The Helminth Parasites of Two Sympatric Species of the Genus Apodemus (Rodentia, Muridae) from South-Eastern Slovakia

Home , Apodemus

DOI: 10.2478/s11686–010–0043–1 © W. Stefan´ski Institute of Parasitology, PAS Acta Parasitologica, 2010, 55(4), 369–378; ISSN 1230–2821 The helminth parasites of two sympatric species of the genus Apodemus (Rodentia, Muridae) from south-eastern Slovakia

Jarmila Ondríková1*, Dana Miklisová2, Alexis Ribas3 and Michal Stanko1,2 1Institute of Zoology, Slovak Academy of Sciences, Division of Medical Zoology, Löfflerova 10, 04001 Košice, Slovakia; 2Parasitological Institute, Slovak Academy of Sciences, Hlinkova 3, 04001 Košice, Slovakia; 3Department of Population Biology, Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Studenec 122, 675 02 Koněšín, Czech Republic

Abstract The helminths of two sympatric species of rodents, the striped field mouse Apodemus agrarius and the yellow-necked mouse, Apodemus flavicollis from Slovakia were studied to determine whether there are similarities in the composition of the helminth fauna of two closely related host species living in the same area. A total of twelve species of helminths were identified in these rodent populations, including Brachylaima sp. (Trematoda); Hymenolepis diminuta (Rudolphi, 1819), Mesocestoides sp. larvae, Rodentolepis fraterna (Stiles, 1906), Rodentolepis straminea (Goeze, 1782), Skrjabinotaenia lobata (Baer, 1925), Taenia taeniaeformis larvae (Batsch, 1786) (Cestoda); Aonchotheca annulosa (Dujardin, 1845), Heligmosomoides polygyrus (Du- jardin, 1845), Heterakis spumosa Schneider, 1866, Mastophorus muris (Gmelin, 1790) and Syphacia stroma (Linstow, 1884) (Nematoda). In A. agrarius, H. polygyrus was the most prevalent, as well as the most abundant helminth, but R. fraterna was the species with the highest mean intensity. In contrast, S. stroma dominated the A. flavicollis helminth fauna with the highest prevalence, mean abundance and mean intensity. Both rodent populations harboured nine helminth species, although the mean individual species richness was significantly higher in A. agrarius than in A. flavicollis. The analysis of helminth diversity at both component and infracommunity levels revealed differences between the two rodent populations, which are most likely at- tributable to the specific host ecology.

Keywords Helminth community, Apodemus agrarius, Apodemus flavicollis, Rodentia, Muridae, south-eastern Slovakia

Introduction 1999, Bryja and Rehak 2002). In contrast, A. flavicollis, belonging to the subgenus Sylvaemus, is widespread in the west- Mice of the genus Apodemus Kaup, 1829, are the most wide- ern part of the Palearctic region (Montgomery 1999). spread small rodents in natural habitats such as broadleaf Apodemus agrarius and A. flavicollis are very common forests and fields in the temperate zone of the Palearctic re- small mammals in eastern Slovakia (Stanko 1994). The eco- gion. They depend greatly on forest resources, such as acorns, logical preferences of these species overlap and their popula- insects, and other small vertebrates. Apodemus species show tions frequently coexist sympatrically and even syntopically in a species-specific limited distribution, with two or more many habitats (Stanko et al. 1996). They dominate small species often living together in the same forest (Musser and mammal communities in agricultural landscapes and usually Carleton 1993, Orlov et al. 1996). The striped field mouse, co-occur with several other rodent species, mainly Myodes Apodemus agrarius (Pallas, 1771) and the yellow-necked field glareolus (Schreber, 1780) (Stanko et al. 2004) but they dif- mouse, Apodemus flavicollis (Melchior, 1834) differ in their fer in some respects regarding their habitat preference. The distributions and current spread (Filippucci et al. 2002, yellow-necked mouse is strongly dependent on the forest en- Michaux et al. 2002). A. agrarius, belonging to the subgenus vironment preferring mature deciduous woodlands (Mont- Apodemus, is found across the Palearctic and Oriental regions. gomery 1985), whereas the striped field mouse is a species Its distribution in the Palearctic region is uneven but includes typical of the agricultural field-forest habitat mosaic (Koza- Central and Eastern Europe. In recent decades A. agrarius has kiewicz et al. 1999), and in border areas prefers moist habitats spread westward from Central Europe (Gliwicz and Kryštufek (Zejda 1967).

*Corresponding author: [email protected] 370 Jarmila Ondríková et al.

In Europe, many parasitological studies on the helminth were identified by reference to the original descriptions and communities of small mammals have been reported, focusing the number of each species from each infracommunity was largely on the wood mouse, A. sylvaticus (e.g. Behnke et al. recorded. 1999, Abu-Madi et al. 2000, Goüy de Bellocq et al. 2003, The helminth community composition and structure for Fuentes et al. 2004, Milazzo et al. 2005, Eira et al. 2006), with each rodent species was analysed and the prevalence, mean very few investigating A. agrarius or A. flavicollis. The preva- abundance, mean and median intensity calculated according to lence of helminth species in A. agrarius from Belorussia was Bush et al. (1997).The structure of the helminth component reported by Shimalov (2002) and the metazoan parasite fauna community was studied by determining the number of hel- of A. flavicollis from Germany was described by Klimpel et al. minth species, analysing the frequency of occurrence of each (2007a). Only Hildebrand et al. (2009) have reported the nem- species, the abundance index and the frequency distribution. atode fauna of both the striped field mouse and the yellow- The abundance index AI was calculated for each helminth necked mouse from Poland. In Slovakia, the helminth fauna of taxon after Pence and Eason (1980). The Z-value (prevalence wild rodent species has been monitored for the last fifty years. multiplied by abundance) for each taxon was first calculated, However, these studies focus mainly on faunistics and taxon- then the AI was determined as a percent index of infection by omy (e.g. Erhardova and Rysavy 1955; Erhardova 1956, dividing each Z-value by the sum of all Z-values for species 1958), with few reporting quantitative data on helminth com- with at least one mature individual or 0 otherwise. This index munities (Mituch 1975, Mituch et al. 1987, Stefancikova classifies the species as either: dominant (AI>1), where the et al. 1994). species is strongly characteristic of the community; codomi- Intensive parasitological and epidemiological research nant (0.01≤AI<1), where the species contributes significantly evaluating the importance of small mammals as hosts of a to the community, though to a lesser degree; successful im- wide spectrum of arthropods which are important vectors of migrant (0

ence of the factors on each host. All of 2006 and the follow- and S. stroma were dominant species on the basis of I values. ing winter period were excluded from this analyses (a total of H. polygyrus was the most prevalent as well as most abundant 4 hosts), and all factors have two levels. The analysis for helminth species, but R. fraterna was the species with the prevalences was carried out by using binary logistic regres- highest mean intensity. These two represented 82.8% of all re- sion, while a multifactorial general linear model (GLM) was covered helminths (N = 4213) from A. agrarius individuals. used for the analyses of the rest of the quantitative parame- H. spumosa, H. diminuta and Brachylaima sp. were codomi- ters. The helminth abundance was transformed by ln (x + 1), nant species and contributed significantly to the parasite com- as the aggregated distribution of helminths must be normal- munity of A. agrarius. ized for the GLM method. STATISTICA 9.0 (StatSoft, Inc., The frequency distributions for helminth species recorded 2009) was used for these analyses. in A. agrarius are summarised in Table I. The index of discrepancy D reflected an aggregated frequency distribution for all but H. polygrus species, which had D clearly smaller than Results 1. All but H. polygrus and H. diminuta showed a negative binomial distribution. In this work, a total of 96 striped field mice and 51 yellow- A very low percentage of non-parasitized mice (4.2%) was necked mice were examined for helminths. Twelve species recorded, and hosts with multiple helminth species were rare, were recorded including Brachylaima sp. (Trematoda); Hy- with more than 84% of mice harbouring one or two parasite menolepis diminuta (Rudolphi, 1819), Mesocestoides sp. lar- species with infracommunities of up to four species. The fre- vae, Rodentolepis fraterna (Stiles, 1906), Rodentolepis stra- quency distribution in the number of helminth species showed minea (Goeze, 1782), Skrjabinotaenia lobata (Baer, 1925), a tendency to a Poisson distribution (Fig. 1), although it is not Taenia taeniaeformis larvae (Batsch, 1786) (Cestoda); Aon- aggregated enough (D = 0.259) to fit the negative binomial. chotheca annulosa (Dujardin, 1845), Heligmosomoides poly- However, the frequency distribution of total numbers of gyrus (Dujardin, 1845), Heterakis spumosa Schneider, 1866, helminths in A. agrarius was aggregated, but still did not fit a Mastophorus muris (Gmelin, 1790) and Syphacia stroma (Lin- negative binomial distribution (Table I). stow, 1884) (Nematoda). A summary of the prevalence, abun- The values of the diversity indices reflecting the diver- dance, importance, intensity and distribution characteristics sity/uniformity of the helminth community in A. agrarius are of these helminths is provided in Table I. presented in Table II. No significant differences were found when comparing the prevalence of infection with respect to Characteristics of the helminth community of A. agrarius the sex and age of the hosts (Table III). The overall mean number of helminth species harboured per host was 1.6 ± 0.1 In A. agrarius, 92 individuals (95.8%) carried at least one of (S.E.M.) with non-significant difference between sexes, but a nine helminth species comprising of 1 digenetic trematode significant difference between age groups (t = 3.290, p<0.005), (0.6% of all helminths), 5 cestodes (47.6%) and 3 nematodes as subadult mice harboured the fewest species of helminths. (51.8%). Of these nine helminths, H. polygyrus, R. fraterna Finally, the Brillouin index showed an increase in diversity

Fig. 1. Frequency distribution of the striped field mouse, A. agrarius (black bars) and the yellow–necked mouse, A. flavicollis (grey bars), according to the number of helminth species harboured Helminth diversity of Apodemus in Slovakia 373

Table II. Diversity analysis of helminth communities in A. agrarius maximum number of species recorded in an individual mouse and A. flavicollis was four. However, the percentage of non-parasitized mice and the percentage of mice harbouring two helminth species Index A. agrarius A. flavicollis were unequivocally lower in A. flavicollis than in A. agrarius Species richness 9 9 (Fig. 1), though the stochastic equality of distributions was 1-Simpson 0.65 0.52 not confirmed. Although the index of discrepancy (D = 0.452) Shannon 1.26 1.12 Shannon evenness 0.57 0.51 was greater than for A. agrarius, it was not aggregated enough Berger–Parker 0.44 0.66 to fit a negative binomial distribution. Margalef 0.96 1.20 The frequency distributions of the helminth species in A. flavicollis showed aggregated distribution according to with increasing age of mice and a slightly higher mean value index of discrepancy and, except for S. lobata, fitted a negative for females. binomial (Table I). Unlike A. agrarius, a negative binomial distribution was not rejected for the total number of helminths Characteristics of the helminth community of A. flavicollis found in A. flavicollis. The test of stochastic equality of inten- and comparison with A. agrarius sity distributions confirmed significant differences (Brunner- Munzel test, p<0.005) between distributions of both mice. In A. flavicollis, nine species of helminths were recorded, in- The values of the diversity indices of helminth community cluding 5 cestodes (24.1% of all helminths) and 4 nematodes in A. flavicollis (Table II) indicated lower diversity than in (75.9%) (Table I). Thirty-seven individuals (72.5%) were par- A. agrarius, except equal species richness and Margalef index asitized with at least one of these species, with S. stroma, with opposite tendency. The Shannon index was significantly H. diminuta, H. polygyrus and A. annulosa as dominant greater for A. agrarius than for A. flavicollis (t = 3.373, df = species on the basis of AI values. S. stroma dominated the 1008, p<0.001). helminth fauna with the highest prevalence, mean abundance There was a greater diversity of helminth species (deter- and dominance, representing 66.1% of all recovered helminths mined by the Brillouin value index) in the adult population (N = 800). S. lobata, M. muris and R. straminea were codom- of A. flavicollis than in the subadult population, as well as inant species and contributed significantly to the parasite com- in females compared to males (Table III). A nonsignificant munity of A. flavicollis. but higher prevalence among female mice compared with Generally, A. flavicollis showed significantly lower total males was detected and prevalence of infection significantly prevalence of infection (χ2 = 16.804, df = 1, p<0.001), abun- (χ2 = 11.033, df = 1, p<0.001) increased with age (Table dance (t = 2.925, p<0.01), and median intensity (t = 2.925, III).There was a significantly greater mean species richness p<0.05) than A. agrarius. When comparing the most preva- in female than male hosts (t = 3.116, p<0.005), and the mean lent helminth species found in both rodents, statistically sig- species richness increased significantly with age (t = 3.169, nificant differences were found for the prevalences of H. di- p<0.005). minuta (χ2 = 6.797, df = 1, p<0.01), H. polygyrus (χ2 = 88.033, The diversity of helminth infracommunity expressed by df = 1, p<0.001) and S. stroma (χ2 = 8.180, df = 1, p<0.005). mean Brillouin/Brillouin evenness indices revealed a lower Moreover, statistically significant differences were recorded diversity for A. flavicollis (0.1 ± 0.03 S.E.M./0.16 ± 0.04) than also for the abundance (t = 7.608, p<0.001) and distributions for A. agrarius (0.2 ± 0.03/0.28 ± 0.04). The mean number of (p<0.005) of H. polygyrus. species harboured per host was significantly lower (t = 2.664, Mice with one or two helminth species were the most com- p<0.05) in A. flavicollis (1.1 ± 0.1) in comparison with mon categories in A. flavicollis, and as for A. agrarius, the A. agrarius (1.6 ± 0.1).

Table III. Diversity characteristics of the helminth infracommunities in A. agrarius and A. flavicollis

A. agrarius* A. flavicollis adult subadult male female adult subadult male female Number of host examined 32 60 50 42 33 18 29 22 % of hosts infected 100.0 93.3 94.0 97.6 87.9 44.4 62.07 86.4 Mean helminth abundance 69.1±18.4 30.4±9.2 52.8±13.2 33.1±11.7 18.4±6.2 10.7±4.9 18.1±7.1 12.5±4.0 Mean Brillouin index 0.26±0.05 0.16±0.03 0.18±0.04 0.20±0.04 0.15±0.04 0.03±0.02 0.03±0.02 0.20±0.06 Mean Brillouin evenness index 0.33±0.06 0.24±0.05 0.24±0.04 0.31±0.06 0.24±0.01 0.05±0.03 0.07±0.04 0.28±0.08 B.I infected hosts only 0.26 0.17 0.19 0.21 0.17 0.07 0.06 0.23 B.evenness I. infected hosts only 0.33 0.25 0.25 0.32 0.25 0.12 0.12 0.33 Mean number of species 1.9±0.2 1.4±0.1 1.6±0.1 1.5±0.1 1.4±0.2 0.6±0.2 0.8±0.1 1.6±0.3

Means ± S.E.M. shown; *4 individuals could not be assigned to sex and age subgroups. 374 Jarmila Ondríková et al.

Table IV. Multifactorial GLM for species richness and helminth diversity in A. agrarius and A. flavicollis by host age and host sex, year and period of capture as independent factor variables. Only statistically significant results – F values, associated probabilities (P) and degree of freedom (df) are reported

Diversity parameter/source of variation A. agrarius A. flavicollis dfFPF P Species richness Host sex 1 – – 9.525 0.003 Host age 1 5.055 0.027 4.540 0.039 Helminth diversity Host sex 1 – – 6.809 0.012

Table V. Multifactorial GLM for mean abundances of the helminth dominant species occurred in A. agrarius and A. flavicollis by host age and host sex, year and period of capture as independent factor variables. Only statistically significant results – F values, associated probabilities (P) and degree of freedom (df) are reported

Helminth species/source of variation A. agrarius A. flavicollis dfFPF P H. diminuta Host age 1 8.559 0.004 – – H. polygrus Period of capture 1 9.411 0.003 – – S. stroma Period of capture 1 8.339 0.005 – –

Table VI. Logistic regression model for prevalences of the helminth dominant species occurred in A. agrarius and A. flavicollis by host age and host sex, year and period of capture as independent factor variables. Only statistically significant results – χ2 values, associated probabilities (P) and degree of freedom (df) are reported

Helminth species/source of variation A. agrarius A. flavicollis df χ2 Pχ2 P H. diminuta Host sex 1 4.572 0.032 – – S. lobata Host sex 1 4.482 0.034 – – S. stroma Host age – – 4.418 0.036 Total helminths Host sex 1 4.249 0.039 – – Host age 1 10.352 0.001 4.288 0.038

Analysis of the role played by extrinsic and intrinsic factors in None of the studied factors influenced mean abundance of the helminth infracommunities of A. agrarius and A. flavicollis the helminth species (Table V) in A. flavicollis. Significant results were confirmed only for A. agrarius where mean abun- The results of analysis (Tables IV and V) show, in general, dances of H. polygyrus and S. stroma were strongly affected the more significant role of intrinsic factors than extrinsic fac- by period of capture, and host age had a significant influence tors on the helminth communities, especially in A. agrarius. on mean abundance of H. diminuta. Multifactorial GLM analysis (Table IV) showed that the Logistic regression models for prevalences (Table VI) con- variation of species richness and helminth diversity are af- firmed the effect of host age for total helminths in both hosts fected by host sex only for A. flavicollis. The significant role and for S. stroma in A. flavicollis only. Host sex affected of host age on species richness was confirmed for both host H. diminuta, S. lobata and total helminths prevalence only in species. However, there was no significant influence of period A. agrarius. and year of capture on these parameters. Helminth diversity of Apodemus in Slovakia 375

Discussion The analysis of diversity at both the component and infracommunity level showed that diversity indices and mean In this paper we present our examination of the helminth fauna species richness were higher for A. agrarius than for A. flavi- of two abundant field mice species, A. agrarius and A. flavicollis. Higher helminth diversity and species richness in the collis, sampled from the same ecological habitat. The nine adult subpopulation was observed for both A. agrarius and helminth species recorded from both rodents represented a rel- A. flavicollis. The same pattern of species richness and hel- atively impoverished helminth community, but was in agree- minth diversity in subpopulations determined by host age was ment with Klimpel et al. (2007a) who obtained similar results in agreement with studies of A. sylvaticus (Behnke et al. 1999; for A. flavicollis from Germany with ten helminth species de- Fuentes et al. 2004, 2007; Eira et al. 2006). This effect may be tected, though with a different community structure. Similar related to increasing host age where there is a corresponding species-poor parasite communities were previously reported increase in total time for exposure to helminth infections, and also for A. sylvaticus (Montgomery and Montgomery 1990, the fact that helminth burden accumulates with time (Fuentes Behnke et al. 1999, Abu-Madi et al. 2000) and Myodes glare- et al. 2007). A higher intake of invertebrates in the diet olus (Behnke et al. 2001, 2008; Klimpel et al. 2007b). In com- amongst the adults could provide another explanation for dif- parison, sixteen helminth species (3 trematodes, 7 cestodes ferences between age groups. The absence of significant dif- and 6 nematodes) were reported in A. agrarius from Be- ferences between the infracommunities determined by host lorussian Polesie (Shimalov 2002). This difference may be re- sex in A. agrarius is in agreement with Behnke et al. (1999) lated to food resources and/or invertebrate intermediate host and Fuentes et al. (2004, 2007) who determined the same pat- availability in the case of helminth species with indirect life tern for A. sylvaticus. However, significant difference in the cycles. The Slovak site sampled here is significantly different mean species richness among females mice compared with to the reclaimed marsh environment of Belorussian Polesie males in A. flavicollis was detected. with a wide network of drainage channels which may be more Our statistical analysis has revealed a more significant ef- suitable for the development of infective stages of some fect of intrinsic factors (host age and sex) than extrinsic ones helminths with aquatic life cycles. Moreover, probably due to (year and period of capture) on helminth communities in the the lower avifauna species richness and abundance in our two rodent species analysed. In both A. agrarius and A. flavi- study area, no helminth species involved in the life cycles of collis only intrinsic factors significantly affect the variation of birds was detected. the mean species richness and the mean helminth diversity, Here we show that differences in the helminth commu- whereas year and period of capture had no significant influ- nities of the two rodent species exist at both component and ence. By contrast Fuentes et al. (2004) and Behnke et al. infracommunity level. Of the nine helminth species detected, (1999) found a clear influence of the year of capture on the six were found in both rodents. Both helminth communities mean number of species in A. sylvaticus. A seasonal effect was have 3–4 dominant species with the nematode H. polygyrus demonstrated only in A. agrarius. Two of the species detected, and cestode R. fraterna dominant in A. agrarius, and the H. polygyrus and S. stroma, showed significant seasonal vari- nematode S. stroma dominant in A. flavicollis. The impor- ation in abundance consistent with previous studies of wood tance of H. polygyrus and S. stroma in the intestinal helminth mice (Abu-Madi et al. 1998, 2000; Eira et al. 2006). fauna of these rodents is in agreement with previous studies The higher helminth burdens and diversity seen here in of Apodemus sp. from other European localities (Behnke et A. agrarius may be a result of several factors. One may sim- al. 1999, Abu-Madi et al. 2000, Klimpel et al. 2007a). Two ply be the small numbers of A. flavicollis analysed in this helminths recorded here are of medical and veterinary im- work. However, other factors should also be considered. Par- portance. H. diminuta can cause sporadic zoonotic infections asite species richness depends on various morphological and in human following accidental ingestion of invertebrate in- ecological traits of host animals. Numerous biotic (e.g. feed- termediate hosts (Tena et al. 1998, Marangi et al. 2003, Craig ing ecology, habitat preferences, host age and sex, richness of and Ito 2007), and T. taeniaeformis is a cestode parasite of host species in the area) and abiotic (e.g. humidity, tempera- cats. ture) factors can affect the spatial and temporal distribution of The comparative analysis of helminths found in both parasite species richness by influencing the survival and/or A. agrarius and A. flavicollis populations demonstrated sig- transmission of parasites (Behnke et al. 1999, Abu-Madi et al. nificant differences. Lower quantitative helminth burdens 2000, Bordes et al. 2009). The trophic niches of A. agrarius were recorded in A. flavicollis and prevalence values for the and A. flavicollis are similar. Both are granivorous, with seeds three most common species found in both rodents significantly and fruits the predominant food resource. However, the yel- differed. The number of helminths per host indicated an ag- low-necked mouse is more of a seed specialist but will sup- gregated distribution for both species, but it followed a nega- plement its diet with up to 20% invertebrates, while the tive binomial distribution only in A. flavicollis. However, in stripped field mouse has more varied diet with up to 40% in- both rodent populations, most mice tended to harboured a few vertebrates (Holisova 1967, Obrtel and Holisova 1974). The helminths, whilst a minority harboured the largest proportion higher proportion of invertebrate fauna in the diet of A. agrar- of the helminth population. ius may explain the higher diversity of its helminth commu- 376 Jarmila Ondríková et al.

nity. An alternative interpretation of our data could be based on Apodemus sylvaticus from three contrasting habitats in south- differences in habitat preferences between rodent species. east England. Journal of Helminthology, 72, 93–100. DOI: A. flavicollis is strongly dependent on the forest environment 10.1017/S0022149X00016254. Abu-Madi M.A., Behnke J.M., Lewis J.W., Gilbert F.S. 2000. Seasonal (Montgomery 1985), whereas A. agrarius, during the crop and site specific variation in the component community struc- vegetation period (spring to autumn), regularly uses both agri- ture of intestinal helminths in Apodemus sylvaticus from three cultural fields and forests. In the autumn, when field work is contrasting habitats in south-east England. Journal of Hel- finished, individuals move to the forest where they spend the minthology, 74, 7–15. DOI: 10.1017/S0022149X00000020. winter (Kozakiewicz et al. 1999). Hence, A. agrarius proba- Babinska-Werka J., Gliwicz J., Goszczynski J. 1981. Demographic processes in a urban population of the striped mouse. Acta bly uses a greater diversity of habitats, which potentially har- Theriologica, 26, 275–283. bour a higher diversity of parasitic infective stages and in- Behnke J.M., Bajer A., Harris P.D., Newington L., Pidgeon E., Row- cludes a greater diversity of hosts, than A. flavicollis. lands G., Sheriff C., Kulis-Malkowska K., Sinski E., Gilbert Host mobility and home range size are regarded as impor- F.S., Barnard C.J. 2008. Temporal and between-site variation tant determinants of parasite transmissions and, therefore, of in helminth communities of bank voles (Myodes glareolus) from N.E. Poland. 1. Regional fauna and component com- parasite diversity (Morand 2000). Interestingly, Bordes et al. munity levels. Parasitology, 135, 985–997. DOI: 10.1017/ (2009), by focusing on helminths in wild mammals, found a S0031182008004393. negative correlation between home range area and parasite Behnke J.M, Barnard C.J., Bajer A., Bray D., Dinmore J., Frake K., species richness in carnivores and glires. Male home ranges Osmond J., Race T., Sinski E. 2001. Variation in the helminth generally exceed those of females in small-mammal popula- community structure in bank voles (Clethrionomys glareolus) from three comparable localities in the Mazury Lake District tions, particularly during the breeding season (e.g. Bergstedt region of Poland. Parasitology, 123, 401–414. DOI: 10.1017/ 1966, Tew and MacDonald 1994, Vukicevic-Radic et al. 2006, S0031182001008605. Stradiotto et al. 2009) and our results of lower species richness Behnke J.M., Lewis J.W., Mohd Zain S.N., Gilbert F.S. 1999. and diversity for males particularly in A. flavicollis support Helminth infections in Apodemus sylvaticus in southern Eng- this negative correlation. Since data on small-mammal move- land: interactive effects of host age, sex and year on the prevalence and abundance of infections. Journal of Helminthology, ments and sizes of home ranges are not consistent, such com- 73, 31–44. DOI: 10.1017/S0022149X99000049. parison are limited for A. agrarius and A. flavicollis in middle Bergstedt B. 1966. Home ranges and movements of the rodent Europe, and suggest that home range size is variably influ- species Clethrionomys glareolus (Schreber), Apodemus flavi- enced by habitat type, season, mouse age and sex (Babinska- collis (Melchior) and Apodemus sylvaticus (Linné) in south- Werka et al. 1981, Horvath and Trocsanyi 1998, Vukice- ern Sweden. Oikos, 17, 150–157. Bordes F., Morand S., Kelt D.A., Van Vuren D.H. 2009. Home range vic Radic et al. 2006). Furthermore, Brown et al. (1994) ob- and parasite diversity in mammals. American Naturalist, 173, served an association between parasite infection and move- 467–474. DOI: 10.1086/597227. ment parameters and home range of males in the wood mouse Brown E.D., MacDonald D.W., Tew T.E., Todd I.A. 1994. Apode- A. sylvaticus. mus sylvaticus infected with Heligmosomoides polygyrus (Ne- To summarize this work, we have documented differences matoda) in an arable ecosystem: epidemiology and effects of infection on the movement of male mice. Journal of Zoology, in the composition of the helminth fauna of two rodent 234, 623–640. DOI: 10.1111/j.1469-7998.1994.tb04869.x. species, A. agrarius and A. flavicollis, which are probably re- Bryja J., Rehák Z. 2002. Další doklady současné expanze areálu lated to host ecology, specifically to differences in dietary and myšice temnopásé (Apodemus agrarius) na Moravě. Lynx, 33, environmental requirements. Further studies of these sym- 69–77. patric populations or of other species of the Apodemus genus Bush A.O., Lafferty K.D., Lotz J.M., Shostak A.W. 1997. Parasitol- ogy meets ecology on its own terms: Margolis et al. revisited. will allow a better understanding of how helminths are dis- Journal of Parasitology, 83, 575–583. DOI: 10.2307/328 tributed in closely-related hosts sharing the same habitat. 4227. Corbet G., Ovenden D. 1980. The Mammals of Britain and Europe. Acknowledgements. This study was supported by the Slovak Grant William Collins Sons and Co., Ltd, Glasgow, 253 pp. Agency (grants no. 2/0043/09 and 2/0042/10) and project APVV Cislakova L., Stanko M., Fricova J., Mosansky L., Travnicek M., Ha- 0108–06. A. Ribas was supported by grant 2008BP A 00045 (Gener- lanova M., Mardzinova S., Stefancikova A. 2004. Small mam- alitat de Catalunya). The authors wish to thank A. We thank two mals (Insectivora, Rodentia) as a potential source of chlamy- anonymous reviewers for constructive comments that help us to im- dial infection in East Slovakia. Annals of Agricultural and En- prove our presentation. Spiers for language correction and helpful vironmental Medicine, 11, 139–143. comments and suggestions. We would also like to thank L. Mosan- Craig P., Ito A. 2007. Intestinal cestodes. Current Opinion in Infec- ský and J. Fricova for their technical collaboration in the field work. tious Diseases, 20, 524–532. DOI: 10.1097/QCO.0b013e32 We thank J. Danoff-Burg J and Ch Xu whose Biodiversity Calcula- 82ef579e. tor was also used for statistical testing. Eira C., Torres J., Vingada J., Miquel J. 2006. Ecological aspects influencing the helminth community of the wood mouse Apode- mus sylvaticus in Dunas de Mira, Portugal. Acta Para- sitologica, 51, 300–308. DOI: 10.2478/s11686-006-0046-0. References Erhardova B. 1956. Parazitičtí červi našich myšovitých hlodavců II. Československá Parasitologie, 3, 49–66. Abu-Madi M.A., Behnke J.M., Lewis J.W., Gilbert F.S. 1998. De- Erhardova B. 1958. Parazitičtí červi hlodavců ČSSR. Českosloven- scriptive epidemiology of Heligmosomoides polygyrus in ská Parasitologie, 5(1), 27–103. Helminth diversity of Apodemus in Slovakia 377

Erhardova B., Rysavy B. 1955. Příspěvek k poznání cizopasních Michaux J.R., Chevret P., Filippucci M.G., Macholan M. 2002. Phy- červů našich myší a hrabošů. Zoologické a Entomologické logeny of the genus Apodemus with a special emphasis on the Listy, 4, 71–83. subgenus Sylvaemus using the nuclear IRBP gene and two mi- Filippucci M.G., Macholan M., Michaux J.R. 2002. Genetic variation tochondrial markers: cytochrome b and 12S rRNA. Molecu- and evolution in the genus Apodemus (Muridae: Rodentia). lar Phylogenetics and Evolution, 23, 123–136. DOI: Biological Journal of the Linnean Society, 75, 395–419. DOI: 10.1016/S1055-7903(02)00007-6. 10.1046/j.1095-8312.2002.00032.x. Milazzo C., Aloise G., Cagnin M., Di Bella C., Geraci F., Feliu C., Fuentes M.V., Sáez S., Trelis M., Galán-Puchades M.T., Esteban Casanova J.C. 2005. Helminths of Apodemus sylvaticus J.G. 2004. The helminth community of the wood mouse, (Muridae) distributed on the southern European border (Ital- Apodemus sylvaticus, in the Sierra Espuña, Murcia, Spain. ian peninsula). Vie et Milieu, 55, 45–51. Journal of Helminthology, 78, 219–223. DOI: 10.1079/JOH Mituch J. 1975. Helmintocenózy cicavcov masívu Poľany. Záverečná 2003226. správa, HELÚ SAV, Košice, 150 pp. Fuentes M.V., Sainz-Elipe S., Galán-Puchades M.T. 2007. Ecologi- Mituch J., Hovorka J., Hovorka I., Tenkacova I. 1987. Helminty a cal study of the wood mouse helminth community in a burned helmintocenózy cicavcov karpatského oblúka. Záverečná Mediterranean ecosystem in regeneration five years after a správa, HELÚ SAV, Košice, 145 pp. wildfire. Acta Parasitologica, 52, 403–413. DOI: 10.2478/ Montgomery W. 1985. The behaviour of Apodemus. Symposia of the s11686-007-0056-6. Zoological Society of London, 55, 89–115. Gliwicz J., Kryštufek B. 1999. Apodemus agrarius (Pallas, 1771). Mongomery W. 1999. Apodemus flavicollis (Melchior, 1834). In: In: (Eds. A. Mitchell-Jones, G. Amori, W. Bogdanowicz, B. (Eds. A. Mitchell-Jones, G. Amori, W. Bogdanowicz, B. Kryštufek, P.J.H. Reinders, F. Spitzenberger, M. Stubbe, Kryštufek, P.J.H. Reinders, F. Spitzenberger, M. Stubbe, J.B.M. Thissen, V. Vohralík and J. Zima) The atlas of Euro- J.B.M. Thissen, V. Vohralík and J. Zima) The atlas of Euro- pean Mammals. Academic Press, London, 266–267. pean Mammals. Academic Press, London, 270–271. Goüy de Bellocq J., Sarà M., Casanova J.C., Feliu C., Morand S. Montgomery S.S.J., Montgomery W.I. 1990. Structure, stability and 2003. A comparison of the structure of helminth communities species interactions in helminth communities of wood mice, in the woodmouse, Apodemus sylvaticus, on islands of the Apodemus sylvaticus. International Journal for Parasitology, western Mediterranean and continental Europe. Parasitology 20, 225–242. DOI: 10.1016/0020-7519(90)90105-V. Research, 90, 64–70. DOI: 10.1007/s00436-002-0806-1. Morand S. 2000. Wormy word: comparative tests of theoretical hy- Hildebrand J., Zalesny G., Okulewicz A., Baszkiewicz K. 2009. Pre- potheses on parasite species richness. In: (Eds. R. Poulin, S. liminary studies on the zoonotic importance of rodents as a Morand and A. Skorping) Evolutionary biology of host para- reservoir of toxocariasis from recreation grounds in Wroclaw site: theory meets reality. Elsevier Science, Amsterdam, 63–79. (Poland). Helminthologia, 46, 80–84. DOI: 10.2478/s11687- Musser G.G., Carleton M.D. 1993. Family Muridae. In: (Eds. D.E. 009-0016-9. Wilson and D.M. Reeder) Mammal Species of the World. 2nd Horvath G., Trocsanyi B. 1998. Home range size of Apodemus agrar- Edition, Smithsonian Institute Press,Washington D.C. and ius and small mammal population dynamics in the rodent as- London, 501–806. semblage of a Querco-robori-carpinetum forest habitat. Tiscia, Obrtel R., Holisova V. 1974. Trophic niches of Apodemus flavicollis 31, 63–69. and Clethrionomys glareolus in low-land forest. Acta Scien- Holisova V. 1967. The food of Apodemus agrarius (Pall.). Zoologické tiarum Naturalium Academiae Scientiarum Bohemicae Brno, Listy, 16, 1–14. 8, 1–37. Klempa B., Stanko M., Labuda M., Ulrich R., Meisel H., Krüger Orlov V.N., Bulatova N.S., Nadjafova R.S., Kozlovsky A.I. 1996. D.H. 2005. Central European Dobrava Hantavirus isolate Evolutionary classification of European wood mice of the from striped field mouse (Apodemus agrarius). Journal of subgenus Sylvaemus based on allozyme and chromosome Clinical Microbiology, 43, 2756–2763. DOI: 10.1128/JCM. data. Bonner Zoologische Beiträge, 46, 191–202. 43.6.2756-2763.2005. Pelikan J. 1965. Reproduction, population structure and elimination Klimpel S., Förster M., Schmahl G. 2007a. Parasites of two abun- of males in Apodemus agrarius (Pall.). Folia Zoologica, 14, dant sympatric rodent species in relation to host phylogeny 317–332. and ecology. Parasitology Research, 100, 867–875. DOI: Pence D.B., Eason S. 1980. Comparison of the helminth faunas of 10.1007/s00436-006-0368-8. two sympatric top carnivores from rolling plains of Texas. Klimpel S., Förster M., Schmahl G. 2007b. Parasite fauna of the Journal of Parasitology, 66, 115–120. DOI: 10.2307/3280 bank vole (Clethrionomys glareolus) in an urban region of 601. Germany: reservoir host of zoonotic metazoan parasites? Poulin R. 1993. The disparity between observed and uniform distri- Parasitology Research, 102, 69–75. DOI: 10.1007/s00436- butions: a new look at parasite aggregation. International 007-0725-2. Journal for Parasitology, 23, 937–944. DOI: 10.1016/0020- Kozakiewicz M., Gortat T., Kozakiewicz A., Barkowska M. 1999. 7519(93)90060-C. Effects of habitat fragmentation on four rodent species in Pol- Reiczigel J., Rózsa L. 2005. Quantitative Parasitology 3.0. Budapest. ish farm landscape. Landscape Ecology, 14, 391–400. DOI: Rózsa L., Reiczigel J., Majoros G. 2000. Quantifying parasites in 10.1023/A:1008070610187. samples of hosts. Journal of Parasitology, 86, 228–232. DOI: Lefkovitch L.P. 1966. An index of spatial distribution. Researches 10.1645/0022-3395(2000)086[0238:QPISOH]2.0.C0;2. on Population Ecology, 8, 89–92. Shimalov V.V. 2002. Helminth fauna of the striped field mouse Magurran A.E. 1988. Ecological Diversity and Its Measurement. (Apodemus agrarius Pallas 1778) in ecosystems of Beloruss- Croom Helm, London, 179 pp. ian Polesie transformed as a result of reclamation. Parasitol- Magurran A.E. 2004. Measuring Biological Diversity. Wiley-Black- ogy Research, 88, 1009–1010. DOI: 10.1007/s004360100437. well, 256 pp. Stanko M. 1994. Small mammals communities of windbreaks and Marangi M., Zechini B., Fileti A., Quaranta G., Aceti A. 2003. Hy- adjacent fields in the Eastern Slovakia lowlands. Folia Zoo- menolepis diminuta infection in a child living in the urban logica, 43, 135–143. area of Rome, Italy. Journal of Clinical Microbiology, 41, Stanko M., Fricova J., Schniererova E., Mosansky L., Mardzinova 3994–3995. DOI: 10.1128/JCM.41.8.3994-3995.2003. S. 2004. Fauna drobných cicavcov (Insectivora, Rodentia, 378 Jarmila Ondríková et al.

Carnivora) okolia Rozhanoviec (Košická kotlina). Natura fects of density and resource availability. Journal of Mam- Carpatica, 45, 107–116. malogy, 90, 704–714. DOI: 10.1644/08-MAMM-A-120R1.1. Stanko M., Krasnov B.R., Miklisova D., Morand S. 2007. Simple Tena D., Purez Simon M., Gimeno C., Purez Pomata M.T., Illescas epidemiological model predicts the relationships between S., Amondarain I., Gonzalez A., Dominguez J., Bisquert J. prevalence and abundance in ixodid ticks. Parasitology, 134, 1998. Human infection with Hymenolepis diminuta: Case re- 59–68. DOI: 10.1017/S0031182006001296. port from Spain. Journal of Clinical Microbiology, 36, 2375– Stanko M., Mosansky L., Fricova J. 1996. Small mammals in frag- 2376. ments of Robinia pseudoacacia stands in the East Slovakian Tew T.E., MacDonald D.W. 1994. Dynamics of space use and male lowlands. Folia Zoologica, 45, 145–152. vigour amongst wood mice, Apodemus sylvaticus, in the ce- Stefancikova A., Derdakova M., Lencakova D., Ivanova R., Stanko real ecosystem. Behavioral Ecology and Sociobiology, 34, M., Cislakova L., Petko B. 2008. Serological and molecular 337–345. DOI: 10.1007/BF00197004. detection of Borrelia burgdorferi sensu lato and Anaplasma- Vukicevic-Radic O., Matic R., Kataranovski D., Stamenkovic S. taceae in rodents. Folia Microbiologica, 53, 493–499. 2006. Spatial organization and home range of Apodemus flavi- Stefancikova A., Gajdos O., Macko J., Tomasovicova K. 1994. collis and A. agrarius on Mt. Avala, Serbia. Acta Zoologica Helminth fauna of small mammals in the urban and suburban Academiae Scientiarum Hungaricae, 52, 81–96. area of Košice. Biologia, 49, 147–152. Zejda J. 1967. Habitat selection in Apodemus agrarius (Pallas, 1778) Stradiotto A., Cagnacci F., Delahay R., Tioli S., Nieder L., Rizzoli A. (Mammalia: Muridae) on the border of the area of its distri- 2009. Spatial organization of the yellow-necked mouse: ef- bution. Folia Zoologica, 16, 15–30.

(Accepted July 10, 2010)