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Many macroparasites change their host species during their life cycle. Frequently, one or more asexual larval stages live in prey species and develop to an adult sexual stage in a predator species. It is assumed that a parasite enhances its transmission rate by having a larval stage in an abundant intermediate host that is a frequent prey species for a final host (Choisy et al. 2003), and that this strategy also increases the chances of finding a sexual mate (Brown et al. 2001). In addition, the different temporal and spatial dynamics of intermediate and definitive host species could enhance dispersal and increase the persistence of a parasite population (Mackiewicz 1988). However, this alternation between species makes a parasite dependent on the prey–predator interaction, and changes in food acquisition by the definitive host (which can be caused by factors such as environmental change) could adversely affect the parasite's life cycle (Mackiewicz 1988).
The prey–predator interplay is therefore a key factor in understanding the transmission dynamics of obligatory heteroxenous parasites such as cestodes. For example, the small fox tapeworm Echinococcus multilocularis Leuckart is a zoonotic parasite with a dixenous life cycle (Eckert & Deplazes 2004). The adult, intestinal stage lives in various carnivores and eggs are excreted in faeces. Intermediate hosts are infected by ingestion of these eggs and harbour the parasite's larval stage (metacestode) in their liver. To complete the life cycle of the parasite, a definitive host must ingest fully developed metacestodes by preying on infected intermediate hosts.
In east and central Europe, the main definitive host is the red fox (Vulpes vulpes L.), with arvicolid species, predominantly the common vole (Microtus arvalis Pallas) and the fossorial form of the water vole (Arvicola terrestris scherman L.), acting as intermediate hosts (Eckert 1998). Although E. multilocularis is remarkably prevalent in foxes in endemic areas (20–70% individuals are infected), prevalence rates in intermediate species are generally low (<1–6%) (Eckert 1998), and rarely exceed 20% (Gottstein et al. 1996; Henttonen et al. 2001) with infection recorded only occasionally in murid rodents (Eckert et al. 2001).
In the city of Zurich, the prevalence of E. multilocularis in foxes varies both temporally and spatially, with the highest prevalence rate (47%) occurring in winter (Hofer et al. 2000). Prevalence rates in potential intermediate host species are also variable, being remarkably high in water voles (22%), substantially lower in both common voles (4·9%) and bank voles (Clethrionomys glareolus Schreber) (2·4%), and zero in wood mice (Apodemus sylvaticus L.) and yellow-necked mice (Apodemus flavicollis Melchior) (Stieger et al. 2002; unpublished data). These different rodent species exhibit distinct differences in ecology and habitat preferences: arvicolid species (A. terrestris and M. arvalis) live mainly in meadows and pastures, whereas murid species (e.g. A. sylvaticus) prefer bushy habitats with more shelter, such as forests and hedges (Hausser 1995), but can also reach high density in urban habitats such as public parks and residential areas (Dickman & Doncaster 1987). Consequently, we would expect (1) the distribution of rodent species to vary with the size and fragmentation of these key habitat types in the urban environment; (2) that this variation would be reflected in the diet of the red fox; and (3) that this would, in turn, affect the transmission dynamics of E. multilocularis.
Central Zurich is a densely built urban area which is ringed by residential areas with more green space; beyond the city border are rural areas dominated by forests and agriculture. Within the urban area a high supply of anthropogenic food is available for urban foxes (Contesse et al. 2004). Thus we made the following predictions: (1) the supply of suitable habitat for voles – and thus their availability – decreases from peri-urban areas towards urban areas; (2) as a functional response, foxes in urban areas would consume fewer voles and more anthropogenic food sources than in the adjacent peri-urban area; and (3) the prevalence of E. multilocularis in foxes would correspond to the predation rate of suitable intermediate hosts.
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Parasites depending on a prey–predator system are limited to locations where the distributions of definitive and intermediate hosts intersect. Their occurrence and persistence depend on the availability of host species and the specific environmental conditions that enable the survival of free-living stages.
Our data indicate that the supply of intermediate hosts for E. multilocularis is strongly reduced in urban areas. The intermediate hosts A. terrestris and M. arvalis are strongly associated with meadows and pastures (Hausser 1995), but these habitats were 12·3 times less abundant in the urban area than in the adjacent border area (Fig. 2a). Furthermore, meadows and pastures sustained substantially lower densities of A. terrestris in the urban zone (Fig. 2b), possibly because of the increased fragmentation of these habitats, which would affect the connectivity of subpopulations, and because of the lower dispersal potential of arvicolid species relative to murid species (Dickman & Doncaster 1989). Consequently, the rodent community in the urban zone is likely to consist of a substantially greater proportion of murid species.
Predation by foxes on A. terrestris and M. arvalis correlates in general with the abundance of these two prey species (Weber & Aubry 1993; Kjellander & Nordström 2003), with foxes switching to alternative prey when voles become rare (Kjellander & Nordström 2003). Few signs of the arvicolid M. arvalis were detected in the meadows and pasture investigated here, although we recorded M. arvalis as frequently as A. terrestris in fox stomachs. Despite their dietary plasticity, different studies point out that foxes show preferences for certain prey species (Macdonald 1977; Green 2002). Microtus species appear to be more attractive than other arvicolid species, and arvicolid species in general are more attractive than murid species (Macdonald 1977). Correspondingly, we found that the decrease in predation on vole species (Fig. 2c,d) was much less pronounced than one would expect given the observed decrease in the supply of vole prey towards the city centre (Fig. 2a,b).
Nevertheless, in accordance with prediction 2, the analyses of stomach content indicate that foxes can shift their diet to murid species (which are less susceptible to E. multilocularis infection) if arvicolid species are rare (Fig. 2d). In addition, the total predation rate on rodents was significantly lower for foxes in urban areas than for foxes in the urban periphery, further reducing the total uptake of intermediate hosts (Fig. 2c). This functional response may be caused by the surplus of anthropogenic food accessible to foxes in urban areas, reflected in the increased contribution of such items to the fox diet (Fig. 2e).
A high amount of anthropogenic food available enables foxes to fulfil their requirements within small home ranges encompassing not more than 30 ha (Gloor 2002). We have shown in a preceding experimental study that this small-scale spatial organization of urban foxes is reflected in a low spatial dynamic of the life cycle of E. multilocularis. In six areas, each 1 km2, foxes were dewormed regularly by the delivery of anthelmintic baits over 2 years. However, the effect of this treatment was detectable only within a range of 500 m around the baiting areas (Hegglin et al. 2003). This finding corresponds to the manifold decrease of E. multilocularis prevalence within a distance of not more than 500 m along the urban periphery (prediction 3; Fig. 2f). Hence we believe that the low supply of suitable intermediate hosts and the high levels of anthropogenic food sources available, combined with the resulting small-scale spatial organization of urban foxes, are responsible for the pronounced differences in the prevalence of E. multilocularis over small distances.
Conversely, however, anthropogenic food sources could enhance the transmission of E. multilocularis by increasing host densities. In urban areas, fox densities can exceed 10 adults per km2, much higher than observed in rural areas (Baker et al. 2000; Gloor 2002). Thus the transmission of E. multilocularis could be especially intense in the transition zone between urban and peri-urban areas where high fox population densities are sustained by high anthropogenic food resources and suitable habitat for arvicolid species is abundant (Deplazes et al. 2004).
Our results suggest that the temporal and spatial dynamics of E. multilocularis is also affected by the age structure of fox populations. In juvenile foxes, the spatial variation of the prevalence rates was less pronounced than in adult foxes. This may reflect the spatial behaviour of juvenile foxes, which frequently show exploratory behaviour and/or disperse before they establish a territory. Furthermore, dispersion occurs mainly during late autumn and winter (Trewhella 1988), the period when the prevalence in juvenile foxes was highest in our study. Thus juvenile foxes may have best access to voles, and their roaming behaviour may play an important role in the spread of this parasite.
The larval stage of E. multilocularis can cause human alveolar echinococcosis, a severe helminthic zoonosis which is fatal if left untreated (Ammann & Eckert 1995). However, low incidence rates of human alveolar echinococcosis have been recorded in Europe to date (Kern et al. 2003). Apart from individual risk factors (e.g. owning dogs, living in a farmhouse; Kern et al. 2004), ecogeographical factors such as a high vole densities appear to increase the risk for human alveolar echinococcosis (Viel et al. 1999). The growing fox population in Western Europe (Chautan, Pontier & Artois 2000), and the newly observed colonization of urban habitats in many central European cities (Gloor et al. 2001), raise concern about the risk of a possible increased infection pressure for this disease in densely populated areas (Eckert & Deplazes 2004). Therefore knowledge about the factors affecting the population dynamic of this zoonotic parasite is relevant to public health.
This study confirmed our predictions that the relative supply of arvicolids does correlate with the predation of foxes on these rodent species and, as a consequence, corresponds with the spatial differences in the prevalence of E. multilocularis in foxes. Our results support the hypothesis that the supply of prey species, acting as intermediate hosts, and the abundance of alternative food sources, can significantly affect the population dynamics of dixenous parasites and confirm the crucial role of plasticity in predation behaviour of definitive hosts for this type of parasite. Hence the functional response of final hosts to a varying supply of intermediate hosts and alternative food sources can be considered as a key factor for the transmission dynamics of parasites that depend on a predator–prey interplay.