Skip to main content
SpringerLink
Log in

Blood O2 affinity of a large polar elasmobranch, the Greenland shark Somniosus microcephalus

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

Abstract

The Greenland shark (Somniosus microcephalus. Bloch & Schneider 1801) is a polar elasmobranch that is hypothesised to possess a unique metabolic physiology due to its extreme large size, the cold waters it inhabits and its slow swimming lifestyle. Our results therefore provide the first insight into the metabolic physiology of this unique shark, with a focus on blood O2 affinity. An evaluation of blood O2 affinity at 2 °C using tonometry revealed a P 50 of 11.7 mmHg at a PCO2 of 2.25 mmHg and a Bohr effect (binding sensitivity of blood to pH, ϕ = Δlog P 50/ΔpH) of −0.26. A comparative evaluation of blood O2 affinity across elasmobranch fishes suggests that S. microcephalus has a high blood O2 affinity (i.e., low P 50) and a small Bohr effect but these are common traits in sluggish elasmobranch fishes, with little evidence for any relationship of blood O2 affinity to the low metabolic rates, low environmental temperatures, or large body mass of S. microcephalus. After gathering this physiology data, a subsidiary aim attempted to understand whether a warming scenario would impose a negative effect on blood O2 binding. Incubating blood to a slightly elevated temperature of 7 °C resulted in a small but significant reduction of blood O2 affinity, but no significant change in the Bohr effect. The Hill’s cooperativity coefficient (n H) was also small (1.6–2.2) and unaffected by either PCO2 or temperature. The moderate sensitivity of Greenland shark blood O2 affinity to warming potentially implies little vulnerability of functional O2 supply to the temperature changes associated with the regular vertical movements of this species or warming of polar seas resulting from directional climate change.

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

Similar content being viewed by others

References

  • Butler PJ, Metcalfe JD (1988) Cardiovascular and respiratory systems. In: Shuttleworth TJ (ed) Physiology of elasmobranch fishes. Springer, Berlin, pp 1–47

    Google Scholar 

  • Fago A, Wells RMG, Weber RE (1997) Temperature-dependent enthalpy of oxygenation in Antarctic fish hemoglobins. Comp Biochem Physiol 118(A):319–326

    Article  Google Scholar 

  • Feller G, Poncin A, Aittaleb M, Schyns R, Gerday C (1994) The blood proteins of the Antarctic icefish Channichthys rhinoceratus: biological significance and purification of the 2 main components. Comp Biochem Physiol 109B:89–97

    CAS  Google Scholar 

  • Fisk AT, Lydersen C, Kovacs KM (2012) Archival pop-off tag tracking of Greenland sharks Somniosus microcephalus in the High Arctic waters of Svalbard, Norway. Mar Ecol-Prog Ser 468:255–265

    Article  Google Scholar 

  • Gallagher AJ, Frick LH, Bushnell PG, Brill RW, Mandelman JW (2010) Blood gas, oxygen saturation, pH, and lactate values in elasmobranch blood measured with a commercially available portable clinical analyzer and standard laboratory instruments. J Aquat Anim Health 22:229–234

    Article  PubMed  Google Scholar 

  • Herbert NA, Skov PV, Wells RMG, Steffensen JF (2006) Whole blood-oxygen binding properties of four cold-temperate marine fishes: blood-affinity is independent of pH-dependent binding, routine swimming performance and environmental hypoxia. Physiol Biochem Zool 79:909–918

    Article  CAS  PubMed  Google Scholar 

  • Hopkins TE, Cech JJ (1995) Temperature effects on blood-oxygen equilibria in relation to movements of the bat ray, Myliobatis californica in Tomales Bay, California. Mar Behav Physiol 24:227–235

    Article  Google Scholar 

  • Howell BJ, Baumgard FW, Bondi K, Rahn H (1970) Acid-base balance in cold-blooded vertebrates as a function of body temperature. Am J Physiol 218:600–606

    CAS  PubMed  Google Scholar 

  • Hughes GM, Wood SC (1974) Respiratory properties of the blood of the thornback ray. Experientia 30:167–168

    Article  Google Scholar 

  • Leclerc LM, Lydersen C, Haug T, Glover KA, Fisk AT, Kovacs KM (2011) Greenland sharks (Somniosus microcephalus) scavenge offal from minke (Balaenoptera acutorostrata) whaling operations in Svalbard (Norway). Polar Res 30:7342

    Article  Google Scholar 

  • Leclerc LM, Lydersen C, Haug T, Bachmann L, Fisk AT, Kovacs KM (2012) A missing piece in the Arctic food web puzzle? Stomach contents of Greenland sharks sampled in Svalbard, Norway. Polar Biol 35:1197–1208

    Article  Google Scholar 

  • Lenfant C, Johansen K (1966) Respiratory function in elasmobranch Squalus suckleyi G. Respir Physiol 1:13–29

    Article  CAS  PubMed  Google Scholar 

  • Macdonald JA, Montgomery JC, Wells RMG (1987) Comparative physiology of Antarctic fishes. Adv Mar Biol 24:321–388

    Article  Google Scholar 

  • MacNeil M, McMeans B, Hussey N, Vecsei P, Svavarsson J, Kovacs K, Lydersen C, Treble M, Skomal G, Ramsey M, Fisk A (2012) Biology of the Greenland shark Somniosus microcephalus. J Fish Biol 80:991–1018

    Article  CAS  PubMed  Google Scholar 

  • Mandelman JW, Skomal GB (2009) Differential sensitivity to capture stress assessed by blood acid-base status in five carcharhinid sharks. J Comp Physiol B 179:267–277

    Article  PubMed  Google Scholar 

  • McMeans BC, Arts MT, Lydersen C, Kovacs KM, Hop H, Falk-Petersen S, Fisk AT (2013) The role of Greenland sharks (Somniosus microcephalus) in an Arctic ecosystem: assessed via stable isotopes and fatty acids. Mar Biol 160:1223–1238

    Article  Google Scholar 

  • Morrison PR, Gilmour KM, Brauner CJ (2016) Oxygen and carbon dioxide transport in elasmobranchs. In: Shadwick RE, Farrell AP, Brauner CJ (eds) Fish Physiology, vol 34B. Physiology of elasmobranch fishes—internal processes. Elsevier, London, pp 127–217

    Google Scholar 

  • Nielsen J, Hedeholm RB, Simon M, Steffensen JF (2014) Distribution and feeding ecology of the Greenland shark (Somniosus microcephalus) in Greenland waters. Polar Biol 37:37–46

    Article  Google Scholar 

  • Nielsen J, Hedeholm RB, Heinemeier J, Bushnell PG, Christiansen JS, Olsen J, Bronk RC, Brill RW, Simon M, Steffensen KF, Steffensen JF (2016) Eye lens radiocarbon reveals centuries of longevity in Greenland shark (Somniosus microcephalus). Science 353:702–704

    Article  CAS  PubMed  Google Scholar 

  • Pleschka K, Albers C, Spaich P (1970) Interaction between CO2 transport and O2 transport in blood of dogfish Scyliorhinus canicula. Respir Physiol 9:118–125

    Article  CAS  PubMed  Google Scholar 

  • Prothero JW (2016) The design of mammals: a scaling approach. Cambridge University Press, Cambridge

    Google Scholar 

  • Samaja M, Melotti D, Rovida E, Rossibernardi L (1983) Effect of temperature on the P 50 value for human blood. Clin Chem 29:110–114

    CAS  PubMed  Google Scholar 

  • Schmidt-Nielsen K (1984) Scaling. Why is animal size so important?. Cambridge University Press, London

    Book  Google Scholar 

  • Screen JA, Simmonds I (2010) The central role of diminishing sea ice in recent Arctic temperature amplification. Nature 464:1334–1337

    Article  CAS  PubMed  Google Scholar 

  • Sherman K, Belkin IM, Friedland KD, O’Reilly J, Hyde K (2009) Accelerated warming and emergent trends in fisheries biomass yields of the world’s large marine ecosystems. Ambio 38:215–224

    Article  PubMed  Google Scholar 

  • Skomal GB, Benz GW (2004) Ultrasonic tracking of Greenland sharks, Somniosus microcephalus, under Arctic ice. Mar Biol 145:489–498

    Article  Google Scholar 

  • Stokesbury MJW, Harvey-Clark C, Gallant J, Block BA, Myers RA (2005) Movement and environmental preferences of Greenland sharks (Somniosus microcephalus) electronically tagged in the St. Lawrence Estuary, Canada. Mar Biol 148:159–165

    Article  Google Scholar 

  • Tetens V, Wells RMG (1984) Oxygen binding properties of blood and hemoglobin solutions in the carpet shark (Cephaloscyllium isabella)—roles of ATP and urea. Comp Biochem Physiol 79A:165–168

    Article  CAS  Google Scholar 

  • Tetens V, Wells RMG, DeVries AL (1984) Antarctic fish blood respiratory properties and the effects of thermal acclimation. J Exp Biol 109:265–279

    CAS  Google Scholar 

  • Tucker VA (1967) Method for oxygen content and dissociation curves on microlitre blood samples. J Appl Physiol 23:410–414

    CAS  PubMed  Google Scholar 

  • Watanabe YY, Lydersen C, Fisk AT, Kovacs KM (2012) The slowest fish: swim speed and tail-beat frequency of Greenland sharks. J Exp Mar Biol Ecol 426:5–11

    Article  Google Scholar 

  • Wells RMG (1999) Haemoglobin function in aquatic animals: molecular adaptations to environmental challenge. Mar Freshwater Res 50:933–939

    Article  CAS  Google Scholar 

  • Wells RMG (2005) Blood-gas transport and hemoglobin function in polar fishes: does low temperature explain physiological characters? In: Farrell AP, Steffensen JF (eds) The physiology of polar fishes. Academic Press, London, pp 1–408

    Google Scholar 

  • Wells RMG, Davie PS (1985) Oxygen binding by the blood and hematological effects of capture stress in two big gamefish—Mako Shark and Striped Marlin. Comp Biochem Physiol 81A:643–646

    Article  CAS  Google Scholar 

  • Wells RMG, Weber RE (1983) Oxygenational properties and phosphorylated metabolic intermediates in blood and erythrocytes of the dogfish, Squalus acanthias. J Exp Biol 103:95–108

    CAS  PubMed  Google Scholar 

  • Wells RMG, Baldwin J, Ryder JM (1992) Respiratory function and nucleotide composition of erythrocytes from tropical elasmobranchs. Comp Biochem Physiol 103A:157–162

    Article  CAS  Google Scholar 

  • Wells RMG, Baldwin J, Seymour RS, Christian KA, Farrell AP (2007) Air breathing minimizes post-exercise lactate load in the tropical Pacific tarpon, Megalops cyprinoides Broussonet 1782, but oxygen debt is repaid by aquatic breathing. J Fish Biol 71:1649–1661

    Article  Google Scholar 

  • Wood CM, Perry SF, Walsh PJ, Thomas S (1994) HCO3 − dehydration by the blood of an elasmobranch in the absence of a Haldane effect. Resp Physiol 98:319–337

    Article  CAS  Google Scholar 

  • Wright PA, Wood CM (2016) Regulation of ions, acid–base, and nitrogenous wastes in elasmobranchs. In: Shadwick RE, Farrell AP, Brauner CJ (eds) Fish physiology, vol 34B. Physiology of elasmobranch fishes—internal processes. Academic Press, San Diego, pp 280–347

    Google Scholar 

Download references

Acknowledgements

Considerable gratitude and appreciation are extended to the following: the crew of RV Dana for the skilled logistical support and cooperation provided across the whole 10-day research period. Financial support from the Danish Center for Marine Research, the Carlsberg Foundation, Save Our Seas Foundation (Grant No. P219), and KVUG (Commission for Scientific Research in Greenland). Mention of trade names or commercial companies is for identification purposes only and does not imply endorsement by the National Marine Fisheries Service, NOAA. The views expressed are those of the authors and do not necessarily reflect the views of NOAA or any of its sub-agencies.

Author information

Authors and Affiliations

  1. Leigh Marine Laboratory, Institute of Marine Science, The University of Auckland, Warkworth, 0941, New Zealand

    N. A. Herbert

  2. National Institute of Aquatic Resources, Technical University of Denmark, North Sea Science Park, 9850, Hirtshals, Denmark

    P. V. Skov

  3. Marine Biological Section, University of Copenhagen, Strandpromenaden 5, 3000, Helsingør, Denmark

    B. Tirsgaard & J. F. Steffensen

  4. Department of Biological Sciences, Indiana University South Bend, 1700 Mishawaka Avenue, South Bend, IN, USA

    P. G. Bushnell

  5. James J. Howard Marine Sciences Laboratory, Northeast Fisheries Science Center, National Marine Fisheries Service, NOAA, Highlands, NJ, USA

    R. W. Brill

  6. Department Veterinarian, Dalhousie University, Halifax, NS, B3H4R2, Canada

    C. Harvey Clark

Authors
  1. N. A. Herbert
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. V. Skov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. B. Tirsgaard
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. P. G. Bushnell
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. W. Brill
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. C. Harvey Clark
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. J. F. Steffensen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N. A. Herbert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Herbert, N.A., Skov, P.V., Tirsgaard, B. et al. Blood O2 affinity of a large polar elasmobranch, the Greenland shark Somniosus microcephalus . Polar Biol 40, 2297–2305 (2017). https://doi.org/10.1007/s00300-017-2142-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-017-2142-z

Keywords

Search

Navigation