Skip to main content
SpringerLink
Log in

Increases in arterial blood oxygen during exercise in the lemon shark (Negaprion brevirostris)

  • Published:
Journal of comparative physiology Aims and scope Submit manuscript

Summary

Polyethylene cannulae were implanted in pre- and post-branchial blood vessels allowing nonstressful blood sampling over a variety of activity ranges in an active tropical elasmobranch, the lemon shark (Negaprion brevirostris). TheP 50 was found to be 11.8 Torr at 24°C and pH of 7.7. A Bohr shift of −0.36 was also found. BloodP o 2 and oxygen content were measured during rest, routine swimming, and exercise in unanesthetized, free swimming juveniles. Under all conditions venous oxygen levels were low with venousP o 2 of 7.1±2.7 Torr, and venous oxygen content (\(C\bar v_{O_2 } \)) of 0.56±0.4 vol%. However, a large variability was found in arterial blood measurements. ArterialP o 2 ranged from 7 to 80 Torr, while arterial oxygen content (Cao 2) varied from 1.6 vol% to 6.8 vol% among ten experimental animals. A significant increase in arterialP o 2, oxygen content, and hematocrit was noted during increased activity. Since the venous system provides little or no oxygen reserve, increased oxygen extraction from the blood (\(Ca_{O_{_2 } } - C\bar v_{O_2 } \)) appears to be met by an increase inCao 2 rather than a decrease in\(C\bar v_{O_2 } \). Mechanisms to accomplish this may include increasing hematocrit and vacular gill shunts.

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

Similar content being viewed by others

References

  • Baumgarten-Schumann D, Piiper J (1968) Gas exchange in the gills of resting unanesthetized dogfish (Scyliorhinus stellaris). Respir Physiol 5:317–325

    Google Scholar 

  • Bettex-Galland M, Hughes GM (1972) Demonstration of a contractile actomyosin like protein in the pillar cells of fish gills. Experientia 28:744

    Google Scholar 

  • Black EC, Chiu WG, Forbes FD, Hanislip A (1959) Changes in pH, carbonate, and lactate of the blood of yearling kamloops trout,Salmo gairdneri, during and following severe muscular activity. J Fish Res Board Can 16:391–402

    Google Scholar 

  • Black EC, Connor AR, Lam KC, Chiu WG (1962) Changes in glycogen, pyruvate, and lactate in rainbow trout (Salmo gairdneri) during and following muscular activity. J Fish Res Board Can 19:409–436

    Google Scholar 

  • Black EC, Manning GT, Hayashi K (1966) Changes in levels of hemoglobin, oxygen, carbon dioxide, pyruvate, and lactate in venous blood of rainbow trout (Salmo gairdneri) during and following severe muscular activity. J Fish Res Board Can 23:783–795

    Google Scholar 

  • Brett JR (1964) The respiratory metabolism and swimming performance of young sockeye salmon. J Fish Res Board Can 21:1183–1190

    Google Scholar 

  • Brett JR (1965) The relation of size to the rate of oxygen consumption and sustained swimming speeds of sockeye salmon (Oncorhynchus nerka). J Fish Res Board Can 22:1491–1501

    Google Scholar 

  • Brett JR (1972) The metabolic demand for oxygen in fish, particularly salmonids, and a comparison with other vertebrates. Respir Physiol 14:151–170

    Google Scholar 

  • Brett JR, Blackburn JM (1978) Metabolic rate and energy expenditure of the spiny dogfish,Squalus acanthias. J Fish Res Board Can 35:816–821

    Google Scholar 

  • Butler PS, Taylor EW (1971) Response of the dogfish (Scyliorhinus canicula L.) to slowly induced and rapidly induced hypoxia. Comp Biochem Physiol [A] 39:307–323

    Google Scholar 

  • Butler PJ, Taylor EW (1975) The effect of progressive hypoxia on respiration in the dogfish (Scyliorhinus canicula L.) at different seasonal temperatures. J Exp Biol 63:117–130

    Google Scholar 

  • Cameron JN (1970) The influence of environmental variables on the hematology of the pinfish (Lagodon rhomboides) and striped mullet (Mugil cephalus). Comp Biochem Physiol 32:175–192

    Google Scholar 

  • Cameron JN, Randall DJ, Davis JC (1971) Regulation of the ventilation-perfusion ratio in the gills ofDasyatis sabina andSqualus suckleyi. Comp Biochem Physiol [A] 39:509–519

    Google Scholar 

  • Cooke IRC (1980) Functional aspects of the morphology and vascular anatomy of the gills of the endeavor dogfish,Centrophorus scalpratus. (McCulloch) (Elasmobranchii: Squalidae). Zoomorphologie 94:167–183

    Google Scholar 

  • Dejours PD (1975) Principles of comparative respiratory physiology. North-Holland/American Elsevier, New York, pp 1–253

    Google Scholar 

  • Dill DB, Edwards HT, Florkin M (1932) Properties of the blood of the skate. Biol Bull 62:23–36

    Google Scholar 

  • Eddy FB (1974) Blood gases of the tench (Tinca tinca) in well aerated and oxygen-deficient waters. J Exp Biol 60:71–83

    Google Scholar 

  • Garey WF (1967) Gas exchange, cardiac output and blood pressure in free swimming carp (Cyprinus carpio). PhD dissertation University of New York, Buffalo, New York

    Google Scholar 

  • Garrick JA (1967) A broad view of theCarcharinus species, their systematics and distribution. In: Gilbert PW (eds) Sharks, skates, and rays. Johns Hopkins Press, Baltimore, pp 85–93

    Google Scholar 

  • Grigg GC (1970) Use of the first gill slits for water intake in a shark. J Exp Biol 52:569–574

    Google Scholar 

  • Grigg GC (1974) Respiratory function of blood in fishes. In: Florkin M, Scherr BT (eds) Chemical zoology, vol VIII. Academic Press, New York, pp 331–363

    Google Scholar 

  • Gruber SH (1980) Keeping sharks in captivity. J Aquaricult 1:6–14

    Google Scholar 

  • Hanson D, Johansen K (1970) The relationship of gill ventilation and perfusion in the Pacific dogfish,Squalus suckleyi. J Fish Res Board Can 27:551–564

    Google Scholar 

  • Holbert PW, Boland EJ, Olson KR (1979) The effects of epinepherine and acetylcholine on the distribution of red cells within the gills of the channel catfish (Ictalurus punctatus). J Exp Biol 79:135–146

    Google Scholar 

  • Hughes GM (1978) On the respiration ofTorpedo marmorata. J Exp Biol 73:85–105

    Google Scholar 

  • Hughes GM, Umezawa SI (1968) Oxygen consumption and gill water flow in the dogfish (Scyliorhinus canicula). J Exp Biol 49:557–564

    Google Scholar 

  • Itzawa Y, Takeda T (1978) Gas exchange in the carp gill in normoxic and hypoxic conditions. Respir Physiol 35:263–269

    Google Scholar 

  • Kiceniuk JW, Jones DR (1977) The oxygen transport system in trout (salmo gairdneri) during sustained exercise. J Exp Biol 69:247–260

    Google Scholar 

  • Kline RP, Ripps H, Dowling JE (1975) Generation of b-wave currents in the skate retina. Proc Natl Acad Sci USA 75:5727–5731

    Google Scholar 

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

    Google Scholar 

  • Lutz PL (1982) Oxygen transport in vertebrate blood: challenges. In: Taylor CR, Johansen K, Bolis L (eds) A companion to animal physiology. Cambridge University Press, Cambridge,pp 65–72

    Google Scholar 

  • Manwell C (1958) Ontogeny of hemoglobin in the skateRaja binoculata. Science 128:419

    Google Scholar 

  • Manwell C (1963) Fetal and adult hemoglobins of the spiny dogfish,Squalus suckleyi. Arch Biochem Biophys 101:504–511

    Google Scholar 

  • Olson KR, Kent B (1980) The microvasculature of the elasmobranch gill. Cell Tiss Res 209:49–63

    Google Scholar 

  • Moss SA (1972) The feeding mechanisms of sharks of the family Carcharhinidae. J Zool (Lond) 167:423–436

    Google Scholar 

  • Piiper J, Meyer M, Worth H, Willmer H (1977) Respiration and circulation during swimming activity in the dogfish,Scyliorhinus stellaris. Respir Physiol 30:221–239

    Google Scholar 

  • Piiper J, Schumann D (1967) Efficiency of O2 exchange in the gills of the dogfish,Scyliorhinus stellaris. Respir Physiol 2:135–148

    Google Scholar 

  • Randall DJ, Holeton GF, Stevens ED (1967) The exchange of O2 and CO2 across the gills of rainbow trout. J Exp Biol 46:339–348

    Google Scholar 

  • Richards BD, Fromm PO (1969) Patterns of blood flow through filaments and lamellae of isolated-perfused rainbow trout (Salmo gairdneri) gills. Comp Biochem Physiol 29:1963–1970

    Google Scholar 

  • Riggs A (1970) Properties of fish hemoglobins. In: Hoar WS. Randall DJ (eds) Fish physiology, vol IV. Academic Press, New York, pp 209–246

    Google Scholar 

  • Robin ED, Murdaugh HV, Millen JE (1965) Acid-base, fluid and electrolyte metabolism in the elasmobranch. III. Oxygen, CO2, bicarbonate, and lactate exchange across the gill. J Cell Physiol 67:93–100

    Google Scholar 

  • Short S, Taylor EW, Butler PJ (1979) The effectiveness of oxygen transfer during normoxia and hypoxia in the dogfish (Scyliorhinus canicula) before and after cardiac vagotomy. J Comp Physiol 132:289–295

    Google Scholar 

  • Smith DG, Johnson DW (1977) Oxygen exchange in a simulated trout gill secondary lamella. Am J Physiol 233:R145–161

    Google Scholar 

  • Soivio A, Oikari A (1976) Haematological effect of stress on a teleost,Esox lucias L. J Fish Biol 8:397–411

    Google Scholar 

  • Steen JB, Kruysse A (1964) The respiratory function of teleostean gills. Comp Biochem Physiol 12:127–142

    Google Scholar 

  • Stevens ED (1968) The effects of exercise on the distribution of blood to various organs in rainbow trout. Comp Biochem Physiol 25:615–625

    Google Scholar 

  • Stevens ED, Randall DJ (1967a) Change in blood pressure, heart rate, and breathing rate during moderate swimming activity in rainbow trout. J Exp Biol 46:307–315

    Google Scholar 

  • Stevens ED, Randall DJ (1967b) Changes of gas concentrations in blood and water during moderate swimming activity in rainbow trout. J Exp Biol 46:329–337

    Google Scholar 

  • Taylor EW, Short S, Butler PJ (1977) The role of the cardiac vagus in the response of the dogfish (Scyliorhinus canicula) to hypoxia. J Exp Biol 70:57–75

    Google Scholar 

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

    Google Scholar 

  • Vogel W (1978) Arteriovenous anastomoses in the afferent region of trout gill filaments (Salmo gairdneri Richardson, Teleostei). Zoomorphologie 90:205–212

    Google Scholar 

  • Vogel W, Vogel V, Pfautsch M (1976) Arterio-venous anastomoses in rainbow trout gill filaments. Cell Tiss Res 167:373–385

    Google Scholar 

  • Vogel W, Vogel V, Schlote W (1974) Ultra-structural study of arteriovenous anastomoses in gill filaments ofTilapia mosambica. Cell Tiss Res 155:491–512

    Google Scholar 

  • Yamamoto K, Itazawa Y, Kobayashi H (1980) Supply of erythrocytes into the circulating blood from the spleen of exercised fish. Comp Biochem Physiol [A] 65:5–11

    Google Scholar 

Download references

Author information

Author notes

  1. J. F. Steffensen

    Present address: Department of Zoophysiology, University of Aarhus, DK-8000, Aarhus C, Denmark

  2. A. Oikari

    Present address: Division of Physiological Zoology, Department of Zoology, University of Helsinki, Arkadiankatv 7, SF-00100, Helsinki 10, Finland

Authors and Affiliations

  1. University of Miami, Division of Biology and Living Resources, Rosenstiel School of Marine and Atmospheric Science, 4600 Rickenbacker Causeway, 33149, Miami, Florida, USA

    P. G. Bushnell, P. L. Lutz, J. F. Steffensen, A. Oikari & S. H. Gruber

Authors
  1. P. G. Bushnell
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. L. Lutz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. F. Steffensen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. A. Oikari
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. S. H. Gruber
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bushnell, P.G., Lutz, P.L., Steffensen, J.F. et al. Increases in arterial blood oxygen during exercise in the lemon shark (Negaprion brevirostris). J Comp Physiol B 147, 41–47 (1982). https://doi.org/10.1007/BF00689288

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00689288

Keywords

Search

Navigation