An Electron Microscope Study of the Fate of Bacteria Phagocytized by Granulocytes of Crassostrea virginica

  • Thomas C. Cheng
  • Ann Cali


It is well established that the primary line of defense in molluscs, in all invertebrates for that matter, to foreign materials, biotic and abiotic, is what has been generally designated as cellular immunity (see Cheng, 1967, and Cheng and Rifkin, 1970, for reviews), although it could be argued that this may not be “immunity” sensu strictu since the involvement of antibodies in the form of immunoglobulins has not been demonstrated (Cheng, 1969, 1973). Nevertheless, as a rule, foreign elements, molecules, or organisms naturally or experimentally introduced into naive molluscs are phagocytized (Stauber, 1950; Tripp, 1958a, b, 1960, 1961; Feng, 1959, 1965; Arcadi, 1968; Cheng et al. 1969; Pauley and Krassner, 1972), encapsulated (Drew and De Morgan, 1910; Labbé, 1928, 1929, 1930; Newton, 1952, 1954; Brooks, 1953; Sudds, 1960;Mackin, 1961; Cheng and Rifkin, 1968), or nacrezized (Dubois, 1901, 1907; Perrier, 1903; Jameson, 1902; Giard, 1907; Alverdes, 1913; Nishikawa, 1917; Mikimoto, 1918; Tsujii, 1960). These appear to be highly efficient mechanisms for arresting and eliminating foreign materials, although exceptions are known (Naville, 1926; Goetsch and Scheuring, 1926; Yonge, 1936; Yonge and Nicholas, 1940; Prytherch, 1940; Mackin, 1951; Michelson, 1961; Feng, 1966; Feng and Stauber, 1968). In these instances, the foreign organisms are either not reacted against or are phagocytized but not degraded intracellularly. The reason(s) for these exceptions remains undetermined, although in the case of the organisms not reacted against, it is evident that the hosts do not recognize them as being nonself.


Electron Microscope Study Foreign Material Slime Mold Schistosoma Mansoni Crassostrea Virginica 
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  1. Altman, P. L. and Dittmer, D. S. (eds.), 1971, Respiration and Circulation, p. 930, Fed. Amer. Soc. Exp. Biol. Bethesda.Google Scholar
  2. Alverdes, F., 1913, Ueber Perlen und Perlbildung, Z. Wiss. Zool. 105: 598–633.Google Scholar
  3. Arcadi, J. A., 1968, Tissue response to the injection of charcoal into the pulmonate gastropod Lehmania poirieri, J. Invert. Pathol. 11: 59–62.CrossRefGoogle Scholar
  4. Brooks, C. P., 1953, A comparative study of Schistosoma mansoni in Tropicorbis havanensis and Australorbis glabratus, J. Parasitol. 39: 159–163.Google Scholar
  5. Cheng, T. C., 1966, The coracidium of the cestode Tylocephalum and the migration and fate of this parasite in the American oyster, Crassostrea virginica, Trans. Am. Microscop. Soc. 85: 246–255.CrossRefGoogle Scholar
  6. Cheng, T. C., 1967, Marine molluscs as hosts for symbioses with a review of known parasites of commercially important species, in: Advanced Marine Biology, Vol. 5, pp. 1–424 ( F. S. Russell, ed.), Academic Press, London.Google Scholar
  7. Cheng, T. C., 1969, An electrophoretic analysis of hemolymph proteins of the snail Helisoma duryi normale experimentally challenged with bacteria, J. Invert. Pathol. 14: 60–81.CrossRefGoogle Scholar
  8. Cheng, T. C., 1973, General Parasitology, Academic Press, New York.Google Scholar
  9. Cheng, T. C. and Cooperman, J. S., 1964, Studies on host-parasite relationships between larval trematodes and their hosts. V. The invasion of the reproductive system of Helisoma trivolvis by the sporocysts and cercariae of Glypthelmins pennsylvaniensis, Trans. Am. Microscop. Soc. 83: 12–23.CrossRefGoogle Scholar
  10. Cheng, T. C. and Foley, D. A., 1973, A scanning electron microscope study of the cytoplasmic granules of Crassostrea virginica granulocytes, J. Invert. Pathol. 19: 383–394.Google Scholar
  11. Cheng, T. C. and Lee, F. O., 1971, Glucose levels in the mollusc Biomphalaria glabrata infected with Schistosoma mansoni, J. Invert. Pathol. 18: 395–399.CrossRefGoogle Scholar
  12. Cheng, T. C. and Rifkin, E, 1968, The occurrence and resorption of Tylocephalum metacestodes in the clam Tapes semidecussata, J. Invert. Pathol. 10: 65–69.CrossRefGoogle Scholar
  13. Cheng, T. C. and Rifkin, E., 1970, Cellular reactions in marine molluscs in response to helminth parasitism, in: A Symposium on Diseases of Fishes and Shellfishes (S. F. Snieszko, ed.), Spec. Publ. No. 5, American Fisheries Society, Washington, D.C.Google Scholar
  14. Cheng, T. C., Shuster, C. N., Jr., and Anderson, A. H., 1966, A comparative study of the susceptibility and response of eight species of marine pelecypods to the trematode Himasthla quissetensis, Trans. Am. Microscop. Soc. 85: 284–295.CrossRefGoogle Scholar
  15. Cheng, T. C. Thakur, A. S., and Rifkin, E., 1969, Phagocytosis as an internal defense mechanism in the mollusca with an experimental study of the role of leucocytes in the removal of ink particles in Littorina scabra, Linn. Proc. Symp. Mollusca, Part II, pp. 546–563, The Bangalore Press, Bangalore, India.Google Scholar
  16. Cheng, T. C., Cali, A., and Foley, D. A., 1974, Cellular reactions in marine pelecypods as a factor influencing endosymbioses, in: Symbiosis in the Sea (W. A. Vernberg and F. J. Vernberg, eds. ), University of Southern Carolina Press,Google Scholar
  17. Chemin, E., 1962, The unusual life history of Daubaylia potomaca (Nematoda: Cephalobidae) in Australorbis glabratus and in certain other fresh-water snails, Parasitology, 52: 459–481.CrossRefGoogle Scholar
  18. Drew, G. H. and De Morgan, W., 1910, The origin and formation of fibrous tissue produced as a reaction to injury in Pecten maximus, as a type of the Lamellibranchiata, Quart. J. Microscop. Sci. 55: 595–620.Google Scholar
  19. Dubois, R., 1901, Sur le mécanisme de la formation des perles fines dans le Mytilus edulis, C.R. Hebd. Séanc. Acad. Sci. (Paris) 133: 603–605.Google Scholar
  20. Dubois, R., 1907, Action de la chaleur sur le distome immature de Gymnophallus margaritarum, C.R. Séanc. Soc. Biol. 63: 502–504.Google Scholar
  21. Feng, S. Y., 1959, Defense mechanism of the oyster, Bull. N.J. Acad. Sci. 4: 11.Google Scholar
  22. Feng, S. Y., 1965, Pinocytosis of proteins by oyster leucocytes, Biol. Bull. 128: 95–105.CrossRefGoogle Scholar
  23. Feng, S. Y., 1966, Experimental bacterial infections in the oyster Crassostrea virginica, J. Invert. Pathol. 8: 505–511.CrossRefGoogle Scholar
  24. Feng, S. Y. and Stauber, L. A., 1968, Experimental hexamitiasis in the oyster Crassostrea virginica, J. Invert. Pathol. 10: 94–110.CrossRefGoogle Scholar
  25. Feng, S. Y., Feng, J. S., Burke, C. N., and Khairallah, L. H., 1971, Light and electron microscopy of the leucocytes of Crassostrea virginica (Mollusca: Pelecypoda), Z. Zellforsch. 120: 222–245.PubMedCrossRefGoogle Scholar
  26. Foley, D. A. and Cheng, T. C., 1972, Interaction of molluscs and foreign substances: The morphology and behavior of hemolymph cells of the American oyster, Crassostrea virginica, in vitro, J. Invert. Pathol. 19: 383–395.CrossRefGoogle Scholar
  27. Galtsoff, P. S., 1964, The American oyster, Crassostrea virginica Gmelin. Fisheries Bull, Fish Wildlife Service U.S., 64: 1–480.Google Scholar
  28. Gezelius, K., 1959, The ultrastructure of cells and cellulose membranes in Acrasiae, Exptl. Cell Res. 18: 425–453.PubMedCrossRefGoogle Scholar
  29. Gezelius, K., 1961, Further studies in the ultrastructure of Acrasiae, Exp. Cell. Res. 23: 300–310.CrossRefGoogle Scholar
  30. Giard, 1907, Sur les trématodes margaritigènes du Pas-de-Calais (Gymnophallus somateriae Levinsen et G. bursicola Odhner), C.R. Séanc. Soc. Biol. 63: 416–420.Google Scholar
  31. Goetsch, W. and Scheuring, L., 1926, Parasitismus und Symbiose der Algengattung Corella, Z. Morphol. Oekol. Tiere 7: 220–253.CrossRefGoogle Scholar
  32. Hohl, H. R., 1965, Nature and development of membrane systems in food vacuoles of cellular slime molds predatory upon bacteria, J. Bacteriol. 90: 755–765.PubMedGoogle Scholar
  33. Holtz, F. and von Brand, T., 1940, Quantitative studies upon some blood constituents of Helix pomatia, Biol. Bull. 79: 423–431.CrossRefGoogle Scholar
  34. Jameson, H. L., 1902, On the origin of pearls, Proc. Zool. Soc. London 1: 140–166.Google Scholar
  35. Jullien, A., 1940, Sur les reactions des mollusques céphalopodes aux injections de goudron, C.R. Séanc. Soc. Biol. 210: 608–610.Google Scholar
  36. Labbé, A., 1928, Production expérimentale de tissue conjonctif par les amoebocytes chez Doris tuberculata L., C.R. Hebd. Sêanc. Acad. Sci. (Paris) 187: 1073–1075.Google Scholar
  37. Labbé, A., 1929, Reactions expérimentales des mollusques a l’introduction de stylets de celloidine, C.R. Séanc. Soc. Biol. 100: 166–168.Google Scholar
  38. Labbé, A., 1930, Réaction du tissu conjonctif au goudron chez un mollusque: Doris tuberculata Cuvier, C.R. Séanc. Soc. Biol. 103: 20–22.Google Scholar
  39. Mackin, J. G., 1951, Histopathology of infection of Crassostrea virginica (Gmelin) by Dermocystidium marinum Mackin, Owen, and Collier, Bull. Marine Sci. Gulf Caribbean 1: 72–87.Google Scholar
  40. Mackin, J. G., 1961, Oyster leucocytes in infectious disease, Am. Zool. 1: 371.Google Scholar
  41. Mercer, E. H. and Shaffer, B. M., 1960, Electron microscopy of solitary and aggregated slime mold cells, J. Biophys. Biochem. Cytol. 7: 353–356.PubMedCrossRefGoogle Scholar
  42. Michelson, E. H., 1961, An acid-fast pathogen of fresh-water snails, Am. J. Trop. Med. Hyg. 10: 423–421.PubMedGoogle Scholar
  43. Mikimoto, K., 1918 (Cited in Tsujii, T., 1960 ), Studies on the mechanism of shell- and pearl-formation in Mollusca, J. Fac. Fisheries Prefect. Univ. Mie 5: 1–70.Google Scholar
  44. Naville, A., 1926, Notes sur les Eolidiens. Un Eolidien d’eau saumatre. Origine des nématocytes. Zooxanthelles et homochromie. Rev. Suisse Zool. 33: 251–289.Google Scholar
  45. Newton, W. L., 1952, The comparative tissue reaction of two strains of Australorbis glabratus to infection with Schistosoma mansoni, J. Parasitol. 38: 362–366.CrossRefGoogle Scholar
  46. Newton, W. L., 1954, Tissue response to Schistosoma mansoni in second generation snails from a cross between two strains of Australorbis glabratus, J. Parasitol. 40: 1–4.Google Scholar
  47. Nishikawa, T., 1917 (Cited in Tsujii, T., 1960 ), Studies on the mechanism of shell-and pearl-formation in Mollusca, J. Fac. Fisheries Prefect. Univ. Mie 5: 1–70.Google Scholar
  48. Pauley, G. B. and Krassner, S. M., 1972, Cellular defense reactions to particulate materials in the California sea hare, Aplysia californica, J. Invert. Pathol. 19: 18–27.CrossRefGoogle Scholar
  49. Perrier, E., 1903, Remarques de M. Edm. Perrier à propos de la communication de M. Raphaël Dubois, de 19 Octobre dernier, “sur les huîtres perlières vraies,” Compt. Rend. 137: 682.Google Scholar
  50. Prytherch, H. F., 1940, The life cycle and morphology of Nematopsis ostrearum sp. nov., a gregarine parasite of the mud crab and oyster, J. Morphol. 66: 39–64.CrossRefGoogle Scholar
  51. Reynolds, E. S., 1963, The use of lead citrate at high pH as an electron opaque stain in electron microscopy, J. Cell Biol. 17: 208–212.PubMedCrossRefGoogle Scholar
  52. Stauber, L. A., 1950, The fate of India ink injected intracardially into the oyster Ostrea virginica Gmelin, Biol. Bull. 98: 221–241.CrossRefGoogle Scholar
  53. Sudds, R. H., Jr., 1960, Observations on schistosome miracidial behavior in the presence of normal and abnormal snail hosts and subsequent tissue studies of these hosts, J. Elisha Mitchell Sci. Soc. 76: 121–133.Google Scholar
  54. Swift, H. and Hruban, Z., 1964, Focal degradation as a biological process, Federation Proc. 23: 1026–1037.Google Scholar
  55. Tripp, M. R., 1958a, Disposal by the oyster of intracardially injected red blood cells of vertebrates, Proc. Nat. Shellfisheries Assoc. 48: 143–141.Google Scholar
  56. Tripp, M. R., 1960, Mechanisms of removal of injected microorganisms from the American oyster, Crassostrea virginica (Gmelin), Biol. Bull. 119: 210–223.CrossRefGoogle Scholar
  57. Tripp, M. R., 1961, The fate of foreign materials experimentally introduced into the snail Australorbis glabratus, J. Parasitol. 47: 745–751.Google Scholar
  58. Tsujii, T., 1961, Studies on the mechanism of shell- and pearl-formation in Mollusca, J. Fac. Fisheries Prefect. Univ. Mie 5: 1–70.Google Scholar
  59. Yonge, C. M., 1926, Structure and physiology of the organs of feeding and digestion in Ostrea edulis, J. Marine Biol. Assoc. U.K. 14: 295–386.CrossRefGoogle Scholar
  60. Yonge, C. M., 1936, Mode of life, feeding, digestion, and symbiosis with zooxanthellae in the Tridacnidae, Sci. Rep. Great Barrier Reef Exped. 1: 283–321.Google Scholar
  61. Yonge, C. M. and Nicholas, H. M., 1940, Structure and function of the gut and symbiosis with zoothanthellae in Tridacna crispata (Oerst.), Bgk. Papers Tortugas Lab. Carnegie Inst. 32: 287–301.Google Scholar

Copyright information

© Plenum Press, New York 1974

Authors and Affiliations

  • Thomas C. Cheng
    • 1
  • Ann Cali
    • 1
  1. 1.Institute for Pathobiology Center for Health SciencesLehigh UniversityBethlehemUSA

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