Diversity and ecology of intestinal nematodes of the yellow-necked mouse (Apodemus flavicollis Melchior, 1834) on the territory of Serbia

Vršeno je istraživanje intestinalnih nematoda žutogrlog miša (Apodemus flavicollis  Melchior, 1834) uzorkovanog sa 18 lokaliteta na teritoriji Srbije, južno od Save i Dunava, sa ciljem proširenja i upotpunjavanja saznanja o ovoj komponenti parazitofaune glodara u ovom delu Evrope. Fauna nematoda crevnog trakta je analizirana sa više aspekata: kvantitativnog, aspekta zajednica, biološkog, aspekta biodiverziteta i aspekta polne strukture. Pored toga, ispitan je uticaj odabranih spoljašnjih i unutrašnjih faktora na prevalencu i abundancu parazitske infekcije. Zabeleženo je prisustvo devet vrsta intestinalnih nematoda, pri čemu je broj vrsta po lokalitetu varirao od 1 do 7. Ukupna prevalenca infekcije iznosila je 81,6%. Najčešće vrste u uzorku bile su Heligmosomoides polygyrus i  Syphacia stroma, koje su se odlikovale najvišim prevalencama i intenzitetima infekcije. Distribucija nematoda unutar domaćina je bila agregirana. Broj vrsta po domaćinu varirao je od 1 do 5, ali su najzastupljenije bile infekcije jednom ili dvema vrstama. Najčešća kombinacija vrsta bila je  H. polygyrus-S. stroma; međutim, odsustvo podataka iz ranijih istraživanja i adekvatnih polaznih modela sprečava donošenje zaključaka o mogućim interakcijama i asocijacijama između vrsta. Monoksene nematode su bile brojnije i imale veću prevalencu od heteroksenih nematoda, što oslikava  razlike u njihovim životnim ciklusima. Među monoksenim nematodama, geohelminti u užem smislu su se odlikovali najvećim prevalencama, a ageohelminti najvećom abundancom, u skladu sa životnim strategijama koje teže ka disperziji ili akumulaciji.Šenonov indeks diverziteta cele uzoračke populacije iznosio je 1,44 što je visoka vrednost u odnosu na one iz drugih delova Evrope. Nije uočena značajna negativna korelacija između udaljenosti lokaliteta i vrednosti Sorensenovog indeksa,ukazujući da je prostorni faktor značajan u strukturiranju zajednica intestinalnih nematoda i na lokalnom nivou. Odnos polova je bio neravnomeran, uglavnom u korist ženki, u skladu sa podacima drugih autora. Ženke su ujedno bile krupnije od mužjaka, saglasno sa ranijim nalazima za parazitske nematode. Nadmorska visina nije uticala na abundancu intestinalnih nematoda. Pol domaćina je uticao na prevalencu dve vrste: prevalenca  S. stroma  je bila veća kod mužjaka, a prevalenca Trichuris muris  kod ženki. Kao značajan faktor uticao je na abundancu samo kod vrste  Aonchotheca annulosa; abundanca ove vrste bila je veća kod mužjaka. Rezultati sugerišu da je uticaj pola domaćina na nivo parazitske infekcije izuzetno kompleksan fenomen.  Prevalenca i abundanca infekcije intestinalnim nematodama je bila veća kod domaćina sa B hromozomima.  Lokalitet je bio značajan faktor u variranju abundance nematoda. Uzrast i prisustvo drugih vrsta nematoda su  takođe ispoljavali značajan efekat. Povećanje abundance nematoda sa uzrastom  se vezuje za dužu izloženost starijih jedinki parazitima. Iako je registrovan uticaj abundance jedne vrste na abundancu druge, on ne predstavlja čvrst dokaz za postojanje interakcija između vrsta.A study of intestinal nematode parasites was conducted on the yellow-necked mouse (Apodemus flavicollis  Melchior, 1834) sampled from 18 sites from Serbia south of the Sava and Danube rivers. The aim of the study was to broaden and enrich the data on this category of rodent parasites in this part of Europe. The nematode fauna of the gastrointestinal tract was analysed from quantitative, community, biological, biodiversity and sex ratio aspects. In addition, selected extrinsic and intrinsic factors were tested for their influence on the prevalence and abundance of infection. Nine species of  intestinal nematodes were noted, 1 to 7 per site. Total sample prevalence was 81.6%. Heligmosomoides polygyrus  and  Syphacia stroma were the most common species, with the highest prevalence and intensity values. Nematodes were aggregated within their hosts. Infracommunity richness varied from 1 to 5, but infections with one or two species were most common. The most frequent combination  of species was H. polygyrus-S. stroma, but in absence of prior research and adequate null models, conclusions of possible interactions and associations between species could not be drawn. Monoxenous nematodes were more abundant and prevalent than heteroxenous species, reflecting the differences in their life cycles. Of the monoxenous nematodes, geohelminths sensu stricto had the highest prevalence values, whereas ageohelminths were most abundant, with respect to their life strategies that favour either dispersal or accumulation. Shannon’s diversity index for the total sample was 1.44, a high value compared to those from other European based studies. A significant negative correlation between site distance and Sorensen index values was not found, implying that spatial factors have an important role in structuring intestinal nematode communities on a local scale. Sex ratio was generally female-biased, in agreement with data from other authors. In addition, females were larger than males, congruent with previous findings for parasitic nematodes. Elevation did not significantly influence intestinal nematode abundance. Host sex influenced the prevalence of two species: for S. stroma prevalence was higher in males, and for Trichuris muris in females. Influence of host sex on abundance was found only for Aonchotheca annulosa, with abundances of this parasite higher in male mice. The results suggest that the effectof host sex on parasite infection levels is a highly complex phenomenon.  Infection prevalence and abundance was higher in hosts that carried B chromosomes. Site was a significant factor in explaining variations in nematode abundance. Hostage and presence of other nematode species  also exibited effects.  An increase in nematode abundance with host age  is explained by prolonged exposure to parasites in older host individuals. Although results indicate that the abundance of one species influences the abundance of another, this is not firm evidence of the existence of species interactions

Is there a host sex bias in intestinal nematode parasitism of the yellow-necked mouse (Apodemus flavicollis) at Obedska bara pond, Serbia?

Fifty-one yellow-necked mice from the Obedska bara locality were analysed for the presence of intestinal nematode parasites in order to assert whether there was a host sex bias in infection. Previous research indicated that males would be the more infected sex, either due to the immunosuppressive effect of testosterone or their different allocation of resources towards immune defence. Quantitative infection parameters were compared between host sexes for all nematode species and nematodes in general. In addition, the influence of host sex, age, total body length, body mass and presence of other nematode species on parasite abundance was analysed. No statistically significant differences between males and females were noted for any of the studied quantitative parameters, leading to an absence of sex-biased parasitism in this study

B. burgdorferi infekcija u krpeljma uklonjenih sa ljudi i prisustvo antitela protiv borelija kod pacijenata infestiranih krpeljima

The primary objectives of this study were (1) to determine the presence of Borrelia burgdorferi infection in ticks removed from patients for the purpose of singling out sites with increased risk of Lyme borreliosis, and (2) to determine the presence of IgM and/or IgG antibodies against B. burgdorferi sensu lato (s. l.) complex in sera of patients who had ticks removed. From 108 ticks removed from patients, all were examined zoologically and a sub-sample of 91 ticks was tested using PCR analysis to determine the presence of DNA indicating B. burgdorferi infection. To detect anti-Borrelia IgM and/ or IgG antibodies in 61 patients bitten by ticks, we used line recombinant immunoblot test. The most common tick identified was Ixodes ricinus. B. burgdorferi s. l. was present in 37 of 91 tested ticks (40.7%). Seroconversion against B. burgdorferi s. l. antigen was detected in 12 of 61 patients (19.7%). Most of the infected ticks were from the province of Vojvodina (11 municipalities), with the city of Novi Sad proving to be the site with the highest number of infected ticks, 6 in total.Glavni cilj ove studije je bio da se ispita prisustvo B. burgdorferi infekcije u krpeljma uklonjenih sa pacijenata radi utvđivanja lokaliteta sa povećanim rizikom za obolevanje od lajm borelioze, kao i ispitivanje prisustva IgM i/ili IgG antitela usmerenih protiv B. burgdorferi s. l. kompleksa u serumu pacijenata infestiranih krpeljima. Sa pacijenata je prikupljeno i zoološki ispitano 108 krpelja. PCR analiza krpelja korišc'ena je za utvrđivanje prisustva B. burgdorferi s. l. kompleks kod 91 krpelja od ukupnih 108. Za otkrivanje IgM i/ili IgG antitela protiv B. burgdorferi s. l. korišćeni su linijski rekombinantni imunoblot testovi. Najčešc'i identifikovani krpelj je Ixodes ricinus. B. burgdorferi s. l. je bila prisutna u 37 od 91 testiranog krpelja (40,7%). Prisustvo IgM/IgG antitela protiv B. burgdorferi s. l. otkriveno je kod 12 od 61 pacijenta (19,7%). Najviše inficiarnih krpelja je sa teritorije AP Vojvodine (11 opština), gde je urbani deo Novog Sada lokalitet sa najvećim brojem inficiranih krpelja - 6

Diversity and ecology of intestinal nematodes of the yellow-necked mouse (Apodemus flavicollis Melchior, 1834) on the territory of Serbia

Vršeno je istraživanje intestinalnih nematoda žutogrlog miša (Apodemus flavicollis  Melchior, 1834) uzorkovanog sa 18 lokaliteta na teritoriji Srbije, južno od Save i Dunava, sa ciljem proširenja i upotpunjavanja saznanja o ovoj komponenti parazitofaune glodara u ovom delu Evrope. Fauna nematoda crevnog trakta je analizirana sa više aspekata: kvantitativnog, aspekta zajednica, biološkog, aspekta biodiverziteta i aspekta polne strukture. Pored toga, ispitan je uticaj odabranih spoljašnjih i unutrašnjih faktora na prevalencu i abundancu parazitske infekcije. Zabeleženo je prisustvo devet vrsta intestinalnih nematoda, pri čemu je broj vrsta po lokalitetu varirao od 1 do 7. Ukupna prevalenca infekcije iznosila je 81,6%. Najčešće vrste u uzorku bile su Heligmosomoides polygyrus i  Syphacia stroma, koje su se odlikovale najvišim prevalencama i intenzitetima infekcije. Distribucija nematoda unutar domaćina je bila agregirana. Broj vrsta po domaćinu varirao je od 1 do 5, ali su najzastupljenije bile infekcije jednom ili dvema vrstama. Najčešća kombinacija vrsta bila je  H. polygyrus-S. stroma; međutim, odsustvo podataka iz ranijih istraživanja i adekvatnih polaznih modela sprečava donošenje zaključaka o mogućim interakcijama i asocijacijama između vrsta. Monoksene nematode su bile brojnije i imale veću prevalencu od heteroksenih nematoda, što oslikava  razlike u njihovim životnim ciklusima. Među monoksenim nematodama, geohelminti u užem smislu su se odlikovali najvećim prevalencama, a ageohelminti najvećom abundancom, u skladu sa životnim strategijama koje teže ka disperziji ili akumulaciji.Šenonov indeks diverziteta cele uzoračke populacije iznosio je 1,44 što je visoka vrednost u odnosu na one iz drugih delova Evrope. Nije uočena značajna negativna korelacija između udaljenosti lokaliteta i vrednosti Sorensenovog indeksa,ukazujući da je prostorni faktor značajan u strukturiranju zajednica intestinalnih nematoda i na lokalnom nivou. Odnos polova je bio neravnomeran, uglavnom u korist ženki, u skladu sa podacima drugih autora. Ženke su ujedno bile krupnije od mužjaka, saglasno sa ranijim nalazima za parazitske nematode. Nadmorska visina nije uticala na abundancu intestinalnih nematoda. Pol domaćina je uticao na prevalencu dve vrste: prevalenca  S. stroma  je bila veća kod mužjaka, a prevalenca Trichuris muris  kod ženki. Kao značajan faktor uticao je na abundancu samo kod vrste  Aonchotheca annulosa; abundanca ove vrste bila je veća kod mužjaka. Rezultati sugerišu da je uticaj pola domaćina na nivo parazitske infekcije izuzetno kompleksan fenomen.  Prevalenca i abundanca infekcije intestinalnim nematodama je bila veća kod domaćina sa B hromozomima.  Lokalitet je bio značajan faktor u variranju abundance nematoda. Uzrast i prisustvo drugih vrsta nematoda su  takođe ispoljavali značajan efekat. Povećanje abundance nematoda sa uzrastom  se vezuje za dužu izloženost starijih jedinki parazitima. Iako je registrovan uticaj abundance jedne vrste na abundancu druge, on ne predstavlja čvrst dokaz za postojanje interakcija između vrsta.A study of intestinal nematode parasites was conducted on the yellow-necked mouse (Apodemus flavicollis  Melchior, 1834) sampled from 18 sites from Serbia south of the Sava and Danube rivers. The aim of the study was to broaden and enrich the data on this category of rodent parasites in this part of Europe. The nematode fauna of the gastrointestinal tract was analysed from quantitative, community, biological, biodiversity and sex ratio aspects. In addition, selected extrinsic and intrinsic factors were tested for their influence on the prevalence and abundance of infection. Nine species of  intestinal nematodes were noted, 1 to 7 per site. Total sample prevalence was 81.6%. Heligmosomoides polygyrus  and  Syphacia stroma were the most common species, with the highest prevalence and intensity values. Nematodes were aggregated within their hosts. Infracommunity richness varied from 1 to 5, but infections with one or two species were most common. The most frequent combination  of species was H. polygyrus-S. stroma, but in absence of prior research and adequate null models, conclusions of possible interactions and associations between species could not be drawn. Monoxenous nematodes were more abundant and prevalent than heteroxenous species, reflecting the differences in their life cycles. Of the monoxenous nematodes, geohelminths sensu stricto had the highest prevalence values, whereas ageohelminths were most abundant, with respect to their life strategies that favour either dispersal or accumulation. Shannon’s diversity index for the total sample was 1.44, a high value compared to those from other European based studies. A significant negative correlation between site distance and Sorensen index values was not found, implying that spatial factors have an important role in structuring intestinal nematode communities on a local scale. Sex ratio was generally female-biased, in agreement with data from other authors. In addition, females were larger than males, congruent with previous findings for parasitic nematodes. Elevation did not significantly influence intestinal nematode abundance. Host sex influenced the prevalence of two species: for S. stroma prevalence was higher in males, and for Trichuris muris in females. Influence of host sex on abundance was found only for Aonchotheca annulosa, with abundances of this parasite higher in male mice. The results suggest that the effectof host sex on parasite infection levels is a highly complex phenomenon.  Infection prevalence and abundance was higher in hosts that carried B chromosomes. Site was a significant factor in explaining variations in nematode abundance. Hostage and presence of other nematode species  also exibited effects.  An increase in nematode abundance with host age  is explained by prolonged exposure to parasites in older host individuals. Although results indicate that the abundance of one species influences the abundance of another, this is not firm evidence of the existence of species interactions

Significance of the red fox as a natural reservoir of intestinal zoonoses in Vojvodina, Serbia

In the present study, 223 foxes were collected from various localities in the northern part of the Republic of Serbia (Vojvodina province) and examined for intestinal helminths. Among the examined foxes 178 (79.8%) were infected. The most frequently identified parasites were Mesocestoides spp. (49.3%) and Toxascaris leonina (36.3%). The parasite with the lowest prevalence was Pterygodermatites affinis (0.9%), and this is the first confirmed finding in Serbia. The other recovered species were Alaria alata (25.6%), Taenia spp. (6.3%), Echinococcus multilocularis (13%), Toxocara canis (16.6%) and Uncinaria stenocephala (14.8%). The highest number of foxes infected with E. multilocularis were in the Srem area. The results of this study indicate the presence of helminth species in red foxes in Vojvodina which may also infect humans

Host–Parasite Relationship—Nematode Communities in Populations of Small Mammals

Nematode burdens and variation in morphological characteristics were assessed in eighty-eight animals from three host species (Apodemus sylvaticus, Apodemus flavicollis, and Myodes glareolus) from eight localities in Serbia. In total, 15 species of nematodes were identified, and the overall mean parasite species richness (IndPSR) was 1.61 per animal (1.98 in A. flavicollis, 1.43 in M. glareolus, and 0.83 in A. sylvaticus). Furthermore, the studied host species significantly differed in individual parasite load (IndPL) and in the following morphological characters: spleen mass, body condition index (BCI), and body mass. We aimed to analyze the relationship between the burden of intestinal nematodes, on one hand, and the body conditions of the host and its capability to develop immune defends on the other. Spleen mass was considered as a measure of immune response. In all host species, larger animals with a better condition (higher BCI) were infected with more parasites species (IndPSR), while parasite load was not related to BCI. Only in A. flavicollis were males significantly larger, but females of the same sizes were infected with more parasite species. This female-biased parasitism is contrary to the theoretical expectation that males should be more parasitized, being larger, more active, with a wider home range. Although the spleen size was significantly correlated with body condition and body mass, IndPSR was not related to spleen mass in any studied species, but in M. galareolus, we found that a smaller spleen was related to higher infection intensity (IndPL)

Data from: Possible influence of B chromosomes on genes included in immune response and parasite burden in Apodemus flavicollis

Genetic background underlying wild populations immune response to different parasites is still not well understood. We studied immune response to multiple infections and to competition between different parasite species at different developmental stages in population of yellow-necked mouse, Apodemus flavicollis. Quantitative real-time PCR was used to investigate associations of MHC II-DRB, IL-10 and Tgf-β genes expressions with presence of intestinal parasites at different developmental stages. Furthermore, we were interested whether the host related characteristics (sex, age, body condition, presence of B chromosomes or expression of other genes) or characteristics of present parasites (number of adult parasites of each identified species, egg count of each parasite genus, total number of nematode individuals) affect differential expression of the studied genes. A significant invert association between the expression of MHC II-DRB and Tgf-β gene was found, which together with absence of IL-10 association confirmed modified Th2 as the main type of immune response to nematode infections. Effect of recorded parasites and parasite life-cycle stage on expression levels of MHC II-DRB gene was detected only through interactions with host-related characteristics such as sex, age, and the presence of B chromosomes. The presence of B chromosomes is associated with lower expression level of Tgf-β gene. Although the influence of host genetic background on parasite infection has already been well documented, this is the first study in mammals that gave presence of B chromosomes on immune response full consideration

Suplementary file for: Possible influence of B chromosomes on genes included in immune response and parasite burden in Apodemus flavicollis

Host-related (sex, age, body condition index, presence of Bs in genotype, expression of other genes) and parasite-related (number of adult parasites of each identified species, egg count of each parasite genus, total number of nematode individuals) variables used in analysis