Aleksandra Penezić

A European concern? genetic structure and expansion of golden jackals (canis aureus) in Europe and the caucasus

In the first continent-wide study of the golden jackal (Canis aureus), we characterised its population genetic structure and attempted to identify the origin of European populations. This provided a unique insight into genetic characteristics of a native carnivore population with rapid large-scale expansion. We analysed 15 microsatellite markers and a 406 base-pair fragment of the mitochondrial control region. Bayesian-based and principal components methods were applied to evaluate whether the geographical grouping of samples corresponded with genetic groups. Our analysis revealed low levels of genetic diversity, reflecting the unique history of the golden jackal among Europe’s native carnivores. The results suggest ongoing gene flow between south-eastern Europe and the Caucasus, with both contributing to the Baltic population, which appeared only recently. The population from the Peloponnese Peninsula in southern Greece forms a common genetic cluster with samples from south-eastern Europe (ΔK approach in STRUCTURE, Principal Components Analysis [PCA]), although the results based on BAPS and the estimated likelihood in STRUCTURE indicate that Peloponnesian jackals may represent a distinct population. Moreover, analyses of population structure also suggest either genetic distinctiveness of the island population from Samos near the coast of Asia Minor (BAPS, most STRUCTURE, PCA), or possibly its connection with the Caucasus population (one analysis in STRUCTURE). We speculate from our results that ancient Mediterranean jackal populations have persisted to the present day, and have merged with jackals colonising from Asia. These data also suggest that new populations of the golden jackal may be founded by long-distance dispersal, and thus should not be treated as an invasive alien species, i.e. an organism that is “non-native to an ecosystem, and which may cause economic or environmental harm or adversely affect human health”. These insights into the genetic structure and ancestry of Baltic jackals have important implications for management and conservation of jackals in Europe. The golden jackal is listed as an Annex V species in the EU Habitats Directive and as such, considering also the results presented here, should be legally protected in all EU member states.

First records of Dirofilaria repens in wild canids from the region of Central Balkan.

Dirofilaria repens causes an emerging zoonotic disease in Europe, particularly in its southern part, the Mediterranean region. Many reports on human dirofilariosis have been published recently, but little is known about the wildlife hosts and reservoirs of this parasite in nature. This paper presents the first records of adult D. repens specimens from free-ranging carnivores in Central Balkan countries (Serbia and Macedonia). During the period 2009-2013, a total of 145 regularly shot canids were examined for the presence of D. repens adults. In order to investigate their role as hosts and potential wild reservoirs of this zoonosis, 71 wolves (Canis lupus), 48 foxes (Vulpes vulpes) and 26 jackals (Canis aureus) were examined. Under the skin of two wolves (one from Serbia and one from Macedonia) and of a red fox from Serbia D. repens adults were found. In all three cases only one parasite was present. Further research on wild canids is needed, particularly on species widening their range (such as jackals) and those living near human settlements (foxes and jackals), which facilitates the transmission of the parasites to dogs and humans.

Levels of infection of intestinal helminth species in the golden jackal Canis aureus from Serbia.

During the past decade, golden jackal populations have substantially increased, yet little is known of their potential for transmitting parasites within animal and human hosts. In the present study, between 2005 and 2010, 447 jackals from six localities in Serbia were examined for intestinal parasites. Two species of trematodes (Alaria alata, Pseudamphistomum truncatum), three nematodes (Toxocara canis, Ancylostoma caninum, Gongylonema sp.), and seven cestodes (Taenia pisiformis, Taenia hydatigena, Multiceps multiceps, Multiceps serialis, Mesocestoides lineatus, Mesocestoides litteratus, Dipylidium caninum) were identified. Pseudamphistomum truncatum and M. serialis species were recorded for the first time. The overall prevalence of parasitic infection was 10.3%. No significant differences were found in the prevalence of infection between males and females (P>0.817), between localities (P>0.502), or with regard to annual cycles (P>0.502). In the infected jackal population, 65% harboured multiple infections and one individual was a host to five different types of parasite species, the highest number of parasites we recorded in a single host. These findings indicate that although the prevalence of gastrointestinal helminths in the jackal population in Serbia is significantly lower than expected from earlier studies, further monitoring is required given the jackals rapid population increase.

Echinococcus multilocularis in the European beaver (Castor fibre L.) from Serbia: first report

Echinococcus multilocularis is a tapeworm of canid carnivores. It is widely present in the Northern Hemisphere with endemic regions in central Europe, northern and central Eurasia, and in parts of North America. The main definitive host in Europe is the red fox ( Vulpes vulpes ), with a prevalence of more than 50 per cent in some studies (Losson and others 1997, Roming and others 1999, Hofer and others 2000, Tackmann and others 2001, Casulli and others 2005, Vervaeke and others 2006). At the beginning of the 1990s, this parasite started to spread from the endemic areas in central Europe (Roming 2002, Vervaeke and others 2006). It is suggested that one of the main causes of its spread is the increased number of foxes in European countries, which occurred after the decrease of the incidence of rabies as a result of successful peroral vaccination (Chautan and others 2000). E. multilocularis is a pathogenic zoonosis. Rodents are the usual intermediate host, but humans can be an accidental intermediate host. Humans are infected by ingesting eggs from a contaminated environment. Oncospheres are released in the digestive tract and further spread through the entire body through hepatopulmonary ways (Kulisic and others 1999). They are usually found in the liver causing alveolar echinococcosis, which is lethal if left untreated …

Do rivers and human-induced habitat fragmentation affect genetic diversity and population structure of the European ground squirrel at the edge of its Pannonian range?

The European ground squirrel (EGS) (Spermophilus citellus) populations of Vojvodina (Serbia) represent the southernmost part of its distribution in the Pannonian lowland. For species with low dispersal abilities a presence of even weak barriers can have significant influence on genetic structure among adjacent populations. We examined here the effects of habitat fragmentation and river barriers on the genetic structure of the EGS based on 12 microsatellite loci. Bayesian clustering methods were used as additions to classical population genetic approaches. We found that EGS populations in Vojvodina are highly fragmented, but their genetic variation is still higher than in peripheral populations in Central Europe. Populations in Vojvodina consistently grouped into three genetic clusters. The Danube, but not the Tisza River, represents an important barrier to gene flow. EGS populations in the studied area did not show the signs of recent genetic bottlenecks, as would be expected from observations of recent population declines. Conservation strategy should be focused on maintenance of remained suitable habitats and optimal population sizes.

Presence of Leishmania and Brucella Species in the Golden Jackal Canis aureus in Serbia

The golden jackal Canis aureus occurs in south-eastern Europe, Asia, the Middle East, the Caucasus, and Africa. In Serbia, jackals neared extinction; however, during the last 30 years, the species started to spread quickly and to increase in number. Few studies in the past have revealed their potential role as carriers of zoonotic diseases. Animal samples were collected over a three-year period (01/2010–02/2013) from 12 sites all over Serbia. Of the tissue samples collected, spleen was chosen as the tissue to proceed; all samples were tested for Leishmania species and Brucella species by real-time PCR. Of the 216 samples collected, 15 (6.9%) were positive for Leishmania species, while four (1.9%) were positive for B. canis. The potential epidemiologic role of the golden jackal in carrying and dispersing zoonotic diseases in Serbia should be taken under consideration when applying surveillance monitoring schemes.

Intestinal helminth parasites of the grey wolf (Canis lupus L.) in Serbia.

The grey wolf (Canis lupus L.) is the most widespread large carnivore in Europe with large populations in the Eastern part of Europe and the Balkan Peninsula. In this study, a total of 102 wolves were examined for intestinal helminth parasites. The carcasses were collected within the Serbian part of the wolfs range during the period 2009-2014. Nine helminth species were found: one nematode, Toxocara canis (3.9%), one trematode, Alaria alata (1.0%), and seven cestodes, Taenia pisiformis (1.0%), T. hydatigena (9.8%), T. polyacantha (2.9%), T. taeniaeformis (2.0%), T. (syn. Multiceps) multiceps (3.9%), T. serialis (1.0%) and Mesocestoides litteratus (1.0%). Taenia (syn. Hydatigera) taeniaeformis has been registered for the first time in a wolf from Europe. An overall moderate prevalence (16.7%) of infected wolves was recorded. There was no statistically significant difference in prevalence between sexes. Of the years studied, the highest prevalence was found in 2014 (57.1%). The maximum number of helminth species per host specimen was four.

Golden jackals (Canis aureus) as hosts for ticks and tick-borne pathogens in Serbia

The golden jackal (Canis aureus) is a medium-sized canid species native to Europe. This species is characterized by rapid large-scale expansion. A similar trend is also observed in Serbia, where the species is now distributed in more than a half of the territory. Although jackals prefer habitats in human-dominated landscapes, these animals have not been studied well enough from an eco-epidemiological point of view, and little is known about their potential for carrying zoonotic pathogens. In a study conducted during a three-year period (01/2010-02/2013), a total of 216 hunted or road-killed golden jackals were collected from 10 localities in Serbia. Ticks, when present, were removed, and after necropsy, spleen samples were collected from each animal. All tick and spleen samples were tested for the DNA of bacterial and protozoan tick-borne pathogens (Borrelia species, Bartonella species, Rickettsia species, Anaplasma species, Coxiella burnetii, Francisella species and Babesia species) by multiplex real-time PCR, conventional PCR and sequencing analyses. The DNA of Babesia canis was detected in nine out of 216 (4.2%) spleen samples, and two samples (0.9%) tested positive for Anaplasma phagocytophilum. In 118 ticks collected from jackals, the DNA of two Babesia species (Ba. canis and Ba. microti), three Borrelia species (Bo. garinii, Bo. valaisiana, and Bo. lusitaniae) and A. marginale was detected. From the aspect of public health surveillance, the potential role of the golden jackal in the maintenance of vector-borne zoonotic pathogens in Serbia must be considered, and further eco-epidemiological studies should be performed to determine the precise role of this animal species in zoonotic disease transmission cycles.

First report of a naturally patent infection with Dirofilaria immitis in an otter ( Lutra lutra )

Dirofilaria immitis causes a severe and life-threatening cardio-pulmonary disease in Europe, Asia, Africa, and the Americas; also, zoonotic infections have been reported. This parasitic vector-borne disease is mostly common in domestic and wild canids and felids. Here, we present a rare finding of this roundworm in the heart of a Eurasian otter (Lutra lutra). Four mature specimens of D. immitis were found in the right ventricle of the heart. Necropsy was performed after the animal was found road-killed in Eastern Serbia, close to the Danube River. Two heartworms were females, one was male and sex for one remained unidentified. Microfilariae were present in the uterus of one of the female heartworms, indicating that otters can act as reservoirs of dirofilariasis in the wild. This is the first report of a patent infection in a free-ranging otter.

Concentrations of Selected Elements in Liver Tissue of Grey Wolves ( Canis lupus ) from Serbia

The grey wolf (Canis lupus) is a large carnivore species and a top predator in the ecosystems that it inhabits. Considering its role in food webs, wolves may be exposed to high concentrations of potentially harmful elements. Therefore liver samples from 28 legally hunted wolves were analyzed for concentrations of 16 elements using inductively coupled plasma optical emission spectrometry. The Mann–Whitney U test showed a significant difference between the genders only for Li, and there were no differences between individuals caught in different years. The majority of statistically significant correlations between element levels were positive, except for three cases. Compliance with several criteria for suitable bioindicator organisms imply that wolves may serve for monitoring environmental contamination.