The fine structure of the branchial heart appendage of the cephalopod Octopus dofleini martini

  • Astrid Witmer
  • Arthur W. Martin


The branchial heart appendage of Octopus dofleini martini has been investigated electron microscopically. This organ is dominated by peripherally lobed blood sinuses. It contains free hemocyanin (often aligned in rows), amoebocytes, endothelial cells, and muscle cells which occur mainly in connection with neurons. The neurons are often exposed to the blood. The blood sinuses are enclosed by a basement membrane which contains collagen equivalents and fine fibrillar elements. The sinuses are covered by two different epithelia: 1) the epithelium in the caoity of the appendage consisting of irregularly shaped cells with processes, the so called (∼ 30 μ high) podocytes, and 2) the epithelium (∼ 40 μ in height) on the surface of the organ, which is composed of two parts: a) a “lacuna”-forming portion directly adjacent to the basement membrane, which is topped by b) a continuous tissue portion with occasional “lacuna”-canals. The intercellular spaces of the inner and outer epithelium are connected. The structures of these epithelial cells are discussed in relation to the formation of the pericardial fluid.

Key words

Pericardial gland Octopus Excretory organ Electron microscopy 


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  1. Altner, H.: Die Ultrastruktur der Labialniere von Onychiurus quadriocellatus (Collembola). J. Ultrastruct. Res. 24, 349–366 (1968).Google Scholar
  2. Andrews, E., Little, C.: Ultrafiltration in the gastropod heart. Nature (Lond.) 234, 411–412 (1971).Google Scholar
  3. Baleydier, Ch., Nicaise, G., Ceccatty, M.P. de: Etat fibroblastique et différenciation fibrocytaire des cellules conjonctives de Glossodoris (Gastéropode, Opisthobranche). C.R. Acad. Sci. (Paris) 269, 175–178 (1969).Google Scholar
  4. Barber, V.C., Graziadei, P.: The fine structure of cephalopod blood vessels. I. Some smaller peripheral vessels. Z. Zellforsch. 66, 765–781 (1965).Google Scholar
  5. Barber, V.C., Graziadei, P.: The fine structure of cephalopod blood vessels. II. Vessels of the nervous system. Z. Zellforsch. 77, 147–161 (1967).Google Scholar
  6. Bargmann, W.: Über Struktur und Speicherungsvermögen des Nierenglomerulus. Z. Zellforsch. 14, 73–137 (1931).Google Scholar
  7. Bargmann, W.: Weitere histologische Untersuchungen am Nierenkörperchen. Z. Zellforsch. 18, 166–191 (1933).Google Scholar
  8. Bargmann, W., Hehn, G. v.: Über das Nephron der Elasmobranchier. Z. Zellforsch. 114, 1–21 (1971).Google Scholar
  9. Bear, R.S.: Long X-ray diffraction spacings of collagen. J. Amer. chem. Soc. 64, 727 (1942).Google Scholar
  10. Bloom, W., Fawcett, D.W.: A textbook of histology, nineth edition. Philadelphia-London: W.B. Saunders Company 1968.Google Scholar
  11. Bonga, S.E.W., Boer, H.H.: Ultrastructure of the reno-pericardial system in the pond snail Lymnea stagnalis (L.). Z. Zellforsch. 94, 513–529 (1969).Google Scholar
  12. Bouillon, J.: Ultrastructure des cellules rénales des Mollusques. I. Gastéropodes pulmonés terrestres. Annls. Sci. nat. (2) 12, 719–749 (1960).Google Scholar
  13. Bowers, B.: Coated vesicles in the pericardial cells of the aphid (Myzus persicae Sulz). Protoplasma (Wien) 59, 351–367 (1965).Google Scholar
  14. Brooks, R.E.: Ultrastructure of the physostomatous swimbladder of rainbow trout (Salmo gairdneri). Z. Zellforsch. 106, 473–483 (1970).Google Scholar
  15. Wondrak, G.: Die Ultrastruktur der Zellen aus dem interstitiellen Bindegewebe von Arion rufus (L.), Pulmonata, Gastropoda. Z. Zellforsch. 95, 249–262 (1969).Google Scholar
  16. Yamada, E.: The fine structure of the renal glomerulus of the mouse. J. biophys. biochem. Cytol. 1 (6), 551–566 (1955).Google Scholar
  17. Zebe, E.: Feinbau und Funktionsweise der Muskeln in vergleichender Sicht. Zool. Anz. 30, Suppl. Bd. (1967).Google Scholar
  18. Zimmermann, K.W.: Über den Bau des Glomerulus der Säugerniere. Z. mikr.-anat. Forsch. 32, 176–278 (1933).Google Scholar
  19. Bruchhausen, F. von, Merker, H.J.: Morphologischer und chemischer Aufbau isolierter Basalmembranen aus der Nierenrinde der Ratte. Histochemie 8, 90–108 (1967).Google Scholar
  20. Bruggen, E.F.J. van, Wiebenga, E.H., Gruber, M.: Structure and properties of hemocyanins. II. Electron micrographs of the hemocyanins of Sepia officinalis, Octopus vulgaris and Cancer pagurus. J. molec. Biol. 4, 8–9 (1962).Google Scholar
  21. Buchholz, K., Kuhlmann, D., Nolte, A.: Aufnahme von Trypanblau und Ferritin in die Blasenzellen des Bindegewebes von Helix pomatia und Cepaea nemoralis (Stylommatophora, Pulmonata). Z. Zellforsch. 113, 203–215 (1971).Google Scholar
  22. Cuénot, L.: Études physiologiques sur les Gastéropodes pulmonés. Arch. Biol. (Liège) 12, (1892).Google Scholar
  23. Cuénot, L.: L'excrétion chez les Mollusques. Arch. Biol. (Liège) 16, 49–96 (1899).Google Scholar
  24. El-Hifnawi, E.S., Seifert, G.: Über den Feinbau der Maxillarnephridien von Polyxenus lagurus (L.) (Diplopoda, Penicillata). Z. Zellforsch. 113, 518–530 (1971).Google Scholar
  25. Eriksson-Quensel, J., Svedberg, T.: The molecular weights and pH stability regions of the hemocyanins. Biol. Bull. 71, 498–547 (1936).Google Scholar
  26. Fain-Maurel, M.A., Cassier, P.: Différenciations cytoplasmiques en relation avec la fonction excrétrice dans les reins céphaliques de Petrobius maritimus Leach (Insecte, Aptérygote). J. Microscopie 10, 163–178 (1971).Google Scholar
  27. Farquhar, M.G., Palade, G.E.: Segregation of ferritin in glomerular protein absorption droplets. J. biophys. biochem. Cytol. 7, 297–304 (1960).Google Scholar
  28. Farquhar, M.G., Palade, G.E.: Functional evidence for the existence of a third cell type in the renal glomerulus. Phagocytosis of filtration residues by a distinctive “third” cell. J. Cell Biol. 13, 55–87 (1962).Google Scholar
  29. Farquhar, M.G., Palade, G. E.: Junctional complexes in various epithelia. J. Cell Biol. 17, 375–412 (1963).Google Scholar
  30. Fawcett, D.W.: Histochemical Society Symposium on Structure and Function at Cell Surfaces: Chicago, Illinois, April 12, 1964. Surface specializations of absorbing cells. J. Histochem. Cytochem. 13, 75–91 (1965).Google Scholar
  31. Flemming, W.: Über die Blutzellen der Acephalen und Bemerkungen über deren Blutbahn. Arch. mikr. Anat. 15, 243–255 (1978).Google Scholar
  32. François, J.: Ultrastructure du rein labial céphalique de Campodea chardardi Condé (Diplura, Insecta). Z. Zellforsch. 127, 34–49 (1972).Google Scholar
  33. Fredericq, L.: Recherches sur la physiologie du poulpe commun. (Octopus vulgaris). Arch. Zool. expér. et gen. 7, 535–583 (1878).Google Scholar
  34. Fürth, O. v.: Über den Stoffwechsel der Cephalopoden. Hoppe-Seylers Z. physiol. Chem. 31, 353–380 (1900).Google Scholar
  35. Gabe, M.: Données histologiques sur le rein céphalique des Thysanoures (Insectes, Aptérygotes). Ann. Soc. ent. Fr. 3, 681–713 (1967).Google Scholar
  36. Gray, E.G.: Electron microscopy of the glio-vascular organization of the brain of Octopus. Phil. Trans. B 255, 13–32 (1968).Google Scholar
  37. Graziadei, P.: The ultrastructure of the motor nerve endings in the muscles of cephalopods. J. Ultrastruct. Res. 15, 1–13 (1966).Google Scholar
  38. Grimpe, G.: Das Blutgefäßsystem der dibranchiaten Cephalopoden. 1. Teil. Octopoda. Z. wiss. Zool. 104, 531–621 (1913).Google Scholar
  39. Grobben, G.: Morphologische Untersuchungen über den Harn- und Geschlechtsapparatus, sowie Leibeshöhle der Cephalopoden. Arb. zool. Inst. Wien 5, 179–252 (1884).Google Scholar
  40. Groepler, W.: Feinstruktur der Coxalorgane bei der Gattung Ornithodorus (Acari, Argasidae). Z. wiss. Zool. 178, 235–275 (1969).Google Scholar
  41. Hall, B.V.: Studies of normal glomerular structure by electron microscopy. Proc. V. Ann. Conf. Nephrotic Syndrome. New York: The National Nephrosis Foundation, Inc. 1953.Google Scholar
  42. Hancock, A.: On certain points in the anatomy and physiology of the dibranchiate cephalopoda. (Nat. Hist. Rev.) Quart. J. Biol. Sci. 1, 473–484 (1861).Google Scholar
  43. Harless, E.: Über die Nieren der Sepia oder die sogenannten Venenanhänge. Wiegmann-Erichsons Arch. f. Naturgesch. 13; 1, 1–8 (1847).Google Scholar
  44. Harrison, F.M., Martin, A.W.: Excretion in the cephalopod, Octopus dofleini. J. exp. Biol. 42 (1), 71–98 (1965).Google Scholar
  45. Haupt, J.: Zur Feinstruktur der Maxillarnephridien von Scutigerella immaculata Newport (Symphyla, Myriapoda). Z. Zellforsch. 101, 401–407 (1969a).Google Scholar
  46. Haupt, J.: Zur Feinstruktur der Labialniere des Silberfischchens Lepisma saccharina L. (Thysanura, Insecta). Zool. Beitr., N. F., 15, 139–170 (1969b).Google Scholar
  47. Hecker, H., Diehl, P.A., Aeschlimann, A.: Recherches sur l'ultrastructure et l'histochimie de l'organe coxal d'Ornithodorus moubata (Murray) (Ixodoidea, Argasidae). Acta trop. (Basel) 26, 346–359 (1969).Google Scholar
  48. Herter, K., Urich, K.: Vergleichende Physiologie der Tiere. I. Stoff- und Energiewechsel. Berlin: Walter de Gruyter und Co. 1966. Göschen Sammlung, Bd. 972/972a.Google Scholar
  49. Hollande, A.: La cellule pericardiale des insectes. Archs. Anat. microsc. 18, 85–307 (1921).Google Scholar
  50. Ito, S.: The enteric surface coat on cat intestinal microvilli. J. Cell Biol. 27, 475–491 (1965).Google Scholar
  51. Johansen, K., Martin, A.W.: Circulation in the cephalopod, Octopus dofleini. Comp. Biochem. Physiol. 5, 161–176 (1962).Google Scholar
  52. Kenyon, K.R.: The synthesis of the basement membrane by the corneal epithelium in bullous keratopathy. Invest. Ophthal. 8 (2), 156–168 (1969).Google Scholar
  53. Kirschner, L.B., Wagner, S.: The site and permeability of the filtration locus in the crayfish antennal gland. J. exp. Biol. 43, 385–395 (1965).Google Scholar
  54. Knoll, Ph.: Über die Blutkörperchen bei wirbellosen Tieren. S.-B. Akad. Wiss. Wien, math.-nat. Kl., Abt. 3, 102, 440 (1893).Google Scholar
  55. Koechlin, N.: Ultrastructures du plexus sanguin périoesophagien; ses relations avec la néphridie de Sabella pavonina Savigny. C. R. Acad. Sci. (Paris) 262, Ser. D., 1266–1269 (1966).Google Scholar
  56. Kümmel, G.: Das Cölomsäckchen der Antennendrüse von Cambarus affinis Say (Decapoda, Crustacea). Zool. Beitr., N. F., 10, 227–252 (1964).Google Scholar
  57. Kümmel, G.: Druckfiltration als ein Mechanismus der Stoffausscheidung bei Wirbellosen. In: Funktionelle und morphologische Organisation der Zelle, 2. wiss. Konf. Ges. Dtsch. Naturf. u. Ärzte, S. 203–227. Berlin-Heidelberg-New York: Springer 1965.Google Scholar
  58. Kümmel, G.: Die Podocyten. Zool. Beitr., N.F., 13 (2–3), 245–263 (1967).Google Scholar
  59. Lee, J.C., Hurley, S., Hopper, J.: Secretory activity of the juxtaglomerular granular cells of the mouse. Morphologic and enzyme histochemical observations. Lab. Invest. 15 (9), 1459–1476 (1966).Google Scholar
  60. Lindemann, W.: Urämie bei Cephalopoden. Beitr. z. path. Anat. 27, 491–493 (1900).Google Scholar
  61. Martin, A.W.: Recent advances in knowledge of invertebrate renal function. In: Recent advances in invertebrate physiology, p. 247–276. Oregon: University of Oregon Publications 1957.Google Scholar
  62. Martin, A.W., Harrison, F.M.: Excretion (Chapter 11; in Physiology of Mollusca). Wilbur, K. M., Yonge, C.M. (eds). New York and London: Academic Press 1966.Google Scholar
  63. Maunsbach, A.B.: Absorption of I125-labeled homologous albumin by rat kidney proximal tubule cells. A study of microperfused single proximal tubules by electron microscopic autoradiography and histochemistry. J. Ultrastruct. Res. 15, 197–241 (1966).Google Scholar
  64. Meyer, W.Th.: Die Anatomie von Opisthoteuthis depressa. Z. wiss. Zool. 85, 183–269 (1906/07).Google Scholar
  65. Miller, F.: Hemoglobin absorption by the cells of the proximal convoluted tubule in mouse kidney. J. biophys. biochem. Cytol. 8, 689–718 (1960).Google Scholar
  66. Mills, R.P., King, R.C.: The periocardial cells of Drosophila melanogaster. Quart. J. micr. Sci. 106, 261–268 (1965).Google Scholar
  67. Möllendorff, v. W.: Einige Beobachtungen über den Aufbau des Nierenglomerulus. Z. Zellforsch. 6, 441–450 (1927).Google Scholar
  68. Möllendorff, v. W.: Der Exkretionsapparat. Handbuch der mikroskopischen Anatomie des Menschen (v. Möllendorff). Berlin: Springer 1930.Google Scholar
  69. Nisbet, R.H., Plummer, J.M.: Fibroblast and collagen in Achatinidae. J. Physiol. (Lond.) 196, 18P-20P (1968).Google Scholar
  70. Pease, D.C.: Fine structures of the kidney seen by electron microscopy. J. Histochem. Cytochem. 3 (4), 295–308 (1955).Google Scholar
  71. Picken, L.E.R.: The mechanism of urine formation in invertebrates. II. The excretory mechanism in certain mollusca. J. exp. Biol. 14, 20–34 (1937).Google Scholar
  72. Plummer, J.M.: Collagen-formation in Achatinidae (Pulmonata) associated with a specific cell type. Proc. malacological Soc. Lond. 37, 189–198 (1966).Google Scholar
  73. Potts, W.T.W.: Ammonia excretion in an octopus. (In: 47th annual meeting of the Federation of American Societies for Experimental Biology, 1963). Fed. Proc. 22 (2 Pt 1), 662 (1963).Google Scholar
  74. Potts, W.T.W.: Ammonia excretion in Octopus dofleini. Comp. Biochem. Physiol. 14 (2), 339–355 (1965).Google Scholar
  75. Potts, W.T.W.: Excretion in the molluscs. Biol. Rev. 42, 1–41 (1967).Google Scholar
  76. Potts, W.T.W.: Aspects of excretion in the molluscs. Symp. zool. Soc. Lond. 22, 187–192 (1968).Google Scholar
  77. Potts, W.T.W., Martin, A.W.: The process of ammonia excretion in an octopus. Proc. Internat. Congr. Zool. 16, 78 (1963).Google Scholar
  78. Potts, W.T.W., Parry, G.: Osmotic and ionic regulation in animals. Oxford-London-New York-Paris: Pergamon Press 1968.Google Scholar
  79. Potts, W.T.W., Todd, M.: Kidney function in the Octopus. Comp. Biochem. Physiol. 16, 479–489 (1965).Google Scholar
  80. Rasmont, R.: Structure et ultrastructure de la glande coxale d'un scorpion. Ann. Soc. roy. zool. Belg. 89, 239–272 (1960).Google Scholar
  81. Rhodin, J.A.G.: The diaphragm of capillary endothelial fenestrations. J. Ultrastruct. Res. 6, 171–185 (1962).Google Scholar
  82. Rifkin, E., Cheng, T.C., Hohl, H.R.: An electron microscope study of the constituents of encapsulating cysts in the American oyster, Crassostrea virginica formed in response to Tylocephalum (Metacestodes). J. Invertebrate Pathol. 14, 211–226 (1969).Google Scholar
  83. Rogers, D.C.: Fine structure of the epineural connective tissue sheath of the subesophageal ganglion in Helix aspersa. Z. Zellforsch. 102, 99–112 (1969).Google Scholar
  84. Ruddell, C.L.: A cytological and histochemical study of the wound repair in the Pacific oyster, Crassostrea gigas. Ph. D. Thesis, Univ. of Washington, 1969.Google Scholar
  85. Ruddell, C.L., Wellings, S.R.: The ultrastructure of the oyster brown cell, a cell with a fenestrated plasma membrane. Z. Zellforsch. 120, 17–28 (1971).Google Scholar
  86. Schipp, R., Höhn, P., Schäfer, A.: Elektronenmikroskopische und histochemische Untersuchungen zur Funktion des Kiemenherzanhanges (Pericardialdrüse) von Sepia officinalis. Z. Zellforsch. 117, 252–274 (1971).Google Scholar
  87. Schipp, R., Schäfer, A.: Vergleichende elektronenmikroskopische Untersuchungen an den zentralen Herzorganen von Cephalopoden Sepia officinalis. Feinstruktur und Funktion der Kiemenherzen. Z. Zellforsch. 101, 367–379 (1969).Google Scholar
  88. Schipp, R., Schäfer, A.: Zur Feinstruktur und Funktion der Pericardialdrüse der Cephalopoden. Verh. dtsch. zool. Ges. 64, 113–117 (1971).Google Scholar
  89. Schmekel, L.: Zur Feinstruktur der Spezialzellen von normal ernährten und hungernden Aeolidiern (Gastropoda, Nudibranchia). Z. Zellforsch. 124, 419–432 (1972).Google Scholar
  90. Schmidt-Nielsen, B., Gertz, K.H., Davis, L.E.: Excretion and ultrastructure of the antennal gland of the fiddler crab Uca mordax. J. Morph. 125, 473–495 (1968).Google Scholar
  91. Schmitt, F.O., Hall, C.E., Jakus, M.A.: Electron microscope investigations of the structure of collagen. J. cell. comp. Physiol. 20, 11–33 (1942).Google Scholar
  92. Smith, D.S.: Insect cells. Their structure and function, p. 171–181. Edinburgh: Oliver and Boyd Ltd. 1968.Google Scholar
  93. Stang-Voss, Ch.: Zur Ultrastruktur der Blutzellen wirbelloser Tiere. III. Über die Hämocyten der Schnecke Lymnea stagnalis L. (Pulmonata). Z. Zellforsch. 107, 142–156 (1970).Google Scholar
  94. Strangways-Dixon, J., Smith, D.S.: The fine structure of gill “podocytes” in Planulirus argus (Crustacea). Tissue and Cell 2 (4), 611–624 (1970).Google Scholar
  95. Thaemert, J.C.: The ultrastructure and the disposition of vesiculated nerve processes in smooth muscle. J. Cell Biol. 16, 361–377 (1963).Google Scholar
  96. Tyson, G.E.: The fine structure of the maxillary gland of the brine shrimp, Artemia salina: The end sac. Z. Zellforsch. 86, 129–138 (1968).Google Scholar
  97. Vigelius, W.J.: Über das Exkretionssystem der Cephalopoden. Niederl. Arch. Zool. 5, 115–184 (1880).Google Scholar
  98. Wilke, U.: Feinstruktur des Glomerulus von Glossobalanus minutus Kowalewsky (Enteropneusta). Cytobiol. 5, 439–447 (1972).Google Scholar
  99. Wolburg-Buchholz, K.: Blasenzellen im Bindegewebe des Schlundrings von Cepaea nemoralis L. (Gastropoda, Stylommatophora). I. Feinstruktur der Zellen. Z. Zellforsch. 128, 100–114 (1972).Google Scholar
  100. Wondrak, G.: Die Ultrastruktur der Zellen aus dem interstitiellen Bindegewebe von Arion rufus (L.), Pulmonata, Gastropoda. Z. Zellforsch. 95, 249–262 (1969).Google Scholar
  101. Yamada, E.: The fine structure of the renal glomerulus of the mouse. J. biophys. biochem. Cytol. 1 (6), 551–566 (1955).Google Scholar
  102. Zebe, E.: Feinbau und Funktionsweise der Muskeln in vergleichender Sicht. Zool. Anz. 30, Suppl. Bd. (1967).Google Scholar
  103. Zimmermann, K.W.: Über den Bau des Glomerulus der Säugerniere. Z. mikr.-anat. Forsch. 32, 176–278 (1933).Google Scholar

Copyright information

© Springer-Verlag 1973

Authors and Affiliations

  • Astrid Witmer
    • 1
  • Arthur W. Martin
    • 2
  1. 1.I. Zoologisches Institut der Freien Universität BerlinGermany
  2. 2.Department of ZoologyUniversity of WashingtonSeattle

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