Hostname: page-component-848d4c4894-nmvwc Total loading time: 0 Render date: 2024-06-19T01:04:47.859Z Has data issue: false hasContentIssue false
  • English
  • Français

Morphological characterization of the haemocytes of the ivory snail, Babylonia areolata (Neogastropoda: Buccinidae)

Published online by Cambridge University Press:  01 February 2011

G.L. Di ,
Z.X. Zhang ,
C.H. Ke ,
J.R. Guo ,
M. Xue ,
J.B. Ni  and
D.X. Wang
G.L. Di
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Oceanography and Environmental Science, Xiamen University, Xiamen, 361005, China
Z.X. Zhang
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Oceanography and Environmental Science, Xiamen University, Xiamen, 361005, China
C.H. Ke*
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Oceanography and Environmental Science, Xiamen University, Xiamen, 361005, China
J.R. Guo
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Oceanography and Environmental Science, Xiamen University, Xiamen, 361005, China
M. Xue
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Oceanography and Environmental Science, Xiamen University, Xiamen, 361005, China
J.B. Ni
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Oceanography and Environmental Science, Xiamen University, Xiamen, 361005, China
D.X. Wang
Affiliation:
State Key Laboratory of Marine Environmental Science, College of Oceanography and Environmental Science, Xiamen University, Xiamen, 361005, China
*
Correspondence should be addressed to: C.H. Ke, State Key Laboratory of Marine Environmental Science, College of Oceanography and Environmental Science, Xiamen University, Xiamen, 361005, China email: chke@xmu.edu.cn.
Get access Rights & Permissions [Opens in a new window]

Abstract

The nucleus diameter/cell diameter (N/C) ratio and morphological characteristics of the haemocytes of the snail Babylonia areolata were studied using microscopy. Our results revealed two major types of haemocytes, namely granulocytes and hyalinocytes. In granulocytes, the cytoplasm was purplish red with Wright's staining, but it was blue in hyalinocytes. Hyalinocytes were smaller than granulocytes and had a higher N/C ratio. The granulocytes were sub-categorized into type I granulocytes and type II granulocytes based on the shape and the number of granules. Hyalinocytes were sub-categorized into large and small hyalinocytes based on the diameter and N/C ratio. Snails with a shell length from 2.7 to 3.3 cm showed no differences in the abundance of haemocytes.

Keywords

Babylonia areolatahaemocytesmorphologyclassification
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 7 , November 2011 , pp. 1489 - 1497
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Adamowicz, A. and Bolaczek, M. (2003) Blood cells morphology of the snail Helix aspersa maxima (Helicidae). Zoologica Poloniae 48, 93–101.Google Scholar
Adema, C.M., Harris, R.A. and Van Deutekom-Mulder, E.C. (1992) A comparative study of hemocytes from six different snails: morphology and functional aspects. Journal of Invertebrate Pathology 59, 24–32.CrossRefGoogle ScholarPubMed
Adema, C.M., Mohandas, A., Van Der Knaap, W.P. and Sminia, T. (1994) Separation of Lymnaea stagnalis haemocytes by density gradient centrifugation. Developmental and Comparative Immunology 18, 25–31.CrossRefGoogle Scholar
Armstrong, D.A., Armstrong, J.L., Krassner, S.M. and Pauley, G.B. (1971) Experimental wound repair in the black abalone, Haliotis cracherodii. Journal of Invertebrate Pathology 17, 216–227.CrossRefGoogle ScholarPubMed
Barracco, M.A., Steil, A.A. and Gargioni, R. (1993) Morphological characterization of the hemocytes of the pulmonate snail Biomphalaria tenagophila. Memórias Instituto Oswaldo Cruz 88, 73–83.Google Scholar
Bayne, C.J. (1983) Molluscan immunobiology. In Saleuddin, A.S.M. and Wilbur, K.M. (eds) ‘The Mollusca’, Volume 5, physiology, part 2. New York: Academic Press, pp. 407–486.Google Scholar
Bender, R.C., Broderick, E.J., Goodall, C.P. and Bayne, C.J. (2005) Respiratory burst of Biomphalaria glabrata hemocytes: Schistosoma mansoni-resistant snails produce more extracellular H2O2 than susceptible snails. Journal of Parasitology 91, 275–279.Google Scholar
Cheng, T.C. (1975) Functional morphology and biochemistry of molluscan phagocytes. Annals of the New York Academy of Sciences 266, 343–379.Google Scholar
Cheng, T.C. (1981) Bivalves. In Ratcliffe, N.A. and Rowley, A.F. (eds) Invertebrate blood cells. London: Academic Press, pp. 233–299.Google Scholar
Cheng, T.C. (1984) A classification scheme of molluscan hemocytes based on functional evidences. In Bullo, L.A. and Cheng, T.C. (eds) Comparative pathology. New York: Plenum Press, pp. 111–146.Google Scholar
Chen, J.H., Yang, H.Y., Peng, S.W., Chen, Y.J. and Tsai, K.Y. (1996) Characterization of abalone (Haliotis diversicolor) hemocytes in vitro. Biology Bulletin 31, 31–38.Google Scholar
Cima, F., Matozzo, V., Marin, M.G. and Ballarin, L. (2000) Haemocytes of the clam Tapes philippinarum (Adams & Reeve, 1850): morphofunctional characterisation. Fish and Shellfish Immunology 10, 677–693.Google Scholar
Cossarizza, A., Pinti, M., Troiano, L. and Cooper, E. (2005) Flow cytometry as a tool for analyzing invertebrate cells. Invertebrate Survival Journal 2, 32–40.Google Scholar
Cuénot, L. (1891) Études sur le sang et les glandes lymphatiques dans la série animale. Archives de Zoologie Experimentale et Générale (Série 2) 9, 13–90.Google Scholar
Davies, P.S. and Partridge, T. (1972) Limpet haemocytes studies on aggregation and spike formation. Journal of Cell Science 11, 757–769.Google Scholar
Dikkeboom, T., Tijnagel, J.M. and Van Der Knaap, W.P.W. (1988) Monoclonal antibodies recognize hemocyte subpopulations in juvenile and adult Lynmaea stagnalis: functional characteristics and lectin binding. Developmental and Comparative Immunology 12, 17–32.Google Scholar
Donaghy, L., Hong, H.-K., Lambert, C., Park, H.-S., Shim, W.J. and Choi, K.-S. (2010) First characterisation of the populations and immune-related activities of hemocytes from two edible gastropod species, the disk abalone, Haliotis discus discus and the spiny top shell, Turbo cornutus. Fish and Shellfish Immunology 28, 87–97.Google Scholar
Feng, Y.Q., Zhou, Y.C., Xie, Z.Y., Pu, L.Y., Lu, N., Lin, Z.Y., Zhou, J.X. and Fu, X.Y. (2008) Studies on the techniques of healthy culture for Babylonia areolata. Chinese Fishery Modernization 35, 39–41.Google Scholar
Gopalakrishnan, S., Thilagam, H., Huang, W.B. and Wang, K.J. (2009) Immunomodulation in the marine gastropod Haliotis diversicolor exposed to benzo (a) pyrene. Chemosphere 75, 389–397.Google Scholar
Gorbushin, A.M. and Iakovleva, N.V. (2006) Haemogram of Littorina littorea. Journal of the Marine Biological Association of the United Kingdom 86, 1175–1181.Google Scholar
Granath, W.O. and Yoshino, T.P. (1983) Characterisation of molluscan phagocyte subpopulations based on lysosomal enzymes markers. Journal of Experimental Zoology 226, 205–210.CrossRefGoogle Scholar
Hahn, U.K., Bender, R.C. and Bayne, C.J. (2000) Production of reactive oxygen species by hemocytes of Biomphalaria glabrata: carbohydrate-specific stimulation. Developmental and Comparative Immunology 24, 531–41.Google Scholar
Hine, P.M. (1999) The inter-relationships of bivalve haemocytes. Fish and Shellfish Immunology 9, 367–385.CrossRefGoogle Scholar
Humphries, J.E. and Yoshino, T.P. (2008) Regulation of hydrogen peroxide release in circulating hemocytes of the planorbid snail Biomphalaria glabrata. Developmental and Comparative Immunology 32, 554–62.CrossRefGoogle ScholarPubMed
Jing, X. and Wenbin, Z. (2005) Characterisation of monoclonal antibodies to haemocyte types of scallop (Chlamys farreri). Fish and Shellfish Immunology 19, 17–25.Google Scholar
Kumazawa, H., Tanigawa, T., Tanaka, Y., Osatake, H. and Tanaka, K. (1990) Preliminary study on culture and morphology of hemocytes of two gastropod molluscs Clithon retropictus and Nerita albicilla. Venus (Japanese Journal of Malacology) 49, 233–239.Google Scholar
Kumazawa, N.H., Tanigawa, T., Kasagi, N. and Tanaka, Y. (1991) Characterization of hemocytes of an estuarine gastropod mollusk Clithon retropictus, based on lysosomal enzymes. Journal of Veterinary Medical Science 53, 725–726.Google Scholar
Leippe, M. and Renwrantz, L. (1988) Release of cytotoxic and agglutinating molecules by Mytilus hemocytes. Developmental and Comparative Immunology 12, 297–308.Google Scholar
Mahilini, H.M. and Rajendran, A. (2008) Categorization of hemocytes of three gastropod species Trachea vittata (Müller), Pila globosa (Swainson) and Indoplanorbis exustus (Dehays). Journal of Invertebrate Pathology 97, 20–26.Google Scholar
Malham, S.K., Lacoste Gélébart, F., Cueff, A. and Poulet, S.A. (2003) Evidence for a direct link between stress and immunity in the mollusk Haliotis tuberculata. Journal of Experimental Zoology 295A, 136–144.CrossRefGoogle Scholar
Martello, L.B., Friedman, C.S. and Tjeedema, R.S. (2000) Combined effects of pentachlorophenol and salinity stress on phagocytic and chemotactic function in two species of abalone. Aquatic Toxicology 49, 213–225.Google Scholar
Martello, L.B. and Tjeerdema, R.S. (2001) Combined effects of pentachorophenol and salinity stress on chemiluminescence activity in two species of abalone. Aquatic Toxicology 51, 351–362.Google Scholar
Martin, G.G., Oakes, C.T., Tousignant, H.R., Crabtree, H. and Yamakawa, R. (2007) Structure and function of haemocytes in two marine gastropods, Megathura crenulata and Aplysia californica. Journal of Molluscan Studies 73, 355–365.Google Scholar
Matricon-Gondran, M. and Letocart, M. (1999a) Internal defenses of the snail Biomphalaria glabrata. Journal of Invertebrate Pathology 74, 224–234.Google Scholar
Matricon-Gondran, M. and Letocart, M. (1999b) Internal defenses of the snail Biomphalaria glabrata. III. Observations on tubular helical filaments induced in the hemolymph by foreign material. Journal of Invertebrate Pathology 74, 248–254.Google Scholar
Mitta, G., Vandenbulcke, F., Hubert, F., Salzet, M. and Roch, P. (2000) Involvement of mytilins in mussel antimicrobial defense. Journal of Biological Chemistry 275, 954–962.Google Scholar
Monteil, J.F. and Matricon-Gondran, M. (1993) Structural and cytochemical study of hemocytes in normal and trematode infected Lymnaeatruncatula. Parasitology Research 79, 675–682.Google Scholar
Narain, A.S. (1973) The amoebocytes of lamellibranch molluscs, with special reference to the circulating amoebocytes. Malacology Review 6, 1–12.Google Scholar
Ottaviani, E. (1992) Immunorecognition in the gastropod molluscs with particular reference to the freshwater snail Planorbarius corneus (L.) (Gastropoda, Pulmonata). Bollettino di Zoologia 59, 129–139.Google Scholar
Pauley, G.B., Krassner, S.M. and Chapman, F.A. (1971) Bacterial clearance in the California sea hare, Aplysia californica. Journal of Invertebrate Pathology 18, 227–230.Google Scholar
Poncet, J.M. and Lebel, J.M. (2003) Influence of cryoprotective agent and cooling rate on frozen and thawed hemocytes from the mollusk Haliotis tuberculata. Cryobiology 47, 184–189.Google Scholar
Renwrantz, L. and Stahmer, A. (1983) Opsonising properties of an isolated hemolymph agglutinin and demonstration of lectin-like recognition molecules at the surface of hemocytes from Mytilus edulis. Journal of Comparative Physiology 149, 535–546.Google Scholar
Russo, J. and Lagadic, L. (2004) Effects of environmental concentrations of atrazine on hemocyte density and phagocytic activity in the pond snail Lymnaea stagnalis (Gastropoda, Pulmonata). Environmental Pollution 127, 303–311.Google Scholar
Russo, J. and Madec, L. (2007) Haemocyte apoptosis as a general cellular immune response of Lymnaea stagnalis (Gastropoda, Pulmonata) to a toxicant. Cell and Tissue Research 328, 431–441.Google Scholar
Russo, J., Madec, L. and Brehélin, M. (2008) Effect of a toxicant on phagocytosis pathways in the freshwater snail Lymnaea stagnalis. Cell and Tissue Research 333, 147–158.Google Scholar
Sahaphong, S., Linthong, V., Wanichanon, C., Riengrojpitak, S., Kangwanrangsan, N., Viyanant, V., Upatham E., S., Pumthong, T., Chansue, N. and Sobhon, P. (2001) Morphofunctional study of the haemocytes of Haliotis asinina. Journal of Shellfish Research 20, 711–717.Google Scholar
Schoenberg, D.A. and Cheng, T.C. (1980) Lectin-binding specificities of two strains of Biomphalaria glabrata as demonstrated by microhaemabsorption assays. Developmental and Comparative Immunology 4, 617–628.Google Scholar
Serpentini, A., Ghayor, C.Poncet, J.M., Hebert, V., Galera, P., Pujol, J.P., Boucaud-Camou, E. and Lebel, J.M. (2000) Collagen study and regulation of the de novo synthesis by IGF-1 hemocytes from the gastropod mollusk, Haliotis tuberculata. Journal of Experimental Zoology 287, 275–284.Google Scholar
Sminia, T. (1972) Structure and function of blood and connective tissue cells of the freshwater pulmonate Lymnaea stagnalis studied by electron microscopy and enzyme histochemistry. Zeitschrift für Zellforschung und Mikroskopische Anatomie 130, 497–526.Google Scholar
Sminia, T. (1974) Hematopoiesis in the freshwater snail Lymnea stagnalis studied by electron microscopy and autoradiography. Cell and Tissue Research 150, 443–454.Google Scholar
Sminia, T. and Barendsen, L.H. (1980) A comparative morphological and enzyme histochemical study on blood cells of the freshwater snails Lymnaea stagnalis, Biomphalaria glabrata and Bulinus truncates. Journal of Morphology 165, 31–39.Google Scholar
Sminia, T., Van Der Knaap, W.P. and Boerrigter-Barendsen, L.H. (1982) Peroxidase-positive blood cells in snails. Journal of the Reticuloendothelial Society 31, 339–404.Google Scholar
Sparks, A.K. and Morado, J.F. (1988) Inflammation and wound repair in bivalve molluscs. American Fisheries Society Special Publication 18, 139–152.Google Scholar
Takatsuki, S. (1934) On the nature and functions of the amoebocytes of Ostrea edulis. Quarterly Journal of Microscopical Science 76, 379–431.Google Scholar
Travers, M.A., Mirella Da Silva, P., Le Goïc, N., Marie, D., Donval, A., Huchette, S., Koken, M. and Paillard, C. (2008) Morphologic, cytometric and functional characterisation of abalone (Haliotis tuberculata) haemocytes. Fish and Shellfish Immunology 24, 400–411.Google Scholar
Wright, B., Lacchini, A.H., Davies, A.J. and Walker, A.J. (2006) Regulation of nitric oxide production in Lymnaea stagnalis defence cells: a role for protein kinase C and extracellular signal-regulated kinase signalling pathways. Biology of the Cell 98, 265–278.Google Scholar
Voltzow, J. (1994) Gastopoda: Prosobranchia. In Harrison, F.W. and Kohn, A.J. (eds) Microscopic anatomy of invertebrates. New York: Wiley-Liss, Inc., pp. 111–252.Google Scholar
Yonow, N. and Renwrantz, L. (1986) Studies on the hemocytes of Acteon tornatilis (L.) (Opisthobranchia: Acteonidae). Journal of Molluscan Studies 52, 150–155.Google Scholar
Yoshino, T.P. and Granath, W.O. Jr (1985) Surface antigens of Biomphalaria glabrata (Gastropoda) hemocytes: functional heterogeneity in cell populations recognized by a monoclonal antibody. Journal of Invertebrate Pathology 45, 174–186.Google Scholar