Skip to main content

Oxygen delivery to the fish eye: blood flow in the pseudobranchial artery of rainbow trout (Oncorhynchus mykiss)

Abstract

Similar to gas secretion into the swimbladder, some teleosts also exhibit ocular gas secretion to supply their thick and avascular retina with oxygen. The process in the eye, however, is complicated by the fact that the retina is supplied with arterial blood only indirectly through the pseudobranch, a reduced gill arch of still unknown function. Approaches for closer analysis of the physiological implications of this serial blood supply arrangement and the associated process of O2 release include complete unilateral vascular isolation of eye and/or pseudobranch while maintaining normal blood flow characteristics for undisturbed operation of the counter-current rete mirabile.

Blood flow velocity in the afferent pseudobranchial artery (aPA; essentially equal to ophthalmic artery flow) of rainbow trout was measured by application of ultrasonic Doppler techniques. Accurate determination of flow rate in the untouched vessel was facilitated by mounting the Doppler crystal with a custom-made holder on the bone of the jaw and raw signal analysis by Fast Fourier Transformation for improved signal/noise ratio. Normal unilateral aPA blood flow was 746 μl min−1 kg−1 body weight, (∼1.6% of cardiac output), the tissue-weight-specific blood flow was 3.6 ml min−1 g−1 for pseudobranch and 2.3 ml min−1 g−1 for the retina. Only about 28% of the oxygen potentially available with maximal activation of the Root effect is actually consumed in pseudobranch and retina. This generous supply of blood and the implicit safety margin may serve minimization of pH disturbances of retinal tissues, but may also come suitable during unilateral occlusion of supplying arteries for continued oxygen supply to the retinae. During contralateral occlusion, flow through the ipsilateral aPA increased to 136%. According to the normally low O2 extraction, a minimal flow of 36% through bilateral anastomosis and contralateral ophthalmic artery may maintain complete contralateral oxygen supply.

This is a preview of subscription content, access via your institution.

Abbreviations

aPA:

afferent pseudobranchial artery

DA:

dorsal aorta

FFT:

Fast Fourier Transformation

[Hb]:

haemoglobin concentration

P O 2 :

oxygen partial pressure.

References

  • D.A Baeyens J.R Hoffert P.O Fromm (1973) ArticleTitleA comparative study of oxygen toxicity in the retina, brain and liver of the teleost, amphibian and mammal Comp. Biochem. Physiol. A 45 IssueID4 925–932 Occurrence Handle10.1016/0300-9629(73)90328-9 Occurrence Handle1:CAS:528:DyaE3sXkvVyjs7Y%3D Occurrence Handle4146108

    Article  CAS  PubMed  Google Scholar 

  • C.M Ballintijn D.D Beatty R.L Saunders (1977) ArticleTitleEffects of pseudobranchectomy on visual pigment density and ocular P O 2 in Atlantic salmon, Salmo salar J. Fish. Res. Board Can. 34 2185–2192

    Google Scholar 

  • M Barron B Tarr W Hayton (1987) ArticleTitleTemperature-dependence of cardiac output and regional blood flow in rainbow trout, Salmo gairdneri Richardson J. Fish Biol. 31 IssueID6 735–744

    Google Scholar 

  • Berenbrink, M. 1995. Die Kontrolle des intrazellulären pH in den Erythrozyten von Knochenfischen. PhD thesis, Heinrich-Heine-Universität Düsseldorf, Germany

  • N.J Bernier S.F Perry (1999) ArticleTitleCardiovascular effects of angiotensin-II-mediated adrenaline release in rainbow trout (Oncorhynchus mykiss) J. exp. Biol. 202 55–66 Occurrence Handle1:CAS:528:DyaK1MXht1yis7c%3D Occurrence Handle9841895

    CAS  PubMed  Google Scholar 

  • C.R Bridges M Berenbrink R Müller W Waser (1998) ArticleTitlePhysiology and biochemistry of the pseudobranch: an unanswered question? Comp. Biochem. Physiol. A 119 IssueID1 67–77 Occurrence Handle1:STN:280:DC%2BD3M3gsFOmuw%3D%3D

    CAS  Google Scholar 

  • T Brittain (1987) ArticleTitleThe root effect Comp. Biochem. Physiol. B 86 473–481 Occurrence Handle10.1016/0305-0491(87)90434-2 Occurrence Handle1:STN:280:BiiB2crjsVM%3D Occurrence Handle3297477

    Article  CAS  PubMed  Google Scholar 

  • S.J Cringle D-Y Yu V.A Alder E-N Su P.K Yu (1996) ArticleTitleOxygen consumption in the avascular guinea pig retina Amer. J. Physiol. 40 IssueID3 Pt 2 H1162–H1165

    Google Scholar 

  • S.J Cringle D-Y Yu P.K Yu E-N Su (2002) ArticleTitleIntraretinal oxygen consumption in the rat in vivo Invest. Ophthalmol. Vis. Sci. 43 IssueID6 1922–1927 Occurrence Handle12037000

    PubMed  Google Scholar 

  • P.R Desforges S.S Harman K.M Gilmour S.F Perry (2002) ArticleTitleSensitivity of CO2 excretion to blood flow changes in trout is determined by carbonic anhydrase availability Am. J. Physiol. (Regul. Integr. Comp. Physiol.) 282 R501–R508 Occurrence Handle1:CAS:528:DC%2BD38XhtFCqu7o%3D

    CAS  Google Scholar 

  • M.B Fairbanks J.R Hoffert P.O Fromm (1969) ArticleTitleThe dependence of the oxygen-concentrating mechanism of the teleost eye (Salmo gairdneri) on the enzyme carbonic anhydrase J. Gen. Physiol. 54 203–211 Occurrence Handle10.1085/jgp.54.2.203 Occurrence Handle1:CAS:528:DyaF1MXlt1SqsLY%3D Occurrence Handle4978732

    Article  CAS  PubMed  Google Scholar 

  • M.B Fairbanks J.R Hoffert P.O Fromm (1974) ArticleTitleShort circuiting of the ocular oxygen concentrating mechanism in the teleost Salmo gairdneri using carbonic anhydrase inhibitors J. Gen. Physiol. 64 263–273 Occurrence Handle10.1085/jgp.64.3.263 Occurrence Handle1:CAS:528:DyaE2cXls1Kksbk%3D Occurrence Handle4415760

    Article  CAS  PubMed  Google Scholar 

  • P Gallaugher A.P Farrell W Hoar D.J Randall (1998) Hematocrit and blood oxygen-carrying capacity S.F Perry B.L Tufts (Eds) Fish Physiology Academic Press New York, London 185–227

    Google Scholar 

  • Heisler, N. 2004. Frontiers in comparative respiratory physiology. I. Adaptations in respiratory gas transport. Respir. Physiol. Neurobiol. in press

  • T.M Hoagland L Weaver SuffixJr. J.M Conlon Y Wang K.R Olson (2000) ArticleTitleEffects of endothelin-1 and homologous trout endothelin on cardiovascular function in rainbow trout Am. J. Physiol. (Regul. Integr. Comp. Physiol.) 278 R460–R468 Occurrence Handle1:CAS:528:DC%2BD3cXhsVOhs7k%3D

    CAS  Google Scholar 

  • G.F Holeton P Neumann N Heisler (1983) ArticleTitleBranchial ion exchange and acid–base regulation after strenuous exercise in rainbow trout (Salmo gairdneri) Resp. Physiol. 51 303–318 Occurrence Handle10.1016/0034-5687(83)90025-7 Occurrence Handle1:CAS:528:DyaL3sXhvFGgurc%3D

    Article  CAS  Google Scholar 

  • J Kanwisher A Ebeling (1957) ArticleTitleComposition of swim-bladder gas in bathypelagic fishes Deep-sea Res. 4 211–217 Occurrence Handle10.1016/0146-6313(56)90051-X Occurrence Handle1:CAS:528:DyaG1MXktFejsw%3D%3D

    Article  CAS  Google Scholar 

  • H Kobayashi B Pelster P Scheid (1989) ArticleTitleSolute back-diffusion raises the gas concentrating efficiency in counter-current flow Resp. Physiol. 78 59–71 Occurrence Handle10.1016/0034-5687(89)90142-4 Occurrence Handle1:STN:280:By%2BD2cfitVU%3D

    Article  CAS  Google Scholar 

  • H Kobayashi B Pelster P Scheid (1990) ArticleTitleCO2 back-diffusion in the rete aids O2 secretion in the swimbladder of the eel Resp. Physiol. 79 231–242 Occurrence Handle10.1016/0034-5687(90)90129-M Occurrence Handle1:STN:280:By%2BB1cfit1w%3D

    Article  CAS  Google Scholar 

  • W Kuhn A Ramel H Kuhn E Marti (1963) ArticleTitleThe filling mechanism of the swimbladder. Generation of high gas pressures through hairpin countercurrent multiplication Experientia 19 IssueID10 497–552 Occurrence Handle1:STN:280:CCuD2M7nt1E%3D Occurrence Handle14094048

    CAS  PubMed  Google Scholar 

  • P Laurent S Dunel-Erb (1984) The pseudobranch. Morphology and function W.S Hoar D.J Randall (Eds) Fish Physiology Academic Press New York, London 285–323

    Google Scholar 

  • J Maetz (1956) ArticleTitleLe rôle biologique de l′anhydrase carbonique chez quelques téléostéens Bull. Biol. France, Belgique (Paris) Supplement 40 1–129

    Google Scholar 

  • J.E McKendry S.F Perry (2001) ArticleTitleCardiovascular effects of hypercarbia in rainbow trout (Oncorhynchus mykiss): a role for externally oriented chemoreceptors J. exp. Biol. 204 115–125 Occurrence Handle1:STN:280:DC%2BD3M7hvFGnsg%3D%3D Occurrence Handle11104715

    CAS  PubMed  Google Scholar 

  • Müller, J. 1839. Vergleichende Anatomie der Myxinoiden. III. Über das Gefäßsystem. Abh. Kgl. Dt. Akad. Wiss. Berlin 175–303

  • Müller, R. 1995. Untersuchungen zur Funktion der Pseudobranchie bei Teleosteern. Masters thesis, Heinrich-Heine-Universität Düsseldorf, Germany

  • P Neumann G.F Holeton N Heisler (1983) ArticleTitleCardiac output and regional blood flow in gills and muscles after exhaustive exercise in rainbow trout (Salmo gairdneri) J. exp. Biol. 105 1–14

    Google Scholar 

  • K.R Olson (1996) ArticleTitleSecondary circulation in fish: anatomical organization and physiological significance J. Exp. Zool. 275 172–185 Occurrence Handle10.1002/(SICI)1097-010X(19960601/15)275:2/3<172::AID-JEZ9>3.0.CO;2-A

    Article  Google Scholar 

  • K.R Olson D.J Conklin L Weaver SuffixJr. D.W Duff C.A Herman X Wang J.M Conlon (1997) ArticleTitleCardiovascular effects of homologous bradykinin in rainbow trout Am. J. Physiol. (Regul. Integr. Comp. Physiol.) 272 R1112–R1120 Occurrence Handle1:CAS:528:DyaK2sXjtVSitr4%3D

    CAS  Google Scholar 

  • B Pelster D.J Randall (1998) The physiology of the Root effect S.F Perry B.L Tufts (Eds) Fish Physiology Academic Press New York, London 113–139

    Google Scholar 

  • B Pelster P Scheid (1992) ArticleTitleThe influence of gas gland metabolism and blood flow on gas deposition into the swimbladder of the European eel Anguilla anguilla J. exp. Biol. 173 205–216

    Google Scholar 

  • B Pelster R.E Weber (1990) ArticleTitleInfluence of organic phosphates on the Root effect of multiple fish haemoglobins J. exp. Biol. 149 425–437 Occurrence Handle1:CAS:528:DyaK3cXktlKlsrY%3D

    CAS  Google Scholar 

  • S.F Perry R Fritsche T.M Hoagland D.W Duff K.R Olson (1999) ArticleTitleThe control of blood pressure during external hypercapnia in the rainbow trout (Oncorhynchus mykiss) J. exp. Biol. 202 2177–2190 Occurrence Handle10409489

    PubMed  Google Scholar 

  • R Root (1931) ArticleTitleThe respiratory function of the blood of marine fishes Biol. Bull. 61 427–456 Occurrence Handle1:CAS:528:DyaA38XitFeksg%3D%3D

    CAS  Google Scholar 

  • P.F Scholander L Van Dam (1953) ArticleTitleComposition of the swim bladder gas in deep sea fishes Biol. Bull. 104 IssueID1 75–86 Occurrence Handle1:CAS:528:DyaG3sXkt1ehuw%3D%3D

    CAS  Google Scholar 

  • A Soivio K Nynolm K Westman (1975) ArticleTitleA technique for repeated sampling of the blood of individual resting fish J.␣exp. Biol. 62 207–217

    Google Scholar 

  • J.B Steen (1963) ArticleTitleThe physiology of the swimbladder in the eel Anguilla vulgaris. III. The mechanism of gas secretion Acta Physiol. Scand. 59 221–241 Occurrence Handle1:CAS:528:DyaF2cXlsVKrsw%3D%3D Occurrence Handle14078660 Occurrence Handle10.1111/j.1748-1716.1963.tb02738.x

    Article  CAS  PubMed  Google Scholar 

  • E.D Stevens D.J Randall (1967) ArticleTitleChanges of gas concentrations in blood and water during moderate swimming activity in rainbow trout J. exp. Biol. 46 329–337 Occurrence Handle1:STN:280:CCiB3cbmtV0%3D Occurrence Handle6033999

    CAS  PubMed  Google Scholar 

  • V Tetens N.J Christensen (1987) ArticleTitleBeta-adrenergic control of blood oxygen affinity in acutely hypoxia exposed rainbow trout J. Comp. Physiol. B 157 667–675 Occurrence Handle10.1007/BF00700988 Occurrence Handle1:CAS:528:DyaL1cXjsFWlsg%3D%3D Occurrence Handle2826555

    Article  CAS  PubMed  Google Scholar 

  • F.R Winton L.E Bayliss (1962) Human Physiology J. & A. Churchill Ltd London

    Google Scholar 

  • J.B Wittenberg B.A Wittenberg (1961) ArticleTitleActive transport of oxygen and the eye of fish Biol. Bull. 121 379

    Google Scholar 

  • J.B Wittenberg B.A Wittenberg (1962) ArticleTitleActive secretion of oxygen into the eye of fish Nature 194 106–107 Occurrence Handle1:STN:280:CC2C1MbmvVU%3D Occurrence Handle14007771

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to W.P. Waser.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Waser, W., Heisler, N. Oxygen delivery to the fish eye: blood flow in the pseudobranchial artery of rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 30, 77–85 (2004). https://doi.org/10.1007/s10695-005-0268-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-005-0268-3

Key words

  • choroid rete mirabile
  • eye
  • retina
  • teleost