Skip to main content
Log in

Structural and circulatory responses to hypoxia in the secondary lamellae ofSalmo gairdneri gills at two temperatures

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

Summary

The first gill arch ofSalmo gairdneri was fixed from normoxic (O2 saturation of the water >90%) and hypoxic (O2 saturation 25–30% for 5 days) fish at 10 °C and 18 °C, and from fish after one-day recovery from hypoxia at 18 °C. The secondary lamellae of the gills were analysed with morphometric methods for structural, haemotological and circulatory changes. During hypoxia a marked vascular distension took place at both temperatures. At both temperatures the vascular distension coincided with a shortening of the diffusion distance (36% at 10 °C and 21% at 18 °C) and a swelling of the erythrocytes (60% at 10 °C and 42% at 18 °C). The effects of these changes on the oxygen uptake of the gills are discussed.

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.

Similar content being viewed by others

References

  • Barnard T (1976) An empirical relationship for the formulation of glutaraldehyde-based fixatives, based on measurements of cell volume change. J Ultrastruct Res 54:478

    Google Scholar 

  • Booth JH (1978) The distribution of blood flow in the gills of fish: application of a new technique to rainbow trout (Salmo gairdneri). J Exp Biol 73:119–130

    Google Scholar 

  • Booth JH (1979a) The effects of oxygen supply, epinephrine and acetylcholine on the distribution of blood flow in trout gills. J Exp Biol 83:31–39

    Google Scholar 

  • Booth JH (1979b) Circulation in trout gills: the relationship between branchial perfusion and the width of the lamellar blood space. Can J Zool 57:2183–2185

    Google Scholar 

  • Cameron JN (1974) Blood flow distribution as indicated by tracer microspheres in resting and hypoxic arctic grayling (Thymallus arcticus). Comp Biochem Physiol 52A:441–444

    Google Scholar 

  • Davis JC (1972) An infrared photographic technique useful for studying vascularization of fish gills. J Fish Res Board Can 29:109–111

    Google Scholar 

  • Farrell AP, Sobin SS, Randall DJ, Crosby S (1980) Intralamellar blood flow patterns in fish gills. Am J Physiol 239:R428-R436

    Google Scholar 

  • Gannon BJ, Campbell G, Randall DJ (1973) Scanning electron microscopy of vascular casts for the study of vessel connections in a complex vascular bed — The trout gill. 31st. Ann Proc Elect Microsc Soc Am 31:442–443

    Google Scholar 

  • Hargens AR, Millard RW, Johansen K (1974) High capillary permeability in fishes. Comp Biochem Physiol 48A:675–680

    Google Scholar 

  • Haswell MS, Perry SF, Randall DJ (1978) The effect of perfusate oxygen levels on CO2 excretion in the perfused gill (1). J Exp Zool 205:309–312

    Google Scholar 

  • Holeton GF, Randall DJ (1967a) Changes in blood pressure in the rainbow trout during hypoxia. J Exp Biol 46:297–305

    Google Scholar 

  • Holeton GF, Randall DJ (1967b) The effect of hypoxia upon the partial pressure of gases in blood and water afferent and efferent to the gills of rainbow trout. J Exp Biol 46:317–327

    Google Scholar 

  • Hughes GM (1972) Morphometrics of fish gills. Respir Physiol 14:1–25

    Google Scholar 

  • Hughes GM (1976) Fish respiratory physiology. In: Spencer Davies P (ed) Perspectives in experimental biology, vol I, Zoology. Pergamon Press, Oxford New York, pp 235–245

    Google Scholar 

  • Hughes GM (1980) Functional morphology of fish gills. In: Lahlou B (ed) Epithelial transport in the lower vertebrates, part I, Morphological aspects. Cambridge University Press, Cambridge, pp 15–36

    Google Scholar 

  • Hughes GM, Grimstone AV (1965) The fine structure of the secondary lamellae of the gills ofGadus pollachius. Q J Microsc Sci 106:343–353

    Google Scholar 

  • Hughes GM, Koyama T (1975) Gas exchange of single red blood cells within secondary lamellae of fish gills. J Physiol (Lond) 246:82–83

    Google Scholar 

  • Hughes GM, Perry SF (1976) Morphometric study of trout gills: A light-microscopic method suitable for the evaluation of pollutant action. J Exp Biol 64:447–460

    Google Scholar 

  • Hughes GM, Saunders RL (1970) Responses of the respiratory pumps to hypoxia in the rainbow trout,Salmo gairdneri. J Exp Biol 53:529–545

    Google Scholar 

  • Hughes GM, Wright DE (1970) A comparative study of the ultrastructure of the water/blood pathway in the secondary lamellae of teleost and clasmobranch fishes — benthic forms. Z Zellforsch 104:478–493

    Google Scholar 

  • Hughes GM, Tuurala H, Soivio A (1978) Regional distribution of blood in the gills of rainbow trout in normoxia and hypoxia: a morphometric study with two fixatives. Ann Zool Fenn 15:226–234

    Google Scholar 

  • Laurent P, Dunel S (1976) Functional organization of the teleost gill. I, Blood pathways. Acta Zool 57:189–209

    Google Scholar 

  • Laurent P, Dunel S (1980) Morphology of gill epithelia in fish. Am J Physiol 238:R147-R159

    Google Scholar 

  • Luft JH (1961) Improvements in epoxy resin embedding methods. J Biophys Biochem Cytol 9:409–414

    Google Scholar 

  • Mertz WA (1967) Die Streckenmessungen an gerichteten Strukturen im Mikroskop und ihre Anwendung zur Bestimmung von Oberflächen — Volumen — Relationen im Knochengewebe. Mikroskopie 22:132–142

    Google Scholar 

  • Morgan M, Tovell PWA (1973) The structure of the gill of the trout,Salmo gairdneri (Richardson). Z Zellforsch 142:147–162

    Google Scholar 

  • Mount DI (1961) Development of a system for controlling dissolved oxygen content of water. Trans Am Fish Soc 90:323–327

    Google Scholar 

  • Newstead JD (1967) Fine structure of the respiratory lamellae of teleostean gills. Z Zellforsch 79:396–428

    Google Scholar 

  • Nikinmaa M, Tuurala H, Soivio A (1980) Thermoacclimatory changes in blood oxygen binding properties and gill secondary lamellar structure ofSalmo gairdneri. J Comp Physiol 140:255–260

    Google Scholar 

  • Payan P, Girard JP (1977) Adrenergic receptors regulating patterns of blood flow through the gills of trout. Am J Physiol 232:H18-H23

    Google Scholar 

  • Pettersson K, Nilsson S (1979) Nervous control of the branchial vascular resistance of the Atlantic cod,Gadus morhua. J Comp Physiol 129:179–183

    Google Scholar 

  • Randall DJ (1970) Gas exchange in fish. In: Hoar WS, Randall DJ (eds) Fish physiology, vol IV. Academic Press, New York London, pp 253–292

    Google Scholar 

  • Randall DJ, Holeton GF, Stevens ED (1967) The exchange of oxygen and carbon dioxide 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 29:1063–1070

    Google Scholar 

  • Smith DG (1977) Sites of cholinergic vasoconstriction in trout gills. Am J Physiol 233:R222-R229

    Google Scholar 

  • Smith DG, Johnson DW (1977) Oxygen exchange in a simulated trout gill secondary lamella. Am J Physiol 233:R145-R161

    Google Scholar 

  • Soivio A, Hughes GM (1978) The influence of hypoxia and anaesthesia on the blood volume and haematocrit value in the secondary lamellae ofSalmo gairdneri gills. Ann Zool Fenn 15:221–225

    Google Scholar 

  • Soivio A, Nikinmaa M (1981 in press) The swelling of erythrocytes in relation to the oxygen affinity of rainbow trout blood. In: Pickering AC (ed) Stress in fish. Academic Press, New York

    Google Scholar 

  • Soivio A, Nyholm K, Westman K (1975) A technique for repeated sampling of the blood of individual resting fish. J Exp Biol 62:207–217

    Google Scholar 

  • Soivio A, Nikinmaa M, Westman K (1980) The blood oxygen binding properties of hypoxicSalmo gairdneri. J Comp Physiol 136:83–87

    Google Scholar 

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

    Google Scholar 

  • Vogel W, Vogel V, Kremers H (1973) New aspects of the intrafilamental vascular system in gills of a euryhaline teleost,Tilapia mossambica. Z Zellforsch 144:573–583

    Google Scholar 

  • Vogel W, Vogel V, Pfautsch M (1976) Arteriovenous anastomoses in rainbow trout gill filaments. A scanning and transmission electron microscopic study. Cell Tiss Res 167:373–385

    Google Scholar 

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

    Google Scholar 

  • Vogel WOP (1978b) The origin of Fromm's arteries in trout gills. Z Mikrosk Anat Forsch 92:565–570

    Google Scholar 

  • Westfall BA (1943) Specific gravity of fish blood during rapidly developed anoxia. J Cell Comp Physiol 22:177–186

    Google Scholar 

  • Whittaker SFR, Winton FR (1933) The apparent viscosity of blood flowing in the isolated hind limb of the dog, and its variation with corpuscular concentration. J Physiol (Lond) 78:339–369

    Google Scholar 

  • Wood CM (1974) A critical examination of the physical and adrenergic factors affecting blood flow through the gills of the rainbow trout. J Exp Biol 60:241–265

    Google Scholar 

  • Wood CM, Shelton G (1980a) Cardiovascular dynamics and adrenergic responses of the rainbow troutin vivo. J Exp Biol 87:247–270

    Google Scholar 

  • Wood CM, Shelton G (1980b) The reflex control of heart rate and cardiac output in the rainbow trout: interactive influences of hypoxia, haemorrhage and systemic vasomotor tone. J Exp Biol 87:271–284

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Soivio, A., Tuurala, H. Structural and circulatory responses to hypoxia in the secondary lamellae ofSalmo gairdneri gills at two temperatures. J Comp Physiol B 145, 37–43 (1981). https://doi.org/10.1007/BF00782591

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00782591

Keywords

Navigation