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Morphological and pharmacological basis for pulmonary ventilation in Amphiuma tridactylum

An ultrastructural study


The lung of the giant salamander, Amphiuma tridactylum, is divided into respiratory alveoli by muscular septa that increase the surface area of the lung as well as provide a mechanism for its almost complete collapse during exhalation. The epithelium of the internal surface is of two types: respiratory, composed of a single layer of pneumocytes overlying anastomosing capillaries, and non-respiratory, composed of ciliated cells and mucus-secreting goblet cells. Non-respiratory epithelium covers the apical edges of the septa, whereas the respiratory epithelium lines the alveoli. The smooth muscle of the septa and walls of the lung was studied in preparations of uninflated and acetylcholine-contracted lung. The muscle cells are ultrastructurally similar to other types of smooth muscle but are surrounded by extraordinary amounts of extracellular matrix, containing collagen and elastic fibers and numerous fine fibrils of unknown composition. Smooth muscle in isolated lung strips contracted in a dose-dependent manner when treated with acetylcholine or methacholine; contraction was blocked by atropine. Responses of lung strips to adrenergic agents were limited; only high doses of adrenalin caused slight relaxation of previously contracted muscle. These observations support the hypothesis that contraction of pulmonary smooth muscle is responsible for the ventilatory efficiency of the lung.

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  1. Bell PB, Stark-Vanes VI (1983) SEM study of the microarchitecture of the lung of the giant salamander Amphiuma tridactylum. Scan Electr Microsc (1983) 449–456

  2. Bils RF, Hughes GM (1978) Inner surface ultrastructure of the lungs of frog and lizard. Ninth Intl Congr Electron Microsc 2:504–505

  3. Boyle PJ, Conway J (1947) Potassium accumulation in muscle and associated changes. J Physiol 100:1–63

  4. Brecht K, Fraessle K (1967) Über die Wirkung elektrischer Reizung des Vagosympathicus auf die Froschlunge. Pflügers Arch ges Physiol 247:755–766

  5. Brooks RE (1970) Lung alveolar cell cytosomes: a consideration of their significance. Z Zellforsch 106:484–497

  6. Cotta-Pereira G, Rodrigo FG, David-Ferreira JF (1977) The elastic system fibers. In: Sandberg LB, Gray WR, Franzblau C (eds). Elastin and elastic tissues. Adv Exptl Med Biol 79, Plenum Press, New York pp 19–30

  7. Czopek J (1962a) Smooth muscles in the lungs of some urodeles. Nature 193:798

  8. Czopek J (1962b) Vascularization of respiratory surfaces in some caudata. Copeia 3:576–487

  9. Donnelly P, Woolcock AJ (1977) Ventilation and gas exchange in carpet phython Morelia spilotes variegata. J Comp Physiol 127:403–418

  10. Franzblau C, Faris B (1981) Elastin. In: Hay ED (ed). Cell biology of the extracellular matrix. Plenum Press, New York, pp 65–93

  11. Gans C (1970) Strategy and sequence in the evolution of the external gas exchangers of ectothermal vertebrates. Forma et Functio 3:61–104

  12. Goniakowska-Witalinska L (1978) Ultrastructural and morphometric study of the lung of the European salamander Salamandra salamandra. Cell Tissue Res 191:343–356

  13. Goniakowska-Witalinska L (1980) Scanning and transmission electron microscopic study of the lung of the newt, Triturus alpestris Laur. Cell Tissue Res 205:133–145

  14. Gratz RK (1978) Ventilation and gas exchange in the diamond-back water snake, Natrix rhomifera. J Comp Physiol 127:299–305

  15. Gratz RK, Ar A, Geiser J (1981) Gas tension profile of the lung of the viper, Vipera xanthina palestinae. Resp Physiol 44:165–176

  16. Guimond RW, Hutchison VH (1974) Aerial and aquatic respiration in the Congo eel Amphiuma means means (Garden). Resp Physiol 20:147–159

  17. Guimond RW, Hutchison VH (1976) Gas exchange of the giant salamanders of North America. In: Hughes GM (ed). Respiration of amphibious vertebrates. Academic Press, London

  18. Heisler N, Forcht G, Ultsch GR, Anderson JF (1982) Acid-base regulation in response to environmental hypercapnia in two aquatic salamanders, Siren lacertina and Amphiuma means. Resp Physiol 49:141–158

  19. Hightower JA, Burke JD, Haar JL (1975) A light and electron microscopic study of the respiratory epithelium of the adult aquatic newt Notophthalmus viridescens. Can J Zool 53:465–472

  20. Humason GL (1979) Animal tissue techniques, 4th ed. WH Freeman and Co., San Francisco

  21. Kobayasi S, Yoda C (1960) Effects of adrenaline and acetylcholine upon the smooth muscle of isolated lungs of Japanese toads. Acta Med Biol Niigata 8:241–250

  22. Leak LV, Burke JF (1968) Ultrastructural studies on the lymphatic anchoring filaments. J Cell Biol 36:129

  23. Martin KM, Hutchison VH (1979) Ventilatory activity in Amphiuma tridactylum and Siren lacertina. J Herpet 13:427–434

  24. McDonald HS (1959) Respiratory function of the ophidian air sac. Herpetologica 15:193–198

  25. McLean JR, Burnstock G (1967) Innervation of the lungs of the toad (Bufo marinus) — II. Fluorescent histochemistry of catecholamines. Comp Biochem Physiol 22:755–766

  26. Meban C (1977) Ultrastructure of the respiratory epithelium in the lungs of the newt Triturus cristatus. Acta Zool 58:151–156

  27. Meban C (1979) An electron microscopy study of the respiratory epithelium in the lungs of the fire salamander (Salamandra salamandra). J Anat 128:215–221

  28. Okada Y, Ishiko S, Daido S, Kim J, Ikeda S (1962) Comparative morphology of the lung with special reference to the alveolar epithelial cells. I. Lung of the amphibia. Acta Tuberculosa Jpn 11:63–72

  29. Pattle RE, Schock C, Creasely JM, Hughes GM (1977) Surpellic films, lung surfactant, and their cellular origin in newt, caecilian, and frog. J Zool 182:125–136

  30. Rose FL, Zambernard J, Pogany GS (1965) Hepatic glycogen depletion in Amphiuma during induced anoxia. Science 147:1467–1468

  31. Rosenberg HI (1973) Functional anatomy of pulmonary ventilation in the garter snake, Thamnophis elegans. J Morphol 140:171–184

  32. Sheehan DC, Hrapchak BB (1980) Theory and practice of histotechnology, 2nd ed. CV Mosby Co., St. Louis

  33. Shimada K (1966) Mechanical properties of the smooth muscle in the lung of the toad. Acta Med Biol 14:23–33

  34. Smith DG, Campbell G (1976) The anatomy of the pulmonary vascular bed in the toad Bufo marinus. Cell Tissue Res 165:199–213

  35. Toews DP (1971a) Factors affecting the onset and termination of respiration in the salamander, Amphiuma tridactylum. Can J Zool 49:1231–1237

  36. Toews DP (1971b) A mechanism for the selective distribution of blood in amphibians. Can J Zool 49:957–959

  37. Toews DP (1973) Oxygen consumption in Amphiuma tridactylum. Can J Zool 51:664–666

  38. Toews DP, Shelton G, Randall DJ (1971) Gas tensions in the lungs and major blood vessels of the urodele amphibian, Amphiuma tridactylum. J Exp Biol 55:47–61

  39. Willnow I (1964) Die Lunge von Amphiuma means means. I. Mitteilung: Morphologie. Zool Beitr Berl 10:29–84

  40. Willnow I (1968) Die Lunge von Amphiuma means means. II. Mitteilung: Diskussion. Zool Beitr Berl 14:359–386

  41. Wood MJ, Burnstock G (1967) Innervation of the lungs of the toad (Bufo marinus) — I. Physiology and Pharmacology. Comp Biochem Physiol 22:755–766

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Correspondence to Paul B. Bell Jr..

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Stark-Vancs, V., Bell, P.B. & Hutchison, V.H. Morphological and pharmacological basis for pulmonary ventilation in Amphiuma tridactylum . Cell Tissue Res. 238, 1–12 (1984).

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Key words

  • Lung
  • Amphibia
  • Ultrastructure
  • Smooth muscle
  • Extracellular matrix