program to his constructive comments on the manuscript. We also thank Adrian Gleiss for helpful discussions. Finally, this study would have not been carried out without financial support from the California Department of Fish and Game’s Oil Spill Response Trust Fund (through the Oiled Wildlife Care Network at the Wildlife Health Center, School of Veterinary Medicine, University of California, Davis) and the Royal Society for Prevention of Cruelty to Animals (RSPCA, Wilberforce Way, Southwater, Horsham, West Sussex, RH13 9RS, United Kingdom).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. E. Hauber.
Rights and permissions
About this article
Cite this article
Vandenabeele, S.P., Shepard, E.L., Grogan, A. et al. When three per cent may not be three per cent; device-equipped seabirds experience variable flight constraints. Mar Biol 159, 1–14 (2012). https://doi.org/10.1007/s00227-011-1784-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-011-1784-6