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Experimental & Applied Acarology

, Volume 25, Issue 8, pp 641–660 | Cite as

Behavioural and chemoreceptor cell responses of the tick, Ixodes ricinus, to its own faeces and faecal constituents

  • Stoyan Grenacher
  • Thomas Kröber
  • Patrick M. Guerin
  • Michèle Vlimant
Article

Abstract

Ticks are ectoparasites of vertebrates and utilize a variety ofinfochemicals for host finding and acceptance as well as for intraspecificaggregation and mating responses. Individual male and female Ixodesricinus, the vector of Lyme disease in Europe, readily arrest onfilter paper strips contaminated with their own faeces. I.ricinus also responds, but to a lesser degree, tofaeces-contaminatedpapers enclosed in metal mesh envelopes, i.e. without directly contacting thefaeces, suggesting a role for volatiles in the arrestment response. The faecalconstituents guanine, xanthine, uric acid and 8-azaguanine (a bacterialbreakdown product of guanine) also caused arrestment of individual I.ricinus males and females. However, mixtures of these productsinduced arrestment of I. ricinus at doses one hundred foldlower than the lowest active dose of any of them tested singly. Saline extractsof faeces activated receptor cells in terminal pore sensilla on the first legtarsi of I. ricinus. One cell in these sensilla respondedin a similar dose dependent manner to guanine and 8-azaguanine, whereas asecondcell was more sensitive to lower doses of 8-azaguanine. The response thresholdapproached 100 fM for both cells. These findings suggest thatfaeces and faecal breakdown products are implicated in aggregation responses ofI. ricinus. This may account for the clumped distributionof this ectoparasite on the ground and contribute to the high proportion ofmated individuals recorded prior to host colonization.

Aggregation pheromone Behaviour Chemosensilla Guanine Gustation Ixodes ricinus Purines Tick 

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References

  1. Balashov Y.S. 1983. An atlas of Ixodid tick ultrastructure. In: Raikhel A.S. and Hoogstraal H. (eds), Special Publication, Entomological Society of America.Google Scholar
  2. Barré N., Naves M., Aprelon R., Fargetton M. and L'Hostis M. 1998. Attractivity of cattle infested by Amblyomma variegatum (Acari: Ixodidae) for conspecific adult ticks from the field in Guadeloupe. Exp. Appl. Acarol. 22: 297-308.Google Scholar
  3. Chu Wang I.W. and Axtell R.C. 1973. Comparitive fine structure of the claw sensilla of a soft tick, Argas (Persicargas) arboreus Kaiser, Hoogstraal, Kohls, and a hard tick, Amblyomma americanum (L). J. Parasitology 59: 545-555.Google Scholar
  4. Cochran D.G. 1985. Nitrogenous excretion. In: Kerkut G.A. and Gilbert L.I. (eds), Comprehensive Insect Physiology Biochemistry and Pharmacology. 4th edn. Pergamon Press, pp. 467-506.Google Scholar
  5. de Bruyne M. and Guerin P.M. 1998. Contact chemostimuli in the mating behaviour of the cattle tick Boophilus microplus. Arch. Insect Biochem. Physiol. 39: 65-80.Google Scholar
  6. Diehl P.A., Guerin P.M., Vlimant M. and Steullet P. 1991. Biosynthesis, production site, and emission rates of aggregation-attachment pheromone in males of two Amblyomma ticks. J. Chem. Ecol. 17: 833-847.Google Scholar
  7. Dusbábek F., Zahradnickova H. and Simek P. 1998. Chemical stability of assembly pheromone of argasid ticks (Ixodoidea: Argasidae). Folia Parasitol. 45: 62-66.Google Scholar
  8. Dusbábek F., Jegorov A. and Simek P. 1991a. Artificial assembly pheromone of argasid ticks (Ixodoidea: Argasidae). In: Dusbábek F. and Bukva V. (eds), Modern Acarology: Proc. VIIth. Int. Congr. Acarol. Vol. I. Czechoslovak Academy of Science, Prague, pp. 59-68.Google Scholar
  9. Dusbábek F., Simek P., Jegorov A. and Troska J. 1991b. Identification of xanthine and hypoxanthine as components of assembly pheromone in excreta of argasid ticks. Exp. Appl. Acarol. 11: 307-316.Google Scholar
  10. Egan M.E. 1976. The chemosensory bases of host discrimination in a parasitic mite. J. Comp. Physiol. A, Sens. Neural. Behav. Physiol. 109: 69-89.Google Scholar
  11. Falk-Vairant J., Guerin P.M., de Bruyne M. and Rohrer M. 1994. Some observations on mating and fertilization in the cattle tick Boophilus microplus. Med. Vet. Entomol. 8: 101-103.Google Scholar
  12. Feldman-Muhsam B. and Borut S. 1971. Copulation in Ixodid ticks. J. Parasitology 57: 630-634.Google Scholar
  13. Foelix R.F. and Chu Wang I.W. 1972. Fine structural analysis of palpal receptors in the tick Amblyomma americanum (L.). Zeit. für Zellforsch. 129: 548-560.Google Scholar
  14. Geigy Scientific Tables 1981. Units of Measurement, Body Fluids, Composition of the Body, Nutrition 1, ed. Lentner C. Ciba-Geigy, Basle, pp. 108-112.Google Scholar
  15. Gigon F. 1985. Biologie d'Ixodes ricinus L. sur le Plateau Suisse-Une contribution á l'Écologie de ce vecteur. Ph.D., University of Neuchâ tel.Google Scholar
  16. Gothe R., Weck P. and Kraiss A. 1984. Zur pheromonal induzierten kommunikation von Argas (Persicargas) walkerae und biologisch-chemischen Bekampfung durch kombinierten Einsatz eines Pheromons und Pheromon-Analogons mit flurmethrin. Zentralblatt für Veterinärmedizin, Reihe B 31: 161-179.Google Scholar
  17. Gothe R. 1987. Tick pheromones. Onderstepoort J. Vet. Res. 54: 439-441.Google Scholar
  18. Graf J.F. 1974. Ecologie et Ethologie d'Ixodus ricinus L. en Suisse (Ixodoidea: Ixodidae) Troisiè me note: Copulation, nutrition et ponte. Acarologia 16: 636-642.Google Scholar
  19. Graf J.-F. 1975. Ecologie et éthologie d'Ixodes ricinus L. en Suisse (Ixodoidea; Ixodidae), cinquiè me note: Mise en è vidence d'une phéromone sexuelle chez Ixodes ricinus. Acarologia 17: 436-441.Google Scholar
  20. Graf J.-F. 1978. Copulation, nutrition et ponte chez Ixodes ricinus L. (Ixodoidea: Ixodidae)-2e partie. Bull. de la Soc. Entomol. Suisse 51: 241-253.Google Scholar
  21. Grenacher S. and Guerin P.M. 1994. Inadvertent introduction of squalene, cholesterol, and other skin products into a sample. J. Chem. Ecol. 20: 3017-3025.Google Scholar
  22. Guerin P.M., Kröber T., McMahon C.P., Guerenstein P., Grenacher S., Vlimant M. et al. 2000. Chemosensory and behavioural adaptations of ectoparasitic arthropods. Novo Acta Leopoldina 83: 197-213.Google Scholar
  23. Haggart D.A. and Davis E.E. 1979. Electrophysiological responses of two types of ammonia-sensitive receptors on the first tarsi of ticks. In: Rodriguez J.G. (ed.), Recent Advances in Acarology. Academic Press, New York, pp. 421-425.Google Scholar
  24. Haggart D.A. and Davis E.E. 1980. Ammonia-sensitive neurones on the first tarsi of the tick, Rhipicephalus sanguineus. J. Insect. Physiol. 26: 517-523.Google Scholar
  25. Hamdy B.H. 1977. Biochemical and physiological studies of certain ticks (Ixodoidea). Excretion during ixodid feeding. J. Med. Entomol. 14: 15-18.Google Scholar
  26. Hamilton J.G.C., Papadopoulos E., Harrison S.J., Lloyd C.M. and Walker A.R. 1994. Evidence for a mounting sex pheromone in the brown ear tick Rhipicephalus appendiculatus, Neuman 1901 (Acari: Ixodidae). Exp. Appl. Acarol. 18: 331-338.Google Scholar
  27. Hassanali A., Nyandat E., Obenchain F.D., Otieno D.A. and Galun R. 1989. Humidity effects on response of Argas persicus (Oken) to guanine, an assembly pheromone of ticks. J. Chem. Ecol. 15: 791-798.Google Scholar
  28. Hess E. and Vlimant 1986. Leg sense organs of ticks. In: Sauer J.R. and Hair J.A. (eds), Morphology, Physiology, and Behavioural Biology of Ticks. Ellis Horwood, Chichester, pp. 361-390.Google Scholar
  29. Hirasawa H. and Isono K. 1978. Formation of 8-azaguanine from guanine by Streptomyces albus. J. Antibiotics 31: 628-629.Google Scholar
  30. Hodgson E.S., Lettvin J.Y. and Roeder K.D. 1955. Physiology of a primary chemoreceptor unit. Science 122: 417-418.Google Scholar
  31. Jorgensen W.K. 1984. The ultrastructure of the sense organ of tarsus 1, the palps and chelicerae of the larval cattle tick Boophilus microplus (Canestrini) (Ixodidae), including a study of the ultrastructure and function of the cattle tick podium. PhD Dissertation, University of Queenskland, St. Lucia, Australia.Google Scholar
  32. Kaufman W.R. and Sauer J.R. 1982. Ion and water balance in feeding tick: mechanisms of tick excretion. In: Obenchain F.D. and Galun R. (eds), Physiology of Ticks. Pergamon, Oxford, pp. 213-244.Google Scholar
  33. Kröber T. and Guerin P.M. 1999. Ixodid ticks avoid contact with liquid water. J. Exp. Biol. 202: 1877-1883.Google Scholar
  34. Leahy M.G. 1979. Pheromones of argasid ticks. In: Rodriguez J.G. (ed.), Recent Advances in Acarology. Vol. II. Academic Press, New York, pp. 297-308.Google Scholar
  35. Leahy M.G., Galun R. and van de Hey R. 1973. Assembly pheromone(s) in the soft tick Argas persicus (Oken). Nature 246: 515-516.Google Scholar
  36. Leahy M.G., Sternberg S., Mango C. and Galun R. 1975. Lack of species specifity in the assembly pheromones of soft ticks (Acari: Argasidae). J. Med. Entomol. 12: 413-414.Google Scholar
  37. Leahy M.G., Hijkovi Z. and Boucholavi J. 1981. Two female pheromones in the metastriate tick Hyalomma dromedarii (Acarina, Ixodidae). Acta Entomol. Bohemoslovaca 78: 224.Google Scholar
  38. Lees A.D. 1948. The sensory physiology of the sheep tick, Ixodes ricinus. J. Exp. Biol. 25: 145-207.Google Scholar
  39. Levinson H.Z., Levinson A.R. and Müller K. 1991. Functional adaptation of two nitrogenous waste products in evoking attraction and aggregation of flour mites (Acarus siro L.). Anz. Schädlingskde. Pflanzenschutz, Umweltschutz 64: 55-60.Google Scholar
  40. Lorenzo Figueras A.N., Kenigsten A. and Lazzari C.R. 1994. Aggregation in the haematophagous bug Triatoma infestans: Chemical signals and temporal pattern. J. Insect Physiol. 40: 311-316.Google Scholar
  41. McFarlane J.E., Steeves E. and Alli I. 1983. Aggregation of larvae of the house cricket, A cheta domesticus (L) by propionic acid present in the excreta. J. Chem. Ecol. 9: 1307-1314.Google Scholar
  42. McFarlane J.E., Steeves E. and Alli I. 1986. Aggregation of larvae of Blattella germanica (L.) by lactic acid present in excreta. J. Chem. Ecol. 12: 1369-1375.Google Scholar
  43. McMahon C. and Guerin P.M. 2000. Responses of the tropical bont tick, Amblyomma variegatum (Fabricius), to its aggregation-attachment pheromone presented in an air stream on a servosphere. J. Comp. Physiol. A. 186: 95-103.Google Scholar
  44. Neitz A.W.H. and Gothe R. 1984. Investigations into the volatility of female pheromones and the aggregation-inducing property of guanine in Argas (Persicargas) walkerae. Onderstepoort J. Vet. Res. 51: 197-201.Google Scholar
  45. Obenchain F.D. 1984. Behavioural interactions between the sexes, and aspects of species specificity pheromone mediated aggregation and attachment in Amblyomma. In: Griffith D.A. and Bowman C.E. (eds), Acarology. Vol. 1. Ellis Horwood, Chichester, pp. 387-392.Google Scholar
  46. Oliver J.H. 1974. Symposium on the reproduction of arthropods of medical and veterinary importance IV. Reproduction in ticks (Ixodoidea). J. Med. Entomol. 11: 26-34.Google Scholar
  47. Otieno D.A., Hassanali A., Obenchain F.D., Sternberg A. and Galun R. 1985. Identification of guanine as an assembly pheromone of ticks. Insect. Sci. Applic. 6: 667-670.Google Scholar
  48. Osterkamp J., Wahl U., Schmalfuss G. and Haas W. 1999. Host-odour recognition in two tick species is coded in a blend of vertebrate volatiles. J. Comp. Physiol. A, Sens. Neural. Behav. Physiol. 185: 59-67.Google Scholar
  49. Petney T.N. and Bull C.M. 1981. A non-specific aggregation pheromone in two Australian reptile ticks. Anim. Behav. 29: 181-185.Google Scholar
  50. Petney T.N. 1988. Demonstration of aggregation in free-living nymphs and adults of the bont tick, Amblyomma hebraeum. J. Parasitol. 74: 375-378.Google Scholar
  51. Phillips J.S. and Sonenshine D.E. 1993. Role of the male claw sensilla in the perception of female mounting sex pheromone in Dermacentor variabilis, Dermacentor andersoni and Amblyomma americanum. Exp. Appl. Acarol. 17: 631-653.Google Scholar
  52. Rechav Y., Parolis H., Whitehead G.B. and Knight M.M. 1977. Evidence for an assembly pheromone(s) produced by males of the bont tick Amblyomma hebraeum (Acarina, Ixodidae). J. Med. Entomol. 14: 71-78.Google Scholar
  53. Rechav Y., Norval R.A.I., Tannock J. and Colborne J. 1978. Attraction of the tick Ixodes neitzi to twigs marked by the klipspringer antelope. Nature 275: 310-311.Google Scholar
  54. Schöni R., Hess E., Blum W. and Ramstein K. 1984. The aggregation-attachement pheromone of the tropical bont tick Amblyomma variegatum Fabricius (Acari:Ixodidae): isolation, identification and action of its components. J. Insect Physiol. 30: 613-618.Google Scholar
  55. Smith J.J.B., Mitchell B.K., Rolseth B.M., Whitehead A.T. and Albert P.J. 1990. SAPID tools: microcomputer programs for analysis of multi-unit nerve recordings. Chemical Senses 15: 253-270.Google Scholar
  56. Steullet P. and Guerin P.M. 1992a. Perception of breath components by the tropical bont tick, Amblyomma variegatum Fabricius (Ixodidae) I. CO2-excited and CO2-inhibited receptors. J. Comp. Physiol. A, Sen. Neur. and Behav. Physiol. 170: 665-676.Google Scholar
  57. Steullet P. and Guerin P.M. 1992b. Perception of breath components by the tropical bont tick Amblyomma variegatum Fabricius (Ixodidae) II. Sulfide receptors. J. Comp. Physiol. A, Sen. Neur. and Behav. Physiol. 170: 677-685.Google Scholar
  58. Steullet P. and Guerin P.M. 1994a. Identification of vertebrate volatiles stimulating olfactory receptors on tarsus I of the tick Amblyomma variegatum Fabricius (Ixodidae) I. Receptors within the Haller's organ capsule. J. Comp. Physiol. A, Sen. Neur. and Behav. Physiol. 174: 27-38.Google Scholar
  59. Steullet P. and Guerin P.M. 1994b. Identification of vertebrate volatiles stimulating olfactory receptors on tarsus I of the tick Amblyomma variegatum Fabricius (Ixodidae) II. Receptors outside the Haller's organ capsule. J. Comp. Physiol. A, Sen. Neur. and Behav. Physiol. 174: 39-47.Google Scholar
  60. Taneja J. and Guerin P.M. 1997. Ammonia attracts the haematophagous bug Triatoma infestans: behavioural and neurophysiological data on nymphs. J. Comp. Physiol. A, Sen. Neur. and Behav. Physiol. 181: 21-34.Google Scholar
  61. Tatchell R. 1964. Digestion in the tick Argas persicus Oken. Parasitol. 54: 423-440.Google Scholar
  62. Thonney F. 1987. F. Etude morphologique et structurale des récepteurs sensoriels du tarse I de la tique Ixodes ricinus L. Ph.D., University of Neuchâ tel.Google Scholar
  63. Treverrow N.L., Stone B.F. and Cowie M. 1977. Aggregation pheromone in two Australian hard ticks, Ixodes holocyclus and Aponomma concolor. Experientia 33: 680-682.Google Scholar
  64. Uspensky I.V. and Emeliyanova Yu.O. 1980. Existence of pheromone associations in ticks of the genus Ixodes. Zool. Zhurnal. 59: 699-704.Google Scholar
  65. van Loon J.J.A. 1990. Chemoreception of phenolic acids and flavonoids in larvae of two species of Pieris. J. Comp. Physiol. A, Sen. Neur. and Behav. Physiol 166: 889-899.Google Scholar
  66. Waladde S.M. and Rice M.J. 1982. The sensory basis of tick feeding behaviour. In: Obenchain F.D. and Galun R. (eds), Physiology of Ticks. Pergamon Press, Oxford, pp. 71-118.Google Scholar
  67. Wang O. H., Paesen G.C., Nuttall P.A. and Barbour A.G. 1998. Male ticks help their mates to feed. Nature 391: 754-755.Google Scholar
  68. Yoder J.A. and Smith B.E. 1997. Enhanced water conservation in clusters of convergent lady beetles, Hippodamia convergens. Entomol. Exp. Applic. 85: 87-89.Google Scholar
  69. Zolotarev E.Kh. and Sinitsina E.E. 1965. Chemoreceptive organs on the forelegs of ixodid ticks. Vestnik Moskovskogo Universiteta Seria VI Biologija Pocvovedenie 20: 17-25.Google Scholar

Copyright information

© Kluwer Academic Publishers 2001

Authors and Affiliations

  • Stoyan Grenacher
    • 1
  • Thomas Kröber
    • 1
  • Patrick M. Guerin
    • 1
  • Michèle Vlimant
    • 1
  1. 1.Institute of ZoologyUniversity of NeuchâtelNeuchâtelSwitzerland

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