Cell and Tissue Research

, Volume 218, Issue 3, pp 499–517 | Cite as

Morphology and vascular anatomy of the gills of a primitive air-breathing fish, the bowfin (Amia calva)

  • Kenneth R. Olson


The morphology of the gills of a primitive air breather (Amia calva) was examined by light microscopy of semithin sections of gill filaments, and gill perfusion pathways were identified by scanning-electron microscopic analysis of corrosion replicas prepared by intravascular injection of methyl methacrylate. The arrangement of gill filaments and respiratory lamellae is similar to that of teleosts with the exception of an interfilamental support bar that is fused to the outer margins of lamellae on adjacent filaments. The prebranchial vasculature is also similar to that of teleosts, whereas the postbranchial circulation of arches III and IV is modified to permit selective perfusion of the air bladder. Gill filaments contain three distinct vascular systems: (1) the respiratory circulation which receives the entire cardiac output and perfuses the secondary lamellae; (2) a nutrient system that arises from the postlamellar circulation and perfuses filamental tissues; (3) a network of unknown function consisting of subepithelial sinusoids surrounding afferent and efferent margins of the filament and traversing the filament beneath the interlamellar epithelium. Prelamellar arteriovenous anastomoses (AVAs) are rare, postlamellar AVAs are common especially at the base of the filament where they form a dense network of small tortuous vessels before coalescing into a large filamental nutrient artery. Unlike in most teleosts, the outer vascular margins of the lamellae are embedded in the interfilamental support bar and become the sole vasculature of this tissue. Arterial-arterial lamellar bypass vessels were not observed. Previously observed decreases in oxygen transfer across the gills during air breathing can be explained only by redistribution of blood flow between or within the respiratory lamellae.

Key words

Gills Blood vessels Amia calva Air breathing 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Allis EP Jr (1912) The pseudobranchial and carotid arteries in Esox, Salmo and Gadus, together with a description of the arteries in the adult Amia. Anat Anz Bd 41:113–142Google Scholar
  2. Bettex-Galland M, Hughes GM (1973) Contractile filamentous material in the pillar cells of fish gills. J Cell Sci 13:359–370Google Scholar
  3. Bevelander G (1934) The gills of Amia calva specialized for respiration in an oxygen deficient habitat. Copeia B: 123–127Google Scholar
  4. Boland EJ, Olson KR (1979) Vascular organization of the catfish gill filament. Cell Tissue Res 198:487–500Google Scholar
  5. Cooke IRC (1980) Functional aspects of the morphology and vascular anatomy of the gills of the endeavour dogfish, Centrophorus scalpratus (McCulloch) (Elasmobranchii: Squalidae). Zoomorphologie 94:167–183Google Scholar
  6. Cooke IRC, Campbell G (1980) The vascular anatomy of the gills of the smooth toadfish (Torquiginer glaber) (Teleostei: Tetraodontidae). Zoomorphologie 94:151–166Google Scholar
  7. Dunel S, Laurent P (1977) La vascularisation branchiale chez l'Anguille: action de l'acetylcholine et de l'adrénaline sur la répartition d'une résine polymérisable dans les différents compartiments vasculaires. CR Acad Sc Paris 284:2011–2014Google Scholar
  8. Dunel S, Laurent P (1980) Functional organisation of the gill vasculature in different classes of fish. In: B Lahlou (ed) Epithelial transport in the lower vertebrates. Cambridge Univ Press, London, 37–58Google Scholar
  9. Farrell AP (1980) Vascular pathways in the gill of ling cod, Ophiodon elongatus. Can J Zool 58:796–806Google Scholar
  10. Farrell AP, Daxboeck C, Randall DJ (1979) The effect of input pressure and flow on the pattern and resistance to flow in the isolated perfused gill. J Comp Physiol 133:233–240Google Scholar
  11. Farrell AP, Sobin SS, Randall DJ, Crosby S (1980) Intralamellar blood flow pattern in fish gills. Am J Physiol 239:R 428-R 436Google Scholar
  12. Gannon BJ, Campbell G, Randall DJ (1973) Scanning electron microscopy of vascular casts for the study of vessel connections in a complex vascular bedthe trout gill. 31st Ann Proc Elect Micros Soc Amer 31:442–443Google Scholar
  13. Hodde KC, Miodonski A, Bakker C, Veltman WAM (1977) Scanning electron microscopy of microcorrosion casts with special attention on arterio-venous differences and application to the rats cochlea. In: O Johari (ed) Scanning Electron Microscopy/III: IIT Research Institute, Chicago, Ill., 369–374Google Scholar
  14. Holbert PW, Boland EJ, Olson KR (1979) The effect of epinephrine and acetylcholine on the distribution of red cells within the gills of the channel catfish (Ictalurus punctatus). J Exp Biol 79:135–146Google Scholar
  15. Hughes GM (1972) Morphometrics of fish gills. Respir Physiol 14:1–26Google Scholar
  16. Ishimatsu A, Itazawa Y, Takeda T (1979) On the circulatory systems of the snakeheads Channa maculata and C. argua with reference to biodal breathing. Jpn J Ichthyol 26:167–180Google Scholar
  17. Johansen K, Hanson D, Lenfant C (1970) Respiration in a primitive air breather, Amia calva. Respir Physiol 9:162–174Google Scholar
  18. Laurent P, Dunel S (1976) Functional organization of the teleost gill I. Blood Pathways. Acta Zool (Stockh) 57:189–209Google Scholar
  19. Laurent P, Delaney RG, Fishman AP (1978) The vasculature of the gills in the aquatic and aestivating lungfish (Protopterus aethiopicus). J Morphol 156:173–208Google Scholar
  20. Morgan M, Tovell PWA (1973) The structure of the gill of the trout, Salmo gairdneri (Richardson). Z Zellforsch 142:147–162Google Scholar
  21. Murakami T (1971) Application of the scanning electron microscope to the study of the fine distribution of the blood vessels. Arch Histol Jpn 32:445–454Google Scholar
  22. Nakao T, (1978) An electron microscopic study of the cavernous bodies in the lamprey gill filaments. Am J Anat 151:319–336Google Scholar
  23. Olson KR (1980) Application of corrosion casting procedures in identification of perfusion distribution in a complex microvasculature. In: O Johari (ed) Scanning Electron Microscopy/III: AMF O'Hare, Chicago, ill., 357–364Google Scholar
  24. Olson KR, Kent B (1980) The Microvasculature of the elasmobranch gill. Cell Tissue Res. 209:49–63Google Scholar
  25. Smith DG (1976) The structure and function of the respiratory organs of some lower vertebrates. Ph.D. Thesis, University of Melbourne, Victoria, AustraliaGoogle Scholar
  26. Smith DG, Johnson DW (1977) Oxygen exchange in a simulated trout gill secondary lamella. Am J Physiol 233:R 145-R 161PubMedGoogle Scholar
  27. Srivastava CBL, Singh M (1980) Occurrence of carotid labyrinth in the catfish group of teleost fishes. Experientia 36:651–653Google Scholar
  28. Steen JB, Kruysse A (1964) The respiratory function of teleostean gills. Comp Biochem Physiol 12:127–142Google Scholar
  29. Vogel WOP (1978) Arteriovenous anastomoses in the afferent region of trout gill filaments (Salmo gairdneri Richardson, Teleostei). Zoomorphologie 90:205–212Google Scholar
  30. Vogel W, Vogel V, Kremers H (1973) New aspects of the intrafilamental vascular system in gills of a euryhaline teleost, Tilapia mossambica. Z Zellforsch 144:573–583Google Scholar
  31. Vogel W, Vogel V, Schlote W (1974) Ultrastructural study of arterio-venous anastomoses in gill filaments of Tilapia mossambica. Cell Tissue Res 155:491–512Google Scholar
  32. Vogel W, Vogel V, Pfautsch M (1976) Arterio-venous anastomoses in rainbow trout gill filaments. Cell Tissue Res 167:373–385Google Scholar
  33. Wilder BG (1877) On the respiration of Amia. Proc Am Assoc Adv Sci 26:306–313Google Scholar

Copyright information

© Springer-Verlag GmbH & Co. KG 1981

Authors and Affiliations

  • Kenneth R. Olson
    • 1
  1. 1.Indiana University School of Medicine, South Bend Center, Notre Dame UniversityNotre DameUSA

Personalised recommendations