Skip to main content

Advertisement

SpringerLink
Log in

Energy expenditure and food consumption of foraging Imperial cormorants in Patagonia, Argentina

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Energy management during the breeding season is crucial for central place foragers since parents need to feed themselves and their offspring while being spatially and temporally constrained. In this work, we used overall dynamic body acceleration as a measure of activity and also to allude to the foraging energy expenditure of breeding Imperial cormorants Phalacrocorax atriceps. We also analyzed how changes in the time or energy allocated to different activities affected the foraging trip energy expenditure and estimated the daily food requirements of the species. Birds spent 42 % of the total energy flying to and from the feeding areas and 16 % floating at sea. The level of activity underwater was almost 1.5 times higher for females than for males. The most expensive diving phase in terms of rate of energy expenditure was descending though the water column. The total foraging trip energy expenditure was particularly sensitive to variation in the amount of time spent flying. During the breeding season, adult cormorants breeding along the Patagonian coast would consume approximately 10,000 tons of food.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bishop CM, Butler PJ (1995) Physiological modelling of oxygen consumption in birds during flight. J Exp Biol 198:2153–2163

    Google Scholar 

  • Brooke ML (2004) The food consumption of the world’s seabirds. P Roy Soc Lond B Bio 271:246–248

    Article  Google Scholar 

  • Brown JH, Gilloly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  • Bulgarella M, Cella Pizarro L, Quintana F, Sapoznikow A, Gosztonyi AE, Kuba L (2008) Diet of Imperial Cormorants (Phalacrocorax atriceps) and rock shags (P. magellanicus) breeding sympatrically in Patagonia, Argentina. Ornitol Neotr 19:553–563

    Google Scholar 

  • Casaux R, Favero M, Silva P, Baroni A (2001) Sex differences in diving depths and diet of Antarctic shags at the South Shetland Islands. J Field Ornithol 72:22–29

    Google Scholar 

  • Cook TR, Bailleul F, Lescroël A, Tremblay Y, Bost CA (2008) Crossing the frontier: vertical transit rates of deep diving cormorants reveal depth zone of neutral buoyancy. Mar Biol 154:383–391

    Article  Google Scholar 

  • Cook TR, Kato A, Tanaka Y, Ropert-Coudert Y, Bost CA (2010) Buoyancy under control: underwater locomotor performance in a deep diving seabird suggest respiratory strategies for reducing foraging effort. PLoS ONE 5:e9839. doi:10.1371/journal.pone.0009839

    Article  Google Scholar 

  • Culik BM, Wilson RP (1994) Underwater swimming at low energetic cost by Pygoscelid penguins. J Exp Biol 197:65–78

    Google Scholar 

  • Cury PM, Boyd IL, Bonhommeau S, Anker-Nilssen T, Crawford RJM, Furness RW, Mills JA, Murphy EJ, Österblom H, Paleczny M, Piatt JF, Roux JP, Shannon L, Sydeman WJ (2012) Global seabird response to forage fish depletion—one third for the bird. Science 334:1703–1706

    Article  Google Scholar 

  • Enstipp MR, Daunt F, Wanless S, Humphreys EM, Hamer KC, Benvenuti S, Grémillet D (2006) Foraging energetics of North Sea birds confronted with fluctuation prey availability. In: Boyd IL, Wanless S, Camphuysen CJ (eds) Top predators in marine ecosystems, their role in monitoring and management. Cambridge University Press, Cambridge, pp 191–210

    Chapter  Google Scholar 

  • Favero M, Casaux R, Silva P, Barrera-Oro E, Coria N (1998) The diet of the Antarctic shag during summer at Nelson Island, Antarctica. Condor 100:112–118

    Article  Google Scholar 

  • Forbes SL, Jajam M, Kaiser GW (2000) Habitat constraints and spatial bias in seabird colony distributions. Ecography 23:575–578

    Article  Google Scholar 

  • Fossette S, Schofield G, Lilley MKS, Gleiss A, Hays GC (2012) Acceleration data reveal the energy management strategy of a marine ectotherm during reproduction. Funct Ecol 26:324–333

    Article  Google Scholar 

  • Frere E, Quintana F, Gandini P (2005) Cormoranes de la costa Patagónica: Estado poblacional, ecología y conservación. Hornero 20:35–52

    Google Scholar 

  • Gleiss AC, Dale JJ, Holland KN, Wilson RP (2010) Accelerating estimates of activity-specific metabolic rate in fishes: testing the applicability of acceleration data-loggers. J Exp Mar Biol Ecol 385:85–91

    Article  Google Scholar 

  • Gleiss AC, Wilson RP, Shepard ELC (2011) Making overall dynamic body acceleration work; on the theory of acceleration as a proxy for energy expenditure. Methods Ecol Evol 2(1):23–33

    Article  Google Scholar 

  • Gómez Laich A, Wilson RP, Quintana F, Shepard ELC (2008) Identification of Imperial cormorant Phalacrocorax atriceps behaviour using accelerometers. Endang Spec Res 10:29–37

    Article  Google Scholar 

  • Gómez Laich A, Wilson RP, Gleiss A, Shepard ELC, Quintana F (2011) Use of overall dynamic body acceleration for estimating energy expenditure in cormorants. Does locomotion in different media affect relationships? J Exp Mar Biol Ecol 399:151–155

    Article  Google Scholar 

  • Gómez Laich A, Quintana F, Shepard ELC, Wilson RP (2012) Intersexual differences in the diving behaviour of Imperial Cormorants. J Ornith 153:139–147

    Article  Google Scholar 

  • Gonzalez Miri L, Malacalza V (1999) Perfil nutricional de las principales especies en la dieta del Cormorán Real (Phalacrocorax albiventer) en Punta León (Chubut, Argentina). Ornitol Neotr 10:55–59

    Google Scholar 

  • Gosztonyi AE, Kuba L (1998) Fishes in the diet of the Imperial cormorant Phalacrocorax atriceps at Punta Lobería Chubut, Argentina. Mar Ornithol 26:59–61

    Google Scholar 

  • Green J, Halsey LG, Wilson RP, Frappell PB (2009) Estimating energy expenditure of animals using the accelerometry technique: activity, inactivity and comparison with the heart-rate technique. J Exp Biol 212:471–482

    Article  CAS  Google Scholar 

  • Grémillet D, Wright G, Lauder A, Carss DN, Wanless S (2003) Modelling the daily food requirements of wintering great cormorants: a bioenergetics tool for wildlife management. J App Ecol 40:266–277

    Article  Google Scholar 

  • Halsey LG, Shepard ELC, Hulston CJ, Venables MC, White CR, Jeukendrup AE, Wilson RP (2008a) Acceleration versus heart rate for estimating energy expenditure and speed during locomotion in animals: tests with an easy model species, Homo sapiens. Zoology 111:231–241

    Article  Google Scholar 

  • Halsey LG, Shepard ELC, Quintana F, Gómez Laich A, Green JA, Wilson RP (2008b) The relationship between oxygen consumption and body acceleration in a range of species. Comp Biochem Phys A 152:197–202

  • Halsey LG, Green JA, Wilson RP, Frappell PB (2009) Accelerometry to estimate energy expenditure during activity: best practice with data loggers. Physiol Biochem Zool 82:396–404

    Article  CAS  Google Scholar 

  • Halsey LG, Shepard ELC, Wilson RP (2011) Assessing the development and application of the accelerometry technique for estimating energy expenditure. Comp Biochem Physiol Part A 158:305–314

    Article  Google Scholar 

  • Harris S, Quintana F, Raya Rey A (2012) Prey Search behaviour of the Imperial Cormorant (Phalacrocorax atriceps) during the breeding season at Punta León, Argentina. Waterbirds 35:312–323

    Google Scholar 

  • Hedenstrom A, Alerstam T (1995) Optimal flight speed of birds. Philos Trans R Soc Lond B Biol Sci 348:471–487

    Article  Google Scholar 

  • Kacelnik A (1984) Central place foraging in starlings (Sturnus-vulgaris).1. Patch residence time. J Anim Ecol 53:283–299

    Article  Google Scholar 

  • Kato A, Nishiumi I, Naito Y (1996) Sexual differences in the diet of king cormorants at Macquarie Island. Polar Biol 16:75–77

    Google Scholar 

  • Kato A, Watanuki Y, Shaughnessy P, Le Maho Y, Naito Y (1999) Intersexual differences in the diving behaviour of foraging subantarctic cormorant (Phalacrocorax albiventer) and Japanese cormorant (P. filamentosus). CR Acad Sci 322:557–562

    Article  CAS  Google Scholar 

  • Kato A, Watanuki Y, Nishiumi I, Kuroki M, Shaughnessy P, Naito Y (2000) Variation in foraging and parental behavior of king cormorants. Auk 117:718–730

    Google Scholar 

  • Kramer DL (1988) The behavioural ecology of air breathing by aquatic animals. Can J Zool 66:89–94

    Article  Google Scholar 

  • Elliot KH, Le Vaillant, M, Kato A, Speakman JR, Ropert Coudert Y (2013) Accelerometry predicts daily energy expenditure in a bird with high activity levels. Biol Lett. doi:10.1098/rsbl.2012.09191744-957X

  • Liordos V, Goutner V (2009) Sexual differences in the diet of great cormorants Phalacrocorax carbo sinensis wintering in Greece. Eur J Wildl Res 55:301–308

    Article  Google Scholar 

  • Malacalza VE, Hall MA (1988) Sexing adult King Cormorants (Phalacrocorax albiventer) by discriminant analysis. Colon Waterbird 11:32–37

    Article  Google Scholar 

  • Orians GH, Pearson NE (1979) On the theory of central place foraging. In: Horn DJ, Mitchell RD, Stairs GR (eds) Analysis of ecological systems. Ohio State University Press, Columbus, pp 154–177

    Google Scholar 

  • Orta J (1992) Family Phalacrocoracidae (Cormorants). In: del Hoyo J, Elliott A, Sargatal J (eds) Handbook of the birds of the world, vol 1. Barcelona, Lynx Edicions, pp 326–353

    Google Scholar 

  • Pennycuick CJ (2008) Modelling the flying bird. Elsevier, Amsterdam

    Google Scholar 

  • Punta GE, Saravia JRC, Yorio PM (1993) The diet and foraging behaviour of two patagonian cormorants. Mar Ornithol 21:27–36

    Google Scholar 

  • Punta GE, Yorio P, Herrera G, Saravia JCR (2003) Biología reproductiva de los cormoranes imperial (Phalacrocorax atriceps) y cuello negro (P. magellanicus) en el golfo San Jorge, Chubut, Argentina. Hornero 18:103–111

  • Quintana F, Wilson R, Dell′Arciprete P, Shepard E, Gómez Laich A (2011) Women from Venus, men from Mars: inter-sex foraging differences in the Imperial cormorant Phalacrocorax atriceps a colonial seabird. Oikos 120:350–358

    Article  Google Scholar 

  • R Development Core Team I (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Schmidt-Nielsen K (1990) Animal physiology: adaptation and environment. Cambridge University Press, Cambridge

    Google Scholar 

  • Schreiber EA, Burger J (2002) Biology of marine birds. CRC Press LL, Florida

    Google Scholar 

  • Shepard ELC, Wilson MP, Quintana F, Gómez Laich A, Liebsch N, Albareda D, Halsey LG, Gleiss A, Morgan DT, Myers AE, Newman C, Macdonald DW (2008) Identification of animal movement patterns using tri-axial accelerometry. Endang Spec Res 10:47–60

    Article  Google Scholar 

  • Shepard ELC, Wilson RP, Quintana F, Gómez Laich A, Forman DW (2009) Pushed for time or saving fuel: fine-scale energy budgets shed light on currencies in a diving bird. Proc R Soc B 276:3149–3155

    Article  Google Scholar 

  • Shepard ELC, Wilson RP, Gómez Laich A, Quintana F (2010) Buoyed up and slowed down: sped limits for diving birds in shallow water. Aquat Biol 8:259–267

    Article  Google Scholar 

  • Stearns SC (1992) The evolution of life history. Oxford University Press, New York

    Google Scholar 

  • Svagelj W, Quintana F (2007) Sexual size dimorphism and sex determination by morphometric measurements in breeding shags (Phalacrocorax atriceps). Waterbirds 30:97–102

    Article  Google Scholar 

  • Svagelj W, Quintana F (2011) Breeding performance of the Imperial Shag (Phalacrocorax atriceps) in relation to year, laying date and nest location. Emu 111:162–165

    Google Scholar 

  • Wanless S, Harris MP, Morris JA (1992) Diving behavior and diet of the blue-eyed shag at South-Georgia. Polar Biol 12:713–719

    Article  Google Scholar 

  • Watanabe YY, Takahashi A, Sato K, Viviant M, Bost CA (2011) Poor flight performance in deep-diving cormorants. J Exp Biol 214:412–421

    Article  Google Scholar 

  • Wilson RP, Quintana F (2004) Surface pauses in relation to dive duration in imperial cormorants; how much time for a breather? J Exp Biol 207:1789–1796

    Article  Google Scholar 

  • Wilson RP, Hustler K, Ryan PG, Noeldeke C, Burger AE (1992) Diving birds in cold water: do Archimedes and Boyle determine energy costs? Am Nat 140:179–200

    Article  Google Scholar 

  • Wilson RP, Putz K, Charrassin JB, Lage J (1997) Long-term attachment of transmitting and recording devices to penguins and other seabirds. Wildlife Soc B 25:101–106

    Google Scholar 

  • Wilson RP, Steinfurth A, Ropert-Coudert Y, Kato A, Kurita M (2002) Lip-reading in remote subjects: an attempt to quantify and separate ingestion, breathing and vocalisation in free-living animals using penguins as a model. Mar Biol 140:17–27

    Google Scholar 

  • Wilson RP, White CR, Quintana F, Halsey LG, Liebsh N, Martin GR, Butler PJ (2006) Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant. J Anim Ecol 75:1081–1090

    Article  Google Scholar 

  • Wilson RP, Shepard ELC, Liebsch N (2008a) Prying into the intimate details of animal lives: use of a daily diary on animals. Endang Spec Res 4:123–137

    Article  Google Scholar 

  • Wilson RP, Vargas FH, Steinfurth A, Riordan P, Ropert-Coudert Y, Macdonald DW (2008b) What grounds some birds for life? Movement and diving in the sexual dimorphic Galápagos Cormorant. Ecol Monogr 78:633–652

    Article  Google Scholar 

  • Wilson RP, McMahon CR, Quintana F, Frere E, Scolaro A, Hays GC, Bradshaw CJA (2011a) N-dimensional animal energetic niches clarify behavioral options in a variable marine environment. J Exp Biol 214:646–656

    Article  Google Scholar 

  • Wilson RP, Quintana F, Hobson VJ (2011b) Construction of energy landscapes can clarify the movement and distribution of foraging animals. P Natl Acad Sci 279:975–980

    Google Scholar 

  • Yoda K, Naito Y, Sato K, Takahashi A, Nishikawa J, Ropert-Coudert Y, Kurita M, Le Maho Y (2001) A new technique for monitoring the behaviour of free-ranging Adelie penguins. J Exp Biol 204:685–690

    CAS  Google Scholar 

  • Yorio P, Copello S, Kuba L, Gosztonyi A, Quintana F (2010) Diet of Imperial Cormorants, Phalacrocorax atriceps, breeding at Central Patagonia, Argentina. Waterbirds 33:70–78

    Article  Google Scholar 

Download references

Acknowledgments

This research was funded by grants from the Wildlife Conservation Society, Consejo Nacional de Investigaciones Científicas y Técnicas de la República Argentina (CONICET) and Agencia de Promoción Científica y Tecnológica to F. Quintana and by a Rolex Award for Enterprise awarded to R.P. Wilson. We would like to thank the Organismo Provincial de Turismo for the permits to work in Punta León and the Centro Nacional Patagónico (CENPAT-CONICET) for institutional and logistical support. A. Gómez-Laich is supported by a Postdoctoral fellowship from the Consejo Nacional de Investigaciones Científicas y Técnicas de la República Argentina (CONICET).

Author information

Authors and Affiliations

  1. Centro Nacional Patagónico-CONICET, Boulevard Brown 2915, Puerto Madryn (U9120ACD), Chubut, Argentina

    Agustina Gómez-Laich & Flavio Quintana

  2. Biological Sciences, Institute of Environmental Sustainability, University of Wales, Swansea, SA2 8PP, UK

    Rory P. Wilson & Emily L. C. Shepard

  3. Wildlife Conservation Society, Amenabar 1595, (C1426AKC), Ciudad de Buenos Aires, Argentina

    Flavio Quintana

Authors
  1. Agustina Gómez-Laich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rory P. Wilson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Emily L. C. Shepard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Flavio Quintana
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Agustina Gómez-Laich.

Additional information

Communicated by S. Garthe.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gómez-Laich, A., Wilson, R.P., Shepard, E.L.C. et al. Energy expenditure and food consumption of foraging Imperial cormorants in Patagonia, Argentina. Mar Biol 160, 1697–1707 (2013). https://doi.org/10.1007/s00227-013-2222-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2222-8

Keywords

Search

Navigation