Skip to main content
Log in

Prey ecology and behaviour affect foraging strategies in the Great Cormorant

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

Abstract

The fine link between a particular dive pattern and a specific prey item represents a challenging task in the analysis of marine predator–prey relationships. There is growing evidence that prey type affects diving seabirds’ foraging strategies, dive shapes and underwater activity costs. This study investigates whether a generalist diver, the Great Cormorant Phalacrocorax carbo, modifies the time budget allocated to prey-capture behaviour and breathing strategies (reactive vs. anticipatory) with respect to the prey type (pelagic vs. benthic). Video recordings of 91 Great Cormorants show how the ecology and behaviour of their main prey, Mullets (Mugilidae) and Flounders Platichthys flesus, affect dive/surface durations and the diving pattern. The demersal habit and the low mobility of Flounders leads to an easy access to prey with an anticipatory strategy. Moreover, the patchy distribution of this fish species increases prey-capture rates. Conversely, Mullets exploit the whole water column and are highly mobile, and this is reflected in the need of performing two sequential dives to capture a prey, both longer and likely more expensive, with a consequent switch of strategy from reactive in the searching phase to anticipatory breathing during prey-capture events. This study provides evidence that a generalist diver may switch between different foraging strategies, and it shows how each of them may be optimal under particular ecological conditions. These constraints influence the dynamics that operate within the marine food chains and have relevant implications in managing lagoon areas, including fish ponds.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ashmole NP (1971) Seabird ecology and marine environment. In: Fraser DS, King JR (eds) Avian biology, vol I. Academic, New York, pp 221–271

    Google Scholar 

  • Baccetti N, Boldreghini P, Santolini R (1993) Le Grand Cormoran en Italie: effectif, régime alimentaire et conflits avec la pisciculture. Bull Mens Off Nat Chasse 178:22–25

    Google Scholar 

  • Baccetti N, Dall’Antonia P, Magagnoli P, Melega L, Serra L, Soldatini C, Zenatello M (2002) Risultati dei censimenti degli uccelli acquatici svernanti in Italia: distribuzione, stima e trend delle popolazioni nel 1991–2000. Biol Cons Fauna 111:1–240

    Google Scholar 

  • Baldwin J (1988) Predicting the swimming and diving behaviour of penguins from muscle biochemistry. Hydrobiologia 34:255–261

    Article  Google Scholar 

  • Bost CA, Handrich Y, Butler PJ, Fahlman A, Halsey LG, Woakes AJ, Ropert-Coudert Y (2007) Changes in dive profiles as an indicator of feeding success in king and Adélie penguins. Deep-Sea Res Pt II 54:248–255

    Article  Google Scholar 

  • Bost CA, Jaeger A, Huin W, Koubbi P, Halsey LG, Hanuise N, Handrich Y (2008) Monitoring prey availability via data loggers deployed on seabirds: advances and present limitations. In: Tsukamoto K, Kawamura T, Takeuchi T, Beard TD, Kaiser MJ (eds) Fisheries for global welfare and environment, 5th World Fisheries Congress 2008: pp 121–137

  • Carscadden JE, Wilhjalmsson H (2002) Capelin: what are they good for? ICES J Mar Sci 59:863–869

    Article  Google Scholar 

  • Carss DN (ed) (2003) Reducing the conflict between Cormorants and fisheries on a pan-European scale. REDCAFE Final Report. Report of a Concerted Action funded by the European Union. Study contract no. Q5CA-2000-31387

  • Carss DN, The Diet Assessment and Food Intake Working Group (1997) Techniques for assessing Cormorant diet and food intake: towards a consensus view. Suppl Ric Biol Selv 26:197–230

    Google Scholar 

  • Charnov EL (1976) Optimal foraging and the marginal value theorem. Theor Pop Biol 9:129–136

    Article  CAS  Google Scholar 

  • Cooper J (1986) Diving patterns of Cormorants (Phalacrocoracidae). Ibis 128:562–570

    Article  Google Scholar 

  • Cosolo M (2008) Interazioni tra avifauna ittiofaga ed attività produttive nella laguna di Grado e Marano. PhD thesis. University of Trieste, 114 pp

  • Cosolo M, Utmar P, Roppa F, Sponza S (2009) Interactions between fish-eating birds and fish ponds in the Grado and Marano lagoon: the case of the Great cormorant (Phalacrocorax carbo). Acrocephalus 29(140):17–23

    Article  Google Scholar 

  • Coyle KO, Hunt GL Jr, Decker MB, Weingartner TJ (1992) Murre foraging, epibenthic sound scattering and tidal advection over a shoal near St. George Island, Bering Sea. Mar Ecol Prog Ser 83:1–14

    Article  Google Scholar 

  • Cramp S, Simmons KLS (1977) The birds of the western paleartic: ostrich to ducks. Oxford University Press, Oxford

    Google Scholar 

  • Croxall JP, Naito Y, Kato A, Rothery P, Briggs DR (1991) Diving patterns and performance in the Antarctic blue-eyed shag Phalacrocorax atriceps. J Zool Lond 225:177–199

    Article  Google Scholar 

  • Davoren GK (2000) Variability in foraging in response to changing prey distribution in rhinoceros auklets. Mar Ecol Prog Ser 198:283–292

    Article  Google Scholar 

  • Davoren GK, Montevecchi WA, Anderson JT (2003) Search strategies of a pursuit-diving marine bird and the persistence of prey patches. Ecol Monogr 73:463–481

    Article  Google Scholar 

  • Elliott KH, Davoren GK, Gaston AJ (2008a) Time allocation by a deep-diving bird reflects prey type and energy gain. Anim Behav 75:1301–1310

    Article  Google Scholar 

  • Elliott KH, Woo K, Gaston AJ, Benvenuti S, Dall’Antonia L, Davoren GK (2008b) Seabird foraging behaviour indicates prey type. Mar Ecol Prog Ser 354:289–303

    Article  Google Scholar 

  • Elliott KH, Woo K, Benvenuti S (2009) Do activity costs determine foraging tactics for an arctic seabird? Mar Biol 156:1809–1816

    Article  Google Scholar 

  • Enstipp MR, Grémillet D, Jones DR (2007) Investigating the functional link between prey abundance and seabird predatory performance. Mar Ecol Prog Ser 331:267–279

    Article  Google Scholar 

  • Eschmeyer WN, Herald ES, Hammann H (1983) A field guide to Pacific coast fishes of North America. Houghton Mifflin Company, Boston, p 336

    Google Scholar 

  • Green JA, Halsey LG, Butler PJ (2005) To what extent is the foraging behaviour of aquatic birds constrained by their physiology? Physiol Biochem Zool 78:766–781

    Article  PubMed  Google Scholar 

  • Grémillet D, Argentin G, Schulte B, Culik BM (1998) Flexible foraging techniques in breeding Cormorants Phalacrocorax carbo and Shags Phalacrocorax aristotelis: benthic or pelagic feeding? Ibis 140:113–119

    Article  Google Scholar 

  • Grémillet D, Wilson RP, Storch S, Gary Y (1999) Three dimensional space utilization by a marine predator. Mar Ecol Prog Ser 183:263–273

    Article  Google Scholar 

  • Grémillet D, Kuntz G, Delbart F, Mellet M, Kato A, Robin JP, Chaillon PE, Gendner JP, Lorentsen SH, Le Maho Y (2004) Linking the foraging performance of a marine top predator to local prey abundance. Funct Ecol 18:793–801

    Article  Google Scholar 

  • Grémillet D, Kuntz G, Gilbert C, Woakes AJ, Gilbert C, Butler PJ, Le Maho Y (2005) Cormorants dive through the Polar night. Biol Lett 1:469–471

    Article  PubMed  Google Scholar 

  • Grémillet D, Enstipp MR, Boudiffa M, Liu H (2006) Do Cormorants injure fish without eating them? An underwater video study. Mar Biol 148:1081–1087

    Article  Google Scholar 

  • Halsey LG, White CR, Enstipp MR, Jones DR, Martin GR, Butler PJ (2007) When cormorants go fishing: the differing costs of hunting for sessile and motile prey. Biol Lett 3:574–576

    Article  PubMed  Google Scholar 

  • Houston AI, Carbone C (1992) The optimal allocation of time during the dive cycle. Behav Ecol 3:233–262

    Article  Google Scholar 

  • Jodice PGR, Collopy MW (1999) Diving and foraging patterns of Marbled murrelets (Brachyramphus marmoratus): testing predictions from optimal breathing models. Can J Zool 77:1409–1418

    Article  Google Scholar 

  • Johnsgard PA (1993) Cormorants, darters and pelicans of the world. Smithsonian Institution Press, Washington

    Google Scholar 

  • Kailola PJ, Williams MJ, Stewart PC, Reichelt RE, McNee A, Grieve C (1993) Australian fisheries resources. Bureau of Resource Sciences, Canberra 422 pp

    Google Scholar 

  • Kato A, Watanuki Y, Naito Y (1998) Benthic and pelagic foraging of two Japanese cormorants, determined by simultaneous recording of location and diving activity. J Yamashina Inst Ornithol 30:101–108

    Google Scholar 

  • Kato A, Ropert-Coudert Y, Grémillet D, Cannell B (2006) Locomotion and foraging strategy in foot-propelled and wing-propelled shallow-diving seabirds. Mar Ecol Prog Ser 308:293–301

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lea SEG, Daley C, Boddington PJC, Morison V (1996) Diving patterns in Shags and Cormorants (Phalacrocoracidae): test of an optimal breathing model. Ibis 138:391–398

    Article  Google Scholar 

  • Lescroël A, Bost CA (2005) Foraging under contrasting oceanographic conditions: the gentoo penguin at Kerguelen Archipelago. Mar Ecol Prog Ser 302:245–261

    Article  Google Scholar 

  • Litzow MA, Piatt JF, Abookire AA, Prichard AK, Robards MD (2000) Monitoring temporal and spatial variability in sand eel (Ammodytes hexapterus) abundance with pigeon guillemot (Cepphus columba) diets. ICES J Mar Sci 57:976–986

    Article  Google Scholar 

  • Marchesan M (2008) Analisi quali-quantitativa e distribuzione del pescato in Laguna di Grado e Marano. In: Benassi MC, Facchin G, Fabro C, Florit F, Ferrero E, Iacumin C, Serra L, Sponza S, Susmel P, Zanetti M (eds) Progetto ANSER. Ruolo ecologico delle zone umide per la sosta e lo svernamento degli uccelli acquatici nell’Adriatico settentrionale: linee guida per la conservazione e la gestione del patrimonio marino costiero. Relazione progettuale finale. Regione Autonoma Friuli Venezia Giulia—Direzione centrale risorse agricole, naturali e forestali, Udine, pp 184–190

  • Modin J, Pihl L (1996) Small-scale distribution of juvenile plaice and flounder in relation to predatory shrimp in a shallow Swedish bay. J Fish Biol 49(6):1070–1085

    Article  Google Scholar 

  • Montevecchi WA (1993) Birds as indicators of change in marine prey stocks. In: Furness RW, Greenwood JJD (eds) Birds as monitors of environmental change. Chapman and Hall, London, pp 217–265

    Google Scholar 

  • Mori Y (1998) The optimal patch use in divers: optimal time budget and the number of dive cycles during bout. J Theor Biol 190:187–199

    Article  Google Scholar 

  • Mori Y, Takahashi A, Mehlum F, Watanuki Y (2002) An application of optimal diving models to diving behaviour of Brünnich’s guillemots. Anim Behav 64:739–745

    Article  Google Scholar 

  • Muus BJ, Dahlström P (1974) Collins guide to the sea fishes of Britain and North-Western Europe. Collins, London, p 244

    Google Scholar 

  • Nelson Bryan J (2005) Pelicans, cormorants, and their relatives. The Pelecaniformes. Oxford University Press, Oxford, p 661

    Google Scholar 

  • Pitcher TJ, Parrish JK (1993) Functions of shoaling behaviour in teleosts. In: Pitcher TJ (ed) Behaviour of teleost fishes, 2nd edn. Chapman & Hall, London, pp 363–439

    Google Scholar 

  • Privileggi N (2003) Great cormorants (Phalacrocorax carbo sinensis) wintering in Friuli Venezia Giulia, Northern Adriatic: specific and quantitative diet composition. Vogelwelt 124:237–243

    Google Scholar 

  • Rayner MJ, Hauber ME, Clout MN, Seldon DS, Van Dijken S, Bury S, Phillips RA (2008) Foraging ecology of the Cook’s petrel Pterodroma cookii during the austral breeding season: a comparison of its two populations. Mar Ecol Prog Ser 370:271–284

    Article  Google Scholar 

  • Rheman S, Islam ML, Shah MMR, Mondal S, Alan MJ (2002) Observation on the fecundity and Gonadosomatic Index (GSI) of Grey mullet Liza parsia (Ham.). J Biol Sci 2(10):690–693. (Online)

    Article  Google Scholar 

  • Ribak G, Weihs D, Arad Z (2004) How do Cormorants counter buoyancy during submerged swimming? J Exp Biol 207:2101–2114

    Article  PubMed  Google Scholar 

  • Ropert-Coudert Y, Wilson RP (2005) Trends and perspectives in animal-attached remote sensing. Front Ecol Environ 3:437–444

    Article  Google Scholar 

  • Ropert-Coudert Y, Kato A, Bost CA, Rodary D, Sato K, Le Maho Y, Naito Y (2002) Do Adélie penguins modify their foraging behaviour in pursuit of different prey? Mar Biol 140:647–652

    Article  Google Scholar 

  • Ropert-Coudert Y, Kato A, Wilson RP, Cannell B (2006a) Foraging strategies and prey encounter rate of free-ranging Little Penguins. Mar Biol 149:139–148

    Article  Google Scholar 

  • Ropert-Coudert Y, Grémillet D, Kato A (2006b) Swim speeds of free-ranging Great cormorants Phalacrocorax carbo. Mar Biol 149:415–422

    Article  Google Scholar 

  • Rulifson RA (1977) Temperature and water velocity effects on the swimming performance of young of-the-year Striped mullet (Mugil cephalus), Spot (Leiostomus xanthurus) and Pinfish (Lagodon rhomboids). J Fish Res Board Canada 34:2316–2322

    Google Scholar 

  • Sambilay VC (1990) Interrelationships between swimming speed, caudal fin aspect ratio and body length of fishes. Fishbyte 8(3):16–20

    Google Scholar 

  • Schmid D, Grémillet D, Culik BM (1995) Energetics of underwater swimming in the Great cormorant (Phalacrocorax carbo sinensis). Mar Biol 123:875–881

    Article  Google Scholar 

  • Sokal RR, Rohlf FJ (1969) Biometry. WH Freeman and Co, San Francisco

    Google Scholar 

  • Sponza S, Cimador B, Cosolo M, Ferrero EA (2010) Diving costs and benefits during post-breeding movements of the Mediterranean shag in the North Adriatic Sea. Mar Biol 157:1203–1213

    Article  Google Scholar 

  • Strod T, Izhaki I, Arad Z, Weihs D, Katzir G (2003) Cormorants Phalacrocorax carbo swallow fish under water. Vogelwelt 124:270–276

    Google Scholar 

  • Takahashi A, Dunn MJ, Trathan PN, Sato K, Naito Y, Croxall JP (2003) Foraging strategies of chinstrap penguins at Signy Island, Antarctica: importance of benthic feeding on Antarctic krill. Mar Ecol Prog Ser 250:279–289

    Article  Google Scholar 

  • Tremblay Y, Cherel Y (2000) Benthic and pelagic dives: a new foraging behaviour in rockhopper penguins. Mar Ecol Prog Ser 204:257–267

    Article  Google Scholar 

  • Voslamber B, Platteew M, Van Eerden MR (1995) Solitary foraging in sand pits by breeding Cormorants Phalacrocorax carbo sinensis: does specialized knowledge about fishing sites and fish behaviour pay off? Ardea 83(1):199–212

    Google Scholar 

  • Walton P, Ruxton GD, Monaghan P (1998) Avian diving, respiratory physiology and the marginal value theorem. Anim Behav 56:165–174

    Article  PubMed  Google Scholar 

  • Watanuki Y, Kato A, Mori Y, Naito Y (1993) Diving performance of Adélie penguins in relation to food availability in fast sea ice areas: comparison between years. J Anim Ecol 62:634–646

    Article  Google Scholar 

  • Watanuki Y, Ishikawa K, Takahashi A, Kato A (2004) Foraging behaviour of a generalist marine top predator, Japanese cormorants (Phalacrocorax filamentosus), in years of demersal versus epipelagic prey. Mar Biol 145:427–434

    Article  Google Scholar 

  • Weimerskirch H, Gault A, Cherel Y (2005) Prey distribution and patchiness: factors in foraging success and efficiency of wandering albatrosses. Ecology 86:2611–2622

    Article  Google Scholar 

  • White CR, Day N, Butler PJ, Martin GR (2007) Vision and foraging in Cormorants: more like herons than hawks? PloSOne doi:10.1371/journal.pone.0000639

  • Wilson RP, Wilson MPT (1988) Foraging behaviour in four sympatric Cormorants. J Anim Ecol 57:943–955

    Article  Google Scholar 

  • Wilson RP, Ropert-Coudert Y, Kato A (2002) Rush and grab strategies in foraging marine endotherms: the case for haste in penguins? Anim Behav 63:85–95

    Article  Google Scholar 

  • Wilson RP, Scolaro JA, Grémillet D, Kierspel MAM, Laurenti S, Upton J, Gallelli H, Quintana F, Frere E, Müller G, Straten MT, Zimmer I (2005) How do Magellanic Penguins cope with variability in their access to prey? Ecol Monogr 75:379–401

    Article  Google Scholar 

  • Wilson RP, White CR, Quintana F, Halsey LG, Liebsch 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  PubMed  Google Scholar 

  • Zwanette J (2001) Transport and retention of Flounder larvae (Platichthys flesus) in the Dollard nursery (Ems estuary). J Sea Res 45:153–171

    Article  Google Scholar 

Download references

Acknowledgments

We thank P. Utmar for extensive help in the field. F. Roppa, N. Ventolini and N. Privileggi helped with data collection. M. Tofful and C. Trani contributed to Great Cormorant population monthly surveys. We thank also the staff of the ‘Office for Studies on Wild Fauna’ of Friuli Venezia Giulia Region and the personnel of Valle Noghera fishing ‘valli’ and Valle Cavanata Natural Reserve for data and support. PhD scholarship to M. Cosolo was partially granted by the European Community Initiative INTERREG IIIB ‘CADSES’ Project “Management and sustainable development of protected transitional waters”. Finally, we would like to thank the anonymous referees and the Associate Editor for valuable criticism.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mauro Cosolo.

Additional information

Communicated by M. E. Hauber.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cosolo, M., Ferrero, E.A. & Sponza, S. Prey ecology and behaviour affect foraging strategies in the Great Cormorant. Mar Biol 157, 2533–2544 (2010). https://doi.org/10.1007/s00227-010-1517-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-010-1517-2

Keywords

Navigation