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Unique biological rhythm in the reproductive behaviour of female ticks of reptiles

Published online by Cambridge University Press:  07 January 2009

N. B. CHILTON ,
C. M. BULL  and
R. H. ANDREWS
N. B. CHILTON*
Affiliation:
School of Biological Sciences, Flinders University of South Australia, SA5072, Australia Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, S7N 5E2, Canada
C. M. BULL
Affiliation:
Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, S7N 5E2, Canada
R. H. ANDREWS
Affiliation:
School of Biological Sciences, Flinders University of South Australia, SA5072, Australia School of Pharmacy and Medical Sciences, University of South Australia, GPO Box 2471, Adelaide, SA 5001, Australia
*
*Corresponding author: Department of Biology, University of Saskatchewan, 112 Science Place, Saskatoon, SK, S7N 5E2, Canada. Tel: +1 306 9664407. Fax: +1 306 9664461. E-mail: [email protected]
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Summary

We report the discovery of a biological rhythm in the reproductive behaviour of the tick Bothriocroton hydrosauri that was absent in Amblyomma limbatum, a species that occurs on the same species of reptile host. Female B. hydrosauri mated in autumn or winter delayed oviposition until the following spring, while there was no diapause in conspecific females mated in spring or early summer. Initiation of ovipositional diapause in ticks is usually related to photoperiodic stimuli, but this was not the case for B. hydrosauri. The sinusoidal pattern in pre-oviposition times of B. hydrosauri females mated in different months in the laboratory suggests an internal seasonal time-keeping mechanism. We hypothesize that hormones imbibed by females during their bloodmeal may provide environmental cues associated with the induction of diapause. Irrespective of the mechanism underlying the rhythm, diapause by B. hydrosauri females mated during autumn or winter is of adaptive advantage because it synchronizes oviposition with favourable environmental conditions for egg hatching and increases the chance of larvae finding a host. The lack of a similar biological rhythm in A. limbatum may be a reflection of the different environmental conditions this species experiences throughout most of its range as compared with B. hydrosauri.

Keywords

biological rhythmpre-oviposition periodmorphogenetic diapausereptile ticksBothriocroton hydrosauriAmblyomma limbatum
Type
Research Article
Information
Parasitology , Volume 136 , Issue 1 , January 2009 , pp. 77 - 84
Copyright
Copyright © 2009 Cambridge University Press

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References

REFERENCES

Adkisson, P. L. (1966). Internal clocks and insect diapause. Science 154, 234–241.CrossRefGoogle ScholarPubMed
Andrews, R. H. (1982). Mating behaviour and reproductive isolation of three species of reptile tick. Animal Behaviour 30, 514–524.CrossRefGoogle Scholar
Balashov, Y. S. (1972). Bloodsucking ticks (Ixodoidea) – Vectors of disease of man and animals. Miscellaneous Publications of the Entomological Society of America 8, 1–376.Google Scholar
Belozerov, V. N. (1982). Diapause and biological rhythms in ticks. In Physiology of Ticks (ed. Obenchain, F. D. and Galun, R.), pp. 469–500. Pergamon, New York.CrossRefGoogle Scholar
Bull, C. M. and Burzacott, D. (1994). Reproductive interactions between two Australian reptile tick species. Experimental and Applied Acarology 18, 555–565.CrossRefGoogle ScholarPubMed
Bull, C. M. and Sharrad, R. D. (1980). Seasonal activity of the reptile tick, Aponomma hydrosauri (Denny) (Acari: Ixodidae) in experimental enclosures. Journal of the Australian Entomological Society 19, 47–52.CrossRefGoogle Scholar
Bull, C. M., Sharrad, R. D. and Petney, T. N. (1981). Parapatric boundaries between Australian reptile ticks. Proceedings of the Ecological Society of Australia 11, 95–107.Google Scholar
Carroll, J. F. and Pickens, L. G. (1987). Spectral sensitivity to light of two species of ticks (Acarina: Ixodidae). Annals of the American Society of Entomology 80, 256–262.CrossRefGoogle Scholar
Chilton, N. B. (1992). An index to assess the reproductive fitness of female ticks. International Journal for Parasitology 22, 109–111.CrossRefGoogle ScholarPubMed
Chilton, N. B. (1994). Differences in the life cycles of two species of reptile tick: Implications for species distributions. International Journal for Parasitology 24, 791–795.CrossRefGoogle ScholarPubMed
Chilton, N. B. and Andrews, R. H. (1988). Mating behaviour and parapatry in two species of Australian reptile tick. Oecologia 75, 146–152.CrossRefGoogle ScholarPubMed
Chilton, N. B., Andrews, R. H. and Bull, C. M. (1992). Delayed mating and the reproductive fitness of Aponomma hydrosauri (Acari: Ixodidae). International Journal for Parasitology 22, 1197–1200.CrossRefGoogle Scholar
Chilton, N. B., Andrews, R. H. and Bull, C. M. (1993). Effect of delayed mating and prolonged engorgement on the reproductive fitness of female Amblyomma limbatum (Acari: Ixodidae) in marginal population areas. Oecologia 94, 67–71.CrossRefGoogle ScholarPubMed
Chilton, N. B. and Bull, C. M. (1991). A comparison of the reproductive parameters of females of two reptile tick species. International Journal for Parasitology 21, 907–911.CrossRefGoogle ScholarPubMed
Chilton, N. B. and Bull, C. M. (1993 a). Oviposition by two Australian species of reptile tick. Acarologia 34, 115–121.Google Scholar
Chilton, N. B. and Bull, C. M. (1993 b). A comparison of the off-host survival times of larvae and nymphs of two species of reptile ticks. International Journal for Parasitology 23, 693–696.CrossRefGoogle Scholar
Chilton, N. B. and Bull, C. M. (1993 c). Interspecific differences in microhabitat choice by two species of Australian reptile tick. International Journal for Parasitology 23, 1045–1051.CrossRefGoogle Scholar
Chilton, N. B. and Bull, C. M. (1994). Influence of environmental factors on oviposition and egg development in Amblyomma limbatum and Aponomma hydrosauri (Acari: Ixodidae). International Journal for Parasitology 24, 83–90.CrossRefGoogle ScholarPubMed
Danks, H. V. (2005). How similar are daily and seasonal biological clocks? Journal of Insect Physiology 51, 609–619.CrossRefGoogle ScholarPubMed
Denlinger, D. L. (2002). Regulation of diapause. Annual Review of Entomology 47, 93–122.CrossRefGoogle ScholarPubMed
El-Shoura, S. M. and El-Shoura, S. M. (1988). Fine structure of the sight organs in the tick Hyalomma (Hyalomma) dromedarii (Ixodoidea: Ixodidae). Experimental and Applied Acarology 4, 109–116.CrossRefGoogle Scholar
Escobedo, G., Roberts, C. W., Carrero, J. C. and Morales-Montor, J. (2006). Parasite regulation by host hormones: an old mechanism of host exploitation? Trends in Parasitology 21, 588–593.CrossRefGoogle Scholar
Firth, B. T., Kennaway, D. J. and Rosenbilds, M. A. M. (1979). Plasma melatonin in the scincid lizard, Trachydosaurus rugosus: diel rhythm, seasonality, and the effect of constant light and constant darkness. General and Comparative Endocrinology 37, 493–500.CrossRefGoogle ScholarPubMed
Gwinner, E. (1986). Circannual Rhythms. Springer, Berlin, Germany.CrossRefGoogle Scholar
Kerr, G. D. and Bull, C. M. (2006). Interactions between climate, host refuge usage, and tick population dynamics. Parasitology Research 99, 214–222.CrossRefGoogle Scholar
Lees, K. and Bowman, A. S. (2007). Tick neurobiology: recent advances and the post-genomic era. Invertebrate Neuroscience 7, 183–198.CrossRefGoogle ScholarPubMed
Mead-Briggs, A. R. and Rudge, A. J. B. (1960). Breeding of the rabbit flea, Spilopsyllus cuniculi (Dale): requirement of a ‘factor’ from a pregnant rabbit for ovarian maturation. Nature, London 201, 1303–1304.CrossRefGoogle Scholar
Oliver, J. H. JR. (1989). Biology and systematics of ticks (Acari: Ixodida). Annual Review of Ecology and Systematics 20, 397–430.CrossRefGoogle Scholar
Paine, S. H., Kemp, D. H. and Allen, J. R. (1983). In vitro feeding of Dermacentor andersoni (Stiles) – effects of histamine and other mediators. Parasitology 86, 419–428.CrossRefGoogle ScholarPubMed
Paul, M. J., Zucker, I. and Schwartz, W. J. (2008). Tracking the seasons: the internal calendars of vertebrates. Philosophical Transactions of the Royal Society B 363, 341–361.CrossRefGoogle ScholarPubMed
Pegram, R. G., Mwase, E. T., Zivkovic, D. and Jongejan, F. (1988). Morphogenetic diapause in Amblyomma variegatum (Acari: Ixodidae). Medical and Veterinary Entomology 2, 301–307.CrossRefGoogle ScholarPubMed
Phillis, W. A. III and Cromroy, H. L. (1997). The microanatomy of the eye of Amblyomma americanum (Acari: Ixodidae) and resultant implications of its structure. Journal of Medical Entomology 13, 685–698.CrossRefGoogle Scholar
Rees, H. H. (2004). Hormonal control of tick development and reproduction. Parasitology 129 (Suppl.), S127–S143.CrossRefGoogle ScholarPubMed
Rothschild, M. and Ford, B. (1964). Breeding of the rabbit flea (Spilopsyllus cuniculi (Dale)) controlled by the reproductive hormones of the host. Nature, London 201, 103–104.CrossRefGoogle Scholar
Saunders, D. S. (2002). Insect Clocks. Elsevier Science B.V., Amsterdam, The Netherlands.Google Scholar
Smallridge, C. J. and Bull, C. M. (1999). Transmission of the blood parasite Hemolivia mariae between its lizard and its tick hosts. Parasitology Research 85, 858–863.CrossRefGoogle ScholarPubMed
Stenos, J., Graves, S., Vsevolod, L. P. and Walker, D. H. (2003). Aponomma hydrosauri, the reptile-associated tick reservoir of Rickettsia honei on Flinders Island, Australia. American Journal of the Tropical Medicine and Hygiene 69, 314–317.CrossRefGoogle ScholarPubMed
Smyth, M. (1973). The distribution of three species of reptile ticks, Aponomma hydrosauri (Denny), Amblyomma albolimbatum Neumann, and Amb. limbatum Neumann. I. Distribution and hosts. Australian Journal of Zoology 21, 91–101.CrossRefGoogle Scholar