Analysis of the Distribution of the Tick Ixodes Ricinus L. (Acari: Ixodidae) In
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ARTICLE IN PRESS Int. J. Hyg. Environ. Health 212 (2009) 87–96 www.elsevier.de/ijheh Analysis of the distribution of the tick Ixodes ricinus L. (Acari: Ixodidae) in a nature reserve of western Germany using Geographic Information Systems Alexandra Schwarza,Ã, Walter A. Maiera, Thomas Kistemannb, Helge Kampena aInstitute for Medical Microbiology, Immunology and Parasitology, University of Bonn, Germany bInstitute for Hygiene and Public Health, University of Bonn, Germany Received 22 April 2007; received in revised form 9 November 2007; accepted 18 December 2007 Abstract From May to November 2003, at five selected sites of the ‘Siebengebirge’, a nature reserve near Bonn, Germany, data on microclimate, pedology, plant sociology and tick abundance were collected weekly and correlated. A total of 2832 host-seeking Ixodes ricinus (2660 nymphs and 172 adults) were collected, with maximal abundance in June and a minor second increase in abundance in August. The spatial and temporal variation in tick abundance was closely related to the air temperature, relative humidity, soil water content and specific vegetation type. Increases in tick abundances in individual habitats were most likely caused by climate change and/or anthropogenic interventions such as increased numbers of wild boar, a host of I. ricinus. When combined with data from previous investigations a correlation of plant communities with six semi-qualitative tick abundance categories (ranging from ‘no ticks’ to ‘very high tick abundance’) was revealed, and GIS analysis indicated that 56.5% of the ‘Siebengebirge’ is made up of plant communities belonging to the three highest tick abundance categories. Therefore, the risk of visitors in the ‘Siebengebirge’ of being exposed to tick bites and being infected by Borrelia burgdorferi sensu lato had increased. r 2008 Elsevier GmbH. All rights reserved. Keywords: Ixodes ricinus; Tick distribution; Tick abundance; Vegetation type; GIS Introduction plays an outstanding role. Together with I. persulcatus, it is responsible for about 95% of all tick-transmitted In Europe, tick-borne diseases are of greater impor- infectious diseases (Su¨ ss and Schrader, 2004). The tance to humans than infections transmitted by insects geographic distribution of I. ricinus ranges from 601 to (Su¨ ss and Schrader, 2004). Among the hard ticks 401 northern latitude, i.e. from southern Scandinavia to (Ixodidae), which are the most important vectors of the Mediterranean Sea. Furthermore, it occurs in some zoonotic diseases worldwide (Gray, 1991), Ixodes ricinus regions of Asia (Ural mountains) and North Africa (Pe´ rez and Rodhain, 1977). In Germany, I. ricinus is by far the most common species of the tick fauna à Corresponding author at: Sternberg Laboratory, School of (Matuschka et al., 1990). Biological Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Aberdeen AB24 2TZ, UK. Geographic distributions of I. ricinus as well as Tel.: +44 1224 272272; fax: +44 1224 272396. abundances depend on various abiotic and biotic factors E-mail address: [email protected] (A. Schwarz). such as temperature, humidity, vegetation and host 1438-4639/$ - see front matter r 2008 Elsevier GmbH. All rights reserved. doi:10.1016/j.ijheh.2007.12.001 ARTICLE IN PRESS 88 A. Schwarz et al. / Int. J. Hyg. Environ. Health 212 (2009) 87–96 density (Estrada-Pen˜ a, 2001; Lindgren et al., 2000). Kampen et al., 2004; Lindgren et al., 2000). As tick Favoured habitats of this tick are coniferous and mixed infection prevalence is correlated to tick abundance deciduous woodlands (Estrada-Pen˜ a, 2001; Gray, 1991; (Jauda et al., 2004; Kurtenbach et al., 1995), and the Lindstrom and Jaenson, 2003). I. ricinus has no latter to the microclimate, which is correlated with a pronounced host specificity and feeds on about 240 given plant community (Kampen et al., 2004; Kurten- host species (Anderson and Magnarelli, 1993). However, bach et al., 1995), we performed an assessment of the it predominantly infests small rodents (mouse species), I. ricinus distribution in the ‘Siebengebirge’, a nature passerine birds and larger mammals such as hedgehogs, reserve near Bonn, western Germany. Data of tick hares, squirrels, wild boar and roe deer (Mejlon and collections, microclimatic measurements, pedological Jaenson, 1997). and plant sociological surveys at selected sites in the Tick-borne encephalitis and Lyme disease are among ‘Siebengebirge’ and data of previous investigations the most important human infectious diseases trans- in the ‘Siebengebirge’ (Kurtenbach et al., 1995; mitted by I. ricinus in Europe. Viral tick-borne Kurtenbach, 1986, unpublished data) were analysed encephalitis is endemic in most European countries, using Geographic Information Systems (GIS). and 43000 cases are reported annually for Europe including the Baltic States (Haglund, 2002). For Lyme disease caused by spirochetes of Borrelia burgdorferi sensu lato, the estimated annual average incidence for Materials and methods Central Europe ranges from 40 to 300 cases per 100,000 inhabitants (O’Connell et al., 1998). Study area These incidence rates of Lyme disease may be underestimated since Lyme disease is a notifiable disease The nature reserve ‘Siebengebirge’ is a forested only in a few European countries (World Health hilly region (about 4800 ha), which offers an excellent Organization, 2004). In Europe, the infection preva- place for local recreation and tourism (Fig. 1). It is lences of host-seeking I. ricinus with B. burgdorferi sensu located in the south-east of Bonn (50170N, 7160E) and lato vary – depending on the geographical region and consists of about 40 hills with altitudes from 78 to 459 m the developmental stage – from 0% to 11% in larvae, above sea level. The sub-Atlantic climate provides 2% to 43% in nymphs and 3% to 58% in adults mean annual temperatures between 8 and 9 1C and an (Huba´ lek and Halouzka, 1998). average annual precipitation between 650 and 850 mm. Over the last decade, not only tick infection pre- The patchy geological, soil typological and climatic valences with various pathogens but also tick abun- habitat conditions have enabled the development of a dances seem to have increased (Daniel et al., 2004; multifarious and species-rich flora contributing to Fig. 1. Map of Germany and the nature reserve ‘Siebengebirge’ presenting the location of five different plant communities at which I. ricinus had been collected: (1) Luzulo-Fagetum, Fagetum nudum variant, (2) Galio-Fagetum typicum, (3) Fraxino-Aceretum pseudoplatani, (4) Luzulo-Fagetum milietosum, Athyrium filix-femina variant and (5) Luzulo-Fagetum. ARTICLE IN PRESS A. Schwarz et al. / Int. J. Hyg. Environ. Health 212 (2009) 87–96 89 approximately 100 different plant communities (Bouil- Tick collection lon et al., 1994). Data sampling was performed at five sites representing From May to November 2003, host-seeking nymphal different plant communities (Table 1, Fig. 1). Four of and adult ticks were collected once a week either in the these sites (the Fagetum nudum variant of the Luzulo- morning or afternoon by blanket dragging (Estrada- Fagetum typicum, the Athyrium filix-femina variant of Pen˜ a, 2001; Jensen et al., 2000), but only at air the Luzulo-Fagetum milietosum, the Fraxino-Aceretum temperatures between 7 and 24 1C and relative humid- pseudoplatani and the Galio-Fagetum typicum) were ities between 45% and 100%, considering the temporal chosen because in previous surveys, they differed and spatial appetence behaviour of ticks, i.e. during the significantly in I. ricinus abundance and nymphal highest questing activities (Huba´ lek et al., 2003; Perret infection prevalences with borreliae (Kurtenbach et al., et al., 2000). We could verify that weekly collection did 1995; Kurtenbach, 1986, unpublished data). The Luzulo- not cause any systematic or continuous reduction in the Fagetum had not been considered previously. The area tick population during the collecting period. Sampling of each site was about 225 m2, suitable for the evaluation was not carried out, when it was raining or very windy of tick abundances, and still fulfilling the minimum (Huba´ lek et al., 2003). Collected ticks were preserved in requirements of the area size for plant sociological 70% ethanol and identified to species level according to surveys (Glavac, 1996). Hillyard (1996). Table 1. Characteristics of plant communities selected for the tick collections in the ‘Siebengebirge’ Plant community Characteristics Luzulo-Fagetum Fresh and heterogeneous vegetation typea Dominant species: Juncus inflexus, Ilex aquifolium, Oxalis acetosella, Poa nemoralis, Milium effusumb Well-developed herb and shrub layersa Soil: moderate water capacity, nutrient-poor and nutrient-rich, lime-rich and acidic soilsc Luzulo-Fagetum typicum, Fagetum nudum Dry vegetation typea variant Species-poor floraa Dominant species: Luzula luzuloides, Luzula sylvaticab No herb and shrub layers, well-developed leaf litter layera Soil: low to moderate water capacity, nutrient-poor, lime-free and acidicc Luzulo-Fagetum milietosum, Athyrium filix- Wet vegetation typea femina variant Richest plant community in species and plant densitiesa Dominant species: Athyrium filix-femina, Oxalis acetosella, Hedera helixb Lusher herb and shrub layers than the Luzulo-Fagetuma Soil: high water capacity, moderate acidicc Fraxino-Aceretum pseudoplatani Dry to fresh vegetation typea Richer in species than the Luzulo-Fagetum typicuma Dominant species: Dentaria bulbifera, Hedera helix, Viola reichenbachiana,