INTRODUCTION
A core assumption in the population dynamic theory of parasites is the existence of a positive relationship between parasite transmission rates and host population densities (e.g. Anderson and May, Reference Anderson and May1978). This relationship is expected to give rise to a curvilinear asymptotic increase in the abundance of parasites with increasing host densities (Arneberg et al. Reference Arneberg, Skorping, Grenfell and Read1998). However, while a positive relationship between parasite abundance and host density has been found for many directly transmitted helminths (e.g. Arneberg et al. Reference Arneberg, Skorping, Grenfell and Read1998), few studies have shown such a pattern for helminths that have intermediate hosts in their life cycle (e.g. Haukisalmi and Henttonen, Reference Haukisalmi and Henttonen1990; Decker et al. Reference Decker, Duszynski and Patrick2001; Deter et al. Reference Deter, Berthier, Chaval, Cosson, Morand and Charbonnel2006; Hegglin et al. Reference Hegglin, Bontadina, Contesse, Gloor and Deplazes2007). This poor fit between theory and field observations may have a plethora of reasons, including poor estimates of the density of the available intermediate and definitive host species, and unaccounted for variability due to (1) delays in the dynamics of the parasite populations in relation to the host populations, (2) extrinsic (environmental) factors, (3) host age structure, and (4) immune responses and other density-dependent processes in the parasite population. In the High Arctic, the available number of host species is low. This makes parasite transmission networks relatively simple, and may therefore make it simpler to estimate the relationship between host densities and parasite abundances.
On the High Arctic islands of Svalbard, the Arctic fox is the terrestrial top predator and a main scavenger of carcasses. Only 2 other terrestrial mammalian species are present, the Svalbard reindeer (Rangifer tarandus platyrhynchus) and the sibling vole (Microtus levis, earlier known as M. rossiaemeridionalis). The Arctic fox and the Svalbard reindeer are native species found throughout the Svalbard archipelago. In contrast, the spatial distribution of the introduced sibling vole is restricted to an 8 km stretch of coastline on the main island, Spitsbergen (Fredga et al. Reference Fredga, Jaarola, Ims, Steen and Yoccoz1990; Yoccoz et al. Reference Yoccoz, Steen and Ims1990).
The Arctic fox on Svalbard is known to be the natural definitive host of the cestode Taenia krabbei which uses the reindeer as its obligatory intermediate host (Bye, Reference Bye1985). In addition, metacestodes of Echinococcus multilocularis were detected in the sibling vole population on Svalbard in 1999 (Henttonen et al. Reference Henttonen, Fuglei, Gower, Haukisalmi, Ims, Niemimaa and Yoccoz2001). The typical life cycle of E. multilocularis is sylvatic with foxes (Vulpes vulpes, V. lagopus) as definitive hosts (Rausch, Reference Rausch, Thompson and Lymberty1995; Eckert and Deplazes, Reference Eckert and Deplazes2004). On Svalbard, the infection risk to Arctic foxes is restricted by the spatial extent of the sibling vole population. This causes spatial aggregation in the distribution of infected foxes and, accordingly, an E. multilocularis coproantigen survey found infected Arctic fox scats only in the immediate surroundings of the vole population (Fuglei et al. Reference Fuglei, Stien, Yoccoz, Ims, Eide, Prestrud, Deplazes and Oksanen2008).
The low biodiversity of terrestrial vertebrates on Svalbard makes their parasite communities simple with no alternative host species. Here, we analyse data on intestinal parasites of Arctic foxes (Vulpes lagopus) on Svalbard. We report the results from a survey of intestinal parasites of Arctic foxes, and include data from the sibling vole population on the prevalence of its vole transmitted cestodes. The focus of our analysis is on the relationship between the prevalence of the parasites and spatial patterns in the distribution and abundance of available intermediate hosts. In particular, we investigate the importance of the distance from the trap site of the foxes to the area occupied by the sibling vole population, and the reindeer density around the fox-trapping sites for parasite prevalences. In addition, patterns of infection in relation to host age and sex are reported.
MATERIALS AND METHODS
Arctic fox samples
Arctic foxes were harvested on Svalbard by fur trappers using baited traps between November 1 and March 15. A sample of 353 foxes from the 8 trapping seasons, 1996–97 (n=10), 1997–98 (n=108), 1998–99 (n=48), 1999–2000 (n=32), 2000–01 (n=21), 2001–02 (n=110), 2002–03 (n=17), and 2003–04 (n=7) was available for the present study. To remove the laboratory hazard associated with potentially E. multilocularis positive carcasses, the carcasses were frozen at −80°C for a minimum of 7 days (Veit et al. Reference Veit, Bilger, Schad, Schäfer, Frank and Lucius1995). Later storage was at −20°C until necropsy.
The ages of 294 of the foxes were determined by counting the annuli in the cementum of a sectioned canine tooth (Grue and Jensen, Reference Grue and Jensen1976). Mean age was 1·8 years (s.e.=0·12), and the oldest fox was a 13-year-old female.
For 300 of the fox samples the trappers had reported a trapping location. However, only the location of the trapping station was reported for most samples from 2 of the trapping stations and it was assumed that the foxes were trapped locally. All of the samples with a reported trapping location were from Spitsbergen, the largest island in the Svalbard archipelago (Fig. 1). The study area was divided in two by the fjord Isfjorden. The ice cover on this fjord varies substantially among and within winters depending on temperature and wind conditions. This made it difficult to devise an exact continuous measure of shortest fox dispersal distances from the sibling vole population. To overcome this problem we grouped the samples according to distance from the vole site in the euclidean distance classes 0–10 km, 10–20 km, 20–40 km, 40–70 km, and >70 km (Fig. 1), as this grouping gives a similar order for the samples regardless whether euclidean or land – line distances were considered. In addition, the foxes were classified with respect to which reindeer management area they were trapped in. The investigated foxes were all trapped in reindeer management areas R1, R5, R6 or R7 with associated crude density estimates of 0·41, 0·46, 0·13 and 2·19 reindeer per km2 (The Governor of Svalbard, unpublished report). The Arctic fox abundance is monitored only in a fraction of the total trapping area so that similar data on the spatial variation in the fox population density were not available.
Fig. 1. The sample sites of Arctic foxes on Spitsbergen, Svalbard (black circles) with sample sizes given on a continuous scale by the size of the circles (scale given in the left part of the figure). The distances of 10, 20, 40 and 70 km from the vole population in Grumant shown as dashed grey circles. The dashed black lines give the borders between reindeer management district R1 and R5-7. The inserted map of Svalbard, with lines giving latitudinal degrees north and longitudinal degrees east, show the position of the more detailed map of the sampling area on Spitsbergen (rectangle).
Sibling vole samples
Sibling voles were caught in August every year using snap traps: 2001 (n=123), 2002 (n=10), 2003 (n=48), 2004 (n=46), 2005 (n=124), 2006 (n=36). The traps were placed out on the 3 sites used by Henttonen et al. (Reference Henttonen, Fuglei, Gower, Haukisalmi, Ims, Niemimaa and Yoccoz2001) and 1 additional site within the 8 km stretch of coastline with suitable vole habitat. In addition, a sample of voles caught in live traps in the core sibling vole site was sacrificed in September 2003 (n=87) and 2006 (n=32). The voles caught in snap traps were dissected immediately after capture, while the voles caught in live traps were euthanized and kept cool (0–5°C) for the first 2–3 days and kept frozen thereafter until dissection. At dissection, vole sex, body weight and length to the base of the tail were recorded.
Parasitological investigations
The Arctic fox intestines were dissected at the Vantaa Research Unit of the Finnish Forest Research Institute. The small intestines were examined in 6 equally long sections and with the caecum as a seventh section. Each section was slit longitudinally, and the intestinal content and scraped mucosa were examined thoroughly under a dissecting microscope.
Voles were investigated macroscopically for metacestodes. All the livers of voles were checked for E. multilocularis infection and the maximum cyst diameters were measured using a ruler. During dissection of snap-trapped voles, the existence of Taenia polyacantha in the vole populations was confirmed twice by the finding of 1 infected vole in 2004 and 2 infected voles in 2005. However, only in the live-trapped voles were subcutaneous tissues and body cavities consistently investigated for Taenia crassiceps and T. polyacantha.
The nematodes and acanthocephalans found in the Arctic fox were transferred directly to 70% EtOH. The adult nematodes were all found to be ascaridoid nematodes. Male and juvenile nematodes could not be fully identified to species by the methods used by us, while female Toxascaris leonina nematodes were separated from the related Toxocara canis based on the shape and surface structure of their eggs. The presence of T. leonina was confirmed in a subsample of female nematodes investigated, while no T. canis were found. T. leonina has also been the dominant ascaridoid present in other Arctic fox populations studied (Rausch et al. Reference Rausch, Fay and Williamson1983, Reference Rausch, Fay and Williamson1990; Skirnisson et al. Reference Skirnisson, Eydal, Gunnarsson and Hersteinsson1993; Kapel and Nansen, Reference Kapel and Nansen1996). However, the large numbers of unidentified nematode individuals in the samples cannot exclude the possibility that T. canis was present also at a low prevalence.
The adult tapeworms were transferred to tap water where they were washed and relaxed for a few hours. The Taenia species were identified microscopically, primarily following Loos-Frank (Reference Loos-Frank2000), by the number, size and shape of the rostellar hooks using glycerine-ethanol (70%) preparations. It is our long-term experience that microscopic identification of these cestode species works well also on previously frozen samples. In addition to microscopic identification, the identification of T. crassiceps from a sibling vole and the Arctic fox, and a T. polyacantha from the Arctic fox, was confirmed using molecular methods (see Table 1 in Lavikainen et al. Reference Lavikainen, Haukisalmi, Lehtinen, Henttonen, Oksanen and Meri2008). As E. granulosus is absent on Svalbard, adult E. multilocularis specimens were in general identified by the characteristic Echinococcus morphology. This identification was confirmed on a sample of 12 adult Echinococcus specimens, collected from 3 foxes, that were stained with iron-acetocarmine and identified as E. multilocularis by the position of the genital pores in mature segments and the number and distribution of testes (see Rausch, Reference Rausch1956 and Thompson, Reference Thompson, Thompson and Lymbery1995 for the identification of Echinococcus species). The identification of E. multilocularis metacestodes in the livers of voles was based on their characteristic structure with small fluid-filled pockets that contain protoscolices in mature metacestodes. This species identification was confirmed on a subsample of 10 mature metacestodes, for which the protoscolices were checked microscopically for the characteristic hook pattern. Very small metacestodes (<5 mm diameter) cannot be identified with certainty macroscopically; however, excluding these small cysts from the statistical analyses did not affect any conclusions. The identity of E. multilocularis metacestodes in the sibling voles on Svalbard has previously been confirmed using molecular methods (Henttonen et al. Reference Henttonen, Fuglei, Gower, Haukisalmi, Ims, Niemimaa and Yoccoz2001).
Table 1. Number of positive samples (n) and prevalence with 95% CI for the different parasite species found in the 353 arctic foxes from Spitsbergen, Svalbard
Statistical analyses
Prevalence data were analysed using logistic regression. The predictor variables used when analysing the fox data were distance from the vole population fitted as a 5 level factor, reindeer density, fox sex and age, and year of sampling. In addition, we investigated whether the prevalence of the parasite species differed between foxes trapped ⩽10 km from the sea and more inland (>10 km from the sea), but found no effect of distance to the sea for any of the parasite species investigated (all P values >0·20). Fox age was investigated both as a linear term, a second order polynomial, fitted as a 4 level factor with animals grouped as juveniles, 1 year olds, 2–5 year olds and ⩾6 year olds, and investigated using a smoothing spline (Wood, Reference Wood2006). The predictor variables when analysing the vole data were sample site, vole sex and length, and year of sampling. Model selection was based on the AIC criterion given by AIC=−2 Log likelihood+2*np, where np is the number of parameters estimated in the model (e.g. Wood, Reference Wood2006). As recommended by Agresti and Coull (Reference Agresti and Coull1998), score test based confidence limits were calculated for the proportions reported in Table 1, Fig. 2 and Fig. 5. Logistic regression model parameters and predicted effects are given ±1 s.e. The goodness of fit of the logistic regression models was checked using the method of le Cessie and van Houwelingen (Reference Le Cessie and Van Houwelingen1991).
Fig. 2. Prevalence (%, ±95% CI) of the most common parasites found in the Arctic foxes with known trapping location, plotted against their distance (km) from the vole population at Grumant. Sample sizes for each distance class are given along the top row. T. polyacantha, T. crassiceps and E. multilocularis all use the voles as intermediate hosts, T. krabbei uses reindeer as intermediate host and the ascaridoid nematodes have a direct life cycle, but may also use paratenic hosts.
RESULTS
The Arctic fox
The parasite fauna found in the small intestine of the 353 Arctic foxes included the previously documented cestodes E. multilocularis and T. krabbei. In addition, the cestodes T. crassiceps and T. polyacantha were found for the first time on Svalbard. Both species use rodents as intermediate hosts, and therefore depend on sibling voles as their intermediate host on Svalbard. Three additional parasites were found: a cestode (Diphyllobothrium sp.), ascaridoid nematodes (probably predominantly T. leonina), and an unidentified acanthocephalan. Of these, Diphyllobothrium sp. and the acanthocephalan occurred in very few hosts (1–2% prevalence, Table 1), while the ascaridoid nematodes were common (33%, Table 1). The most prevalent parasite in the Arctic fox was T. krabbei (50%, Table 1). The vole-transmitted cestodes, E. multilocularis, T. crassiceps and T. polyacantha, occurred in 8–14% of the foxes and showed a high degree of species co-occurrence with 50% of the infected foxes (n=61) being infected with more than one of these species.
The prevalence of the vole-transmitted cestodes was highest (27–46%) in Arctic foxes caught adjacent (0–10 km distance) to the vole population and decreased with increasing distance to the sibling vole population (Fig. 2). However, a low number of foxes (n=8), of which 3 were infected with E. multilocularis, were found infected with these parasites more than 70 km from the vole site. In our dataset, all of these long-distance dispersal events occurred in the winter 1997–98. This was a winter with an exceptionally extensive ice cover on the fjords on the west coast of Spitsbergen and this may have facilitated the long distance dispersal events.
When the effect of distance to the vole population was controlled for using logistic regression, there was no evidence for a difference between foxes of different sex or age with respect to their prevalence of E. multilocularis or prevalence of T. crassiceps (all P values >0·18). The prevalence of T. polyacantha showed, however, evidence for an increase with age that predominantly was due to a lower prevalence in animals in their first year of life than in older foxes (Table 2). Prevalence of T. polyacantha increased from an estimated 30% in the youngest age class to 67% in older foxes trapped 0–10 km from the vole site (Table 2). As expected, none of the vole-transmitted cestodes showed evidence of a change in prevalence associated with reindeer density (all P values >0·17).
Table 2. Analysis of deviance table and parameter estimates with s.e. for the logistic regression model analysing the prevalence of T. polyacantha in Arctic foxes
(The factor predictor variables ‘distance to the vole site’ and age >1 years were added sequentially for the analysis of deviance and the intercept was excluded when estimating the model parameters.)
The prevalence of T. krabbei was not related to distance from the vole site (P=0·41), but increased with both host age and reindeer density (Table 3). However, the sample of male foxes from the reindeer management district with the lowest reindeer density had a high prevalence of infection, suggesting that the positive effect of reindeer density was mainly valid for female foxes (Table 3, Fig. 3).
Fig. 3. Estimated (±95% CI) and predicted prevalence (%, ±1 s.e.) of T. krabbei in male (filled circles and top line) and female (open circles and lower line) 1-year-old Arctic foxes in relation to estimated reindeer density (km−2) in the trapping area. Predictions are based on the model given in Table 2 and point estimates are based on the same model structure, but with reindeer density fitted as a factor. Samples sizes are given for male (above) and female (below) foxes.
Fig. 4. Estimated (±95% CI) and predicted prevalence (%, ±1 s.e.) of ascaridoid nematodes in relation to fox age for foxes trapped 0–10 km from the vole site. Predictions are based on the model given in Table 4 and the point estimates are based on the same model structure, but with fox age fitted as a factor. Sample sizes within each age are given above the point estimates. Confidence limits have not been drawn for sample sizes <5.
Table 3. Analysis of deviance table and parameter estimates with s.e. for logistic regression model analysing the prevalence of T. krabbei in Arctic foxes. Terms were added sequentially
As found for the vole-transmitted cestodes, the prevalence of the ascaridoid nematodes decreased also with increasing distance to the vole site (Table 4), while it showed no relationship to reindeer density (P=0·48). In addition, its prevalence decreased with fox age, the best description of this relationship being a second order polynomial (Table 4, Fig. 4).
Table 4. Analysis of deviance table and parameter estimates with s.e. for the logistic regression model analysing the prevalence of ascaridoid nematodes in Arctic foxes
(The predictor variables ‘distance to the vole site’ and terms in the second order polynomial model for ‘age’ were added sequentially for the analysis of deviance and the intercept was excluded when estimating the model parameters.)
Cestode infections in the sibling vole population
In the voles caught using snap traps the overall prevalence of E. multilocularis infection was 19%. As found by Henttonen et al. (Reference Henttonen, Fuglei, Gower, Haukisalmi, Ims, Niemimaa and Yoccoz2001), the prevalence of E. multilocularis increased with increasing body size of the voles (Table 5), which is related to age and maturity. The smallest vole found infected was 95 mm long. This minimum size probably reflects the minimum vole age at which the parasite has been able to develop to a macroscopically detectable size. To remove some of the vole size-dependent variability in the prevalence of E. multilocularis we focused on voles of more than >100 mm length. In this subsample of voles, the prevalence showed a complex pattern with differences between sample sites, with year of sampling and vole length, and with two-way interactions between sample site and year, and sample site and vole length (Table 6). However, contrary to the findings of Henttonen et al. (Reference Henttonen, Fuglei, Gower, Haukisalmi, Ims, Niemimaa and Yoccoz2001), there was little evidence for a difference in E. multilocularis infection between male and female voles (P=0·22). In one of the sites we obtained a reasonable sample of voles every year (n=10–81 voles per year) using 100 trap-nights each year. In this site there was a positive correlation between the prevalence of E. multilocularis in voles more than 100 mm long and the number of voles caught the same year, giving evidence of a density-dependent transmission rate (r=0·93, P=0·01, Fig. 5), and no evidence of the expected positive lagged effect of vole density on the prevalence the following year (r=−0·68, P=0·20).
Fig. 5. Prevalence of Echinococcus multilocularis (±95% CI) in sibling voles with body length >100 mm, in relation to the number of voles caught at the site the same year. The year of sampling is given above the estimate.
Table 5. The prevalence of E. multilocularis infection in sibling voles on Svalbard given for different vole sex and length classes
(95% C I given in parentheses.)
Table 6. Analysis of deviance table for the logistic regression model analysing the prevalence of E. multilocularis in sibling voles longer than 100 mm length caught in snap traps
(Terms were added sequentially.)
In the sample of voles thoroughly investigated for T. crassiceps and T. polyacantha, there was an overall prevalence of E. multilocularis in 2003 of 10% (n=79) and of 16% (n=36) in 2006. Two voles were found with T. crassiceps in the 2003 sample (prevalence=2·5%) and none in 2006. No voles with T. polyacantha were found in these samples. Similarly, in the sample of 224 voles from 1999 and 2000 thoroughly examined by Henttonen et al. (Reference Henttonen, Fuglei, Gower, Haukisalmi, Ims, Niemimaa and Yoccoz2001), not a single specimen of T. crassiceps or T. polyacantha was found.
DISCUSSION
Our results show that the prevalence of the intestinal parasites of the Arctic fox on Svalbard, to a large degree, was determined by the abundance and distribution of the intermediate hosts. We found (1) a strong negative relationship between the prevalence of vole-transmitted cestodes (E. multilocularis, T. crassiceps and T. polyacantha) and the distance between the site the foxes were trapped and the vole population on the archipelago; (2) for female foxes a positive correlation between the prevalence of T. krabbei, which uses reindeer as its intermediate host, and the estimated density of reindeer in the area the foxes were trapped; (3) within the vole population, a positive relationship between the prevalence of E. multilocularis and the abundance of voles. In addition, the prevalence of the ascaridoid nematodes showed a negative relationship with distance to the vole population. It is likely that the nematodes were predominantly T. leonina, a common parasite of Arctic foxes which has basically a direct life-cycle, but has been suggested to use rodents as paratenic hosts (Rausch et al. Reference Rausch, Fay and Williamson1990). The elevated prevalence near the vole population may therefore indicate that both the direct and indirect transmission routes are of importance at Svalbard, as has also been suggested for T. leonina in red foxes in Switzerland (Reperant et al. Reference Reperant, Hegglin, Fischer, Kohler, Weber and Deplazes2007).
The finding that the prevalence of the vole-transmitted parasites showed a decrease with increasing distance from the vole population was expected since a similar pattern has previously been documented by E. multilocularis coproantigen analyses on samples of Arctic fox faeces (Fuglei et al. Reference Fuglei, Stien, Yoccoz, Ims, Eide, Prestrud, Deplazes and Oksanen2008). However, while the previous survey showed a very rapid decrease in E. multilocularis prevalence, reaching non-detectable levels at 10 km distance from the vole site, the current study shows that infected foxes may disperse long distances during the approximately 3 months that E. multilocularis survive in the fox gut (Kapel et al. Reference Kapel, Torgerson, Thompson and Deplazes2006). This implies that there is a risk of human E. multilocularis infection all over Svalbard, and, in particular, fox trappers should be aware of this hazard when handling their catch.
The long dispersal distances suggested by the parasitological data are consistent with our current understanding of the spatial ecology of the Arctic foxes on Svalbard. Reproducing Arctic foxes on Svalbard defend summer home ranges that vary in area between 4 and 60 km2 (Eide et al. Reference Eide, Jepsen and Prestrud2004). However, food availability decreases dramatically after the migrating birds have left Svalbard by October and carcasses from reindeer and seals are not available until late winter (Prestrud, Reference Prestrud1992). Thus, Arctic foxes on Svalbard need to have an opportunistic strategy and behaviour to survive the long and dark winter, increasing the likelihood for long migrations. In particular non-breeding individuals seem to have a migratory behaviour and may roam over areas of 500–1000 km2 or more (Frafjord and Prestrud, Reference Frafjord and Prestrud1992).
The prevalence of the vole-transmitted cestodes in the fox did not reflect their prevalence in the intermediate host. In the sibling vole population, the overall prevalence of E. multilocularis was 19%, while both T. crassiceps and T. polyacantha existed at prevalences close to zero. In contrast, all 3 species were found at similar prevalences in the fox population. Such a pattern has previously also been reported by Rausch et al. (Reference Rausch, Fay and Williamson1990) on St Lawrence Island. The difference between the parasite species in prevalence of infection in the 2 host species may be due to differences between the species in demographic rates, transmission rates and their sensitivity to host immune responses. We suggest that the pattern could be caused by very high vole consumption by the foxes when voles are available, resulting in a high probability of acquiring all 3 cestode species even at low infection levels in the voles. The finding that 50% of the foxes infected by one of the vole-transmitted cestodes were also infected by one of the other two species, is consistent with this hypothesis. The prevalence of T. polyacantha was slightly elevated in the fox population, when compared to the prevalence of E. multilocularis and T. crassiceps. This is probably due to the higher life expectancy of T. polyacantha in the fox (>2 years, Rausch and Fay, Reference Rausch and Fay1988) when compared to E. multilocularis (3 months, Kapel et al. Reference Kapel, Torgerson, Thompson and Deplazes2006) and T. crassiceps (9 months, Freeman, Reference Freeman1962). When voles are unavailable as prey due to e.g. fox dispersal away from the vole site, extensive snow cover or vole population crashes (Yoccoz and Ims, Reference Yoccoz and Ims1999), T. polyacantha infections will then remain for longer in the foxes than the other two species. Also the increase in T. polyacantha prevalence with fox age supports the notion of a high life expectancy in the fox.
Several studies have previously shown that the prevalence or abundance of E. multilocularis decrease with the age of its definitive host (Rausch et al. Reference Rausch, Fay and Williamson1990; Torgerson, Reference Torgerson2006), a pattern that may indicate that the host responds to infection with efficient acquired immunity (Anderson and Gordon, Reference Anderson and Gordon1982; Woolhouse, Reference Woolhouse1993). We found no evidence for such a decrease in the prevalence of the cestode species with host age. However, indicative of such a process being important for the ascaridoid nematodes we found a marked decrease in their prevalence with host age, a pattern also previously reported for T. leonina in Arctic foxes (Rausch et al. Reference Rausch, Fay and Williamson1990; Kapel and Nansen, Reference Kapel and Nansen1996).
The intestinal parasite community of Arctic foxes on Svalbard was dominated by cestodes that use the sibling vole (E. multilocularis, T. polyacantha and T. crassiceps) or reindeer (T. krabbei) as their intermediate hosts. In addition, ascaridoid nematodes with a direct life cycle, which probably also use voles as paratenic hosts, were common. The other parasite species detected use fish or invertebrates as their intermediate hosts and were rare (Diphyllobothrium sp. and an acanthocephalan). As expected from the high arctic location and high degree of isolation, the observed parasite species richness of the Arctic fox population on Svalbard was low when compared to populations investigated in other parts of its distribution range such as Alaska, Iceland and Greenland (Rausch et al. Reference Rausch, Fay and Williamson1983, Reference Rausch, Fay and Williamson1990; Skirnisson et al. Reference Skirnisson, Eydal, Gunnarsson and Hersteinsson1993; Kapel and Nansen, Reference Kapel and Nansen1996). However, the identity and prevalence of the core parasites was well within the range observed in other locations where reindeer and/or rodent intermediate hosts are present.
ACKNOWLEDGEMENTS
We would like to thank the trappers for providing the arctic fox carcasses and especially the local resident trapper Harald A. Solheim who, in addition, provided help with some of the demographic data. Thanks also to the Governor of Svalbard for help with the collection of carcasses from the most remote trapping stations. We thank the Norklima research programme of the Norwegian Research Council, the Norwegian Polar Institute and the Strategic Fund of the Polar Environmental Centre for funding.
