Update of the helminth fauna in Eurasian lynx (Lynx lynx) in Poland

  • Marta Kołodziej-Sobocińska
  • Yegor Yakovlev
  • Krzysztof Schmidt
  • Zuzana Hurníková
  • Iwona Ruczyńska
  • Michał Bednarski
  • Małgorzata Tokarska
Open Access
Original Paper
  • 6 Downloads

Abstract

The Eurasian lynx (Lynx lynx) is a strictly protected species of large carnivore in Poland. It inhabits forest complexes in north-eastern Poland and the Carpathian region in southern Poland. The status of the lynx within Poland requires special attention because its range decreased between 1980 and 2001 and has not yet recovered. One of the factors negatively affecting lynx populations is diseases, particularly parasites. The helminth fauna of the Eurasian lynx is not fully known in Poland. Previous coprological studies revealed that Polish lynx have been infected with seven species of nematodes, three species of cestodes, and one species of trematode. In this study, we present new data based on examination of opportunistically collected lynx carcasses. The aim of the study was to complement data on the helminth fauna of Eurasian lynx inhabiting Poland based on morphological and molecular analysis of parasites. Four species of cestodes—Taenia lynciscapreoli, Mesocestoides lineatus, Spirometra sp., and Taenia krabbei—were found for the first time in Eurasian lynx from Poland and three previously reported species of nematodes—Ancylostoma tubaeforme, Toxascaris leonina, and Toxocara cati—were confirmed. Larvae of Trichinella britovi were also detected in Eurasian lynx in Poland for the first time.

Keywords

Carnivores Felidae Eurasian lynx Helminth fauna Endangered species 

Introduction

The Eurasian lynx (Lynx lynx) is a strictly protected large carnivore species in Poland. Despite protection and a general increasing trend in other countries (Chapron et al. 2014), its population within Poland decreased dramatically between 1980 and 2001 (Jędrzejewski et al. 2002) and has not yet recovered. Habitat fragmentation in central Europe has been suggested as a major cause of this situation due to a strong affiliation between these felids and forest habitat (Kowalczyk et al. 2015; Podgórski et al. 2008; Schmidt 1998). Infestation with parasites has been shown to be an important mortality factor in lynx (Breitenmoser et al. 2000; Schmidt-Posthaus et al. 2002; Andren et al. 2006; Szczęsna et al. 2008). Therefore, monitoring parasite load in wildlife showing negative population trends may be crucial for understanding their status.

The helminth fauna of Eurasian lynx in Europe reported so far consists of 25 species including 11 species of cestodes, one species of trematode, and 14 species of nematodes (Furmaga 1953; Merkusheva and Bobkova 1981; Yushkov 1995; Samuel et al. 2001; Bagrade et al. 2003; Valdmann et al. 2004; Szczęsna et al. 2008; Kornnyushin and Varodi 2010; Deksne et al. 2013; Lavikainen et al. 2013; Haukisalmi et al. 2016). Data from lynx in Poland are limited due to rarity of this species and are based on either scant material or fecal samples, which provide underestimated results of helminth prevalence and intensity (Szczęsna et al. 2008). The presence of parasites such as Diphyllobothrium latum (L., 1758); Hydatigera (=Taenia) rileyi (Loewen, 1929) (misidentification, Taenia sp. (Fagasiński, 1961) according to Abuladze [18]); Spirometra janickii Furmaga, 1953; Alaria alata (Goeze, 1782); Aelurostrongylus abstrusus (Railliet, 1898); Ancylostoma tubaeforme (Zeder, 1800); Eucoleus (=Thominx) aerophilus (Creplin, 1839); Metastrongylus sp.; Nematodirus sp.; Toxocara mystax (=T. cati) (Schrank, 1788) Baylis et Daubney, 1923; and Toxascaris leonina (Linstow, 1902) was confirmed to date (Furmaga 1953; Fagasiński 1961; Okulewicz et al. 2002; Górski et al. 2006; Szczęsna et al. 2006, 2008; Filip and Demiaszkiewicz 2017).

In this study, we present new data based on examination of opportunistically collected lynx carcasses. The aim of the study was to contribute data on the helminth fauna of Eurasian lynx inhabiting Poland based on morphological and molecular analysis of parasites. Due to the protected status of lynx in Poland, such comprehensive analyses give a unique opportunity to increase the knowledge on potential limiting factors for the sustainability of the fragmented population of this large felid.

Material and methods

Animal dissections and collecting of helminths

Eleven lynx carcasses were collected in 2007–2017 in northern-eastern and southern Poland (Fig. 1). In all cases, except one which was a road fatality, the lynx were found dead and some of them were strongly emaciated (Table 1). Gastrointestinal tracts and muscle samples were collected for parasitological studies. Isolated helminths were preserved in 70% ethanol for further analysis.
Fig. 1

An outline map of Poland showing sample collection locations. Roman numerals in brackets represent ID numbers of studied lynx

Table 1

Details of the Eurasian lynx studied for helminth fauna and the helminths found in each individual. NE, north-eastern Poland; S, southern Poland; LPG, number of Trichinella larvae per gram of muscle for positive animals. For other parasite species, the number of individuals is presented. Juveniles, up to 1 year; subadults, > 1–2 years; adults, > 2 years

Lynx no.

Localization

Date of death

Circumstances of death

Age

Sex

Parasites

Number of cestodes

Number of nematodes

I

Knyszyńska Forest (NE)

12.04.2010

Found dead, cause unknown

Juvenile

Female

Taenia lynciscapreoli, Taenia krabbei, Toxocara cati

50

2

II

Augustowska Forest (NE)

12.06.2009

Killed by car

Adult

Male

Taenia lynciscapreoli, Trichinella britovi

53

3.2 LPG

III

Piska Forest (NE)

17.07.2009

Found dying, highly emaciated in a dog kennel

Subadult

Female

Taenia lynciscapreoli, Ancylostoma tubaeforme, Toxocara cati

8

62

IV

Lubaczów (S)

10.02.2013

Found dead, autopsy suggested poisoning by unknown substance

?

Male

Mesocestoides lineatus, Spirometra sp., Taenia lynciscapreoli, Taenia krabbei, Ancylostoma tubaeforme, Toxocara cati

180

90

V

Myślenice (S)

01.07.2007

Found dead, strongly emaciated body, together with two siblings

Juvenile

Female

Taenia krabbei, Toxocara cati

1

1

VI

Carpathian Region (S)

02.09.2010

Found dying, strongly emaciated, death caused by prenatal pathology

Subadult

Female

Taenia lynciscapreoli

7

0

VII

Białowieża Forest (NE)

25.11.2015

Found dead, highly emaciated in farm buildings

Juvenile

Male

Taenia krabbei, Toxocara cati

11

1

VIII

Białowieża Forest (NE)

28.02.2016

Found dying, highly emaciated, sarcoptic mange infection

Adult

Female

Taenia lynciscapreoli, Toxocara cati, Trichinella britovi

45

3, 1.8 LPG

IX

Białowieża Forest (NE)

28.02.2016

Found dead near the village, sarcoptic mange infection

Juvenile

Female

Taenia lynciscapreoli, Toxocara cati

32

17

X

Białowieża Forest (NE)

02.01.2017

Found dead, probably bitten by another lynx

Adult

Female

Taenia lynciscapreoli, Trichinella sp.

24

0.1 LPG

XI

Carpathian Region (S)

19.04.2017

Found dead, sarcoptic mange infection

Adult

Female

Teania krabbei, Toxascaris leonina

8

9

Morphological identification of parasites

For light microscope observation, nematodes were processed in 80% solution of phenol in glycerol, for measurement nematodes were processed in enlightening solution made from lactic acid, phenol, glycerol, and distilled water (1:1:1:1). Cestode scolexes were processed in a 50% solution of glycerol in distilled water. The total amounts of scolexes were kept in Berleses medium, and mature and immature proglottids were stained with iron acetocarmine and mounted in Canada balsam (Ivashkin et al. 1971). Observations were done using Amplival Carl Zeiss Jena and Zeiss Axio Imager M1 microscopes and Leica M165C and MBS-9 stereomicroscopes.

Species identification of parasites was based on morphological features. In the case of damaged specimens, a standard coproscopic parasite eggs identification was additionally performed. Comparison with the collection of helminths from the Department of Parasitology of the Schmalhausen Institute of Zoology, specific keys to parasitic nematodes, Mesocestoidata, and Taeniata was used (e.g., Skryabin et al. 1951, 1952; Mozgovoy 1953; Abuladze 1964; Ryzhikov 1978). Infection of Eurasian lynx with helminths was presented by standard parameters: prevalence—number of infected hosts divided by the total number of dissected animals (shown in the form of simple fraction); mean intensity—the total number of parasites divided by the number of infected lynx; mean abundance—the total number of parasites divided by the total number of analyzed animals (Bush et al. 1997).

Digestion and molecular identification of Trichinella species

Muscle samples (diaphragm or foreleg muscle) from eight lynx (15 g each) were individually examined for the presence of Trichinella muscle larvae using the magnetic stirrer method for sample digestion as described by Kapel and Gamble (2000). Obtained muscle larvae were identified based on morphological characteristics and counted, and the number of larvae per gram of muscle tissue (LPG) was calculated. Larvae were washed several times in distilled water and stored in 96% ethanol until speciation by the multiplex polymerase chain reaction (PCR).

DNA was isolated from a pool of five larvae from each sample (if available). Extraction of DNA and PCR amplification was performed according to Pozio and La Rosa (2003) modified by using two pairs of primers: ESVF (5′-GTTCCATGGAACAGCAGT) and ESVR (5′-CGAAAACATACGACAACTGC) amplifying the expansion segment V (ESV) region in all known Trichinella species and genotypes and TBF (5′-GCTACATCCTTTTGATCGGTT) and TBR (5′-AGACACAATATCAACCACAGTACA) that amplify a partial region of ITS-1 specific for T. britovi Britov et Boev, 1972. For amplification, 5 μl DNA was added to the PCR reaction mix (vol. 25 l) by Eppendorf® and PCR was performed in a XP ThermalCycler (BIOER Technology Co., LTD.). Amplification was carried out under the following cycling conditions: 40 cycles of denaturation at 94 °C for 30 s, annealing at 58 °C for 30 s, and elongation at 72 °C for 1 min. The amplification products (5 μl) were separated on a 1.6% standard agarose gel and stained with GoldView™ Nucleic Acid Stain before visualization. All PCRs included negative and positive controls—reference strains T. spiralis Owen, 1835 (ISS 004); T. nativa Britov et Boev, 1972 (ISS 042); T. britovi (ISS 1088); and T. pseudospiralis Garkavi, 1972 (ISS 013).

Genetic identification and phylogenetic analysis of Taenia species

To verify the results of microscope examination of the Taenia species that could be misidentified by morphological features, we applied three primer pairs, constructed by Jia et al. (2010), designed for purposes of comparative mitogenomics of Taenia species. The three primer pairs enabled the amplification of four distinct mtDNA fragments containing cytochrome c oxidase (cox, approx. 470 bp), nicotinamide dehydrogenase subunits 1 (nad1, approx. 460 bp) and 5 (nad5, approx. 600 bp), and the small unit of rRNA (rrnS, approx. 400 bp). Amplifications of the fragments were performed in 10 μl of reaction mixture, including 2 μl of the DNA, 5 μl of PCR HotStarTaq Master Mix Kit, and 1 μl of each of two primers (5 pmol/μl). Thermal cycling conditions: 35 cycles of denaturation at 95 °C for 60 s, annealing at 58 °C for 45 s (T_nad1 and T_nad5), 65 °C for 45 s (T-rrnS), and 54 °C for 60 s (Cox1), and elongation at 72 °C for 10–15 min.

To increase the possibility to detect all possible Taenia species, we sampled 1–4 distinct parasites from each lynx, depending on their individual availability. The obtained sequences were BLASTed using the NCBI online tool (http://blast.ncbi.nlm.nih.gov/Blast.cgi) (Altschul et al. 1990). Sequence alignments between the obtained sequences and the evolutionarily closest sequences were performed using ClustalW Multiple Alignment option delivered within BioEdit tools (Hall 1999). Molecular phylogenetic analysis of the lynx parasites by Maximum Likelihood method based on the Tamura-Nei model within MEGA6 tool (Tamura and Nei 1993; Tamura and Kumar 2004) was performed for all the samples and all three mtDNA fragments.

Mean genetic distances between taxa (average evolutionary divergence over sequence pairs between groups of sequences) and within taxa, expressed as the number of base substitutions per site from averaging over all sequence pairs between groups, were estimated based on maximum composite likelihood model (Tamura and Nei 1993) using MEGA6 (Tamura et al. 2013).

Results

All lynx we examined were infected with helminths. We found eight species of parasites, consisting of four species of cestodes: Mesocestoides lineatus, Spirometra sp., Taenia krabbei, and Taenia lynciscapreoli and four species of nematodes: Ancylostoma tubaeforme, Toxocara cati, Toxascaris leonina, and Trichinella britovi (Tables 1 and 2). The four cestode species mentioned above and one nematode (T. britovi) are reported for the first time in lynx inhabiting Poland.
Table 2

Parasites of Eurasian lynx found in Poland. Species of parasites identified for the first time in lynx from Poland are in bold. Method: D, dissection; F, fecal analysis. Localization in Poland: E, eastern; NE, north-eastern; S, southern; NW, north-western; SW, south-western

Parasite

Localization in Poland

Method

References

Nematoda

 Angiostrongylus abstrusus

E

F

Szczęsna et al. 2006, 2008

 Ancylostoma tubaeforme

E, NE, S

F, D

Szczęsna et al. 2008 This study

 Eucoleus aerophilus

E

F

Szczęsna et al. 2008

 Metastrongylus sp.

E

F

Szczęsna et al. 2008

 Nematodirus sp.

E

F

Szczęsna et al. 2008

 Toxocara cati

E, NE, S

F, D

Fagasiński 1961; Górski et al. 2006; Szczęsna et al. 2008

This study

 Toxascaris leonina

NW, SW

F

Okulewicz et al. 2002; Filip and Demiaszkiewicz 2017

This study

Trichinella britovi

NE

D

This study

Cestoda

 Diphyllobothrium latum

E

F

Szczęsna et al. 2008

 Mesocestoides lineatus

S

D

This study

 Spirometra janickii

E

F, D

Furmaga 1953; Szczęsna et al. 2008

 Spirometra sp.

E

D

This study

 Taenia krabbei

NE, S

D

This study

 Taenia lynciscapreoli

NE, S

D

This study

 Taenia sp.

NE

D

Fagasiński 1961

Trematoda

 Alaria alata

E

F

Szczęsna et al. 2008

Most prevalent was T. lynciscapreoli, found in 8 out of 11 studied lynx. We found Taenia krabbei in five lynx and both M. lineatus and Spirometra sp. in one of the lynx. Three individuals were infected with Trichinella sp. with intensity of the latter at 0.1 to 3.2 LPG. T. britovi was confirmed by PCR in two lynx. The highest infection intensity was observed for M. lineatus and the lowest for Spirometra sp. (see Table 3). We observed an untypical location of Spirometra sp., in the large intestine. The results of interspecific mtDNA alignment are presented in Fig. 2a–d.
Table 3

Descriptive statistics for helminth infections in Eurasian lynx in Poland

Parasites

Prevalence

Mean intensity

Mean abundance

Nematoda

9/11

39

32

Toxocara cati

7/11

26

17

Toxascaris leonina

1/11

9

1

Trichinella britovi

3/8

Ancylostoma tubaeforme

2/11

26

5

Cestoda

6/11

50

27

Mesocestoides lineatus

1/11

139

13

Spirometra sp.

1/11

6

1

Taenia krabbei

5/11

6

3

Taenia lynciscapreoli

8/11

24

17

The aggregate results of detected in lynx Nematoda and Cestoda parasites are in bold

Fig. 2

Phylograms for the four mtDNA fragments of the lynx parasite DNA samples collected in the study (in bold type) and the reference sequences from GeneBank (National Center for Biotechnology Information, http://www.ncbi.nlm.nih.gov/). Evolutionary relationships of the taxa were implied using the Neighbor-Joining method (Tamura and Nei 1993) embedded in MEGA6 software (Tamura et al. 2013). The evolutionary distances were computed using the maximum composite likelihood method (Tamura and Kumar 2004) and are expressed in units of the number of base substitutions per site. The molecular phylogenies were drawn based on the following mtDNA fragments: a nicotinamide dehydrogenase subunit 1 (nad1); b nicotinamide dehydrogenase 5 (nad5), c small unit of rRNA (rrnS); and d cytochrome c oxydase (cox). Roman numerals indicate lyx ID, while Arabic numerals preceded by a dash indicate subsequent sampled parasite individuals

Discussion

Our study provided new information on the helminth species of lynx in the territory of Poland. Until now, the accumulated data from the literature along with the results of this study show that the lynx in this area can be a host to at least 14 species of helminths. This data is important considering that lynx populations in Poland are unstable or decreasing (Von Arx et al. 2004), and in central Europe, they are also strongly fragmented and limited to forest areas (Kowalczyk et al. 2015; Schmidt 1998). Therefore, every risk that may contribute to deepening the vulnerability of the population, including parasitic invasions, must be taken into account in conservation strategies.

Lynx feed on ungulates (~ 90% of prey) with roe deer (Capreolus capreolus) and red deer (Cervus elaphus) being the main prey species (Okarma et al. 1997), with smaller animals being preyed upon only occasionally. Intermediate hosts for T. lynciscapreoli and T. krabbei Moniez, 1789, are roe deer and other cervids (Al-Sabi et al. 2013; Haukisalmi et al. 2016). Thus, the relatively high Taenia sp. infection prevalence stated in our study is directly connected with lynx feeding habits. According to our best knowledge, this is the first reported case of lynx as the definitive host for T. krabbei that usually uses canids as its definitive hosts (Priemer et al. 2002; Lavikainen et al. 2011). The life cycle of M. lineatus has not yet been clarified. However, the first intermediate host could be oribatid mites, and the range of the second intermediate hosts is quite wide, including species from different classes of vertebrates (Ryzhikov 1978; Yushkov 1995), which could form part of the lynx diet. T. cati and A. tubaeforme are widespread helminths of cats with A. tubaeforme being a specific parasite of felids. Both species infect hosts percutaneously in dens, during feeding (engulfment of eggs or larvae in rodents or insects or with milk) or through the placental barrier. However, no larvae migrans of these nematodes were found in our study.

Our data suggest that the confirmed southern range of T. lynciscapreoli should be extended. Up to-date, the species has been found and reported in Lohja, Hyvinkää, Hausjärvi (Southern Finland), Mustasaari, Sauvo (Western Finland), Mikhailovskiy raion (Altai Krai), Kolosovsky, and Bolsheukovsky raions (Omskaya oblast, Western Siberia) in the Russian Federation (Haukisalmi et al. 2016).

To our knowledge, we report the first finding of a Trichinella parasite in Eurasian lynx from Poland. T. britovi was detected in two adult females from Białowieża Forest and an adult male from Augustów Forest. The presence of Trichinella in lynx is not surprising, as the species is known to feed occasionally on carnivorous and scavenging mammals (Okarma et al. 1997). Trichinellosis in Eurasian lynx was found in 22 to 67% of individuals in Estonia (Järvis and Miller 1999; Valdmann et al. 2004; Malakauskas et al. 2007; Pozio 2013) in 46 to 98% in Republic of Latvia (Bagrade et al. 2003; Malakauskas et al. 2007) and in Finland, where the prevalence in lynx is the highest among free-living carnivores—up to 70% (Airas et al. 2010). T. britovi was detected also in lynx from Slovakia (Hurníková et al. 2009) and in 27% of Swiss lynx (Frey et al. 2009). This species is also prevalent in other wild mammals in Poland, infecting mainly red fox (Cabaj et al. 2000; Cabaj et al. 2004), but also found in wild boar (Sus scrofa L., 1758) (Bilska-Zając et al. 2013), wolf (Cabaj 2006), martens and badger (Moskwa et al. 2012), and American mink (Neovison vison Schreber, 1777) (Hurníková et al. 2016).

The number of dissected animals in this study was too small to derive conclusions about possible relationships between parasite infestation intensity and lynx mortality or morbidity. However, in the majority of cases, the dead lynx were found emaciated and without an apparent cause of death. However, the harmful influence of helminth invasion on animal health status has been shown previously (Rodriguez and Carbonell 1998).

This study conducted on the rare and unique material of dead lynx from the territory of Poland has yielded unique knowledge of lynx helmith fauna. All these findings may be helpful in explaining parasite transmission patterns in the areas inhabited by lynx. Five new pathogenic agents discovered in endangered Eurasian lynx on the Polish territory could have a negative impact on its condition and fitness.

Notes

Acknowledgements

We would like to thank Amy Eycott and Jamie Cottam and for correcting the English of the manuscript.

Material was deposited in the scientific collection of the Mammal Research Institute, Polish Academy of Sciences in Białowieża. For species identification, material has been made available temporarily to the Department of Parasitology of the Schmalhausen Institute of Zoology NAS of Ukraine.

Funding information

The study was supported by the European Commission’s 7th Framework Programme, Marie Curie Actions project “Biodiversity of East European and Siberian large mammals on the level of genetic variation of populations” (PIRSES-GA-2009-247652-BIOGEAST) conducted by the Mammal Research Institute Polish Academy of Sciences in Białowieża, Poland, in cooperation with Schmalhausen Institute of Zoology in Kyiv, Ukraine.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Abuladze KI (1964) Taeniata—the tapeworms of animals and humans and diseases caused by them. Foundations of Cestodology. Nauka, Moscow, p 540 [In Russian]Google Scholar
  2. Airas N, Saari S, Mikkonen T, Virtala AM, Pellikka J, Oksanen A, Isomursu M, Kilpelä SS, Lim CW, Sukura A (2010) Sylvatic Trichinella spp. infection in Finland. J Parasitol 96:67–76CrossRefPubMedGoogle Scholar
  3. Al-Sabi MN, Chriél M, Holm E, Jensen TK, Ståhl M, Enemark HL (2013) Reappearance of Taenia ovis krabbei muscle cysts in a roe deer (Capreolus capreolus) in Denmark after 60+ years. Vet Parasitol 196:225–229CrossRefPubMedGoogle Scholar
  4. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  5. Andren H, Linnell JDC, Liberg O, Andersen R, Danell A, Karlsson J et al (2006) Survival rates and causes of mortality in Eurasian lynx (Lynx lynx) in multi-use landscapes. Biol Conserv 131:23–32CrossRefGoogle Scholar
  6. Bagrade G, Vismanis K, Kirjušina M, Ozoliņš J (2003) Preliminary results on the helminthofauna of the Eurasian lynx (Lynx lynx) in Latvia. Acta Zool Lituan 13:3–7CrossRefGoogle Scholar
  7. Bilska-Zając E, Różycki M, Chmurzyńska E, Marucci G, Cencek T, Karamon J et al (2013) Trichinella species circulating in wild boar (Sus scrofa) populations in Poland. Int J Parasitol 2:211–213Google Scholar
  8. Breitenmoser U, Breitenmoser-Würsten Ch, Okarma T, Kaphegyi T, Kaphegyi-Wallmann U, Müller UM (2000) Action plan for the conservation of the Eurasian lynx (Lynx lynx) in Europe. Council and Europe Publishing, Nature and Environment 112:1–69Google Scholar
  9. Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583CrossRefPubMedGoogle Scholar
  10. Cabaj W (2006) Wild and domestic animals as permanent Trichinella reservoir in Poland. Wiad Parazytol 52:175–179PubMedGoogle Scholar
  11. Cabaj W, Pozio E, Moskwa B, Malczewski A (2000) Trichinella spiralis and T. britovi in red foxes (Vulpes vulpes) in Poland. Acta Parasitol 45:340–344Google Scholar
  12. Cabaj W, Moskwa B, Pastusiak K, Malczewski A (2004) Trichinosis in free-living animals and pigs in Poland. Med Weter 60:80–83 [In Polish]Google Scholar
  13. Chapron G, Kaczensky P, Linnell JD, von Arx M, Huber D, Andren H et al (2014) Recovery of large carnivores in Europe’s modern human-dominated landscapes. Science 346:1517–1519CrossRefPubMedGoogle Scholar
  14. Deksne G, Laakkonen J, Näreaho A, Jokelainen P, Holmala K, Kojola I, Sukura A (2013) Endoparasites of the Eurasian lynx (Lynx lynx) in Finland. J Parasitol 99:229–234CrossRefPubMedGoogle Scholar
  15. Fagasiński A (1961) A contribution to the knowledge of helminth fauna of the lynx and wildcat in Poland. Acta Parasitol Polonica 9:1–6Google Scholar
  16. Filip K, Demiaszkiewicz AW (2017) Endoparasites of Eurasian lynx (Lynx lynx) (Linnaeus, 1758) from enclosure of of Western Pomeranian Nature Society in Jablonowo. Ann Parasitol 63:33–36PubMedGoogle Scholar
  17. Frey CF, Schnuppers ME, Müller N, Ryser-Degiorgis MP, Gottstein B (2009) Assessment of the prevalence of Trichinella spp. in red foxes and Eurasian lynx from Switzerland. Vet Parasitol 159:295–299CrossRefPubMedGoogle Scholar
  18. Furmaga S (1953) Spirometra janickii sp. n. (Diphyllobothriidae). Acta Parasitol Polonica 1:29–64Google Scholar
  19. Górski P, Zalewski A, Łakomy M (2006) Parasites of carnivorous mammals in Białowieża Primeval Forest. Wiad Parazytol 52:49–53PubMedGoogle Scholar
  20. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Series 41:95–98Google Scholar
  21. Haukisalmi V, Konyaev S, Lavikainen A, Isomursu M, Nakao M (2016) Description and life-cycle of Taenia lynciscapreoli sp. n. (Cestoda, Cyclophyllidea). Zookeys 584:1–23CrossRefGoogle Scholar
  22. Hurníková Z, Kołodziej-Sobocińska M, Dvorožňáková E, Niemczynowicz A, Zalewski A (2016) An invasive species as an additional parasite reservoir: Trichinella in introduced American mink (Neovison vison). Vet Parasitol 231:106–109CrossRefPubMedGoogle Scholar
  23. Hurníková Z, Miterpáková M, Chovancová B (2009) The important zoonoses in the protected areas of the Tatra National Park (TANAP). Wiad Parazytol 55:395–398PubMedGoogle Scholar
  24. Ivashkin VM, Kontrimavichus VL, Nazarova NS (1971) Methods of collecting and studying of helminths of terrestrial mammals. Nauka, Moscow [In Russian]Google Scholar
  25. Järvis T, Miller I (1999) Epizootology of trichinellosis. Eesti Arst 5:414–417 [In Estonian]Google Scholar
  26. Jędrzejewski W, Nowak S, Schmidt K, Jędrzejewska B (2002) The wolf and the lynx in Poland—results of a census conducted in 2001. Kosmos 51:491–499 [In Polish]Google Scholar
  27. Jia WZ, Yan HB, Guo AJ, Zhu XQ, Wang YC, Shi WG, Chen HT, Zhan F, Zhang SH, Fu BQ, Littlewood DTJ, Cai XP (2010) Complete mitochondrial genomes of Taenia multiceps, T. hydatigena and T. pisiformis: additional molecular markers for a tapeworm genus of human and animal health significance. BMC Genomics 11:447CrossRefPubMedPubMedCentralGoogle Scholar
  28. Kapel CMO, Gamble HR (2000) Infectivity, persistence, and antibody response to domestic and sylvatic Trichinella spp. in experimentally infected pigs. Int J Parasitol 30:215–221CrossRefPubMedGoogle Scholar
  29. Kornnyushin VV, Varodi EI (2010) Helminths of domestic and wild cats in Ukraine. Scientific Journal of the National University of Bioresearch and Management of Natural Resources of Ukraine, Veterinary Medicine, Quality and Safety of Animal Produce 51:113–118 [In Ukrainian]Google Scholar
  30. Kowalczyk R, Górny M, Schmidt K (2015) Edge effect and influence of economic growth on Eurasian lynx mortality in the Białowieża Primeval Forest, Poland. Mammal Res 60:3–8CrossRefGoogle Scholar
  31. Lavikainen A, Haukisalmi V, Deksne G, Holmala K, Lejeune M, Isomursu M et al (2013) Molecular identification of Taenia spp. in the Eurasian lynx (Lynx lynx) from Finland. Parasitology 140:653–662CrossRefPubMedGoogle Scholar
  32. Lavikainen A, Laaksonen S, Beckmen K, Oksanen A, Isomursu M, Meri S (2011) Molecular identification of Taenia spp. in wolves (Canis lupus), brown bears (Ursus arctos) and cervids from North Europe and Alaska. Parasitol Int 60:289–295CrossRefPubMedGoogle Scholar
  33. Malakauskas A, Paulauskas V, Järvis T, Keidans P, Eddi C, Kapel CMO (2007) Molecular epidemiology of Trichinella spp. in three Baltic countries: Lithuania, Latvia, and Estonia. Parasitol Res 100:687–693CrossRefPubMedGoogle Scholar
  34. Merkusheva IV, Bobkova AF (1981) Helminths of domestic and wild live animals of Belorussia: catalogue. Nauka i technika, Minsk [In Russian]Google Scholar
  35. Moskwa B, Goździk K, Bień J, Bogdaszewski M, Cabaj W (2012) Molecular identification of Trichinella britovi in martens (Martes martes) and badgers (Meles meles); new host records in Poland. Acta Parasitol 57:402–405CrossRefPubMedGoogle Scholar
  36. Mozgovoy AA (1953) Ascaridata of animals and human and caused diseases by them. In: Skryabin KI (ed) Foundations of nematology. Nauka, Moscow, p 618 [In Russian]Google Scholar
  37. Okarma H, Jędrzejewski W, Schmidt K, Kowalczyk R, Jędrzejewska B (1997) Predation of Eurasian lynx on roe deer and red deer in Białowieża Primeval Forest, Poland. Acta Theriol 42:203–224CrossRefGoogle Scholar
  38. Okulewicz A, Lonc E, Borgsteede FHM (2002) Ascarid nematodes in domestic and wild terrestrial mammals. Polish J Vet Sci 5:277–281Google Scholar
  39. Podgórski T, Schmidt K, Kowalczyk R, Gulczyńska A (2008) Microhabitat selection by Eurasian lynx and its implications for species conservation. Acta Theriol 53:97–110CrossRefGoogle Scholar
  40. Pozio E (2013) The opportunistic nature of Trichinella—exploitation of new geographies and habitats. Vet Parasitol 194:128–132CrossRefPubMedGoogle Scholar
  41. Pozio E, La Rosa G (2003) PCR-derived methods for the identification of Trichinella parasites from animal and human samples. Methods Mol Biol 216:299–309PubMedGoogle Scholar
  42. Priemer J, Krone O, Schuster R (2002) Taenia krabbei (Cestoda: Cyclophyllidea) in Germany and its delimitation from T. ovis. Zool Anz 241:333–337CrossRefGoogle Scholar
  43. Rodriguez A, Carbonell E (1998) Gastrointestinal parasites of the Iberian lynx and other wild carnivores from central Spain. Acta Parasitol 43:128–136Google Scholar
  44. Ryzhikov KM (1978) Tetrabothriata and Mesocestoidata—tapeworms of birds and mammals. Foundations of Cestodology. Nauka, Moscow, p 231 [In Russian]Google Scholar
  45. Samuel WM, Kocan AA, Pybus MJ (2001) Parasitic diseases of wild mammals, 2nd edn. Manson publishing, LondonCrossRefGoogle Scholar
  46. Schmidt K (1998) Maternal behaviour and juvenile dispersal in the Eurasian lynx. Acta Theriol 43:391–408CrossRefGoogle Scholar
  47. Schmidt-Posthaus H, Breitenmoser-Würsten C, Posthaus H, Bacciarini L, Breitenmoser U (2002) Causes of mortality in reintroduced Eurasian lynx in Switzerland. J Wildl Dis 40:356–360Google Scholar
  48. Skryabin KI, Shihobalova NP, Schulz RS, Popova TI, Boev SN, Delamure SL (1952) Strongylata. In: Skryabin KI (ed) Keys to parasitic nematodes. Academy of Sciences of USSR, Moscow, p 892 [In Russian]Google Scholar
  49. Skryabin KI, Shihobalova NP, Mozgovoy AA (1951) Oxyurata and Ascaridata. In: Skryabin KI (ed) Keys to parasitic nematodes. Academy of Sciences of USSR, Moscow, p 634 [In Russian]Google Scholar
  50. Szczęsna J, Popiołek M, Schmidt K, Kowalczyk R (2006) The first record of Aelurostrongylus abstrusus (Angistrongylidae: Nematoda) in Eurasian lynx (Lynx lynx L.) from Poland based on fecal analysis. Wiad Parazytol 52:321–322PubMedGoogle Scholar
  51. Szczęsna J, Popiołek M, Schmidt K, Kowalczyk R (2008) Coprological study on helminth fauna in Eurasian lynx (Lynx lynx) from the Białowieza Primeval Forest in eastern Poland. J Parasitol 94:981–984CrossRefPubMedGoogle Scholar
  52. Tamura K, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Nat Acad Sci USA 101:11030–11035CrossRefPubMedPubMedCentralGoogle Scholar
  53. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  54. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  55. Valdmann H, Moks E, Talvik H (2004) Helminth fauna of Eurasian lynx (Lynx lynx) in Estonia. J Wildl Dis 40:356–360CrossRefPubMedGoogle Scholar
  56. Von Arx M, Breitenmoser-Würsten C, Zimmermann F, Breitenmoser U (2004) Status and conservation of the Eurasian lynx (Lynx lynx) in 2001. KORA Bericht 19Google Scholar
  57. Yushkov VF (1995) Helminths of mammals. Fauna of european north-east of Russia. Nauka, Saint-Petersburg, p 201 [In Russian]Google Scholar

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Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Mammal Research InstitutePolish Academy of SciencesBiałowieżaPoland
  2. 2.Schmalhausen Institute of Zoology NAS of UkraineKyivUkraine
  3. 3.Kyiv Zoological Park of National ImportanceKyivUkraine
  4. 4.Institute of ParasitologySlovak Academy of SciencesKošiceSlovak Republic
  5. 5.Department of Epizootiology and Clinic of Bird and Exotic AnimalsWrocław University of Environmental and Life SciencesWrocławPoland

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