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Do the level of energy reserves, hydration status and Borrelia infection influence walking by Ixodes ricinus (Acari: Ixodidae) ticks?

Published online by Cambridge University Press:  05 January 2012

C. HERRMANN
Affiliation:
Institute of Biology, Laboratory of Eco-Epidemiology of Parasites, University of Neuchâtel, Emile Argand 11, Case Postale 158, 2000 Neuchâtel, Switzerland
L. GERN*
Affiliation:
Institute of Biology, Laboratory of Eco-Epidemiology of Parasites, University of Neuchâtel, Emile Argand 11, Case Postale 158, 2000 Neuchâtel, Switzerland
*
*Corresponding author: Institute of Biology, Laboratory of Eco-Epidemiology of Parasites, University of Neuchâtel, Emile Argand 11, Case Postale 158, 2000 Neuchâtel, Switzerland. Tel: +41 32 718 30 52. Fax: +41 32 718 30 01. E-mail: [email protected]

Summary

Ixodes ricinus horizontal movement within a humidity gradient and the influence of infection by Borrelia burgdorferi sensu lato (s.l.) on tick walking were investigated. Nymphs were placed within an arena containing a humidity gradient ranging from 45 to 95% relative humidity (RH). After 1 h of acclimation at 70% RH ticks were released so that they could either stay, or walk towards either the wet or the dry end. Their position was recorded 2 h post-release. Fat content was quantified and Borrelia infection was detected using real-time PCR and PCR followed by Reverse Line Blotting. Among the 1500 ticks tested, 29·85% were infected. More low-fat nymphs walked inside the arena than high-fat individuals. When nymphs walked, more low-fat ticks walked towards wetter than drier air, whereas more high-fat individuals walked towards drier than wetter air. Among high-fat nymphs, a lower proportion of Borrelia-infected ticks walked inside the arena compared to uninfected individuals, as though spirochetes manipulated their arthropod vector to stay. However, Borrelia infection had no effect on walking direction towards the dry or the wet end. Hence, it appears that I. ricinus nymphs walk horizontally over short distances within a humidity gradient depending on both energy resources and Borrelia infection.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Aeschlimann, A. (1972). Ixodes ricinus, Linné, 1758 (Ixodoidae, Ixodidae). Essai préliminaire de synthèse sur la biologie de cette espèce en Suisse. Acta Tropica 29, 321340.Google Scholar
Alekseev, A. N., Dubinina, H. V., Van de Pol, I. and Schouls, L. M. (2001). Identification of Ehrlichia spp. and Borrelia burgdorferi in Ixodes ticks in the Baltic regions of Russia. Journal of Clinical Microbiology 39, 22372242.Google Scholar
Alekseev, A. N., Jensen, P. M., Dubinina, H. V., Smirnova, L. A., Makrouchina, N. A. and Zharkov, S. D. (2000). Peculiarities of behaviour of taiga (Ixodes persulcatus) and sheep (Ixodes ricinus) ticks (Acarina: Ixodidae) determined by different methods. Folia Parasitologica 47, 147153.Google Scholar
Botto-Mahan, C., Cattan, P. E. and Medel, R. (2006). Chagas disease parasite induces behavioural changes in the kissing bug Mepraia spinolai. Acta Tropica 98, 219223.Google Scholar
Burri, C., Morán Cadenas, F., Douet, V., Moret, J. and Gern, L. (2007). Ixodes ricinus density and infection prevalence with Borrelia burgdorferi sensu lato along a north-facing altitudinal gradient in the Rhône Valley (Switzerland). Vector-Borne and Zoonotic Diseases 7, 5058.Google Scholar
Casati, S., Bernasconi, M. V., Gern, L. and Piffaretti, J. C. (2004). Diversity within Borrelia burgdorferi sensu lato genospecies in Switzerland by recA gene sequence. FEMS Microbiology Letters 238, 115123.Google ScholarPubMed
Casjens, S. R., Fraser-Liggett, C. M., Mongodin, E. F., Qiu, W.-G., Dunn, J. J., Luft, B. J. and Schutzer, S. E. (2011). Whole genome sequence of an unusual Borrelia burgdorferi sensu lato isolate. Journal of Bacteriology 193, 14891490.Google Scholar
Cotté, V., Bonnet, S., Cote, M. and Vayssier-Taussat, M. (2010). Prevalence of five pathogenic agents in questing Ixodes ricinus ticks from western France. Vector-Borne and Zoonotic Diseases 10, 18.Google Scholar
Crooks, E. and Randolph, S. E. (2006). Walking by Ixodes ricinus ticks: intrinsic and extrinsic factors determine the attraction of moisture or host odour. The Journal of Experimental Biology 209, 21382142.Google Scholar
Fiahlo, R. F. and Schall, J. J. (1995). Thermal ecology of a malarial parasite and its insect vector: consequences for the parasite's transmission success. Journal of Animal Ecology 64, 553562.Google Scholar
Gern, L., Douet, V., Lopez, Z., Rais, O. and Morán Cadenas, F. (2010). Diversity of Borrelia genospecies in Ixodes ricinus ticks in a Lyme borreliosis endemic area in Switzerland identified by using new probes for reverse line blotting. Ticks and Tick-borne Diseases 1, 2329.Google Scholar
Goddard, J. (1993). Ecological studies of Ixodes scapularis (Acari: Ixodidae) in central Mississippi: lateral movement of adult ticks. Journal of Medical Entomology 30, 824826.CrossRefGoogle ScholarPubMed
Guy, E. C. and Stanek, G. (1991). Detection of Borrelia burgdorferi in patients with Lyme disease by the polymerase chain reaction. Journal of Clinical Pathology 44, 610611.CrossRefGoogle ScholarPubMed
Herrmann, C. and Gern, L. (2010). Survival of Ixodes ricinus (Acari: Ixodidae) under challenging conditions of temperature and humidity is influenced by Borrelia burgdorferi sensu lato infection. Journal of Medical Entomology 47, 11961204.Google Scholar
Hu, C. M., Wilske, B., Fingerle, V., Lobet, Y. and Gern, L. (2001). Transmission of Borrelia garinii OspA serotype 4 to BALB/c mice by Ixodes ricinus ticks collected in the field. Journal of Clinical Microbiology 39, 11691171.CrossRefGoogle ScholarPubMed
Huegli, D., Hu, C. M., Humair, P.-F., Wilske, B. and Gern, L. (2002). Apodemus species mice are reservoir hosts of Borrelia garinii OspA serotype 4 in Switzerland. Journal of Clinical Microbiology 40, 47354737.CrossRefGoogle ScholarPubMed
Hurd, H. (2003). Manipulation of medically important insect vectors by their parasites. Annual Review of Entomology 48, 141161.Google Scholar
Jouda, F., Perret, J.-L. and Gern, L. (2004). Ixodes ricinus density, and distribution and prevalence of Borrelia burgdorferi sensu lato infection along an altitudinal gradient. Journal of Medical Entomology 41, 162169.Google Scholar
Knülle, W. and Rudolph, D. (1982). Humidity relationships and water balance of ticks. In Physiology of Ticks (ed. Obenchain, F. D. and Galun, R.), pp. 4370. Pergamon Press, Oxford, UK.Google Scholar
Kurtenbach, K., Hanincova, K., Tsao, J. I., Margos, G., Fish, D. and Ogden, N. (2006). Fundamental processes in the evolutionary ecology of Lyme borreliosis. Nature Reviews Microbiology 4, 660669.Google Scholar
Lambrechts, L., Morlais, I., Awono-Ambene, P. H., Cohuet, A., Simard, F., Jacques, J.-C., Bourgouin, C. and Koella, J. C. (2007). Effect of infection by Plasmodium falciparum on the melanisation immune response of Anopheles gambiae. American Journal of Tropical Medicine and Hygiene 76, 475480.Google Scholar
Lees, A. D. (1946). Water balance in Ixodes ricinus L. and certain other species of ticks. Parasitology 37, 120.Google Scholar
Lees, A. D. (1948). The sensory physiology of the sheep tick, Ixodes ricinus. The Journal of Experimental Biology 25, 145207.Google Scholar
Lefèvre, T. and Thomas, F. (2008). Behind the scene, something else is pulling the strings: emphasizing parasitic manipulation in vector-borne diseases. Infection, Genetics and Evolution 8, 504519.CrossRefGoogle ScholarPubMed
MacLeod, J. (1935). Ixodes ricinus in relation to its physical environment. II. The factors governing survival and activity. Parasitology 27, 123144.Google Scholar
Margos, G., Vollmer, S. A., Cornet, M., Garnier, M., Fingerle, V., Wilske, B., Bormane, A., Vitorino, L., Collares-Pereira, M., Drancourt, M. and Kurtenbach, K. (2009). A new Borrelia species defined by multilocus sequence analysis of housekeeping genes. Applied and Environmental Microbiology 75, 54105416.Google Scholar
Morán Cadenas, F., Rais, O., Jouda, F., Douet, V., Humair, P.-F., Moret, J. and Gern, L. (2007). Phenology of Ixodes ricinus and infection with Borrelia burgdorferi sensu lato along a North- and South-facing altitudinal gradient on Chaumont Mountain, Switzerland. Journal of Medical Entomology 44, 683693.Google Scholar
Perret, J.-L. (2002). Computer-assisted laboratory and field studies of the host-finding behaviour of the tick Ixodes ricinus (Acarina: Ixodidae): ecological implications of climate and light. Thesis, Université de Neuchâtel, Neuchâtel, Switzerland.Google Scholar
Perret, J.-L., Guerin, P. M., Diehl, P. A., Vlimant, M. and Gern, L. (2003). Darkness induces mobility, and saturation deficit limits questing duration, in the tick Ixodes ricinus. Journal of Experimental Biology 206, 18091815.CrossRefGoogle ScholarPubMed
Perret, J.-L., Guigoz, E., Rais, O. and Gern, L. (2000). Influence of saturation deficit and temperature on Ixodes ricinus tick questing activity in a Lyme borreliosis-endemic area (Switzerland). Parasitology Research 86, 554557.Google Scholar
Perret, J.-L., Rais, O. and Gern, L. (2004). Influence of climate on the proportion of Ixodes ricinus nymphs and adults questing in a tick population. Journal of Medical Entomology 41, 361365.CrossRefGoogle Scholar
Postic, D., Assous, M. V., Grimont, P. A. D. and Baranton, G. (1994). Diversity of Borrelia burgdorferi sensu lato evidenced by restriction fragment length polymorphism of rrf(5S)-rrl(23S) intergenic spacer amplicons. International Journal of Systematic Bacteriology 44, 743752.CrossRefGoogle ScholarPubMed
Poupon, M.-A., Lommano, E., Humair, P.-F., Douet, V., Rais, O., Schaad, M., Jenni, L. and Gern, L. (2006). Prevalence of Borrelia burgdorferi sensu lato in ticks collected from migratory birds in Switzerland. Applied and Environmental Microbiology 72, 976979.Google Scholar
R Development Core Team (2011). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org.Google Scholar
Randolph, S. E. (1991). The effect of Babesia microti on feeding and survival in its tick vector, Ixodes trianguliceps. Parasitology 102, 916.CrossRefGoogle ScholarPubMed
Randolph, S. E., Green, R. M., Hoodless, A. N. and Peacey, M. F. (2002). An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. International Journal for Parasitology 32, 979989.Google Scholar
Randolph, S. E. and Storey, K. (1999). Impact of microclimate on immature tick-rodent interactions (Acari: Ixodidae): implications for parasite transmission. Journal of Medical Entomology 36, 741748.Google Scholar
Rauter, C. and Hartung, T. (2005). Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Applied and Environmental Microbiology 71, 72037216.Google Scholar
Rijpkema, S. G. T., Golubic, D., Molkenboer, M. J. C. H., Verbeek-De Kruif, N. and Schellekens, J. F. P. (1996). Identification of four genomic groups of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in a Lyme borreliosis endemic region of northern Croatia. Experimental and Applied Acarology 20, 2330.Google Scholar
Rijpkema, S. G. T., Molkenboer, M. J. C. H., Schouls, L. M., Jongejan, F. and Schellekens, J. F. P. (1995). Simultaneous detection and genotyping of three genomic groups of Borrelia burgdorferi sensu lato in Dutch Ixodes ricinus ticks by characterization of the amplified intergenic spacer region between 5S and 23S rRNA genes. Journal of Clinical Microbiology 33, 30913095.CrossRefGoogle ScholarPubMed
Schwaiger, M., Péter, O. and Cassinotti, P. (2001). Routine diagnosis of Borrelia burgdorferi (sensu lato) infections using real-time PCR assay. Clinical Microbiology and Infection 7, 461469.Google Scholar
Sonenshine, D. E. (1991). Biology of Ticks, Vol. 1. Oxford University Press, New York, USA.Google Scholar
Uspensky, I. (1995). Physiological age of Ixodid ticks : aspects of its determination and application. Journal of Medical Entomology 32, 751764.Google Scholar
Vollmer, S. A., Borman, A., Dinnis, R. E., Seelig, F., Dobson, A. D., Aanensen, D. M., James, M. C., Donaghy, M., Randolph, S. E., Feil, E. J., Kurtenbach, K. and Margos, G. (2011). Host migration impacts on the phylogeography of Lyme borreliosis species in Europe. Environmental Microbiology 13, 184192.CrossRefGoogle ScholarPubMed