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Experimental & Applied Acarology

, Volume 13, Issue 3, pp 187–212 | Cite as

Histochemical changes in the midgut of two ixodid tick speciesBoophilus microplus andRhipicephalus appendiculatus during digestion of the blood meal

  • A. D. Agyei
  • N. W. Runham
  • N. Blackstock
Article

Abstract

The changes in the midgut epithelia of two ixodid tick species,Boophilus microplus andRhipicephalus appendiculatus, have been studied using several histochemical techniques. It was revealed that there is an accumulation of RNA at the time of tick attachment to the host and prior to the arrival of the blood meal, indicating that the midgut digest cell is furnished with the machinery characteristic of a synthetic cell. There appears to be a synchrony in the appearance of granules with peroxidase activity and the uptake of haemoglobin into the midgut digest cells. Alkaline phosphatase activity was observed in the midgut epithelia of all ticks except in a few of the long-starved ticks, and was concentrated in the apical plasma membrane regions of those digest cells involved in absorption and the intracellular digestion of haemoglobin. The presence of these enzymes suggests that the midgut digest cell is a multifunctional cell capable of both secretory and digestive activities. The colloidal material in the midgut lumen was found to result from the accretion of several products both secreted and excreted by the midgut epithelial cells and exhibited different staining reactions depending on which component dominated. The nature of the material suggests that in addition to its digestive function it may serve as a sink to bind all the by-products of digestion and thereby facilitate their excretion.

Keywords

Alkaline Phosphatase Activity Blood Meal Tick Species Apical Plasma Membrane Ixodid Tick 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Agbede, R.I.S. and Kemp, D.H., 1985. Digestion in the cattle tickBoophilus microplus: Light microscope study of the gut cells in nymphs and females. Int. J. Parasitol., 15: 147–157.PubMedGoogle Scholar
  2. Agyei, A.D., 1985. Studies on the biology ofDermacentor reticulatus and a preliminary attempt to vaccinate rabbits against ticks. MSc. thesis, University of Wales, Bangor, 125 pp.Google Scholar
  3. Agyei, A.D., Herbert, I.V. and Runham, N.W., 1991. Histochemical localisation of acid phosphatase and non-specific esterase in the midguts of two ticks,Boophilus microplus andRhipicephalus appendiculatus as determined by light microscopy. Parasitol. Res., 77: 629–634.PubMedGoogle Scholar
  4. Anderson, E. and Harvey, W.R., 1966. Active transport byCecropia midgut (Lepidoptera). II. Fine structure of the midgut epithelium. J. Cell Biol., 31: 107–134.PubMedGoogle Scholar
  5. Arthur, D.R., 1962. Ticks and Disease, Pergamon Press. London.Google Scholar
  6. Balashov, Yu.S., 1972. Bloodsucking ticks (Ixodoidea): Vectors of diseases of man and animals. Entomol. Soc. Am. Misc. Publ., 8: 161–276.Google Scholar
  7. Balashov, Yu.S., 1984. Interaction between blood-sucking arthropods and their hosts and its influence on vector potential. Annu. Rev. Entomol., 29: 137–156.PubMedGoogle Scholar
  8. Bancroft, J.D. and Stevens, A., 1982. Theory and Practice of Histological Techniques. Churchill and Livingstone. Edinburgh, 680 pp.Google Scholar
  9. Bennion, P.J., Horobin, R.W. and Murgatroyd, L.B., 1975. The use of a basic dye (azure A or toluidine blue) plus a cationic surfactant for selective staining of RNA: A technical and mechanistic study. Stain Technol., 50: 307–313.PubMedGoogle Scholar
  10. Berridge, M.J., 1970. A structural analysis of absorption. In: E.I. Neville (Editor), Insect Ultrastructure. Symp. R. Entomol. Soc. Lond., 5: 135–151.Google Scholar
  11. Berridge, M.J. and Gupta, B.L., 1967. Fine structural changes in relation to ion and water transport in the rectal papillae of the blowfly,Calliphora. J. Cell Sci., 2: 89–112.PubMedGoogle Scholar
  12. Boctor, F.N. and Araman, S.F., 1971. Biochemical and physiological studies of certain ticks (Ixodoidea). Total free amino acids in gut, haemolymph and coxal fluids ofArgas (Persicargus) persicus (Oken) andA. (P.) arboreus Kaiser, Hoogstraal and Kohls (Argasidae). J. Med. Entomol., 8: 525–528.PubMedGoogle Scholar
  13. Boveris, A. and Chance, B., 1973. The mitochondrial generation of H2O2. General properties and effect of hyperbaric O2. Biochem. J., 134: 707–716.PubMedGoogle Scholar
  14. Brill, A.S., 1966. Peroxidases and catalase. In: M. Florkin and E.H. Stotz (Editors), Comprehensive Biochemistry, Vol. XIV. Amsterdam, NY, London, pp. 447–478.Google Scholar
  15. Callahan, H.L., Crouch, R.K. and James, E.R., 1988. Helminth with anti-oxidant enzymes: A protective mechanism against host oxidants. Parasitol. Today, 4: 218–225.PubMedGoogle Scholar
  16. Chapman, N., 1975. Dichromatism of bromophenol blue with an improvement in the mercuric bromophenol blue technic for protein. Stain Technol., 50: 25–30.PubMedGoogle Scholar
  17. Chinery, W.A., 1964. The mid-gut epithelium of the tick,Haemaphysalis spinigera Neumann, 1897. J. Med. Entomol., 1: 206–212.Google Scholar
  18. Chiu, D., Lubin, B.H. and Shohet, S.B., 1982. Peroxidase reactions in red cell biology. In: W.A. Pryor (Editor), Free Radicals in Biology. Academic Press, Ontario, pp. 115–154.Google Scholar
  19. Cook, H.C., 1974. Manual of Histological Demonstration Techniques. Butterworths, London.Google Scholar
  20. Coons, L.B., Tarnowski, B.I. and Ourth, D.D., 1982.Rhipicephalus appendiculatus: Localisation of vitellogenin synthesis by immunological methods and electron microscopy. Exp. Parasitol., 54: 331–339.PubMedGoogle Scholar
  21. Coons, L.B., Rosell-Davis, R. and Tarnowski, B.I., 1986. Blood meal digestion in ticks. In: J.R. Sauer and J.A. Hair (Editors), Morphology, Physiology and Behavioural Biology of Ticks. Ellis Horwood/John Wiley, New York, NY, pp. 248–279.Google Scholar
  22. Danielli, J.F., 1951. Cytochemistry: A Critical Approach. John Wiley, New York, NY/Chapman & Hall, London, 139 pp.Google Scholar
  23. Flohe, L., 1982. Role of GHH peroxidase in lipid peroxide metabolism. In: Kunio Yagi (Editor), Lipid Peroxides in Biology and Medicine. Academic Press, pp. 149–178.Google Scholar
  24. Gander, e., 1968. Zur Histologie und Histochemie des Mitteldarmes vonAedes aegypti undAnopheles stephensi in Zusammenhang mit der Blutverdauung. Acta Trop., 25: 133–175.PubMedGoogle Scholar
  25. Graham, R.C., Lundholm, U. and Karnovsky, M.J., 1965. Cytochemical demonstration of peroxidase with 3-amino-9-ethyl carbazole. J. Histochem. Cytochem., 19: 150–152.Google Scholar
  26. Grandjean, O. and Aeschlimann, A., 1973. Contribution to the study of digestion in ticks. Histology and fine structure of the midgut epithelium ofOrnithodorus moubata Murray (Ixodidae, Argasidae). Acta Trop., 30: 193–212.PubMedGoogle Scholar
  27. Hamdy, B.H., 1977. Biochemical and physiological studies of certain ticks (Ixodoidea). II. Excretion in ticks. J. Med. Entomol., 14: 14–18.Google Scholar
  28. Hughes, T.E., 1954. Some histological changes which occur in the epithelium ofIxodes ricinus females during gorging and up to oviposition. Ann. Trop. Med. Parasitol., 46: 54–60.Google Scholar
  29. Joyner, L.P. and Purnell, R.E., 1968. The feeding behaviour on rabbits and in vitro of the tickRhipicephalus appendiculatus Neumann 1901. Parasitology, 58: 715–723.PubMedGoogle Scholar
  30. Karnovsky, M.J., 1965. A glutaraldehyde/formaldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol., 27: 137 A.Google Scholar
  31. Kitaoka, S., 1961. Physiological and ecological studies. IV. Physiological stage and lipid deposit during the blood sucking process in the tick. Natl. Inst. Anim. Health Q., 1: 83–95.Google Scholar
  32. Lees, A.D., 1952. The role of cuticle growth in the feeding process of ticks. Proc. Zool. Soc. Lond., 121: 759–772.Google Scholar
  33. Lojda, Z., Gossrau, R. and Schiebler, T.H., 1979. Enzyme Histochemistry: A Laboratory Manual. Springer, Berlin, 339 pp.Google Scholar
  34. Mills, R.R., Wright, R.D. and Sauer, E.R., 1970. Midgut epithelium of the American cockcroach: Probable mechanics of water excretion. J. Insect. Physiol., 16: 417–427.PubMedGoogle Scholar
  35. Milne, E.M., 1985. The diagnostic value of alkaline phosphatase in canine medicine: a review. J. Small Anim. Pract., 26:267–278.Google Scholar
  36. Moog, F., 1946. The physiological significance of the phosphomonoesterases. Biol. Rev., 21: 46–59.Google Scholar
  37. Morgan, R.H., 1989. Lipid mobilization in midgut digest cells ofI. ricinus andH. punctata. British Society for Parasitology, Spring Meeting, 20–22 March, Southampton, P 60. (Abstract).Google Scholar
  38. Oschman, J.L. and Berridge, M.J., 1970. Structural and functional aspects of salivary fluid secretion inCalliphora. Tissue Cell, 2: 281–310Google Scholar
  39. Paget, T.A., Fry, M. and Lloyd, D., 1990.Nippostrongylus brasiliensis andAscaridia galli: Characterisation of peroxisomes. Exp. Parasitol., 71: 236–240.PubMedGoogle Scholar
  40. Pearse, A.G.E., 1980. Histochemistry. Theoretical and Applied, Vols. 1&2 (4th Edn.). Churchill & Livingstone, Edinburgh, 440 pp. & 615 pp.Google Scholar
  41. Puchtler, H. and Sweat, T., 1962. Amido Black as a stain for haemoglobin. Arch. Pathol., 73: 245–247.PubMedGoogle Scholar
  42. Raikhel, A.S., 1975. An electron microscope study of intracellular digestion in midgut cells of the tick,Hyalomma asiaticum. 1. The formation of primary and secondary lysosomes. Tsitologiya, 17: 748–753.Google Scholar
  43. Raikhel, A.S., 1978. An electron microscope study of intracellular digestion of midgut cells of the tickHyalomma asiaticum: Formation of residual bodies. Tsitologiya, 22: 142–148.Google Scholar
  44. Raikhel, A. S., 1983. The intestine. In: Yu.S. Balashov (Editor), An Atlas of Ixodid Tick Ultrastructure. Entomol. Soc. Am. Spec. Publ., pp. 59–97.Google Scholar
  45. 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.PubMedGoogle Scholar
  46. Roberts, J.A., 1968. Resistance of cattle to the tickBoophilus microplus (Canestrini). 1. Development of ticks onBos taurus. J. Parasitol., 54: 663–666.PubMedGoogle Scholar
  47. Roesler, R., 1934. Histologische, physiologische Untersuchungen über die Verdauung bei der ZeckengattungIxodes Latr. Z. Morphol. Oekol. Tiere, 28: 297–317.Google Scholar
  48. Saunders, B.C., Holmes-Siedle, A.G. and Stark, B.P., 1964. Peroxidase. Butterworths, London, 279 pp.Google Scholar
  49. Schellens, J.P.M., Daems, W.Th., Emeis, J.J., Brederoo, P., de Bruijn, W.C. and Wisse, E., 1977. Electron microscopical identification of lysosomes. In: J.T. Dingle (Editor), Lysosomes, a Laboratory Handbook. North-Holland, Amsterdam, pp. 147–208.Google Scholar
  50. Silverstein, S.C., Steinman, R.M. and Cohn, Z.A., 1976. Endocytosis. Annu. Rev. Biochem., 46: 669–722.Google Scholar
  51. Tarnowski, B.I. and Coons, L.B., 1989, Ultrastructure of the midgut and blood meal digestion in the adult tickDermacentor variabilis. Exp. Appl. Acarol., 6: 263–289.PubMedGoogle Scholar
  52. Tatchell, R.J., 1964. Digestion in the tickArgas persicus, Oken. Parasitology., 54: 423–440.PubMedGoogle Scholar
  53. Thomson, R.G., 1984. General Veterinary Pathology. W.B. Saunders, Philadelphia, 463 pp.Google Scholar
  54. Till, W.M., 1961. A contribution to the anatomy and histology of the brown car tickRhipicephalus appendiculatus Neumann. Mem. Entomol. Soc. S. Afr., 6: 1–124.Google Scholar
  55. Walker, A.R. and Fletcher, J.D., 1987. Histology of digestion in nymphs ofRhipicephalus appendiculatus fed on rabbits and cattle naive and resistant to the ticks. Int. J. Parasitol., 17: 1393–1411.PubMedGoogle Scholar
  56. Wigglesworth, V.B., 1943. The fate of haemoglobin inRhodnius prolixus (Hemiptera) and other blood sucking arthropods. Proc. R. Soc. Lond., 131: 313–339.Google Scholar

Copyright information

© Elsevier Science Publishers B.V. 1992

Authors and Affiliations

  • A. D. Agyei
    • 1
  • N. W. Runham
    • 1
  • N. Blackstock
    • 1
  1. 1.School of Biological SciencesUniv. Col. of North WalesBangorUK

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