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

Parasitology

Volumn 139, Issue 10, 2012, Pages 1273-1281

  Tack, W ^a   Madder, M ^b,c   Baeten, L ^a   De Frenne, P ^a,d   Verheyen, K ^a  

^a GHENT UNIVERSITY   (Belgium)

^b INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^c UNIVERSITY OF PRETORIA   (South Africa)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Borrelia burgdorferi; forest conversion; habitat; Ixodes ricinus; roe deer; tick

Indexed keywords

AIR TEMPERATURE; ARTICLE; BELGIUM; BORRELIA; DEER; FOREST; FOREST STAND; FORESTRY; HABITAT USE; HUMIDITY; INFECTION RATE; IXODES RICINUS; LYME DISEASE; NONHUMAN; NYMPH; OAK; PINE; PLANTATION; PRIORITY JOURNAL; SEASONAL VARIATION; SHRUB; TICK; TREE;

ANIMALS; BELGIUM; BORRELIA; DEER; ECOSYSTEM; IXODES; LARVA; NYMPH; POPULATION DENSITY; TREES;

BORRELIA; BORRELIA BURGDORFERI; CAPREOLUS; CERVIDAE; IXODES RICINUS; IXODIDA;

EID: 84866113439     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182012000625     Document Type: Article

References (53)

1. 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. (Pubitemid 36234419)
2. 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.
3. 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).
4. 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. (Pubitemid 46657347)
5. Bolker, B. M. (2008). Ecological Models and Data. Princeton University Press, Princeton, NJ, USA.
6. Boom, R., Sol, C. J. A., Salimans, M. M. M., Jansen, C. L., Wertheimvan 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. (Pubitemid 20078123)
7. 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.
8. 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. (Pubitemid 41548455)
9. Burnham, K. P. and Anderson, D. R. (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer, New York, USA.
10. 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.
11. 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. (Pubitemid 44061277)
12. 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.
13. 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. (Pubitemid 33614599)
14. 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. (Pubitemid 41739993)
15. 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.
16. 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. (Pubitemid 352773568)
17. Gill, R. M. A. (1990). Monitoring the Status of European and North American Cervids. Global Environment Monitoring System, United Nations Environment Programme, Nairobi, Kenya.
18. Gray, J. S. (1998). The ecology of ticks transmitting Lyme borreliosis. Experimental and Applied Acarology 22, 249-258. doi: 10.1023/A:1006070416135. (Pubitemid 28214173)
19. 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.
20. 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 tickborne pathogens in Ixodes ricinus ticks in pastures and woodlands. Applied and Environmental Microbiology 76, 4413-4420. doi: 10.1128/AEM.00610-10.
21. 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. (Pubitemid 36246195)
22. Hillyard, P. D. (1996). Ticks of North-West Europe. The Natural History Museum, London, UK.
23. 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. (Pubitemid 28243244)
24. 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. (Pubitemid 29043560)
25. 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.
26. 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.
27. Jongejan, F. (2001). Teken en door Teken Overgedragen Ziekten. Stichting Diergeneeskundig Memorandum, Boxtel, The Netherlands.
28. 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. (Pubitemid 28188367)
29. 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.
30. 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. (Pubitemid 38390754)
31. 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.
32. 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. (Pubitemid 37435729)
33. 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. (Pubitemid 29188188)
34. Piesman, J. and Gern, L. (2004). Lyme borreliosis in Europe and North America. Parasitology 129 (Suppl.), S191-S220. doi: 10.1017/S0031182003004694. (Pubitemid 40780696)
35. 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. (Pubitemid 43194214)
36. 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).
37. 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.
38. 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. (Pubitemid 41597237)
39. 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.
40. Smith, H. D., Oveson, M. C. and Pritchett, C. L. (1986). Characteristics of mule deer beds. Great Basin Naturalist 46, 542-546.
41. 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.
42. 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.
43. 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.
44. 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.
45. 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.
46. 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. (Pubitemid 28014008)
47. 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.
48. 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. (Pubitemid 23293384)
49. 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.
50. Waterinckx, M. and Roelandt, B. (2001). De Bosinventaris van het Vlaamse Gewest. Ministerie van de Vlaamse Gemeenschap, Afdeling Bos & Groen, Brussel, Belgium.
51. 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. (Pubitemid 44927661)
52. Wilson, M. L. (1986). Reduced abundance of adult Ixodes dammini (Acari: Ixodidae) following destruction of vegetation. Journal of Economic Entomology 79, 693-696.
53. World Health Organization (2004). The Vector-borne Human Infections of Europe: Their Distribution and Burden on Public Health. World Health Organization, Copenhagen Denmark.