Experimental & Applied Acarology

, Volume 25, Issue 8, pp 661–674 | Cite as

Salivary fluid secretion in the ixodid tick Rhipicephalus appendiculatus is inhibited by Thogoto virus infection

  • W. Reuben Kaufman
  • Alan S. Bowman
  • Patricia A. Nuttall
Article

Abstract

Adult Rhipicephalus appendiculatus ticks, infectedwith Thogoto (THO) virus or control, were fed on guinea pigs and removed atintervals throughout the feeding cycle. Salivary fluid secretion was measuredbyan in vitro technique. The salivary glandsof infected, partially-fed ticks secreted fluid in vitro at about 75% the rateof controls, but the difference between infected and controls among engorgedticks was not statistically significant. Basal and DA-stimulated levels ofcyclic AMP (cAMP) were determined in isolated glands and were significantlyaffected by THO virus infection. The differences in secretory rate amongcontroland infected ticks could not be explained in terms of altered cAMP levels.Haemolymph volume was measured by a tracer-dilution technique using3H-inulin. The mean haemolymph volume for both THO-infected andcontrol groups was between 23–24% body weight throughout the feedingcycle, indicating that infection by this arbovirus did not influence salivaryfluid secretion via altered haemolymph volume. The mechanism by which THO virusaffects secretory activity of its tick vector remains unknown.

Arbovirus Cyclic AMP Rhipicephalus appendiculatus Thogoto virus Tick salivary glands 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Berridge M. and Prince W. 1972. The role of cyclic AMP and calcium in hormone action. Adv Insect Physiol. 9: 1-49.Google Scholar
  2. Davies C.D., Jones L.D. and Nuttall P.A. 1986. Experimental studies on the transmission cycle of Thogoto, a candidate orthomyxovirus, in Rhipicephalus appendiculatus. Am. J. Trop. Med. Hygiene 35: 1256-1262.Google Scholar
  3. Farndale R.W., Allan L.M. and Martin B.R. 1991. Adenylate cyclase and cAMP. In: Milligan G. (ed.), Signal Transduction: A Practical Approach. IRL Press, pp. 80-103.Google Scholar
  4. Fawcett D.W., Binnington K. and Voigt W.P. 1986. The cell biology of the ixodid tick salivary gland. In: Sauer J.R. and Hair J.A. (eds), Morphology, Physiology and Behavioural Biology of Ticks. Ellis Horwood Ltd., Chichester, pp. 22-45.Google Scholar
  5. Gillespie R.D., Mbow M.L. and Titus R.G. 2000. The immunomodulatory factors of bloodfeeding arthropod saliva. Parasite Immunol. 22: 319-331.Google Scholar
  6. Harris R.A. and Kaufman W.R. 1984. Neural involvement in the control of salivary gland degeneration in the ixodid tick Amblyomma hebraeum. J. Exp. Biol. 109: 281-290.Google Scholar
  7. Hume M.E., Essenberg R.C., Mcnew R.W., Bantle J.A. and Sauer J.R. 1984. Adensosine-3,5-monophosphate in salivary glands of unfed and feeding female lone star ticks, Amblyomma americanum (L.). Comp. Biochem. Physiol. 79C: 47-50.Google Scholar
  8. Jaenson T.G.T. 1986. Sex ratio distortion and reduced lifespan of Glossina pallidipes infected with the virus causing salivary gland hyperplasia. Entomol Exp Appl. 41: 265-271.Google Scholar
  9. Jones L.D., Davies C.R., Steele G.M. and Nuttall P.A. 1988. The rearing and maintenance of ixodid and argasid ticks in the laboratory. Anim Tech. 39: 99-106.Google Scholar
  10. Kaufman W. 1976. The influence of various factors on fluid secretion by in vitro salivary glands of ixodid ticks. J. Exp. Biol. 64: 727-742.Google Scholar
  11. Kaufman W.R. 1991. Correlation between haemolymph ecdysteroid titer, salivary gland degeneration and ovarian development in the ixodid tick, Amblyomma hebraeum Koch. J. Insect Physiol. 37: 95-99.Google Scholar
  12. Kaufman W.R., Aeschlimann A.A. and Diehl P.A. 1980. Regulation of body volume by salivation in a tick challenged with fluid loads. Am. J. Physiol. 238: R102-R112.Google Scholar
  13. Kaufman W.R. and Nuttall P. A. 1996. Amblyomma variegatum (Acari: Ixodidae): Mechanism and control of arbovirus secretion in tick saliva. Exp. Parasitol. 82: 316-323.Google Scholar
  14. Kaufman W.R. and Nuttall P.A. 2000. Secretion of Thogoto virus by in vitro salivary glands of Rhipicephalus appendiculatus. In: Kazimirova M., Labuda M. and Nuttall P.A. (eds), Proceedings of the 3rd International Conference “Ticks and Tick-borne Pathogens: Into the 21st Century”. Institute of Zoology, Slovak Academy of Sciences, Bratislava, Slovakia, pp. 217-221.Google Scholar
  15. Kaufman W.R. and Phillips J.E. 1973. Ion and water balance in the ixodid tick, Dermacentor andersoni. I. Routes of ion and water excretion. J. Exp. Biol. 58: 523-536.Google Scholar
  16. Maddrell S.H.P. 1971. The mechanisms of insect secretory systems. Adv Insect Physiol. 8: 199-331.Google Scholar
  17. Megaw M.J. 1978. Virus-like particles pathogenic to salivary glands of the tick Boophilus microplus. Nature 271: 483-484.Google Scholar
  18. Moore J. 1984. Parasites that change the behavior of their hosts. Sci Am. 250: 108-115.Google Scholar
  19. Morgan and Mordue 1981. Stimulated fluid secretion is sodium dependent in the Malpighian tubules of Locusta migratoria. J. Insect Physiol. 27: 271-279.Google Scholar
  20. Nuttall P.A. 1998. Displaced tick-parasite interactions at the host interface. Parasitology 116: 565-572.Google Scholar
  21. Nuttall P.A., Jones L.D., Labuda M. and Kaufman W.R. 1994. Adaptations of arboviruses to ticks. J. Med. Entomol. 31: 1-9.Google Scholar
  22. Paulson S.L., Poirier S.J., Grimstad P.R. and Craig G.B. 1992. Vector capacity of Aedes hendersoni (Diptera: Culicidae) for La Crosse virus: lack of impaired function in virus-infected salivary glands and enhanced virus transmission by sporozoite-infected mosquitoes. J. Med Entomol. 29: 483-488.Google Scholar
  23. Platt K.B., Linthicum K.J., Myint K.S.A., Innis B.L., Lerdthusnee K. and Vaughn D.W. 1997. Impact of dengue virus infection on feeding behavior of Aedes aegypti. Am. J. Trop. Med. Hygiene 57: 119-125.Google Scholar
  24. Samish M. and Rehacek J. 1999. Pathogens and predators of ticks and their potential in biological control. Ann. Rev. Entomol. 44: 159-182.Google Scholar
  25. Sauer J.R., Mcswain J.L., Bowman A.S. and Essenberg R.C. 1995. Tick salivary gland physiology. Ann. Rev. Entomol. 40: 245-267.Google Scholar
  26. Sauer J.R., Essenberg R.C. and Bowman A.S. 2000. Salivary glands in ixodid ticks: control and mechanism of secretion. J. Insect Physiol. 46: 1069-1078.Google Scholar
  27. Scott T.W. and Lorenz H. 1998. Reduction of Culiseta mealnura fitness by eastern equine encephalomyelitis virus. Am. J. Trop. Med. Hygiene 59: 341-346.Google Scholar
  28. Turrell M.J., Rossignol P.A., Spielman A., Rossi C.A. and Bailey C.L. 1984. Enhanced arboviral transmission by mosquitoes that concurrently ingested microfilariae. Science 225: 1039-1041.Google Scholar
  29. Wikel S.K. 1996. Host immunity to ticks. Ann. Rev. Entomol 41: 1-22.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • W. Reuben Kaufman
    • 1
  • Alan S. Bowman
    • 2
  • Patricia A. Nuttall
    • 3
  1. 1.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  2. 2.Department of ZoologyUniversity of AberdeenAberdeenUK
  3. 3.Institute of Virology and Environmental MicrobiologyOxfordUK

Personalised recommendations