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Experimental & Applied Acarology

, Volume 6, Issue 4, pp 263–289 | Cite as

Ultrastructure of the midgut and blood meal digestion in the adult tickDermacentor variabilis

  • Betty I. Tarnowski
  • Lewis B. Coons
Article

Abstract

Digestive cells in the midgut of male and femaleDermacentor variabilis (Say) took up the blood meal in coated vesicles and smooth flask-shaped vesicles, and deposited it in endosomes which were digested via heterophagy. Iron was concentrated in residual bodies.

Digestion occurred in three distinct phases in mated females: (1) continuous digestion (initiated by feeding) occurred during slow engorgement; (2) reduced digestion (initiated by mating) occurred in mated females during the period of rapid engorgement; (3) a second continuous digestion phase (initiated by detachment from the host) occurred throughout the post-feeding periods of preoviposition and oviposition.

It is proposed that the stem cells in the midguts of unfed females were progenitors of digestive, replacement, and presumed vitellogenic cells in midguts of mated feeding females. Digestive cells were present in all three digestion phases. Only during the first continuous digestion phase did digestive cells fill up with residual bodies, rupture and slough into the lumen, or did whole cells slough into the lumen. During the other two digestion phases no sloughing of digestive cells was observed. At the end of oviposition the digestive cells were filled with residual bodies. Replacement cells were present only during the first continuous-digestion phase. Presumed vitellogenic cells were present only during the reduced-digestion phase and during the second continuous-digestion phase. Stem cells in unfed males developed only into digestive cells in feeding males. Fed males and fed unmated females had only the first continuous-digestion phase. After being hand-detached from the host, unmated 13-day-fed females went through cellular changes associated with the reduced-digestion phase and second continuous-digestion phase of fed mated females, then began ovipositing. Maximum development of the basal labyrinth system and lateral spaces matched the known time of maximum water and ion movement across the midgut epithelia.

Spectrophotometric analyses of lumen contents and midgut cells, sampled after detachment from the host, showed that concentrations of protein and hemoglobin at day 1 post-detachment decreased by one-half at the beginning of oviposition, while hematin increased about twofold by the end of oviposition. This supported the idea of the presence of a second continuous-digestion phase.

Keywords

Blood Meal Residual Body Hematin Digestive Cell Midgut Epithelium 
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. Ackerman, S., Brain Clare, F., McGill, T. W. and Sonenshine, D. E., 1981. Passage of host serum components, including antibodies, across the digestive tract ofDermacentor variabilis (Say). J. Parasitol., 67: 373–380.Google Scholar
  2. Aeschlimann, A. and Grandjean, O., 1973. Influence of natural and ‘artificial’ mating on feeding, digestion, vitellogenesis and oviposition in ticks (Ixodoidea). Folia Parasitol., 20: 67–74.Google Scholar
  3. Agbede, R., 1986. Scanning electron microscopy of digest cells in the midgut epithelium ofBoophilus microplus. Exp. Appl. Acarol., 2: 329–335.Google Scholar
  4. Agbede, R. and Kemp, D., 1985. Digestion in the cattle-tickBoophilus microplus: light microscope study of the gut cells in nymphs and females. Int. J. Parasitol., 15: 147–157.Google Scholar
  5. Agbede, R. and Kemp, D., 1986. Immunization of cattle againstBoophilus microplus using extracts derived from adult female ticks: Histopathology of ticks feeding on vaccinated cattle. Int. J. Parasitol.,16: 35–41.Google Scholar
  6. Agbede R. and Kemp, D., 1987. Ultrastructure of secretory cells in the gut of the cattle-tickBoophilus microplus. Int. J. Parasitol., 17: 1089–1098.Google Scholar
  7. Agbede, R., Kemp, D. and Hoyte, H., 1986. Secretory and digest cells of femaleBoophilus microplus: Invasion and development ofBabesia bovis; light and electron microscope studies. In: J. Sauer and J. Hair (Editors), Morphology, Physiology, and Behavioral Biology of Ticks. Ellis Horwood, Chichester, pp. 457–471.Google Scholar
  8. Akov, S., 1982. Blood digestion in ticks. In: F. Obenchain and R. Galun (Editors), Physiology of Ticks. Pergamon Press, Oxford, pp. 197–211.Google Scholar
  9. Araman, S., 1979. Protein digestion and synthesis in ixodid females. In: J. Rodriguez (Editor), Recent Advances in Acarology, Vol. 1. Academic Press, New York, pp. 385–395.Google Scholar
  10. Balashov, Y., 1972. Bloodsucking Ticks (Ixodoidea), Vectors of Diseases to Man and Animals. Akad. Nauk SSSR Zool. Inst. Leningrad (in Russian). Entomol. Soc. Am. Misc. Publ., 8: 161–376. (in English).Google Scholar
  11. Belozerov, V. and Tymopheev, V., 1971. An electron-microscope investigation of the midgut epithelium of the adult female ofDermacentor marginatus Sulz. In: M. Daniel (Editor), Proc. 3rd International Congress of Acarology, 31 August–6 September 1971, Prague. Dr. W. Junk, The Hague, pp. 707–714.Google Scholar
  12. Ben-Yakir, D., Fox, J. C., Homer, J. T. and Barker, R. W., 1986. Quantitative studies of host immunoglobulin G passage into the hemocoel of the ticksAmblyomma americanum andDermacentor variabilis. In: J. R. Sauer and J. A. Hair (Editors), Morphology, Physiology, and Behavioral Biology of Ticks. Ellis Horwood, Chichester, pp. 329–341.Google Scholar
  13. Bogin, E. and Hadani, A., 1973. Digestive enzymes in ‘hard ticks’ (Ixodoidea, Ixodidae). I. Proteolytic enzyme activity in the gut ofHyalomma excavatum female ticks. Z. Parasitenkd., 41: 139–146.Google Scholar
  14. Bradley, T. J., 1985. The excretory system: Structure and physiology. In: G. A. Kerkut and L. I. Gilbert (Editors), Comprehensive Insect Physiology, Biochemistry and Pharmacology, Vol. 4. Regulation: Digestion, Nutrition, Excretion. Pergamon, New York, pp. 421–465.Google Scholar
  15. Brossard, M. and Rais, O., 1984. Passage of hemolysins through the midgut epithelium of femaleIxodes ricinus L. fed on rabbits infested or reinfested with ticks. Experientia, 40: 561–563.Google Scholar
  16. Chinery, W., 1964. The midgut epithelium of the tickHaemaphysalis spinigera Neumann, J. Med. Entomol., 1: 206–212.Google Scholar
  17. Coons, L., Tarnowski, B., Ourth, D., 1982.Rhipicephalus sanguinius: localization of vitellogenin synthesis by immunological methods and electron microscopy. Exp. Parasitol., 54: 331–339.Google Scholar
  18. Coons, L., Lamoreaux, W., Rosell-Davis, R. and Starr-Spires, L., 1986a. Ultrastructure of fat body trophocytes in the life stages ofDermacentor variabilis (Say). Proc. EMSA, 44: 314–315.Google Scholar
  19. Coons, L. B., Rosell-Davis, R. and Tarnowski, B. I., 1986b. Blood meal digestion in ticks. In: J. R. Sauer and A. J. Hair (ittors), Morphology, Physiology, and Behavioral Biology of Ticks. Ellis Horwood, Chichester, pp. 248–279.Google Scholar
  20. Coons, L. B., Lamoreaux, W. J., Rosell-Davis, R., and Tarnowski, B. I., 1989. Onset of vitellogenin production and vitellogenesis, and their relationship to changes in the midgut epithelium and oocytes in the tickDermacentor variabilis. Exp. Appl. Acarol., 6: 291–305.Google Scholar
  21. Ellmann, G., 1962. The biuret reaction: changes in the ultraviolet absorption spectra and its application to the determination of peptide bonds. Anal. Biochem., 3:40–44.Google Scholar
  22. Fain-Maurel, M. A. and P. Cassier, 1972. Une nouveau type de jonctions: les jonctions scalariformes. Étude ultrastructurale et cytochimique. J. Ultrastruct. Res., 39: 222–238.Google Scholar
  23. Fujisaki, K., Kamio, T. and Kitaoka, S., 1984. Passage of host serum components, including antibodies specific forTheileria sergenti, across the digestive tract of argasid and ixodid ticks. Ann. Trop. Med. Parasitol., 78: 449–450.Google Scholar
  24. Grandjean, O., 1983. Blood digestion inOrnithodoros moubata Murray sensu stricto Walton females (Ixodoidea: Argasidae). II. Modification of midgut cells related to the digestive cycle and to the triggering action of mating. Ann. Parasitol. Hum. Comp., 58: 493–514.Google Scholar
  25. Grandjean, O., 1984. Blood digestion inOrnithodoros moubata Murray sensu stricto Walton females (Ixodoidea: Argasidae). I. Biochemical changes in the midgut lumen and ultrastructure of midgut cell, related to intracellular digestion. Acarologia, 25: 147–165.Google Scholar
  26. Holtzman, E., 1976. Lysosomes: A survey. In: M. Alfert, W. Deermann, G. Rudkin, W. Sandritter and P. Sitte (Editors), Cell Biology Monographs. Continuation of Protoplasmatologia, Vol. 3. Springer, New York, 298 pp.Google Scholar
  27. Hoogstraal, H., 1978. Biology of ticks. In: J. K. H. Wilde (Editor), Tickborne Diseases and their Vectors. Proc. Int. Conf., Univ. of Edinburgh, 27 September–1 October 1976. Univ. of Edinburgh, Centre for Tropical Veterinary Medicine, Edinburgh, pp. 3–14.Google Scholar
  28. Hughes, T., 1954. Some histological changes which occur in the gut epithelium ofIxodes ricinus females during engorging and up to oviposition. Ann. Trop. Med. Parasitol., 48: 397–404.Google Scholar
  29. Jaworski, D. C., Barker, D. M., Williams, G. P., Sauer, J. R., Ownby, C. L., and Hair, J. A., 1983. Age-related changes in midgut ultrastructure and surface tegument of unfed adult lone star ticks. J. Parasitol., 69: 701–708.Google Scholar
  30. Jennrich, R., Sampson, P. and Frane, J., 1983. Analysis of variance and covariance including repeated measures. In: W. J. Dixon (Editor), BMDP Statistical Software. Univ. California Press, Berkeley, pp. 359–387.Google Scholar
  31. Kaufman, W. R., and Philips, J., 1973. Ion and water balance in the ixodid tickDermacentor andersoni. I. Routes of ion and water excretion. J. Exp. Biol., 58: 523–536.Google Scholar
  32. Kim, J.-O. and Kohout, F. J., 1975. Analysis of variance and covariance: Subprograms ANOVA and ONEWAY. In: N. H. Nie, C. H. Hull, J. G. Jenkins, K. Streinbrenner and D. H. Bent (Editors), Statistical Package for the Social Sciences, 2nd Edition. McGraw-Hill, New York, pp. 398–433.Google Scholar
  33. Kirk, R., 1983. Current Veterinary Therapy. VIII. Small Animal Therapy. W. B. Saunders, Philadelphia, 1268 pp.Google Scholar
  34. Koch, H. G., Sauer, J. R. and Hair, J. A., 1974. Concentration of the ingested meal in four species of hard ticks. Ann. Entomol. Soc. Am., 67: 861–866.Google Scholar
  35. Lane, N., 1982, Insect intercellular junctions: their structure and development. In: R. King and H. Akai (Editors), Insect Ultrastructure, Vol. 1. Plenum Press, New York, pp. 402–433.Google Scholar
  36. Lane, N., 1985. Structure of components of the nervous system. In: G. A. Kerkut and L. I. Gilbert (Editors), Comprehensive Insect Physiology Biochemstry and Pharmacology, Vol. 5. Nervous System: Structure and Motor Function. Pergamon Press, New York, pp. 1–47.Google Scholar
  37. Lane, N. and Skaer, H., 1980. Intracellular junctions in insect tissues. Adv. Insect Physiol., 15: 35–213.Google Scholar
  38. Locke, M. and Huie, P., 1983. A function for plasma membrane reticular systems. Tissue Cell, 15: 885–902.Google Scholar
  39. Loudt, H. G. H., 1974. The preoviposition period ofBoophilus decoloratus (Koch 1844) (Acarina: Ixodidae). Acarologia, 14: 205–217.Google Scholar
  40. Meredith, J. and Kaufman, W. R., 1973. A proposed site of fluid secretion in the salivary gland of the ixodid tickDermacentor andersoni. Parasitology, 67: 205–217.Google Scholar
  41. Minoura, H., Chinzei, Y. and Kitamura, S., 1985.Ornithodoros moubata: Host immunoglobulin G in tick hemolymph. Exp. Parasitol., 60: 355–363.Google Scholar
  42. Mollenhauer, H., 1964. Plastic embedding mixtures for use in electron microscopy. Stain Technol., 39: 111–115.Google Scholar
  43. Nagar, S., 1968. On the significance of the duration of preoviposition and oviposition periods in ixodid tikks. Acarologia, 10: 621–29.Google Scholar
  44. O'Hagan, J., 1974.Boophilus microplus: digestion of hemoglobins by the engorged female tick. Exp. Parasitol., 35: 110–118.Google Scholar
  45. Oschman, J. and Wall, B., 1969. The structure of the rectal pads ofPeriplaneta americana L. with regard to fluid transport. J. Morphol., 127: 475–134.Google Scholar
  46. Palade, G., 1975. Intracellular aspects of the process of protein synthesis. Nobel Lecture, 1974; Science, 189: 347–358.Google Scholar
  47. Pappas, P. and Oliver, J., 1972. Reproduction in ticks (Acari: Ixodoidea). 2. Analysis of the stimulus for rapid and complete feeding of femaleDermacentor variabilis (Say). J. Med. Entomol., 9: 47–50.Google Scholar
  48. Raikhel, A., 1983. The Intestine. In: Y. Balashov (Editor), An Atlas of Ixodid Tick Ultrastructure. Entomol. Soc. Am. Spec. Publ., pp. 59–97.Google Scholar
  49. Roesler, R., 1934. Histologische, physiologische und serologische Untersuchungen uber die Verdauüng bei der ZeckengattungIxodes Latr. Z. Morphol. Oekol. Tiere, 28: 297–317.Google Scholar
  50. Saito, Y., 1960. Studies in ixodid ticks. IV. The internal anatomy in each stage ofHaemaphysalis flava Neumann 1894. Acta Med. Biol., 8: 189–239.Google Scholar
  51. Sato, T., 1968. A modified method for lead staining. J. Electron Microsc., 17: 158–159.Google Scholar
  52. Sauer, J. and Hair, J., 1972. The quantity of blood ingested by the lone star tick (Acarina: Ixodidae). Ann. Entomol. Soc. Am., 65: 1065–1068.Google Scholar
  53. Sonenshine, D., Silverstein, R. and Rechav, Y., 1982. Tick pheromone mechanisms. In: F. Obenchain and R. Galun (Editors), Physiology of Ticks. Pergamon Press, Oxford, pp. 439–468.Google Scholar
  54. Tatchell, R. J., 1967. Salivary secretion in the cattle tick as a means of water elimination. Nature, 213: 940–941.Google Scholar
  55. Tatchell, R. J., 1969. The ionic regulatory role of the salivary secretion of the cattle tickBoophilus microplus. J. Insect Physiol., 15: 1421–1430.Google Scholar
  56. Till, W., 1961. A contribution to the anatomy and histology of the brown ear tickRhipicephalus appendiculatus Neumann. Mem. Entomol. Soc. S. Afr., 6: 1–124.Google Scholar
  57. Williams, J. P., Barker, D. M., Sauer, J. R., Hair, J. A., Ownby, C. and Koch, H., 1985. Ultrastructural changes in the midgut epithelium of unfed lone star ticks with increasing age. Ann. Entomol. Soc. Am., 78: 62–69.Google Scholar

Copyright information

© Elsevier Science Publishers B. V. 1989

Authors and Affiliations

  • Betty I. Tarnowski
    • 1
  • Lewis B. Coons
    • 2
  1. 1.Department of OtolaryngologyMedical University of South CarolinaCharlestonUSA
  2. 2.Biology DepartmentMemphis State UniversityMemphisUSA

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