Skip to main content
Log in

Crossing the frontier: vertical transit rates of deep diving cormorants reveal depth zone of neutral buoyancy

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Knowing the depth zone of neutral buoyancy of divers is important because buoyancy can determine how animals manage their energy budget. In this study, we estimate the depth zone of neutral buoyancy of free-ranging cormorants for the first time, using time-depth recorders. We discovered that vertical ascent rates of 12 Crozet and 15 Kerguelen diving blue-eyed shags (respectively Phalacrocorax melanogenis and P. verrucosus) slowed down considerably at the 50–60 m depth zone. We suggest this was due to birds trying to reach the surface from that point upwards using reduced locomotor activity because the force of buoyancy becomes greater than the force of gravity at that depth. The results show a shift of this depth zone in relation to maximum targeted dive depth, suggesting cormorants may control buoyancy through respiratory air volume adjustment. Interestingly, 60 m is close to the maximum depth zone reached by these two species during dives lasting 4 min, their estimated behavioural aerobic dive limit. This suggests that the decision to swim deeper has a direct consequence on the energy budget, with time spent recovering at the surface (time thus lost to foraging) strongly increasing relative to the preceding time of submergence. Resources found in deeper waters must be of sufficient quantity or quality to justify crossing the frontier of physical neutral buoyancy.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alexander RM (1990) Size, speed and buoyancy adaptations in aquatic animals. Am Zool 30:189–196

    Article  Google Scholar 

  • Biuw M, McConnell B, Bradshaw CJA, Burton H, Fedak M (2003) Blubber and buoyancy: monitoring the body condition of free-ranging seals using simple dive characteristics. J Exp Biol 206:3405–3423

    Article  Google Scholar 

  • Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77:837–899

    Article  CAS  Google Scholar 

  • Chastel O, Weimerskirch H, Jouventin P (1995) Body condition and seabird reproductive performance: a study of three petrel species. Ecology 76:2240–2246

    Article  Google Scholar 

  • Cook TR, Cherel Y, Bost C-A, Tremblay Y (2007) Chick-rearing Crozet shags (Phalacrocorax melanogenis) display sex-specific foraging behaviour. Antarct Sci 19:55–63

    Google Scholar 

  • Crocker DE, Le Boeuf BJ, Costa DP (1997) Drift diving in female northern elephant seals: implications for food processing. Can J Zool 75:27–39

    Article  Google Scholar 

  • Eckert R, Randall D, Burggren W, French K (1999) Animal physiology: mechanisms and adaptations. De Boeck, Paris

    Google Scholar 

  • Elliot KH, Davoren GK, Gaston AJ (2007) The influence of buoyancy and drag on the dive behaviour of an Arctic seabird, the thick-billed murre. Can J Zool 85:352–361

    Article  Google Scholar 

  • Halsey LG, Butler PJ, Blackburn TM (2006) A phylogenetic analysis of the allometry of diving. Am Nat 167:276–287

    Article  Google Scholar 

  • Hays GC, Metcalfe JD, Walne AW (2004) The implications of lung regulated buoyancy control for dive depth and duration. Ecology 85:1137–1145

    Article  Google Scholar 

  • Hochscheid S, Bentivegna F, Speakman JR (2003) The dual function of the lung in chelonian sea turtles: buoyancy control and oxygen storage. J Exp Mar Biol Ecol 297:123–140

    Article  Google Scholar 

  • Hustler K (1992) Buoyancy and its constraints on the underwater foraging behaviour of reed cormorants Phalacrocorax africanus and darters Anhinga melanogaster. Ibis 134:229–236

    Article  Google Scholar 

  • Grémillet D, Chauvin C, Wilson RP, Le Maho Y, Wanless S (2005) Unusual feather structure allows partial plumage wettability in diving great cormorants Phalacrocorax carbo. J Avian Biol 36:57–63

    Article  Google Scholar 

  • Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314

    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). C R Acad Sci Paris 322:557–562

    Article  CAS  Google Scholar 

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

    Article  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 

  • Kooyman GL (2004) Genesis and evolution of bio-logging devices: 1963–2002. Mem Natl Inst Polar Res 58:15–22

    Google Scholar 

  • Kooyman GL, Hammond DD, Schroeder JP (1970) Bronchograms and tracheograms of seals under pressure. Science 169:82–84

    Article  CAS  Google Scholar 

  • Lovvorn JR, Croll DA, Liggins GA (1999) Mechanical versus physiological determinants of swimming speeds in diving Brünich’s guillemots. J Exp Biol 202:1741–1752

    CAS  PubMed  Google Scholar 

  • Lovvorn JR, Watanuki Y, Kato A, Naito Y, Liggins GA (2004) Stroke patterns and regulation of swim speed and energy cost in free-ranging Brünnich’s guillemots. J Exp Biol 207:4679–4695

    Article  Google Scholar 

  • Meister W (2005) Histological structure of the long bones of penguins. Anat Rec 143:377–387

    Article  Google Scholar 

  • Miller PJO, Johnson MP, Tyack PL, Terray EA (2004) Swimming gaits, passive drag and buoyancy of diving sperm whales Physeter macrocephalus. J Exp Biol 207:1953–1967

    Article  Google Scholar 

  • Minamikawa S, Naito Y, Sato K, Matsuzawa, Bando T, Sakamoto W (2000) Maintenance of neutral buoyancy by depth selection in the loggerhead turtle Caretta caretta. J Exp Biol 203:2967–2975

    CAS  PubMed  Google Scholar 

  • Orta J (1992) Family Phalacrocoracidae (Cormorants). In: Del Hoyo J, et al (ed) Handbook of the birds of the world, vol 1. Lynx Edicions, Barcelona, pp 326–353

    Google Scholar 

  • Quintana F, Wilson RP, Yoria P (2007) Dive depth and plumage air in wettable birds: the extraordinary case of the imperial cormorant. Mar Ecol Prog Ser 334:299–310

    Article  Google Scholar 

  • Ropert-Coudert Y, Grémillet D, Kato A (2005) Diving angles of great cormorants. Polar Biosci 18:54–59

    Google Scholar 

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

    Article  Google Scholar 

  • Ribak G, Weihs D, Arad Z (2005) Submerged swimming of the great cormorant Phalacrocorax carbo sinensis is a variant of the burst-and-glide gait. J Exp Biol 208:3835–3849

    Article  Google Scholar 

  • Sato K, Naito Y, Kato A, Niizuma Y, Watanuki Y, Charrassin JB, Bost C-A, Handrich Y, Le Maho Y (2002) Buoyancy and maximal diving depth in penguins: do they control inhaling air volume? J Exp Biol 205:1189–1197

    PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Schmidt-Nielsen K (1983) Animal physiology. Cambridge University Press, Cambridge

    Google Scholar 

  • Schreer JF, Kovacs KM (1997) Allometry of diving capacity in air-breathing vertebrates. Can J Zool 75:339–358

    Article  Google Scholar 

  • Skrovan RC, Williams TM, Berry PS, Moore PW, Davis RW (1999) The diving physiology of bottlenose dolphins (Tursiops truncatus) II. Biomechanics and changes in buoyancy at depth. J Exp Biol 202:2749–2761

    CAS  PubMed  Google Scholar 

  • Tremblay Y, Cook TR, Cherel Y (2005) Time budget and diving behaviour of chick-rearing Crozet shags. Can J Zool 83:971–982

    Article  Google Scholar 

  • Watanuki Y, Niizuma Y, Gabrielsen GW, Sato K, Naito Y (2003) Stroke and glide of wing-propelled divers: deep diving seabirds adjust surge frequency to buoyancy change with depth. Proc R Soc Lond B 270:483–488

    Article  Google Scholar 

  • Watanuki Y, Takahashi A, Daunt F, Wanless S, Harris M, Sato K, Naito Y (2005) Regulation of stroke and glide in a foot-propelled avian diver. J Exp Biol 208:2207–2216

    Article  Google Scholar 

  • Webb PM, Crocker DE, Blackwell SB, Costa DP, Le Boeuf BJ (1998) Effects of buoyancy on the diving behaviour of northern elephant seals. J Exp Biol 201:2349–2358

    CAS  PubMed  Google Scholar 

  • Williams TM, Davis RW, Fuiman LA, Francis J, Le Boeuf BJ, Horning M, Calambokidis J, Croll DA (2000) Sink or swim: strategies for cost-efficient diving by marine mammals. Science 288:133–136

    Article  CAS  Google Scholar 

  • Wilson RP (2006) Fishing made easy: tips and tricks on decisions for optimal foraging in Magellanic penguins, Spheniscus magellanicus. Acta Zool Sin 52(Suppl):514–523

    Google Scholar 

  • Wilson RP, Zimmer I (2004) Inspiration by Magellanic Penguins: reduced swimming effort when under pressure. Mar Ecol Prog Ser 278:303–307

    Article  Google Scholar 

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

    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  Google Scholar 

Download references

Acknowledgments

We wish to thank Yoshihisa Mori for a most interesting discussion on optimal output strategy in diving animals and Pierre Legagneux for a debate on the use of statistics in ecology. Thank’s also to François Brischoux for most valuable critiques of an earlier version of the manuscript, and to anonymous reviewers for their constructive recommendations during the revision process. Special thanks go to Jon Cook for his advice on English usage. Animals in this study were cared for in accordance with the guidelines of the ethics committee of the French Polar Institute (Institut Paul Emile Victor – IPEV). This work was supported financially and logistically by the IPEV (Program 109 and 394) and the Terres Australes et Antarctiques Françaises (TAAF).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Timothée Romuald Cook.

Additional information

Communicated by M.I. Taylor.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cook, T.R., Bailleul, F., Lescroël, A. et al. Crossing the frontier: vertical transit rates of deep diving cormorants reveal depth zone of neutral buoyancy. Mar Biol 154, 383–391 (2008). https://doi.org/10.1007/s00227-008-0939-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-008-0939-6

Keywords

Navigation