Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-26T21:05:07.918Z Has data issue: false hasContentIssue false
  • English
  • Français

The abundance of Ixodes ricinus ticks depends on tree species composition and shrub cover

Published online by Cambridge University Press:  13 April 2012

W. TACK ,
M. MADDER ,
L. BAETEN ,
P. DE FRENNE  and
K. VERHEYEN
W. TACK*
Affiliation:
Laboratory of Forestry, Department of Forest and Water Management, Ghent University, Geraardsbergsesteenweg 267, 9090 Melle-Gontrode, Belgium
M. MADDER
Affiliation:
Unit of Vector Biology, Department of Biomedical Sciences, Institute of Tropical Medicine, Nationalestraat 155, 2000 Antwerp, Belgium Department of Veterinary Tropical Diseases, Faculty of Veterinary Science, University of Pretoria, Onderstepoort, 0110, South Africa
L. BAETEN
Affiliation:
Laboratory of Forestry, Department of Forest and Water Management, Ghent University, Geraardsbergsesteenweg 267, 9090 Melle-Gontrode, Belgium Terrestrial Ecology Unit, Department of Biology, Ghent University, K. L. Ledeganckstraat 35, 9000 Ghent, Belgium
P. DE FRENNE
Affiliation:
Laboratory of Forestry, Department of Forest and Water Management, Ghent University, Geraardsbergsesteenweg 267, 9090 Melle-Gontrode, Belgium Forest Ecology and Conservation Group, Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK
K. VERHEYEN
Affiliation:
Laboratory of Forestry, Department of Forest and Water Management, Ghent University, Geraardsbergsesteenweg 267, 9090 Melle-Gontrode, Belgium
*
*Corresponding author: Laboratory of Forestry, Department of Forest and Water Management, Ghent University, Geraardsbergsesteenweg 267, 9090 Melle-Gontrode, Belgium. Tel: +32 (0) 9 264 90 30. Fax: +32 (0) 9 264 90 92. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The mainstream forestry policy in many European countries is to convert coniferous plantations into (semi-natural) deciduous woodlands. However, woodlands are the main habitat for Ixodes ricinus ticks. Therefore, assessing to what extent tick abundance and infection with Borrelia spirochetes are affected by forest composition and structure is a prerequisite for effective prevention of Lyme borreliosis. We selected a total of 25 pine and oak stands, both with and without an abundant shrub layer, in northern Belgium and estimated tick abundance between April and October 2008–2010. Additionally, the presence of deer beds was used as an indicator of relative deer habitat use. Borrelia infections in questing nymphs were determined by polymerase chain reactions. The abundance of larvae, nymphs, and adults was higher in oak stands compared to pine stands and increased with increasing shrub cover, most likely due to differences in habitat use by the ticks' main hosts. Whereas tick abundance was markedly higher in structure-rich oak stands compared to homogeneous pine stands, the Borrelia infection rates in nymphs did not differ significantly. Our results indicate that conversion towards structure-rich deciduous forests might create more suitable tick habitats, but we were unable to detect an effect on the infection rate.

Keywords

Ixodes ricinusBorrelia burgdorferitickroe deerhabitatforest conversion
Type
Research Article
Information
Parasitology , Volume 139 , Issue 10 , September 2012 , pp. 1273 - 1281
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Allan, B. F., Keesing, F. and Ostfeld, R. S. (2003). Effect of forest fragmentation on Lyme disease risk. Conservation Biology 17, 267–272. doi: 10.1046/j.1523-1739.2003.01260.x.CrossRefGoogle Scholar
Bacon, R. M., Kugeler, K. J. and Mead, P. S. (2008). Surveillance for Lyme disease—United States, 1992–2006. Morbidity and Mortality Weekly Report 57, 1–9.Google Scholar
Bates, D., Maechler, M. and Bolker, B. (2011). Lme4: Linear Mixed-Effects Models Using S4 Classes. R package version 0.999375-42, URL http://CRAN.R-project.org/package=lme4/ (accessed November 18, 2011).Google Scholar
Bíró, Z., Szemethy, L., Katona, K., Heltai, M. and Petö, Z. (2006). Seasonal distribution of red deer (Cervus elaphus) in a forest-agriculture habitat in Hungary. Mammalia 70, 70–75. doi: 10.1515/MAMM.2006.016.Google Scholar
Bolker, B. M. (2008). Ecological Models and Data. Princeton University Press, Princeton, NJ, USA.Google Scholar
Boom, R., Sol, C. J. A., Salimans, M. M. M., Jansen, C. L., Wertheim-van Dillen, P. M. E. and van der Noordaa, J. (1990). Rapid and simple method for purification of nucleic acids. Journal of Clinical Microbiology 28, 495–503.Google Scholar
Boyard, C., Vourc'h, G. and Barnouin, J. (2008). The relationship between Ixodes ricinus and small mammal species at the woodland-pasture interface. Experimental and Applied Acarology 44, 61–76. doi: 10.1007/s10493-008-9132-3.Google Scholar
Brownstein, J. S., Skelly, D. K., Holford, T. R. and Fish, D. (2005). Forest fragmentation predicts local scale heterogeneity of Lyme disease risk. Oecologia 146, 469–475. doi: 10.1007/s00442-005-0251-9.CrossRefGoogle ScholarPubMed
Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer, New York, USA.Google Scholar
Cederlund, G., Bergqvist, J., Kjellander, P., Gill, R., Gaillard, J. M., Boisaubert, B., Ballon, P. and Duncan, P. (1998). Managing roe deer and their impact on the environment: maximising the net benefits to society. In The European Roe deer: The Biology of Success (ed. Andersen, R., Duncan, P. and Linnell, J. D. C.), pp. 337–372. Scandinavian University Press, Oslo, Norway.Google Scholar
Comstedt, P., Bergström, S., Olsen, B., Garpmo, U., Marjavaara, L., Mejlon, H., Barbour, A. G. and Bunikis, J. (2006). Migratory passerine birds as reservoirs of Lyme borreliosis in Europe. Emerging Infectious Diseases 12, 1087–1095.Google Scholar
Demaerschalck, I., Ben Messaoud, A., De Kesel, M., Hoyois, B., Lobet, Y., Hoet, P., Bigaignon, G., Bollen, A. and Godfroid, E. (1995). Simultaneous presence of different Borrelia burgdorferi genospecies in biological fluids of Lyme disease patients. Journal of Clinical Microbiology 33, 602–608.CrossRefGoogle ScholarPubMed
Estrada-Peña, A. (2001). Distribution, abundance, and habitat preferences of Ixodes ricinus (Acari: Ixodidae) in northern Spain. Journal of Medical Entomology 38, 361–370. doi: 10.1603/0022-2585-38.3.361.CrossRefGoogle ScholarPubMed
Estrada-Peña, A., Osácar, J. J., Pichon, B. and Gray, J. S. (2005). Hosts and pathogen detection for immature stages of Ixodes ricinus (Acari: Ixodidae) in North-Central Spain. Experimental and Applied Acarology 37, 257–268. doi: 10.1007/s10493-005-3271-6.CrossRefGoogle ScholarPubMed
Gassner, F., van Vliet, A. J. H., Burgers, S. L. G. E., Jacobs, F., Verbaarschot, P., Hovius, E. K. E., Mulders, S., Verhulst, N. O., van Overbeek, L. S. and Takken, W. (2011). Geographic and temporal variations in population dynamics of Ixodes ricinus and associated Borrelia infections in The Netherlands. Vector-Borne and Zoonotic Diseases 11, 523–532. doi: 10.1089/vbz.2010.0026.CrossRefGoogle ScholarPubMed
Gassner, F., Verbaarschot, P., Smallegange, R. C., Spitzen, J., Van Wieren, S. E. and Takken, W. (2008). Variations in Ixodes ricinus density and Borrelia infections associated with cattle introduced into a woodland in The Netherlands. Applied and Environmental Microbiology 74, 7138–7144. doi: 10.1128/AEM.00310-08.CrossRefGoogle ScholarPubMed
Gill, R. M. A. (1990). Monitoring the Status of European and North American Cervids. Global Environment Monitoring System, United Nations Environment Programme, Nairobi, Kenya.Google Scholar
Gray, J. S. (1998). The ecology of ticks transmitting Lyme borreliosis. Experimental and Applied Acarology 22, 249–258. doi: 10.1023/A:1006070416135.CrossRefGoogle Scholar
Gray, J. S., Kahl, O., Janetzki, C. and Stein, J. (1992). Studies on the ecology of Lyme disease in a deer forest in County Galway, Ireland. Journal of Medical Entomology 29, 915–920.Google Scholar
Halos, L., Bord, S., Cotté, V., Gasqui, P., Abrial, D., Barnouin, J., Boulouis, H. J., Vayssier-Taussat, M. and Vourc'h, G. (2010). Ecological factors characterizing the prevalence of bacterial tick-borne pathogens in Ixodes ricinus ticks in pastures and woodlands. Applied and Environmental Microbiology 76, 4413–4420. doi: 10.1128/AEM.00610-10.Google Scholar
Hanincová, K., Schäfer, S. M., Etti, S., Sewell, H. S., Taragelová, V., Ziak, D., Labuda, M. and Kurtenbach, K. (2003). Association of Borrelia afzelii with rodents in Europe. Parasitology 126, 11–20. doi: 10.1017/S0031182002002548.CrossRefGoogle ScholarPubMed
Hillyard, P. D. (1996). Ticks of North-West Europe. The Natural History Museum, London, UK.Google Scholar
Humair, P. F. and Gern, L. (1998). Relationship between Borrelia burgdorferi sensu lato species, red squirrels (Sciurus vulgaris) and Ixodes ricinus in enzootic areas in Switzerland. Acta Tropica 69, 213–227. doi: 10.1016/S0001-706X(97)00126-5.CrossRefGoogle ScholarPubMed
Humair, P. F., Rais, O. and Gern, L. (1999). Transmission of Borrelia afzelii from Apodemus mice and Clethrionomys voles to Ixodes ricinus ticks: differential transmission pattern and overwintering maintenance. Parasitology 118, 33–42. doi: 10.1017/S0031182098003564.Google Scholar
Hurvich, C. M. and Tsai, C. L. (1989). Regression and time series model selection in small samples. Biometrika 76, 297–307. doi: 10.1093/biomet/76.2.297.CrossRefGoogle Scholar
Jaenson, T. G. T., Jaenson, D. G. E., Eisen, L., Petersson, E. and Lindgren, E. (2012). Changes in the geographical distribution and abundance of the tick Ixodes ricinus during the past 30 years in Sweden. Parasites & Vectors 5, 8. doi: 10.1186/1756-3305-5-8.Google Scholar
Jongejan, F. (2001). Teken en door Teken Overgedragen Ziekten. Stichting Diergeneeskundig Memorandum, Boxtel, The Netherlands.Google Scholar
Kurtenbach, K., Peacey, M., Rijpkema, S. G. T., Hoodless, A. N., Nuttall, P. A. and Randolph, S. E. (1998). Differential transmission of the genospecies of Borrelia burgdorferi sensu lato by game birds and small rodents in England. Applied and Environmental Microbiology 64, 1169–1174.CrossRefGoogle ScholarPubMed
Linard, C., Lamarque, P., Heyman, P., Ducoffre, G., Luyasu, V., Tersago, K., Vanwambeke, S. O. and Lambin, E. F. (2007). Determinants of the geographic distribution of Puumala virus and Lyme borreliosis infections in Belgium. International Journal of Health Geographics 6, 15. doi: 10.1186/1476-072X-6-15.Google Scholar
Lindström, A. and Jaenson, T. G. T. (2003). Distribution of the common tick, Ixodes ricinus (Acari: Ixodidae), in different vegetation types in southern Sweden. Journal of Medical Entomology 40, 375–378. doi: 10.1603/0022-2585-40.4.375.Google Scholar
Olsthoorn, A. F. M., Bartelink, H. H., Gardiner, J. J., Pretzsch, H., Hekhuis, H. J. and Franc, A. (1999). Management of Mixed-Species Forest: Silviculture and Economics. DLO Institute for Forestry and Nature Research (IBN-DLO), Wageningen, The Netherlands.Google Scholar
Ostfeld, R. S. and LoGiudice, K. (2003). Community disassembly, biodiversity loss, and the erosion of an ecosystem service. Ecology 84, 1421–1427. doi: 10.1890/02-3125.Google Scholar
Pichon, B., Mousson, L., Figureau, C., Rodhain, F. and Perez-Eid, C. (1999). Density of deer in relation to the prevalence of Borrelia burgdorferi s.l. in Ixodes ricinus nymphs in Rambouillet forest, France. Experimental and Applied Acarology 23, 267–275. doi: 10.1023/A:1006023115617.CrossRefGoogle Scholar
Piesman, J. and Gern, L. (2004). Lyme borreliosis in Europe and North America. Parasitology 129 (Suppl.), S191–S220. doi: 10.1017/S0031182003004694.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, 7203–7216. doi: 0099-2240/05/$08.00+0.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/ (accessed November 18, 2011).Google Scholar
Ruiz-Fons, F. and Gilbert, L. (2010). The role of deer as vehicles to move ticks, Ixodes ricinus, between contrasting habitats. International Journal for Parasitology 40, 1013–1020. doi: 10.1016/j.ijpara.2010.02.006.CrossRefGoogle ScholarPubMed
Saïd, S. and Servanty, S. (2005). The influence of landscape structure on female roe deer home-range size. Landscape Ecology 20, 1003–1012. doi: 10.1007/s10980-005-7518-8.Google Scholar
Schulze, T. L., Jordan, R. A. and Hung, R. W. (1995). Suppression of subadult Ixodes scapularis (Acari: Ixodidae) following removal of leaf litter. Journal of Medical Entomology 32, 730–733.Google Scholar
Smith, H. D., Oveson, M. C. and Pritchett, C. L. (1986). Characteristics of mule deer beds. Great Basin Naturalist 46, 542–546.Google Scholar
Sood, S. K., O'Connell, S. and Weber, K. (2011). The emergence and epidemiology of Lyme borreliosis in Europe and North America. In Lyme Borreliosis in Europe and North America: Epidemiology and Clinical Practice (ed. Sood, S. K.), pp. 1–35. John Wiley & Sons, Inc., New Jersey, USA. doi: 10.1002/9780470933961.ch1.CrossRefGoogle Scholar
Spiecker, H., Hansen, J., Klimo, E., Skovsgaard, J. P., Sterba, H. and von Teuffel, K. (2004). Norway Spruce Conversion—Options and Consequences. Koninklijke Brill, Leiden, The Netherlands.CrossRefGoogle Scholar
Spielman, A. (1994). The emergence of Lyme disease and human babesiosis in a changing environment. Annals of the New York Academy of Sciences 740, 146–156. doi: 10.1111/j.1749-6632.1994.tb19865.x.CrossRefGoogle Scholar
Tack, W., Madder, M., Baeten, L., Vanhellemont, M., Gruwez, R. and Verheyen, K. (2012). Local habitat and landscape affect Ixodes ricinus tick abundances in forests on poor, sandy soils. Forest Ecology and Management 265, 30–36. doi: 10.1016/j.foreco.2011.10.028.Google Scholar
Tack, W., Madder, M., De Frenne, P., Vanhellemont, M., Gruwez, R. and Verheyen, K. (2011). The effects of sampling method and vegetation type on the estimated abundance of Ixodes ricinus ticks in forests. Experimental and Applied Acarology 54, 285–292. doi: 10.1007/s10493-011-9444-6.CrossRefGoogle ScholarPubMed
Tälleklint, L. and Jaenson, T. G. T. (1997). Infestation of mammals by Ixodes ricinus ticks (Acari: Ixodidae) in south-central Sweden. Experimental and Applied Acarology 21, 755–771. doi: 10.1023/A:1018473122070.CrossRefGoogle ScholarPubMed
Tufto, J., Andersen, R. and Linnell, J. (1996). Habitat use and ecological correlates of home range size in a small cervid: the roe deer. Journal of Animal Ecology 65, 715–724. doi: 10.2307/5670.Google Scholar
van Dam, A. P., Kuiper, H., Vos, K., Widjojokusumo, A., de Jongh, B. M., Spanjaard, L., Ramselaar, A. C. P., Kramer, M. D. and Dankert, J. (1993). Different genospecies of Borrelia bugdorferi are associated with distinct clinical manifestations of Lyme borreliosis. Clinical Infectious Diseases 17, 708–717. doi: 10.1093/clinids/17.4.708.Google Scholar
Verkem, S., De Maeseneer, J., Vandendriessche, B., Verbeylen, G. and Yskout, S. (2003). Zoogdieren in Vlaanderen. Ecologie en Verspreiding van 1987 tot 2002. Natuurpunt Studie & JNM-Zoogdierenwerkgroep, Mechelen & Gent, Belgium.Google Scholar
Waterinckx, M. and Roelandt, B. (2001). De Bosinventaris van het Vlaamse Gewest. Ministerie van de Vlaamse Gemeenschap, Afdeling Bos & Groen, Brussel, Belgium.Google Scholar
Wielinga, P. R., Gaasenbeek, C., Fonville, M., de Boer, A., de Vries, A., Dimmers, W., Akkerhuis Op Jagers, G., Schouls, L. M., Borgsteede, F. and van der Giessen, J. W. B. (2006). Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in The Netherlands. Applied and Environmental Microbiology 72, 7594–7601. doi: 10.1128/AEM.01851-06.CrossRefGoogle ScholarPubMed
Wilson, M. L. (1986). Reduced abundance of adult Ixodes dammini (Acari: Ixodidae) following destruction of vegetation. Journal of Economic Entomology 79, 693–696.CrossRefGoogle ScholarPubMed
World Health Organization (2004). The Vector-borne Human Infections of Europe: Their Distribution and Burden on Public Health. World Health Organization, Copenhagen Denmark.Google Scholar