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

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Summary

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.

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Reference

  • 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 41:113–142

    Google Scholar 

  • Bettex-Galland M, Hughes GM (1973) Contractile filamentous material in the pillar cells of fish gills. J Cell Sci 13:359–370

    Google Scholar 

  • Bevelander G (1934) The gills of Amia calva specialized for respiration in an oxygen deficient habitat. Copeia B: 123–127

  • Boland EJ, Olson KR (1979) Vascular organization of the catfish gill filament. Cell Tissue Res 198:487–500

    Google Scholar 

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

    Google Scholar 

  • Cooke IRC, Campbell G (1980) The vascular anatomy of the gills of the smooth toadfish (Torquiginer glaber) (Teleostei: Tetraodontidae). Zoomorphologie 94:151–166

    Google Scholar 

  • 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 284:2011–2014

    Google Scholar 

  • 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, 37–58

    Google Scholar 

  • Farrell AP (1980) Vascular pathways in the gill of ling cod, Ophiodon elongatus. Can J Zool 58:796–806

    Google Scholar 

  • 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 133:233–240

    Google Scholar 

  • Farrell AP, Sobin SS, Randall DJ, Crosby S (1980) Intralamellar blood flow pattern in fish gills. Am J Physiol 239:R 428-R 436

    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 bedthe trout gill. 31st Ann Proc Elect Micros Soc Amer 31:442–443

    Google Scholar 

  • 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., 369–374

    Google Scholar 

  • 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 79:135–146

    Google Scholar 

  • Hughes GM (1972) Morphometrics of fish gills. Respir Physiol 14:1–26

    Google Scholar 

  • 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 26:167–180

    Google Scholar 

  • Johansen K, Hanson D, Lenfant C (1970) Respiration in a primitive air breather, Amia calva. Respir Physiol 9:162–174

    Google Scholar 

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

    Google Scholar 

  • Laurent P, Delaney RG, Fishman AP (1978) The vasculature of the gills in the aquatic and aestivating lungfish (Protopterus aethiopicus). J Morphol 156:173–208

    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 

  • Murakami T (1971) Application of the scanning electron microscope to the study of the fine distribution of the blood vessels. Arch Histol Jpn 32:445–454

    Google Scholar 

  • Nakao T, (1978) An electron microscopic study of the cavernous bodies in the lamprey gill filaments. Am J Anat 151:319–336

    Google Scholar 

  • 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., 357–364

    Google Scholar 

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

    Google Scholar 

  • Smith DG (1976) The structure and function of the respiratory organs of some lower vertebrates. Ph.D. Thesis, University of Melbourne, Victoria, Australia

    Google Scholar 

  • Smith DG, Johnson DW (1977) Oxygen exchange in a simulated trout gill secondary lamella. Am J Physiol 233:R 145-R 161

    CAS  PubMed  Google Scholar 

  • Srivastava CBL, Singh M (1980) Occurrence of carotid labyrinth in the catfish group of teleost fishes. Experientia 36:651–653

    Google Scholar 

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

    Google Scholar 

  • Vogel WOP (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, 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, Schlote W (1974) Ultrastructural study of arterio-venous anastomoses in gill filaments of Tilapia mossambica. Cell Tissue Res 155:491–512

    Google Scholar 

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

    Google Scholar 

  • Wilder BG (1877) On the respiration of Amia. Proc Am Assoc Adv Sci 26:306–313

    Google Scholar 

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Supported by NSF Grant No. PCM 79-23073

The author wishes to thank Miss K. Drajus and D. Kullman for their excellent technical assistance and Dr. W. Gingerich, Mr. J. Crowther and D. Zurn for help in obtaining bowfin

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Olson, K.R. Morphology and vascular anatomy of the gills of a primitive air-breathing fish, the bowfin (Amia calva) . Cell Tissue Res. 218, 499–517 (1981). https://doi.org/10.1007/BF00210110

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